CONSERVATION AND SCIENCE REPORT Issue 7, 2016 By Bill Bakke Founder and Science & Conservation Director Native Fish Society

CONSERVATION AND SCIENCE REPORT Issue 7, 2016 By Bill Bakke Founder and Science & Conservation Director Native Fish Society Scientifically Defensible Fish Conservation and Recovery Plans? Maas-Hebner, Kathleen G., Carl Schreck, Robert M. Hughes, J. Alan Yeakley & Nancy Molina (2016) Scientifically Defensible Fish Conservation and Recovery Plans: Addressing Diffuse Threats and Developing Rigorous Adaptive Management Plans, Fisheries, 41:6, 276-285 FRESHWATER ECOSYSTEM INTRASPECIFIC AND INTERSPECIFIC COMPETITION The ODFW and other fisheries managers face a dilemma in trying to rehabilitate wild salmon and steelhead populations, many of them listed under the Endangered Species Act, while trying to provide consistent harvest opportunities by rearing and releasing hatchery fish. This is a difficult balancing act because of the clear contradiction between maintaining or increasing hatchery production to sustain near-term harvest and decreasing that production to reduce genetic, competitive, and other risks to wild populations. For example, improved understanding of the genetic consequences of hatchery fish straying to spawning grounds (e.g., Ford 2002; Araki et al. 2007, 2008) and of the potential for hatchery-origin salmonids to have ecological effects on their wild counterparts (e.g., Kostow and Zhou 2006; Buhle et al. 2009; Naman and Sharpe 2012; Tatara and Berejikian 2012; Carmichael et al. 2015) has clarified the need for substantial changes in hatchery programs to conserve wild fish. Fisheries managers have responded by changing hatchery broodstocks, improving hatchery practices within facilities, shifting some hatchery releases to areas where terminal fisheries encounter few at-risk salmon, and attempting to better control natural spawning by hatchery-origin fish. With the exception of Oregon coast and lower Columbia River Coho Salmon populations, however, the region s fishery managers have generally chosen to avoid the most obvious source of impacts aggregate hatchery output to reduce risks to wild anadromous salmonids (Paquet et al. 2011; NMFS 2014; ODFW 2014). The ODFW (2014) has proposed establishing refuge areas where hatchery programs are excluded as a way to protect selected wild populations from risks posed by continued large releases of hatchery fish, at least within the freshwater environment. There may be difficulties in applying this approach given that (1) hatchery-origin spawners stray into refuges from large programs outside their boundaries, and (2) resistance to refuge designation is strong when in conflict with existing hatchery programs, even in areas previously identified as being of high priority for conserving wild salmon. (Stray hatchery adults are a recognized problem for recovery and protection of wild native salmonids. Recent information has identified stray hatchery smolts as a problem too. This first showed up on the Oregon Coast when private aquaculture coho became known as Wrong-Way Smolts when they went upstream instead of heading for the ocean. Now in SW Washington wrong-way smolts have been found in the E.F. Lewis River, a newly formed wild gene bank river. Hatchery steelhead smolts from downstream tributaries such as Germany Creek and Elochoman River have migrated up the Columbia, entered the N.F. Lewis River and continued upstream to the E.F. Lewis and into tributaries of that river. Hatchery juveniles can compete for food and rearing space with native wild salmonids, eat juvenile salmonids, and decide to stick around and spawn with wild female steelhead. More evaluation is needed, but this discovery suggests that megahatchery programs used to feed the fisheries are double jeopardy for wild steelhead.) BMB 1

Hearing Impairment in Hatchery Salmon Reimer, T., T. Dempster, F. Warren-Myers, A. J. Jensen, and S. E. Swearer. 2016. High prevalence of vaterite in sagittal otoliths causes hearing impairment in farmed fish. Scientific Reports. doi: 10.1038/srep25249 http://www.ncbi.nlm.nih.gov/pmc/articles/pmc4848507/ Abstract The rapid growth of aquaculture raises questions about the welfare status of mass-produced species. Sagittal otoliths are primary hearing structures in the inner ear of all teleost (bony) fishes and are normally composed of aragonite, though abnormal vaterite replacement is sometimes seen in the wild. We provide the first widespread evaluation of the prevalence of vaterite in otoliths, showing that farmed fish have levels of vaterite replacement over 10 times higher than wild fish, regardless of species. We confirm this observation with extensive sampling of wild and farmed Atlantic salmon in Norway, the world s largest producer, and verify that vateritic otoliths are common in farmed salmon worldwide. We demonstrate that average levels of vaterite replacement result in a 28 50% loss of otolith functionality across most of a salmonid s known hearing range and throughout its life cycle. The underlying cause(s) of vaterite formation remain unknown, but the prevalence of hearing impairment in farmed fish has important implications for animal welfare, the survival of escapees and their effects on wild populations, and the efficacy of restocking programs based on captive-bred fish. Quotes from the study: Aquaculture is the world s fastest-growing food production industry, producing over 66 million tonnes of seafood per year. Growth in production has been driven by increased use of intensive farming systems, creating health and welfare challenges, such as increased incidence of deformities, diseases and parasites. Intensive culture systems are also widely used for re-stocking and conservation purposes; if the performance of reared fish is compromised, the efficacy of such programs is likely diminished. One approach for detecting potential welfare effects of animal culture systems is to document differences between wild and farmed populations. Recently, differences have been observed between the otoliths of farmed and wild fish. Otoliths are calcium carbonate structures in the inner ear labyrinths of vertebrates. They are primitive and conserved sensory organs which contribute to hearing, balance, gravity sensation and linear acceleration, and are thus crucial for survival. Otoliths are well studied in many wild fish species, as sagittal otoliths in particular provide an accurate record of age and growth. However, as the age and growth of farmed fishes is usually known, their otoliths are rarely studied. Vaterite otoliths typically occur in fewer than 10% of wild fish, although there are exceptions. Prevalence of vateritic otoliths in farmed fish may differ markedly from wild populations; several studies report vaterite in 50 60% of otoliths from hatchery-reared fish. However, comparisons between the prevalence of vaterite otoliths in farmed and wild populations are few. No large-scale sampling has yet determined if vaterite is consistently more common in farmed populations, nor if the phenomenon is localized or widespread. Here, we synthesise previous knowledge on vaterite otoliths, and provide a detailed and mechanistic understanding of their consequences. We analysed all known published comparisons of vaterite otoliths in wild and farmed populations to test if they are more prevalent in farmed fish. We conducted broad-scale sampling of farmed and wild Atlantic salmon throughout Norway, the world s largest farmed salmon producer and a country with extensive wild populations, to eliminate confounding variables related to species, age and method of vaterite classification. To test if patterns were 2

globally generalizable, we also sampled harvest-size farmed Atlantic salmon from Australia, Scotland, Canada and Chile. Finally, using a mechanistic model and data from Atlantic salmon of three different sizes, we examined how the extent of vaterite replacement affects hearing, including into the infrasound range, at different stages of the life history. Fish raised in hatcheries are up to 10 times more likely to have vateritic sagittal otoliths than their wild counterparts, and may experience hearing loss as a result. Cultured fish worldwide may lose hearing sensitivity due to the farming process. As deformity is a consequence of disease, the formation of vateritic sagittal otoliths infringes on the freedom from pain, injury or disease. Loss of hearing in captive-bred fishes could have negative ecological impacts worldwide. Many wild rivers are deliberately stocked with hatchery-reared salmon: in 2013, 5 10 9 juveniles were released into the Northern Pacific Ocean alone, and in some areas reared juveniles comprise over 70% of returning salmon. However, ocean survival rate of reared salmon is low varying between 1% and 15%. Vaterite replacement may contribute to this low return rate by impairing navigation and habitat selection important for survival. Oregon Should Convert Some Fish Hatcheries to Research By Jim Myron Opinion, Capital Press - May 10, 2002 Gov. John Kitzhaber has taken the bold action of closing three coastal fish hatcheries as part of the additional cuts that were required to bring the state's budget into balance. This move was taken when it became clear that the Oregon Legislature did not have the political will to close any hatcheries, and that the alternative was even further cuts to education and social services. While the Legislature may still find a way to thwart the will of the governor and keep all of Oregon's hatcheries open, the day of reckoning for fish hatcheries and their supporters is clearly at hand. Anyone who has studied the hatchery issue with an open mind would have to conclude that the state hatchery system, as operated, is part of the problem for wild fish, not part of the solution. Reports in recent years from the National Research Council, the Independent Multidisciplinary Science Team, the Independent Scientific Advisory Board and others have concluded that the hatchery system is in need of major reform. This background of studies on the issue provides Oregon with a golden opportunity to begin fixing the hatchery problem, and the governor has taken advantage of this opportunity. Oregon operates 34 fish hatcheries, 15 remote rearing/fish facilities and provides direct financial assistance for 25 salmon trout enhancement program facilities, in addition to supporting the Clatsop Economic Development Commission facilities in Astoria and the Port of Newport's Yaquina Bay acclimation facility. Collectively, these facilities release about 53 million salmon, steelhead and trout into Oregon waters each year. Closing the Salmon River, Trask River and Cedar Creek hatcheries would reduce this production to approximately 50 million fish. The operational costs of the state hatchery program exceed $20 million annually. State and federal taxpayers pay about 85 percent of the costs and angling license fees cover the remainder. This public expenditure for the hatchery program represents a major public subsidy, primarily to benefit recreational and commercial fishing interests. In addition to the annual operating costs, Oregon has historically deferred maintenance at state hatcheries due to lack of available funding. Depending upon the source of the information, the bill for this deferred maintenance ranges from $30 million to $100 million. As a result of direction by the state Legislature, the Oregon Department of Fish and Wildlife must prepare a report on this problem. By later this year, the real scope of this issue should be known. It seems obvious that the state's hatchery program cannot be sustained at current levels without a major infusion of capital in the near term and much larger annual budgets for the foreseeable future. A better solution would be to reduce and restructure the hatchery program to make it sustainable, economically and environmentally, and to encourage the restoration of naturally spawning wild fish to support future fisheries. 3

There is a future for hatcheries in Oregon, but that future looks much different from the present hatchery system. Rather than production hatcheries scattered across the landscape, whose only goal is to provide fish for consumptive use, hatchery/harvest programs should be separated from wild fish populations and limited to areas where harvest can be carefully controlled to eliminate adverse impacts to wild fish. Examples of a program where this may be working are the select area fisheries in Young's Bay near Astoria. Oregon should convert some of its hatcheries to research facilities to help determine what role, if any, hatcheries might be able to play in the restoration of naturally spawning populations of wild fish. These programs must be operated as carefully controlled scientific experiments with sufficient monitoring and evaluation to determine their effectiveness. Gov. Kitzhaber has shown his political courage by providing some much-needed leadership on this issue. closing deteriorated hatcheries that the state doesn't have the money to maintain in the first place makes good fiscal sense, as well as making sense from a biological perspective. Restructuring the remaining hatchery program based upon a new vision for the future of hatcheries in Oregon will take time, but it's an effort that should begin now if Oregon is to have wild salmon and steelhead for future generations to appreciate and enjoy. Jim Myron is conservation director for Oregon Trout in Portland (Mr. Myron s letter serves as a reminder that government is cautious about moving too fast to resolve problems and, of course, if the public is not raising hell, the gap between science, good sense, and management can get enormous.) BMB Do Sneakers Influence Size of Fighter Males? Weir, Laura K., Holly K. Kindsvater, Kyle A. Young, and John D. Reynolds. 2016. Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon.The American Naturalist. University of Chicago Press. http://www.journals.uchicago.edu/doi/abs/10.1086/687253 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. 4

Wild Steelhead Abundance in the Columbia River in the 1890s and 2014 By Bill Bakke July 3, 2016 Comparing wild steelhead harvest in the Columbia River for the years 1890 through 1892 to the steelhead passing Bonneville dam in 2014, illustrates a tremendous decline in wild steelhead. The 1890 through 1892 commercial fishery was confined to a period from April 10 to August 10, while the count of fish passing Bonneville Dam includes the full five months. During those years the harvest during April was just 1.5 to 15% of the total catch, making the months May, June and July a period of highest harvest. Of course the steelhead in the early years are of wild origin while 20% of the steelhead in 2014 are of wild origin based on the assumption that 80% of the Columbia River salmonid run is of hatchery origin. Not all the hatchery steelhead are marked with an adipose fin removed, so the number of true wild fish passing Bonneville Dam is less than the count of so called unclipped steelhead. Harvest, even when it is intense, does not consume all the fish, so kill of wild steelhead is likely a less than the total run for the period of the fishery in the late 1800s. The passage at Bonneville Dam does not include wild steelhead harvested below the dam, even though they cannot be legally harvested, there is some unquantified by-catch mortality, and so the Bonneville Dam count does not include all the wild steelhead that entered the river. In addition, a few wild summer steelhead enter tributaries below the dam. Given those limitations it is still possible to compare wild steelhead abundance in the Columbia in the late 1800s to that of recent times. Also, the months considered are during the time period of the summer steelhead migration. In 2014 the passage of unclipped steelhead at Bonneville Dam from April 1 through August 31 was 42,914 fish. In 1890 the catch of wild steelhead from April 10 through August 10 was 287,375 fish. In 1891 the catch for this same time period was 218,205 wild steelhead and in 1892 it was 464,926 fish. It is worth noting that the average weight of wild steelhead in the catch was 10 pounds with some fish weighing 40 pounds. The passage of wild steelhead at Bonneville dam in 2014 for the full five months was 15% of the 1890 catch, 19% of the 1891 catch and 9.2% of the 1892 catch. It should also be noted that in the late 1800s the Columbia River catch was declining and it was a concern of the managers as well as the fishermen and canners. Their concern led to the first fish hatchery in the Columbia basin in 1877 for the purpose of increasing the supply of salmon for the commercial fishery. The commercial fishery was started in 1866 and the commercial pack peaked in 1883 and 1884 then continued to decline. McDonald, U.S. Fish Commissioner said In 1889 the packers began canning bluebacks (sockeye) and steelheads to make up the deficiency of the supply (of chinook) and extended their fishery into September. This comparison, to the extent that it can be made with the stated variables, indicates that there has been a rather large decline in wild steelhead in the Columbia River. Setting measurable recovery criteria for wild steelhead may require some major shifts in management, mitigation, and harvest if it is to be biologically meaningful, including expected ecological services. References: Marshall McDonald. 1895. Bulletin of the United States Fish Commission, Washington, D.C. U.S. Army Corps of Engineers.2014.Annual Fish Passage Report. 5

The History of Salmonid Management on the Columbia River Affects the Whole Northwest By Bill Bakke A timeline for following the management of salmon and steelhead would tell us that since 1850 that salmon management has been privatizing the public commons (ISAB 2013). The history of Columbia River salmonid management has set the stage for the entire West Coast. That is why what happens on the Columbia and efforts to recover populations that are threatened with extinction should be informative about what is going on in the whole region. Knowing something about the historical context of salmon management will probably help one to better understand the present day problems. If one draws a line from 1850 to 2016 there are events, insights and discoveries that are worth knowing about. As you follow down that line to the present there is a branch that describes a divergent perspective about salmon and management. So let s start walking down that line. First, though, there are a few things worth noting. There are beliefs, facts and money which all play a decisive role in the outcome. Initially, the salmon were excessively exploited by the commercial fishery. At that time the focus of management was to support the commercial fishery and that perspective has persisted. For example: It has been shown that the present intensity of fishing is such that, in 1938, over 80 percent of the spring run and between 60 and 70 percent of the main fall run of chinook salmon were taken in the commercial fishery. It seems reasonably certain that, at least for the spring run of chinooks on the Columbia, the escapement is well below the level that would provide the maximum sustained yield. For the May run of chinooks it is shown that only about 1 fish out of 7 escapes the commercial fishery and available for the future maintenance of the run. (Rich 1942) 1875: Spencer Baird, U.S. Fish Commissioner, told The Oregonian that by investing in hatcheries it would no longer be necessary to regulate harvest and protect of habitat. He did not have any proof to support that conclusion but he did believe the states would not effectively manage wild salmon based on his experience on the East Coast with Atlantic salmon. Baird set the stage for the future because it let the government and the politicians off the hook. All he needed was money to fund the hatcheries. The public now would fund programs to mitigate fishery impacts and watershed development. 1878: Livingston Stone at Baird s request came to the Clackamas River and developed the first salmon hatchery on the Columbia because the runs had declined. Stone was an advocate that salmon were not locally adapted, but returned to rivers randomly, primarily to those rivers with a vigorous, rapid flow. 1894: Barton W. Evermann, Ph.D. (Ichthyologist of the United States Fish Commission) The alarming decrease in the salmon catch of the Columbia River within recent years, the importance of preventing the continuance of this decrease, and the desire and hope that the salmon industry may be rebuilt to its former importance, render imperative a most careful study of the natural history of the salmon and more accurate knowledge of the location of their spawning beds, their time of spawning, and the temperature and other physical conditions under which their spawning takes place. 1894: Marshall McDonald (U.S. Commissioner of Fish and Fisheries)...fisheries in a large measure prevent the run of salmon into and up the rivers, then a serious decline in the fisheries is inevitable. The regulation of the fisheries should assure the largest opportunity practicable for reproduction under natural conditions. Artificial propagation should 6

be invoked as an aid and not as a substitute for reproduction under natural conditions. It is evident, therefore, that fishcultural operations cannot be relied upon exclusively or chiefly to maintain the salmon supply of the Columbia. 1902: David Starr Jordan (Stanford University) was an influential thinker and expert on salmon. He said, We fail to find any evidence that salmon return to spawn on the same spawning grounds So now we know that salmon are do not return to the river of their birth and that hatcheries can replace the salmon and their habitats. These beliefs had a profound effect on development of salmon management that is still operating today. 1917: John Cobb, soon to become the head of fisheries at the University of Washington wrote: In some sections an almost idolatrous faith in the efficacy of artificial culture of fish for replenishing the ravages of man and nothing has done more harm than the prevalence of such an idea. 1927: Willis Rich, concluded, based on his salmon tagging work, Since each race is self-propagating, it becomes perfectly apparent that all parts of the salmon run must be given protection if the run as a whole is to be maintained. 1948: Willis Rich recommended: The importance of the fact that the salmon and steelhead return as adults to their home streams and tributaries is obvious; it is essential that each independent, self-perpetuating population of fish be preserved if depletion is to be avoided. The beliefs of Baird, Stone and Jordan were challenged by scientific investigation. Willis Rich established the concept of the Home Stream Theory as the only management approach to conserve the salmon and maintain the fisheries. The concept of salmon management in place for 73 years diverged based on fact rather than belief. There are now two perspectives on salmon management: 1) Conservation and 2) privatizing the public commons to produce a product for the market economy. Which perspective will win? The divergent perspective of Rich led to Oregon s Wild Fish Management Policy in 1978, the ESA in 1991, and the 1996 review of Northwest salmon management by the National Research Council in the book Upstream. In discussing hatcheries the NRC said: Hatcheries have resulted in reduced genetic diversity within and between salmon populations, increased the effect of mixed-population fisheries on depleted natural populations, altered behavior of fish, caused ecological problems by eliminating the nutritive contributions of carcasses of spawning salmon from streams, and probably displaced the remnants of wild runs. 1947: The U.S. Department of Interior said, The Northwest and the Department Committees have each assumed that the Columbia River fisheries cannot be allowed indefinitely to block the full development of the other resources of the river. It is, therefore, the conclusion of all concerned that the overall benefits to the Pacific Northwest from a thorough going development of the Snake and Columbia are such that the present salmon run must be sacrificed. This means that the Department s efforts should be directed toward ameliorating the impact of this development upon injured interests and not toward a vain attempt to hold still the hands of the clock. Hatchery mitigation eclipsed the Home Stream conservation recommendations of Willis Rich. Rocky Reach Dam (1933) was already in operation on the upper Columbia soon to be followed by Bonneville Dam (1938) and Grand Coulee Dam (1941). Spencer Baird was correct the government was unwilling to protect the salmon therefore his promise that hatcheries would maintain the fishery would dominate social and professional perspectives. 1938: The Mitchell Act was passed and became the primary source of federal funding for hatchery development in the Columbia basin. 1960: Milo Moore, Director of the Washington Department of Fisheries, said: artificial taking of spawn may provide the reality salmon without rivers. 7

1980: The Power Planning Council was established by Congress and through its fish and wildlife program with Bonneville Power Administration funding over $15 billion on salmon passage, habitat and hatcheries, but that has failed to achieve the goal of generating a run of 5 million hatchery, natural (naturally spawning hatchery fish) and wild fish in the Columbia River. 1991: The first wild salmon populations were given protection as a threatened species through the Endangered Species Act. The hatchery promise to provide harvest mitigation for the fisheries has not yet materialized and recovery of wild salmon through the authority of the ESA has not yet been effectively applied, and the conservation recommendations of Willis Rich have been set aside; a footnote in history. The following table contains information that is difficult to find, but in 2015 the Power Planning and Conservation Council provided an update. It is still not easy to find and that is probably why most people do not realize that 190 populations of salmon and steelhead are threatened with extinction in the Columbia River. The intense commercial fishery and declining harvest caused the cannery owners, fishermen and fish managers to be build the first hatchery on the river in 1878. The public took action to eliminate some forms of commercial gear (1927) in order to increase spawning escapement, but it did not work. The public got the Snake River chinook protected through the Endangered Species Act in 1992. More hatcheries were built but an effective program for wild salmonid recovery has not yet been applied. BMB ESA Protected Species and Populations - Columbia River Basin Domain Species Populations ESA Listing Willamette/ Lower Columbia Chum Salmon 16 Threatened (1999) Chinook Salmon Spring/Fall Chinook 32 Threatened (1999) Chinook Salmon Upper Willamette Chinook 7 Threatened (1999) Steelhead Lower Columbia River Steelhead 23 Threatened (1999) Coho Salmon Lower Columbia River Coho 24 Threatened (2005) Steelhead Upper Willamette River Steelhead 5 Threatened (1999) Interior Columbia Chinook Salmon Snake River Fall Chinook 1 Threatened (1992) Chinook Salmon Snake River Spring/Summer Chinook 31 Threatened (1992)* Chinook Salmon Upper Columbia River Spring Chinook 3 Endangered (1999) Steelhead Snake River Basin Steelhead 24 Threatened (1997) Steelhead Middle Columbia River Steelhead 18 Threatened (1999) Steelhead Upper Columbia River Steelhead 5 Threatened (1997) 8

Sockeye Salmon Snake River Sockeye 1 Endangered (1992) Total by species: Chum 16 Chinook 74 Steelhead 75 Coho 24 Sockeye 1 Total Populations Protected by the ESA: 190 Source: N.W. Power Planning and Conservation Council (Updated 11-3-2015) http://rs.nwcouncil.org/hli_summary.cfm?mnu=hli#1a1 Fine Scale Adaptation to Water Temperature and Pathogens LARSON, W. A., P. J. LISI, J. E. SEEB, L. W. SEEB & D. E. SCHINDLER. 2016. Major histocompatibility complex diversity is positively associated with stream water temperatures in proximate populations of sockeye salmon. Journal for Evolutionary Biology. Abstract Local adaptation to heterogeneous environments generates population diversity within species, significantly increasing ecosystem stability and flows of ecosystem services. However, few studies have isolated the specific mechanisms that create and maintain this diversity. Here, we examined the relationship between water temperature in streams used for spawning and genetic diversity at a gene involved in immune function [the major histocompatibility complex (MHC)] in 14 populations of sockeye salmon (Oncorhynchus nerka) sampled across the Wood River basin in south-western Alaska. The largest influence on MHC diversity was lake basin, but we also found a significant positive correlation between average water temperature and MHC diversity. This positive relationship between temperature and MHC diversity appears to have been produced by natural selection at very local scales rather than neutral processes, as no correlation was observed between temperature and genetic diversity at 90 neutral markers. Additionally, no significant relationship was observed between temperature variability and MHC diversity. Although lake basin was the largest driver of differences in MHC diversity, our results also demonstrate that fine-scale differences in water temperature may generate variable selection regimes in populations that spawn in habitats separated by as little as 1 km. Additionally, our results indicated that some populations may be reaching a maximum level of MHC diversity. We postulate that salmon from populations in warm streams may delay spawning until late summer to avoid thermal stress as well as the elevated levels of pathogen prevalence and virulence associated with warm temperatures earlier in the summer. Quotes and Comments: 9

Genotypic and phenotypic diversity within species can generate portfolio effects that maintain ecosystem functions and flows of ecosystem services, even in the presence of significant environmental fluctuation. Temperature and temperature variation can significantly influence pathogen communities and the ability of pathogens to infect their hosts. For example, higher temperatures can increase the virulence, diversity and prevalence of pathogens. Additionally, high temperature variation can facilitate pathogen transmission at lower mean temperatures and influence the developmental rate of pathogens. Further, with anticipated climate change, there is a need to understand how populations may respond to new environmental conditions generated by changing thermal and precipitation regimes. Here, we combine genetic and environmental data to investigate the influence of water temperature on adaptive genetic diversity at an immune response gene, the major histocompatibility complex (MHC), in sockeye salmon (Oncorhynchus nerka) sampled across a single river basin in south-western Alaska (USA). The relationship between temperature and the effects of pathogens is especially evident in salmon, which often complete an arduous migration from the marine environment to their natal freshwater habitats to spawn. Elevated temperatures during this migration and on the spawning grounds can increase pathogen prevalence and virulence and eventually lead to prespawn mortality. Salmon from warmer streams may delay spawning to avoid thermal stress and the increased levels of pathogen prevalence and virulence associated with warmer temperatures that occur during summer. Indeed, for sockeye salmon populations spawning in south-west Alaska, there is a positive correlation between summer stream water temperatures and the seasonal timing of spawning. Different patterns of MHC diversity may have also evolved in salmon populations that experience thermal stress compared to those that are not subjected to elevated temperatures and, therefore, likely reflect evolutionary responses to thermal stress in a population s evolutionary history. It is unclear whether variation in MHC diversity is associated with fine-scale differences in temperature commonly found among tributaries within river basins. Here, we investigated the influence of temperature and temperature variation on MHC diversity in sockeye salmon (Oncorhynchus nerka) from 14 streams in the Wood River basin in south-western Alaska. Previous studies have demonstrated that differences in MHC diversity are associated with life history type (beach, river, stream) in populations of sockeye salmon from the Wood River basin. Our results extend these findings and suggest that, although lake basin has a large effect of MHC diversity, fine-scale differences in thermal regimes can result in differences in MHC diversity among stream populations that are separated by as little as 1 km. We also investigated the relationship between temperature patterns throughout the summer and spawn timing and found that changes in spawn timing may represent an additional mechanism to cope with the increased levels of pathogen prevalence and virulence associated with high water temperatures. We speculate that the significant relationship we observed between temperature and MHC HO was driven by increased pathogen-mediated selection due to increases in pathogen virulence, prevalence, and diversity in warm environments. We did not observe a significant relationship between within-stream variability in temperature and MHC diversity. These results suggest that the strength of pathogen-mediated selection is more influenced by average thermal conditions rather than temperature variability in our study system. The few studies investigating the relative influence of temperature and temperature variation on pathogen prevalence and virulence demonstrate a complex interplay between these two variables. (This suggests that the major kill of Columbia River sockeye in 2015 due to an unusual interplay of drought and excessive temperatures created an environment that was not an average thermal condition to which sockeye are adapted. However, 10

these conditions are expected to become common as global warming affects the Columbia River. The sockeye may adjust their run timing to avoid a hot water environment and pathogen infection. But that assumes the river temperature is predictable rather than one of random occurrence. Thermal refuges provided by Columbia River tributaries can offer some relief, but pathogen infected fish were found dying and dead in thermal refuges.) BMB Temperature variation likely influences pathogen communities in our study system, but the complexities of these interactions may have prevented us from demonstrating a clear relationship between temperature variation and MHC diversity. Sockeye salmon in the Wood River basin spend a large portion of their life cycle (up to 3 years) rearing in nursery lakes and likely spend the majority of this time in lakes that are proximate to their streams of origin (Quinn, 2005). These juvenile salmon are exposed to different environments depending on the lake that they inhabit, possibly resulting in the differences in MHC diversity that we observed due to differences in pathogen exposure. For example, it is possible that pathogen communities in Lakes Nerka and Beverley are more diverse than those in Lake Aleknagik, resulting in higher levels of MHC diversity in sockeye salmon that spawn in tributaries connected to these lakes. It is also possible that differences in pathogen virulence among these lakes may be responsible for the MHC diversity that we observed. The large differences in patterns of MHC diversity between sockeye and Atlantic salmon parallel the thermal tolerance characteristics of these species. Sockeye salmon show large differences in thermal tolerance over extremely small spatial scales, whereas Atlantic salmon show little variation in temperature tolerance over large latitudinal gradients. This similarity between surveys of MHC variation and thermal tolerance suggests that Atlantic salmon may have adopted a more generalist approach to cope with high temperatures and the associated high levels of pathogens, whereas sockeye salmon appear to be locally adapted to the thermal regimes and pathogen communities present in the environments that they experience. In conclusion, we found that MHC diversity was highly influenced by lake basin but also discovered a significant positive relationship between water temperature and MHC diversity that was not likely produced through neutral processes. This result suggests that differences in temperature among proximate streams may influence pathogen-mediated selection and promote population diversity on the scale of only a few kilometres. Additionally, we postulated that variation in spawn timing among populations may represent an adaptive behavioural mechanism for avoiding summer thermal stress and the increased pathogen prevalence and virulence associated with high temperatures. Our findings are especially relevant given the anticipated impacts of climate change. Many studies have attempted to address whether organisms will be able to adapt to a changing climate. Although these studies often assume that responses to climate change will be similar across relatively large spatial scales (1000s of km), our findings suggest that adaptation to climate change may also occur on much smaller scales. This fine-scale diversity can help to maintain ecosystem stability and ecological processes (Schindler et al., 2015), even in the face of environmental fluctuation. (Fine scale adaptation of salmonids to variable ecological conditions of natal streams is real and scientific studies are confirming such adaptation, as this one does, at the watershed level. Management, on the other hand, is primarily gross scale, ignoring the local adaptation of salmonids within watersheds, estuaries, and ocean environments, thus limiting the ability of management to recognize this diversity and provide effective management of habitats, harvests, and production. In large rivers like the Columbia, Willamette, and Snake rivers the migrational habitat may become lethal to salmonids as the climate changes, even though they may be able to cope with changes in their spawning streams. This may mean that salmonids are unable to reach their natal tributaries of large developed rivers.)bmb 11