Marine Biology (2002) 141: 315–319 DOI 10.1007/s00227-002-0820-y
T. Arai Æ A.V. Levin Æ A.N. Boltunov Æ N. Miyazaki
Migratory history of the Russian sturgeon Acipenser guldenstadti in the Caspian Sea, as revealed by pectoral fin spine Sr:Ca ratios
Received: 16 April 2001 / Accepted: 10 February 2002 / Published online: 6 April 2002 Springer-Verlag 2002
Abstract Ontogenic patterns of change in pectoral fin spine Sr:Ca ratios were examined in the Russian sturgeon Acipenser guldenstadti from the Caspian Sea. Pectoral fin spine Sr:Ca ratios of the sturgeon fluctuated strongly along the life history transect in accordance with the migration pattern from freshwater to sea (brackish) water habitats, i.e. all specimens exhibited a typical anadromous pattern in the ratio. Several specimens showed two transition points in pectoral fin spine Sr:Ca ratios from low ratios to high, indicating that those specimens had a flexible migration strategy in the ambient water, and could migrate downstream to the Caspian Sea multiple times after spawning.
Introduction The Russian sturgeon Acipenser guldenstadti, a semianadromous fish found in the Black, Azov, and Caspian Seas, migrates to the adjacent rivers for spawning (Doroshov 1985). However, some non-migrating (landlocked) individuals remain in freshwater as a fluvial form. The decision for sea-run or freshwater residence is based on individual growth history, sex, and ambient environmental conditions (Doroshov 1985). Thus, the Communicated by T. Ikeda, Hakodate T. Arai (&) Æ N. Miyazaki Otsuchi Marine Research Center, Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan E-mail:
[email protected] Tel.: +81-193-425611 Fax: +81-193-423715 A.V. Levin Caspian Scientific Research Institute of Fisheries, 414056 Astrakhan, Russia A.N. Boltunov All-Russian Research Institute for Nature Protection, Znamenskoe-Sadki 113628 Moscow, Russia
migratory pattern over the life cycle is variable and complicated. Information on individual migratory histories would provide basic knowledge for both fish migration studies and fishery management, allowing effective and sustainable use of the Russian sturgeon resources. Recent chemical analytic techniques have enabled identification of life history events in individual fish by detecting trace elements in the microstructure of their otoliths (Kalish 1989; Radtke 1989; Radtke et al. 1990). Oxygen isotopic ratios (Nelson et al. 1989; Tsukamoto et al. 1989) and strontium (Sr) incorporation (Kalish 1989; Radtke 1989; Radtke et al. 1990; Secor et al. 1995; Arai et al. 1997) in fish otoliths are of special interest because of their potential utility as indicators of past environmental (temperature, salinity) and physiological conditions (ontogeny, migration). The deposition of strontium (Sr) and calcium (Ca) in fish otoliths during growth varies between freshwater and marine habitats (Kalish 1989, 1990; Radtke 1989; Secor et al. 1995; Arai and Tsukamoto 1998; Tsukamoto et al. 1998; Tzeng et al. 2000; Tsukamoto and Arai 2001). Arai and Miyazaki (2001) examined the otolith Sr:Ca ratio of Russian sturgeon collected in a coastal area of the Caspian Sea. They found that the otolith Sr:Ca of the sturgeon fluctuated strongly along the life history transect in accordance with the migration pattern, i.e. all specimens exhibited a typical anadromous pattern in the ratio. In addition to otoliths, the pectoral fin spine, a bony structure in the pectoral fin, holds a potential historical record of physiological and environmental influences. Sr is easily substituted for Ca and is deposited in fish scales as well as otoliths in proportion to the Sr:Ca ratio of the water in which the organism lives (Coutant and Chen 1993). Furthermore, Sr is easily incorporated into bone (Yamada et al. 1987; Koch et al. 1992). Therefore, fin spine material deposited while the Russian sturgeon are in an estuary or at sea would be expected to contain correspondingly higher concentrations of Sr than fin spine material deposited when an individual is living in freshwater.
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Otoliths of sturgeon are irregularly shaped (Stevenson and Secor 1999; Arai and Miyazaki 2002), and no studies have yet validated the periodicity of annulus deposition in sturgeon, though clear translucent and opaque zones were found to be deposited in the Russian sturgeon (Arai and Miyazaki 2002). Pectoral fin spine sections in sturgeon have been preferred for determination of age because the annuli in sections can be consistently interpreted (Rien and Beamesderfer 1994; Stevenson and Secor 1999), and fin spines are easily collected and processed without the sacrifice of fish. Therefore, the pectoral fin spine seems to have greater potential as a convenient and powerful tool with which to reconstruct the individual migratory history, as well as life history traits and ontogenic development, than does the otolith. The objective of the present study was to describe the ontogenic changes in the pectoral fin spine Sr:Ca ratios of the Russian sturgeon, and to examine the usefulness of this technique in reconstructing the migratory history of the species.
epoxy resin (Strues, Epofix), mounted on glass slides, and ground using a grinding machine equipped with a diamond cup-wheel (Struers, Discoplan-TS). After being polished with 6- and 1-lmgrain diamond paste on a polishing wheel (Strues, Planopol-V), they were cleaned in an ultrasonic bath, then rinsed with deionized water. Pectoral fin spine X-ray microprobe analysis For electron microprobe analyses, 18 pectoral fin spines (5 subadult specimens, 13 adults) were given a Pt-Pd coating by high vacuum evaporator. Sr and Ca concentrations were measured along the longest axis of the pectoral fin spines, from the center to the edge (Fig. 1), using a wavelength dispersive X-ray electron microprobe (JEOL JXA-8900R), as described by Arai et al. (1997, 2000, 2001) and Arai and Miyazaki (2001). Calcite (CaCO3) and strontianite (SrCO3) were used as standards. Accelerating voltage and beam current were 15 kV and 1.2·10–8 A, respectively. The electron beam was focused on a point about 10 or 20 lm in diameter, with measurements taken at a 10 or 20 lm interval. Each datum point represents the average of three measurements of 4.0 s each. We reported Sr:Ca ratios as concentration ratios of Sr and Ca.
Results The representative life history transects in the Sr:Ca ratios of subadults (3 specimens) and adults (3 specimens) are shown in Figs. 2 and 3, respectively.
Materials and methods Fish and pectoral fin spine preparation According to Doroshov (1985), fish 15 years and older were classified as adults, and younger fish were considered subadults. Subadults of Acipenser guldenstadti were collected by gill nets in the coastal waters of the North Caspian Sea (Russia), 29 May–14 July 1987 (Table 1). Adults of the Russian sturgeon were collected by gill nets in the coastal waters of the North Caspian Sea (Russia), 25 May–2 July 1993. Pectoral fin spines were obtained from each fish after measurement of the total length (range: 40–167 cm) and were subsequently cross-sectioned. According to Rien and Beamesderfer (1994), we considered the number of rings of the sectioned pectoral fin spine to indicate the age of each specimen (Table 1). After determining the age in each specimen, the pectoral fin spine samples were stored in a desiccator until X-ray microprobe analyses were carried out in 2000. Then, the pectoral fin spines were embedded in
Table 1. Acipenser guldenstadti. Biological and sampling information for the Russian sturgeon collected in the Caspian Sea Fish number
Sampling date
Total length (cm) Age (years)
RuCA-1 RuCA-2 RuCA-3 RuCA-4 RuCA-5 RuCA-6 RuCA-7 RuCA-8 RuCA-9 RuCA-10 RuCA-11 RuCA-12 RuCA-13 RuCA-14 RuCA-15 RuCA-16 RuCA-17 RuCA-18
30 May 1987 1 Jun 1987 14 Jul 1987 29 May 1987 29 May 1987 8 Jun 1993 25 May 1993 2 Jul 1993 2 Jul 1993 24 Jun 1993 2 July 1993 30 Jun 1993 2 Jul 1993 18 Jun 1993 25 May 1993 18 Jun 1993 15 Jun 1993 2 Jul 1993
40 42 45 46 46 135 131 127 140 147 133 152 161 152 154 143 167 158
1+ 1+ 2+ 2+ 2+ 15+ 15+ 15+ 16+ 17+ 18+ 22+ 22+ 22+ 22+ 22+ 24+ 25+
Life history transects in subadults Pectoral fin spine Sr:Ca ratios from the subadult stage of the Russian sturgeon showed dramatic changes along the measured transect (Fig. 2). In all specimens examined (5 specimens), the pectoral fin spine Sr:Ca ratios dropped slightly, averaging 4.2·10–3 (range: 3.6–4.8· 10–3), from the center to the point at 440–680 lm. Subsequently, this ratio increased to a maximum level of approximately 8–12·10–3 around the outermost region. Some samples had high values but then a slight decrease at the edge to values similar to those of the center region (e.g. RuCA-3, RuCA-5 in Fig. 2). All subadult specimens showed changes in the Sr:Ca ratios that indicated at least a single movement from a habitat of one salinity to a habitat of another. Life history transects in adults In the adult stage, all specimens also had relatively low Sr:Ca ratios from the center region to the point 400–1340 lm, averaging 4.3·10–3 (range: 3.4–5.5·10–3) (Fig. 3). Subsequently, the patterns of these sturgeons were roughly divided into two types. The specimens with the first pattern (11 specimens) showed changes in the Sr:Ca ratios that indicated a single movement from one salinity habitat to another. Most of these specimens (7 specimens) showed a temporary increase in Sr:Ca ratios (maximum increase: around 6–9·10–3), then a gradual decrease around the outermost region (RuCA-7
317 Fig. 1. Acipenser guldenstadti. Photograph showing thin crosssection of pectoral fin spine. The Russian sturgeon (58.8 mm TL) was collected in a coastal area of the Caspian Sea (C center; E edge). Scale bar: 2000 lm
Fig. 2. Acipenser guldenstadti. Transects of pectoral fin spine Sr:Ca ratios of subadults measured with a wavelength dispersive electron microprobe, from the center to the edge. Number at the upper right indicates fish number
Fig. 3. Acipenser guldenstadti. Transects of pectoral fin spine Sr:Ca ratios of adults measured with a wavelength dispersive electron microprobe, from the center to the edge. Number at the upper right indicates fish number
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Fig. 3), although some specimens (4 specimens) showed an increase around the outermost region (RuCA-11 in Fig. 3). These latter specimens presumably went downstream to the Caspian Sea and settled in the sea habitat then returned to the estuary or freshwater habitat, where they were collected. The second pattern (2 specimens) is characterized by frequent transitions between freshwater, estuarine, and seawater habitats (RuCA-15 in Fig. 3). These specimens showed two peaks with values >6.0·10–3, and lower values in between.
Discussion This study confirmed that pectoral fin spine Sr:Ca ratios in the Russian sturgeon Acipenser guldenstadti reflected changes in ambient environmental conditions and could indicate habitat transitions, although the salinity in the Caspian Sea ranges from 0.2 to 12–13& (Golubev 1998). The Caspian Sea is brackish and has an estuarine character. All specimens had a transition point of pectoral fin spine Sr:Ca ratios from 4·10–3 to 6–12·10–3 in the life history transects, from the center to the edge (Figs. 2, 3). Veinott et al. (1999) estimated the individual migratory history of the white sturgeon Acipenser transmontanus by examining Sr concentrations in the pectoral fin spines by laser ablation–inductively coupled plasma–mass spectrometry. The patterns of Sr concentrations in the pectoral fin spines of the white sturgeon reflect similar changes in ambient environmental salinity, which are related to changes in the individual’s life history. Furthermore, many studies have shown that migrations to estuarine or marine environments produce 1.5- to 3-fold variation in the Sr:Ca ratios of the otolith (Kalish 1990; Secor et al. 1995; Radtke et al. 1996; Tzeng 1996; Arai and Tsukamoto 1998; Tsukamoto et al. 1998; Tzeng et al. 2000; Tsukamoto and Arai 2001; Arai and Miyazaki 2001). Tzeng (1996) showed that there was an approximate 1.5-fold difference in the Sr:Ca ratios from 4.2 to 6.5·10–3 between freshwater and brackish water. Thus, bone, scales, or otoliths produced in equilibrium with the water would be expected to show similar differences in Sr:Ca ratios. Indeed, the otoliths in Tzeng’s (1996) study, which were exposed to brackish and marine environments, did exhibit Sr:Ca ratios that were distinct and similar to the ratios found in the waters to which they were exposed. Therefore, the Sr:Ca ratios of 4·10–3 and 6–12·10–3 in the pectoral fin spine in the Russian sturgeon might indicate a freshwater versus a brackish water environment, respectively. Nonetheless, we could not be sure that fin rays would incorporate Sr and Ca in the same proportions as otoliths. According to the previous study, all specimens in the present study might have experienced the sea environment at least one or two times following downstream migration. These findings suggest that Russian sturgeon have both flexible migration strategies, with a high degree of behavioral plasticity, and the ability to utilize the full range of salinity in the sea.
Despite the fact that all specimens were collected from the Caspian Sea, in several specimens a clear, high Sr:Ca ratio was not observed at the pectoral fin spine edge, though a slight increase was detected in other specimens. The former finding might be due to the low salinity (3.0–4.5&) of the coastal area of the Caspian Sea (Arai and Miyazaki 2001). Furthermore, some fluctuations in the Sr:Ca ratios were also observed in the estimated freshwater growth regions. Changes in otolith Sr:Ca ratios have been considered to be related not only to salinity but also to water temperature (Radtke et al. 1990; Townsend et al. 1995) and physiological factors such as growth and maturation (Kalish 1989). Similar effects may also influence incorporation in the pectoral fin spine. For greater accuracy, however, mark–recapture studies using micro-data loggers will be needed to determine the precise correspondence between fish movement and Sr:Ca ratios in the pectoral fin spine. The Russian sturgeon is known to have several spawning ecotypes, which differ in migration season and gonadal development stage at the initiation of upstream migration (Doroshov 1985). All sturgeon require a much longer time to reach sexual maturity and to complete the gametogenic cycle than do modern teleost fish (Doroshov 1985). The median age of fish at their first spawning varies from 5 to 25 years in different species, and is between 10 and 20 years in most species (Doroshov 1985). In the present study, several adult specimens (>20 years old) had multiple transition points in Sr:Ca ratios of the pectoral fin spine. Arai and Miyazaki (2001) also found multiple transition points in otolith Sr:Ca ratios in the Russian sturgeon. Therefore, these findings might also suggest that several specimens performed multiple downstream migrations after spawning in freshwater. All sturgeon have demersal eggs; the females broadcast their ova at a specific velocity of river current, and hatching occurs 5–10 days after fertilization in most sturgeon species (Doroshov 1985). Juvenile sturgeon remain in the lower reaches of rivers or in river deltas for a prolonged period of time, ranging from several months to several years (Doroshov 1985). This migratory history during the early stage was confirmed in pectoral fin spine microchemical analysis. In the present study, the data from RuCA-1, a 1-yearold fish (Fig. 2), had high Sr:Ca ratios after showing the lowest ratio in the center. This phenomenon indicated that the Russian sturgeon might migrate downstream to the Caspian Sea within a year after hatching, though some adult-stage specimens remained in the freshwater environment for over a year, based on findings that the transition point in pectoral fin spine Sr:Ca ratios was >5000 lm from the center and corresponded to an age of 1–2 years (Fig. 2). However, further studies are required on the growth patterns of pectoral fin spine and Sr metabolism in the spines in order to understand the minute ontogenic changes in the pectoral fin spine Sr:Ca ratios.
319 Acknowledgements This work was supported in part by grant-inaid nos. 07306022 and 13760138 from the Ministry of Education, Science, Sports and Culture, Japan.
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