Decreased Sr/Ca ratios in the otoliths of two marine eels, Gymnothorax reticularis and Muraenesox cinereus, during metamorphosis.

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INTRODUCTION

Otoliths are biomineralized aragonitic crystals com-posed of calcium carbonate with a small quantity of organic matrix (Degens et al. 1969) that occur in the otic vesicles of teleost fishes and play a role in hearing and balance. They are deposited daily in alternating protein-rich and carbonate-rich layers as the fish grow (Pannella 1971). This variable deposition enables the determination of daily fish ages and study of their early growth history.

During otolith formation some trace elements are occasionally co-precipitated with calcium carbonate (Campana 1999). Strontium (Sr) is one of the most com-mon elements replacing calcium (Ca) in otoliths be-cause of its similar ionic radius, valence and chemical activity (Amiel et al. 1973). The incorporation of Sr into the otolith is a complex biogeochemical process that is influenced by physiological and environmental factors

(Kalish 1989, 1991, Radtke & Shafer 1992, Sadovy & Severin 1992). The Sr/Ca ratios in the otoliths of Japan-ese eels Anguilla japonica drastically decrease when the eel larvae pass through a salinity gradient during migration from spawning ground to estuary while simultaneously transitioning from the leptocephalus to glass eel developmental stage (Tzeng & Tsai 1994). Otake et al. (1994) suggested that this sharp decrease in Sr/Ca ratios marks the onset of metamorphosis. However, no direct evidence was given to validate this claim.

To evaluate whether salinity or developmental stage transition is responsible for in the drastic decrease of Sr/Ca ratios during metamorphosis in anguillid eels, we examined Sr/Ca ratios in the otoliths of the moray eel Gymnothorax reticularis and the pike eel Murae-nesox cinereus, marine species that spend their entire lives in the ocean (Shen 1993, Nelson 1994). Both eels metamorphose from leptocephalus to glass eel in

sea-© Inter-Research 2005 · www.int-res.com *Corresponding author. Email: wnt@ccms.ntu.edu.tw

Decreased Sr/Ca ratios in the otoliths of

two marine eels,

Gymnothorax reticularis and

Muraenesox cinereus, during metamorphosis

Y. J. Ling

1

, Y. Iizuka

2

, W. N. Tzeng

3,

*

1Department of Life Sciences, College of Life Science, National Taiwan University, Taipei 106, Taiwan, ROC 2Institute of Earth Sciences, Academia Sinica, Nankang, Taipei 115, Taiwan, ROC

3Institute of Fisheries Science, College of Life Science, National Taiwan University, Taipei 106, Taiwan, ROC

ABSTRACT: Sr/Ca ratios in the otoliths of 2 marine eels, the moray eel Gymnothorax reticularis and the pike eel Muraenesox cinereus, decreased greatly when the crystal structure of otolith daily growth increments changed from concentric to radiate form. This decrease is proposed to correspond to the timing of metamorphosis from the leptocephalus to glass eel stage, similar to freshwater eels (Anguilla spp.). In freshwater eels, ontogenetic and habitat shifts might influence the decrease. How-ever, marine eels do not migrate into freshwater after completing metamorphosis, so the decrease in these species must be the result of metamorphosis-related physiological, rather than environmental, effects. The mean age at metamorphosis of the moray eels was significantly lower than that of pike eels, and both were lower than that of freshwater eels (p < 0.05). Consequently, the spawning ground of marine eels is presumed to be closer than that of freshwater eels to the continental shelf.

KEY WORDS: Otolith · Sr/Ca ratio · Growth increment · Daily age at metamorphosis · Gymnothorax reticularis · Muraenesox cinereus

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water and do not migrate to brackish water after meta-morphosis (Devadoss & Pillai 1979, Masuda & Allen 1993). Therefore, if the Sr/Ca ratios in otoliths of the marine eels also decrease greatly at metamorphosis, then we can confirm that the similar decrease in Sr/Ca ratios in the otoliths of freshwater eels is caused by physiological rather than environmental factors.

MATERIALS AND METHODS

Forty moray eels and 31 pike eels were collected from the landing of the local trawler at the fish market in the Da-Shi fishing port, I-Lan Prefecture, northeast-ern Taiwan from May to September 2002. The fishing ground of the trawl fisheries was around Turtle Moun-tain Island (Guishandao) off the prefecture (Fig. 1). After collection, the eels were immediately preserved, brought back in ice and then frozen at –20°C in the laboratory. Both species were identified using morpho-logical characteristics (Shen 1993). The total length and body weight were measured to the nearest 0.1 mm and 0.1 g, respectively. Sagittal otoliths were removed for microstructural and microchemical analyses.

The otoliths were embedded in epofix resin, ground and polished with sandpapers of 1500 and 2400 grit until the primordia were exposed. They were then washed with distilled water, dried at 80°C in an oven overnight and coated with carbon. The Sr and Ca concentrations were measured from the otolith pri-mordium to the edge by Electron Probe Microanalyzer (EPMA, JEOL JXA-8900R) with an electron beam condition of 15 kV and 5 nA, beam size 10 µm, at a measuring interval of 10 µm.

After EPMA analysis, 23 moray and 18 pike eel otoliths were randomly selected for microincrement analysis. They were repolished to remove the carbon coating, etched with 0.05 M HCl for 30 s, and then dried in the oven and coated with gold for scanning electron microscope (SEM) analysis to reveal the growth microincrements. The growth microincrements in the otoliths of these 2 marine eels were assumed to be deposited daily, as for other eels (Mochioka et al. 1989, Umezawa et al. 1989). The daily age of the eels at metamorphosis was determined from the growth microincrements counted from the primordium to the growth check (GC), where Sr/Ca ratios decreased greatly and the growth mircoincrements changed from a circular to a radiate pattern. The GC was assumed to be deposited at metamorphosis, similar to Japanese eel Anguilla japonica (Cheng & Tzeng 1996). The maxi-mum radius from the primordium to the GC (Rm) was

divided by the corresponding daily age (Tm) to

esti-mate the mean daily otolith growth rate (Gm) of the eels

in the leptocephalus stage. The mean incremental

widths were measured from the primordium to the GC with an increment interval of 5 and evaluated to reveal their early life history.

The differences in age at metamorphosis, Rmand Gm

between the 2 species were examined by analysis of variance (ANOVA). Data on Japanese eels Anguilla japonica (Cheng & Tzeng 1996) were adopted to enable further comparisons with the 2 marine eels.

RESULTS

Otolith microstructure and age at metamorphosis

The general otolith microstructure was similar for moray eel and pike eel (Fig. 2). Concentric rings appeared from the primordium to the growth check (GC). Beyond the GC, the growth pattern changed to radiate and the growth increments became unclear and uncountable. The GC was considered to be deposited at metamorphosis. The patterns of otolith increment width and age at metamorphosis were dif-ferent for these 2 marine eels (Fig. 3).

Fig. 1. Sampling area of moray eel Gymnothorax reticularis

and pike eel Muraenesox cinereus in waters around Turtle

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In moray eels, the otolith increment width increased rapidly until the mean age at metamorphosis and decreased beyond that age. The minimum age at metamorphosis in moray eels ranged from 24 to 48 d. The discrepancy in age at metamorphosis among

indi-viduals led the standard error in increment width to increase from the 24th day. In pike eels increment width remained relatively constant, and the increase was not obvious before the mean age at metamorpho-sis, 65 d. The minimum age at metamorphosis in pike eels was 38 d, but most were between 50 and 70 d. The increment width was relatively larger for the specimen metamorphosed at the 103rd day.

Variations in Sr/Ca ratios

The otolith Sr/Ca ratios of the moray eel increased from ca. 7.5 × 10– 3in the primordium to a maximum of

9.5 × 10– 3 around the GC and then decreased to

4.0× 10–3 (Fig. 4). The timing of the decrease in Sr/Ca

ratios coincided with the appearance of the GC (Fig. 2a), after which the ratios fluctuated between 4.0 and 9.0 × 10– 3. The Sr/Ca ratios in pike eel otoliths

increased similarly from 8.0 × 10– 3in the primordium to

a peak of 9.0 × 10– 3at the GC, then decreased sharply

to ca. 4.0 × 10– 3, after which they fluctuated between

3.0 and 6.5 × 10– 3(Fig. 4). Thus, the Sr/Ca ratios in the

otoliths of both marine eels decreased greatly at the GC, which was assumed to be deposited during meta-morphosis.

Comparison of age at metamorphosis and growth rates

The mean daily age of moray eels at metamorphosis was 37 d, which was significantly smaller than that of pike eels (66 d), and both were significantly smaller than that of Japanese eels Anguilla japonica (116 d) (F = 60.05, p < 0.001). Conversely, the mean maximum otolith radius from the primordium to the GC for moray eels was 98.1 µm, which was significantly larger than that of pike eels (66.1 µm) (F = 36.32, p < 0.001) but similar to that of the Japanese eel (105.5 µm) (p > 0.05). Furthermore, the mean otolith growth rate of moray eels before GC (2.7 µm d–1) was significantly larger

than that of pike eels (1.0 µm d–1) (Table 1) and

Japan-ese eels (0.9 µm d–1) (F = 14.98, p < 0.001) but showed

no significant difference between pike eels and Japan-ese eels (p > 0.05).

DISCUSSION

In general, the otolith microstructure and the Sr/Ca ratios around the GC in the otoliths of both moray eels and pike eels were similar to those around the meta-morphosis check of anguillid eels such as Anguilla japonica (Tzeng 1990), A. rostrata and A. anguilla Fig. 2. (a) Gymnothorax reticularis, and (b) Muraenesox

cine-reus. SEM microphotographs showing changing pattern and

growth check (GC) of daily growth increments in otoliths of moray eel (total length [TL] = 464.09 mm, body weight [BW] = 144.6 g) and pike eel (TL = 497.47 mm, BW = 189.05 g). P = primordium. Square spots indicate where Sr/Ca ratios

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(Wang & Tzeng 2000) and marine eels such as Conger conger (Correia et al. 2003), C. oceanicus (Correia et al. 2004) and C. myriaster (Lee & Byun 1996, Otake et al. 1997). Thus, we believe that the GC in the otoliths of the moray and pike marine eels will have been deposited during the metamorphosis from lepto-cephalus to elvers.

Japanese eels and both marine eels all have a similar temporal change in otolith Sr/Ca ratios, which greatly decrease at metamorphosis. After metamorphosis,

Japanese eels migrate toward an estuary where salinity is lower (Tzeng & Tsai 1994, Cheng & Tzeng 1996). Consequently, environ-mental effects on the large decrease in otolith Sr/Ca ratios cannot be excluded because for Japanese eels they decreased as salinity decreased (Tzeng 1996, Tzeng et al. 2002). In contrast, the marine-resident moray eels and pike eels did not migrate toward an estuary after metamorphosis. Thus, the large decrease in otolith Sr/Ca ratios of both marine eels at metamorphosis may be attributed to physiolog-ical rather than environmental effects. This hypothesis was also strengthened by the find-ing that seawater-resident freshwater eels did not enter freshwater but their Sr/Ca ratios around the GC in the otolith of the eel de-creased (e.g. Tzeng et al. 2000).

Pfeiler (1984, 1986, 1991) found large amounts of glycosaminoglycans (GAG) in the extracellular gelatinous matrix of leptocephali. GAG have high affinity for Sr (Nishizawa 1978), and thus the higher content of GAG in the leptocephali might promote the uptake of Sr in the body and subsequent deposition in otoliths. Pfeiler (1986) divided the lepto-cephalus stage into 2 phases: phase 1, growth of fish length; phase 2, metamorphosis from leptocephalus to glass eel, in which the body length does not increase and may even decrease. Bishop et al. (2000) further parti-tioned phase 1 into 2 subphases based on metabolic energy use. Subphase 1, use of metabolic energy mostly for body growth; sub-phase 2, energy storage, in which the extracel-lular gelatinous matrix, including GAG, is accumulated to meet the huge energy require-ments for metamorphosis. Thus, the amount of GAG in the body reaches its maximum before metamorphosis and consequently also the Sr/Ca ratios in the otoliths of leptocephali. Metamorphosis consumes large amounts of extracellular gelatinous matrix and subse-quently causes a decrease in GAG in the body. The decrease in the corporal GAG leads to a reduction in a fish’s ability to absorb Sr, and thus the Sr/Ca ratios in leptocephalus otoliths dramatically decrease during metamorphosis, as previous sug-gested by Otake et al. (1997).

The huge release of energy from the breakdown of GAG at metamorphosis from leptocephalus to glass eel would cause an enhanced ossification to meet the demands for recombination and reconstruction of body structures. This might also be a factor leading to in-creased otolith growth rates, represented by the wider 0 2 4 6 8 10 12 100 90 80 70 60 50 40 30 20 10 0 Age in days

Mean incremental width (

μ m d –1 ) 0 0 1 2 3 4 5 6 7 8 9 10 1000 1500 500 2000

Distance from primordium (μm)

Sr/Ca ratios (

×

1000)

Fig. 3. Gymnothorax reticularis and Muraenesox cinereus. Mean (± SD)

daily growth increment width measured along maximum otolith radius from primordium to GC for moray eels (n = 18, thick line) and pike eels (n = 15, thin line). Arrows = mean daily age at GC of 37 and 66 d, for

the 2 species respectively

Fig. 4. Gymnothorax reticularis and Muraenesox cinereus. Temporal

changes in Sr/Ca ratios, composed of averages of 3 measured values from primordium to otolith edge for moray eel (thick line) and pike eel

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incremental widths during otolith growth around the GC. Additionally, Yamono et al. (1991) found that thyroid hormones increased in metamorphosing, and this increase may lead to the rapid otolith growth rate at metamorphosis (Shiao & Hwang 2004).

Pfeiler (1986) indicated that the amount of NaCl in the body fluid of leptocephali decreased at metamor-phosis. The metamorphic leptocephali had lower and less variable osmolarities of body fluid (Hulet & Robins 1989), and the osmoregulation-related cells, the chlo-ride-type cells, were found in the integuments of the phase II leptocephali of Albula sp. (Pfeiler & Lindley 1989), suggesting that the ability to osmoregulate becomes stronger in metamorphosis. This may also cause the decrease in Sr uptake and subsequent depo-sition in the otolith. Consequently, it is possible that not only does the GAG break down but the enhanced osmoregulation influences the variability in otolith Sr/Ca ratios of eels during metamorphosis.

The daily ages at metamorphosis of moray eels and pike eels were significantly smaller than that of Japan-ese eels (Cheng & Tzeng 1996). The age at metamor-phosis and growth rate of leptocephali of Japanese eels plays an important role in determining their dispersal distance when leptocephali are transported by oceanic currents from the oceanic spawning ground toward the nursery ground (Cheng & Tzeng 1996, Wang & Tzeng 1998, 2000, Shiao et al. 2002). Moray eels metamor-phosed at a younger age than did pike eels and Japan-ese eels, which implies that the spawning grounds of moray eels and pike eels are less distant than that of Japanese eel. It might also be very difficult for moray and pike leptocephali to drift as far as Japanese eel leptocephali, which hatch in and migrate from the west of the Mariana Islands (Tsukamoto 1992). Pike eels and moray eels may spawn near the continental shelf and

migrate a much shorter distance than freshwater eels. McCleave (1993) proposed that leptocephali that metamorphose at a young age might favor short-distance migration, while those that are older at meta-morphosis might favor migration. Thus, instead of a distant dispersal, the moray eel that metamorphoses at a much younger age than Japanese eels might ‘choose’ to stay closer to the continental shelf grounds. This implies the adoption of different migration and meta-morphosis strategies.

The mean otolith daily growth increment width and its variability in moray eels during early development are more apparent than for pike eels, indicating that the growth rates of moray eels may be higher and more variable. Moreover, moray eels may inhabit a more variable shallow-water marine environment that is nutrient-rich but fluctuates greatly in environmental conditions such as water temperature due to the influ-ence of a nearby continent. Thus moray eels may have evolved to a shorter larval duration, and higher and varied larval growth in order to pass from a pelagic to a benthic habitat as soon as possible.

Acknowledgements. This survey was supported by a Summer

Students Program of the National Science Council, ROC (No. 91CFA0100082). We thank Miss C. Y. Lin, College of Life Sci-ence, National Taiwan University (NTU), and Ms. S. J. Jih, College of Agriculture, NTU, for their help with SEM photog-raphy and the fishermen at the Da-Shi fishing port for provid-ing samples. We are also grateful to all our colleagues at the Fishery Biology Laboratory, Institute of Fisheries Science, NTU, for providing technical and skills assistance for otolith preparation and analysis. Special thanks to Mr. B. M. Jessop and 4 anonymous reviewers for their useful comments in the early drafts of the manuscript.

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Editorial responsibility: Otto Kinne (Editor-in-Chief), Oldendorf/Luhe, Germany

Submitted: November 23, 2004; Accepted: July 17, 2005 Proofs received from author(s): November 11, 2005

數據

Fig. 1. Sampling area of moray eel Gymnothorax reticularis and pike eel Muraenesox cinereus in waters around Turtle
Fig. 1. Sampling area of moray eel Gymnothorax reticularis and pike eel Muraenesox cinereus in waters around Turtle p.2
Fig. 3. Gymnothorax reticularis and Muraenesox cinereus. Mean (± SD) daily growth increment width measured along maximum otolith radius from primordium to GC for moray eels (n = 18, thick line) and pike eels (n = 15, thin line)
Fig. 3. Gymnothorax reticularis and Muraenesox cinereus. Mean (± SD) daily growth increment width measured along maximum otolith radius from primordium to GC for moray eels (n = 18, thick line) and pike eels (n = 15, thin line) p.4
Fig. 4. Gymnothorax reticularis and  Muraenesox cinereus. Temporal changes in Sr/Ca ratios, composed of averages of 3 measured values from primordium to otolith edge for moray eel (thick line) and pike eel
Fig. 4. Gymnothorax reticularis and Muraenesox cinereus. Temporal changes in Sr/Ca ratios, composed of averages of 3 measured values from primordium to otolith edge for moray eel (thick line) and pike eel p.4

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