Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams

In coastal areas of the North Pacific Ocean, annual returns of spawning salmon provide a substantial influx of nutrients and organic matter to streams and are generally believed to enhance the productivity of recipient ecosystems. Loss of this subsidy from areas with diminished salmon runs has been hypothesized to limit ecosystem productivity in juvenile salmon rearing habitats (lakes and streams), thereby reinforcing population declines. Using five to seven years of data from an Alaskan stream supporting moderate salmon densities, we show that salmon predictably increased stream water nutrient concentrations, which were on average 190% (nitrogen) and 390% (phosphorus) pre-salmon values, and that primary producers incorporated some of these nutrients into tissues. However, benthic algal biomass declined by an order of magnitude despite increased nutrients. We also measured changes in stream ecosystem metabolic properties, including gross primary productivity (GPP) and ecosystem respiration (ER), from three salmon streams by analyzing diel measurements of oxygen concentrations and stable isotopic ratios (delta O-O2) within a Bayesian statistical model of oxygen dynamics. Our results do not support a shift toward higher primary productivity with the return of salmon, as is expected from a nutrient fertilization mechanism. Rather, net ecosystem metabolism switched from approximately net autotrophic (GPP > or = ER) to a strongly net heterotrophic state (GPP < ER) in response to bioturbation of benthic habitats by salmon. Following the seasonal arrival of salmon, GPP declined to <12% of pre-salmon rates, while ER increased by over threefold. Metabolism by live salmon could not account for the observed increase in ER early in the salmon run, suggesting salmon nutrients and disturbance enhanced in situ heterotrophic respiration. Salmon also changed the physical properties of the stream, increasing air-water gas exchange by nearly 10-fold during peak spawning. We suggest that management efforts to restore salmon ecosystems should consider effects on ecosystem metabolic properties and how salmon disturbance affects the incorporation of marine-derived nutrients into food webs.     

Temperature-associated population diversity in salmon confers benefits to mobile consumers

Habitat heterogeneity can generate intraspecific diversity through local adaptation of populations. While it is becoming increasingly clear that population diversity can increase stability in species abundance, less is known about how population diversity can benefit consumers that can integrate across population diversity in their prey. Here we demonstrate cascading effects of thermal heterogeneity on trout-salmon interactions in streams where rainbow trout rely heavily on the seasonal availability of anadromous salmon eggs. Water temperature in an Alaskan stream varied spatially from 5 degrees C to 17.5 degrees C, and spawning sockeye salmon showed population differentiation associated with this thermal heterogeneity. Individuals that spawned early in cool regions of the 5 km long stream were genetically differentiated from those spawning in warmer regions later in the season. Sockeye salmon spawning generates a pulsed resource subsidy that supports the majority of seasonal growth in stream-dwelling rainbow trout. The spatial and temporal structuring of sockeye salmon spawn timing in our focal stream extended the duration of the pulsed subsidy compared to a thermally homogeneous stream with a single population of salmon. Further, rainbow trout adopted movement strategies that exploited the multiple pulses of egg subsidies in the thermally heterogeneous stream. Fish that moved to track the resource pulse grew at rates about 2.5 times higher than those that remained stationary or trout in the reference stream with a single seasonal pulse of eggs. Our results demonstrate that habitat heterogeneity can have important effects on the population diversity of dominant species, and in turn, influence their value to species that prey upon them. Therefore, habitat homogenization may have farther-reaching ecological effects than previously considered.     

Biotic control of stream fluxes: spawning salmon drive nutrient and matter export

Organisms can control movements of nutrients and matter by physically modifying habitat. We examined how an ecosystem engineer, sockeye salmon (Oncorhynchus nerka), influences seasonal fluxes of sediments, nitrogen (N), and phosphorus (P) in streams of southwestern Alaska. The purpose of this study was to investigate whether salmon act as net importers or net exporters of matter and nutrients from streams and how these roles change as a function of salmon population density. We measured discharge and concentrations of suspended sediments and total N and P every 7-14 days for up to four summers in 10 streams spanning a gradient in salmon densities. We statistically allocated whole-season fluxes to salmon activities, such as excretion and bioturbation, and to export by hydrologic discharge. In addition, we used counts of spawning salmon to estimate nutrient and matter imports by salmon to streams. Large seasonal pulses of suspended sediments, P, and N were associated with salmon spawning activities, often increasing export an order of magnitude higher than during pre-salmon levels. Years and streams with more salmon had significantly higher levels of export of sediments and nutrients. In addition, years with higher precipitation had higher background export of P and N. Salmon exported an average of the equivalent of 189%, 60%, and 55% of total matter, P, and N that salmon imported in their bodies. The relative magnitude of export varied; salmon exported more than their bodies imported in 80%, 20%, and 16% across all streams and years for sediments, P, and N, respectively. A bioassay experiment indicated that the P exported by salmon is directly available for use by primary producers in the downstream lake. These results demonstrate that salmon not only move nutrients upstream on large spatial scales via their migration from the ocean and subsequent death, but also redistribute matter and nutrients on finer spatial scales through their spawning activities.