th Microstructure nd the Growth of nc~rhynehus ke under Different

Prey ~ations"

Eric C. Volk, Robert C. Wissrnar, Charles A. Simenstad, and Douglas M. Eggers Fisheries Research Institute, University of Washington, Seattle, IVA 98 7 95, USA

Volk, E. C . , R. C. Wissmar, C. A. Simenstad, and D, M. Eggers. 1984. Relationship between ototith micro- structure and the growth of juvenile chum saErnon (Qncorhynchus keta) under different prey rations. Can. 8 . Fish. Aquat. Sci. 41: 126-733.

Effects of different prey taxa and daiiy ration levels on fish growth and the relationship between fish growth sate and mean otolith increment width were investigated for juvewiie chum salmon (Qncohynchus keta) ir% saltwater aquaria. Growth was positively correlated with ration, and food conversion efficiency was much higher for fish fed the harpacticsid cspepod, Tigriopus caBiPorni~us, than either the calanoid cope- pod, Pseudoca8anus minutus, or the gammarid amphipod, Paramsera mmohri0 Otolith increments were produced daily for at least the first 160d after hatching and there was a direct relationship between mean daily otolith increment width and fish growth rate. These results illustrate the possibility that otolith microstructure recapitulates juvenile churn growth histories during estuarine residence.

O n a etudic.5 Ies effets de diffkrents taxons de proie et des rations alimentaires quotidiennes sur la crois- sance des poissons ainsi que la relation entre le rythme de croissance des poissons et la largeur rnoyeone de I'accroissernent des otolithes pour de jeunes saurnons ketas (Oncorynchus keta) gardes dans des aquariums alimenttis en eau sal&e. On a trouv6 une correlation positive entae la crsissance et la ration akirnentaire ; en outre, la transformation de la nlourriture 6tait beaucoup plus efficace pour les psisssns nsurris du cspepode karpacticoi'de, Tigriopus cajifomicus, qtle du coptipode caIanoi.de, Pseudocabanus minutus, ou de Ifampkipode du groupe des gammarid&, Paramsem mohPi. II y a eld accroissement des otolithes chaque jour pour au rnoins [es 168 premiers joksrs apes ['6slosir~n et il y wait une relation direct@ entre la [argeur moyenne quotidienne de I'accrsissement des otolithes et ie rythme de crsissance des poissons. Ces r&su!tats indiquent la pcsssibilite que la microstructure des otoiithes recapitule Ifhistoire de la croissance des jeunes saurnans au tours de leur sejour dans Ees estuaires.

Received january 331, 198.3 Accepted September 23, 7383

pibenthic hqacttcoid copepods represent the predsrni- nant prey for 48-70 million juvenile (30-50 mm fork length) chum salmon (B~acsrhynch~s keta) early in their outmigation though estuaries of Puget Sound, with

gammarid amphipds second in importance (Simenstacl et al. 1982b). Simenstad and Salo (1982) found that large depressions En epibentkic zooplankton abundance during this salmon out- migration through Hood Canal appeared coincident with mas- sive hatchery releases sf chum and that the estuarine residence time of these juvenile fish was inversely related to prey abundance. They suggested that insufficient zoop%anktora prey limit the production of sdmsn in the estuary.

However, our ability to evaluate estuarine growth and residence time of Juvenile salmon has been ~aditionalky hindered by inadequate methods, particularly fm the smaller juvenile chum salmon. The commonly used mark and recapture method of estimating juvenile salmon growth rates (Bax and Mitrnus 198 1) suffers from several drawbacks that can severely reduce the accuracy of growth estimates: ( 1 ) possible tagging effects on fish growth, (2) the need to mark huge numbers sf fish ts obtain significant recaptures, (3) size-related rnsrta%ity be-

%20ntributisn No. 644, School of Fisheries, University s f Washing- ton, Seattle, WA 98195, USA.

tween marking and recapture of a group. and (4) the need for reasonably long periods between marking and recapture.

An alternative method for deteminiang the growth rates sf juvenile fish is the use of perisdie patterns in their otoliahs (or ear stones). (In this paper, otolith refers to the sagittae, the largest pair of calcareous otic elements found in the sacculus of the membranous labyrinth.) Daily increments in fish otoliths have been shown for a variety of marine and freshwater species (Brothers et a%. 1996; Taubert and esble 1977; Marshall and Parker 1982; Neilson and Geen 1982; and others), and otolith development has been demonstrated to be proportional to fish growth (Ralstsn 1976; Blacker 1974; Marshall and Barker 1982; and others). Growth rates can be calculated using otolith size-fish size and fish size-age relationships (Ralstsn 1976; Struhsaker and Uchiyama 1878; Wilson and Larkin 1982). The major advantage s f this method is its direct application to individual fish, which provides infomation on variation in a fish's growth, while eliminating the bias imposed by size- selective mortality. Second, this method reduces the number of samples required to estimate growth rates fmm size-frequency dishbutions. This paper reports laboratory experiments that examined the relationship between changes in otolith increment width and juvenile chum salmon growth rates under varying regimes of prey ration and taxa.

126 Can. 9. Fish. Aquar. Scd., Voi. 48, 1984

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Materials and Methods Aquhum Experiments

growth obsewed in that week. The large difference between actual and prescribed rations for Tigriopus was due to an emor in the initial dry weight deteminaatisn for Tigriopu~.

The effects sf rev ration and tawa on chum growth were A d 61

investigated in saltwater aquaria. Ten-litre plastic aquaria were connected in series to the University of Washington Friday Harbor Laboratory's (San Juan Island, WA) seawater system and maintained ~ u t d ~ o r s in the shade. In-line Nitex filters (225 pm) prevented the inQoduction of exBanesus prey organisms and prey from escaping the enclosures. Physicd conditions were ambient over the 8-wk exp~menta l period (March-May); temperature averaged $ .9 2 0.52"C (range '3.6-10.2"C) and salinity averaged 32.7 k 0.54%~ (range 29.8-33.6%~).

Churn salmsn hatched in egg boxes from Bevertsn Creek, %an Juan Island, were transferred directly to full-strength seawater after yolk absorption and fed ad libitum on Oregon Moist Pellets@- For 3 d prior to the initiation of experiments they were fed their respective prey organisms. Prey species used in this study were the calaaoid copepod, ~seudockaiareus minufus (35 % -500 pm) , the epibenthic hqacricoid capepod, Tigtiopus cal$~micus (35 1-500 pm), and the gammarid amphipod, Pammoera mohri (500- 1000 pm). Details sf their collection, culture, and characteristics were presented in %amenstad et aB. (1982a). During the experiments these fish were fed the three experimental prey species at four different ration levels. Akl treatments contained five fish per tank except for the high ration levels, which, due to the number of prey wecessq to support such high rations, contained two fish per tank. Fish were fed once each day at 14:00 for a period of 8 wk.

The prescribed daily ration levels within each prey category were 1 , S , 10, md 20% of the fish's body weight (% b.w. - k p - ' ) .

Live fish were weighed each week in water-filled weigh plans to update rations. Excess water cmied by the fish to and from the balance was estimated by weighing 38 live fish and comparing their live determined weights with their dead wet weights, with excess water blotted away. This produced a correction factor of 0.79 X ""Eve weight," which was applied to experimental fish ts estimate dead wet weights. Multiple live weighings of 10 individuals produced coefficients of variation not exceeding 1 % and deviations from dead wet weight not exceeding 7%. Since fish were not individually identified, weekly weights were averaged over all fish in a treatment. Prey dry weights were determined by drying Iarge samples sf each at WO°C for 48 h, thereby allowing the calculated ration weights ts be sonve~ed to prey number. Counts of Tigriogus and Pseudocalanus were estimated using v ~ l u ~ ~ ~ e t r i c extrapolation of sample counts from cultures, and Pas-amoera were counted directly. Coefficients s f variation for prey counts never exceeded 15%.

To calculate rations, both fish and prey had to be expressed in terns of dry weight, since wet weights of prey proved highly variable and impractical. To estimate fish dry weights, a sansple s f 30 fish sf a wide size range was weighed and then dried at 80°C for 48 h to obtain a conversion factor from wet to dry weight (8.21 x wet weight). We realize that the actual dry weights of the experimental fish would be somewhat different among fish at different ration Bevels (Brett 1979) but feel that they represent reasonable approximations for ration detemina-

Otolith Analyses

Juvenile chum salmon for otolith analyses originated from the Washington Depafiment of Fisheries hatchery at Hoodspo~, Washington, Beveflon Creek egg boxes, and the growth expe~ments described above. Fish not in the growth experi- ments were maintained on Oregon Moist Pelletsa in seawater holding tanks at Friday Habesr Laboratory. To determine increment periodicity, samples of each stock were sacrificed periodically between March and June, 1981, and were immedi- ately preserved in 95% ethanol or frozen.

Otoliths were removed from each fish and stored on glass slides in immersion oil. The lateral surhce of each otolith was ground by hand on a glass plate in a successisn of 3 85 and 680 carbomnduw grit and immersion oil colloid followed by polishing with I -pm diamond paste. Otoliehs were gghsnd do a plane that included the otolith primordiurn and were viewed under transmitted light with as Zeiss compound photornicros- cope. A standad axis in the postersdsrsal quadrant ofthe otolith was measured with an scuIa.r micrometer at 25 X .

Ve~fication of increment' periodicity required the identifica- tion of reference points in the otolith csmesponding to known dates in the life of the fish. Several investigators have demonstrated that recognizable checks may be formed in otokiths in response to specific environmental or physiolcpgical events (BanneHa I97 1 ; Marshall and Parker 1982). Ten otoliths were examined from fish transferred to seawater only 2 d earlier. Without. exception, a distinctly darker daily increment was obvious very near the edge of the otolith (Fig. 1). Alehaugh we cannot be certain exactly what physioksgicaH or envimnmental factors produced this check, it served as ;k dated reference cheek from which to enumerate otolith increments in experimental fish. Increments were counted from the very dark Increment closest to the otolith primordium (Fig. 2) in a smaller number of specimens sacrificed on seven different dates up to 168 d after hatching. Based on csnclusisns sf Marshall and Baker (1982) for a similar ccheck in sockeye salmon (Oncor~tynchus nerkw) okoliths, we hypothesized that this check canesponded to the date of hatching. Increment counts from these referewce points to the edge of the otolith were csmpaed with h e actual number of days that had elapsed fmm seawater transfer or hatching to sacrifice. All increment counts recorded were made by the same reader and represent the mean of at least two counts,

Fish stoliths from the growth experiments were prepwed in the same way as others atnd photographed s n a standard axis in the anteroventral quadrant at B088>1 after grinding. The photographs were enlarged to a total magnification of 3367X and an axis was drawn along the photcsgraphs on which individual increments were measured with calipers. Daiiy increment widths for each fish were averaged over each week of the experiment to coincide with gghwth measurements, and this mean daily Increment width was averaged over all fish in a treatment, since individuals could not be identified in weekly weighings .

&ion. The actual ~at iom received by each tmitment On a pt?Kentage 2 ~ W i n d i ~ i $ ~ ; I otolith increment is defined as a thin d a k band (&-

of body weight basis differed fmm the prescribed ration and continlrsaas zone) and a wider Iight band (incremental zone) when were calculated at the end of each week based on the actual fish viewed with transmitted light (Mugiya ea al. 1981).

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FIG. 1. Seawater transfer check (ST) and daily increments in a chum salmon otolith. Mag. = 1OOOx.

Results Otolith Increments and Reference Checks

Fish Growth at Different Prey Rations

Mean fish weights deternine8 weekly for each ration and prey species treatment conformed well to an exponential model for growth (y = aebR) (Wicker 1979). CsnsQnt instantarnous growth sates (b ) for all treatments ranged from -0.77% b.w. a

$-'at arationsf1.1% b.w.~d-16~ 3.37% b.w:d-I ataratioga of 11.4% ba W. a d-'- Fish growth within each prey category was significantly different (P < 0.05) at each s f the four ration %evels, and growth rate increased with greater ration in each prey category (FdlaBsle 1 ) . A more direct comparison of fish growth rates in response to ration level and prey taxa was obtained by f l o t~ng fish growth versus ration level or food ecsnversion efficiency ( K -- GlR x 10095, where G is growth rate and R is ration received). Fish fed Barams~ra and Pseudoc.a&n~aus had

The number of otolith increments formed after the seawater transfer check was directly related to the number of days elapsed from placement of fish Into seawater to teminatisn s f the experiment (Fig. 3, r = 0.39, P < 8.01). Coefficients of variation for mean counts ranged from 0.3 ts 83.6%. Average counts s f increments formed after the hypothesized hatching check for fish sacrificed up to l60d after hatching were also directly related to the number of days elapsed from hatching to sacrifice ( y - 0 . 9 4 ~ -+ 6.70; r. -- 8-96. P < 0.01). Coefficients of variation for these mean counts ranged from 2.2 ts 12.4%. Regression analysis over the range of fish sizes examined for all three stocks combined indicated a negatively allometric rela- tionship between otolith radius md fish weight ( y - 404.64~~). 17;

P = 0.92, B < 0.05),

maximum K values of 16.3 and 20.0% for rations of 9.8 and Otolith lncre merit Width and Fish Growth Rate 9.5% b.w. - 8- ', respectively, while fish fed Tipkopeks had a maximum K value bf 40.1% for a ration of 5:78 bed. - d l Mean daily otolith increment widths for fish grown under the (Table 1). Maximum K values far fish in all prey categories different ration regimes changed little rover the course of the occuned at intermediate rations. experiment. The slopes s f these curves were not significantly

M~m%alities among low ration fish were common after the different from zero with the exception of the low-ration Parc4- 4th wrk of the experiment. At the conciusiegn of the study, four moew treatment (Table 2). However, with the exception of the Pammoera-fed fish, one T i g ~ i ~ q ~ d s - f e d fish, and all Pse~do- two low-sation Paramocrcr treatments and the two low-rdtion calanus-fed fish from the lowest ration treatments had died, Pseudocabanus treatments, mean otolith increment widths for

f 28 ['can. 1. Fish. Aqua!. Sci., WOE. 41, 19114

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I . 2 . Hatching cheek (H) and daily increments in a chum salmon otolith. Mag. = 1000 X .

TABLE 1. Mean daily rations, fish weights, conversion efficiencies, and parameters for the exponential growth equation y - ssebx, where y = fish weight (g) and x = time ( Q ) . Neg. = negative.

Dail y ration I~ritiaE Final Conversion k 2 se Time weight weight efficiency

Prey (%b.av:d-" ((d) (g) (%I b( x 1 0 ~ ~ ) " aa r

Neg . 11.2 16.3 15.6

Neg . 35.0 40.1 29.9

"95% confidence limits.

Can. J . Fish. Aqua!. Sci., Val. 41, 19144

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TABLE 4. Mean daily rations, mean otolith increment widths for the study period, and parameters for the regression y = b.x -t a of otolith increment width and time for the experimental period, where y - increment width (pm) znd x = time (d). NS = nut significant.

Daily Mean ration increment 2 SE Time width

Prey (% b.w:~-') (d) & ~ s ~ ( y r n ) a" la" r N P

% 95 confidence limits.

0 0 Q. 5 1.6 1.5 2 -0

G R O W T H R A T E [ In m e a n % weight a d-I1

FIG. 4. Regression of mean daily otolith increment width with growth rate (In (growth rate + 1)) of chum for each treatment. Each point represents the constant instantaneous growth rate and mean otolith increment width for each treatment over the study period.

PIG. 3. Regression 5of number of otcaIith increments counted from the seawater transfer check against the number of days elapsed from trans- fer to sacrifice. Error bars = 1 SE.

each treatment within a prey category were significantly different from one another (Table 2, P < 0.05). Mean daily increment widths for positively growing fish ranged from 1-15 prn for fish fed rations of 4.5% b. w. ~ d - (Par~mssrgl.) to 2.14p.mataratioe%sf 11.4%b.w:d-'(Tigrkopus). Tlnerewasa Bog-linear relationship between mean daily otolith increment width and instantaneous growth rate (F ig . 4, r = 0.98, P < 0.0%) for positively growing fish. Otoliehs from the high-ration Pseudoca&anus and Pwmmoera treatments were not Ptiinciuded in this analysis, as preparcitions were of poor quality. Incxment widths for fish experiencing negative growth ranged from 0.7 to 1.5 pm and were similar to those for slow-growth fish.

The results of sun: growth experiments with juvenile chum salmon indicate that fish growth increased with greater daily ration in all prey categories. However, growth rates were generally lower than growah rates estimated in situ (Healey 19'99) as well as those reported by LeBrasseur (1969) for juvenile churn feeding on similar ratiotas of planktonic prey (2.2-5.796 b.w:dsl for rations of 3-17% b.w:d-'1. The much colder water used in our experiments (8-10°C), as apposed to the 14-16"C range in LeBr'dsseur's, may explain some of the disparity. Reduction in growth of 2 2 - 3 7% for

130 Can. J. Fish. Aquaf . Sci., Vol. 41, 1984

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0 0 2 0 4 8

D A Y S FIG. 5 . Daily fluctuations of otolith increment width for three experi~neneal fish. Broken and sokid lines represent repeat measurements. Prey and approximate rations are as follows: (A) T.ik'gri(~p~us, 3*0% b.w. ~8-'; QB) Paramoem, 4.5% b.w. .d-'; (G) Pseutkoca/a!~kcs, 9.5% h.w. -d-'*

several species of juvenile salmonids reared at 10 versus 15°C has been noted (McComick et al. 1872; Shelboume et a]. 1873). The relatively small aquaria and the inability of the fish to sschml may also have retarded fish growth in this study (Brett 197s).

Fssd conversion efficiencies were musk higher for chum fed TigB'B'opus (29.9-40.1 %I than for either Buramoera or Pseudo- sa%anus (1 2 -2 - 16.3 and 8 2.7-20.8%, respectively). The val- ues fall within the range reported for other salmonids feeding on natural prey: for brown trout (Salmo frk~tm) feeding on Chironsmus (43.5%) and on Cammckr~ds. 15 -2%) (Pandian 8967) and for coho salmon (Oncorhyachus kisutch) feeding on fly larvae (55%) (Averett 1969). Comparisons with these other studies are difficult, however, because different fish sizes, experimental conditions, rand methods of growth detemiination can produce widely divergent results (Palsheims and Diekie 1966; Pandiaw 1967; Chesney and Estevez 1976).

The disparity in food carnversim efficiency s f fish feeding on the three prey taxa may be explained by comparing the relative energetic benefits of each prey for the fish (Palatheirno and Dickie 19648; Wmena and Davis 1967). Ht has been shown that caloric values for hqact ics id copepods and marine calanaoid copepods are at least 35% higher than for ampkpods (Caprnmins md Wuycheck 19'7 1). Amphipods also have a thick, chitinous exoskeleton and may be absorbed less efficiently during digestion than the other prey (Papadian 1967; Brett and Groves 1979). This implies that copepods may return more energy per gram of ingested ration than amphipods. Furthemore, in concunent churn feeding studies, we have observed that the percentage of successful prey capture attempts by chum on Ti'e'griopm was much higher than that with Pseudocwlanrss or Paramoem (unpublished data), indicating &at Parcarnoera agld Pseukd&acahnus have more highly develspd escape responses than Tigriopus. Vinyxd (1982) provided evidence that the

Can. J . Fish. Aqucab. Sci., Vol. 41, 1984 B 3 1

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energetic expenditure s f yellow perch (Perca Pavescens) consuming evasive prey (Diagsha~sosoma) was as much as 55% higher than when feeding on nonevasive prey (Diapto~na~). In light of this, we conclude that the low energetic cost for churn capturing Tigmiopus relative to Paramsem and Pseudocalanus and their relatively high caloric return explain the increased food conversion efficiencies and growth s f chum feeding on Tik'griopurs.

Our investigations confirm a kog-linear relationship between otolith increment width and. fish growth rate for juvenile cE.sum salmon between 0.60 and 4.50 g and growth rates amp to 3 -4% b.w. mdsL. The same rehatiowship results whether the mean fish growth rate and mean otolith increment width are calculated on a weekly basis or over the entire study per id . The nonsignifr- came of all but owe otolith increment width plot over the study period (Table 2) indicates that fish size had little effect on otolith increment width for fish growing at these rather constant rates.

Mthough the notion that otolith microstmcbure can predict fish growth rate is no& a new one, we feel that this study represents a step toward defining a relationship during short intervals suck as their outmigration through estuarine and nearshore habitats. However. &en though the relationship of ~tolieh increment width to fish growth rate is valid for weekly mean values, there is increasing rancedainty in predicting growth rates for intervals s f shorter duration. Calcium deposi- tion and resultant increment width may be affected by a wide variety of factors including quality - and quantity o f diet, temperature, and photo period (IPie 19668; Neiksogn and Geen 1982), and these effects may not be completely tied to growth rate changes. For example, we observed that while weekly mean otolith increment width among all fish ine a treatment remained fairly constant over the study period, the width of otolith incren~ents in chum may exhibit large daily fluctuations (Fig. 5) . If we accept a literal inteprektisn of the otolith increment width to fish growth rate relationship on a daily resoHution, growth rates may change as mush as 14-fold in I d and exceed 10% of the body weight per day. Since variation is Wow in our replicate otolith increment width plots (Fig. 51, influences other than enpeknnental emoe are suggested. Since such radical changes in daily growth are unlikely, envirorsmen- ta% and physio~sgieal factors probably influence calcium deposi- tion to otokiths in ways not reflected in fish weight changes. It is dso important to note that the relationship s f otolith increment width to fish growth rate was based on experiments with fish grown at rather constant rates. Because physiological condition of the fish will likely influence the deposition s f calcium to the otoliths, similar growth rates in fish of different physiological ""histories" may be represented differently in otolith micro- stmsture.

En summary, there is increasing evidence that early m u i ~ ~ e sskwivd ahof juvenile chum is related 1s their size at outmigration (Paker B 97 1 ; Healey 1982). These findings underscore the adaptive significance of estuarine residence for juvenile salaoa, where rapid growth rates are chracteristic and potentially enhance marine survival. A more thorough understmding of the biologicak and physical processes that affect individual growth and produedon of juvenile chum salmon in estuaries still remains a central goal of fisheries research. This study provides a basic link towads this end by illustrating a potentially powedul methodology that can easily be applied to in sieu detemination sf estuuine and early marine growth of churn without expensive, complicated m&k and recapture experi- ments.

The authors extend gacisus thanks to Kam~ Fresh (bvashington Department s f Fisheries), Ernest Sals, Ole Mathisen, and Bruce Snyder (Fisheries Research Institute) , and Charlie Nash (Friday Harbor, Washington) for providing experimental fish. We also wish to thank Craig and Krispy Staude (University of Wzshierg- ton's Friday Harbor Laboratsy) and Jeff Cordell and William Kinney (Fisheries Research Institute) for their invaluable help with zooplankton collection, identification, sorting, and cul- turing.

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1982. Timing and relative intensity of size sclective- mortality of juvenile chum salmon (Oncorhynchu.~ kefa) during early sea life. Can. 1. Fish. Aquat. Sci. 39: 952-95'7.

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MeCoa~ac~, J. W., K. E. F. HOKANSON, AND B. R. JONES. 19'92. Effects of temperature OR growth and survival of young brook trout, Sal~~elknus fontinakks. J. Fish. Res. Board Can. 29: 1187-2112.

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