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Ecology and salmon related articles

Riparian Soil Nitrogen Cycling and Isotopic Enrichment in
Response to a Long-Term Salmon Carcass Manipulation Experiment

by Megan L. Feddern, Gordon W. Holtgrieve, Steven S. Perakis, Julia Hart, Hyejoo Ro, Thomas P. Quinn
Ecosphere, November 21, 2019


Nitrogen pathways in soil where marine-derived nitrogen enters terrestrial systems via decay of salmon organic tissues or excretion from direct salmon consumers such as bears. Arrows represent conversion pathways with the potential to impart isotopic fractionations on plant-available nitrogen. Abstract

Pacific salmon acquire most of their biomass in the ocean before returning to spawn and die in coastal streams and lakes, thus providing subsidies of marine-derived nitrogen (MDN) to freshwater and terrestrial ecosystems. Recent declines in salmon abundance have raised questions of whether managers should mitigate for losses of salmon MDN subsidies. To test the long-term importance of salmon subsidies to riparian ecosystems, we measured soil nitrogen cycling in response to a 20-yr manipulation where salmon carcasses were systematically removed from one bank and deposited on the opposite bank along a 2-km stream in southwestern Alaska. Soil samples were taken at different distances from the stream bank along nine paired transects and measured for organic and inorganic nitrogen concentrations, and nitrogen transformation rates. Marine-derived nitrogen was measured using 15N/14N for bulk soils, and and soil pools. Stable isotope analyses confirmed 15N/14N was elevated on the salmon-enhanced bank compared to the salmon-depleted bank. However, 15N/14N values of plant-available inorganic nitrogen exceeded the 15N/14N of salmon inputs, highlighting nitrogen isotope fractionation in soils that raises significant methodological issues with standard MDN assessments in riparian systems. Surprisingly, despite 20 yr of salmon supplementation, the presence of MDN did not cause a long-term increase in soil nitrogen availability. This finding indicates the importance of MDN to ecosystem nitrogen biogeochemistry, and riparian vegetation may be overestimated for some systems. Given that essential nutrients can also be pollutants, we urge more critical analyses of the role of MDN to inform compensatory mitigation programs targeting salmon nutrient enhancement.

Introduction

Pacific salmon (Oncorhynchus spp.) migration from marine environments to freshwater spawning grounds is a textbook case of cross-ecosystem nutrient subsidies. Dozens of studies have identified the presence of marine-derived nitrogen (MDN) from salmon cross-ecosystem boundaries from oceans to freshwaters and into the terrestrial environment (sensu Polis et al. 2004, Gende et al. 2002, Schindler et al. 2003). Declines in Pacific salmon populations in many areas, caused by human activities (overharvest, habitat degradation, dams; Gustafson et al. 2007), and the concern over loss of MDN to coastal watersheds have made restoration of salmon nutrients a focal point for many management and mitigation strategies. For example, in the Columbia River Basin where Pacific salmon populations have declined, legislation requiring compensatory mitigation has led to nutrient enhancement programs, on the foundation that habitats have lost critical nutrients from salmon, and therefore, augmentation is necessary to maintain ecosystem function (Collins et al. 2015).

Salmon bring nutrients, including phosphorus (P) and other compounds in addition to nitrogen (N), into freshwater and terrestrial food webs through two pathways: (1) direct consumption of tissues by predators and scavengers, and (2) autotrophic or heterotrophic assimilation of nutrients released as salmon spawn, die, and eventually decay (Gende et al. 2002). Salmon are enriched in the heavy isotope of nitrogen (15N) relative to the light isotope (14N) when compared to terrestrial and watershed-derived N. This isotopic enrichment has been used to quantitatively trace the presence of salmon-derived nutrients into watersheds (Schindler et al. 2003). For example, the proportion of N derived from salmon ranges from approximately 30% to 75% in fish and aquatic invertebrates (Naiman et al. 2002), 10–90% in piscivorous mammals such as bears, and 20–40% in piscivorous fishes near salmon spawning grounds (Bilby et al. 1996, Hilderbrand et al. 1999, Chaloner et al. 2002, Claeson et al. 2006).

The annual return of this predictable and abundant, yet temporally limited, high-quality resource drives the foraging ecology of both terrestrial and aquatic consumers (Schindler et al. 2013, Quinn 2018). Carcasses and roe are documented food sources for over 22 species of mammals, birds (Cederholm et al. 1989), fishes (Scheuerell et al. 2007), and invertebrates (Minakawa et al. 2002, Meehan et al. 2005, Winder et al. 2005). Bear population density, body size, and reproductive output have been correlated with meat (primarily salmon) consumption, with piscivorous populations having 55 times higher density than their meat-limited counterparts (Hilderbrand et al. 1999). In aquatic ecosystems, salmon carcass abundance has been correlated with elevated growth rates of invertebrates, and with size, density, and condition factor of juvenile salmonids (Bilby et al. 1998, Minakawa et al. 2002, Wipfli et al. 2003).

The presence of MDN has been documented in aquatic primary producers, though its overall ecological importance remains ambiguous. Via this bottom-up pathway, salmon supply critical limiting nutrients that can increase primary and/or bacterial productivity, which are subsequently transferred to consumers and up through the food web (Wipfli et al. 1998, Chaloner et al. 2002, Holtgrieve and Schindler 2011). Higher salmon returns are correlated with MDN signatures in lower trophic levels including zooplankton and periphyton (Kline et al. 1993, Finney et al. 2000, Holtgrieve et al. 2010). Both direct ecological evidence and paleolimnological evidence suggest MDN and P positively influence primary production in lakes (Moore et al. 2007). For example, commercial fisheries remove upwards of two-thirds of MDN, which would otherwise enter some freshwater lakes in Alaska, resulting in a threefold decline in algal production (Schindler et al. 2005). In stream ecosystems, the decomposition of salmon increases dissolved organic and inorganic nutrients, including highly available forms such as orthophosphate () and ammonia/ammonium (NH3/). These nutrients can stimulate epilithon growth (bacteria and algae), though the magnitude of this response is highly variable and dependent on other growth limiting factors such as sunlight and disturbance (Johnston et al. 2004, Mitchell and Lamberti 2005, Janetski et al. 2009).

In the terrestrial realm, bottom-up effects of MDN from salmon are also thought to be ecologically important, though this has been difficult to demonstrate rigorously. Studies across the range of salmon in North America have inferred that up to 26% of foliar N in riparian plants is marine-derived, with foliar N levels often correlating with salmon abundance and distance from the salmon spawning location (e.g., Hocking and Reynolds 2012, Reimchen and Fox 2013). While MDN is clearly present in terrestrial producers, direct evidence of the importance of MDN for ecosystem function and productivity is much less evident. Helfield and Naiman (2001) measured tree growth increments in areas with and without salmon and found higher growth in one species (Sitka spruce) in areas where salmon nutrients were present, although these findings were later contested on statistical grounds (Kirchhoff 2003). Hocking and Reynolds (2012) observed decreased understory plant diversity with increasing salmon abundance, though this pattern was largely attributed to increased dominance of a single N-tolerant species (salmonberry). Reimchen and Fox (2013) suggested that salmon abundance increased tree growth, but tree ring 15N/14N values were not related to salmon abundance; other growth limiting factors such as temperature and location were important covariates. Most recently, Quinn et al. (2018) examined tree growth increments in the riparian zone of a small Alaskan stream before and after a 20-yr, >200,000 kg, salmon carcass manipulation. In the two decades prior to manipulation, white spruce (Picea glauca) on average grew faster on one bank compared to the other. The subsequent decades of carcass manipulation enriched the naturally slower growing side and were associated with increased growth. However, the growth effect of the carcasses was smaller than the natural side-to-side variation, and other important site and landscape factors such as forest demography, climate, aspect, and water availability were not fully considered, a common trend in MDN studies of riparian vegetation.

Interpreting the contributions of MDN to terrestrial producers using stable isotopes is often highly simplified, and does not consider how variability of N sources and overall N availability may confound results. MDN analyses apply simple two-source mixing models to infer the proportion of total N derived from salmon. When applied to terrestrial vegetation, the terrestrial end-member for the mixing models is typically determined by sampling the 15N/14N of the same species of plant either laterally away from the stream (where MDN contribution is expected to be small), upstream of barriers to salmon migration, or in watersheds without salmon. For the salmon end-member, a single value equal to the average 15N/14N of salmon (12.62 ± 0.31 per mil for sockeye salmon) is typically used (Appendix S1: Eq. S1). Inherent assumptions with these models therefore include the following: (1) reference sites are biogeochemically similar to salmon sites, and (2) the isotopic signature of salmon is unchanged in the soils prior to plant uptake. N cycling in soils is strongly controlled by position in the landscape and contains a number of chemical reactions that fractionate N isotopically (Högberg 1997, Wheeler et al. 2014; Fig. 1); therefore, these assumptions may not be valid.

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Megan L. Feddern, Gordon W. Holtgrieve, Steven S. Perakis, Julia Hart, Hyejoo Ro, Thomas P. Quinn
Riparian Soil Nitrogen Cycling and Isotopic Enrichment in Response to a Long-Term Salmon Carcass Manipulation Experiment
Ecosphere, November 21, 2019

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