Concepts such as "window of opportunity" and "bottleneck" have been given survival significance in estuaries since we first began evaluating that phase of Pacific salmon (Oncorhynchus spp.) early life histories. Estuarine windows of opportunity and bottlenecks both refer to the influence of estuarine conditions (e.g., food, predators, physicochemical conditions affecting physiology and performance, etc.) to enhance or detract from overall survival disproportional to influences in fresh water or the ocean. Early salmon management, and particularly salmon hatchery release policies which generally sought to hold fish to a size and time that minimized estuarine utilization, tended to consider estuaries as "sinks," contributing more to juvenile salmon mortality than survival; despite contrary evidence, these attitudes and practices still persist in many governmental and private salmon hatcheries. These concepts are more recently represented in management paradigms promoting artificial enhancement and manipulation (e.g., salmon hatchery releases) that can be controlled "adaptively" in comparative real time to take advantage of estuarine conditions in order to maximize survival and buffer poor ocean conditions. In employing any of these concepts, we imply that favorable conditions for juvenile salmon rearing in estuaries are "scheduled" or reach some "optimum" or "convergence" that may dictate survival to return as adults. This issue avoids the question of whether the effect of estuarine productivity is independent of other mortality factors in the sequential salmon life history continuum, or whether there are either compensatory or depensatory relationships between estuarine factors and those affecting freshwater and ocean survival.
One factor commonly considered to regulate salmon survival in estuaries is the availability of prey resources; that is, that food carrying capacity is often limiting and that juvenile salmon have evolved to take advantage of maximal periods of estuarine productivity. This might be considered the "bottom-up" regulation of overall salmon production by some average quantity and timing of primary producers and consumers supporting estuarine food webs utilized by juvenile salmon. This is somewhat contrary to the observation that Pacific salmon populations, with their relatively long numerical response times, have evolved diverse life history strategies (types, races, tactical). These strategies compensate for environmental variation across time and space scales through their entire life cycle, and will tend to average out high frequency components of environmental variation (e.g., interannual/freshwater-estuarine-marine), and respond to low frequency components of variability affecting salmon survival (e.g., oceanic regime shifts). It is also important to realize that "top-down" influences, in which predation or competition independent of salmon size or density prevail, may be just as valid a regulator of salmon production.
A bottom-up view of salmon production in estuaries also assumes that the quantity or quality of food can directly or indirectly limit survival—directly by reducing growth and increasing size-dependent mortality, and indirectly by altering salmon behavioral responses (e.g., migration patterns and rates) that increase their risk to mortality agents such as predators. Understanding spatial and temporal variability in the availability of food organisms, as well as the food web processes that support them, might provide a view into comparable variability in salmon survival. Unfortunately, our appreciation of the effects of estuarine variability have not advanced measurably since reviewed in the predecessor workshop in 1983 (Levings 1984, Levy 1984, Simenstad and Wissmar 1984). While we have a marginally better understanding of the structure and processes in estuarine food webs that contribute to salmon production, there has really been no advancement in our understanding of the spatial and temporal variability in food web linkages to salmon or of the response by individual salmon or their populations to this variability.
The essence of estuaries is that they are extremely variable, pulsed ecosystems; the quantity, composition, timing, and rate of primary and secondary production processes supporting juvenile salmon varies extensively over space and time. Juvenile salmon themselves pulse through the systems, although now perhaps at more punctuated frequencies than in prehatchery eras. Because of the relative independence of many factors regulating the dynamics of juvenile salmon migrations through estuaries and the production of prey organisms and associated food web processes, overlap and coincidence of salmon with peak prey resource availability are likely to be random and uncoupled.
Food webs of estuaries in the Pacific Northwest are based predominantly on detritus, but the composition of organic matter contributing to the estuarine detritus pool may vary significantly depending upon location (e.g., ecoregion), extent and type of watershed and estuary, climate, geology, and oceanic energy regime, among many factors. Comprehensive, estuary-scale accounting of organic matter production and consumption has not been attempted for many estuaries in the region, but annual carbon input budgets have been calculated for three contrasting estuaries: Hood Canal (Simenstad and Wissmar 1985), Grays Harbor (Thom 1981, 1984), and the Columbia River estuary (Simenstad et al. 1990). Not surprisingly, given the considerably greater extent of the Columbia River watershed, the total annual loading of organic carbon to that estuary is about five orders of magnitude greater than either Hood Canal or Grays Harbor (Fig. 1a). While import of fluvial organic matter dominates both the Columbia River estuary (87.2%) and Grays Harbor (80.1%) carbon budgets, phytoplankton (59.7%), and benthic algae (29.7%) contribute much more to the Hood Canal budget, and eelgrass production is of significance (11.3%) primarily in Grays Harbor; emergent marsh production is comparatively insignificant (1.4-4.8%) in all three systems (Fig. 1b).
However, delivery of these different organic matter constituents to the estuarine food web is neither proportional nor coincident to the source inputs. The quality of organic matter is fundamentally more important than bulk organic contribution to the estuary, implying that the sources of organic matter to the estuarine detritus pool may be more important than the bulk delivery. Terrestrial and marsh detritus tends to be much more refractory, and less efficiently incorporated into the estuarine food web, than phytoplankton and benthic algae. Riverine input tends to correspond to river discharge, peaking with winter storms and spring snowmelt, while organic matter from eelgrass production enters the estuary in late winter, benthic algae and phytoplankton in mid-summer, and emergent marsh in the fall (Fig. 2; Thom 1987). Some food web pathways may be almost immediate, as suggested for the incorporation of estuarine foam into littoral flat consumers (Wissmar and Simenstad 1984).
Irrespective of the variation in quantity, quality, and timing of organic matter contributing to the food web, we continue to accumulate evidence that certain species and life history stages of juvenile salmon focus their foraging in estuaries on certain types of prey, which in some cases may be an important factor determining estuarine residence time and growth (Wissmar and Simenstad 1988). Results from our on-going studies of juvenile salmon use of estuarine wetlands in Puget Sound and coastal Washington continue to sustain earlier interpretations that certain salmon species and life history types (e.g., chum salmon, O. keta, and subyearling chinook salmon, O. tshawytscha) prey selectively on specific benthic or epibenthic organisms, such as amphipods (Corophium spp.) and harpacticoid copepods (Harpacticus uniremis, Tisbe sp.) (Simenstad et al. 1988; Wissmar and Simenstad 1988). If we have acquired any additional understanding, it is from tidal freshwater and brackish wetlands, where we also find juvenile salmon (subyearling chinook and coho, O. kisutch) feeding concentrated on emergent marsh and riparian insects (e.g., chironomids, aphids) (Shreffler et al. 1992; Miller 1993; Simenstad et al. 1992, 1993, in press; Miller and Simenstad in revision).
One recent tool that is providing a more powerful identifier of estuarine food web variability is the use of stable natural isotopes, and particularly multiple isotopes (e.g., d 13C, d 15N, d 34S) because significant overlap can occur among isotopic signatures of different organic sources for any one isotope (e.g., differentiating terrestrial inputs from brackish marsh would be impossible without coupling d 34S with d 13C; addition of d 13C further distinguishes trophic level shifts). While d 13C analyses of food web sources and pathways have been used to investigate a variety of estuarine systems (e.g., Hood Canal, Simenstad and Wissmar 1985; Padilla Bay, Puget Sound, Simenstad and Wissmar 1985; Fraser River estuary, Levings 1994; Willapa Bay and Columbia River estuary, C. Simenstad, unpubl. data, School of Fisheries, University of Washington, Box 357980, Seattle, WA 98195-7980), the addition of d 15N has been incorporated for a few of those systems (Padilla Bay, Fraser River) and d 34S has been added for only Willapa Bay and the Columbia River estuary.
As more data from stable isotope studies in these different estuaries emerge, it is becoming apparent that organic matter production and food web processes supporting juvenile salmon production differ across estuaries, often irrespective of seemingly deterministic food web pathways. For instance, d 13C of epibenthic harpacticoid copepods and amphipods may vary by as much as 11‰ (-9‰ to -20‰), and the same species, Corophium salmonis, can differ by as much as 5.5‰ in adjacent estuaries (Willapa Bay, -18.9‰ vs. Columbia River estuary, -24.4‰). Spatial variation within the same estuary is also evident, as indicated by a wide range in d 13C of chinook salmon fry (approximately 20‰ to -30‰) and narrow range (approximately -34‰ to -36‰) for coho salmon presmolts found in the lower Fraser River (Levings 1994), and -19.8‰ for the calanoid copepod Eurytemora affinis in the brackish channels of the Columbia River estuary vs. -29.9‰ from the estuarine turbidity maxima in the portion of the same estuary with varying salinities (Simenstad, unpubl. data, School of Fisheries, University of Washington, Box 357980, Seattle, WA 98195-7980); where the d 15N signature, 7.4, did not differ at all between these samples). These preliminary indicators of food web pathway variability suggest that both differential pulses of organic matter and heterogeneous distributions of the material across an estuary may account for dramatically different trophic support of secondary consumers such as salmon, especially when salmon localize their rearing and migrations in a specific estuarine region or habitat.
As described in the predecessor workshop in 1983 (Levings 1984; Levy 1984; Simenstad and Wissmar 1984), the issue of carrying capacity limitations for juvenile salmon still remains an untested enigma. Few studies have attempted to describe juvenile salmon production, much less survival, relative to temporal and spatial variability in estuarine biochemical conditions, and most of these are prior to 1983. The descriptive comparisons of juvenile fall chinook salmon relative abundance and size in 11 Oregon estuaries in 1977-82 by Herring and Nicholas (1983) still remains one of the few comparisons between salmon use and estuarine structure. Across the distribution of estuary (at mean lower low water) area, from 6,180 ha for Coos Bay to 90 ha for the Chetco River estuary (Fig. 3a), they found a trend in increasing catch per unit effort (CPUE) and decreasing mean fish size (Fig. 3b), although considerable variability in these trends was also evident. Interannual variation was also prevalent within the inverse estuary area/fish length relationship (Fig. 4). Suggestion of a density-dependent limitation on fish growth and production (assuming equal emigration and immigration rates), as indicated by fish length, was implicated beyond a CPUE threshold of about 10 to 20 fish per set (Fig. 5). This may coincide with observations from 16 British Columbia estuaries between 1970 and 1982 (Levings 1984) and our own comprehensive estuarine catch data (C. Simenstad, unpubl. data, School of Fisheries, University of Washington, Box 357980, Seattle, WA 98195-7980) that it is rare to find juvenile chinook salmon densities higher than about 1.0 fish m-2. The implications of an estuarine carrying capacity, as modulated by salmon life history type and timing of estuarine entry, is still sustained principally by Reimer's (1973) seemingly ageless study of the survival of chinook salmon life history type in the Sixes River estuary, which we still have yet to repeat or expand upon for any other estuaries.
While the paradigm of detritus-based estuarine food webs may still be generally applicable across salmonid ecosystems, the actual food web processes supporting specific salmonid prey may not be as indicative of broad-based detritus inputs. Factors regulating the production of primary consumers may not necessarily depend on the availability of food resources; while there appear to be chronosequences of benthic/epibenthic prey community structure and production, considerable temporal and spatial variability prevail. Production of key prey species distributed across estuarine gradients, such as insects (chironomids; tidal freshwater-brackish), amphipods (Corophium spp., brackish-mesohaline), and harpacticoid copepods (Harpacticus uniremis, Tisbe sp.; salinities varying from 5 ppt to over 30 ppt) may not be coincident, and not necessarily linked to processes (natural, or anthropogenically "managed") that regulate juvenile salmon entry, residence, and survival in the estuary. Alternatively, both physical (inflow, temperature) and biological (primary production, predation) factors that affect juvenile salmon and their prey production may be optimal during estuarine residence, but may not coincide with subsequent ocean conditions. Diversity in Pacific salmon species, racial, and tactical life history strategies, which has likely declined under historic exploitation and management, may offer one clue of the salmon's evolutionary solution to such variability in estuarine conditions.
Ultimately, we must recognize that increased knowledge about the influence of dynamic ecosystems such as estuaries on salmon is more likely to elucidate the constraints upon alternative salmon management strategies rather than predictable relationships that can be used to take advantage of estuaries. As pointed out by Levings (1984), it may be entirely unrealistic to use production at lower trophic levels as indicators of estuarine (juvenile salmon) production potential given the variability in fish dependence on specific prey or the spatial distribution of prey.
From salmon biologists' perspectives, ecosystem management of salmon must ultimately deal with managing man's adverse impacts on critical ecosystem processes, and within the scope of natural variability, rather than managing ecosystems per se. Understanding the scope of salmon population responses to estuarine variability will require considerably more focused and intense research into issues such as the following: 1) links between variation in estuarine organic matter production and consumer population dynamics, 2) whether pulses of salmon prey resources are interlinked with salmon behavior, 3) relationships between organic matter quality (sources) and consumer (salmon prey) production, 4) variation in juvenile salmon estuarine entry, residence time, growth and mortality, and relationship to primary and secondary food web pulses, 5) effect of life history diversity on estuarine-ocean variability, and 6) the presence or lack of interdependence between estuarine survival and ocean survival.
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