Habitat modulates population-level responses of freshwater salmon growth to a century of change in climate and competition.

The impacts of climate change are widespread and threaten natural systems globally. Yet, within regions, heterogeneous physical landscapes can differentially filter climate, leading to local response diversity. For example, it is possible that while freshwater lakes are sensitive to climate change, they may exhibit a diversity of thermal responses owing to their unique morphology, which in turn can differentially affect the growth and survival of vulnerable biota such as fishes. In particular, salmonids are cold-water fishes with complex life histories shaped by diverse freshwater habitats that are sensitive to warming temperatures. Here we examine the influence of habitat on the growth of sockeye salmon (Oncorhynchus nerka) in nursery lakes of Canada's Skeena River watershed over a century of change in regional temperature and intraspecific competition. We found that freshwater growth has generally increased over the last century. While growth tended to be higher in years with relatively higher summer air temperatures (a proxy for lake temperature), long-term increases in growth appear largely influenced by reduced competition. However, habitat played an important role in modulating the effect of high temperature. Specifically, growth was positively associated with rising temperatures in relatively deep (>50 m) nursery lakes, whereas warmer temperatures were not associated with a change in growth for fish among shallow lakes. The influence of temperature on growth also was modulated by glacier extent whereby the growth of fish from lakes situated in watersheds with little (i.e., <5%) glacier cover increased with rising temperatures, but decreased with rising temperatures for fish in lakes within more glaciated watersheds. Maintaining the integrity of an array of freshwater habitats-and the processes that generate and maintain them-will help foster a diverse climate-response portfolio for important fish species, which in turn can ensure that salmon watersheds are resilient to future environmental change.

Bias in self-reported parasite data from the salmon farming industry.

Many industries are required to monitor themselves in meeting regulatory policies intended to protect the environment. Self-reporting of environmental performance can place the cost of monitoring on companies rather than taxpayers, but there are obvious risks of bias, often addressed through external audits or inspections. Surprisingly, there have been relatively few empirical analyses of bias in industry self-reported data. Here, we test for bias in reporting of environmental compliance data using a unique data set from Canadian salmon farms, where companies monitor the number of parasitic sea lice on fish in open sea pens, in order to minimize impacts on wild fish in surrounding waters. We fit a hierarchical population-dynamics model to these sea-louse count data using a Bayesian approach. We found that the industry's monthly counts of two sea-louse species, Caligus clemensi and Lepeophtheirus salmonis, increased by a factor of 1.95 (95% credible interval: 1.57, 2.42) and 1.18 (1.06, 1.31), respectively, in months when counts were audited by the federal fisheries department. Consequently, industry sea-louse counts are less likely to trigger costly but mandated delousing treatments intended to avoid sea-louse epidemics in wild juvenile salmon. These results highlight the potential for combining external audits of industry self-reported data with analyses of their reporting to maintain compliance with regulations, achieve intended conservation goals, and build public confidence in the process.

Marine subsidies mediate patterns in avian island biogeography.

The classical theory of island biogeography, which predicts species richness using island area and isolation, has been expanded to include contributions from marine subsidies, i.e. subsidized island biogeography (SIB) theory. We tested the effects of marine subsidies on species diversity and population density on productive temperate islands, evaluating SIB predictions previously untested at comparable scales and subsidy levels. We found that the diversity of terrestrial breeding bird communities on 91 small islands (approx. 0.0001-3 km2) along the Central Coast of British Columbia, Canada were correlated most strongly with island area, but also with marine subsidies. Species richness increased and population density decreased with island area, but isolation had no measurable influence. Species richness was negatively correlated with marine subsidy, measured as forest-edge soil δ15N. Density, however, was higher on islands with higher marine subsidy, and a negative interaction between area and subsidy indicates that this effect is stronger on smaller islands, offering some support for SIB. Our study emphasizes how subsidies from the sea can shape diversity patterns on islands and can even exceed the importance of isolation in determining species richness and densities of terrestrial biota.

Oust the louse: leaping behaviour removes sea lice from wild juvenile sockeye salmon Oncorhynchus nerka.

We conducted a manipulative field experiment to determine whether the leaping behaviour of wild juvenile sockeye salmon Oncorhynchus nerka dislodges ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis by comparing sea-lice abundances between O. nerka juveniles prevented from leaping and juveniles allowed to leap at a natural frequency. Juvenile O. nerka allowed to leap had consistently fewer sea lice after the experiment than fish that were prevented from leaping. Combined with past research, these results imply potential costs due to parasitism and indicate that the leaping behaviour of juvenile O. nerka does, in fact, dislodge sea lice.

Effects of habitat features on size-biased predation on salmon by bears.

Predators can drive trait divergence among populations of prey by imposing differential selection on prey traits. Habitat characteristics can mediate predator selectivity by providing refuge for prey. We quantified the effects of stream characteristics on biases in the sizes of spawning salmon caught by bears (Ursus arctos and U. americanus) on the central coast of British Columbia, Canada by measuring size-biased predation on spawning chum (Oncorhynchus keta) and pink (O. gorbuscha) salmon in 12 streams with varying habitat characteristics. We tested the hypotheses that bears would catch larger than average salmon (size-biased predation) and that this bias toward larger fish would be higher in streams that provide less protection to spawning salmon from predation (e.g., less pools, wood, undercut banks). We then we tested for how such size biases in turn translate into differences among populations in the sizes of the fish. Bears caught larger-than-average salmon as the spawning season progressed and as predicted, this was most pronounced in streams with fewer refugia for the fish (i.e., wood and undercut banks). Salmon were marginally smaller in streams with more pronounced size-biased predation but this predictor was less reliable than physical characteristics of streams, with larger fish in wider, deeper streams. These results support the hypothesis that selective forces imposed by predators can be mediated by habitat characteristics, with potential consequences for physical traits of prey.

Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon.

Species' life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage-structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co-variation in salmonids, we generate new hypotheses for the evolution of trade-offs among life history traits.

Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon.

Large male body size is typically favored by directional sexual selection through competition for mates. However, alternative male life-history phenotypes, such as "sneakers," should decrease the strength of sexual selection acting on body size of large "fighter" males. We tested this prediction with salmon species; in southern populations, where sneakers are common, fighter males should be smaller than in northern populations, where sneakers are rare, leading to geographical clines in sexual size dimorphism (SSD). Consistent with our prediction, fighter male body size and SSD (fighter male∶female size) increase with latitude in species with sneaker males (Atlantic salmon Salmo salar and masu salmon Oncorhynchus masou) but not in species without sneakers (chum salmon Oncorhynchus keta and pink salmon Oncorhynchus gorbuscha). This is the first evidence that sneaker males affect SSD across populations and species, and it suggests that alternative male mating strategies may shape the evolution of body size.

Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages.

A signature of nonrandom phylogenetic community structure has been interpreted as indicating community assembly processes. Significant clustering within the phylogenetic structure of a community can be caused by habitat filtering due to low nutrient availability. Nutrient limitation in temperate Pacific coastal rainforests can be alleviated to some extent by marine nutrient subsidies introduced by migrating salmon, which leave a quantitative signature on the makeup of plant communities near spawning streams. Thus, nutrient-mediated habitat filtering could be reduced by salmon nutrients. Here, we ask how salmon abundance affects the phylogenetic structure of riparian flowering plant assemblages across 50 watersheds in the Great Bear Rainforest of British Columbia, Canada. Based on a regional pool of 60 plant species, we found that assemblages become more phylogenetically dispersed and species poor adjacent to streams with higher salmon spawning density. In contrast, increased phylogenetic clumping and species richness was seen in sites with low salmon density, with steeper slopes, further from the stream edge, and within smaller watersheds. These observations are all consistent with abiotic habitat filtering and biotic competitive exclusion acting together across local and landscape-scale gradients in nutrient availability to structure assembly of riparian flowering plants. In this case, rich salmon nutrients appear to release riparian flowering-plant assemblages from the confines of a low-nutrient habitat filter that drives phylogenetic clustering.

Nutrients from spawning salmon influence leaf area, tissue density, and nitrogen-15 in riparian plant leaves.

Nutrient subsidies have significant impacts on ecosystems by connecting disjunct habitats, often through long-distance animal migrations. Salmon migrations on the North Pacific coasts provide these kinds of nutrient subsidies from senescent fish at the end of their life cycle, which can have significant ecological effects on terrestrial species. This can include impacts on individuals, populations, and communities, where shifts in community composition towards plant species that indicate nitrogen-rich soils have been documented. We investigated the effects of variation in salmon spawning density on the leaf traits of four common riparian plant species on the central coast of British Columbia, Canada. We found that all plant species had higher foliar salmon-derived nitrogen on streams with a higher spawning density. Three of the four species had larger leaves, and one species also had higher leaf mass per area on streams with more salmon. However, we found no differences in leaf greenness or foliar percent nitrogen among our study streams. These results demonstrate that nutrient subsidies from spawning salmon can have significant impacts on the ecology, morphology, and physiology of riparian plants, which lends support to a mechanism by which certain plants are more common on productive salmon streams.

Salmon subsidize an escape from a size spectrum.

A general rule in ecology is that the abundance of species or individuals in communities sharing a common energy source decreases with increasing body size. However, external energy inputs in the form of resource subsidies can modify this size spectrum relationship. Here, we provide the first test of how a marine resource subsidy can affect size spectra of terrestrial communities, based on energy derived from Pacific salmon carcasses affecting a forest soil community beside streams in western Canada. Using both species-based and individual approaches, we found size structuring in this forest soil community, and transient community-wide doubling of standing biomass in response to energy pulses from Pacific salmon carcasses. One group of species were clear outliers in the middle of the size spectrum relationship: larval calliphorid and dryomyzid flies, which specialize on salmon carcasses, and which showed a tenfold increase in biomass in their size class when salmon were available. Thus, salmon subsidize their escape from the size spectrum. These results suggest that using a size-based perspective of resource subsidies can provide new insights into the structure and functioning of food webs.

Experimental addition of marine-derived nutrients affects wildflower traits in a coastal meta-ecosystem.

Organismal movement can bring individuals, resources and novel interactions across ecosystem boundaries and into recipient habitats, thereby forming meta-ecosystems. For example, Pacific salmon ecosystems receive large marine-derived nitrogen subsidies during annual spawning events, which can have a wide range of effects on aquatic and terrestrial plant species and communities. In this study, we evaluate the effects of cross-ecosystem nutrient subsidies on terrestrial plant growth and reproduction. We conducted a large-scale field experiment with four treatments: (i) addition of a pink salmon (Oncorhynchus gorbuscha) carcass, (ii) addition of the drift seaweed rockweed (Fucus distichus), (iii) addition of both salmon + rockweed, and (iv) a control. We examined treatment effects on leaf nitrogen and fitness-associated floral traits in four common estuarine wildflower species. We found elevated leaf ∂15N in all plant species and all sampling years in treatments with salmon carcass additions but did not observe any differences in leaf per cent nitrogen. We also observed larger leaf area in two species, a context-dependent increase in floral display area in two species, and a limited increase in plant seed set in response to both salmon carcass treatments. In sum, our study suggests that marine nutrients can affect terrestrial plant growth and reproduction.

Not all who wander are lost: Trail bias in community science.

The exponential growth and interest in community science programs is producing staggering amounts of biodiversity data across broad temporal and spatial scales. Large community science datasets such as iNaturalist and eBird are allowing ecologists and conservation biologists to answer novel questions that were not possible before. However, the opportunistic nature of many of these enormous datasets leads to biases. Spatial bias is a common problem, where observations are biased towards points of access like roads and trails. iNaturalist-a popular biodiversity community science platform-exhibits strong spatial biases, but it is unclear how these biases affect the quality of biodiversity data collected. Thus, we tested whether fine-scale spatial bias due to sampling from trails affects taxonomic richness estimates. We compared timed transects with experienced iNaturalist observers on and off trails in British Columbia, Canada. Using generalized linear mixed models, we found higher overall taxonomic richness on trails than off trails. In addition, we found more exotic as well as native taxa on trails than off trails. There was no difference between on and off trail observations for species that are rarely observed. Thus, fine-scale spatial bias from trails does not reduce the quality of biodiversity measurements, a promising result for those interested in using iNaturalist data for research and conservation management.

Scale-dependent effects of marine subsidies on the island biogeographic patterns of plants.

Although species richness can be determined by different mechanisms at different spatial scales, the role of scale in the effects of marine inputs on island biogeography has not been studied explicitly. Here, we evaluated the potential influence of island characteristics and marine inputs (seaweed wrack biomass and marine-derived nitrogen in the soil) on plant species richness at both a local (plot) and regional (island) scale on 92 islands in British Columbia, Canada. We found that the effects of subsidies on species richness depend strongly on spatial scale. Despite detecting no effects of marine subsidies at the island scale, we found that as plot level subsidies increased, species richness decreased; plots with more marine-derived nitrogen in the soil hosted fewer plant species. We found no effect of seaweed wrack at either scale. To identify potential mechanisms underlying the decrease in diversity, we fit a spatially explicit joint species distribution model to evaluate species level responses to marine subsidies and effects of biotic interactions among species. We found mixed evidence for competition for both light and nutrients, and cannot rule out an alternative mechanism; the observed decrease in species richness may be due to disturbances associated with animal-mediated nutrient deposits, particularly those from North American river otters (Lontra canadensis). By evaluating the scale-dependent effects of marine subsidies on island biogeographic patterns of plants and revealing likely mechanisms that act on community composition, we provide novel insights on the scale dependence of a fundamental ecological theory, and on the rarely examined links between marine and terrestrial ecosystems often bridged by animal vectors.

Sea to sky: impacts of residual salmon-derived nutrients on estuarine breeding bird communities.

Pacific salmon (Oncorhynchus spp.) returning to streams around the North Pacific Rim provide a nutrient subsidy to these ecosystems. While many species of animals feed directly on salmon carcasses each autumn, salmon-derived nutrients can also be stored in coastal habitats throughout the year. The effects of this storage legacy on vertebrates in other seasons are not well understood, especially in estuaries, which can receive a large portion of post-spawning salmon nutrients. We examine the effects of residual salmon-derived nutrients, forest habitats and landscape features on summer breeding birds in estuary forests. We compared models containing environmental variables and combined chum (Oncorhynchus keta) and pink (Oncorhynchus gorbuscha) salmon biomass to test predictions concerning bird density and diversity. We discovered that total bird, insectivore, golden-crowned kinglet and Pacific wren densities and Shannon's diversity in the summer were strongly predicted by salmon biomass in the autumn. For most metrics, this relationship approaches an asymptote beyond 40 000 kg of salmon biomass. Foliage height diversity, watershed catchment area and estuary area were also important predictors of avian communities. Our study suggests that the legacy of salmon nutrients influences breeding bird density and diversity in estuaries that vary across a wide gradient of spawning salmon biomass.

Salmon subsidies predict territory size and habitat selection of an avian insectivore.

The annual migration and spawning event of Pacific salmon (Oncorhynchus spp.) can lead to cross-boundary delivery of marine-derived nutrients from their carcasses into adjacent terrestrial ecosystems. The densities of some passerine species, including Pacific wrens (Troglodytes pacificus), have been shown to be positively correlated with salmon abundance along streams in Alaska and British Columbia, but mechanisms maintaining these densities remain poorly understood. Riparian areas near salmon streams could provide higher quality habitat for birds through greater food availability and more suitable vegetation structure for foraging and breeding, resulting in wrens maintaining smaller territories. We examined relationships between salmon biomass and Pacific wren territory size, competition, and habitat selection along 11 streams on the coast of British Columbia, Canada. We show that male wren densities increase and territory sizes decrease as salmon-spawning biomass increases. Higher densities result in higher rates of competition as male wrens countersing more frequently to defend their territories along streams with more salmon. Wrens were also more selective of the habitats they defended along streams with higher salmon biomass; they were 68% less likely to select low-quality habitat on streams with salmon compared with 46% less likely at streams without salmon. This suggests a potential trade-off between available high-quality habitat and the cost of competition that structures habitat selection. Thus, the marine-nutrient subsidies provided by salmon carcasses to forests lead to higher densities of wrens while shifting the economics of territorial defence toward smaller territories being defended more vigorously in higher quality habitats.

Effects of spawning Pacific salmon on terrestrial invertebrates: Insects near spawning habitat are isotopically enriched with nitrogen-15 but display no differences in body size.

When Pacific salmon (Oncorhynchus spp.) spawn and die, they deliver marine-derived nutrient subsidies to freshwater and riparian ecosystems. These subsidies can alter the behavior, productivity, and abundance of recipient species and their habitats. Isotopes, such as nitrogen-15 (15N), are often used to trace the destination of marine-derived nutrients in riparian habitats. However, few studies have tested for correlations between stable isotopes and physiological responses of riparian organisms. We examined whether increases in δ 15N in terrestrial insect bodies adjacent to salmon spawning habitat translate to changes in percent nitrogen content and body size. This involved comparisons between distance from a salmon-bearing river, marine-derived nutrients in soils and insects, soil moisture content, and body size and nitrogen content in two common beetle families (Coleoptera: Curculionidae, Carabidae). As predicted, δ15N in riparian soils attenuated with distance from the river but was unaffected by soil moisture. This gradient was mirrored by δ15N in the herbivorous curculionid beetles, whereas carabid beetles, which feed at a higher trophic level and are more mobile, did not show discernable patterns in their δ15N content. Additionally, neither distance from the river nor body δ15N content was related to beetle body size. We also found that nitrogen-15 was not correlated with total percent nitrogen in insect bodies, meaning that the presence of spawning salmon did not increase the percent nitrogen content of these insects. We conclude that while salmon-derived nutrients had entered terrestrial food webs, the presence of δ15N alone did not indicate meaningful physiological changes in these insects in terms of percent nitrogen nor body size. While stable isotopes may be useful tracers of marine-derived nutrients, they cannot necessarily be used as a proxy for physiologically important response variables.

Marine subsidy promotes spatial and dietary niche variation in an omnivore, the Keen's mouse (Peromyscus keeni).

Marine-derived resource subsidies can generate intrapopulation variation in the behaviors and diets of terrestrial consumers. How omnivores respond, given their multiple trophic interactions, is not well understood. We sampled mice (Peromyscus keeni) and their food sources at five sites on three islands of the Central Coast of British Columbia, Canada, to test predictions regarding variation in the spatial behavior and consumption of marine-subsidized foods among individuals. About 50% of detections (n = 27 recaptures) occurred at traps closest to shoreline (25 m), with capture frequencies declining significantly inland (up to 200 m). Stable isotope signatures (δ 13C and δ 15N), particularly δ 15N, in plant foods, forest arthropod prey, and mouse feces were significantly enriched near shorelines compared with inland, while δ 13C patterns were more variable. Bayesian isotope mixing models applied to isotope values in mouse hair indicated that over one-third (35-37%) of diet was comprised of beach-dwelling arthropods, a marine-derived food source. Males were more abundant near the shoreline than females and consumed more marine-derived prey, regardless of reproductive status or availability of other food sources. Our results identify how multiple pathways of marine nutrient transfer can subsidize terrestrial omnivores and how subsets of recipient populations can show variation in spatial and dietary response.

Salmon abundance and patterns of forest greenness as measured by satellite imagery.

Linkages across ecosystems can shape productivity. Salmon carcasses are exemplary of cross-system linkages, because they can fertilize riparian vegetation and shape patterns of terrestrial biodiversity. Detection of salmon fertilization effects has been confined to field-based studies that are limited in scale. Here we use satellite images to quantify the effects of salmon on greenness of riparian vegetation. We measure tree greenness across spatial and temporal gradients of salmon fertilization effects in two regions. In the first case study, we find that deciduous trees are greener in years following large salmon spawning events, and that the magnitude of this effect was related to the specific abundance of spawning salmon. In the second case study we compare greenness of mixed evergreen and deciduous forests across different watersheds that have different salmon spawning densities. We found greenness was related positively to salmon spawning density near streams with high evergreen cover and flat stream banks. These findings suggest that the effect of salmon carcasses on riparian vegetation may be detectable from space. Further work on this approach, especially with high spatial, temporal and spectral data, may allow estimation of the spatial extent of nutrient enrichment from salmon carcasses and aid ecosystem-based management to protect important ecosystem linkages.