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HomeMy WebLinkAboutSUS5004TEMPERATURE PREFERENCE OF JUVENILE ARCTIC CISCO (COREGONUS AUTUMNALIS)FROM THE ALASKAN BEAUFORT SEA, IN RELATION TO SALINITY AND TEM PERATURE ACCLI~~TION by Robert G.Fechhelm LGL Ecological Research Associates,Inc. 1410 Cavitt Street Bryan,Texas 77081 William H.Neill Department of Wildlife and Fisheries Sciences Texas A&M University College Station,Texas 77843 and Benny J .Gallaway LGL Ecological Research Associates .Inc. 1410 Cavitt Street Bryan,Texas 77801 ..1 h lA flG I'~ _H;"riC 11"-' A N ,) 707 ;..SHiH AJ"C}1 C<AGE.AI(9'50 1 March 1982 2 ACKNOWLEDGEM ENTS We wish to express our gratitude to Dave Norton of the Outer Cont inental Shelf Environmental Asses sment Program's Arctic Projects Office (or his support during all phases of the research.Thanks are also extended to the members of the Waterflood Monitoring Program survey team --Bill Griffiths,Dave Schmidt,Brad Adams,Terry Carpenter,Rob Dillinger a nd Dennis Hensel --who provided the fish for the experiment; to Scott And erson for his statis tical a d vi ce ;to Chuck Davis for his help in c ons t r uc t i ng the test apparatus;to Bonnie Bower for drafting the figures;and to the s t a f f s of LGL Ecological Research Associates and LGL Alaska for their help a nd encourag ement. This study was funded partially by the Bureau of Land Management through i nt e ra g e ncy agr eement with the National Oceanic and Atmospheric Administration,as part of the Outer Continental Shelf Environmental Assessment Program. 3 ABSTRACT Ho ri z on t a l - t he rmal - gr ad i ent apparatus of previously undescr ibed design was used to d etermine the temperature preference of juven ile arctic cisco,(oreganus autumnalis,as a function of acclimation temperature and acclimation-test salin ity.Me an preferred t emperature ranged from 11.5 C for fish acclimated to 5 CI5 ppt to 15.4 C for t he 15 C/15 ppt acclimat ion group .Estima ted final temperature preferenda were 13.5 C at 30 ppt and 15.6 C at 15 ppt.Preferred temperatures at 5 and 30 ppt were lowe r (PeO.05)than that at 15 ppt .Qual ita tive observat ions of fish i n t he accl im at ion ta nks suggest ed that phys iolog ically optimal temperatures of j uvenil e arctic cisco also exceed 10 C over the salinity range of 5-30 ppt. These re s ul t s a re cons istent wi t h the summe r d ist ribut ion o f arctic c isco in the Ala s kan Beaufort S ea :fish c oncent r a t e near shore in a narrow band of relatively warm wat er of moderate sali ~ity . Key Wo rds :T emperature preference ,arctic cisco,Be a "fort Sea,salinity, summer d istr ibut ion,b ehavior. 4 INTRODUCTION The arctic cisco,Coregonus autumnalis,is one of the most abundant anadromous fishes in Alaskan arctic waters.From spawning areas in the Mackenzie River system (Hatfield et al.1972;O'Neill et al.1981)and possibly other major river systems of the North Slope region,juveniles migrate into the nearshore waters of the Beaufort Sea where they live during the ice-free period from mid-June to early Sept ember (Craig and "aldorson 1980).Freshwater runoff along with intense solar heating make these shallow coastal habitats relatively warmer and less saline than deeper offsho re waters (Truett 1980).Nearshore areas also serve as primary summer feeding grounds for arctic cisco due to shoreward and longshore transport of invertebrate-rich ocean waters (Griffiths and Dillinger 1980). The abundance of arctic cisco and other anadromous species in the warm-water areas during summer has prompted speculation as to the effects of temperature on the migration and distribution of these fishes.In response,we conducted a laboratory study of the temperature preference of juvenile arctic cisco as a function of both acclimation temperature and acclimation-test salinity.Although a multitude of temperature- preference data has been published (Coutant 1977),none is available for this species nor any other high-arctic coregoninc.Temperature preferences were measures in a horizontal-thermal-gradient apparatus of prev;ously undescribed design. 5 MATERIALS AND ~IETIlODS Arctic cisco (83-136 mm)were taken by fyke net from the Beaufort Sea near Prudhoe Bay ,Alaska,during July and August 1981.The fish were flown tl ·,day of their capture to a laboratory in Fai rb anks.Water temperature and salinity during transport and during an in ~tial 48-hour holding period at the laboratory were maintained at leVE ls similar to those recorded in the field at time and place of capture (i.e.,5-8 C and 10-25 ppt). Groups of 20-25 fish were held in 450-liter filtered aquaria under constant light.(At the latitude --approximately 700 N --and season of fish collection,day length was 24 hours.)Dechlorinated tap water RsupplementedwithInstantOcean salts was used in all phases of the experiment.Conditions of acclimation were organized in a 3x3 design salinities of 5,15 and 30 ppt (~2 ppt)versus temperatures of 5, 10 and 15 C (~0.5 C);however,owing to numerous logistical problems the 5 ppt/15 C acclimation group was never tested.Groups were brought to their specific acclimation conditions by incrementally adjusting temperature and salinity at the rates of 2 C/day and 5 ppt/day,respectively. Fish were maintained at their final acclimation levels for a minimum of ten days prior to testing.During the acclimation period they were fed to satiation 2-3 times daily on a mixture of commercial freeze -dried euphausids and brine shrimp.Once testing of a particular group began, fish were fed to satiation 20-30 minutes before the beginning of each I.emperature-preference trial. Fig.I Fig.2 6 Test Apparatus Horizontal thermal gradients were formed in an elongate chamber made from a 5-m length of transparent polyvinyl chloride (PVC)Excelon R pipe with an internal diameter of 102 mm.Lying within this primary structure,and extending its entire length along the bottom,were three smaller tubes --a 12.7-mm-diamter PVC pipe flanked b y two 15.9-mm-diameter titanium pipes (Fig.I).A 50-mm-wide slit in the top of the primary tube permitted the investigator free access to any portion of the chamber. Gradients were established by pump ing coolant (ethylene glycol) through one titanium pipe while simultaneously pumping hot water through the other in the opposite direction (Fig.I).This countercurrent arrang- ment for heat exchange was augumented by heterogeneous insula tion of the titanium pipes:the upstream third of each was bare;the second third was spirally wrapped with 6.4-mm-thick clear vinyl so that the proportion of bare conductive surface progressively decreased;and the downstream third was completely insulated with vinyl wrap.This system produced linear to slightly sigmoidal gradients as great as 18 C (Fig.2), with specific gradients obtainable through adjustments in the temperature and flow rate of the liquid within each heat exchanger.Compressed air, bubbled from the central PVC line via 0.5-mm holes at 20-cm intervals, prevented cross-sectional thermal variation in addition to providing aeration.A screen of plastic mesh prevented fish from contacting the heat exchangers and aeration pipe. Each of four such gradient tanks (mounted one above another )was marked off at intervals of 50 em,to g ive 10 stations.A copper-constantan thermocouple submerged at each station was int"rfaced with a Baily Instruments Inc.digital thermometer (Model BAT-12;display accuracy 7 0.1 C)to providp data on watpr temperaturp.Florescent light rpflected off a whltp backround pr~vidpd low-level,uniform illumination from the side of thp tank opposite the observer. Experimental Procedure A single fish was netted at random from the desired acclimation group and placed in a pre-formed gradient at the temperature corresponding with that of acclimation.The salinity in the gradient was homogeneous and equal to the accl imation salinity (~1 ppt).In order to accomodate initial disorientation that might have led to the fish rushing headlong into areas of stressful temperature,small blocking nets were placed in the gradient at points equivelent to the acclimation temperature ~3.0 C. The blocking nets were removed after 30 minutes and the fish was given an additional 90 minutes to habituate to the test apparatus.The fish's position in the gradient tank was then recorded in tenths of a division between each marked station (e.g.,1.6,3.7,etc.)every 2 .minutes for 60 consecutive minutes.Gradient temperatures were recorded at the beginning of each trial and after the 10th,20th and 30th observations. Temperature between adjacent thermocouples and between observations taken at a single thermocouple was assumed to vary linearly.Temperatures observed or calculated (if between the~mocouples)for each positional observation were tabulated and the median taken as the preferred tempera- ture for that par ticular trial.Frequency distributions based on tempera- ture (1 C increments)and position (50-cm increments)were also calculated. Fish from a particular acclimation group were tested in a minimum of two different gradient tanks which were oriented in opposite directions, and gradients within specific tanks were varied among trials in order to detect any bias,other than temperature,that may have affected spatial distribution.Analysis of var iance,Student's t test and Duncan's multiple-range test (Ostle and Mensing 197~)were used to evaluate d ifferences amoung acclimation groups. 8 Fig.3 Table 1 9 RESULTS Temperature Preference Trials Individual cisco tended to generate monomodal frequency distributions with respect to temperature.Strongly platykurtic distributions (i.e., those with a moment coefficient of kurtosis greater than 1.0 and position- ally covering more than 807.of the gradient)were removed from the data base because the median temperature in such cases more likely reflected the distribution of gradient temperatures than the fish's temperature preference.Most of the seven (of 110)trials that were rejected on this basis involved fish that appeared highly stressed and unable to adapt to the test apparaLus.The results of three other fish were also discarded because their distributions were sharply truncated at either end of the gradient. Plots of sample variance against standard fish length indicated that size had a negligible effect on temperature-frequency distribution. The possibility of temperature re-acclimation during the course of any experimental trial was discounted because examination of consecutive observations prov ided no indication of consistent drift in the t emperature at which fish were observed.Variation in preferred temperature among gradients and test tanks proved to be non-significant (P>O.10);therefore, data within acclimation groups were pooled for furthur analysis. Mean temperature preferendum ranged from a high of 15.4 C for fish acclimated to 15 C/15 ppt to a low of 11 .5 C for the 5 C/5 ppt acclimation group (Table I,Fig.3).Arctic cisco acclimated to 15 C preferred temperatures that were h igher (PCO.05)than those preferred by either the 5 C or 10 C acclimation groups;however,there was no significant ·.. 10 (P>O.OS)difference in thermal preference between fish acclimated to S and 10 C. The mean temperature preferendum was signifcantly (P<O.OS) higher than the temperature of acclimation in all groups with the exception of those acclimated to 15 C. The final temperature preferendum, de fined as the point at which the temperature-preference trendline in ~ersects the 4So diagonal (Fry 19 47),was graphically estimated to be lS .6 ~at IS ppt and 13.5 C ac 30 ppt (Fi g.3). Preferred temperatures at salinity extremes of Sand 30 ppt were lower (P<O.OS)than that at IS ppt (Fig.4). Behavioral Observations Behavior of the fish in the acclimation tanks suggested that physio- logically optimal temperatures exceed 10 C.Fish acclimated to 15 C appeared alert,perceptive and proved to be extremely elusive during capture attempts.When slowly pursued about the holding tank the majority of individuals tended to form cohesive,well-organized schools.Such characteristics suggest a rather sophisticated degree of both muscular and neurological capability consistant with a poikilotherm operating under optimal thermal conditions.Frenzied feeding activity and a comparatively high rate of food consumption (fish fed to apparent satiation act ively accepted food within two hours were undoubtedly linked to elevated metabolic rates induced by the high temperature.Of approximately 4S fish acclimated to IS C for a period of 10-20 days,the only fatalities involved individuals that jumped out of the holding tanks. Conversely,arctic cisco acclimated to S C appeared lethargic and lacked the locomotory agility noted in their IS C counterparts.Tenuous schools,consisting of loose aggre~ates of 6-8 individuals,persisted no longer than several seconds.Feeding behavior was casual,and thes~fish, 11 once satiated,refused food for at least the next 6-8 hours.A mor t al i ty rate of approximately 0.5 fish/day was noted in all of the 5 C acclimation groups. These qualitative differences were very apparent when co mparisons were made between the 5 and 15 C and between the 5 and 10 C acclimation groups.Differences between the 10 and 15 C groups were subtle except with regard to schooling behavior,which was substantially more conspicuous in the 15 C groups.There were no mortalities in the 10 C acclimation groups. Within temperature-acclimation groups,differences in performance among salinity groups were not detected. 12.,. DISCUSSION Thermal preferenda of arctic cisco varied between 11.5 and 15.4 C,depending on the temperature of acclimation and the salinity at which the fish were acclimated and tested.Given th~t p referred temperatures are typically highest for juveniles of a species (Coutant 1977)and under conditions that simulate summer photoperiod/seasonality (Sullivan and Fisher 1953;Zahn 1963),our results may represent maximum values o f temperature preference for arctic cisco. Current literature suggests,for f ish in general,a strong correl- ation between preferred temperature and the optimum for physiological performance (Brett 1971)in such terms as maximum potential for growt~ (Jobling 1981),maximum sustainable swi.nming speed (Fry and Hart 1949; Brett 1967),maximum distance moved as a result of electrical stimulation (Fisher and Elson 1950),and,most importantly,maximum scope for activity (Brett 1964;Beamish 1970a).Thermal optima reflect the com- bination of an underlying positive effect of temperature on biochemical reaL~ion rates and inherent physiological limitations (e.g.,increasing net cost of oxygen delivery)which come into playas temperature approaches the upper lethal limits of the organism.From this perspective the enhanced survival,schooling,feeding and locomotory performance noted in arctic cisco acclimated to 10 and 1~C qualitatively corroborate the thermal preferenda (11.5-15.4 C)determined from the gradient experiments. The tendency for arctic cisco to select highest temperatures at intermediate salinities is similar to that reported for the threespine stickleback,Gasterosteus aculeatus (Garside et al.1977).In the latter case,intermediate salinities were those isosmotic for the species, suggesting that thermoregulatory behavior may compensate for osmotic - 13 stress.The potential severity of such stress is indi cated by the obser- vations of Rao (1968):in terms of oxygen consumption,the cost of osmo- regulati on for rainbow trout (Salmo gairdneri)reached 20-274 of total metabolic demand as environmental salinity diverged from isosmocity. At salinity extremes,the selection of a lower temperature would reduce standard metabolism and partially offset the elevated oxygen demand created by o smotic loading.Higher oxygen concentrations at lower temperatures might also prove beneficial in supporting increased metabolism.Our experimental temperature gradients were accompanied by relatively linear dissolved oxygen gradients ranging from approximately 9 ~g02/liter at 20 C to 15 mg02/liter at 5 C.Farmer and Beamish (1969)likewise found that oxygen consumption rates for Tilapia nilotica were lowest under isosmotic conditions.Yet,this species,when acclimdted from 15 to 30 C,showed a preferred-temperature trend essentially opposite that of arctic cisco and threespine stickleback:selected temperatures were lowest at intermediate salin ities (Beamish 1970b).Such contrasting results lead one to consider the importance of habitat and niche diversity when assessing the species-specific effects o~temperature and salinity interactions. Regardless of the variat ion induced by salinity and acclimation t emperature,the selected temperatures.of juvenile arctic cisco either approach or exceed the upper limits of the thermal spectrum typically available to them during the summer season.Moderately saline (18-25 ppt),ne arshore waters of the Alaskan Beaufort Sea reach an annual max imum temperature of 10-12 C during the month of August (Craig and Haldorson 1980),although temperatures as high as 15 C have been reported (D.Schm idt, pers.corom.).Given these environmental conditions and the results of I 14 our gradient experiments,t emperature would seem to playa role in the summer distribution of this species.Valtonen (1970)presumed a similar role of thermal preference in the tendency of juvenile Coregonus nasus to occupy warm nearsho re waters along the coast of the Bay of Bothea, Finland. During the summer,arctic coastal waters not only prOVide the highest tempe ratures local ly a va i l a bl e ,but also generate intense trophic support for t he f ish species t ha t oc cupy them.This simultaneous occurence of elevated temperature and abundant forage no doubt confers an ecological advantage i n terms of grow th potential.Jobling (1981),using a n accumulation of publ ished data for 49 s pecies of fish,concluded that there is good correlation between prefe rred temperature and the temper- ature that promotes maximum growth.Assum ing this relationship holds for a r c t i c cisco,juven il es a r e ecologically and physiologically positioned to make optimal use of their limited feeding season. Although our expe riments implicate tempe rature as an environmental determinant in the summer distribution of arctic cisco,it is only one of many factors that can affect population movement .Variables such a s abundance of forage.shallowness of nearshore waters.substrate composition or the dynamics of coastal currents may compete directly with temperature in determining specific patterns of dispersion and migration.Laboratory st udies have d emonstrated that behavioral thermo- regulation in fishes can be modified by a variety of biotic and abiotic factors (Reynolds and Casterlin 1979).Yet,while the exact ecological role of temperature will depend upon temporal and spatial i nt eg r a t i on of both species and environmental characteristics,the strong thermal dependency of phys iological mecha nisms in fishp.s demands i t s serious ·.15 consideration.ln th e case of arctic cisco.pre ference for warm waters along the Beau fo rt Sea coast wou l d appear to be a sensible adaptive strategy in that it would enable them to realize their physiological potential and thereby maximize the probability of successfully coping with a rigorous environment. 16 LITERATURE CITED Beamish.F.W.H.1970a.Oxygen consumption of largemouth bass.Micropterus salmoides.in relation to swimming speed and temperature.Can.J. Zool.48:1221-1228. Beamish,F.W.H.1970b.Influence of temperature and salinity acclimation on temperature preferenda of the euryhaline fish,Tilapia nilotica. J.Fish.Res.Board Can.27:1087 -1093. Brett.J.R.1964 .The respiratory metabolism and swimming performance of young sockeye salmon .J.Fish.Res.Board Can.21:1183-1226. Brett.J.R.1967.Swimming performance of sockeye salmon.Onchorhynchus nerka.in relation to fatigue time and temperature.J.Fish.Res. Board Can.24:1731-1741. Brett.J.R.1971.Energetic responses of salmon to temperature.A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka).Am.Zool.11:99-113. Coutant.C.C.1977.Co~pilation of temperature preference data.J. Fish.Res.Board Can.34:739-745. Craig.P.C.and L.J.Haldorson.1980.Beaufort Sea barrier island-lagoon ecological processes studies:Final report.Simpson Lagoon.Part 4.Fishes.Fish.Res.Unit 467.In:Environmental Assessment Alaskan Continental Shelf.Final Report.BLM/NOAA,OCSEAP.Boulder,Colorado. 266 p. Farmer.G.J.and F.W.H.Beamish.1969.Oxygen consumption of Tilapia nilotica (L.)in relation to swimming speed and salinity.J.Fish. Res.Board Can.11:2807-2821. 17 Fisher,K.C.and P.F.El.on.1950.The selected temperature of Atlantic salmon and speckled trout and the effect of temperature on the response to an electrical stimulus.Physiol.Zool.23:27-34. Fry,F.E.J.1947.Effects of environment on animal acti~ity.Univ. Toronto Stud.Biol.,Ser.55;Publ.Onto Fish.Res.Lab.No.68.62 p. Fry,F.E.J.and J.S.Hart .1949.Swimming speed of goldfish at different temperatures.J.Fish.Res.Board Can.7:169-175. Garside,E.T.,D.G.Heinze and S.E.Barbor.1977.Thermal preference in relat ion to salinity in the threespine stickleback,Gasterosteus aculeatus L.,with an interpretation of its significance.Can. J.Zool.55:590-594. Griffiths,W.A.and R.Dillinger.1980.Beaufort Sea barrier island- lagoon ecological processes studies:Final report,Simpson Lagoon. Part 5 .Invertebrates.Fish.Res.Unit 467.In:Environmental Assessment Alaskan Continental Shelf,Final Report Principal Investigator.BLM/NOAA,OCSEAP.Boulder,Colorado 190 p. Hatfield,C.T.,J.N.Stein,M.R.Falk and C.S.Jessop.1972.Fish r esources of the Mackenzie River Valley.Vol.1.Dept.of the Environ.,Fish. Ser.Winnipeg,Manitoba.97 p . Jobling,M.1981.Temperature tolerance and the final preferendum - rapid methods for the assessment ~f optimal growth temperatures. J.Fish.BioI.19:439-455. O'Neill,J.,C.McLeod,L.Norton,L.Hildebrand and T.Clayton.1981. Aquatic investigations of the Laird River,British Columbia and Northwest Territories,relative to proposed hydroelectr ic development at site A.C&G Laboratories Ltd.,Edmonton,Alberta.122pp. Ostle,B.and R.W.Mensing.1975.Statistics in Research.Iowa State University Press.Ammes Iowa.596 p. 18 Rao,G.H .H.1968.Oxygen consumption of rainbow trout (Salmo gairdneri) in relation to activity and salinity.Can.J.Zool.46:781-786. Reynolds,W.'!.and H.E.Casterlin.1 979.Behavioral thermoregulation and the "final preferendum"paradigm.Amer.Zool.19:211-224. Sullivan,C.H.and K.C.Fisher.1953.Seasonal fluctuations in the selected temperature of speckled trout,Salvelinus fontinalis (Hitchell). J.Fish.Res.Board Can.10:187-195. Truett,J.1980.Beaufort Sea barrier island-lagoon ecological processes studies:Final report,Simpson Lagoon.Part 2.Physical processes. Fish.Res.Unit 467.In:Environmental Assessment Alaskan Continental Shelf,Final Report,Principal Investigator.BLH/NOAA,OCSEAP. Boulder,Colorado.51 p. Valtonen,T.1970.The selected temperature of Coregonus ~(Pallas) sensu Svardeon,in natural waters compared with some other fishes, p.347-362.In:D.C.Lindesy and C.S.Woods (eds.).Biology of coregonid fishes.Univ.Hanitoba Press,Winnipeg. Zahn,H.1963.Jahreszeitliche Veranderungen der Vorzugstemperaturen von Scholle (Pleuronectes platessa,Linne.)und Bitterling (Rhodeus sericeus Pallas).Verhandl.Dtsch.Zool.Ces.Huenchen p.562-580. • 19 Table 1.Mean preferred temperature ~1 standard error (sample size)for arctic cisco acclimated to various combinations of temperature and salinity. ACCLIMATI ON ACCLIMATI ON TEMPERJ.TURE (oC) SALINITY (ppt)5 10 15 5 11.5 ..0.7 (12)12.8 ..0.6 (15) .Hl 1°,13 .7 ..0.5 (10)13.8 ..0.4 (14)15 .4 ..0.4 (16)- 3 0 12 . 8 ..0 . 7 (i i)12.7 ..0.6 (12)14.1 .. 0 .9 (10) 20 FIGURES Fig ure 1.Schematic representation of one of the thermal gradient systems (above )and a cross -sectional v iew of a grad ient tank (below). F igure 2.Water temperature versus location (at 50 cm intervals)for a typical horizontal thermal gradient. Figure 3 .Preferred temperature (~1 SE)versus acclimation temperature for acclimation-test salinities of 5 ppt (dotted line),15 ppt (dashed line)and 30 ppt (solid line). Figure 4.Preferred temperature (~1 SE)versus accllmation-test salinity for acclimation temperatures of 5 C (dashed l ine),10 C (solid line)and 15 C (dotted line). ,". I Hot I ......SfIReservoirI ! ®-,-.,- ••Air., t !S I Cold I +--I Reservoir I Plastic Mesh PVC Air Line Titanium Heat Exchangers 20 0 0 I CD 15 "-~... CO"-CD 10Q. E ~ 5 , 0 1 2 3 4 5 6 7 8 9 10 Location 20 0 18 °I 16 Q)--...--:::l 14 ~------------~ tV...12 ...........................Q) c. E 10t! 8 -c Q)6...... Q)....4Q)...a.2 o 2 4 6 8 10 12 14 16 18 20 Acclimation Temperature -"C II)I I I I I I I I I C?...C1. L -0 C1.-C?I I I I II):~.I -~.. I N ..- I ,: I ..---I I~ --0 (I) N ....en-~~:::1 -II)I~.... •\C\0\0 .--\-...... \....,~ \,- \,=\..- ....1-.\----II)(,) (,)<C I •••I •••• 0 en CO ~N 0 en CO ~N 0 N .................... 00 -aJnJeJadwa.l paJJaJaJd