Stable isotope analysis reveals different trophic niche spaces for wild and hatchery origin juvenile Chinook salmon in the Nisqually Delta

Hatchery programs have been used as a conservation tool to bolster declining Chinook salmon (Oncorhynchus tshawytscha) populations throughout much of the Salish Sea. In many watersheds, hatchery fish are released concurrently with the natural-origin population, thus raising the potential for density dependent effects via depleted prey resources, territorial behavior, and movement into sub-optimal habitats. Competition during the critical period for early marine growth and survival might have detrimental effects for wild Chinook salmon populations, highlighting the potential importance of a productive delta habitat mosaic. We used an integrated diet approach with stomach content and stable isotope analyses to evaluate differential patterns of habitat use and prey consumption in a fall run population of juvenile Chinook salmon from the Nisqually River Delta in Puget Sound. We examined size class and origin-level differences throughout the out-migration gradient, from freshwater riverine to nearshore habitat. Natural- and hatchery-origin smolts exhibited distinct habitat use patterns, whereby hatchery-origin individuals were captured less frequently in forested and transitional habitats, and more frequently in the nearshore. Consequently, hatchery-origin juveniles were less likely to consume terrestrial insect drift that was almost twice as energy rich as nearshore crustacean prey. Stable isotope signatures from muscle and liver tissues corroborated this finding, showing that while natural-origin Chinook salmon derived 24–31% of their diets from terrestrially sourced prey, terrestrial insects only made up 2–8% of hatchery-origin diets. This may have explained why natural-origin fish were in better condition and had stomach contents that were 15% more energy-rich on average than hatchery-origin fish. We did not observe strong evidence for trophic overlap in natural- and hatchery-origin juvenile Chinook salmon, but our results suggest that hatchery fish are less likely to take advantage of the terrestrial-aquatic interface, and could suffer behaviorally-mediated consequences to early marine growth and survival

Biplots of Nisqually River Delta invertebrate and fish stable isotope signatures.

To minimize variance and source overlap, invertebrates (Table 2) have been consolidated into coarser source groupings as follows: “riverine insects” (T1), “marsh insects” (T2), “riverine/marsh shoreflies and shorebugs” (T3/4/5), “riverine dipterans” (T6), “marsh dipterans” (T7), “riverine/marsh isopods” (A1/2), “delta mysids and shrimp” (A5/6), “riverine benthics” (B1/4/5), “marsh crustaceans” (B2), “delta crustaceans” (B3), and “delta polychaetes” (B6). Mean δ13C, δ15N, and δ34S values are adjusted for trophic fractionation based on estimates from Davis et al. [68]. Error bars represent ± 1 SD.</p

The Nisqually River Delta food web.

The Nisqually River Delta food web was interpreted from a Bayesian mixing model of δ13C and δ15N. Alphanumeric labels correspond with the source groupings in Table 1 and consumer groupings in Table 2. Thin arrows indicate a 10–24% proportion contribution to diet, medium arrows indicate a 25–50% proportion contribution to diet, and thick arrows indicate a >50% contribution to diet. White arrows show the diets of fish consumers, while black arrows show the diets of invertebrate consumers. Gray numbers along the left-hand side of the figure designate consumer trophic levels based on δ15N values. Primary sources and consumers are visualized along a gradient of delta habitat types with salinity increasing from left to right.</p

Primary source stable isotope signatures.

Terrestrial organic matter is believed to play an important role in promoting resilient estuarine food webs, but the inherent interconnectivity of estuarine systems often obscures the origins and importance of these terrestrial inputs. To determine the relative contributions of terrestrial (allochthonous) and aquatic (autochthonous) organic matter to the estuarine food web, we analyzed carbon, nitrogen, and sulfur stable isotopes from multiple trophic levels, environmental strata, and habitats throughout the estuarine habitat mosaic. We used a Bayesian stable isotope mixing model (SIMM) to parse out relationships among primary producers, invertebrates, and a pelagic and demersal fish species (juvenile Chinook salmon and sculpin, respectively). The study was carried out in the Nisqually River Delta (NRD), Washington, USA, a recently-restored, macrotidal estuary with a diverse habitat mosaic. Plant groupings of macroalgae, eelgrass, and tidal marsh plants served as the primary base components of the NRD food web. About 90% of demersal sculpin diets were comprised of benthic and pelagic crustaceans that were fed by autochthonous organic matter contributions from aquatic vegetation. Juvenile salmon, on the other hand, derived their energy from a mix of terrestrial, pelagic, and benthic prey, including insects, dipterans, and crustaceans. Consequently, allochthonous terrestrial contributions of organic matter were much greater for salmon, ranging between 26 and 43%. These findings demonstrate how connectivity among estuarine habitat types and environmental strata facilitates organic matter subsidies. This suggests that management actions that improve or restore lateral habitat connectivity as well as terrestrial-aquatic linkages may enhance allochthonous subsidies, promoting increased prey resources and ecosystem benefits in estuaries.</div

Pairwise comparisons of invertebrate consumer isotope signatures.

Pairwise comparisons of invertebrate consumer isotope signatures.</p

Percent contribution of primary sources to invertebrate consumer diets.

The percent contribution of primary sources to invertebrate consumer diets in the Nisqually River Delta was predicted using a Bayesian mixing model of δ13C and δ15N isotopes. Bar plots show the estimated mean posterior probability. Colors correspond to source groupings in Fig 7.</p

Percent contribution of invertebrate sources to fish diets.

The percent contribution of invertebrate sources to pelagic (Chinook salmon) and demersal (sculpin) fish diets in the Nisqually River Delta was predicted using a Bayesian mixing model of δ13C, δ15N, and δ34S isotopes. Bar plots show the estimated mean posterior probability. Sources that contributed to Table 2), marsh crustaceans (B2), and delta polychaetes (B6). Colors correspond to source groupings in Fig 3 (except for those sources that were excluded).</p

Estimated proportion of allochthonous and autochthonous organic matter contributions to Nisqually River Delta fish diets.

Allochthonous organic matter includes riverine plants and marsh C3 and C4 plants. Autochthonous organic matter includes riverine, marsh, and delta POM, marsh and delta diatoms, and delta plants.</p

Map of stable isotope sampling sites in the Nisqually River Delta, Puget Sound, Washington, USA.

Primary producers and invertebrate consumers were collected from the freshwater forested (FW), tidally influenced forested (FOR), transitional emergent marsh (EFT), estuarine emergent salt marsh (EEM), delta mudflat (DMF), and eelgrass (EEL) habitats of the Nisqually River Delta in 2015. We also sampled diatoms in the mudflats adjacent to historically-unaltered Animal Slough (EEM) and Red Salmon Slough (RSS) and in restored Madrone Slough (MAD) in 2011 (white stars). Circles in the right-hand panel represent locations where we captured juvenile Chinook salmon in 2011 and 2015 (all locations) and sculpin in 2011 (fyke nets only). Fish samples were collected across a broader spatial scale including the marine intertidal zone to account for the migratory behavior of juvenile salmon. Aerial imagery of the Nisqually River Delta (47°4′48″N, 122°42′20″W) was acquired by GeoTerra Inc. (Portland, Oregon, USA) in 2015.</p