Salmon-derived nitrogen in terrestrial invertebrates from coniferous forests of the Pacific Northwest

BACKGROUND: Bi-directional flow of nutrients between marine and terrestrial ecosystems can provide essential resources that structure communities in transitional habitats. On the Pacific coast of North America, anadromous salmon (Oncorhynchus spp.) constitute a dominant nutrient subsidy to aquatic habitats and riparian vegetation, although the contribution to terrestrial habitats is not well established. We use a dual isotope approach of δ(15)N and δ(13)C to test for the contribution of salmon nutrients to multiple trophic levels of litter-based terrestrial invertebrates below and above waterfalls that act as a barrier to salmon migration on two watersheds in coastal British Columbia. RESULTS: Invertebrates varied predictably in δ(15)N with enrichment of 3–8‰ below the falls compared with above the falls in all trophic groups on both watersheds. We observed increasing δ(15)N levels in our invertebrate groups with increasing consumption of dietary protein. Invertebrates varied in δ(13)C but did not always vary predictably with trophic level or habitat. From 19.4 to 71.5% of invertebrate total nitrogen was originally derived from salmon depending on taxa, watershed, and degree of fractionation from the source. CONCLUSIONS: Enrichment of δ(15)N in the invertebrate community below the falls in conjunction with the absence of δ(13)C enrichment suggests that enrichment in δ(15)N occurs primarily through salmon-derived nitrogen subsidies to litter, soil and vegetation N pools rather than from direct consumption of salmon tissue or salmon tissue consumers. Salmon nutrient subsidies to terrestrial habitats may result in shifts in invertebrate community structure, with subsequent implications for higher vertebrate consumers, particularly the passerines

Endemism and Conservation of Sticklebacks in the Queen Charlotte Islands

"Dr. Peden's contribution was financed by the British Columbia Provincial Museum. Our work was supported by grants from the National Research Council of Canada to J. R. Nursall and G. E. E. Moodie.

Diverse Ecological Pathways of Salmon Nutrients Through an Intact Marine-terrestrial Interface

Based on five years of field studies (1992, 1993, 1994, 1998, 2000), I quantified bi-directional movement of salmon nutrients through an estuary, stream, and old growth forest in a large protected reserve on Haida Gwaii, British Columbia. In 1993, when most data were collected, about 6000 Chum Salmon (Oncorhynchus keta) entered the river of which 22% of the total biomass of senescent carcasses were swept downstream into the estuary and were scavenged by gulls (n = 350) and subtidal invertebrates. Of the 3700 salmon (10 000 kg) transferred by American Black Bear (Ursus americanus) to the riparian zone and partially consumed along the 800 m of stream channel, 5070 kg of salmon tissues abandoned by the bears were scavenged by Northwestern Crows (Corvus caurinus; n = 200) but mostly (4100 kg) by calliphorid blowfly larvae resulting in larval densities averaging 240/m2 throughout the riparian zone. Total nitrogen input to the soils from the combined effects of bear and scavenger activity as well as carcass input was 18 g/m2 within 10 m of the stream channel. δ15N of foliar tissues of Lanky Moss (Rhytidiadelphus loreus), Red Huckleberry (Vaccinium parvifolium), Salal (Gaultheria shallon), and Western Hemlock (Tsuga heterophylla) ranged about 15‰ to 20‰ among adjacent microsites in each species, with higher values occurring in salmon carcass zones. Total nitrogen in foliar tissues ranged from 1% to 2.4% among microsites and was best predicted by positive correlations with foliar 15N values and secondarily by presence/absence of salmon carcasses. This is the first study to integrate estuarine to riparian ecological processes in the cycling of salmonid nutrients and identifies a range of ecological baselines that can inform the multiple restoration programs underway in degraded watersheds in the North Pacific

Early Ontogenetic Diet in Gray Wolves, Canis lupus, of Coastal British Columbia

Within populations, different age classes often consume dissimilar resources, and provisioning of juveniles by adults is one mechanism by which this can occur. Although the diet of Gray Wolves (Canis lupus) has been studied extensively, the diet of pups is largely unknown. We examined faeces deposited by altricial pups and adult providers during the first two months following birth at two den sites over two years on the central coast of British Columbia, Canada. Pups and adult wolves consumed similar species, and Black-tailed Deer (Odocoileus hemionus) constituted most of the diet for both age groups. Pup and adult diet, however, diverged. Specifically, adult deer occurred significantly less frequently in the diet of pups than in the diet of adult wolves, which suggests that adults selectively provisioned pups. We speculate that this may relate to adaptive strategies of adult wolves to provide their offspring with food of optimal nutritional value or reduced parasitic burden, and/or logistic factors associated with provisioning such as prey transportability and availability

Early Ontogenetic Diet in Gray Wolves, Canis lupus, of Coastal British Columbia

Within populations, different age classes often consume dissimilar resources, and provisioning of juveniles by adults is one mechanism by which this can occur. Although the diet of Gray Wolves (Canis lupus) has been studied extensively, the diet of pups is largely unknown. We examined faeces deposited by altricial pups and adult providers during the first two months following birth at two den sites over two years on the central coast of British Columbia, Canada. Pups and adult wolves consumed similar species, and Black-tailed Deer (Odocoileus hemionus) constituted most of the diet for both age groups. Pup and adult diet, however, diverged. Specifically, adult deer occurred significantly less frequently in the diet of pups than in the diet of adult wolves, which suggests that adults selectively provisioned pups. We speculate that this may relate to adaptive strategies of adult wolves to provide their offspring with food of optimal nutritional value or reduced parasitic burden, and/or logistic factors associated with provisioning such as prey transportability and availability

Isotopic Niche Differentiation Among Mammals from a Rainforest in Peninsular Malaysia

We performed stable isotope analysis on eight mammalian species: pig-tailed macaque (Macaca nemestrina), long-tailed macaque (M. fascicularis), dusky leaf monkey (Trachypithecus obscurus), brush-tailed porcupine (Atherurus macrourus), wild boar (Sus scrofa), lesser mouse-deer (Tragulus javanicus), greater mouse-deer (T. napu), and barking deer (Muntiacus muntjac), to test the hypothesis that the differences in diet and habitat types among species, guilds and foraging strategies are reflected in the δ15N and δ13C signatures of their tissues. Whereas the isotopic ratios differed among taxa, the four major isotopic groups observed were: mouse-deer species, primate species, brush-tailed porcupine, and wild boar. The brush-tailed porcupine showed the most divergent isotopic signatures, depleted in both δ15N and δ13C, and the wild boar had isotopic signatures enriched in both δ15N and δ13C. Although results are only indicative, the three habitat types occupied by the species were reflected by differences in isotopic signatures, with the ground-dwelling species having the most divergent isotopic values from arboreal and semi-arboreal species. Likewise, among the four different types of dietary lifestyle groups tested, each group showed either significantly different δ15N or δ13C from other groups. Omnivores had the highest isotopic values, and bark-eater/frugivores had the lowest. By increasing the sample sizes both within the species and the number of species in future analyses, this isotopic technique provides opportunity to elucidate the diets of their putative predators in the rainforests of Peninsular Malaysia

Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments

Repeated adaptation to a new environment often leads to convergent phenotypic changes whose underlying genetic mechanisms are rarely known. Here, we study adaptation of color vision in threespine stickleback during the repeated postglacial colonization of clearwater and blackwater lakes in the Haida Gwaii archipelago. We use whole genomes from 16 clearwater and 12 blackwater populations, and a selection experiment, in which stickleback were transplanted from a blackwater lake into an uninhabited clearwater pond and resampled after 19 y to test for selection on cone opsin genes. Patterns of haplotype homozygosity, genetic diversity, site frequency spectra, and allele-frequency change support a selective sweep centered on the adjacent blue- and red-light sensitive opsins SWS2 and LWS. The haplotype under selection carries seven amino acid changes in SWS2, including two changes known to cause a red-shift in light absorption, and is favored in blackwater lakes but disfavored in the clearwater habitat of the transplant population. Remarkably, the same red-shifting amino acid changes occurred after the duplication of SWS2 198 million years ago, in the ancestor of most spiny-rayed fish. Two distantly related fish species, bluefin killifish and black bream, express these old paralogs divergently in black- and clearwater habitats, while sticklebacks lost one paralog. Our study thus shows that convergent adaptation to the same environment can involve the same genetic changes on very different evolutionary time scales by reevolving lost mutations and reusing them repeatedly from standing genetic variation

Genomic changes underlying repeated niche shifts in an adaptive radiation

In adaptive radiations, single lineages rapidly diversify by adapting to many new niches. Little is known yet about the genomic mechanisms involved, that is, the source of genetic variation or genomic architecture facilitating or constraining adaptive radiation. Here, we investigate genomic changes associated with repeated invasion of many different freshwater niches by threespine stickleback in the Haida Gwaii archipelago, Canada, by resequencing single genomes from one marine and 28 freshwater populations. We find 89 likely targets of parallel selection in the genome that are enriched for old standing genetic variation. In contrast to theoretical expectations, their genomic architecture is highly dispersed with little clustering. Candidate genes and genotype-environment correlations match the three major environmental axes predation regime, light environment, and ecosystem size. In a niche space with these three dimensions, we find that the more divergent a new niche from the ancestral marine habitat, the more loci show signatures of parallel selection. Our findings suggest that the genomic architecture of parallel adaptation in adaptive radiation depends on the steepness of ecological gradients and the dimensionality of the niche space

DNA fragility in the parallel evolution of pelvic reduction in stickleback fish

Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by mechanisms that are still poorly understood. A classic example of repeated evolution is the loss of pelvic hindfins in stickleback fish (Gasterosteus aculeatus). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the Pitx1 gene. Here, we identify molecular features contributing to these recurrent deletions. Pitx1 enhancer sequences form alternative DNA structures in vitro and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by TG-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution

Salmon for Terrestrial Protected areas

Although managers safeguard protected areas for migratory species, little consideration has been given to how migratory species might benefit parks. Additionally, whereas land‐sea connections are considered in management of protected areas, most effort has focused on reducing negative “downstream” processes. Here, we offer a proposal to promote positive “upstream” processes by safeguarding the seasonal pulse of marine nutrients imported into freshwater and riparian ecosystems by spawning migrations of Pacific salmon. Currently, high rates of fishing limit this important contribution to species and processes that terrestrial parks were designed to protect. Accordingly, we propose limiting exploitation in areas and periods through which salmon runs bound for terrestrial protected areas can migrate. Best suited for less commercially valuable but relatively abundant and widespread pink and chum salmon (O. gorbuscha and keta), our proposal thus considers ecosystem and societal needs for salmon. We conclude by outlining strategies to overcome socio‐economic barriers to implementation