Brad W. Taylor

Overfishing of Inland Waters

Abstract Inland waters have received only slight consideration in recent discussions of the global fisheries crisis, even though inland fisheries provide much-needed protein, jobs, and income, especially in poor rural communities of developing countries. Systematic overfishing of fresh waters is largely unrecognized because of weak reporting and because fishery declines take place within a complex of other pressures. Moreover, the ecosystem consequences of changes to the species, size, and trophic composition of fish assemblages are poorly understood. These complexities underlie the paradox that overexploitation of a fishery may not be marked by declines in total yield, even when individual species and long-term sustainability are highly threatened. Indeed, one of the symptoms of intense fishing in inland waters is the collapse of particular stocks even as overall fish production rises—a biodiversity crisis more than a fisheries crisis.

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.

VARIATION IN MAYFLY SIZE AT METAMORPHOSIS AS A DEVELOPMENTAL RESPONSE TO RISK OF PREDATION

Animals with complex life cycles often show large variation in the size and timing of metamorphosis in response to environmental variability. If fecundity increases with body size and large individuals are more vulnerable to predation, then organisms may not be able to optimize simultaneously size and timing of metamorphosis. The goals of this study were to measure and explain large-scale spatial and temporal patterns of phe- notypic variation in size at metamorphosis of the mayfly, Baetis bicaudatus (Baetidae), from habitats with variable levels of predation risk. Within a single high-elevation watershed in western Colorado, USA, from 1994 to 1996 we measured dry masses of mature larvae of the overwintering and summer generations of Baetis at 28 site-years in streams with and without predatory fish (trout). We also estimated larval growth rates and development times at 16 site-years. Patterns of spatial variation in mayfly size could not be explained by resource (algae) standing stock, competitor densities, or physical-chemical variables. However, size at metamorphosis of males and females of summer generation Baetis was smaller in fish streams than in fishless streams and decreased as densities of predatory stoneflies increased. Furthermore, overwintering individuals matured at larger sizes than summer generation Baetis, and the size of emerging Baetis declined over the summer, but predominantly in trout streams. Theoretical consideration of the effect of predation risk on size and timing of metamorphosis accurately predicted the observed temporal variation in size and timing of mayflies at emergence in fish and fishless streams. Baetis populations had similar growth rates but followed different developmental trajectories in high and low risk environments. In risky environments larval development was accelerated, resulting in metamorphosis of younger and smaller individuals, minimizing exposure of larvae to risk of mortality from trout predation, but at the cost of future reproduction. In safe environ- ments, larvae extended their development, resulting in larger, more fecund adults. Thus, we propose that large-scale patterns of variation in size and timing of metamorphosis represent adaptive phenotypic plasticity, whereby mayflies respond to variation in risk of predation, thereby maximizing their fitness in variable environments.

Improving the fluorometric ammonium method: matrix effects, background fluorescence, and standard additions

Abstract Our understanding of the N cycle is affected by how accurately we can measure NH4+ in natural waters. Measuring NH4+ concentrations requires accounting for matrix effects (ME) that are caused by substances in the sample that attenuate or intensify the signal of the samples relative to the standards. We show that the ME calculation in the recently published fluorometric NH4+ method is mathematically incorrect, producing results that consistently underestimate NH4+ concentration as a nonlinear function of the ME. We provide the correct equation and offer an alternative approach that accounts for ME by using sample water rather than deionized water to make the standards, thereby producing a standard curve that contains the same background chemical properties as the samples. In addition, we show that the previous method for measuring a samples background fluorescence does not include the background signal of the reagent or its interaction with the matrix constituents of the sample. We provide a new method for measuring a samples background fluorescence that includes the background fluorescence of the sample, reagent, and their interaction. The simple changes we suggest produce more accurate and precise NH4+ measurements.

INTERACTIONS BETWEEN HERBIVOROUS FISHES AND LIMITING NUTRIENTS IN A TROPICAL STREAM ECOSYSTEM

Ecologists have long been interested in understanding the strengths of con- sumer and resource limitation in influencing communities. Here we ask three questions concerning the relative importance of nutrients and grazing fishes to primary producers of a tropical Andean stream: (1) Are stream algae nutrient limited? (2) Are top-down and bottom-up forces of dual importance in limiting primary producers? (3) Do grazing fishes modulate the degree of resource limitation? We obtained several lines of evidence suggesting that Andean stream algae are nitrogen limited. Addition of nitrogen in flow-through channels resulted in major increases in algal standing crop, whereas there were no measurable effects of phosphorus enrichment. Inter- estingly, the N2-fixing cyanobacteria Anabaena was one of the taxa that responded most dramatically to the addition of nitrogen. Moreover, nutrient uptake rates were significantly higher for inorganic nitrogen (NO3-N and NH4-N) compared to phosphorus (PO4-P). Nutrients and the presence of grazing fishes were manipulated simultaneously in a series of experiments by using nutrient-diffusing substrates in fish exclusions vs. open cages accessible to the natural fish assemblage. We observed strong effects of both nitrogen addition and consumers on algal standing crop, although consumer limitation was found to be of considerably greater magnitude than resource limitation in influencing algal biomass and composition. Finally, the degree of resource limitation varied as a consequence of grazing fishes. Experiments examining nutrient limitation in the presence and absence of fishes showed that the response to nitrogen enrichment was significantly greater on sub- strates accessible to natural fish assemblages compared to substrates where grazing fishes were excluded. These experiments demonstrate simultaneous and interactive effects of top- down and bottom-up factors in limiting primary producers of tropical Andean streams. Whereas other studies have shown that consumers affect nutrient supply in ecosystems, our findings suggest that consumers can play an important role in influencing nutrient

PREDATOR CHEMICALS INDUCE CHANGES IN MAYFLY LIFE HISTORY TRAITS: A WHOLE-STREAM MANIPULATION

In high-elevation streams of western Colorado, mayflies ( Baetis bicaudatus) develop faster, but mature at a smaller size where trout are present compared to streams where fish are absent. These life history traits reduce the time of larval exposure to trout predation, but cost reduced fecundity. We designed a field experiment involving manipu- lation of whole streams to determine whether these changes were caused by the presence of brook trout, and specifically, whether they could be triggered by trout chemical cues. In 1999 and 2000, we introduced water from containers with brook trout (Salvelinus fon- tinalis) into five naturally fishless streams, and fishless stream water into five adjacent control streams, to determine whether these cues alone could induce the mayfly life history traits we have observed in natural trout streams. As in previous small-scale experiments, the size at which mayflies matured declined significantly in streams with added trout chem- icals but did not change in streams with fishless water only. Thus, life history traits similar to those observed in the field were induced within the natural variability inherent in streams. These results demonstrate the strength of this predator-prey interaction and indicate that brook trout are an important agent of natural selection on mayfly life history traits.

Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success

Abstract Many organisms with complex life cycles show considerable variation in size and timing at metamorphosis. Adult males of Megarcyssignata (Plecoptera: Perlodidae) are significantly smaller than females and emerge before females (protandry) from two western Colorado streams. During summer 1992 stoneflies from a trout stream emerged earlier in the season and at larger sizes than those from a colder fishless stream, and size at metamorphosis did not change over the emergence period in either stream. We performed two experiments to determine whether variation in size at metamorphosis affected the fecundity, reproductive success and longevity of individuals of this stonefly species and if total lifetime fecundity was affected by the number of matings. In the first experiment, total lifetime fecundity (eggs oviposited) was determined for adult females held in small plastic cages in the field. Males were removed after one copulation, or pairs were left together for life and allowed to multiply mate. Most copulations occurred in the first few days of the experiment. Females in treatments allowing multiple matings had significantly lower total lifetime fecundity and shorter adult longevity than females that only mated once. Multiple matings also reduced longevity of males. Fecundity increased significantly with female body mass at emergence, but only for females that mated once. While multiple matings eliminated the fecundity advantage of large female body size, number of matings did not affect the significant positive relationship between body mass at metamorphosis and longevity of males or females. In a second experiment designed to determine if body mass at emergence affected male mating success, we placed one large and one small male Megarcys in an observation arena containing one female and recorded which male obtained the first mating. The large and the small male had equal probabilities of copulating with the female. Copulations usually lasted all night, and the unmated male made frequent, but unsuccessful attempts to take over the copulating female. Our data suggest that selection pressures determining body size at metamorphosis may operate independently on males and females, resulting in evolution of sexual size dimorphism, protandry, and mating early in the adult stage. We emphasize the importance of interpreting the fitness consequences of larval growth and development on the timing of and size at metamorphosis in the context of the complete life cycle.

TROPICAL FISHES AS BIOLOGICAL BULLDOZERS: DENSITY EFFECTS ON RESOURCE HETEROGENEITY AND SPECIES DIVERSITY

We examined whether grazing fishes exert density-dependent effects on the spatial heterogeneity of resources and benthic species diversity in a tropical Andean stream. We hypothesized that bulldozer grazers (i.e., all or nothing grazing) can be important sources of spatial heterogeneity and that a unimodal relationship should exist between grazer density and resource heterogeneity. We reasoned that organismally generated heterogeneity would be minimal at low densities if grazers are ineffective, and at high densities if grazers thoroughly remove resources. In contrast, spatial heterogeneity should be highest at inter- mediate densities as bulldozer grazers maintain a dynamic mosaic of resource states. We posited that a corresponding unimodal relationship should exist between grazer density and benthic diversity, if resource heterogeneity is an important mechanism maintaining species diversity. We carried out observational and experimental studies to test our hypotheses. First, we quantified natural spatial patterns of benthic resources across transects using fish feeding scars as surrogates. We then analyzed data using a set of landscape indices that capture different components of heterogeneity. A large degree of spatial heterogeneity of algal and sediment resources was apparent both within and among pools. Second, we manipulated densities of the common grazing fish Parodon apolinari (Parodontidae) in 8-m 2 pens, and quantified spatial heterogeneity and corresponding benthic diversity within enclosures. Par- odon exerted strong density-dependent effects on the spatial heterogeneity of resources. Initially (at 7 d) we observed a unimodal relationship between grazer density and spatial heterogeneity along our density gradient (1.25-10.0 Parodon/m 2 ), as predicted. However, at 14 d, our lowest fish density (1.25 Parodon/m 2 ) was sufficient to generate substantial spatial heterogeneity. Although grazers were major sources of heterogeneity, we found little support for the hypothesis that organismally generated heterogeneity is an important mech- anism for maintaining species diversity. Interestingly, the greatest invertebrate richness occurred in high density treatments, which had the most spatially uniform resource distri- butions. These results suggest that at the within-pool scale, grazers can have important effects on both spatial heterogeneity and benthic diversity, yet their generation of resource patchiness does not appear to be the underlying mechanism driving strong fish effects on species diversity.

Rapid size-specific changes in the drift of Baetis bicaudatus (Ephemeroptera) caused by alterations in fish odour concentration

Abstract Chemical cues from fish can alter the behaviour of stream invertebrates in experimental tanks but their effect in natural streams has received little attention. By adding brook trout (Salvelinus fontinalis) odour to a trout stream in the Rocky Mountains of Colorado, USA, we tested whether changes in the concentration of chemical cues from visually feeding predatory fish would alter the drift of mayfly nymphs (Ephemeroptera). Stream water was piped from stream-side tanks with (odour) and without (control) three brook trout to two locations in the stream 3.5 m upstream of drift nets at six replicate sites. Five-minute drift samples were collected downstream from odour and control pipes before, during and after the release of water from the tanks into the stream during both the day and night. Almost all drift occurred at night and consisted predominantly of Baetis bicaudatus nymphs. The odour manipulation had no measurable effect on Baetis drift during the day but statistical power was low. During the night, however, the drift of large (>0.65 mm head capsule width, HCW) Baetis nymphs decreased significantly during the odour addition compared to control drift. In contrast, the drift of small nymphs (≤0.65 mm HCW) increased both during and after the odour addition in comparison to control drift. Since the stream contains brook trout (0.04–0.18 m−2), and water from the stream (presumably containing fish odour) altered the behaviour of fishless-stream Baetis nymphs in another experiment, we conclude that the changes in Baetis drift density were a response to an increase in the concentration of fish odour in the stream. Furthermore, we were able to detect the effect within 5 min. of odour addition, indicating that mayfly behavioural response to trout odour was rapid. These results suggest that mayflies can distinguish different concentrations of trout odour in natural streams and that the response is size-specific, according to the relative risk of predation of large and small Baetis.

Ecosystem Engineering by a Tropical Tadpole: Density-Dependent Effects on Habitat Structure and Larval Growth Rates

Tadpoles of the web-footed frog, Rana palmipes, are epibenthic consumers that are widely distributed in the Neotropics. Rana tadpoles feed on algae and sediments and potentially act as ecosystem engineers by modifying habitat structure via their foraging activities. We conducted two experiments in the Andean piedmont of Venezuela to examine the following questions: (1) Can Rana tadpoles influence benthic sediment distributions? (2) Are growth rates of sediment-feeding tadpoles density dependent? and (3) Are sediments viable nutritional sources for tadpoles? A field enclosure experiment was conducted in which sediment accrual and daily growth rates were compared among four tadpole density treatments ranging from 1 to 10 individuals per m2. Tadpoles had highly significant effects on stream sediment accrual that were inversely related to tadpole density; thus, benthic sediments rapidly accumulated when tadpole density was low (one tadpole per m2), whereas substrata were thoroughly cleared of sediments when tadpole densities were high (10 tadpoles per m2). Furthermore, over the course of the experiment, daily growth rates of tadpoles were strongly affected by tadpole density, and individuals from low-density treatments displayed greater than five times the daily growth of tadpoles from highdensity treatments. A second experiment was conducted in wading pools to assess the importance of benthic stream sediments as a nutritional source for tadpoles. Tadpole daily growth and development were measured in pools in which diets were supplemented with stream sediments and compared to tadpoles from pools with no sediment addition. Tadpoles displayed net positive growth and significantly higher development rates when stream sediments were added to wading pools. In contrast, tadpoles lost weight in the absence of sediment supplements. Our results suggest that tadpoles can act as ecosystem engineers by reducing sediment accrual rates;