Ecology of Freshwater 2014 Ó 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd ECOLOGY OF FRESHWATER FISH

Predation on native sculpin by exotic brown trout exceeds that by native cutthroat trout within a mountain watershed (Logan, UT, USA)

Christy S. Meredith1,2*, Phaedra Budy1,2,3, Gary P. Thiede1 1Department of Watershed Sciences, Utah State University, Logan, UT 84322, USA 2Ecology Center, Utah State University, Logan, UT 84322, USA 3U. S. Geological Survey, Utah Cooperative Fish and Wildlife Research Unit, Utah State University, Logan, UT 84322, USA

Accepted for publication March 7, 2014

Abstract – We explored potential negative effects of exotic brown trout (Salmo trutta) on native sculpin ( sp.) on the Logan River, Utah, USA by (i) examining factors most strongly correlated with sculpin abundance (e.g., abiotic conditions or piscivory?), (ii) contrasting the extent of brown trout predation on sculpin with that by native cutthroat trout (Oncorhynchus clarkii utah) and (iii) estimating the number of sculpin consumed by brown trout along an elevational gradient using bioenergetics. Abundance of sculpin across reaches showed a strong (r ≥ 0.40) and significant (P < 0.05) correlation with physical variables describing width (positive) and gradient (negative), but not with abundance of piscivorous brown trout or cutthroat trout. In mainstem reaches containing sculpin, we found fish in 0% of age-1, 10% of age-2 and 33% of age-3 and older brown trout diets. Approximately 81% of fish consumed by brown trout were sculpin. Despite a similar length–gape relationship for native cutthroat trout, we found only two fish (one sculpin and one unknown) in the diets of native cutthroat trout similar in size to age-3 brown trout. Based on bioenergetics, we estimate that an average large (> 260 mm) brown trout consumes as many as 34 sculpin per year. Nevertheless, results suggest that sculpin abundance in this system is controlled by abiotic factors and not brown trout predation. Additional research is needed to better understand how piscivory influences brown trout invasion success, including in-stream experiments exploring trophic dynamics and interactions between brown trout and native prey under different environmental conditions.

Key words: brown trout; sculpin; predation; piscivory; bioenergetics

Brown trout (Salmo trutta), one of the world’s Introduction most successful invasive species, exhibits relatively Success of an invasive species depends on both traits high plasticity in diet, including the potential to shift of the invasive species and characteristics of the to piscivory when prey fish are present (McIntosh invading environment (Kolar & Lodge 2001). The et al. 2011). Based on optimal foraging theory, fish ability to occupy a broader niche space than native should shift their diets to eat more fish when higher species is a common trait held by many successful densities of fish prey are available (Pyke 1984). As a invaders (Vazquez et al. 2006). Species that have result, most trout species are opportunistic feeders, broad feeding niches can establish high densities and and many become piscivorous at large sizes (Mittel- biomass by consuming either a wide range of prey or bach & Persson 1998; Keeley & Grant 2001). How- more energetically beneficial prey sources, thus out- ever, within their introduced range, brown trout may competing comparable native species characterised consume more fish than their native counterparts of a by a narrower feeding niche (Simon & Townsend similar size (McHugh et al. 2008; Sepulveda et al. 2003) and altering the population dynamics of native 2009). The highly piscivorous nature of brown trout prey communities (Sakai et al. 2001). in their introduced range appears to contrast with that

Correspondence: C. Meredith, Department of Watershed Sciences, Utah State University, Logan, UT 84322, USA. E-mail: [email protected] * Current address: US Forest Service, Rocky Mountain Research Station, 860 North 1200 East, Logan, Utah 84321, USA. doi: 10.1111/eff.12134 1 Meredith et al. of the species native range, where even larger indi- restricted to headwaters located upstream from waterfalls viduals often feed primarily on drifting invertebrates where they can avoid predation by brown trout (Montori et al. 2006; Budy et al. 2013). The mecha- (Townsend & Crowl 1991). Similarly, in streams in nisms contributing to this lack of diet shift are largely Virginia, densities of native fish are negatively corre- unexplored but may be related to the absence of lated with the presence of brown trout (Garman & avoidance mechanisms by potential prey in brown Nielsen 1982). Further, the impacts of brown trout trout’s exotic versus native range (Townsend 1996) predation may cascade through entire stream ecosys- or low densities or absence of prey fish in their native tems. The presence of exotic brown trout resulted in range versus introduced range (Arismendi et al. the reduction in algae-eating macro-invertebrates and 2012). higher algal biomass within some New Zealand Fish represent a higher-energy prey resource com- streams (Townsend 1996). Despite the potential nega- pared with invertebrates, typically resulting in faster tive effects of brown trout predation on individual growth and condition for brown trout that show some species, communities and ecosystems, studies actu- degree of piscivory. Elliott and Hurley (2000) dem- ally documenting high rates of brown trout predation onstrated that a change in diet from fish to inverte- on native in river systems are relatively rare. brates not only increases energy intake, but also We examined brown trout predation on native scul- increases the efficiency of energy conversion into pin (Cottus sp.) in the Logan River. This study is part growth by approximately 25%. The optimal tempera- of a long-term research project aimed at both moni- ture for trout feeding on fish may also be higher than toring populations of a critical population of native when feeding on invertebrates, resulting in an even Bonneville cutthroat trout as well as documenting greater potential for growth (Elliott & Hurley 2000). impacts of brown trout to the native fish community In addition to increased growth and condition, pisciv- in the Logan River, Utah. Previous research suggests orous trout often attain sexual maturity earlier than that brown trout in the Logan River consume more their nonpiscivorous counterparts (Jonsson et al. fish than native Bonneville cutthroat trout of a similar 1984). The presence of small prey fish may result in size (de la Hoz Franco & Budy 2005; McHugh et al. brown trout becoming piscivorous at an early age, 2008), which may contribute to the species’ competi- because they are less restricted by gape limitations tive advantage over cutthroat trout. (Keeley & Grant 2001). Therefore, an abundance of As part of this research, we investigated (i) which fish prey can lead to increased growth, reproduction factors are most strongly correlated with patterns of and bio-efficiency for brown trout (Budy et al. sculpin abundance (e.g., abiotic conditions or the 2013). abundance of piscivorous trout?), (ii) the contribution Because brown trout are typically superior compet- of sculpin to the diet of different age classes of itors, all else equal, any size advantage gained via brown trout compared with that of native cutthroat piscivory should add to their competitive advantage trout and (iii) the potential number of sculpin con- over other trout species. For example, in a Michigan sumed by brown trout along an elevational gradient, stream, native brook trout (Salvelinus fontanalis) using bioenergetics. chose locations with more favourable water velocities and canopy cover after the removal of brown trout Materials and methods (Fausch & White 1981). Similarly, in experimental enclosures, Rio Grande cutthroat trout (Oncorhyn- Study area chus clarkii virginialis) individuals shifted their feed- ing niches to consume less-energetic prey in the The Logan River is located in southeast and presence of brown trout (Shemai et al. 2007). On the northern Utah. The headwaters originate in the Bear Logan River, Utah, USA, the condition and growth River range in Idaho, and the river drains into the of native Bonneville cutthroat trout (O. c. utah) Bear River and then into the Great Salt Lake in Utah. decreased in experimental enclosures with brown The hydrograph is characterised by spring runoff trout, while, conversely, brown trout performance snowmelt events and a relatively low ratio of peak was unaffected (McHugh & Budy 2005). In these flow to autumn baseflow, due to abundant karst fea- examples, trout displaced by exotic brown trout were tures in the watershed. Discharge data collected native species of conservation concern. hourly at study sites demonstrate that average dis- As a predator, brown trout may also have wide- charge in the mainstem river ranges from spread impacts on native communities. Brown trout 2.16 m3ÁsÀ1 at Franklin Basin to 4.76 m3ÁsÀ1 near predation has been attributed to the decline of native the Logan River USGS gauge located at the very fish in New Zealand and Patagonia (McIntosh 2000; downstream portion of the study area. Average Macchi et al. 2007). In some New Zealand streams, tributary discharge ranges from 0.11 m3ÁsÀ1 for the native galaxiid fish (Galaxias vulgaris)arenow tributary of Spawn Creek to 0.80 m3ÁsÀ1 for Temple

2 Trout predation on sculpin

Fork Creek above the confluence with the Logan Long-term mainstem reaches (listed in order of River. In general, the gradients at mainstem reaches increasing elevation) included Lower Logan, Third (0.005–0.026) are considerably lower than at tribu- Dam, Twin Bridges, Forestry Camp, Red Banks and tary reaches (0.015–0.053) (Table 1). The Logan Franklin Basin. We also sampled the tributary River is relatively pristine within the study area, with reaches of Right Hand Fork, Temple 1 and Spawn the exception of highly localised effects of grazing- Creek (de la Hoz Franco & Budy 2005). Supplemen- related habitat degradation in some headwater tary reaches included the mainstem reaches of Brid- reaches, the presence of three dams and associated ger, Wood Camp and the tributary reaches of Temple habitat alteration near the city of Logan (Fig. 1, 2 and Beaver Creek. Lower Logan site), and a canyon road adjacent to the We collected trout abundance data each year river. (2001–2013) in July or early August, during near- In addition to native Bonneville cutthroat trout, baseflow conditions, at both long-term and supple- exotic brown trout and sculpin, the river also con- mental sampling reaches. We performed all sampling tains native mountain whitefish (Prosopium william- using a backpack (tributaries) or canoe-mounted soni), and small numbers of exotic brook trout (main river) electrofishing unit. We marked captured and stocked rainbow trout (O. mykiss) in isolated brown trout and cutthroat trout > 150 mm at each sections. Exotic brown trout were first introduced to reach during each survey, using individually coded, the study area in the early 1900s. Invertebrate densi- T-bar anchor tags with site-specific colours. We also ties range from 2500 to 6000 individualsÁmÀ2 (de la measured lengths and weights of each trout cap- Hoz Franco & Budy 2005). A more detailed descrip- tured. During collection, we placed a block net at tion of the study area, including information describ- the upstream and downstream ends of each reach. ing the fish community, is available in Budy et al. We estimated brown trout and cutthroat trout popu- (2008). lation abundance for each year using a three-pass, closed, generalised maximum-likelihood removal estimator (Peterson et al. 2004). We determined mean Brown trout and sculpin co-occurrence brown trout and cutthroat trout abundance for each We have collected brown trout and cutthroat trout reach (approximately 100 m: tributaries; approxi- abundance data at twelve reaches in the Logan River mately 200 m: mainstem) by averaging abundance watershed as part of a long-term study since 2001 data across years in which we also collected sculpin (Budy et al. 2008). Our study reaches encompassed abundance data (2008–2013) and average densities more than 50 stream km of the Logan River and by dividing average abundance by the area of the ranged from 1352 to 2023 m in elevation (Fig. 1). reach. Each study reach was approximately twenty channel Sculpin, the only nonsalmonid prey currently in widths in length. Study reaches included eight this system, commonly co-occurs with brown trout long-term reaches, sampled annually, as well as four throughout the Western USA (Bailey 1952; Quist supplementary reaches sampled in a subset of years. et al. 2004b). While the redside shiner, Richardso-

Table 1. Average reach characteristics, estimated from summer long-term and supplemental sampling events.

Mean

Mean watershed Mean Gradient Mean D50 cond-uctivity Mean average Mean summer Mean winter area (km2) width (m) (mÁmÀ1) (mm) (lSÁcmÀ3) temperature (°C) temperature (°C) temperature (°C)

Low elevation Lower Logan 559 12.1 0.005 42 482 8.4 14.4 3.8 Bridger 547 10.2 0.006 80 338 5.6 11.2 3.1 Third Dam 546 10.4 0.010 105 338 5.6 11.2 3.1 Mid elevation Twin Bridges 361 12.0 0.009 136 350 5.7 11.0 2.2 High elevation Forestry Camp 276 12.8 0.016 156 322 5.5 10.9 1.6 Red Banks 227 12.0 0.018 111 323 5.2 9.8 1.6 Franklin Basin 85 9.6 0.026 130 293 4.7 9.2 2.0 Tributaries Beaver Creek 108 6.9 0.015 40 293 5.0 9.5 2.0 Right Hand Fk 64 3.9 0.027 28 393 9.7 11.0 8.8 Temple 1 41 4.5 0.026 62 338 5.9 10.4 2.8 Temple 2 25 4.0 0.030 52 319 5.2 9.0 2.4 Spawn Creek 15 1.8 0.053 42 346 6.3 10.4 3.4

3 Meredith et al.

Fig. 1. Study reaches on the Logan River, Utah. nius balteatus, previously occupied this system, the 50% (2008 and 2009) and up to 700% (2011) species is no longer present. Mottled sculpin (Cottus greater than average baseflow during the sampling bairdi) has been previously reported to occupy the period (July, August), based on a Geo- length of the Logan River from Third Dam to Beaver logical Survey Gaging station (10109000) located Creek (Fig. 1). Paiute sculpin (Cottus beldingi), near Third Dam. Therefore, we estimated average which is similar in physical appearance, may also be sculpin density at each reach using only years where present (Zarbock 1952). Both species are almost we obtained a three-pass depletion. entirely benthic and occur throughout much of the Western USA, but they show some differences in Abiotic habitat characteristics potentially affecting co- environmental preferences (Quist et al. 2004a). For occurrence the purposes of this research, we did not differentiate between species of sculpin. To evaluate factors influencing sculpin abundance, We collected sculpin at long-term and the major- we explored relationships between sculpin abun- ity of supplementary reaches (excluding Wood dance, the abundance of piscivorous brown trout and Camp) during summer surveys during the years cutthroat trout, and abiotic factors. We selected abi- 2008–2013. We performed surveys only at sites otic habitat variables a priori based on previous where sculpin were known to be present based on research highlighting their importance in determining trout surveys conducted in years prior to 2008. For distributions of sculpin (Maret 1997; Quist et al. reaches in which sculpin were not previously 2004b). The abiotic habitat variables evaluated collected, we considered abundance of sculpin to be included wetted width, gradient, D50 (e.g., median 0. We recorded lengths and weights of the first 100 substrate size), conductivity, average temperature, sculpin collected at each reach. We estimated scul- summer temperature and winter temperature pin abundance for each reach and year similar to (Table 1). We estimated wetted width at ten equally above using a three-pass removal estimator. For spaced transects, averaged to obtain an estimate for many of the reaches, we were not able to obtain a the reach. We calculated gradient by dividing the three-pass depletion for the years 2008, 2009 and change in water surface elevation, estimated using an 2011. We attribute this largely to low visibility auto-level, by the length of the reach. We estimated caused by high discharge that was approximately median substrate size from pebble counts conducted

4 Trout predation on sculpin at these equally spaced transects, using a gravelome- Ebner et al. (2007). For cutthroat trout, we used a ter to measure substrate size of ten randomly selected size–gape relationship previously published for particles at each transect. We measured conductivity coastal cutthroat trout (Reimchen 1991). We used and obtained an estimate of wetted width, gradient estimated average sizes of each age class of brown and median substrate size for each reach by averag- trout and cutthroat trout near the time period when ing across years in which we collected habitat data we collected most diet data (August). Estimates were (2008–2011). We based temperature estimates on based on a combination of mark–recapture, length– hourly data collected using data loggers deployed at frequency and scale data. For brown trout, the lengths each site in 2010 and averaged across the time period of age-1 individuals were 100–179 mm, age-2 were of interest; however, the longitudinal thermal pattern age-2 were 180–260 mm, and age-3 and older were is similar across years (de la Hoz Franco & Budy > 260 mm. For cutthroat trout, age-1 individuals 2005; Wood and Budy 2009). Estimated temperature were 100–149 mm, age-2 were 150–249 mm and variables included annual temperature (1 Jan–31 age-3 and older were 250 mm and longer. December), summer temperature (1 July–31 August) In our calculations, we assumed that head width and winter temperature (1 January–28 February and 1 was the limiting factor influencing whether a sculpin November–31 December). For our measure of the could be consumed and estimated head width based density of piscivorous brown trout and cutthroat on a published sculpin length-head width relationship trout, we multiplied the average density of brown for mottled sculpin (Maughan 1978). The resulting trout across years estimated via three-pass depletion formula for maximum total length of sculpin that a by the average proportion of fish > 180 mm (the size brown trout was able to consume in relation to brown above which we observed piscivory). We scaled our trout size was: estimate to a typical reach (2000 m2). We used Pear- Maximum Length Consumed = 0.62 * Brown son correlation coefficients, estimated using Program Trout Total Length (mm) À38.43 R (R Core Development Team 2011), to evaluate the The formula for maximum length of sculpin that a magnitude and significance (P < 0.05) of correlations cutthroat trout could consume was: between sculpin densities, abiotic habitat characteris- Maximum Length Consumed = 0.42 * Cutthroat tics and the densities of piscivorous brown trout and Trout Total Length (mm) À5.27 cutthroat trout. Because sedimentation and altered hydrology near the City of Logan are potentially Consumption of sculpin by brown trout responsible for the near-absence of sculpin at this site, we excluded it from our correlation analysis. We We merged diet data collected during multiple sam- initially noted that sculpin are absent from high-gra- pling events to evaluate rates of piscivory at study dient tributaries, potentially due to the presence of reaches (Bridger, Third Dam, Wood Camp, Twin high gradients; therefore, we performed the correla- Bridges, Red Banks, Franklin Basin, Right Hand tion analysis both across all sites and also excluding Fork, and Temple 1). Diet samples were collected as high-gradient tributaries (> 0.020) to explore poten- part of other research (de la Hoz Franco & Budy tial controlling factors not related to gradient. We 2005; McHugh et al. 2008) and/or were a component present abiotic habitat data for all reaches, excluding of annual surveys occurring from July to November, Wood Camp, at which only diet data was collected. during the years 2001–2009. Because data were col- lected during multiple research projects, the sampling methodology used was not consistent (use of gastric Gape limitation lavage or dissection and number of fish in each size- We compared sculpin sizes collected during electro- class sampled). However, during each sampling event fishing surveys to sculpin sizes in brown trout diets. at a reach, a subset of trout (target of N ≥ 10 per We did not compare sculpin sizes collected to those reach) were collected that were representative of the in cutthroat trout diets, because too few cutthroat sizes of fish present in the reach, including large trout trout (N = 2) had sculpin in diets. We estimated > 260 mm. The exception was at the Wood Camp length–frequency distributions for sculpin from reach, where samplers specifically targeted large cumulative length data collected across 2008–2011 at (> 260 mm) brown trout and no other size class. sample reaches where the majority of diet data were Invertebrates were identified to order, fish to species, also collected (Bridger, Third Dam and Twin and all fish parts in the stomach contents were Bridges). weighed (wet weight, g) and measured (mm). We We determined the range of sculpin lengths that considered a fish to be piscivorous if fish or fish parts could be consumed by brown trout and cutthroat were positively identified in the diet contents. We trout of different ages. We based our estimates of compared differences in rates of piscivory using sizes brown trout gape limitations on relationships in indicative of brown trout age classes (age-1: < 180;

5 Meredith et al. age-2: 180–260 mm; age-3 and older: > 260 mm). measured for each age class during mark–recapture We determined the per cent of piscivorous brown surveys (Budy et al. 2008). We used the proportion trout and cutthroat trout for each size-class group of sculpin in diets collected over the 2001–2009 time within each reach, and grouped all data together to period. While we recognise that the years with diet determine the average for mainstem and tributary data do not overlap entirely with the years of fish sur- reaches. Due to the unusual sampling strategy and veys (2008–2013), we assumed that diet preferences the lack of sampling for cutthroat trout at Wood of brown trout did not change significantly during Camp, this reach was excluded from the calculation the years 2001–2013. Further, although seasonal vari- of average piscivory at mainstem reaches. ation in diet certainly occurs, preliminary simulations We also estimated the average per cent wet weight indicated that the majority of growth (approximately of each major organic diet item (excluding rocks) in 70%) for brown trout on the Logan River occurs dur- the stomach contents of cutthroat trout and brown ing July–September during the time period when diet trout both 180 – 260 mm and > 260 mm in length. data were collected. Based on inputs of thermal Major diet classes included the following: aquatic, regime, diets and brown trout growth as described terrestrial, vegetation, brown trout, unknown fish and above, we used the bioenergetics model to estimate sculpin. The class ‘aquatic’ included nonfish organ- the potential mass of sculpin consumed annually by isms that were in a life-history form requiring water, an average brown trout in each reach. To determine including larvae of macro-invertebrate orders the number of sculpin consumed per individual, we Ephemeroptera, Plecoptera, Diptera, Coleoptera, divided the weight consumed by the weight of Hemiptera, Isopoda, Odonata, Tricoptera, as well as the median size of sculpin found in diets the phylum Annelida. The class ‘terrestrial’ included (75 mm = 6.5 g). We used the number of fish in both nonterrestrial adults of these macro-invertebrate each size class in each reach to estimate total con- orders and organisms that are typically found on sumption by reach. Finally, to estimate per cent of water margins, such as aquatic Hemiptera, grasshop- sculpin in each reach consumed, we divided reach- pers and mice. The class ‘vegetation’ included any level consumption by the upper estimate (using herbaceous or woody material found in the diet. The standard deviation – SD) of abundance in each remaining fish portions of the diet were separated reach. into ‘brown trout’, ‘unknown, fish’ and ‘sculpin’.No cutthroat trout were found in diets. We excluded Results unidentified organic matter from our calculations. Because too few trout were captured at the Red Trout and sculpin co-occurrence Banks and Forestry Camp reaches, which are approx- imately 2.5 km apart, we combined these reaches for We found that sculpin were present primarily in our diet analysis. mainstem reaches. Most tributary reaches contained either no sculpin or very low densities of sculpin, with the exception of Beaver Creek (Fig. 2). Based Potential for individual and population-level on sites and years where we obtained a three-pass consumption on sculpin depletion estimate, sculpin densities ranged from We used the Wisconsin bioenergetics model (Hanson 0.002 fishÁmÀ2 (Temple 1) to 0.20 fishÁmÀ2 (Third et al. 1997) to estimate the potential annual consump- Dam). The average density across sites containing tion of sculpin by individual brown trout and at the sculpin was 0.08 (Æ 0.08 SD). Brown trout and cut- population (reach) level. For this analysis, we esti- throat trout co-occur with sculpin throughout much mated consumption in an example reach at low of the study area (Fig. 2). Similar to other research (Third Dam), mid (Twin Bridges) and high (Red (e. g. de la Hoz Franco & Budy 2005), we found that Banks/Forestry Camp) elevations. We based physio- brown trout are generally more abundant in low-ele- logical parameters on laboratory-derived data for vation mainstem reaches and tributaries downstream brown trout (Dieterman et al. 2004). For all model of the confluence with Temple Fork, whereas cut- runs, we modelled the average thermal history at a throat trout are more abundant in high-elevation daily timestep from 10 August 2009 to 9 August reaches upstream of the confluence. 2010. We chose the 10 August date because it approximates the date of the annual surveys each Factors affecting sculpin distributions year, during which brown trout abundance data are collected. We estimated average daily temperatures We observed significant correlations between sculpin from hourly data collected using temperature loggers densities and variables describing physical habitat deployed at each reach. We estimated growth rates of across our reaches (Fig. 3). Sculpin density was sig- brown trout (gÁdayÀ1) from average weights (g) nificantly positively correlated (+) with wetted width

6 Trout predation on sculpin

(a)

(b)

Fig. 2. (a) Average brown trout and cutthroat densities (Æ 1 SD) and (b) average sculpin densities across years (Æ 1 SD) at study reaches on the Logan River, Utah. An ‘NA’ indicates that no sampling for that species was conducted in the reach. and significantly negatively correlated (À) with sizes were collected in river surveys. Based on their gradient (P < 0.05, N = 11). We also documented gape size, we estimate that both brown trout and cut- that sculpin were generally absent from reaches with throat trout are physically capable of consuming the substrate smaller than cobble sized (< 64 mm). We majority of sculpin sizes present by age-2. did not observe significant correlations between our sculpin density estimates, other temperature variables, Piscivory by brown trout versus cutthroat trout conductivity and densities of piscivorous brown trout or cutthroat trout. However, when we removed high- Brown trout piscivory was widespread across main- gradient tributary reaches (< 0.020) not containing stem reaches (Fig. 5a). No age-1 brown trout con- sculpin from the analysis (N = 7), sculpin densities sumed fish in mainstem or tributary reaches. We were strongly correlated (> 0.40) with gradient (À), documented piscivory by age-2 and age-3 and older D50 (À), winter temperature (+), summer temperature brown trout. We documented piscivorous age-2 (+), piscivorous brown trout abundance (+) and brown trout in each of the mainstem reaches where piscivorous cutthroat trout abundance (À). Given the brown trout occurred (Third Dam, Wood Camp, low sample size, additional sampling would be Twin Bridges and Red Banks/Forestry Camp). needed to fully test these relationships. Across these mainstem reaches, 10% of age-2 brown trout had fish in their stomach contents and 33% of age-3 and older brown trout had fish in their stomach Gape limitations of brown trout and cutthroat trout contents. Consumption of fish prey by brown trout Brown trout consumed sizes of sculpin similar to was less in tributary reaches with no (Right Hand what was available in the environment (Fig. 4). We Fork) or low (Temple 1) sculpin. At Temple 1, we observed no significant difference between the distri- found fish in the stomachs of 0% of age-2 brown bution of sculpin consumed and sculpin present in trout, and 2% (one fish consumed) of age-3 and older the environment based on a Kolmogorov–Smirnov brown trout. At Right Hand Fork, we found fish test (P = 0.3). However, we did not find sculpin (brown trout) in 0% of the stomachs of age-2 brown greater than 100 mm in brown trout diets, even trout and 5% of the stomachs of age-3 brown trout. though these sizes of sculpin were found at sites with Sample sizes of age-2 and age-3 brown trout used in large brown trout (Fig. 4). In addition, we docu- all diet analysis at each reach are provided in Fig. 5a. mented that a large number of sculpin < 50 mm were Sample sizes of age-1 brown trout (0% piscivory) found in diets, even though few fish of these small included in the analysis were the following: Third

7 Meredith et al.

(a) (b) (c)

(d) (e) (f)

(g) (h) (i)

Fig. 3. Average sculpin densities in relation to average brown trout densities, cutthroat trout densities and abiotic variables at each reach. Sculpin densities were averaged across years where we obtained a three-pass depletion. In the upper right corner, r = c1/c2, ‘c1’ refers to the correlation coefficient across all sites excluding Lower Logan (the outlier) and ‘c2’ refers to the correlation coefficient when high-gradi- ent tributaries (Right Hand Fork, Temple 1, Temple 2, Spawn Creek) are excluded. An asterisk (*) indicates significance at P < 0.05.

Dam: 38; Wood camp: 0; Twin Bridges: 27; Red trout, brown trout cannibalised other brown trout. Banks/Forestry Camp: 2; Franklin Basin: 0; Right Brown trout were found in 10% of the stomach con- Hand Fork: 31; Temple 1: 16. tents of > 260 mm brown trout at Right Hand Fork. Approximately 81% of the fish consumed by The average per cent of fish in of the stomach con- brown trout across reaches were sculpin (Fig. 6a,b). tents of piscivorous brown trout across all reaches Sculpin comprised 18%, 9% and 0% of the diets of was 69% (Æ 1SD= 31). age-2 fish at Third Dam, Twin Bridges and Temple Cutthroat trout exhibited much lower rates of pisci- 1, respectively. Sculpin comprised 7% of the diets of vory than did brown trout (Fig. 5b, sample sizes rep- age-3 and older fish at Third Dam, 27% of the diets resented by italics). Within mainstem reaches, no of age-3 and older fish at Twin Bridges, and < 1% of < 180 mm or 180–260 mm cutthroat trout consumed the diets of age-3 and older fish at Temple 1. At Red fish and only two cutthroat trout > 260 mm consumed Banks, fish comprised 37% of the diet of age-3 and fish. Fish consumed by cutthroat trout consisted of older fish; however, we categorised these as one sculpin and one unknown fish consumed at the ‘unknown’ because they could not be identified. At Twin Bridges reach (Fig. 6a,b). We also did not docu- Right Hand Fork, which has no sculpin or cutthroat ment any piscivory by cutthroat trout in Temple 1, the

8 Trout predation on sculpin

Fig. 4. Length–frequency histograms of sculpin captured across reaches (2008–2013) compared with those found in diets of brown trout on the Logan River (2001–2011) and the predicted size of sculpin that could be consumed by brown trout and cutthroat trout in each size class during the average time period of diet surveys (August). only tributary reach where diet data were available for Banks/Forestry Camp) due to low densities of brown cutthroat trout. As previously described, < 180 mm, trout in these reaches. In contrast, reach-level con- 180–260 mm and > 260 mm cutthroat trout are sumption estimates at the Twin Bridges reach equivalent in size to age-1, age-2, and age-3 and older exceeded the estimated number of sculpin present in brown trout, respectively. Sample sizes of age-1 cut- the reach. throat trout (0% piscivory) were the following: Third Dam: 8; Wood Camp: 0; Twin Bridges: 15; Red Discussion Banks/Forestry Camp: 12; Franklin Basin: 38; Right Hand Fork: 0; Temple 1: 13. We illustrated how exotic brown trout can become piscivorous in the presence of high densities of native fish prey, which may contribute to brown trout Potential for individual and population-level invasion success worldwide. In portions of the Logan consumption of sculpin River watershed where exotic brown trout and native According to our bioenergetics simulations, brown sculpin co-occurred, sculpin comprised a significant trout potentially consume a large number of sculpin portion of the diet, and thus the energy budget of each year (Table 2). A typical age-2 brown trout brown trout. In places where sculpin densities were may consume up to 9 sculpin per year, while a typi- low, brown trout generally did not consume other sal- cal age-3 and older brown trout may consume up to monids (e.g., except Right Hand Fork, where they 34 sculpin per year. This consumption varied spa- cannibalised small brown trout). Rates of piscivory tially. We estimated the highest level of consump- by brown trout far exceeded those by native cutthroat tion at the mid-elevation reach Twin Bridges, which trout of the same size. These findings, coupled with has a high abundance of large (> 260 mm), piscivo- past isotopic research showing that Logan River cut- rous brown trout. Although higher numbers of throat trout feed at a lower trophic level than intro- brown trout are present at low elevations (e.g., Third duced brown trout (McHugh et al. 2008), suggest Dam), sculpin consumption is potentially lower than that exotic brown trout represent a novel predator on at mid-elevations in part due to fewer large brown native sculpin in this system, with the potential to trout present. We also estimated that few sculpin are affect sculpin population dynamics (Vazquez et al. consumed at high-elevation reaches (e.g., Red 2006; Salo et al. 2007).

9 Meredith et al.

(a)

(b)

Fig. 5. (a) The per cent of brown trout that are piscivorous in each reach identified by size class, and (b) the per cent of cutthroat trout that are piscivorous in each reach identified by size class. An ‘NP’ indicates that fish of that size class/species are not present in the reach; an ‘NA’ indicates that no fish sampling was conducted in the reach, and ‘0’ indicates that no fish of that size class/species were piscivorous. Sample sizes used to calculate rates of piscivory and stomach contents (Fig. 6) are given above each bar.

One of our goals was to investigate patterns of rather, environmental characteristics that contribute to sculpin density in relation to abiotic factors and greater sculpin densities also contribute to greater densities of piscivorous trout. The sculpin densities brown trout densities. The abundance of mottled that we documented were within the range of what sculpin has been positively associated with cobble- has been recorded for mottled sculpin (probably the boulder substrates, negatively associated with high dominant species in this system) in the Western USA gradients and negatively associated with low summer and previously for the Logan River (Zarbock 1952). water temperatures (< 10 °C) (Maret 1997; Quist Our results suggest that brown trout piscivory is not et al. 2004a). We found similar results showing the main factor controlling sculpin distributions, but that sculpin densities were strongly dependent on

10 Trout predation on sculpin

(a) (b)

(c) (d)

Fig. 6. (a–d). The percentage of each major food type by wet weight comprising the stomach contents of (a) age-2 (180–260 mm) brown trout, (b) age-3 and older (> 260 mm) brown trout, (c) 180–260 mm cutthroat trout and (d) > 260 mm cutthroat trout at each reach where we collected diet data on the Logan River. An ‘NP’ indicates that fish of that size class/species are not present in the reach. temperature and general stream geomorphology. sculpin is evident regardless of the species of sculpin Sculpin were nearly absent from reaches with sub- present. strates less than cobble-sized (< 64 mm) and from Our results demonstrate that brown trout consume higher gradients > 0.020. Cobbles and small- to med- large quantities of sculpin in places where the two ium-sized boulders provide sites for male sculpin to species overlap, but that this degree of consumption prepare nests (Bailey 1952) as well as evade preda- varies dramatically across reaches. We observed tors. High gradients may prevent sculpin from mov- higher rates of predation by brown trout in mid- ver- ing upstream. Our results also suggest that the sus low-elevation reaches (brown trout had low abun- distribution of sculpin may reflect an interaction dance at high elevations), which may be related to between geomorphic and temperature factors. We the presence of flat boulders instead of round cobbles found that higher temperatures (within the range of and boulders, which could contribute to lower protec- sculpin tolerance, < 19° C) contribute to greater scul- tion from predation. The highest reach-level potential pin densities when geomorphic factors are not limit- consumption was at the Twin Bridges, which had a ing (gradient < 0.020). In cases where geomorphic high density of large, piscivorous brown trout. Our factors were suitable, some of the highest densities of estimate of consumption of sculpin at Twin Bridges sculpin occurred at sites with the highest densities of exceeded the amount of sculpin biomass present, brown trout (Third Dam, Bridger), whereas densities which may be related to our inability to accurately of cutthroat trout were negatively associated with estimate sculpin densities, as well as intra-annual var- sculpin densities. Other research also demonstrates iation in diet and presence of brown trout in this that brown trout and mottled sculpin commonly co- reach. For instance, based on unpublished movement occur throughout the Western USA (Maret 1997; data, we hypothesise that some of the large fish in Burbank 2011). It is possible that higher elevations this reach are not present year-round. To better on the Logan River are actually dominated by Paiute quantify effects of brown trout on sculpin populations sculpin, which have a lower temperature tolerance along an elevational gradient, we would have to esti- than mottled sculpin (Quist et al. 2004a); however, mate seasonal vital rates (growth, survival, recruit- the positive association between brown trout and ment) under varying abiotic conditions and densities

11 Meredith et al.

Table 2. Results of bioenergetics analysis indicating the potential individual and reach-level annual consumption of sculpin by brown trout at low-, mid- and high-elevation reaches and the estimated per cent of sculpin abundance consumed calculated from the upper limit of sculpin densities at each site.

Mass of sculpin Sculpin consumed Total trout Total trout in Total sculpin consumed % of reach sculpin Elevation/Age consumed (g) per trout (No.) per reach (No.) size class (No.) per reach (No.) abundance consumed

Low elevation Age-2 60 9 154 77 693 22 ≥ Age-3 42 6 154 46 276 9 Mid-elevation Age-2 32 5 84 18 90 24 ≥ Age-3 219 34 84 45 1530 416 High elevation Age-2 0 0 10 3 0 0 ≥ Age-3 0 27 10 3 81 13 of piscivorous brown trout. Growth rates and fecun- this hypothesis, given that cutthroat trout exhibited dity of sculpin populations can also increase in low piscivory even in reaches with low or no brown response to predation pressure by brown trout trout (Forestry Camp/Red Banks and Franklin Basin). (Anderson 1985). Other factors that could influence However, because environmental conditions and scul- interactions between brown trout and sculpin include pin densities vary between reaches dominated by sculpin predation on brown trout eggs (which has brown trout versus cutthroat trout, an experimental been documented in this system – Zarbock 1952) and approach manipulating densities of both species year-to-year fluctuations in habitat quality. Given under different environmental conditions would be these potentially strong interactions, vital rates more appropriate for testing this hypothesis. We also (fecundity, survival and growth) of sculpin have acknowledge that the sample size of brown trout diets likely evolved in response to the establishment of exceeded that of cutthroat trout for many of our brown trout in this system over 100 years ago. reaches (partly due to lower densities of large cut- Cutthroat trout in this system exhibited lower rates throat trout versus brown trout at many of our sam- of piscivory than brown trout. This lower piscivory pled reaches). Nonetheless, the low rates of piscivory cannot be attributed to a gape limitation, given that observed by cutthroat trout across reaches, even for cutthroat trout have a similar length–gape relationship large individuals, suggest that exotic brown trout in (Reimchen 1991). Potential explanatory factors this system are more piscivorous than native cutthroat include less aggressive behaviour by cutthroat trout trout. compared with brown trout (Wang & White 1994), Piscivorous brown trout have been observed at greater efficiency of brown trout in capturing prey or sizes as small as 130 mm, but in general, piscivory greater overlap in habitat use between sculpin and in brown trout occurs at sizes > 300 mm and at ages brown trout versus cutthroat trout in the Logan River. ≥ 3 (Keeley & Grant 2001; Hasegawa et al. 2012). Rates of piscivory for cutthroat trout > 300 mm in For instance, in a Virginia river, approximately 8% lakes can exceed 50% (Cartwright et al. 1998; No- of brown trout < 280 mm consumed fish prey, while wak et al. 2004), but diet studies of large cutthroat in 28–100% of brown trout > 280 mm consumed fish streams are rare. One such study reported no pisci- prey depending on season (Garman & Nielsen 1982). vory for a different subspecies of cutthroat trout Our findings support that brown trout become more (O. c. clarkii) within headwater streams of Western piscivorous at sizes > 300 mm and ages > 3. Even , but fish were generally smaller than 180 mm so, the rates of piscivory that we observed are in the (Raggon 2010). In a stream located within higher range of what has been observed for brown the Bear River Basin (same drainage as the Logan trout in streams (Keeley & Grant 2001; Kara & Alp River), it was also concluded that Bonneville cut- 2005; Montori et al. 2006). Some studies include throat trout were less piscivorous than brown trout; smaller individuals in calculating rates of piscivory. only 13% of large (> 300 mm) cutthroat trout con- If only larger individuals (e. g. > 260 mm in our sumed fish compared with a rate of 40% for large study) were included in these calculations, these stud- brown trout (Sepulveda et al. 2009). Rates of pisci- ies may have found rates of piscivory closer to our vory also did not vary by cutthroat trout life history estimates. High densities of sculpin and their low with even fluvial cutthroat trout consuming fewer fish mobility (McCleave 1964) could also contribute to than brown trout. One possible explanation for this the high rates of piscivory we documented. The lower piscivory by cutthroat trout in streams is that higher growth of brown trout in lakes versus streams brown trout have displaced cutthroat trout from a has been attributed to higher densities of fish prey more piscivorous niche. Our findings do not support (Keeley & Grant 2001). In Patagonian streams,

12 Trout predation on sculpin brown trout piscivory was more prevalent at sites Based on our findings, the presence of brown trout with the greatest densities of potential native fish is not the dominant factor controlling sculpin distri- prey (Arismendi et al. 2012). The cannibalism that butions in the Logan River watershed. Nonetheless, we observed in Right Hand Fork [with no sculpin but we suggest that brown trout is a novel predator in with high densities of small (< 180 mm) brown trout] this system with the potential to influence sculpin further supports the role of prey density in influencing population dynamics. Novel predators have behav- rates of piscivory in this system. iours or traits which differ from native species and While high densities of sculpin potentially contrib- can result in new predator–prey interactions (Salo ute to the high rates of piscivory on the Logan River, et al. 2007). We have demonstrated that exotic brown they may not explain low rates of piscivory in some trout consume significantly more sculpin than native native streams which probably contain sculpin (Mon- cutthroat trout, which has undoubtedly influenced tori et al. 2006; Fochetti et al. 2008; Budy et al. interactions between sculpin and brown trout. 2013). We know of no studies specifically investigat- Although brown trout have been implicated in the ing brown trout predation on sculpin in Eurasian decline of fish species worldwide and have dramati- streams, but sculpin densities in these systems can be cally altered native fish communities (Garman & similar to the Logan River (Hesthagen & Heggenes Nielsen 1982; Flecker & Townsend 1994) and even 2003). One explanation is that sculpin in the Logan ecosystem processes (McIntosh & Townsend 1996; River and other introduced systems have not evolved Simon & Townsend 2003), to date, there has been con- necessary behaviours to avoid predation because siderably less focus on the potential impacts of brown brown trout is a more aggressive predator than native trout predation compared with those focusing on com- trout. However, we think it is unlikely that sculpin on petitive interactions with other trout (Fausch 1989; the Logan River have not developed at least some McHugh & Budy 2006). These findings suggest that adaptation to brown trout’s presence given that they additional focus should be placed on understanding were introduced over 100 years ago. We hypothesise predatory impacts of brown trout on native eco- that abiotic or environmental mechanism(s) affecting systems. Such studies could include experimental early growth and development of brown trout in the manipulations designed to document behavioural species’ introduced range may instigate an early interactions between brown trout and native fishes in switch to piscivory (Jensen et al. 2004) and/or that varying environmental settings, long-term studies of physical or life-history traits of sculpin differ between community- and population-level responses of native brown trout’s native and introduced range increasing fish to brown trout consumption, and examination of susceptibility to predation. For example, a study of differences in the trophic structure of communities sculpin behaviour hypothesised that species of scul- that have evolved with and without brown trout. pin that exhibited high movement and using more open substrates may be more vulnerable to predation than other sculpin species that burrow or exhibit low Acknowledgements movement (Brown 1991). More targeted research The Utah Division of Wildlife Resources (Sport Fisheries would be needed to verify low rates of brown trout Research, Grant number F-47-R), the U.S. Geological Survey predation on sculpin in native brown trout streams Cooperative Fish and Wildlife Research Unit (in-kind), the U. containing sculpin, as well as potential mechanisms S. Forest Service, the Utah State University Ecology Center, contributing to this pattern. and the Utah State University School of Graduate Studies pro- Such high rates of piscivory can positively influ- vided funding and materials towards this study. We would like ence growth and reproduction of brown trout in to thank Brett Roper, Chris Luecke and Jack Schmidt, who reaches where environmental factors are suitable provided review that greatly improved previous drafts of this (Mittelbach & Persson 1998; Jonsson et al. 1999). A manuscript. We would also like to thank previous graduate students and technicians who helped in the collection and pro- recent cross-continental comparison demonstrated cessing of diet data, including Ernesto de la Hoz, Peter that brown trout in introduced range attain larger McHugh, Eriek Hansen and Jeremiah Wood. We performed sizes than stream-form brown trout in their native this research under the auspices of Utah State University range due to higher realised consumption resulting IACUC Protocol 1082. Any use of trade, firm or product from consuming fish prey (Budy et al. 2013). Larger names is for descriptive purposes only and does not imply brown trout are better competitors and can move endorsement by the U. S. Government. longer distances (Young et al. 1997; Jacob et al. 2007). This study and other research demonstrate References strong overlap in distributions of brown trout and sculpin in the Western USA and thus the potential Anderson, C.S. 1985. The structure of sculpin populations role of sculpin to influence the growth and success of along a stream size gradient. Environmental Biology of brown trout (Burbank 2011). Fishes 13: 93–102.

13 Meredith et al.

Arismendi, I., Gonzalez, J., Soto, D. & Penaluna, B. 2012. Pi- Hanson, P.C., Johnson, T.B., Schindler, D.E. & Kitchell, J.E. scivory and diet overlap between two non-native fishes in 1997. Fish bioenergetics 3.0. No. WISCU-T-97-001. Madi- southern Chilean streams. Austral Ecology 37: 346–354. son, WI: University of Wisconsin, Sea Grant Institute. Bailey, J.E. 1952. Life history and ecology of the sculpin Cot- Hasegawa, K., Yamazaki, C., Tamihisa, O. & Ohkuma, K. tus bairdi punctulatus in Southwestern Montana. Copeia 2012. Food habits of introduced brown trout and native 1952: 243–255. masu salmon are influenced by seasonal and locational prey Brown, L.R. 1991. Differences in habitat choice and behavior availability. Fisheries Sciences 78: 1163–1171. among three species of sculpin (Cottus) in artificial stream Hesthagen, T. & Heggenes, J. 2003. Competitive displacement channels. Copeia 1991: 810–819. of brown trout by Siberian sculpin: the role of size and den- Budy, P., Thiede, G.P., McHugh, P., Hansen, E.S. & Wood, J. sity. Journal of Fish Biology 62: 222–236. 2008. Exploring the relative influence of biotic interactions de la Hoz Franco, E. & Budy, P. 2005. Effects of biotic and and environmental conditions on the abundance and distribu- abiotic factors on the distribution of trout and salmon along tion of exotic brown trout (Salmo trutta) in a high mountain a longitudinal stream gradient. Environmental Biology of stream. Ecology of Freshwater Fish 17: 554–566. Fishes 72: 379–391. Budy, P., Thiede, G.P., Lobon-Cervia, J., Fernandez, G.G., Jacob, A., Nussle, S., Britschgi, A., Evanno, G., Muller, R. & McHugh, P.A., McIntosh, A.R., Vollestad, A., Becares, E. Wedekind, C. 2007. Male dominance linked to size and age, & Jellyman, P. 2013. Limitation and facilitation of one of but not to ‘good genes’ in brown trout (Salmo trutta). BMC the world’s most invasive fish: an intercontinental compari- Evolutionary Biology 7: 1–9. son. Ecology 94: 356–367. Jensen, H., Bohn, T., Amundsen, P.A. & Aspholm, P.E. 2004. Burbank, N.K. 2011. Have introduced brown trout (Salmo tru- Feeding ecology of piscivorous brown trout (Salmo trutta tta) affected native aquatic vertebrates in western United L.) in a subarctic watercourse. Annales Zoologici Fennici States streams? Masters thesis. Utah State University, 41: 318–328. Logan, Utah. Jonsson, B., Hindar, K. & Northcote, T.G. 1984. Optimal age Cartwright, M.A., Beauchamp, D.A. & Bryant, M.D. 1998. at sexual maturity of sympatric and experimentally allopatric Quantifying cutthroat trout (Oncorhynchus clarki) predation cutthroat trout and Dolly Varden charr. Oecologia 61: 319– on sockeye salmon (Oncorhynchus nerka) fry using a bioen- 325. ergetics approach. Canadian Journal of Fisheries and Aqua- Jonsson, N., Naesje, T.F., Jonsson, B., Saksgard, R. & Sandl- tic Sciences 55: 1285–1295. und, O.T. 1999. The influence of piscivory on life history traits Dieterman, D.J., Thorn, W.C. & Anderson, C.S. 2004. Appli- of brown trout. Journal of Fish Biology 55: 1129–1141. cation of a bioenergetics model for brown trout to evaluate Kara, C. & Alp, A. 2005. Feeding habitats and diet composi- growth in southeast Minnesota streams. Minnesota Depart- tion of brown trout (Salmo trutta) in the upper streams of ment of Natural Resources, Section of Fisheries Investiga- River Ceyhan and River Euphrates in Turkey. Turkish Jour- tional Report 513. nal of Veterinary and Sciences 29: 417–428. Ebner, B., Broadhurst, B., Lintermans, M. & Jekabsons, M. Keeley, E.R. & Grant, J.W.A. 2001. Prey size of salmonid 2007. A possible false negative: lack of evidence for trout fishes in streams, lakes, and oceans. Canadian Journal of predation on a remnant population of the endangered Mac- Fisheries and Aquatic Sciences 58: 1122–1132. quarie perch, Macquaria australasica, in Cotter Reservoir, Kolar, C.L. & Lodge, D.M. 2001. Progress in invasion biol- Australia. New Zealand Journal of Marine and Freshwater ogy: predicting invaders. Trends in Ecology and Evolution Research 41: 231–237. 16: 199–204. Elliott, J.M. & Hurley, M.A. 2000. Daily energy intake and Macchi, P.J., Pascual, M.A. & Vigliano, P.H. 2007. Differen- growth of piscivorous brown trout, Salmo trutta. Freshwater tial piscivory of the native Percichthys trucha and exotic sal- Biology 44: 237–245. monids upon the native forage fish Galaxias maculatus in Fausch, K.D. 1989. Do gradient and temperature affect distri- Patagonian Andean lakes. Limnologica - Ecology and Man- butions of, and interactions between, brook char (Salvelinus agement of Inland Waters 37: 76–87. fontinalis) and other resident salmonids in streams? Physiology Maret, T.R. 1997. Fish assemblages and environmental corre- and Ecology Japan 1: 303–322. lates in least-disturbed streams of the upper Snake River Fausch, K.D. & White, R.J. 1981. Competition between brook Basin. Transactions of the American Fisheries Society 126: trout (Salvelinus fontinalis) and brown trout (Salmo trutta) 200–216. for positions in a Michigan stream. Canadian Journal of Maughan, O.E. 1978. Morphometry of sculpins (Cottus) in the Fisheries and Aquatic Sciences 38: 1220–1227. Clearwater drainage, Idaho. Western North American Natu- Flecker, A.S. & Townsend, C.R. 1994. Community-wide con- ralist 38: 115–122. sequences of trout introduction in New Zealand streams. McCleave, J.D. 1964. Movement and population of the mot- Ecological Applications 4: 798–807. tled sculpin (Cottus bairdi Girard) in a small Montana Fochetti, R., Roberto, A. & Manuel Tierno de Figeueroa, J. stream. Copeia 1964: 506–513. 2008. Feeding ecology of various age-classes of brown trout McHugh, P. & Budy, P. 2005. An experimental evaluation of in River Nera, Central Italy. Belgium Journal of Zoology competitive and thermal effects on brown trout (Salmo tru- 138: 128–131. tta) and Bonneville cutthroat trout (Oncorhynchus clarkii Garman, G.C. & Nielsen, L.A. 1982. Piscivory by stocked utah) performance along an altitudinal gradient. Canadian brown trout (Salmo trutta) and its impact on the nongame Journal of Fisheries and Aquatic Sciences 62: 2784–2795. fish community of Bottom Creek, Virginia. Canadian Jour- McHugh, P. & Budy, P. 2006. Experimental effects of nal of Fisheries and Aquatic Sciences 39: 862–869. nonnative brown trout on the individual- and population-level

14 Trout predation on sculpin

performance of native bonneville cutthroat trout. Transactions Reimchen, T.E. 1991. Foraging failures and the evolution of of the American Fisheries Society 135: 1441–1455. body size in stickleback. Copeia 4: 1098–1104. McHugh, P., Budy, P., Thiede, G. & VanDyke, E. 2008. Tro- Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molof- phic relationships of nonnative brown trout, Salmo trutta sky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., and native Bonneville cutthroat trout, Oncorhynchus clarkii Ellstrand, N.C., McCauley, D.E., O’Neil, P., Parker, I.M., utah, in a northern Utah, USA river. Environmental Biology Thompson, J.N. & Weller, S.G. 2001. The population biol- of Fishes 81: 63–75. ogy of invasive species. Annual Review of Ecology and McIntosh, A.R. 2000. Habitat- and size-related variations in Systematics 32: 305–332. exotic trout impacts on native galaxiid fishes in New Zea- Salo, P., Korpimaki, E., Banks, P.B., Nordstrom, M. & Dick- land streams. Canadian Journal of Fisheries and Aquatic Sci- man, C.R. 2007. Alien predators are more dangerous than ences 57: 2140–2151. native predators to prey populations. Proceedings: Biological McIntosh, A.R. & Townsend, C.R. 1996. Interactions between Sciences 274: 1237–1243. fish, grazing invertebrates and algae in a New Zealand Sepulveda, A.J., Colyer, W.T., Lowe, W.H. & Vinson, M.R. stream: a trophic cascade mediated by fish-induced changes 2009. Using nitrogen stable isotopes to detect long-distance to grazer behaviour? Oecologia 108: 174–181. movement in a threatened cutthroat trout (Oncorhynchus McIntosh, A.R., McHugh, P.A. & Budy, P. 2011. Brown trout clarkii utah). Canadian Journal of Fisheries and Aquatic Sci- (Salmo trutta), Chapter 24. In: Francis, R.A., ed. A hand- ences 66: 672–682. book of global freshwater invasive species. London: Earth- Shemai, B., Sallenave, R. & Cowley, D.E. 2007. Competition scan, pp. 285–298. between hatchery-raised Rio Grande cutthroat trout and wild Mittelbach, G.G. & Persson, L. 1998. The ontogeny of pisci- brown trout. North American Journal of Fisheries Manage- vory and its ecological consequences. Canadian Journal of ment 27: 315–325. Fisheries and Aquatic Sciences 55: 1454–1465. Simon, K.S. & Townsend, C.R. 2003. Impacts of freshwater Montori, A., de Figueroa, J.M. & Santos, X. 2006. The diet of invaders at different levels of ecological organization, with brown trout Salmo trutta (L.) during the reproductive period: emphasis on salmonids and ecosystem consequences. Fresh- size related and sexual effects. International Review of water Biology 48: 982–994. Hydrobiology 91: 438–450. Townsend, C.R. 1996. Invasion biology and ecological Nowak, G.M., Tabor, R.A., Warner, E.J. & Fresh, K.L. 2004. impacts of brown trout Salmo trutta in New Zealand. Bio- Ontogenic shifts in habitat and diet of cutthroat trout in Lake logical Conservation 78: 13–22. , Washington. North American Journal of Fish- Townsend, C.R. & Crowl, T.A. 1991. Fragmented population eries Management 24: 624–635. structure in a native New Zealand fish: an effect of intro- Peterson, J.T., Thurow, R.F. & Guzevich, J.W. 2004. An eval- duced brown trout? Oikos 61: 347–354. uation of multipass electrofishing for estimating the abun- Vazquez, D.M., Cadotte, S., McMahon, S. & Fukami, T. 2006. dance of stream-dwelling salmonids. Transactions of the Exploring the relationship between niche breadth and American Fisheries Society 133: 462–475. invasion success. In: Cadotte, M.W., McMahon, S.M. & Fuk- Pyke, G.H. 1984. Optimal foraging theory: a critical review. ama, T., eds. Conceptual ecology and invasion biology: reci- Annual Review of Ecology and Systematics 15: 523–575. procal approaches to nature. Netherlands: Springer, pp. 505. Quist, M.C., Hubert, W.A. & Isaak, D.J. 2004a. Factors Wang, L. & White, R.J. 1994. Competition between wild affecting allopatric and sympatric occurrence of two sculpin brown trout and hatchery greenback cutthroat trout of lar- species across a rocky mountain watershed. Copeia 3: 617– gely wild parentage. North American Journal of Fisheries 623. Management 14: 475–487. Quist, M.C., Hubert, W.A. & Isaak, D.J. 2004b. Fish assem- Wood, J. & Budy, P. 2009. The role of environmental factors blage structure and relations with environmental conditions in determining early survival and invasion success of exotic in a Rocky Mountain watershed. Canadian Journal of Zool- brown trout. Transactions of the American Fisheries Society ogy 82: 1554–1565. 138: 756–767. R Core Development Team. 2011. R: a language and environ- Young, M.K., Wilkison, R.A., Phelps, J.M. III & Griffith, J.S. ment for statistical computing. Vienna, Austria: R Founda- 1997. Contrasting movement and activity of large brown tion for Statistical Computing. trout and rainbow trout in Silver Creek, Idaho. Western Raggon, M.F. 2010. Seasonal variability in diet and consump- North American Naturalist 57: 238–244. tion by cottid and salmonid fishes in headwater streams in Zarbock, W.M. 1952. An ecological study of the Utah sculpin, western Oregon. Master’s thesis, Oregon State University, Cottus baridi semiscaber in Logan River, Utah. Logan, UT: Corvallis, USA. Masters thesis, Utah State University.

15