Seasonal Patterns of Predation on Juvenile Pacific Salmon by ...

Transactions of the American Fisheries Society 137:165–181, 2008 Ó Copyright by the American Fisheries Society 2008 DOI: 10.1577/T07-049.1

[Article]

Seasonal Patterns of Predation on Juvenile Pacific Salmon by Anadromous Cutthroat Trout in Puget Sound ELISABETH J. DUFFY* School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, Washington 98195-5020, USA

DAVID A. BEAUCHAMP U.S. Geological Survey, Washington Cooperative Fish and Wildlife Research Unit, School of Aquatic and Fishery Sciences, University of Washington, Box 3550207, Seattle, Washington 98195-5020, USA Abstract.—In the marine environment, Pacific salmon Oncorhynchus spp. suffer the greatest natural losses during early marine residence, and predation is hypothesized to be the key source of mortality during this life history stage. In the face of recent declines in Puget Sound salmon populations, our goal was to determine the extent of predation mortality on salmon during early marine life. In spring and summer of 2001–2003, we caught juvenile salmon and potential predators at nearshore areas in northern and southern regions of Puget Sound, Washington. We focused on the potential predation impact of coastal cutthroat trout O. clarkii clarkii, which were caught in low but consistent numbers in both regions and were the most abundant large-bodied potential predators of juvenile salmon in our catches. Cutthroat trout consumed a diverse and dynamic array of diet items and became increasingly piscivorous with increasing fork length above 140 mm. Cutthroat trout consumed a greater biomass of Pacific herring Clupea pallasii than any other prey fish species, but juvenile salmon were particularly important prey between April and June, making up greater than 50% of the fish prey consumed. Cutthroat trout exhibited size-selective predation, eating salmon that were smaller than the average size of conspecific prey available in the environment. For a hypothetical size-structured population of 1,000 cutthroat trout, pink salmon O. gorbuscha and chum salmon O. keta contributed the greatest number of salmon to the diet but Chinook salmon O. tshawytscha contributed the greatest salmonid biomass. On an order-of-magnitude basis, these predation estimates represented a relatively minor amount of early marine mortality for Chinook salmon and lower rates for the other salmon species. Conversely, juvenile salmon contributed significantly to the spring energy budget for cutthroat trout in Puget Sound.

In the marine environment, Pacific salmon Oncorhynchus spp. suffer the greatest natural losses during estuarine and early marine residence (Parker 1962; Royal 1962; Furnell and Brett 1986). Predation is hypothesized to be the key source of the mortality during this life history stage (Parker 1971; Beamish and Mahnken 1998; Brodeur et al. 2003). Juvenile salmon enter the nearshore marine environment at a size vulnerable to many potential predators, including larger salmon (Parker 1971; Kaczynski et al. 1973; Fresh et al. 1981; Wing 1985; Mortensen et al. 2000; Orsi et al. 2000), coastal cutthroat trout O. clarkii clarkii (Salo et al. 1980; Fresh et al. 1981; Jauquet 2002), Pacific cod Gadus macrocephalus (Salo et al. 1980), walleye pollock Theragra chalcogramma (Willette 1996), Pacific hake Merluccius productus (Emmett 2006; Emmett and Krutzikowsky, in press), spiny dogfish Squalus acanthias (Beamish et al. 1992; Orsi et al. 2000), birds, and marine mammals (Emmett * Corresponding author: [email protected] Received March 5, 2007; accepted September 9, 2007 Published online January 8, 2008

1997). Size at ocean entry partially determines predation risk for salmon smolts (Parker 1971; Healey 1982; Ward et al. 1989; Holtby et al. 1990; Henderson and Cass 1991). According to size spectrum theory, large fast-growing individuals are less vulnerable to gape-limited predators than their smaller, slowergrowing conspecifics (Sogard 1997). Consequently, favorable early marine growth conditions are considered a key to high salmon survival, as faster early marine growth has been associated with elevated overall marine survival for several salmon species (Holtby et al. 1990; Hargreaves 1997; Murphy et al. 1998; Tovey 1999; Beamish et al. 2004; Moss et al. 2005). Anadromous coastal cutthroat trout have complex and diverse life history patterns (Johnson et al. 1999). Coastal cutthroat trout mature at approximately age 4 and have been known to spawn for more than six consecutive years. Much of the population migrates seaward in the spring and returns to freshwater in the late fall to overwinter and spawn. Juvenile cutthroat trout first enter the protected waters of Puget Sound at age 2 (a few as early as age 1), slightly earlier than

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populations on the open coast (Trotter 1989). Entry of subadult and adult cutthroat trout into Puget Sound peaks in the early spring (Wenburg 1998), just before the peak ocean migration periods of juvenile salmon and trout (Wenburg 1998; Brennan et al. 2004; Duffy et al. 2005). Spatial and temporal overlap of cutthroat trout with these and other nearshore prey resources might have influenced selection for the timing of marine entry (Johnston 1982; Wenburg 1998). In Puget Sound, a few studies have reported low levels of salmon predation by cutthroat trout (1 fish per stomach) based on estimates from limited diet analysis (Mathews and Buckley 1976; Cardwell and Fresh 1979; Fresh et al. 1981; Simenstad et al. 1982); however, most studies were not designed to investigate predation. A recent study in southern Puget Sound found that cutthroat trout preyed heavily (15–46% of the diet by wet weight, depending on predator size) on juvenile chum salmon O. keta when the fry were available in March and April but not at all during the remaining months (Jauquet 2002). To infer an overall potential predation impact, diet data must be collected at the appropriate spatial and temporal scales and must be used in conjunction with predator abundances (Beauchamp et al. 1995). Even low apparent levels of predation can translate into substantial losses if predator populations are large and predation occurs over a protracted time interval. In addition, intense predation events can be episodic—for example, during pulses of fish associated with natural migrations (Jauquet 2002) or hatchery releases (Scheel and Hough 1997; Cartwright et al. 1998; Baldwin et al. 2000) and at physical bottlenecks, such as river mouths (Emmett 1997; Roby et al. 2003). Several salmon populations in Puget Sound have experienced recent declines, most notably Chinook salmon O. tshawytscha, which are now listed under the U.S. Endangered Species Act. These declines may reflect increased predation mortality, more degraded rearing conditions, or both, relative to periods of higher marine survival. Ocean-type Chinook salmon make extensive use of estuarine environments (Stober et al. 1973; Shepard 1981; Healey 1982; Simenstad et al. 1982) and spend the longest duration in nearshore habitats among all salmon species in Puget Sound (Congleton et al. 1982; Simenstad et al. 1982; Hodgson and Brakensiek 2003; Brennan et al. 2004; Toft et al. 2004; Duffy et al. 2005). Upon entry into Puget Sound, Chinook salmon are roughly twice the size of pink salmon O. gorbuscha and chum salmon, and coho salmon O. kisutch are up to four times the size of these fish (Brennan et al. 2004; Duffy et al. 2005). Consequently, based on size alone, pink and chum salmon would be expected to be most vulnerable to a

wider range of potential predators, while coho salmon would be least susceptible to heavy predation losses; moreover, coho salmon are potential predators of pink and chum salmon fry (Hunter 1959; Duffy 2003). However, factors such as timing of entry, residence time, and habitat choice may also affect the realized predation risk to individual salmon species. Bioenergetically based food web models used in conjunction with directed field sampling provide an effective method for quantifying the dynamics of predation impacts within a temporal, spatial, and ontogenetic framework (Ney 1990; Hansen et al. 1993). The widely used Wisconsin bioenergetics model (Hanson et al. 1997) employs an energy balance approach for estimating consumption (C) that responds to changes in body size, temperature, and diet. The Wisconsin model is very adaptable and operates on a daily time step, which allows for a fine-grained analysis of trophic interactions over short time scales. This sensitivity is particularly appropriate for dynamic conditions, like those experienced by migrating salmon and trout, for which residence times are variable and temporary and environmental factors (i.e., water temperature), diets, and prey sizes are rapidly changing. In spring and summer of 2001–2003, we collected juvenile salmon, potential competitors, and potential predators in northern Puget Sound (NPS) and southern Puget Sound (SPS; Figure 1). Cutthroat trout were caught in low but consistent numbers in both regions; based on stomach content analysis of many nearshore fishes, cutthroat trout represented the most likely potential piscine predator of juvenile salmon encountered in nearshore areas. Our objectives were to determine the feeding habits of cutthroat trout and to identify the extent to which they prey on juvenile salmon in Puget Sound. We examined both temporal– spatial variability and ontogenetic shifts in the diet of cutthroat trout to determine whether predation on juvenile salmon was size structured. We used the Wisconsin bioenergetics model to estimate (1) sizespecific seasonal consumption demand by individual cutthroat trout for juvenile salmon prey (by species when available) and (2) the potential impacts on specific salmon populations. We hypothesized that although cutthroat trout eat juvenile salmon episodically, salmon are an important component of their diets; we also hypothesized that predation by cutthroat trout substantially affects specific salmon populations. Study Area Puget Sound is a deep, elongated glacial fjord composed of underwater valleys, ridges, and basins, and has an average depth of 135 m. The Main Basin, from Admiralty Inlet to the Tacoma Narrows, is the

CUTTHROAT TROUT PREDATION ON JUVENILE SALMON

167

FIGURE 1.—Northern Puget Sound (NPS) and southern Puget Sound (SPS), Washington, study regions and sampling locations, where cutthroat trout predation on juvenile salmonids was examined (circles ¼ nearshore and squares ¼ delta beach seining and gillnetting locations; triangle ¼ site sampled only in 2003). Gray shading indicates the Main (dark), Whidbey (medium), and Southern (light) basins of Puget Sound.

deepest basin on average and contains the deepest point (.280 m: Burns 1985). On the northeast edge of the Main Basin, the Whidbey Basin is fed by Puget Sound’s largest rivers (Skagit, Snohomish, and Stillaguamish rivers) and receives 60% of the freshwater entering Puget Sound (Burns 1985). The Southern Basin receives less than 10% of the freshwater draining into Puget Sound; its primary freshwater sources are the Nisqually and Deschutes rivers but also smaller rivers and streams (Burns 1985). We focused on two sampling areas: the NPS region located in the southeastern part of Whidbey Basin and the SPS region located south of the Tacoma Narrows sill and north of the Nisqually River in the Southern Basin (Figure 1). These regions included saltwater entry points and presumptive rearing and migration corridors for several juvenile salmon and anadromous trout species, but differed in oceanographic conditions and inputs of hatchery salmon. The NPS region received freshwater inputs from Puget Sound’s three largest rivers and had substantial populations of both

hatchery and naturally produced salmon. The SPS region received substantially less riverine input, was cooler and more saline, and contained salmon populations that were dominated by hatchery production (especially Chinook salmon, but also coho and chum salmon). Within each sampling region, we chose five or six sites that included delta sites close to freshwater inputs and progressively more distant nearshore sites along exposed beaches. Methods Fish sampling.—Field sampling was designed to capture the peak window of juvenile salmon residence and migration through nearshore Puget Sound habitats (Duffy et al. 2005). We conducted biweekly beach seining (two sets per site) at each site in both regions during April–July 2001–2002 and during June–July 2003; monthly beach seining was performed in August–September 2001–2003. We completed 535 beach seine sets: 171 in 2001, 224 in 2002, and 140 in 2003. We used a floating beach seine (37 m long 3 2 m

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high; mesh was graded from 3 cm in the wings to 6 mm at the cod end) according to standard estuarine fish sampling protocol (Simenstad et al. 1991). According to this protocol, each set of the beach seine samples an average area of 520 m2 (Simenstad et al. 1991), which represents approximately 23 m of shoreline. In 2003, we also deployed experimental gill nets (1.8 m deep 3 25.5 m long; divided evenly into panels of 38-, 51-, 64-, 76-, and 89-mm stretch mesh) to target the larger potential salmon predators. We set gill nets perpendicular to shore twice at each site in water ranging from 2.0 to 14.3 m deep. We completed 69 gill-net sets, each lasting 0.5–2.5 h depending on water temperature and catch success. All fish captured in each set were counted and individual fork lengths (FLs; nearest 1 mm) were recorded for subsamples of each species (at least 30 fish/species when available). When possible, wet weights (nearest 0.1 g) were recorded for all cutthroat trout. We used nonlethal gastric lavage to obtain gut contents from cutthroat trout and other potential juvenile salmon predators that had first been anesthetized with tricaine methanesulfonate (MS-222). Stomach contents of cutthroat trout were analyzed in the laboratory. Using a dissecting microscope, we separated invertebrate prey items into broad taxonomic categories and identified each fish prey to species when possible. Blotted wet weights of all prey categories and each prey fish were recorded to the nearest 0.0001 g using an electronic scale. The proportional wet weight contribution of each prey category was calculated individually for all nonempty stomachs. Prey fish FLs were also recorded when available. Size distributions of salmon that had been eaten by cutthroat trout were compared with the species-specific in situ size distributions at coincident locations and dates in two ways. First, we used the Kolmogorov–Smirnov (KS) test (Zar 1999) to determine whether the distributions of sizes differed. Then, we used two-sample t-tests (Zar 1999) to compare the means of the two distributions to determine whether cutthroat trout exhibited sizeselective predation on salmon. The average catch per unit effort (CPUE; number of fish per seine haul) was calculated for cutthroat trout captured by beach seine in each sampling region (over all sampling dates in April–September 2001–2003). Log10(CPUE þ 1) transformed catch data were subjected to analysis of covariance (ANCOVA; Zar 1999) to examine the effects of year (2001–2003), region (NPS, SPS), and zone (delta, near shore) using month as a covariate. Two-way and higher-order interaction terms were omitted if not significant in the initial analysis. Subsequent analyses were conducted on significant main effects and interaction terms

using analysis of variance or ANCOVA and Bonferroni correction for multiple comparisons (Zar 1999). Bioenergetics modeling.—We modeled C by cutthroat trout using the Wisconsin bioenergetics model (Hanson et al. 1997). In the model, total energy consumption (i.e., C) over a particular time frame equals the sum of growth (G, positive or negative), metabolic costs (M), and waste losses (W): C ¼ G þ M þ W: Typically, the model, which operates on a daily time step, is used to estimate C by individuals of a species at a given life history stage. The primary model inputs are thermal experience (temperature experienced by the predator), diet, prey and predator energy densities, and growth. For the cutthroat trout model, we used the model’s default physiological parameters for coho salmon except that we modified two of the temperature-dependent parameters affecting maximum C, or Cmax (critical thermal optimum ¼ 148C and critical thermal maximum ¼ 168C; Beauchamp et al. 1995). Consumption estimates from this parameterization agreed well with independent, field-generated C estimates for piscivorous cutthroat trout (Cartwright et al. 1998; Mazur and Beauchamp 2006). Thermal experience.—We used water temperatures that had been measured in 2001–2002 at nearshore sampling sites (1-m depth) using a YSI Model 55 handheld dissolved oxygen and temperature system (Table 1). The model interpolated temperature values between sampling dates. Growth.—We used pooled catch and size distribution patterns to identify size-based cohorts in the cutthroat trout population based on their modal size at first observation in the catch and determined the relative proportions of these size-classes by region. Size modes were interpreted to represent approximate age-classes or cohorts. We estimated growth in each sampling region from the seasonal increases in these modal lengths. Growth attained during a growing season in Puget Sound was assumed to be the difference between adjacent modes at first appearance in the catch (April– June) and the final sampling dates (mid-September). This measure of apparent growth assumed that fish caught in different months were representative of the common population at large in NPS and SPS during the study period. This method could either under- or overestimate actual growth if the captured cutthroat trout originated from different populations. To obtain seasonal changes in body mass, FL data were converted to wet weights using regressions derived from measurements made in this study (r2 ¼ 0.985, n ¼ 56; FL range ¼ 78–346 mm):


TABLE 1.—Average and SD of water temperatures (T; 8C at 1-m depth) at nearshore sampling sites in northern Puget Sound (NPS) and southern Puget Sound (SPS), Washington, 2001–2002. NPS

SPS

Date

T

SD

9 Apr 18 Apr 23 Apr 3 May 6 May 8 May 15 May 17 May 21 May 29 May 4 Jun 12 Jun 19 Jun 26 Jun 2 Jul 10 Jul 16 Jul 24 Jul 30 Jul 7 Aug 20 Aug 10 Sep 20 Sep

9.6

0.6

10.2 12.7 11.5

0.5 1.2 1.4

11.9 14.5 14.5

0.4 0.5 1.0

15.2 15.3 15.7 16.6 17.4 15.7 16.8 17.0 16.0 15.5 14.8

1.2 1.0 0.3 2.3 0.1 0.8 0.9 1.1 0.2 0.9 0.2

T

SD

9.8 9.6

0.7 0.4

9.6 9.5 10.9 11.3 10.7 12.3 12.0 12.6 12.4 12.5 14.1 13.9 13.3 13.7 14.3 14.4 14.4 14.2 13.9

0.6 0.7 0.9 1.9 0.6 1.6 0.6 0.8 1.2 0.4 0.5 0.9 0.7 0.7 0.9 0.6 0.2 0.8 0.7

Cutthroat trout wet weight ðgÞ ¼ 0:000007 3 FL3:0703 : Diet composition.—We used cutthroat trout cohorts identified in the catch data to determine cohort-specific monthly average diet proportions (by wet weight) using April–September data pooled over 2001–2003 (Table 2). We grouped all invertebrate prey into one category to simplify the variability in diet items and to focus on the piscivorous component of the cutthroat trout diet. Energy density.—We used literature energy density values for prey items that were most comparable with organisms found in Puget Sound and used averages of similar prey types when specific values were unavailable (Table 3). For energy density of cutthroat trout, we used the model’s default equation, which changes as a function of body weight (Cartwright et al. 1998). Simulations.—We ran bioenergetics simulations of seasonal growth for the most abundant cutthroat trout size modes (cohorts 1–3) in each sampling region. In these simulations, we estimated C by calculating the energy required to satisfy the apparent growth rate of cutthroat trout over the specified simulation periods (110–155 d) given the diet composition and thermal regime measured during these periods (Table 4). The purpose of these simulations was to quantify the consumption demand for individual species of juvenile salmon in each sampling region for comparison with the consumption demand for other key prey categories.

169

Results Distribution and Size Cutthroat trout (n ¼ 497) were caught in low but consistent numbers throughout the spring and summer during all years. There were no significant differences in the average CPUE of cutthroat trout between NPS and SPS or among years (ANCOVA: P . 0.05). However, the average cutthroat trout CPUE at delta sites (0.72 fish/haul) was significantly higher (ANCOVA: P , 0.01) than that at nearshore sites (0.29 fish/haul). While the largest cutthroat trout (up to 490 mm FL) were captured by both beach seines and gill nets, the smallest cutthroat trout (,180 mm FL) were captured exclusively in beach seines. The size distribution of cutthroat trout varied both seasonally and between regions (Figure 2). In NPS, small fish were most abundant in the catch during the late spring and early summer (May–July), whereas more of the large fish were caught in September, presumably when mature cutthroat trout began to return to freshwater to overwinter and spawn. In SPS, cutthroat trout were similar in size throughout the sampling season, although a cohort of smaller fish (100–140 mm FL), probably fish entering Puget Sound for the first time, appeared in June and July. We identified three major size cohorts of fish in each region based on the modal FL at the earliest point in the season (Figure 2). We assumed that these cohorts were representative of age-classes or comparable life history strategies. The intermediate-sized (171–270 mm FL; cohort 2) and largest (.270 mm FL; cohort 3) cutthroat trout were present in Puget Sound from mid-April to late September. Small (170 mm FL early in the season; cohort 1) cutthroat trout occupied sampling areas during May–September (NPS) or June–September (SPS), although fish in this cohort entered the catches at a smaller FL in SPS (110 mm) than in NPS (140 mm). These three cohorts were used for model simulations. Diet Diets of cutthroat trout varied by season, region, and predator size (Table 2). We examined the stomach contents of 405 cutthroat trout: 92 in 2001, 183 in 2002, and 130 in 2003. Empty stomachs accounted for 6.5% of 2001 samples, 15.9% of 2002 samples, and 6.2% of 2003 samples. Prey items included benthic (gammarid amphipods, isopods, shrimp, polychaetes, chironomid pupae) and planktonic (euphausiids, hyperiid amphipods, crab larvae, barnacle molts, cladocerans) invertebrates, adult insects, and fish. Cutthroat trout were more piscivorous at NPS sites than at SPS sites. Cutthroat trout fed most heavily on juvenile salmon during April–May in NPS and May–June in SPS (Table 2). Pacific herring Clupea pallasii, Pacific sand lances

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TABLE 2.—Average monthly diet composition (wet weight proportions) for cutthroat trout caught in northern and southern Puget Sound, Washington, during 2001–2003. Values were used as inputs for cohort-specific bioenergetics model simulations. Values of 0.10 or more are in bold type. Invertebratesa Cutthroat trout cohort

1

2

3

1

2

3

a b c

Month

Salmonidsb

Nonsalmonid fishesc

N Average FL (mm) SD BEN PLA INS OTH CHN CHM CHO PNK UNI PHG PSL SSM SPE OTH

May Jun Jul Aug Sep Apr May Jun Jul Aug Sep Apr May Jun Jul–Aug Sep

6 13 30 4 7 6 23 13 30 4 7 14 3 10 6 10

159 160 202 213 254 231 196 203 202 213 254 312 298 338 334 360

11 7 17 11 15 27 21 21 17 11 15 54 10 38 33 55

0.45 0.33 0.23 0.00 0.39 0.09 0.38 0.44 0.23 0.00 0.39 0.71 0.32 0.00 0.17 0.29

Northern Puget Sound 0.24 0.04 0.01 0.00 0.25 0.01 0.00 0.00 0.10 0.16 0.00 0.00 0.00 0.00 0.25 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.03 0.00 0.10 0.00 0.09 0.11 0.10 0.09 0.00 0.00 0.10 0.16 0.00 0.00 0.00 0.00 0.25 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.07 0.00 0.15 0.11 0.08 0.00 0.00 0.00 0.00 0.08 0.00 0.00 0.00 0.17 0.00 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.00 0.07 0.00 0.00 0.00 0.00 0.00 0.07 0.00 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.27 0.02 0.00 0.00

0.17 0.00 0.00 0.00 0.00 0.40 0.09 0.00 0.00 0.00 0.00 0.07 0.00 0.00 0.00 0.00

0.00 0.00 0.02 0.00 0.00 0.12 0.10 0.00 0.02 0.00 0.00 0.00 0.06 0.10 0.00 0.00

0.00 0.00 0.00 0.00 0.29 0.00 0.00 0.00 0.00 0.00 0.29 0.00 0.00 0.60 0.17 0.20

0.09 0.36 0.39 0.00 0.22 0.18 0.04 0.35 0.39 0.00 0.22 0.04 0.00 0.00 0.33 0.31

0.00 0.00 0.00 0.11 0.00 0.00 0.00 0.00 0.00 0.11 0.00 0.04 0.00 0.00 0.00 0.00

0.00 0.00 0.04 0.39 0.00 0.00 0.00 0.00 0.04 0.39 0.00 0.00 0.00 0.10 0.00 0.10

0.00 0.05 0.06 0.25 0.10 0.11 0.09 0.02 0.06 0.25 0.10 0.00 0.00 0.10 0.16 0.10

Jun Jul Aug Sep Apr–May Jun Jul Aug Sep Apr May Jun Aug Sep

19 16 6 22 26 39 10 4 30 5 7 6 4 4

126 130 161 156 218 206 201 192 197 332 326 335 376 310

32 24 6 11 26 27 24 17 19 52 45 35 37 21

0.53 0.54 0.50 0.88 0.43 0.31 0.52 0.31 0.73 0.81 0.14 0.00 0.25 0.00

Southern Puget Sound 0.15 0.01 0.01 0.00 0.23 0.23 0.00 0.00 0.28 0.19 0.03 0.00 0.02 0.10 0.00 0.00 0.24 0.01 0.04 0.03 0.09 0.02 0.06 0.10 0.18 0.04 0.13 0.00 0.22 0.01 0.00 0.00 0.07 0.05 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.43 0.00 0.00 0.00 0.33 0.00 0.00 0.00 0.25 0.08 0.00 0.00 0.00

0.11 0.00 0.00 0.00 0.00 0.03 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.14 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.08 0.00 0.03 0.00 0.00 0.00 0.00 0.00 0.00 0.00

0.04 0.00 0.00 0.00 0.05 0.20 0.07 0.00 0.00 0.00 0.14 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.03 0.05 0.00 0.25 0.00 0.00 0.00 0.30 0.25 0.25

0.04 0.00 0.00 0.00 0.02 0.00 0.00 0.00 0.03 0.19 0.00 0.00 0.00 0.00

0.00 0.00 0.00 0.00 0.00 0.03 0.00 0.00 0.00 0.00 0.00 0.00 0.25 0.24

0.00 0.00 0.00 0.00 0.00 0.00 0.03 0.22 0.09 0.00 0.14 0.20 0.00 0.00

0.10 0.00 0.00 0.00 0.08 0.13 0.00 0.00 0.02 0.00 0.00 0.17 0.00 0.43

Invertebrate types are benthic (BEN), planktonic (PLA), insect (INS), and other (OTH). Salmonids are Chinook (CHN), chum (CHM), coho (CHO), pink (PNK), and unidentified (UNI) salmon. Nonsalmonid fishes are Pacific herring (PHG), Pacific sand lance (PSL), surf smelt (SSM), shiner perch (SPE), and other (OTH).

Ammodytes hexapterus, surf smelt Hypomesus pretiosus, and shiner perch Cymatogaster aggregata were common prey during the summer (Table 2). Predator Size–Prey Size Relationships Cutthroat trout became increasingly piscivorous with increasing size, generally incorporating fish into their

diet at approximately 140 mm FL (as small as 126 mm FL; Figure 3). Fish prey lengths constituted 4–51% of cutthroat trout predator FL (Pacific herring: 19–50%; salmon: 7–36%; Pacific sand lance: 4–46%; Figure 4). Cutthroat trout selectively consumed individuals that were significantly smaller than the in situ size distributions of pink salmon (KS test: P , 0.01; two-

TABLE 3.—Gross caloric density (J/g wet weight) values for cutthroat trout prey organisms and the estimated fraction of prey that is indigestible. Prey group

Energy density (J/g)

Indigestible fraction (%)

Invertebrate

3,321

15

Salmon–juvenile Sand lance–juvenile

5,200 5,315

9 9

Other fish

5,260

9

a

Literature values are summarized in this reference.

Sample area

Reference a

Port Susan, Puget Sound

Davis 1993 ; Davis et al. 1998 Hanson et al. 1997 Duffy 2003

Comments Average for common invertebrate prey in cutthroat trout diets Pink salmon regression from bioenergetics model June 2002, for 25–40 mm FL fish Average of salmon and sand lance juveniles

171


TABLE 4.—Cutthroat trout growth simulations using the bioenergetics model fitted to start and end weights (wet weight, WW). Abbreviations are as follows: G is the average daily growth (in fork length), C is total consumption over the simulation period, p is the proportion of maximum consumption, GE, the growth efficiency, is the ratio of growth to consumption, both in grams; NPS is northern Puget Sound, and SPS is southern Puget Sound. Cohort

Start date

End date

NPS–1 SPS–1 NPS–2 SPS–2 NPS–3 SPS–3

1 May 2 Jun 18 Apr 18 Apr 18 Apr 18 Apr

20 20 20 20 20 20

Sep Sep Sep Sep Sep Sep

Duration (d)

Start WW (g)

End WW (g)

G (mm/d)

p

C (g)

GE (%)

142 110 155 155 155 155

27.19 16.94 58.81 58.81 254.33 254.33

124.83 49.35 181.88 142.25 493.98 453.05

0.63 0.45 0.52 0.39 0.45 0.39

0.63 0.63 0.60 0.54 0.59 0.46

559.38 258.47 857.97 701.11 2020.95 1476.44

17 13 14 12 12 13

sample t-test: P , 0.01), chum salmon (KS test: P , 0.01; two-sample t-test: P , 0.01), and Chinook salmon (KS test: P , 0.01; two-sample t-test: P , 0.01; Figure 5). Bioenergetics Modeling Model simulations indicated that cutthroat trout were feeding at 46–63% of Cmax and exhibited growth efficiencies of 12–17% across all cohorts and regions (Table 4). The two cohorts with the greatest FLs consumed a slightly higher proportion of their theoretical Cmax at NPS than at SPS (Table 4), which is probably due in part to the higher estimates of growth rate in NPS. The two cohorts with the smallest FLs (cohorts 1 and 2) were more piscivorous in NPS than in SPS (Figure 6), which was partly due to the larger FL of cohort 1 in NPS. Cutthroat trout from this cohort began the simulation at the approximate size threshold of 140 mm FL for piscivory, whereas many of the small cutthroat trout in SPS needed to grow past the piscivory size threshold during the simulation period. Growth efficiencies were similar between the two regions, although the smallest cutthroat trout experienced substantially higher growth efficiency in NPS than in SPS (Table 4), which corresponded with the larger fraction of high-energy fish prey in the diet at NPS sites. Overall, Pacific herring, salmon, and Pacific sand lances, in that order, accounted for the greatest biomass of prey fish that were consumed by cutthroat trout in our simulations. In NPS, Pacific sand lances (31%), Pacific herring (25%), and salmon (17%) represented most of the prey fish biomass consumed by all cohorts of cutthroat trout, whereas salmon (30%) and Pacific herring (18%) contributed most of the prey fish biomass consumed in SPS (Figure 6). Surf smelt and shiner perch represented a substantial proportion of the other prey fish consumed in SPS (Figure 6). The cohort with intermediate FLs (cohort 2) consumed salmon primarily between April and June; salmon accounted for 55–66% of fish prey

biomass consumed during those months in SPS and 68% (April) and 37% (May) of fish prey biomass consumed in NPS. The cohorts with the greatest FLs were highly piscivorous in both regions, and Chinook salmon represented the greatest proportion of the salmon biomass eaten by these cohorts, especially during summer (July–August). Salmon contributed significantly to the cutthroat trout’s overall energy budget (total J of energy consumed) in the spring and (to a somewhat lesser extent) early summer. In April–May, salmon were responsible for 48% (SPS) and 29% (NPS) of the total energy budget of cutthroat trout. Salmon made up an additional 25% (SPS) and 12% (NPS) of the energy budget in June–July. The percentage of salmon contributing to the energy budget both increased and extended progressively later into the summer with increasing predator size. We calculated the regional consumption demand for a size-structured population of 1,000 cutthroat trout on individual prey groups based on the relative catch proportions (from Figure 2) of the three size cohorts used in model simulations. In NPS, the consumption demand for this population included 338.9 kg of invertebrate prey, 196.6 kg of Pacific sand lances, 128.5 kg of Pacific herring, 69.2 kg of salmon, 72.7 kg of shiner perch, 15.4 kg of surf smelt, and 103.4 kg of other fish. In SPS, the consumption demand consisted of 323.4 kg of invertebrate prey, 49.6 kg of salmon, 38.7 kg of Pacific herring, 24.7 kg of shiner perch, 15.9 kg of surf smelt, 3.3 kg of Pacific sand lances, and 25.4 kg of other fish. Close to half of the salmonid biomass consumed by this population of cutthroat trout was made up of Chinook salmon (47% for NPS; 56% for SPS). Based on the size distribution of each salmon species found in cutthroat trout stomachs (Table 5), we converted wet weight C by this size-structured population of 1,000 cutthroat trout into numerical predation estimates on juveniles of individual salmon species (Table 6). The size-structured population of

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FIGURE 2.—Length frequency (20-mm FL bins) of cutthroat trout caught by beach seining and gillnetting in northern Puget Sound (NPS; black bars) and southern Puget Sound (SPS; gray bars), Washington, during April–September 2001–2003. Reference lines identify cohorts, initial FLs (upper panel: NPS cohorts 1–3 and SPS cohorts 2–3; middle panel: SPS cohort 1), and final FLs (lower panel: black ¼ NPS cohorts 1–3, light gray ¼ SPS cohorts 1–3) used for model simulations.

1,000 cutthroat trout consumed an average of 91,164 juvenile salmon of all species in NPS and 71,804 in SPS but could have consumed up to 164,853 salmon of the smallest sizes found in NPS stomachs and up to 118,273 of the smallest salmon found in SPS stomachs.

Depending on prey size, Chinook salmon would contribute approximately 4,600–16,900 of the juveniles eaten by the size-structured population in NPS and between 3,300 and 13,000 of those consumed in SPS. The cohort with the smallest FLs (cohort 1) consumed


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FIGURE 3.—Cutthroat trout FL (n ¼ 360) versus wet weight (ww) proportions of fish prey consumed in Puget Sound, Washington, during 2001–2003 as determined by gastric lavage. The dotted line represents the apparent size threshold for piscivory.

FIGURE 4.—Cutthroat trout FL versus FL of fish prey consumed in Puget Sound, Washington, during 2001–2003 (sand lance ¼ Pacific sand lance; herring ¼ Pacific herring; smelt ¼ surf smelt; perch ¼ shiner perch). Lines indicate prey FLs that are 40% (black line) and 50% (dotted) of predator length.

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FIGURE 5.—Length frequency distributions (5-mm FL bins) of salmonids captured by beach seining (black bars) or consumed by concurrently seined cutthroat trout (gray bars) in northern Puget Sound (NPS) or southern Puget Sound (SPS), Washington, during April and May 2002.

typically only smaller pink, chum, and unidentified salmon. The cohort with intermediate FLs (cohort 2) consumed the greatest number of salmon, eating predominantly pink salmon and the smaller unidenti-

fied salmon (probably pink and chum salmon, based on size). Identifiable Chinook salmon were only eaten by cutthroat trout larger than 170 mm FL, and only the largest cutthroat trout fed on coho salmon.


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FIGURE 6.—Simulated estimates of monthly individual consumption (g/month) of various prey types (invert ¼ invertebrates; herring ¼ Pacific herring; sand lance ¼ Pacific sand lance; smelt ¼ surf smelt; perch ¼ shiner perch) by three cutthroat trout cohorts in northern Puget Sound (NPS; left panels) and southern Puget Sound (SPS; right panels), Washington, during 2001–2003.

Discussion In nearshore waters of Puget Sound, cutthroat trout consumed a diverse array of diet items suggestive of opportunistic feeding. Cutthroat trout became increas-

ingly piscivorous after attaining 140 mm FL and were more piscivorous in NPS than in SPS. While Pacific herring were the most consumed prey fish (by weight) overall, juvenile salmon were particularly important prey between April and June. In addition to variable

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TABLE 5.—Average (range) fork lengths (FL, mm) and regression-derived wet weights (WW, g) of prey fish consumed by cutthroat trout in Puget Sound, Washington, during 2001–2003. Values in bold type were used to calculate consumption estimates for Table 6. Unidentified salmon Cutthroat Month trout cohort May Jun Jul Apr May Jun Jul Apr May Jun Jul Aug

1 1 1 2 2 2 2 3 3 3 3 3

FL a

32 51 43 30 27 60 64 55a 77a 74

Pink salmon

WW b

(25–42) (50–53) (43) (21–37)d (20–35) (42–82) (55–73) (28–95)b (54–95)b (73–74)

a

0.3 1.1c 0.6c 0.2 0.1c 2.0g 2.5g 2.3 4.3 3.9g

FL

(0.1–0.6) (1.0–1.2) (0.6) (0.1–0.4) (0.1–0.3) (0.7–5.3) (1.5–3.7) (0.1–8.4) (1.4–8.4) (3.7–3.9)

b

WW

Chum salmon FL

WW

34 (30–42)

0.3 (0.2–0.6) 29 (25–32) 35 (27–44)

30 38 49 60 31

0.2 0.4 1.0 1.9 0.2

(21–37) (27–67) (44–64)h (55–73)f (28–34)

(0.1–0.4) (0.1–2.8) (0.7–2.4) (1.4–3.7) (0.1–0.3)

Chinook salmon FL

0.2 (0.1–0.2) 0.3 (0.1–0.7)

32 (30–34) 0.2 (0.2–0.3) 61 (46–77)e 32 (30–34)f 0.2 (0.2–0.3) 61 (46–77) 49 (44–64)h 0.9 (0.7–2.2) 68 (55–89) 36 (31–41)

WW

0.3 (0.2–0.5) 71 71 85 91 97

(54–95)b (54–95) (80–90) (80–109)i (80–128)

2.1 (0.9–4.4) 2.1 (0.9–4.4) 3.0 (1.5–6.8) 3.4 3.4 5.9 7.3 8.9

(1.4–8.4) (1.4–8.4) (4.9–7.1) (4.9–12.8) (4.9–21.1)

a

Average of values from all salmon species for that month. Range of values from all salmon species for that month. A FL–WW regression for pink and chum salmon was used. d April pink salmon values were used. e Corresponding values from May were used. f April values were used. g A FL–WW regression for Chinook salmon was used. h Average of pink salmon values for May and July. i Average of Chinook salmon values for June and August. j Range of values from unidentified salmon for the same month. b c

levels of natural production, millions of salmon smolts are released into Puget Sound from hatcheries each spring and usually in concentrated pulses in May (HSRG 2002; Duffy et al. 2005). Salmon as a group represented over 50% of the fish prey consumed by cutthroat trout in April (NPS and SPS), May (SPS), and June (SPS; the two cohorts with the smallest FLs) and were consumed by all size-classes. Cutthroat trout are known to exploit seasonal overlaps with salmon at other times as well, preferentially feeding on juvenile chum salmon fry (March–April) and salmon eggs (October–January) when available in SPS inlets

(Jauquet 2002). Salmon contributed 26–49% of the spring energy budget of cutthroat trout in NPS and SPS and 11–30% of the early summer energy budget and are therefore important to the overall annual energy requirements for Puget Sound cutthroat trout. As a gape-limited predator, cutthroat trout only consumed salmon measuring less than 40% of their body length, a trend that is consistent among piscine predators of salmon (Brodeur 1990; Pearsons and Fritts 1999; Baldwin et al. 2000; Keeley and Grant 2001; Nowak et al. 2004). Because pink and chum salmon reach Puget Sound earlier and at a smaller size than

TABLE 6.—Estimated total predation (range) by 1,000 simulated cutthroat trout on salmon in northern and southern Puget Sound, Washington, during April–September, based on diet information collected in 2001–2003. Numbers of fish were estimated by dividing monthly consumption (Figure 6) by monthly average FL and wet weight (and range) of salmon in gut contents (Table 5). Biomass consumed (g)

Cohort

Cutthroat trout n

Unidentified salmon

Pink salmon

1 2 3 All cohorts

400 440 160 1,000

883 6,342 8,176 15,401

Northern Puget Sound 2,414 6,088 417 8,919

1 2 3 All cohorts

620 310 70 1,000

574 11,694 1,858 14,126

Southern Puget Sound 0 3,452 0 3,452

Chum salmon

Chinook salmon

Coho salmon

0 410 417 827

0 4,580 27,587 32,167

0 0 11,908 11,908

1,577 1,096 0 2,673

0 4,458 23,129 27,587

0 0 1,734 1,734


TABLE 5.—Extended.

Coho salmon Month May Jun Jul Apr May Jun Jul Apr May Jun Jul Aug

FL

WW

83 (73–92)b 83 (73–92) 62 (62)

All fish prey FL 30 52 50 31 41 43 62 35 46 61

5.2 (3.5–7.1) 5.2 (3.5–7.1) 2.1 (2.1)

(25–42) (27–67) (31–72) (21–37) (13–90) (7–89) (35–110) (13–98) (51–95) (62–135)

74 (55–128)

other species of salmon (Duffy et al. 2005), they were theoretically the most vulnerable to gape-limited predators. As expected, numerical consumption demand by a size-structured population of 1,000 cutthroat trout was highest for pink salmon populations in NPS and potentially highest for chum salmon populations in SPS (unidentified salmon were probably chum salmon based on their size and the negligible presence of pink salmon populations in SPS). The diet of the abundant cohort characterized by intermediate FLs and the highly abundant cohort of small fish contributed to most of this C, nearly all of which occurred during the spring (April–June), when pink and chum salmon were most abundant in nearshore areas (Duffy et al. 2005). During summer (July–August), predation by cutthroat trout on salmon was focused almost exclusively on Chinook salmon and most of the predation demand came from the least abundant cohort, which contained the largest individuals. Despite their relatively low

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abundance, the largest cutthroat trout were the most piscivorous and required greater consumption demand to satisfy their larger body masses. Therefore, the greatest biomass consumption demand for a population of 1,000 cutthroat trout was for Chinook salmon, the primary salmonid prey for the cohort with the largest FLs. The additional summer predation demand on Chinook salmon may be a consequence of their more variable timing of saltwater entry and more extensive nearshore residence time relative to other salmon species in Puget Sound (Congleton et al. 1982; Simenstad et al. 1982; Hodgson and Brakensiek 2003; Brennan et al. 2004; Toft et al. 2004; Duffy et al. 2005). While the absolute size of prey available to a predator is limited by gape width, capture success may also limit a predator’s choice of prey. In general, capture success increases as the ratio of predator size to prey size increases up to a point (Miller et al. 1988). Therefore, one would expect a predator to target individuals with the highest expected capture success—small individuals. This appears to be the case with cutthroat trout, which ate salmon that were smaller than their conspecifics available in the environment. This trend has been commonly observed in both piscivorous fish and crustaceans (Sogard 1997). Parker (1971) found that coho salmon preyed preferentially on the smaller available pink salmon and that juvenile coho salmon predation was responsible for most of the early marine mortality of pink salmon in a British Columbia inlet. The evidence for size-selective predation implies that larger individuals of a species will be less vulnerable to predators such as cutthroat trout and will experience higher early marine survival. Smolt size upon entry into Puget Sound and rapid early marine growth, therefore, are important for the survival of Puget Sound salmon stocks, as has been found

TABLE 6.—Extended.

Number consumed

Cohort

Unidentified salmon

1 2 3 All cohorts

1,174 39,198 2,136 42,508

(1,144–1,210) (14,877–50,158) (1,402–11,813) (17,423–63,181)

1 2 3 All cohorts

521 47,028 558 48,107

(478–574) (16,485–55,252) (221–7,094) (17,184–62,919)

Pink salmon

8,047 24,046 2,085 34,178

Northern (4,024–12,071) (9,739–60,883) (1,390–4,170) (15,153–77,123)

Southern 0 8,556 (3,111–22,820) 0 8,556 (3,111–22,820)

Chum salmon

Chinook salmon

Coho salmon

Puget Sound 0 2,049 (1,366–2,049) 3,438 (2,200–4,133) 5,487 (3,566–6,182)

0 2,181 (1,041–5,089) 6,392 (3,574–11,806) 8,573 (4,615–16,895)

0 0 2,467 (1,887–3,521) 2,467 (1,887–3,521)

Puget Sound 5,258 (2,253–15,774) 3,145 (1,925–3,335) 0 8,403 (4,178–19,110)

0 1,837 (853–4,064) 4,567 (2,425–8,864) 6,404 (3,278–12,928)

0 0 334 (244–496) 334 (244–496)

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elsewhere (Parker 1971; Healey 1982; Ward et al. 1989; Henderson and Cass 1991). In turn, favorable foraging conditions are important, as they result in good early marine growth and increase the chances for salmon to achieve a size associated with lower predation risk (Sogard 1997). Though little is known about present population abundance of cutthroat trout in Puget Sound, reasonable estimates based on our catch densities suggest that populations could number in the thousands in localized areas to tens of thousands in regional basins. These estimates are probably conservative, since they assume an unrealistic 100% capture efficiency for beach seine sets. Approximately 3.8 million hatchery Chinook salmon are produced in the Whidbey Basin, 7.6 million are produced in the Main Basin, and 10.7 million are produced in the Southern Basin of Puget Sound (HSRG 2002); between 44% (NPS) and 98% (SPS) of Chinook salmon using nearshore areas of Puget Sound were of hatchery origin (Duffy et al. 2005). Applying hatchery : wild ratios (and using an average of Whidbey and Southern Basin values for the Main Basin populations) to estimate basinwide Chinook salmon production, we estimate that approximately 8.6 million Chinook salmon were produced in the Whidbey Basin, 10.7 million were produced in the Main Basin, and 10.9 million were produced in the Southern Basin. However, the number of Chinook salmon actually reaching Puget Sound would be lower due to variable and often substantial freshwater mortality. Calculations of regional predation impact based on these order-ofmagnitude-level estimates suggest that predation by cutthroat trout imposes roughly 1% mortality on age-0 Chinook salmon and considerably lower mortality on other species. Predation mortality could presumably be somewhat higher for certain weak stocks in localized areas of Puget Sound during discrete periods. Wild Chinook salmon may be disproportionately affected, since they tend to be smaller than hatchery fish during nearshore residence (Duffy et al. 2005) and since cutthroat trout tended to consume the smaller available individuals. In addition, wild Chinook salmon exhibit more variability in out-migration timing; they enter Puget Sound during March–July, whereas hatchery Chinook salmon tend to occupy nearshore areas in concentrated pulses during May and June (Duffy et al. 2005). These patterns could make wild Chinook salmon particularly vulnerable to predation during both early spring and mid- to late-summer months. It is widely known that piscivory tends to be highest during crepuscular hours (Howick and O’Brien 1983; Beauchamp 1990; Beauchamp et al. 1992), when predators and prey commonly rely on visual contrast (Breck 1993). To measure the extent of juvenile

salmon predation by piscivores in Puget Sound, more intensive sampling is needed during crepuscular and night periods between March and July (known peak out-migration times). Sampling should be conducted in both even years (juvenile pink salmon out-migration) and odd years (adult pink salmon return) to determine whether predation rates are similar in the presence (even years) and absence (odd years) of possibly millions of juvenile pink salmon. In addition, greater spatial coverage both in nearshore and offshore waters will be needed to determine the extent to which our findings are representative of other areas in Puget Sound. Seasonal diet information and comparable data for the Skagit Bay region would be particularly useful, because a large fraction of the wild Chinook salmon production for Puget Sound comes from the Skagit River. Nearshore studies conducted concurrently with this project reported both similar catch rates and sizes of cutthroat trout both in the Main Basin (Brennan et al. 2004; Fresh et al. 2006) and in SPS inlets (Jauquet 2002) during 2001–2002. Since 2001, only one cutthroat trout has been caught during biannual (July and September) midwater trawling in the Main Basin (R. Beamish, Canada Department of Fisheries and Oceans, unpublished data) and similar yields were found with purse seine (2003) and tow net (2002) sets in the Whidbey Basin (E.J.D., unpublished data). Further work could be conducted to quantify cutthroat trout populations and establish the extent of their predation on juvenile salmon, but it appears that predation by cutthroat trout accounts for a relatively minor amount of the early marine mortality experienced by Chinook salmon in Puget Sound. Some exceptions could exist for weak stocks in highly localized and discrete periods. Conversely, juvenile salmon represent a seasonally important prey resource and are important to the overall annual energy requirements for Puget Sound populations of cutthroat trout. Acknowledgments This research was made possible by funding from the Hatchery Scientific Review Group, University of Washington Mason Keeler fellowship, Washington Department of Fish and Wildlife (WDFW), Washington Sea Grant, and Washington Cooperative Fish and Wildlife Research Unit. Thanks to Ray Buckley (WDFW), Mindy Rowse (NOAA, Fisheries), and the many hard workers of the Beauchamp laboratory, including Nathanael Overman, Chris Sergeant, Angie Lind-Null, and Steve Damm, for their tireless efforts during long hours in the field and laboratory. Tom Quinn and Reg Reisenbichler provided valuable critical reviews of this manuscript. The Washington Cooper-


ative Fish and Wildlife Research Unit is jointly sponsored by the U.S. Geological Survey; University of Washington; Washington State Departments of Ecology, Fish and Wildlife, and Natural Resources; Washington State University; U.S. Fish and Wildlife Service; and Wildlife Management Institute. Reference to trade names does not imply endorsement by the U.S. Government. References Baldwin, C. M., D. A. Beauchamp, and J. J. Van Tassell. 2000. Bioenergetic assessment of temporal food supply and consumption demand by salmonids in the Strawberry Reservoir food web. Transactions of the American Fisheries Society 129:429–450. Beamish, R. J., and C. Mahnken. 1998. Natural regulation of the abundance of coho and other species of Pacific salmon according to a critical size and critical period hypothesis. North Pacific Anadromous Fish Commission, Document 319, Vancouver. Beamish, R. J., C. Mahnken, and C. M. Neville. 2004. Evidence that reduced early marine growth is associated with lower marine survival of coho salmon. Transactions of the American Fisheries Society 133:26–33. Beamish, R. J., B. L. Thomson, and G. A. McFarlane. 1992. Spiny dogfish predation on Chinook and coho salmon and the potential effects on hatchery-produced salmon. Transactions of the American Fisheries Society 121:444– 455. Beauchamp, D. A. 1990. Diel and seasonal food habits of rainbow trout stocked as juveniles in Lake Washington. Transactions of the American Fisheries Society 119:475– 482. Beauchamp, D. A., M. G. LaRiviere, and G. L. Thomas. 1995. An evaluation of competition and predation as limits to juvenile kokanee and sockeye salmon production in Lake Ozette, Washington. North American Journal of Fisheries Management 15:193–207. Beauchamp, D. A., S. A. Vecht, and G. L. Thomas. 1992. Seasonal, diel, and size-related food habits of cutthroat trout in Lake Washington. Northwest Science 66:149– 159. Breck, J. E. 1993. Foraging theory and piscivorous fish: are forage fish just big zooplankton? Transactions of the American Fisheries Society 122:902–911. Brennan, J. S., K. F. Higgins, J. R. Cordell, and V. A. Stamatiou. 2004. Juvenile salmon composition, timing, distribution, and diet in marine nearshore waters of central Puget Sound in 2001–2002. King County Department of Natural Resources and Parks, Seattle. Brodeur, R. D. 1990. Feeding ecology of and food consumption by juvenile salmon in coastal waters, with implications for early ocean survival. Doctoral dissertation. University of Washington, Seattle. Brodeur, R. D., K. W. Myers, and J. H. Helle. 2003. Research conducted by the United States on the early ocean life history of Pacific salmon. North Pacific Anadromous Fish Commission Bulletin 3:89–131. Burns, R. 1985. The shape and form of Puget Sound. Washington Sea Grant Program, University of Washington Press, Seattle.

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