Herbivores and periphyton: Littoral zone interactions in Lake Tanganyika Student: Stephanie Miller Mentor: Ellinor Michel Introduction The abundance of periphyton can vary enormously with depth, and standing stocks are often greatest in shallow water (Power 1989). Light penetration decreases with depth, so this alone may be sufficient to explain some variation in periphyton abundance. In many systems, grazers reduce periphyton stocks (e.g. Matthews 1986, Cattaneo 1990), and aerial predators may restrict aquatic herbivores to deeper areas, producing a decrease in algal abundance with depth (Power 1984). Additionally, waves may decrease periphyton biomass in shallow areas by preventing some species from attaching to substrates in the surge zone, but they could also increase biomass through increased water renewal (Cattaneo 1990). Wave energy may also reduce herbivore grazing time or deter organisms from grazing in some areas because of the risk of being swept into habitats with a more diverse assemblage of predators (Trussell 1997). In the littoral zone of Lake Tanganyika, the mean euphotic zone reaches 28 m (Hecky 1991), and there is a diverse assemblage of endemic species that graze epilithic algae. Observations indicate a clear decline in periphyton stocks with depth along the first 5 m of substrate. In this project, I examined the relationship between periphyton biomass, wave energy, and the distribution of herbivorous fish and snails. I tested three hypotheses: 1) periphyton biomass decreases with depth; 2) exposure to herbivorous fish and snails decreases periphyton biomass; and 3) depth and wave energy affect grazers ability to consume periphyton at shallow depths, so herbivory has a stronger effect on periphyton biomass at greater depths. Methods Study site Undisturbed littoral zone habitats of Lake Tanganyika host a diverse and largely endemic fauna, including numerous gastropods and cichild fishes. Jakobsen s beach lies southwest of Kigoma, Tanzania, along the eastern shore of the lake. All of our work was focused on the southern rocky shoreline of Jakobsen s beach #1, a region representative of undisturbed rocky littoral habitats in the region. Quantification of standing stock I quantified the standing stock of periphyton at depths of 0.2, 0.6, 1.0, 2.0, and 5.0 m. Ten flat, upwardfacing rocks (9 x 9 cm to 20 x 20 cm) were collected from each depth along a 50 m stretch of shore line. Rocks collected for sampling were separated by at least 1 m. Rocks were stored in submerged in lake water in complete darkness, and were processed within 12 hours. Periphyton was sampled by placing a 42 mm diameter round jar lid over the center of the rock, removing the surrounding algae using a nylonbristled brush and rinsing with water, then removing the periphyton from the protected area using the same method. Removed periphyton was rinsed from the rock surface to form an algal slurry. This slurry was filtered onto pre-ashed 47 mm Gelman glass fiber filters using a vacuum pump. Chlorophyll a was extracted by placing each filter into 94% EtOH for approximately 26-28 hours under darkness inside a refrigerator. I did not grind the samples, but the vigorous removal from the substrate ensured that cells were ruptured, and intact cells were likely to be ruptured by being frozen for 10-20 days prior to chlorophyll extraction. After extraction, the ethanol solution was placed in a centrifuge tube and spun at maximum speed for 10 minutes. Spectrophotometric absorbance of the supernate was measured at 665 and 750 nm wavelengths to quantify chlorophyll a. Samples were then acidified using 0.1 ml of 1N HCl/ml of extract to control for absorbance by phaeopigments. Chlorophyll a concentration per sq.cm. were estimated as 29.6*((abs(665)-abs(750))-(abs(665acidified)-abs(750acidified))) / 13.85 sq.cm.
Chl a per sq.cm. 1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 y = 0.0892x 2-0.6661x + 1.3563 R 2 = 0.9609 20 60 100 200 500 Depth (cm)
Evaluation of fish grazing A small team recorded fish grazing behavior over a two-week period. Large, flat boulders and bedrock surfaces were selected haphazardly for observation and no surface were observed more than once. During a 15-minute period, an observer at the surface recorded the number of fish visiting the observation area and the species when possible. Both individual bites and total number of visits (defined as sustained feeding activity during which the fish remained less than 10 cm from the substrate) were recorded. Fish feeding behavior was also classified as either scraping or picking. After the observation period ended, I recorded the height of the waves (measured as the average amplitude as they contacted vertical surfaces on the shoreline near the observation area), and the depth and dimensions of the observation area. Experiment: periphyton growth and grazing intensity as a function of depth To measure the rate of periphyton accumulation, we placed ten pairs of unglazed clay tiles (~56 sq.cm.) at both 1 and 5 meters on July 20, 2000. All tiles were covered with 1 cm 2 plastic mesh screening to prevent grazing, and pairs of tiles were secured to 49 cm lengths of rebar. These rebar stakes were wedged in between rocks so that the faces of both tiles were parallel to the water s surface. On August 3, we removed the mesh around one tile in each pair (haphazard selection) to allow access by grazers. To assess the intensity of grazing at each depth independent of periphyton stocks, 5 tile pairs from each depth were transplanted to the other depth (i.e. a reciprocal transplant). This resulted in a 2 x 2 x 2 factorial design in which exposure to grazers was crossed with both initial and final depth. I ended the experiment on August 6 and 7. After collecting 5 tile pairs from each depth on each day, I measured primary production by removing all remaining screening and placing each tile in a separate 800 ml bag of lake water. The dissolved oxygen (DO) and temperature of the water in each bag was recorded using a YSI 57 meter, and then bags were incubated in the sun on a flat, sandy area of Jakobsen s Beach for 40 min. After incubation, DO and temperature were again recorded in each bag. I then quantified periphyton biomass by removing all algae within a 38 x 35.5 mm slide frame. The algal slurry was filtered onto 25 mm Gelman glass fiber filters, and chlorophyll a was extracted and quantified using the method described earlier (except using 90% EtOH, and standardizing per unit area for the slide frame sample). Results Natural periphyton standing stocks generally decreased with depth (Fig. 1). When depth is treated as a categorical variable, there were significant difference between samples (F 4,37 =15.92, p<0.001). Post-hoc tests indicate that the 20 cm sample differed from all other depths, but that the standing stocks at 60-500 cm did not differ statistically. Petrochromis polyodon, Tropheus moorii, and Simochromis diagramma were the dominant herbivorous fishes recorded during the observation periods. There was no clear relationship between depth or wave energy and fish grazing activity. Neither factor predicted the number of bites or visits (/sq.m) by fish in a multiple linear regression. Thus, I have no evidence that the depth gradation of algae is attributable to the distribution of herbivorous fish. However, my observations indicated that fish may graze somewhat less at very shallow depths, and they seemed undeterred by wave action. In the tile experiment, algae accumulated much more rapidly at 1 m than at 5 m (Fig. 2). In addition, protected tiles apparently lost chlorphyll with transplantation to a different depth; this effect was smaller and less consistent in the unprotected tiles. Exposure to herbivores significantly reduced the algal density on tiles (t 19 =-2.89, p<0.01), but the effect of grazing on chlorophyll concentrations was generally higher in non-transplanted tiles than those whose depth was changed. There was no clear difference between depths in the intensity of herbivory. Overall, the reduction in algal standing stock on tiles attributable to herbivores was similar that of increasing depth (Fig. 2). In addition, exposure to herbivores increased production (oxygenesis) per unit chlorophyll during the 40 minute trials (t 19 =2.63, p<0.02; Fig. 3). This effect was particularly pronounced in the 1 m tiles; there was little or no effect on the productivity of 5 m tiles.
Chl a per sq.cm 0.35 0.3 0.25 0.2 0.15 0.1 1 m initial depth, unprotected 1 m initial depth, protected 5 m initial depth, unprotected 5 m initial depth, protected 0.05 0 1 5 Final (transplant) depth (m)
Productivity (mg/l DO per unit chl a) 0.5 0.4 0.3 0.2 0.1 1 m initial depth, unprotected 1 m initial depth, protected 5 m initial depth, unprotected 5 m initial depth, protected 0 1 5 Final (transplant) depth (m)
Discussion In this series of surveys and experiments, I have tried to assess the relative contribution of light intensity, herbivory, and wave action to maintaining low algal standing stocks in the rocky littoral zone of Lake Tanganyika. While light is likely to contribute to the decline in periphyton biomass with depth, it may not be the only factor. The euphotic zone in Lake Tanganyika extends well beyond 5 meters, and I observed an increase in epilithic algae between 2 and 5 m, so it is likely that light limitation is not solely responsible for differences in algal standing stocks with depth. The results of the tile experiment suggest that the effect of herbivores on algal stocks may be as significant as that of light energy. Since herbivore species are mobile, they should be able to target their feeding efforts on the most abundant or highest quality food resources. Since algal stocks decreased with depth, herbivores would be expected to graze more at shallow depths. In some systems, such resource tracking produces a stable distribution of algal density despite variation in productivity (e.g. Power 1984). However, my observations of fish feeding activity indicate that they do not target areas of high algal density. This could reflect their avoidance of shallow depths, where wave-induced turbulence and exposure to aerial predators are highest, but the data also indicate that wave energy has little effect on feeding. Thus, it appears that the dramatic decrease in algal biomass with depth does not result from patterns of feeding by herbivorous cichlids. It remains to be tested whether distributions and abundance of gastropod herbivores better reflects that of algal stocks. Broader and more extensive observations of grazing behavior may elucidate the relationship between herbivores and periphyton stocks in the benthic littoral zone. For instance, I only observed fish on large, flat, upward-facing surfaces, but some species may graze the underside of rocks to avoid predation or territorial aggression. It is also possible that algal quality varies with depth; I have collected algal samples for taxonomic determination, but no information on this subject is available at the moment. Another interesting possibility is that algal productivity may be enhanced by turbulence in shallow water, so standing stocks may simply reflect rates of production. For instance, waves may minimize boundary layers along the rocky substrate, allowing algae access to more water and thus more nutrients and carbon dioxide. Finally, we need to better understand the effect of depth on predation risk for herbivores, since predator avoidance by fish or snails could contribute to accumulation of algal stocks. References Cattaneo, A. 1990. The effect of fetch on periphyton spatial variation. Hydrobiologia 206:1-10 Hecky, R.E. 1991. The pelagic ecosystem. Pages 90-110 in G.W. Coulter, editor. Lake Tanganyika and its life. Oxford University Press, Oxford, United Kingdom. Matthews, W.J., M.E. Power, and A.J. Stewart. 1986. Depth distribution of Campostoma grazing scars in an Ozark stream. Environmental Biology of Fishes 17:291-297. Power, M.E. 1984. Depth distributions of armored catfish: predator-induced resource avoidance? 65:523-528. Power, M.E., T.L. Dudley, S.D. Cooper. 1989. Grazing catfish, fishing birds, and attached algae in a Panamanian stream. Environmental Biology of Fishes 26:285-294. Trussell, G.C. 1997. Phenotypic plasticity in the foot size of an intertidal snail. Ecology 74:1033-1048. Figure Legends Figure 1. Natural pattern of periphyton chlorophyll with depth. These data reflect algal standing stocks on natural substrates. Figure 2. Periphyton chlorophyll on clay tiles as a function of depth and protection from herbivores. Tiles were incubated under plastic screens for 14 days at a depth of either 1 or 5 m, then half of the tiles were transplanted to the opposite depth and the screening was removed from half of them. 3-4 days after transplantation, all tiles were harvested and algal stocks were estimated. Figure 3. Effect of depth and exposure to herbivores on primary production by algae on clay tiles. Primary production was measured as oxygenesis, and has been standardized to be independent of algal biomass.