Are Brown Trout Replacing Or Displacing Bull Trout Populations In

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1 ARTICLE

Are brown trout replacing or displacing bull trout populations in a changing climate? Robert Al-Chokhachy, David Schmetterling, Chris Clancy, Pat Saffel, Ryan Kovach, Leslie Nyce, Brad Liermann, Wade Fredenberg, and Ron Pierce

Abstract: Understanding how climate change may facilitate species turnover is an important step in identifying potential conservation strategies. We used data from 33 sites in western Montana to quantify climate associations with native bull trout (Salvelinus confluentus) and non-native brown trout (Salmo trutta) abundance and population growth rates (␭). We estimated ␭ using exponential growth state-space models and delineated study sites based on bull trout use for either spawning and rearing (SR) or foraging, migrating, and overwintering (FMO) habitat. Bull trout abundance was negatively associated with mean August stream temperatures within SR habitat (r = −0.75). Brown trout abundance was generally highest at temperatures between 12 and 14 °C. We found bull trout ␭ were generally stable at sites with mean August temperature below 10 °C but significantly decreasing, rare, or extirpated at 58% of the sites with temperatures exceeding 10 °C. Brown trout ␭ were highest in SR and sites with temperatures exceeding 12 °C. Declining bull trout ␭ at sites where brown trout were absent suggest brown trout are likely replacing bull trout in a warming climate. Résumé : Il importe de comprendre comment le climat pourrait faciliter le renouvellement des espèces pour cerner des stratégies de conservation potentielles. Nous avons utilisé des données de 33 sites de l’ouest du Montana pour quantifier les associations climatiques avec l’abondance et les taux de croissance de populations (␭) d’ombles a` tête plate (Salvelinus confluentus) indigènes et de truites brunes (Salmo trutta) non indigènes. Nous avons estimé ␭ en utilisant des modèles d’espaces d’états de croissance exponentielle et délimité les sites étudiés selon leur utilisation par l’omble a` tête plate soit comme habitat de frai et d’alevinage (SR) ou d’approvisionnement, de migration et d’hivernage (FMO). L’abondance des ombles a` tête plate était néga- tivement associée aux températures moyennes des cours d’eau en août dans les habitats SR (r = −0,75). L’abondance de la truite brune était généralement maximum a` des températures entre 12 et 14 °C. Nous avons constaté que les ␭ des ombles a` tête plate étaient généralement stables aux sites présentant une température moyenne en août inférieure a` 10 °C, mais qu’il diminuait significativement, l’espèce y étant rare ou disparue, dans 58 % des sites où cette température dépasse 10 °C. Les ␭ des truites brunes étaient maximums dans les habitats SR et les sites caractérisés par des températures supérieures a` 12 °C. Des ␭ en baisse des ombles a` tête plate dans des sites exempts de truites brunes donnent a` penser que ces dernières remplacent probablement For personal use only. les ombles a` tête plate dans un climat en réchauffement. [Traduit par la Rédaction]

Introduction salmonids, particularly in the context of climate change, are often Climate change is likely to substantially alter stream ecosystems not well understood (e.g., Rahel and Olden 2008; Lawrence et al. with pronounced effects for cold-water fishes such as salmonids 2014). This uncertainty stems partly from the paucity of situations (Jonsson and Jonsson 2009; Williams et al. 2009; Elliott and Elliott where changing climatic conditions have been empirically linked 2010). Salmonid life histories, vital rates, and demographics are with salmonid population and demographic data (Kovach et al. strongly tied to factors influenced by climate, including thermal 2016). Likewise, delineating between non-native displacement and hydrologic regimes (Elliott 1994; Lobon-Cervia 2004; Crozier (i.e., declines in native salmonids due to negative interactions with et al. 2008; Warren et al. 2012). With different thermal tolerances non-natives) or replacement (i.e., declines in native salmonids due and life-history expressions, the effects of changing climatic con- to factors unrelated to non-natives) is an inherent challenge in ditions are likely to differ across species. Understanding how cli- species turnover studies (Dunham et al. 2002). mate, among other factors, may be influencing populations is Refining our understanding of the influences of climate change critical for identifying the potential for effective management and non-native species on extant populations of bull trout (Salvelinus and restoration scenarios. confluentus) is essential in designing conservation strategies to enhance long-term persistence. Bull trout are currently listed as “Threat- Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 Non-native salmonids are an additional concern for the conservation of native salmonids across North America (Dunham et al. ened” in the United States under the Endangered Species Act and 2002). Widespread introductions for recreation have resulted in ranked “Of Special Concern” or “Threatened” for three of four geo- naturally producing populations of non-native salmonids in many graphic populations by the Committee on the Status of Endangered streams. The mechanistic threats of non-native species to native Wildlife in Canada. Bull trout are extremely temperature-sensitive

Received 10 June 2015. Accepted 31 December 2015. R. Al-Chokhachy. US Geological Survey, Northern Rocky Mountain Science Center, 2327 University Way, Suite 2, Bozeman, MT 59715, USA. D. Schmetterling, P. Saffel, B. Liermann, and R. Pierce. Montana Fish, Wildlife and Parks, 3201 Spurgin Road, Missoula, MO 59804, USA. C. Clancy and L. Nyce. Montana Fish, Wildlife and Parks, 1801 North 1st Street, Hamilton, MO 59840, USA. R. Kovach. US Geological Survey, Northern Rocky Mountain Science Center, Glacier Field Station, West Glacier, MT 59936, USA. W. Fredenberg. US Fish and Wildlife Service, Creston Fish & Wildlife Center, Kalispell, MT 59901, USA. Corresponding author: Robert Al-Chokhachy (email: [email protected]). Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.

Can. J. Fish. Aquat. Sci. 73: 1–10 (2016) dx.doi.org/10.1139/cjfas-2015-0293 Published at www.nrcresearchpress.com/cjfas on 23 February 2016. Pagination not ﬁnal (cite DOI) / Pagination provisoire (citer le DOI)

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Fig. 1. Major rivers, locations of the long-term monitoring sites (grey circles with numbers distinguishing sample sites; see Table 1), and stream gauges (triangles) in western Montana, USA. Inset denotes location of the study area relative to the western portion of the USA. For personal use only.

relative to other salmonids (Selong et al. 2001), and distributions changing climatic conditions are associated with population trends during summer months are strongly tied to ambient stream temper- and abundance; and (iii) the putative threat brown trout may repre- atures (Dunham et al. 2003; Wenger et al. 2011). However, bull trout sent to extant bull trout populations. exhibit complex life histories, and adults and subadults can season- ally demonstrate large upstream and downstream movements to Materials and methods access foraging and overwintering habitat (Swanberg 1997; Howell et al. 2010; Starcevich et al. 2012). Study area Brook trout (Salvelinus fontinalis) and lake trout (Salvelinus namaycush) Our study area included 33 long-term sampling sites in the Clark have been identified as considerable threats to bull trout populations Fork, Bitterroot, and Blackfoot river drainages in western Mon- through predation (Martinez et al. 2009; Hansen et al. 2010; tana (Fig. 1). Lands within the study area include a mixture of Fredenberg 2014), competition (Guy et al. 2011; Warnock and mostly private lands in the valley bottoms and river corridors and Rasmussen 2014), and nonintrogressive hybridization resulting in state and federal ownership in the tributaries and headwaters. gametic wastage (Leary et al. 1993; DeHaan et al. 2010). Recently, Native vegetation within riparian zones varies elevationally across however, there has been growing concern regarding the effects of sites, but reflects montane forests commonly found in the region. introduced brown trout (Salmo trutta) on bull trout populations in Riparian communities commonly includes a mixture of grasses and Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 western Montana, USA, particularly in light of recent evidence sug- sedges (Carex spp.), shrub-dominated taxa (e.g., Salix spp.), mixed gesting expansion of brown trout into historic bull trout habitat conifer (Pinaceae; e.g., Abies spp.), and poplars (Populus spp.). Cli- (USFWS 2015). Similar to bull trout, brown trout are a fall-spawning mate within the study area is characterized by relatively cold, wet species and considered a top-level predator within streams; however, winter and spring months and relatively warm, dry summers. bull trout have substantially lower thermal tolerances than brown Streamflows are typical for snowmelt-influenced streams in the trout (Elliott 2009) and, as a result, often occupy headwater streams upstream of the distribution of brown trout. northern Rocky Mountains, with high spring flow events during Recent observations of expansion in brown trout abundance May and June and declining flow throughout the summer and and distribution (P. Saffel, personal observation, 2011) elevated early winter. concerns about the effects of brown trout and, more specifically, The sample sites occurred on first- to fourth-order streams (Strahler whether brown trout are displacing or replacing bull trout. Here, 1952) ranging in elevation from 712 to 1893 m. In addition to bull we used long-term monitoring data from locations in the Colum- trout and brown trout, other species commonly found in sample bia River headwaters of western Montana to evaluate (i) popula- surveys included native westslope cutthroat trout (Oncorhynchus tion status and trends of bull trout and brown trout; (ii) how clarkii lewisi), mountain whitefish (Prosopium williamsoni), sculpin

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Al-Chokhachy et al. 3

Table 1. Site numbers (corresponding with location in Fig. 1), stream, latitude, longitude, classification of habitat type for bull trout (Recovery classification), range of years in analyses, the number of years of data (n), and the mean August temperature predicted from the NorWeST stream temperature model. Recovery Mean August Site Stream Latitude (°N) Longitude (°W) classification Year range n temp. (°C) 1 Bertie Lord Creek 45.90909 113.783 SRa 1990–2012 12 11.1 2 Bitterroot River 46.46943 114.116 FMO 1982–2009 9 14.9 3 Bitterroot River 46.83103 114.054 FMO 1989–2009 10 17.4 4 Bitterroot River 46.01525 114.165 FMO 2005–2013 8 18.1 5 Blackfoot River 46.91069 113.691 FMO 1988–2012 14 15.7 6 Blackfoot River 47.02225 113.308 FMO 1985–2013 16 16.4 7 Camp Creek 45.81539 113.954 SRa 2005–2012 11 13.0 8 Clark Fork River 47.02166 114.402 FMO 1980–2012 14 16.5 9 Clark Fork River 46.86888 113.935 FMO 1980–2013 17 18.0 10 Clark Fork River 46.83817 113.847 FMO 1988–2013 11 20.4 11 Daly Creek 46.17873 113.900 SR 1989–2012 13 9.4 12 EF Bitterroot River 45.90939 113.709 FMO 1992–2011 9 11.1 13 EF Bitterroot River 45.91686 114.103 FMO 1995–2013 13 14.7 14 EF Bitterroot River 45.86007 114.026 FMO 1998–2012 10 15.2 15 EF Bull River 48.11330 115.775 SR 2001–2008 8 11.3 16 EF Bull River 48.12529 115.723 SR 2001–2007 7 12.1 17 Fishtrap Creek 47.76384 115.075 SR 1999–2011 9 9.7 18 Gold Creek 46.94177 113.669 SR 1996–2011 11 12.2 19 Martin Creek 45.93969 113.731 SR 1992–2013 10 11.2 20 Meadow Creek 45.84822 113.821 SR 1989–2010 7 8.7 21 Meadow Creek 45.82944 113.802 SR 1989–2011 15 9.2 22 Moose Creek 45.93667 113.717 SR 1991–2011 11 10.7 23 NF Blackfoot River 46.97979 113.100 SR 1989–2001 7 11.9 24 Rock Creek 46.57256 113.686 FMO 1980–2013 15 14.3 25 Rock Creek 46.42300 113.721 FMO 1980–2013 15 14.5 26 Rye Creek 45.99271 114.068 SRa 1990–2011 13 11.9 27 Skalkaho Creek 46.16379 113.899 SR 1989–2013 25 9.9 28 Sleeping Child Creek 46.10994 114.004 SR 1989–2013 25 12.8 29 Thompson River 47.73717 115.022 SRa 1985–2012 13 14.6 30 Thompson River 47.66886 115.108 SRa 1984–2012 17 12.2 31 Warm Springs Creek 45.82392 114.064 SR 1992–2009 10 11.5 32 WF Thompson River 47.66100 115.193 SR 2001–2010 7 8.6 33 WF Thompson River 47.70250 115.207 SR 1999–2010 9 9.3

For personal use only. Note: SR, spawning and rearing; FMO, foraging, migrating, and overwintering. aSites not originally characterized as SR habitat by the USFWS but subsequently designated owing to known bull trout use.

(Cottus spp.), longnose dace (Rhinichthys cataractae), and non-native Stream temperature data rainbow trout (Oncorhynchus mykiss) and brook trout. Year-specific stream temperature data were lacking for all sites and all years. As such, we relied on stream temperature predic- Sampling data tions from a spatially explicit stream temperature model. The Our dataset included relatively long-term monitoring sites sam- NorWeST stream temperature model incorporates spatial statisti- pled by Montana Fish, Wildlife and Parks and US Forest Service cal models to provide estimates of August mean temperature at a biologists. We constrained our analyses to all sites with at least 1 km scale (Isaak et al. 2010). We initially evaluated how well the 5 years of data within watersheds currently occupied by brown year-specific stream temperature predictions from NorWeST matched trout (fifth code hydrologic unit codes; www.nhd.usgs.gov/) and observations from those locations where long-term empirical within the historical range of bull trout. Sampling methods varied temperature data were available. We found a wide range of corre- across sites and included a mixture of backpack electrofishing, lations between empirical and modeled annual data (¯r = 0.75; bank electrofishing, and boat electrofishing. Despite differences range = 0.47–0.95). Given this variability across sites and the fact in approaches across sites, however, the sampling methods were that interannual NorWeST predictions were relatively inaccurate Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 generally consistent through time at any given sampling site. at several sites, we focused only on mean August temperature Survey dates varied from early April through mid-September predictions (1993–2011) from the NorWeST model in our analyses. (see below) and the length of stream sampled varied according to Mean NorWeST predictions across years were highly correlated stream size (see online supplemental material, Table S11). We in- with mean August temperature estimated from empirical data cluded only counts of individuals collected from the first-pass (r = 0.98). electrofishing survey (hereinafter relative abundance), given the difficulties of estimating abundance for species at low densities Analyses (Al-Chokhachy et al. 2009). While single-pass data are known to We delineated the sites in our analyses according to designa- underestimate trout abundance, correlations between single and tions of bull trout occupancy used by the US Fish and Wildlife multiple passes are typically high (Bateman et al. 2005), suggest- Service (USFWS) in the Bull Trout Recovery Plan (Table 1; USFWS ing such difference are unlikely to drastically alter our results. 2014), thereby aligning our results with ongoing management

1Supplementary data are available with the article through the journal Web site at http://nrcresearchpress.com/doi/suppl/10.1139/cjfas-2015-0293.

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strategies. Sites were delineated as either spawning and rearing (SR) Fig. 2. A per survey plot of the mean number per metre of bull or foraging, migrating, and overwintering (FMO) habitat based on trout (open) and brown trout (grey) from single-pass electrofishing bull trout life history and the habitats corresponding to specific surveys and mean August stream temperature at long-term life stages. For migratory bull trout, the SR habitat largely consists monitoring sites within bull trout spawning and rearing (SR; circles) of headwater tributaries, with the FMO habitat occurring down- and foraging, migrating, and overwintering (FMO; squares) habitat stream in mainstem (fourth-order or larger) rivers and lakes. For in western Montana, USA. resident bull trout, which typically occupy second- and third- order streams, there is no clear delineation in SR and FMO habitat. Not all streams within the historical range of bull trout were delineated, and five of our sites occurred on streams undesignated in the Bull Trout Recovery Plan. Given that these five streams all represent tributary habitat and (or) use by bull trout for spawning and rearing, we aggregated these with the SR sites. Sampling dates generally occurred during April–June or September for sites in FMO habitat and July and August for sites in SR habitat. By delineating our results for FMO (n = 13) and SR (n = 20), this approach allowed us to gain insight into population trends for different life-history stages (e.g., migratory components). We used counts of bull trout and brown trout at sites for measures of relative abundance and scaled this to linear stream length (fish·m−1) as survey length differed across sites. We investigated potential autocorrelation among sites using pairwise, interannual correlations in abundance for sites within each river basin (Bitter- Results root, Blackfoot, upper Clark Fork, lower Clark Fork). Given regional shifts in climate since 2000 (e.g., supplemental Fig. S11; Relative abundance Pederson et al. 2010; Al-Chokhachy et al. 2013), we assessed differ- We observed no clear patterns in correlations in bull trout ences in relative abundance (pre-2000 and 2000 and later) using a (¯r = −0.02) or brown trout (¯r = 0.16) relative abundance across all Mann–Whitney rank sum test. sites. In FMO sites, relative abundance of bull trout (mean = We estimated bull trout and brown trout population growth 0.004 fish·m−1; SD = 0.009 fish·m−1) was substantially lower than rate (␭) using exponential growth state space (EGSS) models with brown trout (mean = 0.023 fish·m−1; SD = 0.031 fish·m−1), and restricted maximum likelihood (Humbert et al. 2009). The EGSS brown trout relative abundance exceeded bull trout at all FMO model is a flexible approach to estimate population trends from sites except one (Site 12; Fig. 1). Bull trout and brown trout relative abundance data that can span short time periods (i.e., 10 years) abundance were weakly correlated at sites within bull trout SR habitat (r = −0.34) and across all sites (r = −0.27). and have unequal time steps, which commonly occur in popula- There were considerable changes in bull trout and brown trout tion monitoring data. abundance through time. Brown trout relative abundance was The EGSS model provides point estimates of population growth For personal use only. significantly higher than bull trout at FMO sites during the early rate that are highly concordant with other approaches for esti- (pre-2000; P = 0.05) and late (2000 and later; P < 0.001) sample ␭ mating in an exponential growth model (diffusion approxima- years, and this difference increased between the sample periods tion or linear regression). However, the confidence intervals are (supplemental Fig. S11). In contrast, bull trout relative abundance generally more accurate compared with simple, exponential trend (¯x = 0.058 fish·m−1; SD = 0.071 fish·m−1) was two times higher than analyses (Humbert et al. 2009; Meyer et al. 2014), as this approach brown trout relative abundance (x¯= 0.026 fish·m−1; SD = 0.051 fish·m−1) also accounts for observation error and process variation. The in SR sites; bull trout relative abundance exceeded brown trout at EGSS model assumes that process and observation errors are nor- 14 of the 20 SR sites (brown trout > bull trout at Sites 15, 18, 23, 29, mally distributed and that process noise is independent of obser- and 30; Fig. 1). Bull trout relative abundance exceeded brown trout vation error, and the model more naturally accommodates intrinsic during the early (P < 0.001) and late periods (P = 0.022), but the autocorrelation present in time-series data (Kery and Schaub 2012). difference decreased between the sample periods. We considered the exponential growth model appropriate for our Mean bull trout relative abundance was negatively associated data given the relatively low abundances of bull trout, the fact with August stream temperatures when considering all sites (r = that most observations of brown trout expansions were relatively −0.65; Fig. 2) and sites within SR habitat alone (r = −0.75; Fig. 2). On recent, and the difficulty in understanding the appropriate density- the contrary, brown trout relative abundance demonstrated no dependent structure across sites. apparent correlation with August temperatures at all sites (r = 0.10) and only a weak positive correlation at sites within bull trout

Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 Our analyses included datasets with unequal sample sizes and range of years with sampling data, as the number of sample years SR habitat (r = 0.45). Brown trout relative abundance was generally varied across sites (x¯ = 12.2; range = 7–25 years). However, we found lowest at temperatures below 12 °C, highest between 12 and 14 °C, little evidence of correlations between bull trout or brown trout and generally decreased above 15 °C (Figs. 2 and 3). Despite these patterns, brown trout were frequently detected at sites with tem- population trends with range of years of sample data at sites peratures as low as 8.5 °C. (r < 0.40). Abundances of bull trout and brown trout were low, at least during some time periods, at many sites, and relative abun- Population trends dance values of zero were not uncommon. The EGSS estimates are For extant bull trout populations, we found only one site with performed on a logarithmic scale where values of zero are unde- increasing population trends (Site 6; Fig. 3a), with all other sites fined; thus, we added a value of one to all observations. We used demonstrating stable or decreasing trends. In FMO sites, bull an alpha value of 0.10 for all analyses given the conservation trout populations have been extirpated or occur at extremely low implications of type II error and considered trends significant abundance levels (i.e., trends inestimable, median relative abun- where confidence intervals did not include one (i.e., ␭ = 1, stable dance = 0) at 31% of the sites and demonstrated significant decreas- population trend). ing trends at 23% of the sites and stable population trends at 38%

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Fig. 3. Estimates of population growth rate (␭) for bull trout (open; panel a) and brown trout (grey; panel b) at sites (see Table 1 for list of site numbers) within bull trout foraging, migrating, and overwintering (FMO; squares) and spawning and rearing (SR; circles) habitat in western Montana, USA. The horizontal line is a reference indicating stable population trend, the × symbols indicate sites where bull trout have been extirpated, triangles indicate sites where brown trout have not yet colonized, and diamonds indicate where bull trout or brown trout are infrequent. For personal use only.

of the sites. No bull trout populations exhibited increasing popu- Brown trout population trends were highest in SR and sites with lation trends in SR sites, with one currently extirpated, and 38% of temperatures exceeding 12 °C (Fig. 5b). the sites indicating significant decreasing trends. Brown trout illustrated considerably different patterns in our Discussion analyses, with only one site indicating significant decreasing trends Temperature is a critical component controlling the physiol- (Fig. 3b). Brown trout population trends were stable or signifi- ogy, fitness, and life-history expressions of salmonids (Fry 1971; Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 cantly increasing at all other sites. Where estimates were possible, Elliott 1976; Jonsson and Jonsson 2009; Warren et al. 2012). Chang- brown trout population trends were significantly increasing at ing thermal regimes can alter the distributions and, thus, inter- 31% of the FMO sites and 50% of the SR sites. actions among species (McMahon et al. 2007; Finstad et al. 2011). Brown trout and bull trout population trends were strongly With substantially colder thermal tolerances than most salmonids, associated with August stream temperatures. Similar to observed bull trout are likely to be increasingly stressed under expected patterns for relative abundance, brown trout population trends changes in climate (Rieman et al. 2007; Wenger et al. 2011). Under- were stable at locations with temperatures between 11 and 12 °C, standing the effects of sympatric, non-native species is an impor- increasing between 12 and 15 °C, and stable at temperatures above tant step in developing robust climate adaptation measures to 15 °C (Fig. 4). In SR habitat, we found bull trout population trends enhance the persistence of native salmonids such as bull trout to be generally stable below 10 °C but significantly decreasing, (Peterson et al. 2013). rare (i.e., trend not estimable owing to extremely low abundance), or extirpated at 58% of the sites with temperatures exceeding 10 °C Stream temperature, abundance, and trends (Fig. 5a). Bull trout population trends were significantly decreas- In our study, linkages between summer stream temperatures ing at multiple sites where brown trout have not yet colonized. and bull trout and brown trout abundance were apparent, a pattern

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Fig. 4. Estimates of brown trout population growth rates from all Fig. 6. The relationships between bull trout population growth sample sites in western Montana, USA (circles; 90% CI), locations rates (␭) and relative abundance (mean number of bull trout) at where brown trout have been detected infrequently (allowing for no bull trout spawning and rearing (SR) sites with August stream estimate of population growth rate; diamonds), and where brown temperatures <10 °C (open circles), SR sites with August stream trout have never been detected (triangles) against mean August temperatures >10 °C (black circles), and bull trout foraging, stream temperatures. The horizontal line at ␭ = 1.0 indicates a stable migrating, and overwintering (FMO) sites (grey squares) in western population growth rate. Montana, USA.

Fig. 5. Estimates of bull trout (a) and brown trout (b) population consistent with recent distributional studies (Isaak et al. 2015). We growth rates (␭) at sample sites within bull trout spawning and found the highest brown trout abundances and generally increas- rearing (SR) habitat with different mean August stream ing trends at sites where temperatures were within the optimum temperatures in western Montana, USA. The horizontal line is a range for brown trout from lab and ﬁeld studies (Hari et al. 2006; reference indicating stable population growth rate, the × symbols Elliott 2009). Brown trout were consistently observed where mean indicate sites where bull trout have been extirpated, triangles August temperatures were above 11 °C up to 20 °C (the highest indicate sites where brown trout have not yet colonized, and temperatures at our sites). While the general absence of brown diamonds indicate where either bull trout or brown trout are trout at temperatures below 11 °C suggests thermal regimes may infrequent. be limiting expansion (sensu Isaak et al. 2015), distributions within their native range can occur at thermal regimes as low as 3 °C (Hari et al. 2006), suggesting that colonization of these colder sites is possible. The limited brown trout expansion at colder sites may

For personal use only. ultimately be driven by temperature-mediated competitive ad- vantages for bull trout (sensu Taniguchi and Nakano 2000), a mechanism warranting further research. Indications of bull trout at or near extirpation (i.e., occurring at extremely low relative abundance) at some sites and declining trends in bull trout abundance within FMO and SR habitat high- light concerns for the long-term persistence of bull trout within this region. Bull trout abundance was highest and populations were stable where mean August temperatures were below 10 °C (Fig. 5), again indicating corroboration of results with distribution- only studies (Isaak et al. 2015). There was not a negative relation- ship between population growth and relative abundance for bull trout, indicating stability or declining growth was not density- dependent (Fig. 6). However, many sites demonstrated relatively low abundance (e.g., ≤0.05 bull trout·m−1) and could be suscepti- ble to depensatory growth (i.e., Allee effects with a positive relation between population growth and abundance). Persistence is Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 likely tenuous for these low abundance populations with decreasing or even stable population trends (Stacey and Taper 1992; Rieman and Allendorf 2001). While trend analyses indicated considerable variability in associations with temperature, the relatively low bull trout abundance at warmer sites (Figs. 2 and 6) and inherent difﬁculties of detecting declines in such small populations (Taylor and Gerrodette 1993) suggests extirpation may be inevitable without dramatic intervention (sensu Tilman et al. 1994).

Displacement or replacement? Whereas we expect the distribution of ﬁshes to shift in accor- dance with changing climatic conditions (Almodovar et al. 2012; Comte et al. 2013), it is often unclear whether such changes are

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due to changes in climate-related attributes (e.g., temperature) or 2007). Brown trout are considered to be more resilient to whirling exacerbated by interspecific interactions. Expansion of brown trout disease than other salmonids (Baldwin et al. 2000; Pierce et al. appears to be in part driven by regional air temperature and en- 2014). The higher prevalence of whirling disease at lower-elevation, suing stream temperature warming during the 21st century warmer streams (Baldwin et al. 2000) may have contributed to (Pederson et al. 2010; Isaak et al. 2012; Fig. S21). Conversely, de- enhancing some source populations of brown trout through re- clines in bull trout appear to be at least partly thermally driven, as ductions in sympatric species abundance (e.g., rainbow trout) and evidenced by multiple populations demonstrating significant de- the subsequent increase in brown trout abundance in FMO habi- clines in the absence of brown trout. However, we do acknowl- tat leading to the spread of brown trout to bull trout SR streams. edge that our datasets were not randomly chosen but were the However, considerable differences in brown trout population best data available in our region and thus restrict our inference to trends between adjacent tributaries (e.g., Bitterroot River) suggest the sites included herein. Further analyses using larger datasets the importance of local climatic conditions at sites. are needed to allow for formal statistical testing of factors associated with such patterns. In lieu of these shortcomings, the appar- Declining bull trout populations ent transition from initial bull trout declines followed by While stream temperature and discharge are likely driving the increases in brown trout abundance, rather than concurrent observed patterns of bull trout population trends, a host of other trends, provides considerable support for species replacement factors may have contributed to our results. For example, migra- (Dunham et al. 2002). tory bull trout within the lower Bitterroot River and lower Clark Further contraction of thermally suitable habitat for bull trout Fork River have been largely extirpated or severely reduced for is anticipated in the future for western Montana (Jones et al. 2014; over three decades. Large, migratory fish have considerably higher Isaak et al. 2015; USFWS 2015). Despite indications of bull trout fecundity than smaller resident females (Al-Chokhachy and Budy declines in allopatry as a result of potential thermal constraints, 2008), which may help offset competitive interactions with non- there is uncertainty in how the presence of brown trout and (or) natives such as brown trout. Large pulses of recruitment from increasing trends of brown trout may exacerbate the effects or migratory bull trout spawning may also allow populations to re- warming climate where populations occur in sympatry. Within cover from pulsed disturbances (e.g., Bohlin et al. 2001), as resident- stream ecosystems, both bull trout and brown trout demonstrate only populations may lack resiliency over a period of multiple increasing piscivory with size and are commonly top-level preda- generations. tors (Elliott and Hurley 2000; Lowery 2009; Budy et al. 2013), sug- In addition, bull trout throughout our study area have been gesting potential competition for space and forage resources. directly or indirectly affected by thermal constraints, dewatering, Other mechanisms for negative interactions include redd super- agricultural use, development, and factors associated with increas- imposition (e.g., Essington et al. 1998; Storaasli and Moran 2015), ing human population growth (e.g., increased angling; Al-Chokhachy as both species spawn during the fall–winter, with brown trout et al. 2008). While each factor in isolation may not drive bull trout commonly spawning after the cessation of bull trout spawning population trends, the synergistic effects of multiple stressors (Wood and Budy 2009). Finally, increasing numbers of brown trout along with changing climatic conditions may ultimately result in may exacerbate declining bull trout populations through preda- a tipping point for bull trout (sensu Nelson et al. 2009). Continued tion, particularly at early life stages, thus limiting recruitment monitoring within higher-resolution climate data (e.g., annual (Budy et al. 2013). An interplay of interactions may also occur temperature data) may allow for analyses to disentangle such (Persson et al. 2013), making it challenging to specifically identify effects.

For personal use only. the strength of bull trout – brown trout interactions across differ- Our results indicating relatively low abundance and stable or ent life stages without targeted research. declining population trends at a large portion of our sites are contrary to recent findings for populations of bull trout in Idaho, Beyond thermal relationships USA, that show stable or increasing trends (Meyer et al. 2014). We acknowledge that our analyses have largely focused on ther- Aside from different sampling methodologies (e.g., redd counts, mal relationships, yet additional factors may have contributed to snorkeling, etc.), the observed differences between population the observed population trends. In particular, hydrologic regimes trends in Montana and Idaho require further study but may stem can also act to regulate populations of fall-spawning salmonids from the scale of analyses. We specifically delineated sites by such as bull trout and brown trout (Tonina et al. 2008). Including habitat designations under the US Fish and Wildlife Service’s Bull discharge in our analyses was not possible, as site-specific esti- Trout Recovery Plan and considered trends at the local population mates of discharge were not available. A post hoc analyses of level (i.e., panmictic breeding group; Whitesel et al. 2004), while existing gauging data (www.usgs.gov) suggests the number of Meyer et al. (2014) grouped local populations at a larger “core” high discharge events during November through March, the pe- population level (Whitesel et al. 2004). Given the scale at which riod when both species eggs are typically in the gravel, decreased connectivity between local populations occurs varies across prox- by nearly 75% during the 2000s (Fig. S3a1). The apparent decrease imate landscapes (Whiteley et al. 2006), we chose to evaluate rel- in high discharge events during the winter is likely driven by ative abundance and trends at a finer resolution. Analyses at the reduced snowpack at lower elevations (Mote 2003), such that win- local population level also allowed for inferences across different Can. J. Fish. Aquat. Sci. Downloaded from www.nrcresearchpress.com by USGS LIBRARY on 06/03/16 ter warming events do not result in rain-on-snow freshets. De- habitat types and life-history expressions, a broader understand- creases in the number of high discharge events likely reduced ing of differences in trends within larger populations (sensu scouring of redds and contributed to the increasing population Hanski 1999), and, more specifically, linkages with site-specific growth rates of brown trout (Cattaneo et al. 2002; Daufresne and climatic attributes. Indeed, a comprehensive analysis considering Renault 2006; Unfer et al. 2011). Brown trout populations can also how inference changes across scales is warranted. be limited by high discharge during periods of emergence, thus reducing young-of-year survival (Lobon-Cervia 2014). However, we Management opportunities found little evidence of changes in the frequency of high dis- Identifying effective management strategies to enhance persis- charge events during the period of likely emergence (Fig. S3b1). tence of existing bull trout populations is expected to become Additionally, changes in brown trout abundance may have increasingly valuable (Falke et al. 2015). Concomitantly, brown been influenced by indirect effects of the exotic whirling disease trout represent an important sport fishery in Montana and occupy (Myxobolus cerebralis). Whirling disease was detected in the mid- a niche as a large piscivore that was formerly occupied by bull 1990s and subsequently spread throughout the lower elevations trout — a species that is increasingly scarce and one that currently portions of our study area (Baldwin et al. 1998; Granath et al. offers limited angling opportunities. With little empirical infor-

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8 Can. J. Fish. Aquat. Sci. Vol. 73, 2016

mation describing bull trout – brown trout interactions, uncer- Al-Chokhachy, R., Moran, S., McHugh, P.A., Bernall, S.R., Fredenberg, W., and tainty exists in the effectiveness of controlling brown trout DosSantos, J.M. 2015. Consequences of actively managing a small bull trout population in a fragmented landscape. Trans. Am. Fish. Soc. 144: 515–531. populations where sympatric with declining bull trout popula- doi:10.1080/00028487.2015.1007162. tions. Almodovar, A., Nicola, G.G., Ayllon, D., and Elvira, B. 2012. Global warming Our results clearly suggest streams warming to levels optimal threatens the persistence of Mediterranean brown trout. Global Change Biol. for brown trout (12 to 15 °C) are the most vulnerable to future 18(5): 1549–1560. doi:10.1111/j.1365-2486.2011.02608.x. invasions and major increases in brown trout abundance. Ob- Alvarez, D., Cano, J.M., and Nicieza, A.G. 2006. Microgeographic variation in metabolic rate and energy storage of brown trout: countergradient selection served declines in allopatric bull trout populations suggest remov- or thermal sensitivity? Evol. Ecol. 20(4): 345–363. doi:10.1007/s10682-006-0004-1. ing brown trout where sympatric may not recover populations of Baldwin, T.J., Peterson, J.E., McGhee, G.C., Staigmiller, K.D., Motteram, E.S., bull trout to historical abundance. However, reducing or remov- Downs, C.C., and Stanek, D.R. 1998. Distribution of Myxobolus cerebralis in ing brown trout where sympatric with bull trout may facilitate salmonid fishes in Montana. J. Aquat. Anim. Health, 10(4): 361–371. bull trout persistence under changing climatic conditions (e.g., Baldwin, T.J., Vincent, E.R., Silflow, R.M., and Stanek, D. 2000. Myxobolus cerebralis infection in rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) Peterson et al. 2008). An important next step may be to specifically exposed under natural stream conditions. J. Vet. Diagn. Invest. 12(4): 312–321. evaluate bull trout – brown trout interactions at streams ap- doi:10.1177/104063870001200403. PMID:10907859. proaching 12 °C (e.g., Sites 1, 12, 15, and 19; Table 1), while concom- Bateman, D.S., Gresswell, R.E., and Torgersen, C.E. 2005. Evaluating single-pass itantly quantifying the effectiveness of targeted brown trout catch as a tool for identifying spatial pattern in fish distribution. J. Freshw. removal efforts on the persistence of extant bull trout popula- Ecol. 20(2): 335–345. doi:10.1080/02705060.2005.9664974. Bohlin, T., Pettersson, J., and Degerman, E. 2001. Population density of migratory tions. and resident brown trout (Salmo trutta) in relation to altitude: evidence for a Despite being increasingly used in salmonid conservation to migration cost. J. Anim. Ecol. 70(1): 112–121. doi:10.1046/j.1365-2656.2001.00466.x. combat non-native species, we urge caution in the use of barriers Budy, P., Thiede, G.P., Lobon-Cervia, J., Gonzalez Fernandez, G., McHugh, P., to control brown trout expansion, given the vulnerability of iso- McIntosh, A., Vollestad, L.A., Becares, E., and Jellyman, P. 2013. Limitation and facilitation of one of the world’s most invasive fish: an intercontinental lated populations and likely elimination of migratory bull trout comparison. Ecology, 94(2): 356–367. doi:10.1890/12-0628.1. PMID:23691655. (Falke et al. 2015). Even infrequent returns of large, fecund adults Caissie, D. 2006. The thermal regime of rivers: a review. Freshw. Biol. 51(8): can substantially enhance persistence (Morita and Yamamoto 2002; 1389–1406. doi:10.1111/j.1365-2427.2006.01597.x. Al-Chokhachy et al. 2015), suggesting the importance of including Cattaneo, F., Lamouroux, N., Breil, P., and Capra, H. 2002. The influence of selective passage where barriers are implemented. Additionally, hydrological and biotic processes on brown trout (Salmo trutta) population dynamics. Can. J. Fish. Aquat. Sci. 59(1): 12–22. doi:10.1139/f01-186. isolation will exacerbate the loss of genetic diversity within bull Comte, L., Buisson, L., Daufresne, M., and Grenouillet, G. 2013. Climate-induced trout populations, thereby reducing adaptive potential and in- changes in the distribution of freshwater fish: observed and predicted trends. creasing inbreeding load, a problematic scenario for a fish already Freshw. Biol. 58(4): 625–639. doi:10.1111/fwb.12081. stressed by other human-induced and climatic stressors (Kovach Crozier, L.G., Hendry, A.P., Lawson, P.W., Quinn, T.P., Mantua, N.J., Battin, J., et al. 2015). Certainly more information is needed to understand Shaw, R.G., and Huey, R.B. 2008. Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific the benefits of barrier installations, particularly across a gradient salmon. Evol. Appl. 1(2): 252–270. doi:10.1111/j.1752-4571.2008.00033.x. PMID: of local conditions (e.g., stream productivity). Prioritizing loca- 25567630. tions more resilient to climate change may also be warranted Daufresne, M., and Renault, O. 2006. Population fluctuations, regulation and (Palmer et al. 2009; Peterson et al. 2013). limitation in stream-living brown trout. Oikos, 113(3): 459–468. doi:10.1111/j. In addition to species management considerations, there is need 2006.0030-1299.14295.x. DeHaan, P.W., Schwabe, L.T., and Ardren, W.R. 2010. Spatial patterns of hybrid- to consider options to enhance the climate resilience of streams ization between bull trout, Salvelinus confluentus, and brook trout, Salvelinus For personal use only. supporting bull trout populations. Enhancing riparian conditions fontinalis in an Oregon stream network. Conserv. Genet. 11(3): 935–949. doi: to allow for increased shading and water storage (Caissie 2006)in 10.1007/s10592-009-9937-6. addition to novel approaches to increase groundwater contribu- Dunham, J.B., Adams, S.B., Schroeter, R.E., and Novinger, D.C. 2002. Alien invasions in aquatic ecosystems: toward an understanding of brook trout inva- tions (Pollock et al. 2014) should be evaluated as options for miti- sions and potential impacts on inland cutthroat trout in western North gating warming air temperatures. Preventing or prolonging stream America. Rev. Fish Biol. Fish. 12(4): 373–391. doi:10.1023/A:1025338203702. temperature increases may ultimately allow for bull trout to be- Dunham, J., Rieman, B., and Chandler, G. 2003. Influences of temperature and haviorally or physiologically adapt to changing climatic condi- environmental variables on the distribution of bull trout within streams at the southern margin of its range. N. Am. J. Fish. Manage. 23(3): 894–904. tions (e.g., Alvarez et al. 2006; but see Jonsson and Jonsson 2009). doi:10.1577/M02-028. Elliott, J.M. 1976. The energetics of feeding, metabolism and growth of brown Acknowledgements trout (Salmo trutta L.) in relation to body weight, water temperature and Funding for this project was provided by the US Geological ration size. J. Anim. Ecol. 45: 923–948. doi:10.2307/3590. Survey – USFWS Quick Response Program and Montana Fish Wild- Elliott, J.M. 1994. Quantitative ecology and the brown trout. Oxford University Press, New York. life and Parks. We thank Z. Shattuck (Montana Fish, Wildlife and Elliott, J.M. 2009. Validation and implications of a growth model for brown Parks) for reviewing and commenting on an earlier draft of this trout, Salmo trutta, using long-term data from a small stream in north-west manuscript and D. Isaak (US Forest Service) for assistance with England. Freshw. Biol. 54(11): 2263–2275. doi:10.1111/j.1365-2427.2009.02258.x. NorWeST temperature predictions. Any use of trade, product, or Elliott, J.M., and Elliott, J.A. 2010. Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: pre-

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