The influence of temperature on the fluorine and calcium composition of fish scales

TISSUE AND CELL, 1990 22 (5) 645-654 0 1990 Longman Group UK Ltd.

R.

W. GAULDIE*,

THE INFLUENCE FLUORINE AND FISH SCALES Keywords:

G. COOTEt,

I. F. WEST*,

OF TEMPERATURE CALCIUM COMPOS

Fish scales, temperature,

teleost.

microprobe,

and R. L. RADTKE*

ON THE TION OF

IIt rine. calcium

ABSTRACT. Proton microprobe studies of the scales of the kahawai (Arripis rrurta) and the snapper (Chrysophrys auratus) showed non-linear changes in the fluorine to calcium ratm that increase with increasing temperature. but both species showed a differcnt temperature sensitivity. Fluorine and calcium levels vary within years from summer to winter by up to lOiIO%, making fluorine and calcium levels good markers of seasonal events.

Introduction

the dermis and epidermis (Lanzing and Wright, 1976) resulting in scale growth from both the internal (dermal) and external (epidermal) parts of the scale. Mineralisation results in two discrete mineral phases: large crystals of calcium phosphate, Mandl’s corpuscles, (Schdnbarner et al., 1981), and an amorphous calcium phosphate mineralisation front which follows closely the growing protein of the scale (Lanzing and Wright, 1976; Olson and Watabe. 1980). As they grow scales develop a succession of surface marks (particularly in the part of the scale buried in the dermis) which lead to a succession of circumferential lines. or annuli. The term, annulus, has become synonymous with an annual check, or narrow band of slow (or no) growth in the scale (e.g. see the glossary in Summerfelt and Hall, 1987). The usual English usage of annulus is that it is a space between two concentric circles on a plane. In terms of scales, this would lead to the linguistic contortion of an annulus between two annuli. The term, check, which would seem to have better antecedents for a narrowing due to slow growth has unfortunately come to refer to such narrowings that are not annual (e.g. spawning, tagging, etc. checks) leading to the cumbersome usage, annual annulus. To avoid confusion and abuse of the English language in this paper we refer to the con-

Fish scales are mineralised protein structures embedded in (and entirely derived from) the dermis and covered in life by a thin epidermis (Oosten, 1957). Early studies of fish scales were primarily concerned with their anatomy and fine structure (Baudelot, 1873). Later studies of fish scales, although still primarily concerned with structure, have proceeded in two different directions, classification and ageing; and the age-related problems of the growth of the scale itself (Adelman, 1987). Studies in classification have shown that although the degree, and kind, of mineralisation of scales varied widely amongst fishes (Goodrich, 1907), there were certain general features common to all scales. The common features include a basic structure of layered proteins arranged in a plywood-like arrangement of orthogonal layers found in most teleosts (L.anzing and Wright, 1976), and arranged in rotating layers in sarcopterygians (Meunier, 1981). The protein layers are deposited by scleroblasts from both * Oceanic Biology, Hawaii Institute of Geophysics, University of Hawaii, Honolulu, Hawaii 96822, U.S.A. t Institute of Nuclear Sciences, Private Bag, Gracefield, Lower Halt, New Zealand. $ MAFFish. P.O. Box 297, Wellington, New Zealand. Received 29 March 1990. Revised 2 June 1990. Accepted 2 June 1990. 645

GAULDIE

ventional annual annulus as an annual check to distinguish it from other checks. Denied the use of the word annulus, we will refer to the zone between annual check rings as the annual growth zone, rather than annulus increment (Newman and Weisberg, 1987). Each annual growth zone has been regarded as a measure of a year’s growth in many species of fish. Early growth studies used the annulus technique almost exclusively (Winge, 1915). However, in a review of ageing techniques, Graham (1929) pointed out that up to the time no ageing technique had been validated. In response to Graham’s criticisms, Dannevig (1933) published a study of scale and body growth in the cod in which the same fish were sampled at regular intervals and showed an irregular relationship between scale growth increments (the number of sclerites added on to the scale), body size and water temperature. Dannevig (1933) thought that these observations negated the validity of the scale ageing technique. Dannevig considered that the opaque zones observed in the otolith (although they could not be tested by the same method of direct observation) provided a more regular record of growth that made otoliths more suitable for ageing fish. Nevertheless, scales have continued to be used to age a wide variety of species (Kelley, 1988). In some fish, such as the sockeye salmon, scale-based and otolith-based ages have been very similar (Kim and Roberson, 1968), but in other species there have been large differences in the ages estimated from scales and otoliths (e.g. the kahawai Arripis truttu has scale-based maximum ages of up to 9 (Nicholls, 1973) compared to 22 for otoliths (Eggleston, 1975)). The scales of some species are inherently difficult to read because of poorly developed annual check rings (annuli), and in other cases, the so-called ‘erosion’ or ‘replacement’ scales have little indication of any check ring (annuli) pattern (Paul, 1976; Matlock et al., 1987). However, it is not the question of resolution of the annual check rings of scales that has made them a less popular source of age data than otoliths. The physiological sensitivity of scales to the growth rate of the fish has been seen to be a weakness in their continued use. Because scale growth is obviously tied to body growth it has been thought that low somatic growth rates may

etal.

lead to a loss, or indistinct, annual check rings during periods of slow growth, or no growth at all (Bucholz and Carlander, 1963); or, conversely, that unbroken growth continued through winter due to unusually warm environments (Kelley, 1988). Consequently the consistently younger average ages given by scale-based compared to otolith-based average ages, have been disregarded as being due to growth impairment of scales. Impairment which leads, in the opinion of those believing in older otolith ages, to compression, or unreadability, of the annual check rings at the edges of scales that older ages would imply. The relationship between scale and body growth is only a weakness in terms of legibility of the annual check. If the scale contained other seasonal information that could be used to validate annual checks, or even replace them, then the relationship between scale and body growth would be highly advantageous. Under such circumstances the scales would convey even more reliable information about variable growth rate as well as age (Newman and Weisberg, 1987). The elemental composition of scales has been shown to vary in response to environmental conditions. The strontium levels of scales were shown by Van Coillie and Rousseau (1984) to be different in samples from different geographical locations. The iron content of the scales of brown trout was shown by Bagenal et al., (1957) to be different between sea-run and freshwater fish. High levels of fluorine have been reported from the scales of the coelocanth Latimeria chalumnae (Cowgill et al., 1968). Fluorine also occurs in the scales of the hoki Macrurows novaezlandiae in which there are distinct patterns of high and low fluorine concentration across those parts of the scale in which annuli would normally be expected (Gauldie et al., 1990). In this study, the patterns of fluorine concentration in the scales of the kahawai (Arripis trutta) and snapper (Chrysophrys aurutus) are compared with ambient water temperature change. Materials and Methods

Scales were taken from individual specimens of kahawai (Arripis truttu: Arripidae) and snapper (Chrysophrys auratus: Sparidae)

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647

OF FISH SCALES

which had been kept in the Napier Aquarium (Napier, New Zealand). The kahawai was caught in December 1975 at about 24cm total length and held at the Napier Aquarium (pers. comm. W. Watkins & R. Yarrell, curators, Napier Aquarium, Napier. New Zealand). The fish died on 16 November 1987 at a length of 65.3 cm fork length. A sample of 25 scales was taken from an area caudal to the pectoral fin in the area of the lateral line canal about half-way between head and tail. This location has been shown to provide scales containing the best record of individual growth (Dannevig and Host, 1931). Three scales out of the 25 sampled showed clear annual check rings of the kind conventionally used in fish aging (Bagenal, 1974). The high proportion of scales without clear annual check rings (sometimes referred to as ‘erosion’ or ‘regenerated’ scales) in both kahawai and snapper (below) is not unusual (Paget, 1920) and does not reflect on the overall physiological condition of the fish. The snapper was caught in December 1975 at about 20cm total length and held at the Napier Aquarium (pers. comm. W. Watkin & R. Yarrell). The fish was sacrificed on 23 August 1988 at 67.2 cm fork length. A sample of 26 scales was taken from an area caudal to the pectoral fin in the area of the lateral line canal about half-way between head and tail. Five scales showed clear annual check rings of the kind conventionally used in ageing (Bagenal, 1974). One of these scales was used in this study. An ‘erosion’ scale was also examined. Both kahawai and snapper were maintained on diets developed by the aquarium. Snapper regularly spawn in season in the aquarium indicating a high standard of health and close correspondence to natural conditions. Water supply to the aquarium was taken from an outlet in the sea from which it was filtered and passed through the aquarium without heating or cooling. Daily temperature and salinity records have been maintained at the Napier Aquarium since 1977. Aquarium lighting followed the seasonal cycle of sunrise and sunset using lamps designed to simulate natural lighting. Scales were mounted on pin stubs with epoxy resin and scanned for fluorine and calcium at 50pm intervals on their upper

(epidermal) surface with the proton microprobe following the method of Coote, et al., (1982). After scanning, the scales were photographed and then sputter-coated with gold and photographed using a Philips 505 scanning electron microscope. Traces of ion counts from the proton microprobe were smoothed using the LOESS smoothing programme of the ‘S’ statistical package (Cleveland, 1979). Results

A method of ageing kahawai from scales has been described by Nicholls (1973). Measurement of the annual growth zone involves recognising true annual marks on the scale. However, the literature is not always clear on what constitutes an annual mark. Marks similar to the conventional annual marks can be introduced by the stress of tagging (Kelley, 1988) and a variety of other causes (Lee, 1920). It has been common in the literature to present an illustration of the scale which points to a series of marks that form a pattern with decreasing widths from the focus to the edge of the scale. Evidence has then been presented to argue (with limited success, according to Beamish and McFarland (1983)) a case for marks being annual. Most of such evidence depends on assigning a particular pattern of marks to a scale, because, (as with the check rings in otoliths (Gauldie, 1988)) there are no ultrastructural criteria to distinguish true from ‘false’ annual marks in scales (Lee, 1920; Paget, 1920). However, in the case of both kahawai and snapper approximate ages were already known and were used to calibrate annual marks. A ‘readable’ kahawai scale usually has a clear sequence of annual check rings from the focus to the edge of the scale (Nicholls, 1973), and a clear sequence of annual check rings were observed in scales from the kahawai used in this experiment. The first annual check ring in the kahawai scale is usually recorded in the period September to October in the year following hatching (Nicholls, 1973). This interpretation would indicate that the fish was spawned in 1973. When it was captured in 1975, the fish was about 25 cm fork length which would be consistent with the fish haveing been two years old at capture (Nicholls, 1973). We therefore

GAULDIE

648 3.0

~

2.0

et al.

Napier

Aquarum Stallon#3 PoveIiyBay

-5.0 1975

1976

1977

1976

1979

1960

1961

1962

1963

1964

1965

1986

1987

1988

Fig. 1. Deviations from mean temperature are shown for records kept at the Napier Aquarium and the air temperatures at the Poverty Bay station of the New Zealand Meteorological Service.

concluded that the check rings in the scale of the kahawai were annual marks. Measurement of the increments between scale annual check rings were therefore made in terms of a ‘growth year’ beginning on September 30, rather than a Julian year. Average monthly water temperatures were recorded at the Napier Aquarium from 1979 to 1988. Air temperature records from the Poverty Bay meteorological showed that Napier Aquarium water temperatures in 1979 were relatively colder than air temperatures, but generally the pattern of water

temperatures followed that of air temperature. The air temperature-water temperature relationship over the period 1981-1984 was used in place of Napier Aquarium water temperatures from 19761978 when records were not kept at the Napier Aquarium. Annual deviations of air (Poverty Bay) and water (Napier Aquarium) from the mean temperature are shown in Figure 1. The widths of the annual growth zones of the Kahawai scale are plotted in parallel with the annual water temperatures from 1976-1988 in Figure 2.

40

17

16 -30

Average v

(C)

temperature

Annuluswidth(pm)

-20

-10

IllI, 1974 19751976

19771978

19791980

1981 19821983

19841985

19861987

1988

Year

Fig. 2. Annulus (-+-) in micrometer units and average temperatures against growth years for a kahawai scale.

(-m)

are plotted

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Table 1 Age (years) 1. Length at age Napier Kahawai 2. Length at age eastern Australian Kahawai 3. Length at age New Zealand Kahawai (scales) 4. Length at age New Zealand Kahawai (otoliths)

8

9

10

11

12

13

43

47

53

59

63

65

50

49

52

1234567

13

22

26

29

31

34

38

18

28

34

42

45

48

52

16

24

28

37

43

49

51

53

53

52

16

24

28

37

41

44

45

44

50

50

Length is in cm. Length at age for the Napier specimen was from back calculation. Length at age for Australian kahawai was from a scale-based growth curves of the eastern sub-species from Nicholls (1973). Lengths at age for New Zealand Kahawai were from both scale-, and otolith-based age estimations in Eggleston (1975), New Zealand otolith ages continue to 22 years. Australian and New Zealand scale ages go up to their maximum; sizes are rounded to the nearest cm.

The widths of annual increments in the scale can be used to back calculate length-atage from the length of the fish when it died. As there is only one individual involved back calculation is of necessity by the regression method and not the preferred method of mixtures (Gutreuter, 1987). Lengths at age are shown in Table 1 for the sample Kahawai as well as lengths at age from growth curves for Kahawai from Nicholls (1973), and from Eggleston (1975). The specimen studies here was from the eastern sub-species (Whitley, 1951), the growth of both sub-species was described by Nicholls (1973).

Two overlapping proton microprobe traces were made from the first kahawai scale measuring calcium and fluorine counts at 15 pm intervals from the lateral lefthand corner towards the focus of the scale. Marked points along both traces allowed the two traces to be superimposed (Fig. 3). The fluorine to calcium ratio was calculated as the ratio of the approximate areas under the fluorine and calcium curves respectively. The fluorine to calcium ratio was then plotted against the annual temperature corresponding to the year represented by each annual increment (Fig. 4). Two other kahawai scales from the

.I100 -1000 900 900 0 -700 5 600 8

500 u. -IO0 -3rM 200 200

100

150

200

250

300

350

-100 -0 400

Pointnumber Fig. 3. Two proton microprobe traces have been joined to show the calcium (continuous line) and fluorine (dotted line) for each annulus corresponding to the years as marked, 1987 at the extreme left and 1975 at the extreme right.

650

GAULDIE

et al.

0.3

Q

e 0.2

0 Q

t 2

Q

KAHSD

l

KAHSF

6

KAHSE

0

ss4

0.1

Q

e* e 0.0

I.

12

I.

13

I.

14

4

00

I.

I.

15

16

I

17

Temperature (C) Fig. 4. The fluorine/calcium ratios for three different scales (KAHSD, KAHSF, taken from the same kahawai arc plotted against average annual water temperatures. calcium ratios for the snapper scale (SS4) are also plotted on the same graph.

same fish were scanned at different angles, cutting across annuli from different directions, thereby measuring the elemental composition corresponding to the same year, but in different parts of different scales. The fluorine to calcium ratio for these two otoliths was also plotted (in the same Fig. 4) against the annual water temperature corresponding to the year represented by each annual increment. The method of ageing snapper from scales has been described by a number of authors (Paul, 1976). A normal snapper scale was scanned across annual increments starting from the growing edge corresponding to years 1982-1988 and the corresponding fluorine to calcium ratios plotted against the annual temperature corresponding to each annual increment (Fig. 4). An ‘erosion’ or ‘replacement’ scale was scanned along the

KAHSE) Fluorine/

interior to exterior axis from the growing edge to the focus. the calcium counts along the trace showed a well developed series of peaks and troughs (Fig. 5). Comparison of average annual salinity with the fluorine to calcium ratio showed no relationship, the probability of significant regression was less than 0.001. Discussion

The amount of fluorine in the scale is very high, ranging from l-23% of the calcium content. Fluorine content of other marine organisms is lower, averaging about 300 ppm in foraminifera (Carpenter, 1969) up to 6~3% of the ash of brachiopods (Vinogradov, 1953), but levels in terrestrial tooth enamels are much lower, less than 2% (Legeros, 1981). However, the general mechanism of

TEMPERATURE

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OF FISH SCALES

1

7000 6500 600@

Point number Fig. 5. A calcium scan along the centre line of the ‘erosion’ scale showed a well-defined cycle of peaks and troughs. Arrows indicate putatwe ages.

fluorine uptake in tooth enamels is fairly well known (Legeros, 1981) and one may assume that similar mechanisms occur in scales. Scales are composed of layers of protein mineralised with calcium phosphate. The calcium phosphate in the scale sometimes occurs as single massive crystals, known as Mandl’s corpuscles (Schronborner et al., 1981), but generally calcium phosphate occurs as invasive amorphous crystals that form a mineralisation front close to the growing edge of the scale (Schbnborner et al., 1979). The crystals of tooth enamel are much more organised than those in scales, even though tooth enamel phosphates may have an initial amorphous phase (Young and Brown, 1981). Fluorine is thought to enter the interstices of hydroxy apatite crystals as a competitive replacement for the similar sized and less electronegative hydroxyl radical. The amorphous mineralisation front may simply allow more interstitial spaces, or equivalent surfaces, to become available resulting in higher levels of fluorine. Individual scales showed a strong pattern

in both fluorine and calcium counts, the signal-to-noise ratio for both fluorine and calcium was high and the variability in the signal was marked, highs and lows differing by up to 1000%. Fluorine generally tracked calcium as one would expect from a model of fluorine replacement of hydroxyl ions in calcium salts. Comparing the pattern of highs and lows in calcium and fluorine with the pattern of annual increments in the scales suggest that generally the highs and lows correspond to seasonal cycle in mineralisation. Plotting the fluorine to calcium ratio against the average annual temperatures of the years corresponding to the annual increments in the scale showed a weak, but positive, relationship. The variability in the fluorine to calcium ratio that was not accounted for by temperature was not due to salinity. That is not surprising because the uptake of elements out of seawater by organisms into mineralised tissues is typically highly non-linear against ambient concentrations (Milliman, 1974), and generally in fishes assimulation

GAULDIE et al.

efficiencies are less than 10% and highly variable among individuals (Cross et al., 1975). The uptake of fluorine out of solution into tooth apatite has been shown to behave asymptotically (Legeros, 1981). Uptake of fluorine into tooth apatite is limited at concentrations of about 2% fluorine to apatite. Although this is a much lower level than that observed in scales, the chemical mechanisms can be expected to behave in a similar way. Plotting the fluorine to calcium ratios to temperature in kahawai scales suggests some asymptotic behaviour in which upper temperature limits affect the rate of fluorine uptake. The process of calcium phosphate mineralisation must also act as a control on fluorine Calcium phosphate uptake. precipitation rates change by a factor of two for both temperature gradients (2X37.5”C) and pH gradients (pH 74pH 7.8) in inorganically precipitated calcium phosphates (Meyer and Nancollas, 1972). In poikilotherms pH is affected by temperature as well as metabolic acidosis which is itself temperature dependent. In scales there is direct evidence from glycine uptake studies that scale growth was affected by pH with maximum glycine uptake at pH7.7 and by temperature (Goolish and Adelman, 1983a, b). It is not surprising to find that there is a considerable variability in response to annual water temperature in both mineralisation and in consequent fluorine uptake into the calcium mineral. In addition, the physical dimensions of the annual increments vary in parallel with temperature. The change in width of annual increments affects both the measurement process (the proton microprobe beam remains the same width irrespective of the annual increment width) and the physical space within which the combined processes of protein deposition and mineralization must occur. Back calculation of length at age (Table 1) showed that the Kahawai used in this study grew more slowly than average lengths at age estimated from scales in both Australian and New Zealand Kahawai. This effect can be expected from back calculated length at age (Lee’s phenomena (Gutreuter, 1987)) and does not indigrowth due to cate abnormal any confinement in the aquarium. However, growth in 1985 and 1986 (Fig. 1) was obviously out of step with temperature as

was (apparently) growth in 1975. We interpret these out of phase growth periods as being caused by the inherently high growth of young fish (in 1975) and the effects of senilty in the old age of the fish in 1985 and 1986. The individual Kahawai used in this experiment was believed to have died of old age and its physical condition, particularly its otolith structure, has been described elsewhere (Gauldie et al., 1990b). Scales from the same individual vary considerably in size depending on the part of the fish from which they are sampled. Because scales are generally the same age, the different sizes must reflect differences in growth rate of individual scales from which one might reasonably expect differences in the response of the fluorine to calcium ratio to temperature. The most extreme inter-scale variability lies in the ‘erosion’ or ‘replacement’ scales. The erosion scale examined in this study showed a cycle of calcium counts similar to that found in normal scales suggesting that annual growth continues without necessarily forming annual check rings. It has generally been assumed in the literature that annual check ring formation is strictly related to growth. The erosion scale data suggests that this may not always be a correct assumption. If the peaks in calcium are counted literally from left to right (as indicated by the arrows in Fig. 5) then the narrow peaks would correspond to cooler years, indicating narrower annual increment widths with cooler years, but not necessarily lower calcium content. However, this may reflect the distance between proton beam observation points, very few of which fit into a narrow increment. Replacement scales lack annual checks that would allow calibration of this interpretation. Changes in fluorine concentrations in the calcium minerals offer some scope in validation of ageing methods based on scales with observable annual checks because of the potentially large inter-annual variation in fluorine and calcium. If the use of single scales can be justified by standardising the scale sampled within the species, then fluorine to calcium ratios may also be used to recover the temperature life history of a fish. Thus the growth-dependancy of scales that has qualified their use in ageing studies may be turned to advantage. However, scales as research objective in their own right offer

TEMPERATURE

ON COMPOSITION

OF FISH SCALES

some interesting problems such as the crystal/fluorine interaction and the transport of fluorine ions into the mineralising front. Acknowledgements

The authors wish to thank Kevin Mulligan of MAFFish, New Zealand and David Schafer, HIG, for their technical assistance. This paper was written while R. W. Gauldie was

653

Visiting Associate Ichthyologist at the Hawaii Institute of Geophysics, School of Ocean, Earth Sciences and Technology, University of Hawaii. This research was supported partly by MAFFish, New Zealand, the Institute of Nuclear Sciences, New Zealand and by NSF Grants OCF 88-00686 and INT 87-23084 made to Richard Radtke. This is School of Ocean, Earth Sciences and Technology contribution number 0000.

Adelman. I. R. 1987. Uptake of radioactive amino acids as indices of current growth rate of fish: a review. In: Age and growth of fish, Eds. R. C. Summerfelt and G. E. Hall. Iowa State University Press, Ames. Iowa. 65-79 pp. Bagcnal. T. B. 1974. The ageing of fish, The Proceedings of an International Symposium. Unwin Brothers Limited. Bagenal. T. B., Mackereth, F. J. A. and Heron. J. 1973. The distinction between brown trout and sea trout by the strontium of their scales. _I. Fish. Biol., 5, 555-5.57. Baudelot, M. E. 1873. Recherches sur le developpement, dcs Ccailles des poissons osseux. Arch. Zoo/. Exp. C&VI..2, 87-244. Beamish. R. J. and McFarland. G. A. 1983. The forgotten requirements for age validation m fisheries biology. 7ram Am. Fish. Sm.. 112, 73S-743. Bucholz. M. M. and Carlander, K. D., 1963. Failure of yellow bass, Roccus mississippwxsr.~. to form annuli. Traru Am. Fish. Sot., 92, 3X4-390. Carpenter, R. 1969. Factors controlling the marine geochemistry of fluorine. Geochim. Cosmochim. Acru., 33. I IL1167. Clcvcland, W. S. 1979. Robust locally weighted regression and smoothing scattcrpots. J Am. Star. A.ssoc.. 74, tiZY836. Coote, G. E., Sparks. R. J. and Blattner, P. lY82. Nuclear microprobe measurement of fluorine conccntratton profile\ with applications in archaeology and geology. Nucl. fnsrrum. Merh., 4, 197-221. Cowgill, U. M., Hutchinson, G. E. and Skinner, H. C. W. 1968. The elementary composmon of Lutinwria cha/umw~ Smith Proc. Nat. Acad. Sci. U.S.A., 60, 456463. Crwr, F. A.. Willis, J. N., Hardy, L. H., Jones, N. Y and Lewis, J. M. 1Y7S. Role of penile fish in cyclrng Mn. Fc, Cu and Zn in a coastal-plain estuary. In: Mineral cycling in a south-eastern ecosystem. Proceedings of a Symposium. CONF-740513, Oak Ridge, Tennessee, U.S. Energy Research and Development Admmistration. pp. 45-63. Danncvig. A. 1933. On the age and growth of the cod (G&u callerius L.) from the Norwegian Skagcrrack roast. Fiskeri. Skrifter. 4, %158. Danncvig. A. and Host, P. lY31. Sources of error in computing 11-l2 etc. from scales taken from different part, of the fish. J. Conseil.. 6, 64-93. Eggleston. D. 1975. Determination of age of kahawai Arripul mfta (Bloch & Schneider). N. Z. J. Mar. Prrsh~ Km 9, 293-298. Gauldie. R. W., West, 1. F.. Coote, G. and Radtke, R. L. 19Yoa. Seasonal and cnvironmcntal codes in the chcml\rr\ of the scales of the hoki (Macruronw nouaezelandiae) Tw. Cell, In Press. Gauldie. R. W.. Coote, G. and West, I. F. 1990b. A young fish with an old otolith. the Kahawai (Arripis rrurra). (‘an. J. Fish. Aquat. Sci. (In preparation). Gauldie. R. W. 1988. Similarities in fine structure of annual, and non-annual, check rings in the otolith of the New Zealand snapper (Chrysophrys auratus). N. Z. J. Mar. Freshw. Res.. 22, 273-278. Goodrich. E. S. 1907. On the scales of fish, living and extinct. and their importance in classification. I’roc. Zooi. .Soc Land., 2, 751-774. Goolish. E. M. and Adelman, R. I. 1983x Effects of fish growth rate. acclimation temperature and incubation temperature on in vitro glycine uptake by fish scales. Camp. Biochm. PhysuL 76, 127-134. Goolish. E. M. and Adclman, I. R. 1983b. l’C-glycine uptake by fish scales: refincmcnt of a growth index and eftcct\ of a protein-synthesis inhrhitors. Trans. Am. F&h. Sot., 112: 647-652. Graham. M. 1929. Studies of age determination in fish. Part 11. A survey of the literature. Fish. Invest. Series 111. Vol. XI. No 3.

654 Gutreuter, S. fish, eds: Kelley, D. F. U.K., 68,

GAULDIE

et al.

1987. Considerations for estimation and interpretation of annual growth rates. In: Age and growth of R. C. Summerfelt and G. E. Hall. Iowa State University Press, Ames, Iowa. pp. 115-126. 1988. Age determination in bass and assessment of growth and year-class strength. J. Mar. Biol. Ass. 179-214.

Kim, W. S. and Roberson, K. 1968. On the use of otoliths of sockeye salmon for age determination. In: Further studies of Alaska sockeye salmon. Ed: R. L. Burgner. Unioersity of Washingron Publications in Fisheries. New Series, 3, 14%168. Lanzing, W. J. R. and Wright, R. G. 1976. The ultrastructure and calcification of the scales of Tilapia mossambicn (Peters). Cell. Tim. Res., 167, 37-47. Lee, R. M. 1920. A review of the methods of age and growth determination in fishes by means of scales. Fish. Inuest., Series II, 4(Z), 33 pp. Legeros, R. Z. 1981. Apatites in biological systems. Prog. Crystal Growth Charact., 4, l-45. Matlock, G. C., Colura, R. L., Maciorowski, A. F. and McEachron, L. E. 1987. Use of on-going tagging programs to validate scale readings. In: Age and growth of fish, Eds. R. C. Summerfelt and G. E. Hall. Iowa State University Press, Ames, Iowa. pp. 279-286. Meunier, F. J. 1981. ‘Twisted plywood’ structure and mineralisation in the scales of a primitive living fish Amia c&a. Tissue and Cell, 13, 165-171. Meyer, J. L. & Nancollas, G. H. 1972. The effect of pH and temperature on the crystal growth of hydroxy apatite. Archs. Oral Biol., 17, 162%1627. Milliman, J. D. 1974. Marine carbonates. Springer-Verlag, Berlin, Heidelberg and New York. Newman, R. M. and Weisberg, S. 1987. Among- and within-fish variation of scale growth of fish. Eds. R. C. Summerfelt and G. E. Hall. Iowa State University Press, Ames, Iowa. pp. 159-166. Nicholls, A. G. 1973. Growth in the Australian ‘salmon’ Arripis m_ma (Bloch & Schneider). Ausr. J. Mar. Freshw. Res., 24, 15%176. Olson, 0. P. and Watabe, N. 1980. Studies on the formation and resorption of scales. IV. Ultrastructure of developing scales in newly hatched fry of the Sheepshead minnow Cyprinodon variegarus (Atheriniformes: Cyprinodontidae). Cell. Tim. Res., 211, 303-316. Oosten, J. Van. 1957. The skin and scales. In The Physiology ofFishes (Edited by Brown, M. E.). Acad. Press., New York. Paget, G. W. 1920. Report on the scales of some telostean fish with special reference to their method of growth. Fish. Invest., Series II, 4(3), 28 pp. Paul, L. 1976. A study on age, growth and population structure of the snapper Chrysophrys aurafw (Forster), in the Hauraki Gulf, New Zealand. New Zealand Fisheries Research Bulletin 13. Sch6nbGrner. A. A., Meunier, F. J. and Castanet, J. 1981. The fine structure of calcified Mandl’s corpuscles in teleost fish scales. Tiss. Cell., 13, 589-597. Van Coillie, R. and Rousseau, A. 1974. Composition minkale des Bcailles du Catastomus commersoni issue de dew milieu diffkrents: etude par microscopic Ctectronique analytique. .I. Fish. Res. Board Can., 31, 63-66. Vinogradov, A. P. 1953. The elementary composition of marine organisms. Sears Found. Marine Res. Mem., II, 647 PP. Whitley, G. B. 1951. New fish names and records. Proc. R. Sm. N.S. W., 1949-50, 61-68. Winge, 0. 1915. On the value of the rings in the scales of the cod as a means of age determination. Medelels. Fra. Komm. F. Havundersog., Bd IV., 39 pp. Young, R. A. and Brown, W. E., 1981. Structures of biological minerals. In: Biological mineralization and demineralization, Ed. G. H. Nancollas. Springer-Verlag. Berlin, Heidelberg and New York. 101-142 pp.