What Fish Biologists Should Know About Bivalve Shells

Fisheries Research 46 (2000) 39±49

What ®sh biologists should know about bivalve shells

Robert M. Cerrato*

Marine Sciences Research Center, State University of New York, Stony Brook, NY 11974-5000, USA

Abstract

Similarities between shell and otolith growth patterns are numerous. Both have been shown to have subdaily and daily increments, fortnightly variations, and annual patterns. Some of the less obvious common features include the production of irregular microgrowth patterns at low temperature, increased transparency at high temperature, reduced increment clarity in ®eld to laboratory transferred individuals, and uncoupling between somatic growth and growth of the calci®ed structure. A principal difference between shells and otoliths is that while microgrowth increments are found in bivalve larvae, presence of internal daily increments has not been veri®ed for any species. Applications of shell and otolith growth patterns have also been similar. Both have been used to reconstruct the effect of environmental and ontogenetic events after they have taken place and to obtain age data critical for estimating growth rate, recruitment, and survivorship. Recent evidence suggests that growth in these calci®ed structures has the potential to provide information on physiological processes. Evidence is provided for bivalves that respiration rates could potentially be predicted from shell growth rates. # 2000 Elsevier Science B.V. All rights reserved.

Keywords: Growth increment; Microgrowth increment; Otolith; Bivalve shell

1. Introduction nite (Carter, 1980); however, some species have ara- gonite shells, others are calcite, and a number of In their introduction to the collected papers from the species have both (Wilbur and Saleuddin, 1983). First International Symposium on Fish Otoliths, Secor Vaterite is also found in bivalves but is not common et al. (1995) indicated that otolith growth is more (Wilbur and Saleuddin, 1983). similar to bivalve shell growth than ossi®cation in How similar otolith and shell growth patterns are scales, spines, and other hard parts in ®sh. Both has never been examined in any detail. Pannella otoliths and shells are extracellular, calci®ed struc- (1980) suggested that any similarities are only super- tures. Both are composed of calcium carbonate crys- ®cial since the calci®cation processes differ. Whether tals and organic material. Otoliths are primarily the results from a growth pattern study of one structure aragonitic, but calcite and vaterite, other forms of are in any way transferable to the other is an open calcium carbonate, are also present (Gauldie, 1993). question. Both taxa are responding to the same suite of The primitive crystal type for bivalve shells is arago- environmental conditions, and identifying similarities and differences in their response may be very useful in * Tel.: 1-631-632-8666; fax: 1-631-632-8820. understanding the mechanisms involved. The purpose E-mail address: [email protected] (R.M. Cerrato) of this paper is to attempt a cursory comparison of

0165-7836/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0165-7836(00)00131-4 40 R.M. Cerrato / Fisheries Research 46 (2000) 39±49 otolith and bivalve shell growth patterns and their in water temperature (<0±258C). The most detailed applications in order to suggest why greater exchange growth patterns in Mya arenaria are preserved in the of information and more detailed comparative work chondrophore, an internal, spoon-shaped structure would be useful. projecting from the hinge region of the left valve (Fig. 1a). The small size of this structure makes it an ideal candidate for examination by thin section. 2. A comparison of methods The term microgrowth increment is used to describe daily or subdaily microscopic growth increments in Otoliths are generally prepared for examination bivalve shells; it is equivalent to the term microincre- under transmitted light by clearing, etching, decalci- ment used in otolith studies (Kalish et al., 1995). fying, or grinding. For bivalves, the most common and least labor intensive method is the preparation of 2.1. Growth patterns acetate peels. This involves embedding the shell in an epoxy, sectioning along the axis of maximum A ®rst important similarity between otoliths and growth, grinding, and polishing the sectioned surface shells is that growth of these calci®ed structures is (Kennish et al., 1980). The polished surface is then never negative, even in undernourished or starved etched with a dilute solution of HCl, and an acetate individuals. In ®sh, otolith growth in starved indivi- replica is made by ¯ooding the etched surface with duals has been reported by Campana (1983a,b) and acetone and applying a sheet of acetate. Acetate Neilson and Geen (1984). Pannella and MacClintock replicas are not common as an otolith preparation (1968) held individuals of the hard clam Mercenaria method, although they have been used on occasion mercenaria without food for several months and found (Pannella, 1980; Stequert et al., 1996). evidence for shell growth in the form of thin but The less common method of preparation of bivalve visible sets of increments. Lewis and Cerrato (1997) shells is by thin sectioning. This involves sectioning measured positive shell growth in the soft shell clam the shell from the umbo or hinge region to the growing Mya arenaria in experiments lasting 3 weeks, during edge. A specimen is then mounted onto a petrographic which individuals received only a minimal food ration slide, sectioned a second time, ground, and polished. and lost soft tissue weight. Distinct variations in transparency begin to be seen in Both daily and subdaily microscopic growth incre- thin sections ground to 150±250 mm. Microgrowth ments occur in ®sh and bivalves, but daily patterns are increments are evident only when sections are ground dominant in ®sh and tidal patterns are predominant in thinner to 80±120 mm. While more labor intensive, bivalves. Daily patterns in ®sh are common and re¯ect thin sections tend to produce superior results to acetate entrainment to a light±dark cycle (Campana and peels; however, there are formidable technical dif®- Neilson, 1985). Subdaily increments in otoliths are culties that keep this method from being more popular rare (Pannella, 1980), and have been related to sub- for examining bivalve shells. In addition to the daily feeding periods and ¯uctuations in temperature increased labor, it is dif®cult to produce uniform (Campana and Neilson, 1985). Very often, these sub- thickness (e.g., 80±120 mm) sections for large struc- daily increments are less distinct and can be differ- tures; bivalve shells are often greater than 5 cm in entiated from daily increments (Campana and cross-section. Neilson, 1985). This study was restricted to comparing otolith Early studies of bivalves suggested that daily incre- growth to bivalve shell patterns prepared as thin ment patterns were present in several intertidal and sections. Throughout, opaque and translucent refer subtidal shells (House and Farrow, 1968; Pannella and to the appearance of sections under transmitted light. MacClintock, 1968; Rhoads and Pannella, 1970; Bivalve growth patterns are illustrated primarily with Thompson, 1975; Richardson, 1996). Extensive work thin sections of the soft shell clam Mya arenaria. All primarily by Richardson (1987a,b, 1988a,b, 1989) and individuals were collected from intertidal areas on Richardson et al. (1979, 1980) on a variety of species Long Island, New York. Environmental conditions on brought this early research into question, providing Long Island are temperate with large annual variations strong evidence for the predominance of tidal rhythms R.M. Cerrato / Fisheries Research 46 (2000) 39±49 41

Fig. 1. Microgrowth patterns in the chondrophore of Mya arenaria. Optical micrographs of thin sections: (a) cross-section of hinge region and chondrophore of 2 year-old individual. Chondrophore is to the right of the umbo and part of external shell is to the left; (b) annual cycle; (c) winter (W) and spring (Sp) patterns; (d) summer (Su) and fall (F) patterns. Within summer, strength of pairing of semidiurnal increments varies over fortnightly tidal cycle; (e) fortnightly pattern with wide and narrow increments corresponding to spring (s) and neap (n) tides. Shell transparency also varies over fortnightly cycle. 42 R.M. Cerrato / Fisheries Research 46 (2000) 39±49 within the shell. The only unquestioned evidence for Cenni et al. (1990) and Cenni (1991) reared plank- the presence of dominant daily growth increments has tonic larvae of Mercenaria mercenaria in the labora- been provided by research on scallops (e.g., Clark, tory through metamorphosis under conditions of 1968; Helm and Malouf, 1983; Parsons et al., 1993), continuous light, continuous dark, and a diurnal cycle where external shell ridges (not internal increments of varying photoperiod and light intensity. Examina- which are generally absent) form with a daily fre- tion of photoperiod as an external cue was justi®ed by quency. Scallops are active, mobile epifauna that the investigators because light levels and photoperiod respond strongly to light, so the presence of a daily were known to have a profound effect on the behavior rhythm in these animals is reasonable. of larvae (Carriker, 1961). Results indicated that the Recent work on microgrowth patterns has identi®ed rate of microgrowth increment production was not a distinct correspondence between semidiurnal tidal in¯uenced by light treatment. In addition, during the cycles and the number of subdaily increments in early larval period (age 5±7 days), individuals pro- bivalves (Evans, 1972; Richardson et al., 1979, duced almost six increments per day. Following this 1980; Richardson, 1987a,b, 1988a,b, 1989; Cerrato stage, the rate of production declined quickly to et al., 1991). In Mya arenaria collected in waters off approximately three increments per day. This rate Long Island and growing intertidally, these subdaily was maintained for several weeks and included the increments are deposited twice a day during the warm rest of the larval stage, metamorphosis, and the early months of the year (Fig. 1). Broad increments are post-larval period. These results suggested an endo- deposited in spring. These grade into closely spaced genous origin to the rhythmicity of microgrowth increments in summer. During fall, broad increments increment formation, and failing to identify a syn- are again being formed, but by mid-fall, increment chronization with an external environmental cycle, the widths decrease and the increments begin to appear high frequency of formation makes age estimation irregular in shape. Growth increments remain thin and problematic. Unfortunately, no experiments were con- irregular throughout the winter (Fig. 1c). During late ducted to determine if larval growth patterns could be fall and winter, increments are deposited at less than entrained by tidal rhythms in temperature or pressure. tidal frequency, but some increment production con- Several observational studies appear to show more tinues throughout the year. A similar irregular promising outcomes to the problem of determining the wrinkled structure such as that found during winter age of bivalve larvae. Siddall (1980) found growth for Mya was described in otoliths of the Japanese eel ridge formation at approximately tidal frequency in held at low temperature (Umezawa and Tsukamoto, the tropical mussel Perna viridis raised at different 1991). temperatures. In one other study on larvae, Hurley Unlike ®sh, a method to determine the age of larval et al. (1987) identi®ed daily patterns in the sea scallop bivalves is not generally available, possibly because Placopecten magellanicus, but like adult scallops, daily internal increments have not been identi®ed in these were ridges formed on the outer shell surface bivalve shells. Discovery of daily increments in oto- and were not re¯ected in the internal structure of the liths of larval and early juvenile ®sh has been of shell. fundamental importance in stimulating early life his- Microgrowth increments often occur in related tory research (Brothers et al., 1976). This active series re¯ecting fortnightly tidal patterns, and in adult research ®eld has no equivalent in bivalves. The bivalves, two somewhat different types of patterns problem has not been the absence of microgrowth have been identi®ed. The ®rst pattern involves fort- patterns in larval bivalves but in the interpretation of nightly variation in the width of microgrowth incre- existing patterns. Shells are ®rst produced by bivalve ments (Pannella and MacClintock, 1968; Evans, 1972; larvae as early as 24 h after fertilization (Carriker, Kennish, 1980). This pattern takes the form of a series 1961). Larvae have very distinct growth patterns, and a of wide increments deposited during spring tides clear growth break is formed in the shell at the time of followed by thin increments formed during neap tides settlement (Jablonski and Lutz, 1980). Unfortunately, (Fig. 1e). A second, but less obvious pattern has been daily increments have not been veri®ed, although little observed in the pairing of increments in bivalves research has been done in this area. (Evans, 1972; Richardson et al., 1979, 1981; Richard- R.M. Cerrato / Fisheries Research 46 (2000) 39±49 43 son, 1987a,b; Cerrato et al., 1991). In this pattern, pairs of increments are separated by a diffuse, rather than a distinct boundary and appear coupled (see summer patterns in Fig. 1d). There may be little or no change in increment width, but the pairing often cycles from strong to weak over the fortnightly period. Investigators have found that the alternating diffuse and sharp boundaries between increments are formed either when the semidiurnal tides are mixed (i.e., unequal) or when they are accompanied by large diurnal temperature variations (Evans, 1972; Richard- son et al., 1979, 1981; Richardson, 1987a,b). In ®sh, only the fortnightly variations in increment width have Fig. 2. Correspondence between shell transparency and tempera- been reported (e.g., Pannella, 1971, 1980; Campana, ture in Mya arenaria. Thin section of a single individual collected 1984). intertidally on 29 November 1994 was examined using a Cohu At the seasonal level, patterns of opaque and trans- 4915-2010 B/W camera attached to a Zeiss Standard microscope at lucent zone formation may be opposite in ®sh and 100Â. Image was captured using a Scion LG3 frame grabber and bivalves. In their review, Beckman and Wilson (1995) analyzed with NIH Image version 1.60. Transparency was measured as a brightness value (0±255 grayscale range) along a found a geographic correspondence in the formation line oriented approximately normal to the growth increments. of the opaque zone in otoliths. In temperate latitude Growth of the chondrophore for the year comprised 1349 pixels species, e.g., the opaque zone was deposited during 3± along this line, and a 5-point moving average was applied to the 4 months of the year and translucent zone was formed raw brightness data to obtain transparency. Measurement locations during the remaining 8±9 months. The peak in opaque on the shell were determined by backcalculating from the date of collection. Temperatures were measured near bottom during high zone formation occurred during spring and summer. tide. Day number 0 is 30 November 1993. Correlation coefficient is Evidence linking otolith opaque zone formation to r0.66 between transparency and temperature. spawning was not strong. The authors suggested that opaque zone formation in temperate latitudes tended to be associated with rapid growth and seasonally in microgrowth increments that accompanies this high or increasing temperature, but the evidence transparency pattern, as noted earlier. Both the sea- from the literature was very con¯icting with studies sonal timing and period of time that the translucent reporting opaque zone formation at low temperature, zone is formed in Mya arenaria appears to be unlike high temperature, slow ®sh growth, rapid ®sh growth, that found in temperate ®sh. A very cursory compar- and changing ®sh growth (Beckman and Wilson, ison suggests that the transparency pattern in Mya 1995). corresponds well to seasonal changes in bottom water There has been little research on seasonal changes temperature (Fig. 2). In this ®gure, there is also a clear in bivalve shell transparency because of the domi- indication that shell transparency varies on a shorter nance of the acetate peel method of preparation. In time-scale than can be accounted for by seasonal Mya arenaria (Fig. 1b), the seasonal cycle in the inner changes in bottom water temperature. Finer scale shell layer consists of an opaque region formed in the resolution of temperature may resolve some of these spring, a translucent region in summer, and a second short-term transparency variations. opaque region in fall-winter (Cerrato et al., 1991). The Lewis and Cerrato (1997) found that shell transpar- translucent region is restricted to 3±4 of the warmest ency changed very quickly in response to an abrupt months in the year. It should be noted that this pattern change in temperature (Fig. 3). Short, 24 h tempera- is based on a thin section ground to about 80±120 mm. ture spikes produced a well-de®ned band of contrast- As the section is ground further, the proportion con- ing transparency (i.e., a translucent band in the middle sidered translucent would appear to increase, so this of an opaque region or an opaque band in a translucent classi®cation is highly dependent on preparation region). Soft shell clams in the ®eld often form bands method. There is also a systematic seasonal pattern of contrasting shell transparency that correspond to 44 R.M. Cerrato / Fisheries Research 46 (2000) 39±49

Fig. 3. Comparison between field and laboratory growth in Mya arenaria. Optical micrographs of thin sections of the chondrophore edge. In the laboratory system, animals were held under semidiurnal variations in water level. Water temperature was held constant except as noted: (a) temperature spike formed in response to a 58C increase in temperature for 24 h; (b) temperature spike formed in response to a 58C decrease in temperature for 24 h. periods of about 3±7 days (e.g., see translucent band in arenaria, the transition is marked by a change in shell Fig. 1c). Cerrato et al. (1991) termed one such pro- transparency (Fig. 3). Interestingly, while the change minent translucent band a ``spawning band'', because in transparency occurs rapidly after transplantation, it was formed in the spring by most individuals in the change in increment width and clarity may take population at about the same time spawning occurred. several days to settle down into a regular pattern As an alternate explanation, this band might have been (Fig. 3b). caused by an abrupt increase in water temperature, In comparing growth patterns between otoliths and although this abrupt change could also have induced shells, it should be kept in mind that otoliths are the animals to spawn. Short-term temperature shock internal structures not directly exposed to the envir- generally leaves a distinct pattern in bivalves and is a onment, while most studies of bivalves analyze micro- reliable means of marking shells for growth studies growth increments at the ventral or growing margin of (Richardson et al., 1979; Fritz and Haven, 1983; the shell. The mantle tissue which deposits shell at the Richardson, 1988b, 1989) and has been used to moni- growing edge is directly exposed to the environment tor the impact of water temperature changes created by and has been shown to respond to environmental sudden ¯uctuations in power plant discharges (Ken- disturbances. Kennish (1980), e.g., reported that a nish and Olsson, 1975; Kennish, 1976). Fortnightly storm caused a growth break in the hard clam Merce- cycles are also often accompanied by changes in shell naria mercenaria, and silt grains that found their way transparency (Fig. 1e). Like ®sh, abrupt transparency under the mantle were incorporated into the outer shell changes probably re¯ect stress, but little work has layer. Retraction of the mantle tissue from the growing been done to document the occurrence of the patterns edge when disturbed by temperature extremes, abra- or determine whether the change in transparency can sion, or other disturbances creates a characteristic be quanti®ed. groove or notch visible in hard clam cross-sections The clarity or distinctness of growth increment (Fig. 4). patterns generally declines in both ®sh and bivalves The hinge region in bivalves has a variety of held under conditions less variable than natural structures, including the chondrophore and cardinal (Richardson et al., 1979; Lewis and Cerrato, 1997). platforms, that are internal and not in direct contact In bivalves, a distinct change in the growth pattern is with the external environment, and detailed growth observed corresponding to the time the individual was records in these structures are probably more compar- transplanted from the ®eld to the laboratory (Richard- able to otolith patterns. Bivalve shells consist of two or son et al., 1979; Lewis and Cerrato, 1997). In Mya more calci®ed layers that can differ considerably in R.M. Cerrato / Fisheries Research 46 (2000) 39±49 45

Uncoupling between the growth of somatic tissue and otoliths has been observed frequently in ®sh (e.g., Mosegaard et al., 1988; Reznick et al., 1989; Secor and Dean, 1989; Hoff and Fuiman, 1993). Mosegaard et al. (1988), e.g., found considerable evidence for growth uncoupling in Arctic char raised at different temperatures. In their laboratory experiment, somatic growth rate reached an optimum at an intermediate temperature and declined at the highest temperatures. In contrast, otolith growth rate continued to increase with increased temperature. Mosegaard et al. (1988) explained the decline in somatic growth rate in ener- Fig. 4. Growth break in the outer shell layer of the hard clam getic terms, with respiration progressively utilizing a Mercenaria mercenaria. Optical micrograph of thin section. larger fraction of assimilated energy at higher temperatures. These investigators then proposed that otolith growth was related to some ``metabolic expression composition and structure. These layers are formed by of the ®sh'' that continued to increase with tempera- the mantle tissue in different regions of the shell. The ture. Unfortunately, no metabolic measurements were outer layer is deposited at the growing margin; the available to test this hypothesis. innermost layer forms in interior regions generally In bivalve studies where both tissue weight and shell behind the pallial line (Kennedy et al., 1969), a region size changes have been measured simultaneously, a where the mantle tissue attaches to the shell. Deposi- number of investigators have demonstrated that these tion in the inner shell layer is not simply a re¯ection of measures vary independently and often become patterns found in other parts of the shell (Pannella and uncoupled in time even in non-reproductive indivi- MacClintock, 1968; Fritz and Lutz, 1986; Cerrato duals (e.g., Hilbish, 1986; Borrero and Hilbish, 1988; et al., 1991; Rosenberg and Hughes, 1991). Growth Harvey and Vincent, 1990). For example, Borrero and breaks followed from the outer shell layer become less Hilbish (1988) measured tissue and shell growth over prominent and increment widths tend to be less vari- a complete growing season in a South Carolina popu- able in the inner shell layer (pers. obs.). Cerrato et al. lation of the ribbed mussel, Geukensia demissa. They (1991) have suggested that these internal growth found that rates of tissue and shell growth varied records probably contain less environmental noise independently, and shell growth remained positive, and may also be more closely coupled to systemic even during periods when tissue growth was negative. physiological processes. Lewis and Cerrato (1997) experimentally uncoupled shell and tissue growth in Mya arenaria 2.2. Applications by manipulating temperature, exposure time, and food levels. In their experiments, positive shell growth was Growth increment patterns in both otoliths and observed in all treatments, even those not suf®cient to bivalve shells have been used for two distinct purposes support tissue growth. Their results indicated that (Rhoads and Lutz, 1980): (1) reconstructing the effect under conditions where shell and tissue growth were of environmental (and ontogenetic) events after they uncoupled, shell growth remained correlated to have taken place, and (2) obtaining age data critical for respiration rate (e.g., Fig. 5). To my knowledge, this estimating growth rate, recruitment, and survivorship. experimental study has been the only demonstration Research on ®sh and bivalves seems to be converging that growth of a calci®ed structure remained corre- on a third possible application, i.e., providing infor- lated to a measure of metabolic rate under uncoupled mation on physiological processes. The origin of this conditions. Lewis and Cerrato (1997) also suggested new research area is recent work centered around the that seasonal trends observed in shells supported a observation that growth in calci®ed structures can relationship between shell transparency and metabolic become uncoupled from tissue growth. rate. Shell patterns in Mya arenaria show the greatest 46 R.M. Cerrato / Fisheries Research 46 (2000) 39±49

Fig. 6. Relationship between oxygen consumption (mg O2 per tidal cycle) and shell growth (mm per tidal cycle) in Mya arenaria under various environmental conditions. Results are a composite of three laboratory experiments examining response to temperature (circle), food (triangle), and immersion (square) levels. Treatments were 5, 12, 20, and 278C for temperature, 12.5, 25, 50, and 100% ration for food, and 6, 8, 10, and 11.25 h for immersion time. Clams were carefully matched to be of similar size and weight. Animals were held under semidiurnal tidal conditions for 2±3 weeks, and each point is an average of five replicates. Coefficient of determination was r20.74 with outlier (filled triangle) removed (data from Lewis and Cerrato (1997)).

Lewis and Cerrato (1997) suggested that the transparency of the shell and the width of a growth increment are providing somewhat different information Fig. 5. Tissue growth rate (mg per tidal cycle), shell growth rate about metabolic activity in intertidal Mya arenaria.

(mm per tidal cycle), and oxygen consumption rate (mg O2 per tidal They proposed that transparency of the shell re¯ects cycle) vs. temperature for Mya arenaria held under semidiurnal metabolic rate, while the width of the increment is an tidal conditions for 2±3 weeks on a fixed daily ration. Experiment integrated measure of metabolic activity over the was run as a randomized block design with five replicates of two clams per treatment. Clams were carefully matched to be of similar whole immersion period. Under their proposal, an size and weight. Error bars represent 1 S.E. (data from Lewis and animal could produce opaque, wide increments if it Cerrato (1997)). were metabolizing at a moderate rate over the whole immersion period. Deposition of translucent, thin contrast in winter and summer, as they should if shell increments would also be possible if the animal were transparency re¯ects metabolism (Fig. 1). Mytilus metabolizing at a high rate but was active during only edulis (Richardson, 1989) and Spisula subtruncata a small portion of an immersion period. During the (Richardson, 1988b) show similar seasonal variation. rest of the immersion period, activity levels might be This pattern is quite different than what would be reduced and dependent on anaerobic pathways. These expected from a link between shell growth and tissue two types of microgrowth patterns are observed in production, where winter and summer deposition spring and summer, respectively (Fig. 1b±d). This should have similar patterns since production is proposal, if correct, suggests that it may be possible usually low or negative during both seasons in tem- to estimate some components of metabolism from perate, intertidal environments. Cold winter tempera- information stored in the shell. Using the data col- tures limit production for many bivalve species in lected in their experiments from a wide range of temperate, intertidal environments, while low food temperature, emersion times and food concentrations, concentrations and high temperature limit production respiration rate did show a relationship to shell growth during the summer (Grif®ths and Grif®ths, 1987). rate (Fig. 6). R.M. Cerrato / Fisheries Research 46 (2000) 39±49 47

3. Conclusions environmental variability. Attempts to quantify both measures would be useful, but would require Otolith and shell growth patterns have a number of greater control in the thickness of otolith and shell common features. There are, however, enough differ- sections than is currently practiced. There are, ences demonstrated here to recommend against any however, no insurmountable problems in doing direct transfer of research ®ndings from one structure this. to the other. Both existing differences and similarities, 4. There is accumulating evidence that otolith and however, suggest areas where comparing the response shell patterns preserve records of physiological of the two systems to equivalent environmental for- activity in addition to environmental events. Rapid cing would be of interest. In particular: response in shell transparency to an abrupt change in temperature is very similar to the acute 1. Fish and bivalves co-occur in the same habitats, adjustment in respiration that occurs with short- but their growth rhythms appear to be entrained by term temperature changes (e.g., Grif®ths and different environmental factors. As a result, Grif®ths, 1987). While change in transparency comparative study presents an opportunity for seems to be immediate, adjustment in increment basic research into endogenous rhythms. Also, width and clarity seem to take several days after comparing patterns in ®eld collected individuals conditions are altered. Unraveling the way otoliths of both taxa from the same area might be very and shells are recording metabolic activity should informative, and provide opportunities for envir- be pursued. Several initial research lines would onmental reconstruction not otherwise possible, include investigating acute vs. acclimated re- e.g., the potential to separate causal factors sponses and examining the effects on deposition through differential responses recorded in otoliths of inhibiting the activity of metabolic enzymes and shells. In these studies, care should be such as carbonic anhydrase. exercised to compare otolith to inner shell layer growth patterns. Pannella (1971, 1974) was the ®rst to observe daily 2. The inability to determine the age of bivalve growth patterns in ®sh, and he was also the ®rst to larvae is troubling since it is not clear whether it is verify daily patterns in bivalve shells (Pannella and due to the minimal amount of research that has MacClintock, 1968). As far as I am aware, he has been been carried out or to a fundamental problem. Age the only individual to study both in any detail. It would estimation would stimulate early life history seem, therefore, that a comparative study is long research in bivalves, just as it did ®sh. Finding overdue and could uncover a whole host of new out that age estimation is not possible for clam phenomena, afford greater understanding of deposi- larvae would provide new insights into how tion processes, and ultimately provide additional uses endogenous rhythms and depositional mechan- for the growth patterns in both taxa. isms operate. Either outcome is valuable. 3. Investigators have paid considerable attention to the examination of increment widths, while Acknowledgements signi®cant information preserved in both transparency and increment boundary (i.e., D-zone) I thank R.W. Day, J.M. Kalish, and M.J. Kingsford morphology has been largely overlooked. Trans- for their thoughtful comments on the manuscript. parency has been especially neglected except as a indicator of a discrete event (i.e., annulus, spawning). Transparency has been clearly linked References to temperature change at a variety of time-scales, physiological stress, and metabolic rate. The Beckman, D.W., Wilson, C.A., 1995. Seasonal timing of opaque zone formation in fish otoliths. In: Secor, D.H., Dean, J.H., distinctness of the increment boundary or D-zone Campana, S.E. (Eds.), Recent Developments in Fish Otolith (Campana and Neilson, 1985) separating incre- Research. University of South Carolina Press, Columbia, SC, ments seems to be closely associated with pp. 27±43. 48 R.M. Cerrato / Fisheries Research 46 (2000) 39±49

Borrero, F.J., Hilbish, T.J., 1988. Temporal variation in shell and Hilbish, T.J., 1986. Growth trajectories of shell and soft tissue in soft tissue growth of the mussel Geukensia demissa. Mar. Ecol. bivalves: seasonal variation in Mytilus edulis L. J. Exp. Mar. Progr. Ser. 42, 9±15. Biol. Ecol. 96, 103±113. Brothers, E.B., Matthews, C.F., Lasker, R., 1976. Daily growth Hoff, G.R., Fuiman, L.A., 1993. Morphology and composition of increments in otoliths from larval and adult fishes. Mar. Fish. red drum otoliths: changes associated with temperature, Serv. Fish. Bull. 74, 1±8. somatic growth rate, and age. Comp. Biochem. Physiol. Campana, S.E., 1983a. Feeding periodicity and the production of 106A, 209±219. daily growth increments in the otoliths of steelhead trout House, M.R., Farrow, G.E., 1968. Daily growth banding in the shell (Salmo gairdneri) and starry flounder (Patichthys stellatus). of the cockle, Cardium edule. Nature 219, 1384±1386. Can. J. Zool. 61, 1591±1597. Hurley, G.V., Tremblay, M.J., Couturier, C., 1987. Age estimates of Campana, S.E., 1983b. Calcium deposition and otolith check sea scallop larvae (Placopecten magellanicus) from daily formation during periods of stress in coho salmon, Oncor- growth lines on shells. J. Northwest Atl. Fish. Sci. 7, 123±129. hynchus kitsutch. Comp. Biochem. Physiol. 75A, 215±220. Jablonski, D.J., Lutz, R.A., 1980. Molluscan larval shell morphol- Campana, S.E., 1984. Lunar cycles in otolith growth in the juvenile ogy: ecological and paleontological applications. In: Rhoads, starry flounder, Patichthys stellatus. Mar. Biol. 80, 239±246. D.C., Lutz, R.A. (Eds.), Skeletal Growth of Aquatic Organisms. Campana, S.E., Neilson, J.D., 1985. Microstructure of fish otoliths. Plenum Press, New York, pp. 323±378. Can. J. Fish. Aquat. Sci. 42, 1014±1032. Kalish, J.M., Beamish, R.J., Brothers, E.D., Casselman, J.M., Carter, J.G., 1980. Environmental and biological controls of Francis, R.I.C.C., Mosegaard, H., Panfili, J., Prince, E.R., bivalve shell mineralogy and microstructure. In: Rhoads, Thresher, R.E., Wilson, C.A., Wright, P.J., 1995. Glossary for D.C., Lutz, R.A. (Eds.), Skeletal Growth of Aquatic Organisms. otolith studies. In: Secor, D.H., Dean, J.M., Campana, S.E. Plenum Press, New York, pp. 69±114. (Eds.), Recent Developments in Fish Otolith Research. Carriker, M.R., 1961. Interrelation of functional morphology, University of South Carolina Press, Columbia, SC, pp. 723± behavior, and autecology in early stages of the bivalve 729. Mercenaria mercenaria. J. Elisha Mitchell Sci. Soc. 77, 168± Kennedy, W.J., Taylor, J.D., Hall, A., 1969. Environmental and 241. biological controls on bivalve shell mineralogy. Biol. Rev. 44, Cenni, S., 1991. Periodicity of growth line formation in larvae and 499±530. postlarvae of the hard clam (Mercenaria mercenaria). MS Kennish, M.J., 1976. Monitoring thermal discharges: a natural Thesis. Marine Sciences Research Center, State University of method. Underwater Nat. 9, 8±11. New York, Stony Brook, NY, 114 pp. Kennish, M.J., 1980. Shell microgrowth analysis: Mercenaria Cenni, S., Cerrato, R.M., Siddall, S.E., 1990. Periodicity of growth mercenaria as a type example for research in population lines in larval and postlarval shells of Mercenaria mercenaria. dynamics. In: Rhoads, D.C., Lutz, R.A. (Eds.), Skeletal Growth J. Shellfish Res. 8, 444±445. of Aquatic Organisms. Plenum Press, New York, pp. 255±294. Cerrato, R.M., Wallace, H.V.E., Lightfoot, K.G., 1991. Tidal and Kennish, M.J., Lutz, R.A., Rhoads, D.C., 1980. Preparation of seasonal patterns in the chondrophore of the soft-shell clam acetate peels and fractured sections for observation of growth Mya arenaria. Biol. Bull. 181, 307±311. patterns within the bivalve shell. In: Rhoads, D.C., Lutz, R.A. Clark II, G.R., 1968. Mollusk shell: daily growth lines. Science (Eds.), Skeletal Growth of Aquatic Organisms. Plenum Press, 161, 800±802. New York, pp. 597±601. Evans, J.W., 1972. Tidal growth increments in the cockle Kennish, M.J., Olsson, R.K., 1975. Effects of thermal discharges on Clinocardium nuttalli. Science 176, 416±417. the microstructural growth of Mercenaria mercenaria. Environ. Fritz, L.W., Haven, D.S., 1983. Hard clam Mercenaria mercenaria: Geol. 1, 41±64. shell growth patterns in Chesapeake Bay. Fish Bull. 81, 697± Lewis, D.E., Cerrato, R.M., 1997. Growth uncoupling and the 708. relationship between shell growth and metabolism in the soft Fritz, L.W., Lutz, R.A., 1986. Environmental perturbations shell clam Mya arenaria. Mar. Ecol. Progr. Ser. 158, 177±189. reflected in internal shell growth patterns of Corbicula Mosegaard, H., SvedaÈng, H., Taberman, K., 1988. Uncoupling of fluminea. Veliger 28, 401±417. somatic and otolith growth rates in Arctic Char (Salvelinus Gauldie, R.W., 1993. Polymorphic crystalline structure of fish alpinus) as an effect of differences in temperature response. otoliths. J. Morphol. 218, 1±28. Can. J. Fish. Aquat. Sci. 45, 1514±1524. Griffiths, C.L., Griffiths, R.J., 1987. Bivalvia. In: Pandian, T.J., Neilson, J.D., Geen, G.H., 1984. Effects of feeding regimes and Verberg, F.J. (Eds.), Animal Energetics, Vol. 2. Academic diel temperature cycles on otolith growth increment formation Press, New York, pp. 1±88. in juvenile chinook salmon (Oncorhynchus tshawytscha). Fish. Harvey, M., Vincent, B., 1990. Density size distribution energy Bull. 82, 165±177. allocation and seasonal variation in shell and soft tissue growth Pannella, G., 1971. Fish otoliths: daily growth layers and periodical at two tidal levels of a Macoma balthica (L.) population. J. Exp. patterns. Science 173, 1124±1126. Mar. Biol. Ecol. 142, 151±168. Pannella, G., 1974. Otolith growth patterns: an aid in age Helm, N.E., Malouf, R.E., 1983. Rate of production of external determination in temperate and tropical fishes. In: Bagenal, ridges in the bay scallop, Argopecten irradians. Am. Zool. 23, T.B. (Ed.), The Ageing of Fish. Old Working, Surrey, UK, 1024. pp. 28±39. R.M. Cerrato / Fisheries Research 46 (2000) 39±49 49

Pannella, G., 1980. Growth patterns in fish sagittae. In: Rhoads, Richardson, C.A., Crisp, D.J., Runham, N.W., 1979. Tidally D.C., Lutz, R.A. (Eds.), Skeletal Growth of Aquatic Organisms. deposited growth bands in the shell of the common cockle Plenum Press, New York, pp. 519±560. Cerastoderma edule. Malacologia 18, 277±290. Pannella, G., MacClintock, C., 1968. Biological and environmental Richardson, C.A., Crisp, D.J., Runham, N.W., 1980. An endogen- rhythms reflected in molluscan shell growth. J. Paleontol. 42, ous rhythm in shell deposition in Cerastoderma edule. J. Mar. 64±80. Biol. Assoc. UK 60, 991±1004. Parsons, G.J., Robinson, S.M.C., Roff, J.C., Dadswell, M.J., 1993. Richardson, C.A., Crisp, D.J., Runham, N.W., 1981. Factors influen- Daily growth rates as indicated by valve ridges in postlarval cing shell deposition during a tidal cycle in the intertidal bivalve giant scallop (Placopecten magellanicus) (Bivalvia: Pectini- Cerastoderma edule. J. Mar. Biol. Assoc. UK 61, 465±476. dae). Can. J. Fish. Aquat. Sci. 50, 456±464. Rosenberg, G.D., Hughes, W.W., 1991. A metabolic model for the Reznick, D., Lindbeck, E., Byrga, H., 1989. Slower growth results determination of shell composition in the bivalve mollusc, in larger otoliths: an experimental test with guppies (Poecilia Mytilus edulis. Lethaia 24, 83±96. reticulata). Can. J. Fish. Aquat. Sci. 46, 108±112. Secor, D.H., Dean, J.M., 1989. Somatic growth effects on the Rhoads, D.C., Lutz, R.A., 1980. Skeletal records of environmental otolith±fish size relationship in young pond reared Striped Bass change. In: Rhoads, D.C., Lutz, R.A. (Eds.), Skeletal Growth of Morone saxatilis. Can. J. Fish. Aquat. Sci. 46, 113±121. Aquatic Organisms. Plenum Press, New York, pp. 1±19. Secor, D.H., Dean, J.M., Campana, S.E. (Eds.), 1995. Recent Rhoads, D.C., Pannella, G., 1970. The use of molluscan shell Developments in Fish Otolith Research. University of South growth patterns in ecology and paleoecology. Lethaia 3, 143± Carolina Press, Columbia, SC, 735 pp. 161. Siddall, S.E., 1980. Effects of temperature and salinity on growth, Richardson, C.A., 1987a. Tidal bands in the shell of the clam Tapes survival, metamorphosis, and shell deposition of tropical philippinarum. Proc. R. Soc. Lond. B 230, 367±387. mussel larvae (Perna perna and Perna viridis). Ph.D. Thesis. Richardson, C.A., 1987b. Microgrowth patterns in the shell of the Rosenstiel School of Marine and Atmospheric Science, Miami, Malaysian cockle Anadara granosa (L.) and their use in age FL, 206 pp. determination. J. Exp. Mar. Biol. Ecol. 111, 77±98. Stequert, B., Panfili, J., Dean, J.M., 1996. Age and growth of Richardson, C.A., 1988a. Exogenous and endogenous rhythms of yellowfin tuna, Thunnus albacares, from the western Indian band formation in the shell of the clam Tapes philippinarum.J. Ocean, based on otolith microstructure. Fish. Bull. 94, 124±134. Exp. Mar. Biol. Ecol. 122, 105±126. Thompson, I., 1975. Biological clocks and shell growth in bivalves. Richardson, C.A., 1988b. Tidally produced growth bands in the In: Rosenberg, G.D., Runcorn, S.K. (Eds.), Growth Rhythms subtidal bivalve Spisula subtruncata. J. Mol. Stud. 54, 71±82. and the History of the Earth's Rotation. Wiley, London, Richardson, C.A., 1989. An analysis of the microgrowth bands in pp. 149±161. the shell of the common mussel Mytilus edulis. J. Mar. Biol. Umezawa, A., Tsukamoto, K., 1991. Factors influencing otolith Assn. UK 69, 477±491. increment formation in Japanese eel, Anguilla japonica T. and Richardson, C.A., 1996. Exogenous or endogenous control of S., elvers. J. Fish. Biol. 39, 211±223. growth band formation in subtidal bivalve shells. Bulletin de Wilbur, K.M., Saleuddin, A.S.M., 1983. Shell formation. In: l'Institute oceanographique. Monaco. Numero special 14 (4), Saleuddin, A.S.M., Wilbur, K.M. (Eds.), The Mollusca, Vol. 4. 133±141. Academic Press, New York, pp. 235±287.