Thermal performance of larval longfin dace (Agosiachrysogaster), with implications for climate change

Matthew J. Troia & James E. Whitney & Keith B. Gido

Received: 25 November 2013 /Accepted: 28 April 2014# Springer Science+Business Media Dordrecht 2014

Abstract Temperature is an important factor affectingthe distribution of freshwater fishes. The longfin dace(Agosia chrysogaster) is endemic to the Gila River basinof the southwestern USA and northern Mexico andoccupies a range of thermal environments from coolmountain tributaries to warm desert rivers but informa-tion about its thermal biology is limited, particularly forlarvae. We quantified the effect of rearing temperatureon survival, growth capacity, and critical thermal max-imum (CTM) of larval longfin dace. Broodstocks oflongfin dace were collected from two sites in the upperGila River in New Mexico from which larvae werehatched and reared for 22 days in indoor aquaria atconstant temperatures ranging from 18.0 to 31.0 C.Growth capacity peaked at 27.0 C and was 21 % great-er for larvae hatched from the upstream compared to thedownstream broodstock, indicating intraspecific vari-ability in growth capacity. CTM increased with rearingtemperature and ranged from 33.9 to 39.9 C, indicatingthat thermal acclimation influences maximum thermaltolerance. CTM and acclimation response ratio of larvaeare lower than those of adult longfin dace measured in aprevious study, suggesting that larvae are more sensitiveand less responsive to thermal stress than adults. Watertemperatures in 2012 from six sites in the upper GilaRiver basin did not exceed 27.0 C and larval growthcapacities in May of 2012 ranged from 5 to 28 % of themaximum growth capacity. We assert that rising

temperatures may increase larval growth rates, althoughthis will depend on resource limitation and shifts incommunity interactions.

Keywords Growth capacity . Critical thermalmaximum .Thermalacclimation .Larval fish .GilaRiver

Introduction

Temperature exerts a strong influence on the physiolo-gy, life history, population dynamics, and distribution offreshwater fishes (Brett 1956; Myrick and Cech 2000).Maximum temperature tolerance, measured as criticalthermal maximum (CTM), is probably the most studiedaspect of thermal biology because its effect on survivalis direct and acute (Lutterschmidt and Hutchison 1997;Beitinger et al. 2000). In temperate streams, speciesexhibit innate differences in maximum thermal toler-ance, which constrain their distribution along the rivercontinuum (Rahel and Hubert 1991). Individuals of thesame species can also differ in maximum thermal toler-ance stemming from reversible (Bennett and Beitinger1997; MacNutt et al. 2004) or non-reversible (Kinne1962; Schaefer and Ryan 2006) acclimation as well asgenetically-based local adaptation (Otto 1973; Fangueet al. 2006). Maximum thermal tolerance can also in-crease with age (Hokanson et al. 1973), but this aspectof thermal tolerance has been assessed in a limitednumber of species (Rombough 1997).

Thermal performance of a species can be character-ized as a thermal reaction norm that describes a change

Environ Biol FishDOI 10.1007/s10641-014-0270-7

M. J. Troia (*) : J. E. Whitney :K. B. GidoDivision of Biology, Kansas State University,116 Ackert Hall, Manhattan, KS 66506, USAe-mail: troiamj@ksu.edu

in a physiological rate or behavior along a gradient oftemperatures (Angilletta 2009). Because physiologicalrates and behavior vary over a range of non-lethal tem-peratures and these performance differences can influ-ence ecological processes (e.g., Taniguchi and Nakano2000), characterization of thermal optima andbreadths of ecologically-relevant physiological andbehavioral traits is crucial for understanding thedistribution of species across thermally-variablelandscapes. For example, feeding rate is a com-monly measured thermal reaction norm for fresh-water fishes because it is a practical surrogate forestimating energetic requirements (Alvarez et al.2006). Metabolic rate and growth capacity areinformative thermal reaction norms for testing evo-lutionary hypotheses such as countergradient vari-ation (Schaefer and Walters 2010; Baumann andConover 2011) and macroecological theories suchas the metabolic theory of ecology (Brown et al.2004; Schaefer 2012). Thermal reaction norms ingrowth rate of larvae also are ecologically mean-ingful because larval survival can drive populationdynamics of many freshwater fishes (Velez-Espinoet al. 2006; Piffady et al. 2010). Larval fish thatgrow faster are more resistant to starvation (Einumand Fleming 1999), able to exploit a broader arrayof food resources (Wankowski 1979), and avoidsize-limited predators (Werner and Gilliam 1984).

Characterization of thermal tolerance and reactionnorms of fishes is necessary to predict effects of risingwater temperatures due to anthropogenic climate(Morgan et al. 2001; Caissie 2006) and land cover(LeBlanc et al. 1997) change. This is particularly im-portant in arid regions where, in addition to rising airtemperatures, reduced flows will further increase ther-mal maxima and variability in streams. Much of thearid southwestern United States is drained by theColorado River and its major tributaries, includingthe Gila River. This region contains many endemicfishes that are imperiled due to fragmentation, flowalteration, and the presence of non-native species(Minckley and Deacon 1968; Pool and Olden 2011).Several studies that characterized the acute maximumthermal tolerances of Colorado River fishes provide abasis for predicting how species will respond to al-tered thermal regimes (Otto 1973; Deacon et al.1987). Carveth et al. (2006) measured maximum ther-mal tolerance and acclimation response ratio (a mea-sure of thermal acclimation) of ten native and four

non-native species and found that these thermal per-formance metrics were variable among species butwere not significantly greater for native compared tonon-native species, indicating that native desert fishesare not necessari ly more resistant to risingtemperatures. Other studies have compared growthand survival rates of native Colorado River fishesexposed to chronic temperature differences. Forexample, Widmer et al. (2006) showed that survivaland growth of loach minnow (Tiaroga cobitis) over30 days was suppressed at temperatures above28.0 C, but mortalities occurred when temperatureswere above 30.0 C. Few studies have evaluated thethermal performance of larval desert fishes (but seeBestgen 2008), despite the influence of this life stageon population dynamics (Velez-Espino et al. 2006;Piffady et al. 2010).

We studied lethal and non-lethal aspects of the ther-mal biology of the longfin dace (Agosia chrysogaster,Girard 1856), a cyprinid endemic to the lower ColoradoRiver basin. This species occupies a variety of habitatsalong the river continuum, from high-gradient mountaintributaries to low-gradient desert river mainstems(Minckley and Barber 1971). As a stream-size general-ist, they experience a range of thermal environments,making the study of its thermal biology informative forpredicting distributional responses to rising tempera-tures. Longfin dace also influence ecosystem prop-erties, excreting up to 10 % of the nitrogen that istaken up by algae (Grimm 1988), which makes thestudy of their physiology and distribution relevant tothe understanding of desert stream ecosystems.Previous investigators reported maximum thermaltolerance and plasticity (due to thermal acclimation)in thermal tolerance of adult longfin dace from atributary of the Gila River in Arizona (Carveth et al.2006); however, the thermal performance of larvaeand temperature dependence of other performancemetrics of longfin dace remain unknown. We hadthree objectives for this study: (1) measure thermalreaction norms in larval survival and growth capac-ity to characterize the thermal optimum and breadth,(2) measure CTM of larvae reared at a range oftemperatures to test for plasticity in maximum ther-mal tolerance due to acclimation, and (3) comparethermal optimum to stream temperature regimesthroughout the upper Gila River basin to predictpotential changes in larval performance in responseto rising stream temperatures in the future.

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Methods

Study area, collection of broodstock, stream temperaturedata

We collected broodstocks of adult (>50 mm totallength) longfin dace from two sites on the mainstemof the upper Gila River in southwestern, NewMexico. The upstream broodstock collection site(1,329 m above sea level) is located 20.1 river kmfrom the downstream broodstock collection site(1,239 m above sea level) (Fig. 1). We used a seineto collect 18 to 25 individuals from each site between18 and 22 March 2013. Adults were transported tothe experimental stream facility at Konza PrairieBiological Station in Kansas, USA and housed inexperimental stream channels (see Matthews et al.2006 for description of experimental stream

channels). Spawning occurred between 26 and 30April 2013 and hatched larvae were removed fromexperimental stream channels on 1 May 2013 andtransported to an indoor laboratory at Kansas StateUniversity in Manhattan, Kansas where growth ca-pacity and thermal tolerance experiments were car-ried out.

Stream water temperature was recorded every hourfrom January 2012 to January 2013 at six sites withinthe distributional limits of longfin dace that ranged inelevation from 1,360 to 1,735 m above sea level (Parozet al. 2006; Whitney 2010). These temperature record-ing sites are located upstream of the two broodstockcollection sites, with three located on the Gila Rivermainstem (hereafter Mainstem-Up, Mainstem-Mid,and Mainstem-Down) and three located on tributaries(hereafter West Fork, Middle Fork, and East Fork)of the Gila River (Fig. 1).

Fig. 1 Upstream (open circle)and downstream (filled circle)broodstock collection sites oflongfin dace (Agosiachrysogaster) and locations ofthree tributary (open squares) andthree mainstem (closed squares)temperature recording sites fromthe upper Gila River insouthwestern New Mexico. Grayshading indicates extent of theGila River Basin and dashed boxindicates the upper Gila River andextent of the inset map

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Experimental procedures

Growth capacity and survival We measured growthcapacity as the temperature-specific growth rate at un-limited feeding conditions (Baumann and Conover2011). At the start of the experiment, a subset of 12 to15 larvae from each broodstock were euthanized with alethal dose of MS-222 (tricaine methanosulfonate) andpreserved in 5 % buffered formalin to estimate startingbody size. From each broodstock, ten larvae were rearedin aerated 2 L aquaria that were incubated in 75 L waterbaths maintained at 18.0, 20.4, 21.5, 23.1, 23.7, 25.4,26.4, 28.8, 29.4, or 30.1 C. Larvae were fed an excessof live brine shrimp nauplii (Ocean Star International,Inc., Snowville, UT) twice per day (08:00 and 20:00 h)for 22 days. Unconsumed food and waste were siphonedand a 50 % water change was conducted once per day(08:00 h). We measured the proportion of individualssurviving in each replicate aquarium after 22 days.Following the 22-day growth capacity experiment, asubset of five to seven individuals were retained formeasurement of CTM and remaining individuals wereeuthanized and preserved in formalin. Preserved speci-mens were eviscerated, padded dry with a paper toweland weighed to the nearest 0.1 mg. Daily growth rate ofeach individual was calculated as the eviscerated wetmass on day 22 minus the mean eviscerated wet mass ofindividuals euthanized at the start of the growth capacityexperiment divided by 22 days.

Acute thermal tolerance We measured CTM using theloss of righting response (Lutterschmidt and Hutchison1997). Following the 22 day growth capacity experi-ment, temperatures in all aquaria were equilibrated to24.0 C for 36 h to minimize the effect of acute thermaland handling stress on CTM measurements. Fish werealso fasted for 36 h prior to trials. Five to seven individ-uals from each temperature treatment were selected torepresent the range of body sizes present in each aquar-ium, allowing us to statistically control for the potentialeffect of body size on CTM. Each test individual wasplaced in a 70 ml cup that submerged in an 18 L waterbath and heated at a rate of 0.7 Cmin1 starting at24.0 C. Oxygen concentrations were measured at alltemperatures with a dissolved oxygen probe (YellowSprings Instruments, Yellow Springs, Ohio, USA) andremained >98 % saturated throughout the duration ofeach trial. The temperature at which individuals lostrighting response was recorded and test fish were

immediately removed, euthanized, preserved, and latereviscerated and weighed for body size.

Data analysis

We used growth capacity of the largest individual fromeach aquarium as the maximum growth capacity foreach temperature treatment. To characterize the tem-perature dependence of maximum growth capacity,we used nonlinear least squares regression with a 3parameter Gaussian function (Eq. 1).

growth capacity B e temperatureA 2=2C2 1

This method allows for the estimate of the optimaltemperature (A), maximum performance at the optimum(B), and the breadth of performance (C), and is usefulfor characterizing thermal reaction norms in physiolog-ical processes (Angilletta 2009; Schaefer 2012).Parameter estimates and non-overlapping standard er-rors were used to infer statistically significant differ-ences in optimum growth capacity and maximumgrowth capacity between larvae from the upstream anddownstream broodstocks.

We combined data from the two broodstocks andused linear regression to test for a relationship betweenrearing temperature and two response variables: survivaland CTM. If significant linear relationships were detect-ed, we used analysis of covariance (ANCOVA) to testfor differences in slopes and y-intercepts betweenbroodstocks. Lastly, we calculated the acclimation re-sponse ratio (ARR), which is the slope of a linearregression equation describing the relationship betweenacclimation temperature and CTM. ARR is an index ofthe capacity for thermal acclimation with higher valuesindicating greater ability to acclimate to changing tem-peratures (Claussen 1977).

We used the experimentally-derived thermal reactionnorms in growth capacity and streamwater temperaturesfrom the six temperature recording sites to estimate thepotential larval growth capacity throughout the GilaRiver basin and compare these estimates to theexperimentally-derived optimum. The spawning seasonof longfin dace lasts fromDecember to July and peaks inApril (Lewis 1978), so we calculated mean daily watertemperatures from 1 to 31 May 2012 at each of the sixtemperature recording sites as an estimate of typicalrearing temperatures for larvae. Daily increase in larvalbody mass was calculated from the mean temperature of

Environ Biol Fish

each day in May 2012 using the 3-parameter Gaussianfunctions fit to the thermal reaction norm in growthcapacity. These daily growth rates were summed forMay 2012 at each temperature recording site (hereafterTotal May Growth). We estimated Total May Growthusing the Gaussian functions from the upstream anddownstream broodstocks to explore the range of growthrates stemming from variability in growth capacity be-tween broodstocks.

Results

Growth capacity and survival

Mean larval body size at the start of the experiment forthe upstream (1.32 mg) and downstream (1.26 mg)broodstocks were not significantly different (t-test;t21=0.58; P=0.57). Mean larval body size after 22 daysranged from 26.0 to 141.1 mg for the upstreambroodstock collection site and 24.3 to 124.2 mg for thedownstream broodstock collection and did not differ

significantly between broodstocks (t-test; t19=0.73;P=0.48). Fitted 3-parameter Gaussian functions in-dicated statistically significant relationships betweenrearing temperature and maximum growth capacityfor the upstream (non-linear least squares regression,R2a=0.89, P

Fig. 4 Total growth capacity of larvae estimated for May 2012 atsix temperature recording sites in the upper Gila River basin. Totalgrowth is the summed estimate of daily growth which was calcu-lated from mean daily water temperature at each temperaturerecording site and the experimentally-derived 3-parameter Gauss-ian functions fit to the thermal reaction norms in growth capacityfrom the upstream (open bars) and downstream (filled bars)broodstock collection sites. Sites are ordered from highest (top)to lowest (bottom) elevation. See Fig. 1 for locations of tempera-ture recording sites

Fig. 5 Relationship between rearing temperature and CTM (mea-sured as loss of righting response) of 22 day old longfin daceacclimated at 24.0 C for 36 h. Open and closed circles representprogeny from individuals collected from the upstream and down-stream broodstock collection sites, respectively. The solid linerepresents a best fit line for both populations and the slope repre-sents the acclimation response ratio (ARR)

Fig. 3 Mean daily water temperature for 2012 at (A) three tribu-tary and (B) three mainstem temperature recording sites inthe upper Gila River basin. The dashed line indicates

experimentally-derived optimum for larval growth capacity.See Fig. 1 for locations of temperature recording sites

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Mean daily water temperature in 2012 reached amaximum of 26.1 C in the Middle Fork of the GilaRiver, whereas mean daily water temperature in 2012 atthe West Fork reached a maximum of only 22.8 C(Fig. 3). Mean daily water temperature in May of 2012ranged from 15.3 C in the West Fork to 19.1 C in theMiddle Fork. Total May Growth ranged from 15.3 mgand 9.2 mg (based on equations derived from upstreamand downstream broodstocks, respectively) in the WestFork to 46.3 mg and 39.9 mg in the Middle Fork. Bycomparison, Total May Growth at the experimentally-derived optimum (27.0 C) would be 193.4 mg and162.7 mg based on equations from the upstream anddownstream broodstocks, respectively (Fig. 4).

Acute thermal tolerance

CTM increased with rearing temperature and rangedfrom 33.9 to 39.8 C (Fig. 5). Because CTM was sig-nificantly correlated with body size (linear regression;R2adj=0.27; P

acclimated at 25.0 C and 30.0 C were 38.2 C and40.5 C, respectively (Carveth et al. 2006). LowerCTMs in our study could stem from the earlier devel-opmental stage evaluated in our study compared to thatof Carveth et al. (2006). In other temperate freshwaterspecies, larvae exhibit reduced thermal tolerance com-pared to juveniles and adults due to a limited ability toacclimate metabolic rates (Hokanson et al. 1973;Rombough 1997). Acclimation response ratio was alsolower for our New Mexico population (0.37) comparedto the Arizona population (0.44) (Carveth et al. 2006),which supports the prediction that larvae are less respon-sive to temperature changes than adults (Hokanson1973; Rombough 1997). Alternatively, lower CTMs inour study could be due to local adaptation to lowertemperatures in the higher elevation populations ofNew Mexico compared to Arizona (Fangue et al.2006) or differences in rearing temperatures experi-enced by test fish between these two studies (Schaeferand Ryan 2006). The contribution of these alternativeexplanations cannot be tested independent of age, usingthe currently available information.

Longfin dace in our study were variable in thermaltolerance (CTM), which was related to the differenttemperatures experienced during the 22-day rearing pe-riod. Do these findings suggest that longfin dace atcolder sites (e.g., West Fork) are more susceptible toshort term (i.e., several days to weeks) temperaturefluctuations compared to those at warmer sites (e.g.,Middle Fork)? This depends on the relative contributionof reversible acclimation versus non-reversible (i.e.,developmental) acclimation to the variation in CTM thatwe observed (Schaefer and Ryan 2006; Angilletta2009). If non-reversible acclimation is the overridingcause for the positive relationship between rearing tem-perature and thermal tolerance, then fish reared at lowtemperatures would be susceptible to short term temper-ature fluctuations that surpass the CTM because theirability to acclimate to rising temperatures over thecourse of several days would be limited. By contrast,if acclimation is reversible, then fish reared at lowtemperatures would acclimate to short- termtemperature increases and would not be as vulnerableto thermal stress. Schaefer and Ryan (2006) measuredthe independent effects of reversible and non-reversibleacclimation in zebrafish (Danio rerio) and demonstratedthat reversible acclimation has a stronger effect on CTMthan does non-reversible acclimation. Therefore, if thisphenomenon is general among cyprinids, it is likely that

the majority of variation in thermal tolerance of larvallongfin dace in this study was due to reversible accli-mation (regardless of the thermal environment in whichthey developed), which would buffer longfin dace fromshort-term temperature fluctuations.

Implications for environmental change

Anthropogenic environmental change including chang-es in riparian and catchment land cover, surface waterdiversions and impoundments, and rising air tempera-tureshas and will continue to increase the tempera-tures of freshwater habitats worldwide (Poole andBerman 2001). With regard to stream fish responses toclimate change, much focus has been placed on thepotential negative effects on cold-water species such assalmonids that occupy high elevation streams in westernNorth America (MacNutt et al. 2004; Wenger et al.2011). Comparatively less is known about the potentialresponses of cool- and warm-water stream fishes towarming (but see Buisson et al. 2008). Lyons et al.(2010) used species distribution models to forecast thedistributional changes of stream fishes in Wisconsinunder several warming scenarios and predicted that allcool-water species will decline in distribution whereaswarm-water species may increase or decline. Our resultspredict that warming will increase larval growth capac-ity of longfin dace because current water temperaturesthroughout the upper Gila River basin never exceededtheir optimum of 27.0 C during 2012. Thus, human-induced warming would increase growth capacity oflarval longfin dace. If food is not limiting, faster growthshould transmit to increased population-level perfor-mance because larval growth capacity often is positivelyassociated with age-0 recruitment (Wankowski 1979;Werner and Gilliam 1984; Einum and Fleming 1999)and intrinsic rate of population increase (Velez-Espinoet al. 2006; Piffady et al. 2010). From the perspective ofacute thermal tolerance, it appears unlikely thatwarming will negatively impact longfin dace in theupper Gila River basin because water temperatures dur-ing 2012 did not approach CTM, regardless of therearing temperature. We also show that longfin dacehave greater acclimation potential than other desert fish-es (Carveth et al. 2006), which suggests that plasticitymay act as a stronger buffer against the negative impactof rising temperatures for this species compared to othernative and non-native fishes of the desert southwest(Culumber and Monks 2014). Increasing stream

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temperatures are likely to result in complex changes incommunity level processes such as resource abundance,competition and predation (Davis et al. 1998).Nevertheless, with all else equal, warming should gen-erally favor longfin dace in the upper Gila River basin.

Acknowledgments We thank Josh Perkin for assistance with fieldcollections, Michael Denk and Rebecca Zheng for assistance withexperimental procedures and data collection, and Jake Schaefer forassistance with experimental design. The Konza Prairie BiologicalStation provided use of the experimental stream facility. This researchwas funded by theNational Science Foundation (DEB#1311183), theSouthwestern Association of Naturalists, Prairie Biotic Research Inc.,the Kansas Academy of Science, and the Bureau of ReclamationWater Smart program. Longfin dacewere collected and housed underthe permission of the New Mexico Game and Fish Department(permit #3351), Konza Prairie Biological Station (permit ID#221)and the Institutional Animal Care andUse Committee (permit #2996)

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Thermal performance of larval longfin dace (Agosia chrysogaster), with implications for climate changeAbstractIntroductionMethodsStudy area, collection of broodstock, stream temperature dataExperimental proceduresData analysis

ResultsGrowth capacity and survivalAcute thermal tolerance

DiscussionGrowth capacityAcute thermal toleranceImplications for environmental change

References