Reviews in Fish Biology and Fisheries 13: 219–235, 2003.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Reconstructing migratory patterns of fish based on environmentalinfluences on otolith chemistry

Travis S. Elsdon & Bronwyn M. GillandersSouthern Seas Ecology Laboratories, School of Earth and Environmental Science, The University of Adelaide,Adelaide, SA 5005, Australia(Phone: 61 8 83036224; Fax: 61 8 83034364; E-mail: travis.elsdon@adelaide.edu.au)

Accepted 18 August 2003

Contents

Abstract page 219Introduction 220

Methods of determining fish migrationsHistory of otolith chemistry, stock discrimination and environmental reconstructionsPathways of elemental uptake

Analysis techniques 223Environmental influences 225

Availability of elementsTemperature effectsSalinity effectsInteractions between environmental variables

Biological influences 229Exposure time to environmental variablesOntogeny and age structure

Summary and future research 231Acknowledgments 232References 233

Key words: environmental histories, elements, fisheries, otoliths, stock assessment

Abstract

The analysis of elements in calcified structures of fish (e.g., otoliths) to discriminate among fish stocks anddetermine connectivity between populations is becoming widespread in fisheries research. Recently, theconcentrations of elements in otoliths are being analysed on finer scales that allow the determination of acontinuous record of otolith chemistry over a fish’s entire life history. These elemental concentrations canpotentially be used to reconstruct migration patterns, based upon the influence that water chemistry, temperature,and salinity have on otolith chemistry. In doing so, assumptions are made about how environmental and biologicalfactors influence the concentration of elements in fish otoliths. However, there have been few experiments thathave tested crucial assumptions regarding what influences elemental uptake and incorporation into fish otoliths.Specifically, knowledge regarding interactions among environmental variables, such as the ambient concentrationof elements in water, temperature, and salinity, and how they may affect otolith chemistry, is limited. Similarly,our understanding of the rate at which elements are incorporated into otoliths and the implications this may havefor interpretations is lacking. This review discusses methods of determining movement of fish, the developmentof otolith research, and some physiological aspects of otoliths (e.g., pathways of elemental uptake). The types ofanalysis techniques that will lead to reliable and accurate migratory reconstructions are outlined. The effects that

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environmental variables have on otolith chemistry are reviewed with the specific aim of highlighting areas lackingin experimental data. The influences of the rate of elemental incorporation and ontogeny on otolith chemistry arealso addressed. Finally, future research directions are suggested that will fill the gaps in our current knowledgeof otolith chemistry. Hypotheses that need to be tested in order to reconstruct the migratory histories of fishare outlined, in a bid to clarify the direction that research should take before complex reconstructions are attempted.

Introduction

Methods of determining fish migrations

One of the major problems in fisheries science isthe ability to track the movements of individual fish.This problem largely exists due to the lack of under-standing of fish migrations that can occur acrossdifferent environments, such as movements from estu-aries to open ocean. The best evidence of fish migra-tion is the recognisable movement of fish betweendifferent areas of occupancy. As such data are difficultto obtain, common methods to determine movementof fish include distribution and abundance data, andthe use of artificial and natural tags within fish (seeGillanders et al., 2003 for a review of methods). Tradi-tional methods of determining fish movement relyheavily on estimating the distribution and abundanceof fish of different size classes to infer movements,where a change represents movement to alternativehabitats (e.g., Dorf and Powell, 1997). However,changes in the distribution, abundance, and size struc-ture may not actually represent the movement of fish,but could represent factors, such as mortality (Jones,1991) or the scale at which sampling is done (Roseand Kulka, 1999). Thus, these traditional methodsmay not provide accurate determinations of fishmovements.

External tags (e.g., dart tags) and capture-recapturetechniques have been used in combination to establishthe movements of fish among locations (e.g., Mortonet al., 1993). Such studies can determine only theproportion of a population that has moved from thetagged location to that where the fish were recap-tured, and the distance between these is the assumedmovement. Yet, the time scale of recaptures can be ofmonths to years (30 months, Morton et al., 1993) andthese conventional tagging methods do not allow fordetailed reconstructions of movement patterns duringthis time. Furthermore, tagging studies have inher-ently low recapture rates, with values as low as 1.9%reported in the literature (Hansen and Jacobsen, 2003),making many tagging experiments costly, with lowreward.

Advanced methods of external tags include acou-stic and radio tagging, and associated satellite tele-metry. Both techniques rely on tags emitting signalsthat allow the movement of fish to be determined.Although used extensively in fisheries, recent studieshave also shown promising results in determining fishmovement in the open ocean, with the direction anddistance of movements being determined (Block etal., 2001; Comeau et al., 2002). An example of theuse of archival tags with satellite telemetry is theidentification of four separate migratory behavioursof bluefin tuna (Thunnus thynnus) in the Atlantic,which is a significant advance upon movements deter-mined by conventional tagging methods (Block et al.,2001; Åkesson, 2002). However, satellite telemetryof tag signals has limited application to benthic fishspecies that do not surface and allow tag-to-satellitelinking, and thus can not yet replace existing taggingmethods for these species. Given that satellite tele-metry of fish tags is relatively new, further technolo-gical developments should provide better informationon identifying fish movement when combined withother methods.

In response to problems associated with artificialtagging of fish, the use of natural tags to determinefish movement has received greater attention. Naturaltags that are thought to hold promise for determiningmovements of fish include the elements and stableisotopes that are incorporated into the calcified struc-tures of fish. The most commonly used structures arethe otoliths, or earbones, although scales, fin spines,and eye lenses have also been examined (Radtke andShepherd, 1991; Coutant and Chen, 1993; Dove andKingsford, 1998; Wells et al., 2000). The potentialfor using otoliths as a tool to identify and track fishstocks is reliant on the incorporation of elements fromthe surrounding seawater into the calcium carbonatestructure in a layered manner that preserves the timingof deposition. The type, abundance, and combinationof elements (or elemental signature) can potentiallybe used to discriminate between groups of fish withdifferent origins, as well as the water bodies theyhave inhabited. Therefore, otolith chemistry can bea useful tool for tracking the migratory paths of fish

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based on the reconstruction of environmental historiesas recorded in the layering of the otolith.

This review examines the expanding field of otolithchemistry, with the primary emphasis on under-standing factors that will allow for the reconstructionof environmental histories of fish based on otolithchemistry. Specifically, three major areas of otolithchemistry are reviewed, which when combined shouldsupply the information needed to allow for accuratereconstructions; these are (i) analysis techniques, (ii)environmental influences, and (iii) biological influ-ences. First, analysis techniques that would allow forthe reconstruction of environmental histories of fish atappropriate spatial scales are reviewed. Literature thatexamines the influence of environmental variables ofelemental availability, temperature, salinity, and inter-actions of these on otolith chemistry are examined.Last, biological variables such as the time that fishare exposed to environmental variables, and the influ-ence this may have on otolith chemistry are discussed,along with ontogenetic changes that may influence theinterpretation of environmental variables. This reviewis summarised by proposing hypotheses that need to betested before otolith chemistry can be used to recon-struct environmental histories of fish, and outliningthe future directions fisheries research should take toobtain such information.

History of otolith chemistry, stock discrimination andenvironmental reconstructions

Interest in otolith chemistry within fisheries sciencehas resulted in increased research output in recentyears. Studies have centred primarily on differen-tiating between fish stocks using the concentrationof elements in otoliths as chemical signatures ornatural tags (e.g., Gillanders, 2001). Stock discrim-ination is based on the hypothesis that fish inhabitingdifferent water bodies will incorporate elements intotheir calcified structures, which combine to form aunique chemical signature that reflects the length oftime that the fish occupied the particular water body.The most common application of stock identificationis discriminating between separate populations thatwere previously assumed to be one (Thresher, 1999;Campana et al., 2000). As stock identification doesnot require knowledge of why there are differences inelemental signatures, it is not vital to understand howenvironmental variables (e.g., temperature, salinity,and ambient elemental concentration) may influ-ence chemical incorporation into otoliths. However,

chemical signatures have been used to reconstructenvironmental histories and migratory patterns of fish(Kafemann et al., 2000; Secor and Rooker, 2000;Tsukamoto and Arai, 2001). This has been done basedon the effects that temperature or salinity have onthe chemistry of discrete layers of otolith material,made possible by the daily formation of the otolithmatrix. The reconstruction of migratory patterns offish is a major step forward from stock discrimination,as the underlying assumptions made in many earlystudies of otolith chemistry, concerning how chemicalincorporation is affected by environmental variablesneed to be understood so that our interpretations ofenvironmental histories and migratory patterns can beenhanced.

The ability to reconstruct aspects of a fish’s lifehistory (e.g., migratory patterns) using otoliths relieslargely on predictable responses of otolith chemistryto environmental variables. Examples of these predict-able responses include those described by Edmondset al. (1999) and Kafemann et al. (2000), who usedthe concentration of strontium (Sr) in fish otolithsin an attempt to reconstruct migratory patterns basedon salinity profiles. This was done by collecting fishfrom different salinity environments (e.g., fresh andbrackish water), analysing small regions within theotoliths, and proposing possible migratory patterns forfish in bays (Edmonds et al., 1999) and large rivers(Kafemann et al., 2000). However, there are fourmajor assumptions that are made when reconstructingenvironmental variables of fish, some (or all) of whichmay not have been addressed by these and similarstudies. The four assumptions relate to the influenceof environmental variables on otolith chemistry, theeffect of exposure time to environmental variableson elemental incorporation in otoliths, the influenceof ontogeny and fish/otolith age structure on recon-structing migrations, and the type of analysis that isdone on the otolith to infer environmental histories.

First, it is assumed that the habitat or environ-ment that the fish lived in varied only in salinity (orone other environmental variable), independently ofother environmental variables such as water temper-ature, and ambient elemental concentration. However,rivers and coastal regions often vary in salinity, aswell as in other factors, such as temperature and theconcentration of elements within the water (Palmerand Edmonds, 1989), with these variations often beingsimultaneous and not independent of one another.Thus, the reconstruction of migratory patterns inareas, such as coastal regions (e.g., over broad spatial

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scales of approximately 100 km of river, Kafemannet al., 2000), based solely on single environmentalvariables may provide erroneous interpretations ofenvironmental histories and therefore migrations.

The second and third assumptions are related to therate of elemental uptake into otoliths and the influ-ence of ontogeny and fish/otolith age structure onreconstructions. The reconstruction of environmentalhistories of fish from otolith chemistry assumes thatat any one particular time fish have spent an adequateperiod of time in a body of water to allow for thefull incorporation of elements into discrete layersof the otolith. This assumption is likely to be voidwhen dealing with species that are capable of movingthrough large gradients of temperature and salinityover short time periods, and/or in systems whereenvironmental variables can change rapidly, such asin estuaries. The third assumption is that ontogeneticeffects on otolith chemistry do not occur, or are atleast known. Validation of this assumption is particu-larly important when otoliths are to be analysed acrossdifferent life history stages, such as juvenile and adultotolith growth. This becomes especially importantknowing that otolith growth decreases with fish age(Jones, 2000); thus, the temporal scale of recon-structions at different fish ages needs to be adjustedto account for otolith growth. The assumptions ofontogenetic effects and otolith growth influences arerarely addressed in studies that reconstruct environ-mental histories of fish, yet are important in obtainingaccurate estimates of movement when large migratoryreconstructions (analysing otolith growth greater thanone year) are to be done. The fourth assumption is thatthe technique being used to analyse otoliths is at anappropriate scale to determine environmental historiesof fish. This last assumption is perhaps the easiest toaddress, and becomes a pre-requisite for any studyattempting to reconstruct environmental histories.

In the case where environmental reconstructionsusing otolith chemistry is reliant on the under-standing of one or more of these assumptions, thenthere is a need for laboratory-based experimentswhere the influences of temperature, salinity, ambientelemental concentration, and interactions of theseon otolith chemistry are determined. Knowledge ofhow exposure time to environmental variables affectselemental incorporation into otoliths and ontogeneticinfluences also need to be assessed. This informationshould be coupled with understanding of the environ-ment and fish species, such as the rate of changeof environmental variables and possible rate of fish

movement, so that reconstructions can occur over thecorrect spatial and temporal scales.

Conversely, it is possible to reconstruct environ-mental histories of fish if the first three assumptionsare met for a particular species. Such migrations arereliant on only one environmental variable changing(i.e., salinity), and that fish spend adequate periodsof time in each environment to incorporate elements.Furthermore, it is assumed that ontogenetic influ-ences are absent, or that otoliths are being analysedover short time periods eliminating the effect ofotolith growth on reconstructions. This set of circum-stances may occur when reconstructing environmentalhistories of a slow moving fish in a stable environment,such as a river where salinity is the only variable thatchanges, or where a fish species will actively avoidchanges in temperature rather than migrate throughthem. If otoliths of these fish are analysed over smallscales that represent only months of growth withina given year then promising reconstructions withoutthe need for further scrutinising of both environmentaland biological influences are possible. Reconstruc-tions that are done on small portions of otolith materialare present in the field of otolith chemistry, withKatayama et al. (2000) reconstructing the migration ofresident and anadromous smelt, Hypomesus nippon-ensis, using the concentration of Sr in otoliths andrelating this to salinity over small (less than 100 µm)areas of otolith growth. However, the effect that wintertemperature could have had on the interpretation ofa salinity migration remained unanswered, which asnoted by Katayama et al. (2000) could influence theinterpretation of anadromous smolt within this system,highlighting the need to test assumptions before recon-structing environmental histories of fish.

Pathways of elemental uptake

Unlike other calcium carbonate structures such ascoral skeletons, otoliths are not in direct contactwith the surrounding water. There are three maininterfaces (brachial uptake, cellular transport, andcrystallisation) through which elements must pass ifthey are to be crystallised onto otoliths (Campana,1999). The presence of these interfaces, which eitherconcentrate or dilute elements, means that otolithsdo not directly reflect the elemental composition ofsurrounding seawater (Campana and Thorrold, 2001).The final precipitation of elements into the calciumcarbonate structure is due to the physical chemistry ofbiomineralisation (Nielson and Christoffersen, 1982)

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and can be described by kinetic processes (Gauldieet al., 1995). While a description of these kineticprocesses is beyond the scope of this review (seeGauldie et al., 1995 for a thorough review), theprocesses of biomineralisation are affected by bothphysiological (Kalish, 1989; Hoff and Fuiman, 1993;Borelli et al., 2001) and environmental variables(Kalish, 1989; Hoff and Fuiman, 1995; Tzeng et al.,1997).

The reasons why environmental variables influ-ence the elemental composition of otoliths is thoughtto be due to their effects on biomineralisationprocesses. Temperature is most likely to affect growthrates of fish otoliths, as well as the pH of bloodplasma and endolymph fluid (Romanek and Gauldie,1996). Hence, water temperature may affect otolithchemistry directly, and indirectly through changes inpH. Changes in pH, growth, and temperature are allfactors that are known to influence crystal precipita-tion (Gauldie et al., 1995). Salinity and the concentra-tion of elements in the water are also likely to affect theavailability of elements to the endolymph and proteinmatrix surrounding the otolith (Payan et al., 1997,1999), and hence, the availability of elements to beprecipitated onto the otolith.

It should be noted that elements that are underheavy physiological regulation and are affected greatlyby chemical incorporation, such as Na, K, S, P, andCl (Payan et al., 1999), are unlikely to be useful asnatural tags in otolith chemistry primarily becausetheir concentrations in endolymph fluid are underconstant regulation (Payan et al., 1999). However,elements that are not physiologically regulated, andare therefore more evenly incorporated into otoliths(such as Sr), are ideally suited for the reconstructionof environmental histories of fish as they vary withenvironmental concentrations.

Analysis techniques

To reconstruct fish migratory patterns based on theelemental composition of otoliths and the known influ-ence of environmental variables, it is important toanalyse otoliths at appropriate temporal scales (ofgrowth increments) that reflect the period requiredfor environmental variables to influence otolith chem-istry. Such periods need to be determined by priorcontrolled experiments. Much of the literature on theeffect of environmental variables on otolith chem-istry has been analysed using solution-based analysis,

where whole otoliths were dissolved in acid, diluted,and analysed. In analysing large areas of otolith(whole otolith solution analysis), the presence ofthese large “spiked” bands lose their detectabilityover time as the fish gets older. However, thereare several different techniques for determining theelemental concentrations in otoliths on fine scales (seeCampana et al., 1997 for a review). Of importancehere is not so much the instrument of analysis, butthe size of otolith area analysed (e.g., whole otolithsampling versus small spot sampling). The analysisof otoliths via solution techniques or via large-scalespot analysis may be satisfactory for stock assessment(e.g., Gillanders, 2001), but environmental reconstruc-tions from otoliths need to be done on much finerscales. Fine scale analyses of otoliths are currentlyachieved using laser ablation ICP-MS, electron micro-probe, and micromilling instruments (see Campana etal., 1997). These instruments allow for small areas,down to the diameter of several µm of the otolith to beanalysed (see Markwitz et al., 2000) or the analysis ofcontinuous transects that cut across the otolith, and sorelate the chemical signal laid down in discrete layersof otolith matrix to the fish’s age. With these tech-niques, the concentrations of elements incorporatedinto otoliths can be determined for a specific point intime. Thus, differences in otolith chemistry can bedetected using finer scales of analysis that may notbe detected using solution based analysis of wholeotoliths (Figure 1).

In analysing otoliths using solution-based analysisor large spot samples, it may not be possible to detectdifferences between the otoliths of two fish, where onewas exposed to a high concentration of elements fora short period of time, while the other was exposedto lower concentrations for a longer period of time(see Figure 1). An example of the loss of detectabilitycan be seen in Figure 2, where fish were exposedto different concentrations of elements (0, 2, 4, 8,and 16 × ambient) for 32 days, their otoliths wereanalysed by large (100 µm) and small (30 µm) spots,and a continuous transect at 30 µm width using alaser ablation ICP-MS (see Elsdon and Gillanders,2002 for methodology of spot analysis, and Sinclairet al., 1998 for a similar transect methodology). The30 µm continuous transects were used to determinethe ‘actual’ concentration of elements incorporatedduring the exposure period. The resolved concen-trations of Sr differed between the 30 and 100 µmspots, whilst the 30 µm spot and transect did notdiffer significantly (ANOVA: F10,180 = 71.59, P =

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Figure 1. Diagram comparing solution and laser ablation/microprobe analysis for fish otoliths that have been (a) exposed to different concentra-tions of elements for different time periods, and (b) as a result of this, have either an evenly distributed low concentration of elements or a smallelementally spiked region (shown by dark line). In analysing these otoliths, the solution analysis (c) failed to detect differences in elementalconcentration, whilst (d) laser ablation/microprobe analysis detected differences, such that for 20 days exposure the concentration throughoutthe otolith was stable compared to the 2 days exposure where a spike in concentration was found. Before and after the exposure period (2 daysexposure) the concentration was below that found for the 20 days exposure.

Figure 2. Graph displaying the mean concentration of strontium(± standard error, SE) in otoliths of black bream (Acanthopagrusbutcheri) reared under different elemental concentrations (0, 2, 4,8, and 16 × ambient) and analysed with different techniques usinglaser ablation ICP-MS. Open bars = 30 µm continuous transectanalysis, grey bars = 30 µm spot analysis, and black bars = 100 µmspot analysis.

0.0000, Figure 2). Thus, the scale at which otolithswere analysed influenced the derived concentrations ofelements, and migrations determined using the largerscales of analysis would not reflect actual changes in

environmental variables. It is difficult to determine ifthis problem has occurred in any experiments and ithighlights the need for the otoliths in future experi-ments to be analysed on finer scales than whole otolithanalysis. This will allow for the detection of concen-tration of elements over smaller temporal scales (e.g.,a scale of days) and will allow for the exact concentra-tions of elements to be determined without influencefrom the rest of the otolith matrix.

The use of laser ablation and/or microprobeanalysis also allows for multi-elemental analysis ofotoliths, which is a valuable tool for fisheries research.Multi-elemental signatures are used in stock assess-ment, but have rarely been used in charting migratorypatterns and environmental variables, where researchon Sr alone is most common (e.g., Kafemann et al.,2000; Secor et al., 2001). However, multi-elementalanalysis provides elemental signatures that are likelyto yield strong and clear distinctions between temper-ature, salinity, and elemental concentration gradientsin experiments. Through the use of multivariate statis-tics, elemental signatures may allow for much moreaccurate reconstructions of migratory patterns of wildstocks (e.g., Gillanders and Kingsford, 2000; Gemper-line et al., 2002). These accurate reconstructionsare likely to be achieved using predictive quadraticequations or polynomial functions that describe howenvironmental variables influence otolith chemistry.

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Environmental influences

Availability of elements

Elements that are incorporated into otoliths are likelyto be derived from either the environment that the fishinhabits or its diet. While several experiments havetested the effect of enhanced elemental concentrationin diet on otolith chemistry, none have found a signifi-cant effect, suggesting that element uptake from dietmay be minimal, at least for some species (Hoff andFuiman, 1995; Farrell and Campana, 1996; Miltonand Chenery, 2001). Therefore, water chemistry isthought to be the primary source of elements that areincorporated into otoliths.

The field of fisheries science has taken a simpli-fied viewpoint of elemental distribution in water,concluding that many elements vary in concentra-tion with salinity or nutrient gradients (e.g., Bruland,1983; Ingram and Sloan, 1992). This is despite thefact that the distribution of elements in the water islikely to be the consequence of complex combinationsof factors, including salinity, precipitation, evapora-tion, and the chemical composition of the underlyingbedrock (Palmer and Edmonds, 1989). An exampleof such an elemental distribution is given by Riemanet al. (1994), who suggested that high concentrationof Sr in freshwater environments could be caused bybedrock properties and not only the salinity of thewater. The variation of Sr in otoliths among regionswas therefore increased, which in turn made theregional discrimination of fish stocks based on otolithchemistry difficult. Rieman et al. (1994) concludedthat differences in Sr concentration in water mightconfound attempts to determine the residence timesof migratory fish in freshwater streams. Thus, itshould not be assumed that elemental availability isconstant between environments, or changes in predict-able salinity like gradients.

There have been several experiments that havetested how water chemistry affects the concentrationof elements in calcified structures. While the type ofcalcified structure examined differed among experi-ments, the results are relatively consistent. Experi-ments have always detected a strong positive relation-ship between concentration in water and otoliths. Forexample, the concentration of water Sr had a strongeffect on the chemistry of otoliths (Snyder et al., 1992;Brown and Harris, 1995; Schroder et al., 1995; Farrelland Campana, 1996; Bath et al., 2000; Elsdon andGillanders, 2003) and other calcified structures, such

as spines, scales, and vertebrae (Behrens Yamada andMulligan, 1987; Pollard et al., 1999; Wells et al.,2000). Similarly, the concentration of barium (Ba)in water affected the concentration in otoliths (Bathet al., 2000; Elsdon and Gillanders, 2003). Theseexperiments increased the concentration of elementsin the rearing water and detected strong correspondingeffects in the otoliths. Many of these experiments weredesigned for mass marking purposes and as such, theconcentrations of elements used to spike the waterwere high, with several using up to 40 times theambient Sr concentration (equivalent to approximately1.0 g L−1; e.g., Pollard et al., 1999). However, Snyderet al. (1992) and Bath et al. (2000) both used relativelylow concentrations of Sr (1.8, 3.6, and 5.4 mg L−1,and 1.2, 1.4, and 1.8 × ambient levels, respectively),and also detected significant effects on the otolithchemistry. Furthermore, Bath et al. (2000) detected asignificant effect for Ba when spiking with only lowconcentrations (3, 6, and 10 × ambient levels). Thus,there appears to be a strong relationship between theconcentration of elements in seawater and their uptakeinto calcified structures.

The relationship between water and otolith chem-istry for Sr is not always linear (Schroder et al., 1995)and it is not yet known if these non-linear trendsrepresent sources of Sr other than the ambient water,or active regulation of elemental uptake by individualspecies. An experiment by Elsdon and Gillanders(2003) highlights that sources of elements (Sr andBa) other than that from water are present in fishotoliths, and the degree to which this can influenceotolith chemistry at different ambient concentrationsis unknown. This same experiment found that theconcentration of Mn in fish otoliths could not berelated to ambient concentrations, suggesting that theuptake of all elements do not conform to that of Sr andBa (Elsdon and Gillanders, 2003). However, assumingthat otolith chemistry changes in a predictable mannerwith water chemistry (at least for Sr and Ba) doesshow promise for the reconstruction of environmentalhistories of fish using ambient elemental concentra-tion, especially if other environmental variables do notchange, such as temperature and salinity.

Temperature effects

Water temperature changes both horizontally (betweensites and locations) and vertically (with depth), oversmall and large spatial scales. Temperature differ-ences can often be related to coastal and oceano-

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graphic features, such as bays, estuaries, up-wellings,and currents. Water column temperature also changesseasonally, with annual fluxes often occurring inshallow estuaries. Therefore, it is possible to discrim-inate between water bodies based on temperature bothin space and time. By understanding the influence oftemperature on the uptake of elements into otoliths itmay be possible to predict accurately the migratorypatterns of fish and determine environmental inhabit-ancy.

To date, the effect of temperature on otolith chem-istry has largely been implied through correlative fieldstudies (e.g., Radtke and Kinzie, 1996; Thorrold etal., 1997; Patterson, 1998), which have related theelemental composition in otoliths to that of watertemperature at the time the fish were collected. Thesestudies have formed the basis of equations that areused to determine the relationship between temper-ature and elemental concentration in otoliths (e.g.,Townsend et al., 1992). Such studies have providedbackground information suggesting otolith chemistrymay change with temperature, but this does not allowus to predict confidently the influence of temperatureon otolith chemistry. Thus, it has been necessary todetermine the effects of temperature under controlledlaboratory conditions.

There have been several experimental investi-gations of the effects of temperature on otolithchemical composition (see Table 1), which haveproduced both positive (i.e., temperature increaseswhilst otolith concentration increases) and negativeeffects of temperature on otolith chemistry. Thesedifferent results can most likely be attributed to factorssuch as the range of temperatures used, the speciesinvolved, and differences in the salinity of the water atwhich the temperature experiments were done. Suchvaried results suggest that there is not a single linearpredictive equation for all species that describes theeffect of temperature on otolith chemical composition.Since much of the literature has concentrated on Sruptake, little is known of the effect of temperature onthe concentrations of other elements, whose combinedinfluence as an elemental signature is used for stockdiscrimination (e.g., Gillanders, 2001). Thus, to dategeneralisations may only be possible for Sr and lessso, for Ba, which is discussed further below.

For Sr, positive (Kalish, 1989; Fowler et al., 1995a;Hoff and Fuiman, 1995; Mugiya and Tanaka, 1995;Secor et al., 1995; Bath et al., 2000; Yamashitaet al. 2000; Elsdon and Gillanders, 2002), negative(Secor et al., 1995; Townsend et al., 1995; Elsdon and

Gillanders, 2002), and non-significant (Tzeng, 1996;Chesney et al., 1998; Kawakami et al., 1998) corre-lations between otolith Sr concentrations and temper-ature have been reported (see Table 1). The effect oftemperature may reflect the choice of experimentaltemperatures and the biology of the individual species.The experiments that detected positive effects of Srwith temperature often reared fish at high temperatures(i.e., 20 ◦C and above; Hoff and Fuiman, 1993, 1995;Bath et al., 2000), whereas experiments that reportnegative results usually reared fish at low tempera-tures (i.e., 17 ◦C and below; Townsend et al., 1992,1995). Experiments that bridge this gap, rearing fishat both low and high temperatures, detected bothpositive and negative results, such that Sr concentra-tion was greatest at low and high temperatures (12 ◦Cand 28 ◦C) and decreased in the mid-range tempera-tures (20 ◦C; Elsdon and Gillanders, 2002), or detecteda slight positive result across all temperatures (Kalish,1989). While, Tzeng (1996) and Kawakami et al.(1998) both reared the same species of eel (Anguillajaponica) in low and high temperatures, no effectof temperature on Sr concentration in otoliths wasdetected. Thus, the variety of results may indicatethat the effect of temperature on Sr concentration inotoliths is not linear and that responses are species-specific.

A similar conclusion may also apply to the influ-ence of water temperature on the concentration of Basince both positive (Elsdon and Gillanders, 2002) andnon-significant effects have been reported (Fowler etal., 1995a, b; Bath et al., 2000). However, theselatter studies reared fish at relatively high tempera-tures (20 and 25 ◦C; Fowler et al., 1995a, b; Bath etal., 2000), compared to Elsdon and Gillanders (2002)who detected the greatest difference in Ba concentra-tions between 16 and 20 ◦C, but found no influenceof temperature at 24 and 28 ◦C. Thus, the range oftemperatures used in experiments and that all exper-iments involved different species may account for thedifferent results.

Although widely investigated, our current under-standing of how temperature affects otolith chemistryis incomplete, but is likely to involve species-specificeffects. Equations that have been used to explaintemperature effects on elements are often based onassumed linear relationships (Table 2). However,linear relationships rarely seem to exist, especiallyover a broad temperature range. Thus, there is aneed to investigate the effect of temperature for indi-vidual species, across a range of temperatures that

227

Tabl

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Rev

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ofex

peri

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tsth

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eef

fect

sof

tem

pera

ture

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inity

,and

inte

ract

ions

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ratu

rean

dsa

linity

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chem

istr

y

Spec

ies

Exp

osur

eM

anip

ulat

ions

Ele

men

tsR

esul

tsSa

mpl

ing

Ref

eren

ces

time

(day

s)Te

mpe

ratu

re(◦

C)

Salin

ity(‰

)an

alys

edap

proa

ch

Tem

pera

ture

Arr

ipis

trut

ta66

13,1

6,19

,22

34.8

Sr+v

eSo

lidK

alis

h,19

89

Gad

usm

orhu

a50

5–14

Seaw

ater

Sr–v

eSo

lidTo

wns

end

etal

.,19

95

Ang

uilla

japo

nica

190

22–2

3,27

–28

0,10

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35Sr

0(a

tall

sal.)

Solid

Tze

ng,1

996

Mic

ropo

goni

asun

dula

tus

7120

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2623

elem

ents

Sr:+

ve,M

n,M

g,C

u:-v

e.So

lutio

nFo

wle

ret

al.,

1995

a

Mic

ropo

goni

asun

dula

tus

7120

,25

2623

elem

ents

Mg,

Ba:

–ve

Solid

Fow

ler

etal

.,19

95b

Scia

enop

soc

ella

tus

7821

,23,

27,3

0,34

30Sr

,Mg

Sr:+

ve,M

g:0

Solid

Hof

fan

dFu

iman

,199

5

Car

assi

usau

ratu

s5

16,2

0,24

,28

Fres

hwat

erSr

+ve

Solid

Mug

iya

and

Tana

ka,1

995

Mor

one

saxa

tilis

2115

,25

0,5,

10,1

5,20

,30

Sr+

vean

d–v

e(s

al.d

epen

dent

)So

lidSe

cor

etal

.,19

95

Bre

voor

tiapa

tron

us∗

18,2

2,26

20,2

6,33

.4Sr

0(a

tall

sal.)

Solu

tion

Che

sney

etal

.,19

98

Ang

uilla

japo

nica

5812

,17,

22,2

7Fr

esh,

Saltw

ater

Sr0

(atb

oth

sal.)

Solid

Kaw

akam

ieta

l.,19

98

Lei

osto

mus

xant

huru

s∗

20,2

520

Sr,B

aSr

:+ve

,Ba:

0So

lidB

ath

etal

.,20

00

Pla

ticht

hys

bico

lora

tus

208,

1311

,32

Sr+

ve(a

tbot

hsa

l.)So

lidY

amas

hita

etal

.,20

00

Aca

ntho

pagr

usbu

tche

ri50

12,1

6,20

,24,

2830

Sr,M

n,B

a,B

a:+

ve,S

r:+v

e&

–ve,

Mn,

Solid

Els

don

and

Gill

ande

rs,2

002

Mg

Mg:

0

Salin

ity

Mic

ropo

goni

asun

dula

tus

7120

26,3

523

elem

ents

Sr,M

n,M

g:0,

Ca:

+ve

Solu

tion

Fow

ler

etal

.,19

95a

Scia

enop

soc

ella

tus

7827

10,3

0,32

,38,

40Sr

,Mg

0So

lidH

off

and

Fuim

an,1

995

Ang

ullia

japo

nica

190

22–2

3,27

–28

0,10

,25,

35Sr

+ve

(atb

oth

tem

p.)

Solid

Tze

ng,1

996

Bre

voor

tiapa

tron

us∗

18,2

2,26

20,2

6,33

.4Sr

0(a

tall

tem

p.)

Solu

tion

Che

sney

etal

.,19

98

Ang

uilla

japo

nica

5822

Fres

h,Sa

ltwat

erSr

+ve

Solid

Kaw

akam

ieta

l.,19

98

Aca

ntho

pagr

usbu

tche

ri50

16,2

0,24

5,17

,30

Sr,M

n,B

a,M

n,B

a,M

g:0

(ata

llte

mp.

)So

lidE

lsdo

nan

dG

illan

ders

,200

2

Mg

Sr:0

(16

◦ C),

–ve

(20,

24◦ C

)

Tem

pera

ture

×sa

linity

Mor

one

saxa

tilis

2115

,25

0,5,

10,1

5,20

,30

Srin

ter

Solid

Seco

ret

al.,

1995

Ang

ullia

japo

nica

190

22–2

3,27

–28

0,10

,25,

35Sr

0So

lidT

zeng

,199

6

Bre

voor

tiapa

tron

us∗

18,2

2,26

20,2

6,33

.4Sr

0So

lutio

nC

hesn

eyet

al.,

1998

Ang

uilla

japo

nica

5812

,17,

22,2

7Fr

esh,

Saltw

ater

Sr0

Solid

Kaw

akam

ieta

l.,19

98

Pla

ticht

hys

bico

lora

tus

208,

1311

,32

Sr0

Solid

Yam

ashi

taet

al.,

2000

Aca

ntho

pagr

usbu

tche

ri50

16,2

0,24

5,17

,30

Sr,M

n,B

a,Sr

,Ba:

inte

r,M

n,M

g:–v

eSo

lidE

lsdo

nan

dG

illan

ders

,200

2

Mg

∗=fis

hw

ere

kille

dw

hen

they

had

reac

hed

ace

rtai

nle

ngth

;+ve

=po

sitiv

eef

fect

(inc

reas

edco

ncen

trat

ion

ofel

emen

tsin

otol

iths

with

incr

easi

ngte

mpe

ratu

re/s

alin

ity);

–ve

=ne

gativ

eef

fect

(dec

reas

edco

ncen

trat

ion

ofel

emen

tsin

otol

iths

with

decr

ease

dte

mpe

ratu

re/s

alin

ity);

0=

noef

fect

;in

ter

=in

tera

ctiv

eef

fect

(the

effe

ctof

one

envi

ronm

enta

lva

riab

le[e

.g.,

tem

pera

ture

]is

depe

nded

onth

em

agni

tude

ofan

othe

r[e

.g.,

salin

ity])

;fo

req

uatio

nsse

eTa

ble

2.So

lid=

sam

plin

gba

sed

onso

lidot

olith

sam

ples

such

asla

ser

abla

tion;

solu

tion

=w

hole

otol

iths

wer

edi

ssol

ved

and

anal

yed

via

solu

tion

appr

oach

es.

228

Table 2. Review of equations from experiments that have examined the effects of temperature and/or salinity on otolith chemistry

Species Element Variables examined Equation References

analysed T (◦C) S (‰)

Sciaenops ocellatus Sr:K, Ca, Na ∗ T = –10.334 + [5.276 × (Sr:Ca)] + [5.312 × (10−5 × Hoff and Fuiman, 1995

Ca)] + [2.735 × (10−3 × Na)]

Carassius auratus Sr:Ca ∗ (Sr:Ca) = [(1.21 × T) – 7.05] × 10−4 Mugiya and Tanaka, 1995

Gadus morhua Sr:Ca ∗ (Sr:Ca) × 103 = [25.145 EXP (–T / 5.120)] Townsend et al., 1995

Anguilla japonica Sr:Ca ∗ (Sr:Ca) × 10−3 = 4.665 – (0.394 × T) – (0.041 × T2) Tzeng, 1994

Clupea harengus Sr:Ca ∗ (Sr:Ca) × 103 = 0.08 × T / (–269 + T) Townsend et al., 1992

Anguilla japonica Sr:Ca ∗ (Sr:Ca) × 103 = 3.797 + (0.14 × S) Tzeng, 1996

Morone saxatilis Sr:Ca ∗ S = 40.302 [1 + 56.337 EXP−1523.310 10×(Sr:Ca)−1] Secor et al., 1995

T = temperature (◦C), S = salinity (%). ∗ = Environmental variable used in the equation.

are relevant to the life history and ecology of thatparticular species. Once these results are obtained, itmay then be possible to reconstruct migratory patternsbased on temperature effects using similar equationsto those in Table 2, so long as temperature is the soleenvironmental variable that changes in the habitatsoccupied across the fish’s migratory range.

Salinity effects

Salinity also differs within water bodies both hori-zontally and vertically, and differences in salinitycontribute to stratification of the water column, whichoften defines boundaries between different watermasses (Tomczak and Godfrey, 1994). Changes insalinity can occur due to precipitation and evapora-tion events, and can be greatly influenced by varyingfreshwater input in coastal zones (Dávila et al., 2002),with estuaries typically exhibiting strong gradientsof salinity. It is therefore possible to discriminatebetween water bodies based on salinity, and whensalinity influences the elemental incorporation intootoliths then it is likely that fish which inhabit waterbodies of different salinities may have different chem-ical signatures in their otoliths. However, salinityand the ambient concentration of elements are oftenlinked (see Availability of elements). Therefore, under-standing the effects of salinity on otolith chemicalincorporation is important if predictions are to bemade about migration patterns of fish.

Several experiments have investigated the effectsof salinity on otolith chemistry, particularly for Sr(Fowler et al., 1995a, b; Hoff and Fuiman, 1995;Secor et al., 1995; Tzeng, 1996; Chesney et al., 1998;Yamashita et al., 2000; Elsdon and Gillanders, 2002),with the results of these experiments being somewhat

different. Several experiments have reported a strongpositive relationship between otolith Sr and salinity(Tzeng, 1996; Kawakami et al., 1998; see Table 2for equations), with many experiments detecting non-significant effects (Fowler et al., 1995b; Hoff andFuiman, 1995; Chesney et al., 1998; Yamashita et al.,2000; Elsdon and Gillanders, 2002). This conflict ofresults suggests that other factors may interact withsalinity to affect Sr uptake. Indeed, low tempera-tures (16 ◦C) have been found to reduce the effectsof salinity on otolith Sr concentration (Elsdon andGillanders, 2002), yet at higher temperatures (20and 24 ◦C), strong salinity effects are seen (Tzeng,1996; Kawakami et al., 1998; Elsdon and Gillanders,2002). It is not known whether this pattern would beconsistent for all species, because experiments havealso detected no effect of salinity at high temperatures(e.g., > 20 ◦C, Fowler et al., 1995b; Hoff and Fuiman,1995; Chesney et al., 1998; Yamashita et al., 2000).

The influence of salinity on elements other thanSr is less well studied, with several authors detailingeffects on elements such as Ba, Mg, and Mn (Fowleret al., 1995a; Hoff and Fuiman, 1995; Elsdon andGillanders, 2002; see Table 1). Both Fowler et al.(1995a) and Elsdon and Gillanders (2002) found nosignificant effect of salinity on Ba concentrations inotoliths. Thus, it appears that salinity does not influ-ence all elements simultaneously and equally. Thismeans that there is a requirement for further exper-imental analysis on the influence of salinity on theincorporation of individual elements.

The reconstruction of environmental histories offish based solely on salinity does show promisein species where predictable equations have beenconstructed from experiments. An example is that ofTzeng (1996) in which no interaction was detected

229

between salinity and temperature, with salinity beingthe only variable to influence the concentration of Srin otoliths of the eel, Anguilla japonica (Tables 1and 2). Reconstructions of migratory histories ofthis eel could potentially be done based on salinityalone.

Interactions between environmental variables

The availability of elements in water, temperature,and salinity are the three main environmental vari-ables that are thought to influence otolith chemistry.Given the nature of these variables, they are often notindependent of each other. Various combinations ofthese three factors are possible, for example, whencool fresh-water with high elemental concentrationflows into warm, saline estuaries having low elementalconcentration. Hence, the interactive influence ofenvironmental variables (where the effect of one vari-able is dependent on another) needs to be consideredif reconstructions of past environments occupied byfish are to be done. In cases where interactions arenot assessed, determining environmental origin canbe extremely difficult as highlighted by Rieman et al.(1994, see Availability of elements). To date there havebeen few experimental analyses of such interactionsand none that have examined interactions of all threefactors of temperature, salinity, and ambient elementalconcentration.

Interactions between temperature and salinity ofseawater have been examined in a few experimentalinvestigations in the field of otolith chemistry (Secoret al., 1995; Tzeng, 1996; Chesney et al., 1998;Kawakami et al., 1998; Yamashita et al., 2000;Elsdon and Gillanders, 2002), two of which detectedinteractive effects (Secor et al., 1995; Elsdon andGillanders, 2002). The detection of interactive effectsof temperature and salinity may in part be due tothe fact that both experiments used temperatures thatvaried considerably (e.g., 16, 20, and 24 ◦C, Elsdonand Gillanders, 2002; 15 and 20 ◦C, Secor et al.,1995), with the former experiment indicating thatsalinity has its greatest effect on otolith chemistry athigh temperatures (20 and 24 ◦C), compared to lowtemperatures (16 ◦C). Since the strength of the inter-action was temperature dependent, this may accountfor why other experiments have not shown inter-active effects of temperature with salinity, such asTzeng (1996) who used temperatures of 23 and 28 ◦C,and failed to detect an interactive effect. Alterna-tively, experiments that failed to detect an interac-

tion between temperature and salinity may representspecies-specific responses to environmental variables(Tzeng, 1996; Chesney et al., 1998). When the rangeof an environmental variable used in experimentsspans that experienced by wild fish stocks of the samespecies, the non-interactive effect indicates that singlefactor reconstructions are plausible.

Few experiments have examined the interactiveeffect of temperature and salinity on elements otherthan Sr (an exception is Elsdon and Gillanders 2002,for Ba, Mg, and Mn). The use of combined elementalsignatures is likely to enhance our interpretations ofmigratory patterns, as demonstrated by studies ofstock discrimination. Thus, not only is there a need fora greater number of experiments examining interactiveeffects, but these experiments should also encom-pass the analysis of multiple elements to maximisethe returns from the experiment. Similarly, there areseveral factors other than temperature and salinitythat may influence the concentration of elements inotoliths, including the elemental concentration in thewater, ontogenetic influences, and genetic variation.Experimental designs involving combinations of thesefactors would enhance our understanding of the majorinfluences on otolith chemistry.

Biological influences

Exposure time to environmental variables

The rate at which elements are incorporated intootoliths can greatly influence the spatial and temporalscales at which fisheries biologists can reconstructmigratory patterns based on environmental variables.This is primarily because elements need time to passthrough the physiological barriers before being incor-porated into the otoliths. The time available for incor-poration of elements may be a limiting factor inrecording migratory patterns over temporal and spatialscales. A fast-moving fish that inhabits many differentwater masses over a short time period (i.e., days)may have a somewhat “mixed” elemental signature,depending on the rate at which elements are depos-ited into otoliths, and the periods of exposure todifferent temperature and salinity regimes. Thus, inorder to gain accurate migratory chronologies fromotoliths, it is important to understand the rate ofelemental uptake for the species being examined, andthe minimum time of exposure needed for ambientelemental concentration, temperature, and salinity to

230

influence otolith chemistry. Until such questions areanswered, it will be difficult to define the appro-priate spatial and temporal scales for which migratorypatterns can be reconstructed.

The rate of elemental uptake has been examinedmainly from the mass marking perspective (e.g.,Ennevor and Beames, 1993), where commercially-bred fish for stocking programmes are placed in waterthat has been enhanced with elements in an effortto create an elementally-enhanced region on calcifiedtissues. Catches of wild stocks can then be examinedfor the presence of this elementally-enhanced region toassess the success of a specific release programme. Inorder to ensure the cost effectiveness of mass marking,short time scales and high concentrations of elementspiking are often used, some of which may be indic-ative of the elemental uptake rates of fish in “natural”environments.

There is an abundance of literature on the uptakerates of elements into vertebrae, spines, and scales(see Pollard et al., 1999, for a review), but few exper-iments have documented the uptake rate into otoliths(see Snyder et al., 1992; Ennevor and Beames, 1993;Schroder et al., 1995). In determining the uptakerates of elements in fish there are two factors thatneed to be assessed: the concentration of elementsin the water (discussed earlier) and the period ofexposure to particular concentrations. It is likely thatthe time period of exposure and the concentration ofelements in rearing waters interact (see Pollard et al.,1999), such that at higher concentrations (10 and 40× ambient Sr) the period of exposure needs to be lessto achieve a given concentration in an otolith than atlow concentrations (5 × ambient Sr). However, theseelemental effects have been observed only over shorttime periods (hours to days) and at high concentrationsof elements in mass marking experiments. Consistentwith this are the results of Brown and Harris (1995)who spiked water with Sr at 1 g L−1, for exposureperiods of one, two, and four days. Thus, the requiredperiod of exposure before elements are incorporatedinto otoliths is likely to be in the order of severalhours to days. Given that recent data by Ferris-Pagéset al. (2002) indicates a linear increase in Sr in coralswith exposure time of up to nine days, it seems likelythat greater than nine days exposure would be neededfor elements to be incorporated at maximal concentra-tion in fish otoliths. This requires further investigationusing appropriate concentrations of elements. Never-theless, data do suggest that migratory patterns thatoccur over greater temporal scales than weeks would

allow for the accurate tracking of fish using otolithchemistry.

The period of exposure required for temperatureand salinity to influence otolith chemistry is relativelyunknown. Experiments that examined how temper-ature and salinity affect otolith chemistry are primarilyconcerned with detecting differences in elementalconcentrations not in defining necessary time periodsof elemental incorporation. As such, these experi-ments expose fish to different rearing conditions forlong periods, which are normally in the order ofseveral weeks to months (e.g., 71 days, Fowler etal., 1995a). Such experiments give little insight intothe temporal effects over biologically significant timescales that are relevant to reconstructing migratorypatterns, especially for migrations of less than onemonth. However, there is some information thatdescribes the application of short-term “shocks” oftemperature and salinity as a non-elemental otolithmarking technique, and its effect on otolith micro-structure (e.g., Volk et al., 1999). Similar to elementalspiking, these studies are concerned with markingotoliths via exposure to large changes in temper-ature and salinity over small time scales. Volk et al.(1999) showed that a drop in temperature of 3.5 ◦Cfor short periods (15–240 minutes) resulted in opticalimpacts in otoliths, leaving a permanent mark, with theintensity of the impact being dependent on exposuretime. Similarly, increasing water temperature by 8–10 ◦C for short periods (8 hours) also resulted invisual markings (Negus, 1999), as did exposure tohyperosmotic conditions (0% NaCl to 5–12% NaCl,Beltran et al., 1995). These experiments examinedonly the optical characteristics of otoliths and provideno indication of any associated changes in elementalcomposition over these short time scales. Neverthe-less, the changed physical structure suggests that theremight be a change in elemental composition on similarscales. There is a need to acquire basic knowledgeof the time required for environmental variables toinfluence otolith chemistry. Such experiments willhelp indicate the temporal scales at which migratorypatterns can be reconstructed based on the influenceof environmental variables.

Ontogeny and age structure

Changes in the life history of fish, such as growthfrom larval to juvenile and juvenile to adult stages,result in changes to both morphology and physiologyof individuals. These differences are likely to result

231

in changes in the way otoliths grow by influencingbiomineralisation processes and so influencing theelemental compositions of otoliths. Such changes areobserved when analysing otoliths using transects thatscan the entire life of the fish (see Toole et al., 1993;Fowler et al., 1995b). Scans such as those done byToole et al. (1993) often show peaks of up to threetimes the concentration of Sr close to the core of theotolith (within 100 µm of the focus), after which thereadings drop and stabilise further from the core. Suchvariation in elemental composition within otoliths isthought to be due to ontogenetic changes. Howeverwhen these fish are from wild stocks (as were fish usedby Toole et al., 1993 and Arai et al., 2002), environ-mental variables that could cause these changes (suchas temperature and salinity changes) can not be ruledout. Recognising changes in environmental variablesbecomes especially important when juveniles displayontogenetic habitat shifts, with movement from littoraland profundal zones that can vary considerably inenvironmental characteristics, such as temperature(e.g., littoral 15–20 ◦C, profundal 6–8 ◦C).

There has been limited experimental research thathas examined the effects of ontogeny on otolith chem-istry (e.g., Fowler et al., 1995b). Fowler et al. (1995b)spawned fish and held their larvae in a common tankfor 24 hours, before assigning them to treatments ofdifferent temperatures and salinities that were heldconstant for a further 71 days (see Fowler et al., 1995afor a summary of rearing conditions). The concentra-tions of Sr, Ba, Ca, Mg, B, and Zn were then measuredat the centre, 500 µm from the centre, and at theedge of otoliths using laser ablation ICP-MS. Signifi-cant differences were detected for Sr, Ba, and Zn,indicating ontogenetic influences on otolith chemistry.The influence of ontogeny also varied among treat-ments of temperature and salinity. Similarly, Sadovyand Severin (1992) highlight the potential for fishgrowth rate to influence the concentration of Sr:Ca infish otoliths. Thus, ontogeny influences the chemicalsignature of otoliths, with this being most apparent inearly life history periods.

To understand how ontogeny affects otolith chem-istry, it becomes important to establish relationshipsbetween different life history stages and the chem-istry of the otoliths, where environmental factors,such as the concentration of elements, temperature,and salinity, are held constant. Clearly, maintaininga constant diet throughout ontogenetic developmentwould be far more difficult. Therefore, we may neverconclusively know if ontogeny alone affects otolith

chemistry, but it is important to recognise that lifehistory influences are possible. This becomes espe-cially true if reconstructions of environmental historiesattempt to span different life history stages, such as themigration of fry from streams to estuaries as juven-iles and then to the open ocean as adult fish. In suchcases, the influence of ontogeny is likely to be stronglyconfounded by the influence of change in temperatureand salinity regimes. Thus, it becomes important todetermine the magnitude of effect on otolith chemistryfrom ontogeny relative to other environmental vari-ables, if ontogenetic effects are to be incorporated intomigratory reconstructions.

The reconstruction of environmental historiesacross several life history stages not only bridge onto-genetic influences, but have the added difficulty ofdetermining migrations when fish/otolith growth haschanged. It is well known and documented that otolithradius decreases with fish age (see Jones, 2000), andin such circumstances the ability to determine environ-mental change using transect analysis across otolithsis altered with age. This is especially important withequations that deal with the rate of elemental uptakeinto otoliths, where the experiment may have beendone on juvenile fish and the reconstructions are beingdone by analysing otoliths in both the juvenile andadult otolith matrix. Thus, it becomes important totest for ontogenetic effects on otolith chemistry, andto account for otolith growth when reconstructingenvironmental histories of fish.

Summary and future research

There is an ever-present need in fisheries manage-ment to be able to track the migrations of fish, withone of the most promising techniques currently avail-able being otolith chemistry. As the theory of stockdiscrimination based on multi-elemental signatures ofwhole otoliths becomes grounded in the literature,fisheries scientists are considering the next step, whichis the reconstruction of migratory histories of indi-viduals and fish stocks using the elemental concentra-tions in fine layers in the earbone matrix. Whilst stockdiscrimination theory is based on detecting differ-ences in elemental signatures between fish that inhabitdifferent areas (Gillanders, 2001), the reconstructionof migratory patterns assumes the use of an appro-priate analysis technique, knowledge of how otolithchemistry changes with environmental variables, thetime elements take to be incorporated into otoliths,

232

and the influence of ontogeny and age structure on theinterpretation of environmental histories.

The response of otolith chemistry to changes inenvironmental variables that has been obtained fromexperiments can be used to develop predictive equa-tions such as those displayed in Table 2. Whilst theseequations allow for the determination of environmenttype at a specific point in time along the otolith,they may not allow for the reconstruction of environ-ments should the rate of elemental uptake influencethe concentration of elements in otoliths. Thus, infor-mation regarding timing of elemental uptake needs tobe factored into equations and models that estimateenvironmental characteristics from elemental concen-tration. Such equations or models can then be usedso long as the reconstructions do not bridge acrossconsecutive years of otolith growth where ontogenycould affect otolith chemistry. If information on onto-geny is not known, it is recommended that recon-structions are limited to within year comparisons, orto the analysis of otolith material which correspondsto the age of fish from which experimental resultswere derived. Promising examples of these types ofreconstructions can be found in the literature (seeKatayama et al., 2000), but the potential to gain moreaccurate reconstructions still exists with the adventof further experimentation into interactive effects ofenvironmental variables. Conversely, where ontogen-etic effects are not apparent within a species, recon-structions that bridge several developmental stages,larval, juvenile, and adult fish, would be possible,so long as an adjustment is made for the amountof deposited otolith material within each of thesestages.

Our present understanding of how elementalconcentration in otoliths is affected by environmentaland biological factors is limited for many species,mainly because of the few experiments that have testedassumptions regarding elemental incorporation. Thisis especially so when considering interactive effects oftemperature and salinity on otolith chemistry, whichhave only been reported in a few experiments, andthere are no experiments that detail possible interac-tions between temperature, salinity, and the concen-tration of elements in water bodies. Our understandingof the rate at which elements are incorporated intootoliths is based on a suite of calcified tissues, notonly otoliths. The rate of elemental incorporation isan assumption that is likely to radically change thespatial and temporal resolution required to reconstructmigratory patterns. Thus, testing of this assumption

should be made a priority, as should the identificationof ontogenetic effects for individual species.

Much of the literature regarding experimental dataon the influence of environmental and biologicalfactors on otolith chemistry lean towards species-specific responses of elemental incorporation. Thus,it is recommended that until such time that the fieldof otolith research establishes a set of broad andgeneral rules regarding otolith chemistry, which onall accounts may not exist, that basic knowledgebe obtained for a particular species before recon-structions are attempted. We propose three questionsthat are most important to test before reconstructionof environmental histories of fish: (i) do interac-tions between elemental availability, temperature, andsalinity influence the magnitude of effect of each vari-able on the elemental incorporation into otoliths; (ii)is elemental incorporation into otoliths affected bythe amount of time fish are exposed to environmentalvariables; and (iii) does ontogeny affect otolith chem-istry. Each of these questions can be developed intohypotheses that relate to individual experiments andthis, when combined with a synopsis of present knowl-edge and research in this review, would allow foradequate information for accurate reconstructions ofenvironmental histories for an individual species offish.

The reconstruction of migratory histories of fishbased on environmental variables can be done givena basic knowledge of oceanography. This canbe achieved by comparing otolith signatures andthe related environmental variables to the ambientelemental concentration, temperature, and salinity ofdifferent habitats, and the construction of possiblemigratory paths. Whilst such reconstructions wouldsignificantly enhance the ability of fisheries scientiststo manage stocks, the key to interpreting accuratemigratory patterns of fish based on otolith chemistry isreliant on the quality of experimental data for a partic-ular species. Once steps are taken to address specificissues on what affects elemental uptake and incorpor-ation into fish otoliths, the chemical chronology storedin otoliths will prove to be an invaluable tool for recon-structing migratory paths of fish that will aid in themanagements of fisheries.

Acknowledgments

This work was supported by an APA award to TSEand ARC QEII fellowship and large grant to BMG.

233

Constructive comments on previous versions of themanuscript were made by A.J. Fowler, A.D. Irving,H.M. Patterson, and two anonymous reviewers.

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