Michael J. Vanni

NUTRIENT RECYCLING AND HERBIVORY AS MECHANISMS IN THE “TOP–DOWN” EFFECT OF FISH ON ALGAE IN LAKES

In lakes, top predators (fish) often influence the abundance of primary producers (phytoplankton) through food web interactions: phytoplankton biomass is often greater when planktivorous fish are abundant than when they are rare, and phytoplankton community structure is often affected by fish. Three mechanisms can account for these “top–down” effects of fish: decreased herbivory by zooplankton when fish biomass is high; modification of nutrient recycling rates by the herbivorous zooplankton assemblage as fish biomass varies; and nutrient recycling by fish. These processes were experimentally separated and their relative importance quantified in Tuesday Lake, Michigan. This was accomplished by manipulating the abundance of planktivorous fish or zooplankton in enclosures containing natural phytoplankton communities, and by incubating phytoplankton in nutrient-permeable chambers (which excluded herbivores) placed inside these enclosures. In large enclosures with all trophic levels, several phytoplankton taxa and total phytoplankton biomass showed increased abundance in the presence of fish compared to enclosures without fish. Several taxa also showed significantly greater abundance in nutrient-permeable chambers incubated in enclosures with fish than in chambers incubated in enclosures without fish. The latter result indicates that some phytoplankton taxa respond to fish even when separated from direct herbivory but exposed to nutrients recycled by consumers. Thus, consumer-mediated nutrient recycling had strong effects on phytoplankton community dynamics and could partly explain the “top–down” effects of fish. Most phytoplankton taxa responded to consumer-mediated nutrient recycling, especially dinoflagellates and chrysophytes. In separate enclosures, phytoplankton were exposed to contrasting zooplankton assemblages shaped by fish predation but without fish being present. The response of phytoplankton was not as strong as in the case of fish manipulations. Furthermore, the community-level response of phytoplankton was weaker in nutrient-permeable chambers placed in these enclosures than in chambers incubated in enclosures with fish. Nutrient limitation assays showed that manipulation of fish decreased phosphorus limitation of phytoplankton, while direct manipulation of zooplankton had no effect on phosphorus limitation. These results provide experimental evidence that food web effects on nutrient recycling are important in controlling phytoplankton community dynamics. Results also suggest that some of these effects are expressed via direct recycling of nutrients by fish, as well as by fish-induced effects on nutrient recycling by herbivores. Nutrient-mediated effects of top predators on primary producers should be incorporated into future models of “top–down” control of food web dynamics.

Fish extinctions alter nutrient recycling in tropical freshwaters

There is increasing evidence that species extinctions jeopardize the functioning of ecosystems. Overfishing and other human influences are reducing the diversity and abundance of fish worldwide, but the ecosystem-level consequences of these changes have not been assessed quantitatively. Recycling of nutrients is one important ecosystem process that is directly influenced by fish. Fish species vary widely in the rates at which they excrete nitrogen and phosphorus; thus, altering fish communities could affect nutrient recycling. Here, we use extensive field data on nutrient recycling rates and population sizes of fish species in a Neotropical river and Lake Tanganyika, Africa, to evaluate the effects of simulated extinctions on nutrient recycling. In both of these species-rich ecosystems, recycling was dominated by relatively few species, but contributions of individual species differed between nitrogen and phosphorus. Alternative extinction scenarios produced widely divergent patterns. Loss of the species targeted by fishermen led to faster declines in nutrient recycling than extinctions in order of rarity, body size, or trophic position. However, when surviving species were allowed to increase after extinctions, these compensatory responses had strong moderating effects even after losing many species. Our results underscore the complexity of predicting the consequences of extinctions from species-rich animal communities. Nevertheless, the importance of exploited species in nutrient recycling suggests that overfishing could have particularly detrimental effects on ecosystem functioning.

Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots?

Rates of biogeochemical processes often vary widely in space and time, and characterizing this variation is critical for understanding ecosystem functioning. In streams, spatial hotspots of nutrient transformations are generally attributed to physical and microbial processes. Here we examine the potential for heterogeneous distributions of fish to generate hotspots of nutrient recycling. We measured nitrogen (N) and phosphorus (P) excretion rates of 47 species of fish in an N-limited Neotropical stream, and we combined these data with population densities in each of 49 stream channel units to estimate unit- and reach-scale nutrient recycling. Species varied widely in rates of N and P excretion as well as excreted N:P ratios (6-176 molar). At the reach scale, fish excretion could meet >75% of ecosystem demand for dissolved inorganic N and turn over the ambient NH4 pool in <0.3 km. Areal N excretion estimates varied 47-fold among channel units, suggesting that fish distributions could influence local N availability. P excretion rates varied 14-fold among units but were low relative to ambient concentrations. Spatial variation in aggregate nutrient excretion by fish reflected the effects of habitat characteristics (depth, water velocity) on community structure (body size, density, species composition), and the preference of large-bodied species for deep runs was particularly important. We conclude that the spatial distribution of fish could indeed create hotspots of nutrient recycling during the dry season in this species-rich tropical stream. The prevalence of patchy distributions of stream fish and invertebrates suggests that hotspots of consumer nutrient recycling may often occur in stream ecosystems.

Trophic Cascades and Phytoplankton Community Structure

Two predators of zooplankton, fish (yellow perch) and larval insects (Chaoborus), were manipulated within in situ mesocosms to assess their indirect effects on phytoplankton. The two predators caused similar reductions in zooplankton size and biomass, and as a consequence, zooplankton grazing rates on phytoplankton. However, phytoplankton increased relative to predator—free controls only in enclosures with fish and not in enclosures with Chaoborus, suggesting that fish have effects on phytoplankton independent of their effects on zooplankton grazing rates. Estimation of phosphorus excretion rates of zooplankton and fish suggests that fish render P more available to phytoplankton in two ways: (1) by directly excreting and egesting P, and (2) by increasing rates of P excretion by the zooplankton community. The latter effect resulted because small zooplankton have higher biomass—specific excretion rates than large zooplankton. The importance of nutrient regeneration is further supported by the response of phytoplankton community structure. Phytoplankton taxa exhibiting enhanced biomass in the presence of fish were those with high P requirements, including green and blue—green algae and dinoflagellates; other phytoplankton groups did not respond to manipulations. These results suggest that the mechanisms underlying the tropic cascade are complex and that predators affect phytoplankton by altering nutrient recycling rates as well as zooplankton grazing rates.

EFFECTS OF FOOD AVAILABILITY AND FISH PREDATION ON A ZOOPLANKTON COMMUNITY

The effects of fish predation and food availability on population densities and demography of zooplankton were investigated in Dynamite Lake, Illinois, USA, a lake with a high density of size-selective planktivorous fish and low food levels. Fish predators (bluegill sunfish) and food levels (phytoplankton) were manipulated in replicated, factorial- design field experiments during two summers (1980 and 1981). Overall, population densities of zooplankton were affected much more by manipulations of food availability than by manipulations of fish predation. The cladocerans Bosmina longirostris, Ceriodaphnia lacustris, and Diaphanosoma birgei were greatly increased in density by elevated phytoplankton levels in both years, in the presence and absence of fish. Demographic analysis in 1981 revealed that increased densities in response to elevated food levels resulted from both an increase in birth rates (Bosmina, Diaphanosoma) and a decrease in mortality rates (Ceriodaphnia, Diaphanosoma). The rotifers Lecane and Mon- ostyla also increased dramatically in response to elevated phytoplankton densities. Co- pepods were less responsive to manipulations of food levels, but several taxa exhibited increases in density in response to increased phytoplankton abundance. Few species were reduced in density by fish predation. Ceriodaphnia density was reduced by fish more than any other species in the entire community, and the density of even this species was much more affected by food availability. In terms of percent change relative to controls, increased food availability had much more of an effect than fish predation on the density of most zooplankton species and on total zooplankton abundance. Fish predation had several effects on the size structure and life history traits of the cladocerans. All three species attained larger sizes when fish were excluded than when fish were present. Cladoceran individuals also initiated reproduction at a smaller size and produced smaller offspring in the presence of fish. The reductions in mean body size, size at maturity, and offspring size in the presence of fish were most pronounced in Diapha- nosoma and Ceriodaphnia, the two largest species. Smaller body size and size at maturity apparently allow the cladocerans to reproduce before reaching a size at which they become vulnerable to size-selective fish predators. Larger size at first reproduction and larger off- spring size in the absence of fish may be a response to invertebrate predators, which assume more importance in the absence of fish and prey most heavily on smaller size classes. Flexibility in these life-history traits allows the cladocerans to withstand what appears to be intense size-selective predation by planktivorous fish.

Dissolved and particulate nutrient flux from three adjacent agricultural watersheds: A five-year study

Fluxes of dissolved and particulate nitrogen (N) and phosphorus(P) from three adjacent watersheds were quantified with ahigh-resolution sampling program over a five-year period. The watershedsvary by an order of magnitude in area (12,875, 7968 and 1206 ha), and inall three watersheds intensive agriculture comprises > 90% ofland. Annual fluxes of dissolved N and P per unit watershed area (exportcoefficients) varied ∼2X among watersheds, and patterns were notdirectly related to watershed size. Over the five-year period, meanannual flux of soluble reactive P (SRP) was 0.583 kg P ·ha−1 · yr−1 from the smallestwatershed and 0.295 kg P · ha−1 ·yr−1 from the intermediate-sized watershed, which hadthe lowest SRP flux. Mean annual flux of nitrate was 20.53 kg N ·ha−1 · yr−1 in the smallestwatershed and 44.77 kg N · ha−1 ·yr−1 in the intermediate-sized watershed, which had thehighest nitrate flux. As a consequence, the export ratio of dissolvedinorganic N to SRP varied from 80 (molar) in the smallest watershed to335 in the intermediate-sized watershed. Because most N was exported asnitrate, differences among watersheds in total N flux were similar tothose for nitrate. Hence, the total N:P export ratio was 42(molar) for the smallest watershed and 109 for the intermediate-sizedwatershed. In contrast, there were no clear differences among watershedsin the export coefficients of particulate N, P, or carbon, even though> 50% of total P was exported as particulate P in allwatersheds. All nutrient fractions were exported at higher rates in wetyears than in dry years, but precipitation-driven variability in exportcoefficients was greater for particulate fractions than for dissolvedfractions.Examination of hydrological regimes showed that, for all nutrientfractions, most export occurred during stormflow. However, theproportion of nitrate flux exported as baseflow was much greater thanthe proportion of SRP flux exported as baseflow, for all threewatersheds (25–37% of nitrate exported as baseflow vs.3–13% of SRP exported as baseflow). In addition, baseflowcomprised a greater proportion of total discharge in theintermediate-sized watershed (43.7% of total discharge) than theother two watersheds (29.3 and 30.1%). Thus, higher nitrateexport coefficients in the intermediate-sized watershed may haveresulted from the greater contribution of baseflow in this watershed.Other factors potentially contributing to higher nitrate exportcoefficients in this watershed may be a thicker layer of loess soils anda lower proportion of riparian forest than the other watersheds. Theamong-watershed variability in SRP concentrations and exportcoefficients remains largely unexplained, and might represent theminimum expected variation among similar agriculturalwatersheds.

Effects of Nutrients and Zooplankton Size on the Structure of a Phytoplankton Community

In situ enclosure experiments were conducted over two summers (1980- 1981) to assess the effects of nutrient (N and P) enrichment and zooplankton size structure on the phytoplankton community of an oligo-mesotrophic lake containing planktivorous fish and small zooplankton species. Exclusion of fish from the community resulted in an increase in mean individual zooplankton size, primarily because the cladocerans Cerio- daphnia and Diaphanosoma attained larger sizes. In 1980, total cladoceran biomass was also greater in the absence of fish. In 1980, total phytoplankton density was significantly lower in the fishless enclosures (where zooplankton were larger and grazing rates presumably higher), at a given nutrient level. The proportion of phytoplankton density comprising species with gelatinous sheaths or other protective coverings was greater in the fishless enclosures, under both enriched and unenriched conditions, presumably because these species are relatively resistant to zooplankton grazing. In 1981, when lower fish densities were used (than in 1980), total phytoplankton density was lower in the fishless enclosures only toward the end of the experiment and only in unenriched enclosures. In enriched enclosures the presence of fish had no effect on total phytoplankton density. However, the proportion of phytoplankton density made up of small, edible (to zooplankton) phytoplankton species was lower in the absence of fish throughout the experiment in both unenriched and enriched treatments. In both years, nutrient enrichment caused phytoplankton density to increase greatly, in the presence and absence of fish. Nutrient enrichment increased phytoplankton density a much greater amount than did reduction in zooplankton size. The results of these experiments demonstrate that even relatively small changes in zoo? plankton size (i.e., shifts in size within only small species) can result in significant alterations ofthe phytoplankton community. However, the increase in zooplankton body size resulting from fish exclusion could not buffer all effects of nutrient enrichment on total phytoplankton density.

“TOP–DOWN” TROPHIC INTERACTIONS IN LAKES: EFFECTS OF FISH ON NUTRIENT DYNAMICS

We conducted enclosure experiments over two summers in Tuesday Lake, Michigan, to assess how a gradient of zooplanktivorous fish biomass affected the dynamics of nutrients (nitrogen, N, and phosphorus, P), and their partitioning among ecosystem compartments. In both years, fish (the cyprinid Phoxinus eos) reduced the abundance of large zooplankton species and increased the biomass of phytoplankton as predicted by the top–down control hypothesis. Fish had strong effects on the dynamics and fluxes of N and P. Total P concentrations in the water column declined over time in all enclosures, but fish slowed the rate of decline. Thus total water column P increased with increasing fish biomass. Total N increased less strongly with increasing fish biomass, and thus the total N:P ratio decreased with increasing fish biomass. The concentrations of particulate carbon, nitrogen, and phosphorus in the water column also increased with increased fish biomass. Particulate N:P ratio decreased with increased fish biomass, but effects were weaker compared to effects on total N:P ratios. Nutrient ratios of the zooplankton fraction (particles >63 μm) showed a response that was transient but consistent with observed trends in zooplankton species composition. In particular, when the large cladocerans Daphnia and Holopedium increased upon exclusion of fish, C:P and N:P ratios of the zooplankton fraction showed distinct declines, corresponding to the relatively high body P contents of these taxa. Phosphorus budgets revealed that fish were a net source of P to the water column, because they lost mass during the experiments, even at densities below those in the lake. However, loss of P from fish could not account for the higher total P concentration observed in enclosures with fish compared to fishless enclosures. The absolute amount of P sinking from the water column increased with increasing fish biomass but decreased when expressed as percentage of total P sinking, again suggesting that the presence of fish increases the relative retention of P the water column. The rate of decline in water column total P in the presence of fish was accurately predicted by sedimentation of P from the water column and other fluxes. Our results support the hypothesis that fish can exert major influences on the dynamics, distribution, and ratios of limiting nutrients.

Nutrient Transport and Recycling by Consumers in Lake Food Webs: Implications for Algal Communities

Ecologists have recently focused much attention on quantifying the strengths and relative importance of resource-based (bottom-up) and predator-based (top-down) forces in food webs (e.g., Hunter and Price (1992), Power (1992), and Strong (1992)). Resource abundance and quality can have strong effects on the composition and dynamics of food webs, particularly primary producer assemblages (Tilman, 1982). Predators also have strong influences on lower trophic levels. Top predators in food webs may regulate the abundance of species at lower trophic levels; when the effects of top predators extend through the food web all the way to the primary producers the result is called a trophic cascade effect (Paine, 1980; Carpenter et al., 1985, 1987; McQueen et al., 1986; Power, 1990; Vanni et al., 1990).

ZOOPLANKTON ASSEMBLAGES IN FISHLESS BOG LAKES: INFLUENCE OF BIOTIC AND ABIOTIC FACTORS'

Some bog lakes in northern Wisconsin and Michigan lack fish because of low pH and low winter oxygen concentrations. The lakes are characterized by a dominance of large zooplankton species. Small zooplankton species are scarce, whereas in nearby lakes with fish they are common. The importance of biotic and abiotic factors in preventing the successful invasion of small zooplankton species into these fishless lakes was determined using a series of field manipulations. The relative importance of competition with large herbivores (the cladoceran Daphnia pulex), predation by large invertebrates (the dipteran Chaoborus americanus and the copepod Diaptomus leptopus), and abiotic conditions including pH were examined experimentally. Abiotic and/or resource conditions suppressed the population growth rate of 70% of the small zooplankton species introduced into enclosures in the fishless lakes relative to those introduced into enclosures in their resident lake (a lake with fish). Fewer small zooplankton species were suppressed in a similar experiment when pH was experimentally raised to 7, suggesting that pH is one factor that inhibits the successful invasion of small zooplankton into these lakes. Manipulations of large herbivores and invertebrate predators showed that predation was more important than competition in restricting the distribution of small species. Predation by Chaoborus primarily reduced the densities of crustaceans while predation by Diaptomus reduced the densities of rotifers. Competitive suppression of small zooplankton by Daphnia was not detected. The results suggest that both predation by Chaoborus and Diaptomus and abiotic conditions, including pH, are important factors determining zooplankton community structure in these fishless bog lakes.