doi:10.1111/j.1095-8649.2011.02903.x, available online at wileyonlinelibrary.com
Migratory life history of European eel Anguilla anguilla
from freshwater regions of the River Asi, southern Turkey
and their high otolith Sr:Ca ratios
Y.-J. Lin*†, S. Yalc¸in- ¨
Ozdilek‡, Y. Iizuka§, A. G ¨
um ¨
us¸
and
W.-N. Tzeng*
*Institute of Fisheries Science, National Taiwan University, Taipei, Taiwan, ‡Anafartalar Campus, C¸ anakkale Onsekiz Mart University, C¸ anakkale, Turkey, §Institute of Earth Sciences,
Academia Sinica, Nankang, Taipei, Taiwan and Department of Biology, Ondokuzmayis University, Samsun, Turkey
(Received 10 May 2010, Accepted 24 December 2010)
Otolith Sr:Ca ratios from 32 of 34 European eel Anguilla anguilla collected from three freshwater sites in the River Asi, southern Turkey, indicated that they were resident in fresh water without apparent exposure to salt water since the elver stage. The Sr:Ca ratio criterion indicative of residence in fresh water was more than twice that of values from other European countries. Otolith Sr:Ca ratios of A. anguilla from fresh waters can vary among regions, possibly reflecting regional-specific water chemistry. Hence, the use of Sr:Ca ratios determined in one region to interpret results from a different region might lead to misclassification of migratory life-history types. © 2011 The Authors Journal of Fish Biology© 2011 The Fisheries Society of the British Isles
Key words: freshwater residence; life-history types; water chemistry.
INTRODUCTION
The European eel Anguilla anguilla (L.) is a catadromous species widely distributed in Europe (Dekker, 2003; Tesch, 2003). It is also found in Turkish rivers and streams draining into the Mediterranean Sea, Aegean Sea and parts of the Black Sea (K¨uc¸¨uk
et al., 2005; Yalc¸ın- ¨Ozdilek et al., 2006; Yalc¸ın- ¨Ozdilek & Solak, 2007). The otolith
Sr:Ca ratio is a powerful tool to distinguish the migratory life histories of fishes moving between freshwater and saltwater habitats (Campana, 1999). It has been used to reveal the complicated migratory life histories of A. anguilla in the yellow eel stage in many European countries (Tzeng et al., 1997, 2000; Arai et al., 2006; Daverat & Tom´as, 2006; Shiao et al., 2006; Lin et al., 2009).
It is unclear, however, whether the migratory life histories of A. anguilla in Turkish waters, the eastern limit of the species distribution, are similar to those from other countries. To classify the migratory life histories of A. anguilla, an otolith Sr:Ca ratio indicative of residence in fresh water, brackish water or sea water is needed.
†Author to whom correspondence should be addressed. Tel.: +886-2-33662887; email: YJLin01234@gmail.com
Extrapolating the criterion ratio from one region to another may, however, not be appropriate because of differences between regions in water chemistry, as found for the American eel Anguilla rostrata (Lesueur) (Jessop et al., 2008). Therefore, the objectives of this study were: (1) to identify the otolith Sr:Ca ratio indicative of residence in fresh water using A. anguilla collected from three freshwater sites in the River Asi in southern Turkey, (2) to examine their migratory life histories and (3) to compare the otolith Sr:Ca ratios used to classify migratory history types of A. anguilla among European regions.
MATERIALS AND METHODS
The River Asi (named Orontes in Syria) is c. 380 km in length (94 km in Turkey) and originates in central Lebanon and drains into the Mediterranean Sea at Samanda˘g (Hatay) in Turkey (36◦02N; 35◦57E). Annual precipitation is 400–800 mm, but rainfall is restricted to the rainy season from October to May, when the water temperature can drop to c. 16◦C. In the dry season (July to August), total precipitation is <50 mm with water temperatures varying around 27◦C (Yılmaz & Do˘gan, 2008; Hatay Directorate of Agriculture, 2003; unpubl. data). The width and depth of the river change considerably with the season. In the rainy season, the depth of the river may increase to over 2·5 m at a width of 35–45 m while in the hot and arid summer the depth is <1 m, with the riverbed often drying up completely. Some small freshwater streams feed into the lower Asi from the Ansariye Mountain, such that the mixing region of fresh water and sea water is restricted to <1 km upstream of the river mouth (S. Yalc¸ın- ¨Ozdílek, pers. obs.). Within the delta of the River Asi, A. anguilla is one of the most important commercial species for local consumption or export (Yalc¸ın, 1997).
A total of 34 yellow eels were collected from Demirk¨opr¨u on 10 April and from G¨uzelburc¸ and Samanda˘g on 10 July in 2007 (Fig. 1). Samples were collected by local fishermen using drift nets in Demirk¨opr¨u and fyke nets in G¨uzelburc¸ and Samanda˘g. The mean± s.d. electrical conductivity was 81·8 ± 7·0, 77·1 ± 6·6 and 68·6 ± 4·8 mS m−1 in Demirk¨opr¨u, G¨uzelburc¸ and Samanda˘g, respectively (Tas¸demir & G¨oksu, 2001), corresponding to a salin-ity of <0·5 (Anderson & Cummings, 1999). Therefore, these sampling sites were all in fresh water.
The total length (LT) of A. anguilla was measured to the nearest cm and mass (MT) to the nearest g. Sexes were determined by macroscopic examination (Tesch, 2003). The largest otolith (sagitta) was removed, air dried, embedded in Epofix resin (www.emsdiasum.com), then ground and polished until the core was exposed. The Sr:Ca ratios of the polished otoliths were measured by an electron probe microanalyser (EPMA, JEOL JXA-8900R; www.jeol.com) with a spot size of 10μm and interval of 10 μm, as detailed in Lin et al. (2009). The time represented by one spot might range from several days to perhaps months, depending on the distance from the core.
Fish otoliths are deposited daily (Campana & Thorrold, 2001), and thus the otolith edge is deposited on the day when the fish are caught. In other words, the nearer the measuring points are to the otolith edge, the better these points represent the water chemistry of the collection site. As the A. anguilla were all collected in freshwater habitats and the otolith Sr:Ca ratios were measured from the primordium to the edge, the last three points were used to calculate the value indicative of residence in fresh water.
Otolith Sr:Ca ratios were measured consecutively, meaning that the last three points were not independent and should be compared by repeated measure ANOVA (Elsdon et al., 2008). The ratios were not significantly affected by site, sex or site–sex interaction (all P > 0·5), and so the results were pooled. The mean+2 s.d. of the otolith Sr:Ca ratio from the last three points was used as the criterion for residence in fresh water following Shiao et al. (2006) and Tabouret et al. (2010). Sr:Ca ratios with two consecutive points above this value were considered as indicative of saltwater experience (Jessop et al., 2008). All computations were completed in R (version 2.8.1) (www.R-project.org). The significance level (α) was set at 0·05.
Mediterranean Sea Güzelburç Turkey Turkey Samandag Demirköprü Asi River N 36 ° 00′ E 36 ° 30′ E 37 ° 00′ E 36 ° 00′ N 36 ° 30′ N Syria
Fig. 1. Sampling sites (Samanda˘g, G¨uzelburc¸ and Demirk¨opr¨u) for Anguilla anguilla in the River Asi, southern Turkey. Scale bar= 10 km.
RESULTS
A total of 34 yellow A. anguilla, including 14 females, 15 males and five indi-viduals with undeveloped gonads, were collected from three sites in the River Asi (Table I). The otolith Sr:Ca ratios from the primordium to the edge were similar among individuals from the three sampling sites (Fig. 2). The ratios ranged from 9 to 11× 10−3 in the primordium, increased considerably and reached a peak of 17 to 19× 10−3 at a distance from the primordium of c. 100μm, corresponding to the onset of metamorphosis from leptocephalus to glass eel. After this peak, the ratios decreased drastically, varying between 2 and 3× 10−3 near 200μm, corresponding
Table I. Sample sizes (n), means± s.d. and ranges (in parentheses) of total length (LT) and mass (MT) of Anguilla anguilla collected from Demirk¨opr¨u, G¨uzelburc¸ and Samanda˘g in the River Asi, Turkey by sex: females (F), males (M) and fish with undeveloped gonads (U)
Location Demirk¨opr¨u G¨uzelburc¸ Samanda˘g
Sex F F M F M U n 10 3 3 1 12 5 LT (mm) 45·7 ± 7·3 (39·2–60·0) 56·5 ± 7·4(52·2–65·0) 38·8 ± 3·2(36·7–42·4) 45·5 37·4 ± 2·1(34·8–40·5) 35·8 ± 3·2(33·0–40·2) MT (g) 113·7 ± 57·5 (66·2–228·8) 439(308·0–667·6)·7 ± 198·2 134(116·1–166·4)·5 ± 27·7 171·6 108·3 ± 18·5(81·2–139·5) 96(58·3–160·9)·2 ± 42·4
(a) 20 15 10 5 25 0 400 800 1200 0 1600 (c) 25 20 15 10 5 30 0 0 400 800
Distance from primordium (μm)
1200 1600 (b) 20 15 Sr:Ca ratio × 10 –3 10 5 25 0 0 300 600 900 1200 1500 1800
Fig. 2. Otolith Sr:Ca ratios (×10−3) of Anguilla anguilla collected from (a) Demirk¨opr¨u, (b) G¨uzelburc¸ and (c) Samanda˘g. , the mean+2 s.d. of the otolith Sr:Ca ratios of the last three points (5·29 × 10−3), indicating residence in fresh water (grey region).
to the end of metamorphosis. After metamorphosis, the otolith Sr:Ca ratios fluc-tuated around 3× 10−3, and ranged from 1 to 5× 10−3. The mean± s.d. of the last three points is 2·85 ± 1·22 × 10−3 and the corresponding mean +2 s.d. value is 5·29 × 10−3. Therefore, two consecutive points with ratios >5·29 × 10−3 were considered as saltwater exposure.
After becoming glass eels, the otolith Sr:Ca ratios of collected individuals were generally <5·29 × 10−3 except that one individual from Demirk¨opr¨u had ratios >5·29 × 10−3 at an otolith radius c. 1000–1100μm [Fig. 2(a)], and one in G¨uzelburc¸ had two points >5·29 × 10−3at an otolith radius c. 1100 μm [Fig. 2(b)]. Therefore, all but two individuals from three sampling sites in the River Asi spent their entire yellow eel stage in fresh water and did not return to salt water after they recruited to the River Asi. For the two individuals having a short period of saltwater experience, they had lived in fresh water for most of their yellow eel stage.
The mean otolith, s.d. and coefficient of variation of Sr:Ca ratios after the elver stage of A. anguilla collected from fresh waters in different published studies and the ratios indicative of residence in freshwater, brackish-water and seawater habi-tats in different regions are listed in Table II. The mean Sr:Ca ratio of A. anguilla from the River Asi in southern Turkey is 2·79 × 10−3, close to 2·70 × 10−3 for A. anguilla from the freshwater Fumemorte Canal in southern France. It is, how-ever, approximately two times higher than that from the Garonne and Dordogne Rivers (1·4 × 10−3) and Adour River (1·59 × 10−3), two to three times higher than from five Irish rivers (0·98–1·78 × 10−3), eight times higher than from Lake M¨alaren and Ommen in southern Sweden (0·37 × 10−3), four times higher than from Lake Fardume in Gotland in Sweden (0·71 × 10−3) and also four times higher than from Lake Baluoˇsai in Lithuania (0·72 × 10−3). Consequently, it is reasonable to conclude that the otolith Sr:Ca ratio indicative of residence in fresh water was highest in the River Asi (5·29 × 10−3), followed by that in Lake Baluoˇsai, Lithuania (2·24 × 10−3) and in the Gironde watershed (2·0 × 10−3).
DISCUSSION
Prolonged residence in fresh water without saltwater experience in anguillids appears to be particularly affected by distance of riverine or lacustrine habitats from the tidal limit, by migration barriers, or related to stocking or escapes of cultured anguillids from farms into upstream reaches (Tesch, 2003; Arai et al., 2006; Shiao et al., 2006; Lin et al., 2010). In this study, the distances from the sampling sites to the river mouth are relatively short (2, 20 and 30 km for Samanda˘g, G¨uzelburc¸ and Demirk¨opr¨u, respectively). There has not been any A. anguilla stocking or farming in the Asi catchment and there are no migration barriers, such as dams or hydro-electric power plants, downstream of the riverine sampling sites (S. Yalc¸ın- ¨Ozdílek, pers. obs.). It is possible that the sampled A. anguilla remained in freshwater habitats with a limited home range (Laffaille et al., 2005; Tabouret et al., 2010). The high salinity of the Mediterranean Sea (Pinet, 2009) or high interspecific competition in the river mouth might inhibit the use of brackish habitats.
Habitat use by A. anguilla after the elver stage is facultative and highly variable among different European regions. Nearly all the A. anguilla in the present study lived in fresh water, except two that evidently resided in salt water for a short time.
T able II. Mean, s.d. and coef fi cient o f v ariation (c.v. ) o f o tolith Sr:Ca ratios (× 10 − 3)o f Anguilla anguilla after elver stage from d if ferent European fres h waters . S r:Ca Crit is the criterion Sr:Ca ratio for residence in sea w ater (SW), b rackish w ater (BW) and fresh water (FW). The m ethods used to construct criterion Sr:Ca ratios from individuals from freshwater h abitats: A , m ean + 2 s.d . o f o tolith Sr:Ca ratios o f last three measuring points of individuals from freshwater h abitats; B , m ean + 2 s.d . o f o tolith Sr:Ca ratios o f freshwater-resident individuals after the elver stage; C , linear discriminant analysis using the first point after m etamorphosis for b rack ish w ater and the last measuring point for fresh water; D, from rearing experiment in the laboratory Sr:Ca Crit Location M ean s.d . c.v. SW BW FW Method Reference River A si, southern T u rkey 2· 79 1· 21 43 > 5· 29 < 5· 29 A T his study Adour River, south-western F rance 1· 59 0· 32 20 > 4· 93 2· 2 3–4 ·93 < 2· 23 A T abouret et al . (2010)* Lake Baluo ˇsai, Lithuania 0· 72 0· 76 106 > 3· 23 2· 2 4–3 ·23 < 2· 24 B S hiao et al . (2006) Fumemorte C anal, C amar gue, southern France 2· 70 0· 48 18 C J. P anfili, unpubl. d ata Garonne and D ordogne Rivers, w estern France 1· 40 > 6 2–5 < 2D D av er at & T o m ´as (2006) Five Iris h fres h water rivers 0· 9 8–1 ·78 Arai et al . (2006) Lake M ¨alaren and O mmen, southern Sweden 0· 37 0· 02 5 T zeng et al . (1997) Lake Fardume, Sweden 0· 71 0· 89 126 Tzeng et al . (2000) Lake K¸ ıˇsezers, Latvia 0· 84 0· 77 92 Lin et al . (2009) *Otolith Sr:Ca and Ba:Ca ratios are simultaneously used to classify dif ferent types o f m igratory life h istories.
More than 85% of A. anguilla from the Baltic Sea had at least one brackish-water experience (Tzeng et al., 2000; Shiao et al., 2006), while nearly all individuals from five Irish rivers were resident in fresh water (Arai et al., 2006). Daverat et al. (2006) found a gradient of migratory histories in the Gironde River basin of western France where residence in fresh water of A. anguilla increased towards the upper reaches of the Gironde River, but the proportion of freshwater residents also increased towards the sea. A gradient of migratory life histories was, however, not found in individuals from three sites in the River Asi, not even for Samanda˘g. Similarly, no gradient was found in the River Shannon between the upper (Lough Derrevarga), middle (Castleconnell) and lower parts (Killaloe) (Arai et al., 2006), although the upstream and downstream movement of A. anguilla in the River Shannon might be affected by power plants (e.g. Ardnacrusha power station). The situation in the River Asi can be considered as an exception in relation to gradients in migratory life-history strategies.
It is apparent that the otolith Sr:Ca ratios of A. anguilla living in fresh waters can vary substantially between regions. This may be due to region-specific spatial and temporal variation in Sr:Ca concentrations in water (Kraus & Secor, 2004; Munro et al., 2005), different equipment used for measurement of otolith Sr:Ca ratios, water temperatures (Campana, 1999; Elsdon & Gillanders, 2002; Martin et al., 2004) or fish growth rates (Lin et al., 2007).
In a preliminary examination, the Sr:Ca ratios from one of the paired otoliths (sagitta) of A. anguilla from the Fumemorte Canal were measured by electron probe microanalyser (EPMA) and the other otolith by laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS). Sr:Ca ratios were not significantly different (2·67 ± 0·59 × 10−3 and 2·72 ± 0·32 × 10−3 for EPMA and LA-ICPMS, respec-tively, P > 0·5) between the two machines (J. Panfili, pers. comm.). Therefore, the observed variation in otolith Sr:Ca ratio among fresh waters was probably not due to different measuring machines, at least not for EPMA and LA-ICPMS.
Water temperature can affect otolith Sr:Ca ratios in fishes (Campana, 1999; Elsdon & Gillanders, 2002; Martin et al., 2004). The water temperature in the River Asi (16–27◦ C) and the growth rate of A. anguilla (90 mm year−1) are high compared to other European regions (Yalc¸ın- ¨Ozdilek et al., 2006; Yılmaz & Do˘gan, 2008). High water temperature might lead to elevated otolith Sr:Ca ratios (Martin et al., 2004), but the temperature effects on Sr:Ca ratios are not consistent among studies (Campana, 1999) and otolith Sr:Ca ratios were negatively (Tzeng, 1994) or not affected by temperature in Japanese eel Anguilla japonica Temminck & Schlegel (Tzeng, 1996). Meanwhile, otolith Sr:Ca ratios decreased with increasing somatic growth rate (Lin et al., 2007), unlike the case in the River Asi. Therefore, high water temperature and growth rate may not be the main reasons for the high otolith Sr:Ca ratio.
Otolith Sr:Ca ratios and criterion ratios for freshwater v. seawater exposure may be affected by local water chemistry. The water in the River Asi is hard and alkaline (pH range 7·1–8·3), with relatively high concentrations of alkaline earth elements and other heavy metals (e.g. Ag, Cd and Cr). During the rainy season, the water alkalinity further increases due to the rain dissolving basic calcareous layers (Odemis & Evrendilek, 2007; Yılmaz & Do˘gan, 2008). High water hardness and geological leaching of rockbeds might enhance Sr concentrations in water, possibly leading to the observed high otolith Sr:Ca ratios.
A sample-specific Sr:Ca ratio indicative of residence in freshwater or saltwater habitats should be calculated from the individuals collected from freshwater sites or controlled experiments. Applying a criterion from another region a priori might lead to misclassification of the migratory life histories (Elsdon et al., 2008). For example, if the criterion ratio from Lithuanian waters (2·24 × 10−3) was applied, all A. anguilla from the River Asi might be mistakenly classified as having frequently moved to or been caught in saltwater habitats, whereas they were collected from fresh waters.
We would like to thank the fishermen for sample collection, and J.-C. Shiao, B. Jessop and anonymous reviewers for providing valuable suggestions on this manuscript.
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