The status of summer steelhead in the Upper Columbia River Distinct Population Segment (DPS) was upgraded from endangered to threatened on June 18, 2009.  That decision was based on new data that suggested an increase in abundance and spawning distribution, but also considered supplementation programs that are intended to increase local adaptation and diversity (74 FR 42605; August 24, 2009).  The National Marine Fisheries Service (NMFS) also approved a new policy on the consideration of hatchery origin fish in making ESA determinations (70 FR 37204; June 28, 2005), which was also considered in the status upgrade.  In summary, while the status of steelhead populations in the Upper Columbia River DPS was upgraded, that decision was primarily the result of a change in policy and management regarding hatchery programs, not on realized change in productivity in the natural environment. 

 Hatcheries are one of the main tools that have been used to mitigate for salmon losses caused by the construction and operation of the Columbia River hydropower system.  Historically, the goal of most hatcheries was simply to provide fish for harvest and mitigate for hydro related impacts as well as habitat loss.  As concern for the conservation of wild salmon grew in the late 20^th Century, the intent of many hatchery programs changed from providing fish for harvest and mitigation to conserving and rebuilding natural populations.  As a result, hatcheries now are a large component in most conservation or recovery programs, particularly for populations in the Interior Columbia River Basin.  The use of hatcheries to conserve wild salmon is controversial, however, due in part to concerns about the genetic impacts of even well intentioned hatchery supplementation on wild populations (Waples and Drake 2004). 

 Genetic risks associated with hatchery supplementation include the potential for increased inbreeding (Ryman and  Laikre 1991; Ryman et al. 1995; Wang and Ryman 2001), outbreeding depression (e.g., Gharrett and Smoker 1991) and domestication selection (Ford 2002).  The potential seriousness of these phenomena is reinforced by a long history of studies showing that hatchery fish often reproduce poorly in the wild when compared to natural origin fish (reviewed by Berejikian and Ford 2004; Araki et al. 2008).  Hatchery steelhead, in particular, have been found to have very low relative reproductive success in several studies (Chilcote et al. 1986; Leider et al. 1990; Chilcote 2003; Kostow et al. 2003; McLean et al. 2003; Araki et al. 2007a; Araki et al. 2007b).     

 Evaluating the relative reproductive success of Methow River steelhead is particularly important for several reasons because supplementation is being used as a significant component of the recovery strategy for this population.  In addition, Upper Columbia steelhead have a very large ‘gap’ between current productivity and productivity needed to meet viability goals (ICTRT 2007).  This large gap may be due, at least in part, to the large proportion of hatchery fish in this population.  Understanding the relative reproductive success of hatchery steelhead in this population is therefore particularly important for evaluating the recovery potential for this population.  Here, we develop a study plan for a project that will (1) directly measure the relative reproductive success of hatchery and natural-origin steelhead in the natural environment using a DNA pedigree approach, (2) determine the degree to which any differences in reproductive success between hatchery and natural steelhead can be explained by measurable biological characteristics such as run timing, morphology, spawn timing, or spawning location, and (3) estimate the relative fitness of hatchery-lineage steelhead after they have experienced an entire generation in the natural environment. 

 Life History of Methow Steelhead

 Upstream Migration

 Summer steelhead in the Upper Columbia River DPS destined for the Methow Basin exhibit a protracted upstream migration through the Columbia River.  Summer steelhead may spend between five to ten months in freshwater before making a final migration to the spawning grounds.  We are proposing using a DNA based pedigree approach to assign naturally produced progeny to a parent, either hatchery or naturally produced.  Because of the prolonged migration pattern and uncertainty in survival to spawning, we are proposing to collect and sample potential parents during their spawning migration to a major spawning area in the Twisp River.  A newly modified weir in the Twisp River, built and owned by Douglas County PUD, provides an excellent location to trap and sample nearly 100% of the adult steelhead destined to spawn upstream of the weir (Figure 1).  Because adult steelhead are trapped during their spawning migration, trapping is limited to only a few months in the spring when probability of survival to spawning is both greater and similar (i.e., no sport harvest) for both hatchery and naturally produced components (Figure 2).  More simply stated, because recreational harvest does not occur in the Twisp River and the spawning migration overlaps with the spawning period, we would assume that any steelhead passed upstream of the weir would survive to spawn.  

Figure 1.  Vicinity map of the Methow Basin and Twisp weir.

 Run Escapement

 Estimates of adult steelhead to the mouth of the Methow River are calculated based on in-river sampling conducted at Wells Dam conducted throughout most of the migration period.  The estimated number of hatchery and natural steelhead that migrate upstream of Wells Dam are apportioned to the Methow River based on radio telemetry studies conducted in 1999 and 2001 (English et al. 2001, 2003).   Since 1997, escapement to the Methow River has been predominately hatchery fish, but natural origin steelhead abundance has increased slightly in the last few years (Table 1).  It should be noted that uncertainty exists in how well the sampling at Wells Dam represents the run at large.  Sample rates at Wells Dam typically do not exceed 10% and are weighted towards only one fish ladder trap.  Furthermore, the proportion of hatchery and natural steelhead that migrate to the Methow River is based on two years of data with very low sample sizes.

Figure 2.  Passage of hatchery and wild steelhead at the Twisp Weir, 2009.

Table 1.  Estimated Methow steelhead run escapement and composition monitored at Wells Dam, 1997 - 2009.

Spawning Escapement

 Redd surveys have been used to provide an index of spawning escapement in the Methow Basin since 2004 (Snow et al. 2009).  The Methow River basin was divided into four geographic subbasins; the upper Methow, lower Methow, Chewuch, and Twisp.  Index areas of annual spawning activity were established within each subbasin based on information from historic surveys.  Index areas were surveyed weekly on foot or by raft throughout the spawning season.  Steelhead redds were individually flagged with date, redd number, and location recorded on each flag.  Each redd was also recorded with hand-held global positioning system (GPS) devices for subsequent mapping.  When spawning was perceived to be near peak, non-index areas were surveyed for a total redd count, and index areas were surveyed by a naïve surveyor to determine the proportion of total redds still visible.  Redds observed outside of index areas were expanded by the visible proportion of redds from index area counts.  Index area surveys continued after peak spawning, and additional expansions were made in non-index areas based on the proportion of additional redds found within index areas after peak spawning.  Expanded redd counts from outside the index areas were combined with total redd counts within the index areas to estimate the total number of redds for each stream.  Annual redd surveys in the Methow Basin have met with varying degrees of success.  While estimates of precision are currently not available, the mean annual number redds in the Methow Basin since 2004 was 1,040 (range 740 – 1,784).  The Twisp River accounted for an average of 279 redds annually.  Of those redds, 86% were found upstream of the Twisp weir.   

 Of those fish that spawn in the Twisp River, the proportion of natural origin fish in unknown.  However, in 2009, WDFW operated the modified Twisp weir throughout the spawning migration period (March through May) and trapped, tagged, and released a total of 378 adult steelhead.  Based on scale pattern analysis, 91 (24%) were determined to be of natural origin.  Tagging and subsequent observations on the spawning grounds suggest that the weir efficiency was near 100% (i.e., 3% of the steelhead observed on the spawning grounds were untagged). 

 Smolt Production

 WDFW has operated a smolt trap on the lower Twisp River since 2005, funded by Douglas County PUD.  While a small proportion of naturally produced steelhead emigrate as subyearling parr, smolts emigrate from the Twisp River between age-1 and age-4 (Table 2).  Because steelhead have a complex life history and smolt trapping has only been conducted for a short time period, it is unclear if the low survival of juvenile steelhead is a function of density or poor reproductive success.  We expect that estimating the relative reproductive success at an early life stage (i.e., age-1 parr) will greatly increase our ability in answering that question.

 Table 2.  Estimated emigrant-per-redd and egg-to-emigrant survival of Twisp River steelhead.  Emigrant-per-redd values were not calculated for incomplete brood years.  DNOT = Did not operate trap. 

 Artificial Propagation of Steelhead in the Methow River Basin.

 Wells Hatchery began steelhead production following the completion of Wells Dam in 1968, with the first juvenile fish released into the Methow River in the spring of 1969.  Broodstock for Methow Basin artificial production was derived from adult fish collected from the fish ladders at Wells Dam, and contained a mixture of hatchery and naturally produced adults.  Prior to the 2004 brood, naturally produced fish were retained for broodstock as they occurred in the run at large passing Wells Dam, and comprised on average 7% of the broodstock for the 1995-2003 broods.  Beginning with the 2004 brood, collections targeted an increased proportion of the naturally produced fish and the 2004-2009 broods contained an average of 21% naturally produced fish.  Steelhead progeny were reared at Wells Hatchery and released into the Methow and Okanogan river basins as yearling smolts.  Additionally, juvenile steelhead were routinely released as fry or smolts into the Columbia River directly adjacent to the hatchery, but releases of this type ceased in the mid 1990’s.  With few exceptions, Methow Basin steelhead releases for broods prior to 1997 occurred at a single location annually at rkm 10.  Beginning with the 1997 brood, Methow Basin releases shifted to upper basin tributaries as the program goals changed from production to supplementation purposes.  Since the 1997 brood, mean number of fish released in the Methow River (N = 96,906), Twisp River (N = 109,526), and Chewuch River (N = 97,167) have approximately divided the total basin releases equally. 

 Gametes from naturally produced adults likely contributed to the juvenile steelhead populations at about the same rate at which they were represented in the broodstock (i.e., 7%) prior to the 1997 brood.  After that time, the contribution of naturally produced fish was managed to produce progeny of 100% H x W genetic crosses for study purposes (1997-1999 broods) or to adhere with the tenets of supplementation (2000 brood-present).  Juvenile releases into the Twisp River have been almost exclusively accomplished with progeny of H x W genetic crosses.  These releases have occurred at the river kilometer (rkm) 21, with an additional small group of fish released annually from semi-natural ponds located at rkm 2. 

 Key questions our study will address:

 1)  What is the relative reproductive success of hatchery steelhead when they spawn in nature? 

 This question is important for several reasons.  Many naturally spawning steelhead populations in the Columbia River Basin contain varying numbers of hatchery-produced fish.  If the naturally spawning hatchery fish are part of a supplementation program, then estimating their relative fitness is necessary for evaluating the effects of the program.  For example, if the relative reproductive success of the hatchery fish is low, the program is unlikely to be successful at increasing natural production.  Evaluating relative reproductive success is therefore critical for determining if the considerable investment the region has made in hatchery supplementation programs is actually helping recover populations.  Hatchery fish can also mask the status of natural populations.  For example, in a large scale analysis of the extinction risk of Columbia River salmon populations, McClure et al. (2003) bracketed their analysis by assuming that naturally spawning hatchery fish had a relative fitness of either 0 or 1.  In nearly every case, what was assumed about hatchery fish spawning success had a substantial effect on the estimate of the natural population’s population growth rate, and for 25% of the populations evaluated, the estimates of natural population growth rate changed sign depending on what was assumed about the contributions of naturally spawning hatchery fish to natural population growth.  By directly measuring the relative reproductive success of hatchery fish, the viability of natural populations receiving substantial hatchery fish can be much more accurately evaluated.

 2)  If a difference in relative reproductive success is found between hatchery and natural-origin steelhead, can the difference be explained by differences in measurable biological traits that differ between hatchery and natural fish?

 In specific case studies, several investigators have found biological differences between hatchery and naturally produced fish that, at least in part, explain why hatchery fish may have relatively low fitness in the natural environment.  For example, Fleming and Gross (1992, 1993, 1994) made detailed observations of the spawning behavior of natural and hatchery coho salmon, and found that the hatchery-produced males were less aggressive courting females and less able to fend off other males in competition.  The same investigators also found physical differences between hatchery and natural fish that likely contributed to the poor performance of the hatchery fish.  Fleming et al. (1996) obtained similar results in a more recent study of Atlantic salmon.  In another study, Berejikian (1995) found that hatchery-produced juvenile steelhead were more vulnerable to predation than naturally produced steelhead because the hatchery fish were more aggressive about feeding in the presence of predators.  Schroder et al. (2008) attributed the 5.6% decrease in egg-to-fry survival of first-generation hatchery spring Chinook to subtle differences in spawning behavior and redd location in a spawning channel.  More recently, Ford et al. (2009) reported the spatial distribution of redds within a spawning tributary was a significant factor in the relative reproductive success of hatchery spring Chinook salmon.    

 Despite the studies referenced above, determining the proximate biological mechanisms for any observed differences in fitness between hatchery and natural fish remains an important problem.  Most of the studies examining how morphological and behavioral traits influence fitness in salmonids have been conducted over very limited parts of the life-cycle, and it is important to understand how these traits affect life-time fitness.  There have been relatively few studies examining how variation among individual fish contributes to differences in fitness between hatchery and natural populations.  Instead, most studies (e.g., Leider et al. 1990; Reisenbichler and McIntyre 1977) measured average differences in reproductive success or survival between groups of fish.  By measuring the fitness of individual fish, we will obtain a much more complete picture of how variation in measurable traits influences fitness than has been obtained from most studies conducted to date. 

 Understanding the biological differences between hatchery and natural fish that are the causes of any differences in fitness is important because it will provide insight into how likely it is that the fitness of hatchery fish can be increased by relatively simple changes in rearing, breeding, or release strategies.  For example, early spawn timing by some hatchery steelhead has been hypothesized to contribute to their poor performance (Chandler and Bjornn 1988; Leider et al. 1984), suggesting that maintaining a natural run and spawn timing distribution should be an important goal of steelhead supplementation programs.  In our study, we will be able to specifically estimate the functional relationship between a series of measured characteristics (e.g., spawn timing and redd morphology) of individual fish and correlate life-time fitness for both hatchery and natural fish, thereby increasing our knowledge of not only if hatchery steelhead have lower relative fitness than natural steelhead, but also why.  Unlike similar studies of Pacific salmon, we will attempt to collect data for numerous traits on individual fish on the spawning grounds.  These traits may or may not be genetically-linked, but will provide an opportunity to examine their influence on fitness.     

 3)  If hatchery-produced steelhead have initially low relative reproductive success, to what degree is this effect reduced in their natural origin progeny?  In other words, does the 'hatchery' effect disappear to an appreciable degree after a generation of natural production?

 One of the surprising conclusions from several studies of the fitness of hatchery fish in the natural environment is that genetic-based fitness differences have been found after only two-to-five generations of hatchery rearing .  Early results from the Yakima River suggest that differences between hatchery and wild fish are expressed only after a single generation in the hatchery (Schroder et al. 2008).  That selection in hatcheries can produce such rapid genetic changes in salmon populations is both disturbing and encouraging.  On the one hand, if hatchery breeding and rearing can result in substantial genetic changes in a population after only a few generations, this suggests that selection pressures in typical hatchery environments may be so strong that even relatively recently founded broodstocks may be too “domesticated” to be useful for supplementation purposes.  On the other hand, the very speed with which the changes occur suggests that hatchery fish might be able to rapidly adapt back to the natural environment if given a chance to do so.  There are a large number of hatchery programs in the Pacific Northwest that are releasing locally derived stocks that have been hatchery propagated for many generations.  Measuring how quickly these stocks can readapt to a full life cycle in a natural environment will determine how useful these stocks might be in recovery efforts. Using highly polymorphic microsatellite DNA markers and/or single nucleotide polymorphisms (SNPs; see below), we propose to track individual lineages across two or more generations and then using these data to estimate the rate at which hatchery fish readapt to the natural environment.