Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines

Abstract

Emerging diseases are impacting animals under high-density culture, yet few studies assess their importance to wild populations. Microparasites selected for enhanced virulence in culture settings should be less successful maintaining infectivity in wild populations, as once the host dies, there are limited opportunities to infect new individuals. Instead, moderately virulent microparasites persisting for long periods across multiple environments are of greatest concern. Evolved resistance to endemic microparasites may reduce susceptibilities, but as barriers to microparasite distributions are weakened, and environments become more stressful, unexposed populations may be impacted and pathogenicity enhanced. We provide an overview of the evolutionary and ecological impacts of infectious diseases in wild salmon and suggest ways in which modern technologies can elucidate the microparasites of greatest potential import. We present four case studies that resolve microparasite impacts on adult salmon migration success, impact of river warming on microparasite replication, and infection status on susceptibility to predation. Future health of wild salmon must be considered in a holistic context that includes the cumulative or synergistic impacts of multiple stressors. These approaches will identify populations at greatest risk, critically needed to manage and potentially ameliorate the shifts in current or future trajectories of wild populations.

Keywords: climate; coevolution; cumulative impacts; ecological impacts; infectious disease; microparasite; predation; wild salmon.

Figure 1

Distribution of Flavobacterium psychrophilum, Pacific salmon parvovirus and Nucleospora salmonis among stocks and environments in liver tissues of return-migrating Sockeye Salmon (case study I). Environment explained the highest source of variation, with increasing prevalence at spawning grounds in three (Chilko, Quesnel, Shuswap) of the five stocks. Microbes that were significantly different between environments within each stock are indicated by differing letters (i.e., A and B; P < 0.001, 1-way manova).

Figure 2

Box plots contrasting the distributions of relative loads (50 – CT) of three microparasites (Flavobacterium psychrophilum, Nucleospora salmonis, and Parvovirus) among adult Sockeye Salmon over three environments (ocean, river, and spawning grounds) (case study I). Only samples with detections were used in the calculation of relative loads.

Figure 3

Survivorship analysis for Chilko (top) and Late Shuswap (bottom) stocks based on individual rankings for Principal Component 2 (PC2), and positive (CT<27)/negatives for Piscine Reovirus (PRV) and Loma salmonae (Loma) (case study II). P-values are shown on top right.

Figure 4

Distribution of key microbes among stocks and environments in gill tissue of return-migrating Sockeye Salmon (case study II), including bacteria Flavobacterium psychrophilum, Rickettsia-like organism (RLO), Myxozoa Ceratomyxa shasta, and Parvicapsula minibicornis, ciliate Ichthyophthirius multifiliis, and Tetracapsuloides bryosalmonae.

Figure 5

Percent prevalence of detections (CT <27) of four myxozoan parasites (Ceratomyxa shasta, Parvicapsula minibicornis, Kudoa thyrsites, and Tetracapsuloides bryosalmonae), one ciliate (Ichthyophthirius multifiliis) and one bacteria (Rickettsia-like [RLO]) present at experimental days 14 and 24 in case study III.

Figure 6

Box plots contrasting the distributions of relative loads (50 – CT) of four myxozoan parasites (Ceratomyxa shasta, Parvicapsula minibicornis, Kudoa thyrsites and Tetracapsuloides bryosalmonae), one ciliate (Ichthyophthirius multifiliis) and one bacteria [Rickettsia-like organism (RLO)] of adult Coho Salmon at collection (Day 1; n = 9), after 14 days held at either cool (10°C; n = 17) or warm (15°C; n = 18), and after 24 days (cool: n = 10; warm: n = 7) (case study III).

Figure 7

Percent prevalence of microbes (CT <27) identified in Sockeye Salmon from samples predated upon by Rhinoceros Auklet compared to those from a trawl survey in waters adjacent to sampled colonies (case study IV). A/B indicates a significant difference between groups, tested by microbe.

Figure 8

Box plots revealing differences identified in microbes found in Sockeye Salmon from samples predated upon by Rhinoceros Auklet compared with those from a trawl survey in waters adjacent to sampled colonies (case study IV). (A) Microbe diversity, indicating the number of distinct microbes carried per sample. (B) Highest relative load (50-CT) of any microbe within samples.