Mass-marking of brown trout (Salmo trutta L.) larvae by alizarin: method and evaluation of stocking
2008; Wiley; Volume: 24; Issue: 1 Linguagem: Inglês
10.1111/j.1439-0426.2007.01038.x
ISSN1439-0426
Autores Tópico(s)Fish Biology and Ecology Studies
ResumoJournal of Applied IchthyologyVolume 24, Issue 1 p. 44-49 Free Access Mass-marking of brown trout (Salmo trutta L.) larvae by alizarin: method and evaluation of stocking J. Baer, J. Baer Fisheries Research Station of Baden-Württemberg, Langenargen, GermanySearch for more papers by this authorR. Rösch, R. Rösch Fisheries Research Station of Baden-Württemberg, Langenargen, GermanySearch for more papers by this author J. Baer, J. Baer Fisheries Research Station of Baden-Württemberg, Langenargen, GermanySearch for more papers by this authorR. Rösch, R. Rösch Fisheries Research Station of Baden-Württemberg, Langenargen, GermanySearch for more papers by this author First published: 08 January 2008 https://doi.org/10.1111/j.1439-0426.2007.01038.xCitations: 38 Author's address: Jan Baer, Fisheries Research Station of Baden-Württemberg, Untere Seestrasse 81, D-88085 Langenargen, Germany.E-mail: [email protected] AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Summary This study describes otolith marking of brown trout (Salmo trutta L.) larvae by immersion in different solutions of alizarin red S (ARS). The best results were obtained after marking with ARS at a concentration of 150 mg L−1. To evaluate the efficiency of stocking with brown trout fry, 10 000 20-day-old larvae were marked in years 2002 and 2003 with ARS and released 2 weeks later into sections of a river with natural brown trout reproduction. Electro-fishing surveys carried out 2 months after stocking in 2002 revealed that only 4.8% of all caught young-of-the-year trout originated from stocking; in 2003 the percentage was 8.9%. Based on the substantial natural reproduction and the low ratio of stocked to wild trout, it was recommended to discontinue stocking. Introduction Stocking of hatchery-reared salmonids in rivers has been under investigation for at least half a century (Miller, 1953, 1958; Reimers, 1963). Most of the studies reveal that stocking with hatchery-reared juvenile brown trout Salmo trutta L. is inefficient (Berg and Jørgensen, 1991; Jørgensen and Berg, 1991). It is argued that low recapture rates of hatchery-reared salmonids in the wild are based inter alia on the disadvantages of fish reared under controlled environments. These fish may not be adapted to natural feed (Bachman, 1984), or may not show normal antipredator behaviour (Berejikian et al., 1999; Vilhunen, 2006). As a consequence it was recommended to use eggs or yolk-sac fry, which are less adapted to hatchery conditions than older fish (Näslund, 1998). However, fish from these early stages are not easy to mark and the use of external marks, e.g. fin clipping or anchor tags, is impossible. Hence, only internal markings are of use, such as the labelling of the otoliths with fluorochrome dyes. Data particularly on the survival of stocked younger fish are very important, because stocking of fry is quite common and its influence on the genetics of wild populations may be very high (Morán et al., 1991; Largiadér and Scholl, 1995; Mezzera and Largiadér, 2001). However, because of technical problems with marking, data about stocking efficiency with younger life stages are scarce. The practicability of mass-marking eggs or newly hatched larvae by bathing in fluoromarkers has been demonstrated in many studies (Dabrowski and Tsukamoto, 1986; Hendricks et al., 1991; Ruhlé and Winecki-Kuehn, 1992; Rojas-Beltran et al., 1995, 1996; Champigneulle and Cachera, 2003). In most of these studies antibiotics such as oxytetracycline (OTC) were used. However, OTC has an antibiotic effect and has caused excessive stress, mortality, and variable marking success (Tsukamoto et al., 1989a). In addition, OTC would have regulatory implications because its use is prohibited in many EU countries. Alternatives could be alizarin red S (ARS) and alizarin complexone (AC); these dyes produce an easily readable mark (Blom et al., 1994; Nagiec et al., 1995; Beckman and Schulz, 1996; Iglesias and Rodriguez-Ojea, 1997; Eckmann et al., 1998; Eckmann, 2003; Van der Walt and Faragher, 2003). However, to the knowledge of the authors, there are only two references for immersion of trout in AC solutions (Tsukamoto et al., 1989b; Van der Walt and Faragher, 2003), and only one paper on marking trout with ARS (Champigneulle and Rojas-Beltran, 2001) could be found. The first purpose of the present study was to develop a simple and inexpensive method for mass-marking brown trout fry with ARS. In a second step, this method was used to evaluate the effectiveness of stocking hatchery-reared brown trout fry into a river with a wild trout population. Materials and methods Marking: development and adjustment of the method In 2001 and 2002, concentrations of 0, 50, 150, 300 mg L−1 ARS were tested. Additionally, in order to achieve an osmotic shock and to enhance the transport of the dye into the fish, all marking concentrations contained 10 g L−1 NaCl. In one additional group using a concentration of 150 mg L−1 ARS, the marking was tested without NaCl. Five groups were examined each year. In total, around 10 000 fish were immersed, approximately 5000 per year. For each of the five solutions, around 1000 twenty-day-old brown trout eleutheroembryos (TL 25–29 mm) were immersed for 3 h in small plastic aquaria (40-L volume) separated per group. In both years, water temperature was maintained at around 12°C. In addition, pH was checked regularly during the immersion period in order to maintain the initial value of pH 7.6. After adding 0, 50 or 150 mg L−1 ARS, the pH was relatively stable and around pH 7.6 and 7.7. However, at a concentration of 300 mg L−1 ARS, the pH dropped rapidly. Therefore, in both years 1 mg L−1 NaOH was added to the highest ARS solution to maintain a constant pH. Following immersion, in both years all five groups were held separately in 40-L aquaria at 12°C for 100 days. During this time the fish were fed a commercial trout diet (57% crude protein, 17% crude fat). Mortality was checked immediately after immersion, and after 30, 60 and 100 days of rearing. Mark quality was monitored 60 and 100 days after marking by analysing six fish per group after each period. To compare the final mean length for each group per year, a subsample of around 20 fish per group was measured after 100 days. Quality of the mark (ranked according to no mark; poor mark; good mark) was identified by analysing both sagittae. The whole otoliths were washed and checked without embedding or polishing under an epifluorescent microscope with 545 nm excitation and >590 nm emission filters (Zeiss filters no. 15, Fl S 15). Marking of the stocking material The stocking material originated from a commercial trout farm in the Black Forest (owner: R. Rösch, Gengenbach). The fish were offspring of a stock originating from a Rhine River tributary. In 2002 and 2003 on the farm 10 000 brown trout fry at ages 15–20 days were marked per year. The temperature during egg incubation was between 2 and 8°C. After hatching, the yolk sac fry were held in small raceways supplied by spring water under relatively stable conditions (8°C, pH around 6.8). The fish were fed a commercial larval trout diet (57% crude protein, 17% crude fat). To prepare the marking solutions, 150 mg L−1 ARS and 10 g L−1 NaCl were put into small (40 L), aerated plastic tanks at 8°C water temperature. After the dye was added, an immediate drop in pH to 5.8 was noted. 20 mg L−1 NaOH were added in order to raise the pH to the initial value of 6.8. As soon as the pH was stabilized, the fry were added to the aerated plastic tank for 3 h. Following this marking procedure, the fish remained in the hatchery for 2 weeks in order to control losses. The fish were stocked as soon as the yolk sac had been absorbed and with the beginning of their search for exogenous food. A small sample of each batch was retained in the laboratory to determine the readability of the otoliths as well as the mark quality. Study area The Radolfzeller Aach River is a north-western tributary of Lower Lake Constance. The slow-flowing, spring-fed river is around 32-km long and runs through cultivated fields, some nature reserves and a few small towns. Its width varies between 8 and 14 m. It is characterized by some shallow runs and deep pools, with a coarse substrate consisting largely of gravel and boulders. Water temperature is low during winter and spring, and can rise up to 20°C in summer and early autumn. The conductivity ranges from 460 to 550 μS cm−1. From Lower Lake Constance, fish can migrate upwards approx. 12 km to the first insurmountable weir. Formerly, the Radolfzeller Aach River was known as a good river for trout (D. Dzuiba, pers. comm.). However, in the late 1990s a lack of natural recruitment was assumed due to predation of fish-eating birds, especially cormorants, migration barriers and lack of spawning sites. Angling associations, which had leased stretches of the river, were therefore stocking brown trout fry. The release areas were located in the city of Singen (Fig. 1) where the river has an average depth of around 50 cm and an average width of 14 m, with a high proportion of habitats suitable for juvenile brown trout. The sites are well known by anglers as typically young fish areas where abundance of cormorants is very low. Figure 1Open in figure viewerPowerPoint Location of brown trout (Salmo tutta) release areas (sections 1–3) in Radolfzeller Aach River Stocking In mid-April in 2002 and 2003, the marked brown trout fry were stocked into two 50-m long stretches. In both years 10 000 fish were stocked, approx. 5000 per stretch. The fish were released near the riverbank in shallow water (mean depth: 10 cm). The distance between the two stretches (sections 1 and 3) was around 4000 m (Fig. 1). Sampling In 2002, 60 days after stocking the sections where the larvae had been released were fished using a backpack electrofishing unit (1.5 kW, 450 V; EFKO, Leutkirch, Germany). Only brown trout fingerlings were sampled. In June 2003, the period between stocking and electrofishing was 80 days due to unfavourable water conditions for fishing earlier. In addition to the two stocked sections (sections 1 and 3), a control section (section 2) approx. 1.5 km downstream of the first and 2.5 km upstream of the second section (Fig. 1) was sampled. Each caught young-of-the-year brown trout was killed and transported on ice to the laboratory where the fish were measured to the nearest mm (total length, TL) and weighed to the nearest mg (body weight, BW). The sagittae of all sampled fish were secured and observed with the technique described above. In general, one otolith per specimen was analysed. When the presence of a mark was doubtful, a second otolith was analysed. Statistics Because of non-parametric distribution of some data sets, the Wilcoxon test (Sachs, 1997) was used to compare TL and TW of marked and unmarked fish. Results Marking and analysing procedure In the preliminary tests the best marks were obtained using a concentration of 300 mg L−1 ARS (Table 1). However, this concentration caused an immediate mortality of around or more than 95%. Fluorescent marks of good quality and low mortality rates, which did not differ from the control group (0 mg L−1 ARS), were observed with ARS concentrations of 150 mg L−1 and 10 g L−1 NaCl solution (Table 1). Mark quality was clearly poorer when lower concentrated ARS solutions were used or when sodium chloride was not added (Table 1). In addition, in both years no difference in growth was obvious, neither between years nor between groups (Wilcoxon; P > 0.05). All measured fish from each group showed growth and ranged in size between 84 and 118 mm at the end of the preliminary test (after 100 days). Based on these results, all trout for the stocking experiment were immersed in a solution consisting of a mixture of 150 mg L−1 ARS and 10 g L−1 NaCl. Table 1. Preliminary test results for marking brown trout (Salmo salar) eleutheroembryos with four different Alizarin Red S (ARS) solutions [0 (control), 50 (tank 1), 150 (tank 3) and 300 mg L−1(tank 4)] Year Control Tank 1 Tank 2 Tank 3 Tank 4 ARS (mg L−1) 0 50 150 150 300 NaCl (g L−1) 10 10 – 10 10 Mortality after immersion (%) 2001 – 1 1 1 95 2002 – 1 1 1 99 Mortality after 30 days (%) 2001 5 4 5 4 96 2002 4 5 6 5 99 Mortality after 60 days (%) 2001 5 5 5 5 97 2002 4 5 6 5 99 Mortality after 100 days (%) 2001 5 6 5 6 98 2002 5 5 6 5 99 Mark quality after 60 days 2001 – No mark (n = 5); poor (n = 1) Poor (n = 1); good (n = 5) Good (n = 6) Good (n = 6) 2002 – No mark (n = 6) Poor (n = 3); good (n = 3) Good (n = 6) Good (n = 6) Mark quality after 100 days 2001 – No mark (n = 6) Poor (n = 3); good (n = 3) Poor (n = 1); good (n = 5) Good (n = 6) 2002 – No mark (n = 6) Poor (n = 4); good (n = 2) Poor (n = 1); good (n = 5) Good (n = 6) All concentrations contained 10 g NaCl L−1. One additional group (tank 2, 150 mg L−1 ARS) was tested without adding NaCl. First test in 2001, second in 2002. In total, around 10 000 fish were marked, around 5000 per year, approx. 1000 per group. Each year, 30, 60 and 100 days after marking, mortality was checked; 60 and 100 days after marking, six fish per tank were analysed for mark quality. Preliminary tests suggest that pH drops only in those cases where the ARS concentration exceeds 150 mg L−1. During mass marking on the farm, however, an unexpected drop in pH was recorded. This major difference to the preliminary tests was traced back to the fact that the pH of the water on the farm (6.8) was lower than in the laboratory (7.6). Twenty milligram per litre NaOH was added to reach the initial pH value during mass-marking. Mortality after immersion was nearly zero and the mortality rate was comparable to that of the unmarked fry in the farm until stocking. In both years, mark quality of the subsample of stocked fish retained in the aquaria was good after 60 and 100 days. Each otolith could be viewed as a whole, and grinding was not necessary. Around 5–6 min is needed to open the head of a trout to secure the otoliths and observe them. However, the analysis of otoliths without grinding is only possible in fish up to a certain size. When the marked fish exceeded a body length of 15 cm and a body weight of 50 g, visibility of the mark in the otoliths became poor. From this point on, it was impossible to differentiate marked and unmarked otoliths without grinding. Evaluation of stocking In 2002, 105 young-of-the-year brown trout were caught in the two releasing sites and 4.8% (n = 5) were marked. In 2003, 79 juvenile trout were caught in the release areas and 8.9% (n = 7) were marked (Table 2). The number of young-of-the-year trout caught in the stretch without stocking was comparable to the number caught in the stocked sections (Table 2). In both years, no marked fish were found in the unstocked section. Table 2. Number of caught young-of-the-year brown trout (Salmo trutta) in stocked and unstocked sections, and number of caught marked trout in 2002 and 2003 Year Section 1 Section 2 Section 3 Stocking 2002 Yes No Yes 2003 Yes No Yes Total caught (n) 2002 54 60 51 2003 40 37 39 Marked (n) 2002 2 – 3 2003 4 – 3 In both years, neither a difference in TL nor in TW between marked (i.e. stocked) and wild trout could be detected (Wilcoxon; P > 0.05). However, fish caught in 2003 were significantly larger than fish caught in 2002 (Wilcoxon; P < 0.05). In 2002, marked trout had a mean ± SD TL of 52.4 ± 4.4 mm, and that of the trout originating from the wild stock was 57.8 ± 7.1 mm respectively. In 2003, the TL of marked trout was 95.6 ± 12.6 mm, and that of trout originating from the wild stock was 90.5 ± 12.3 mm. The TL distribution of pooled stocked and wild young-of-the-year brown trout showed unimodal distribution in both years (Fig. 2). In 2002, the mean ± SD TW of marked trout was 1.9 ± 0.5 g and of wild trout 2.5 ± 0.9 g respectively. In 2003, the TW was 11.2 ± 5.1 g and 9.7 ± 3.7 g respectively. Figure 2Open in figure viewerPowerPoint Total length-frequency distribution (% of caught individuals) of stocked and wild young-of-the-year brown trout (Salmo trutta) in stocked sections in 2002 and 2003 Discussion Marking Labelling the otoliths of fish with fluorochrome dyes is a widespread technique used to evaluate stock enhancement programmes (e.g. Dabrowski and Tsukamoto, 1986; Hendricks et al., 1991; Rojas-Beltran et al., 1995; Champigneulle and Cachera, 2003). In the present investigation the larval trout were marked by immersion in ARS solution with a concentration of 150 mg L−1. After marking, no negative effects on growth were detectable. A major advantage of this marking technique is that it requires substantially less time and expense than previously reported techniques, both in applying and detecting the marks. If fish can be sampled during their first summer, i.e. when their body length does not exceed 14 cm TL, grinding of the otoliths is not necessary. Hence, large samples can be analysed in a comparatively short time. However, if otoliths of ARS-marked trout larger than 15 cm have to be analysed, methods for examination of trout marked with other fluoromarkers should be transferable (mounting of a glass strip and polishing to expose the nucleus, e.g. Champigneulle and Cachera, 2003). In contrast to the analysing procedure of fish marked with antibiotics, no expensive epifluorescence microscope is needed. Rather, a normal binocular microscope with a standard filterset for excitation and emission can be used. Although marking results for salmonids were similar for ARS and AC, the required immersion time in AC is much longer (6–24 h, Tsukamoto et al., 1989b; Van der Walt and Faragher, 2003) and the cost of AC is much higher (Blom et al., 1994; Beckman and Schulz, 1996). Thus, ARS is more useful when many fish must be marked quickly and/or large amounts of dye are needed. When NaCl was added to the ARS solution, readability of the marks was better. One possible explanation is that due to the osmotic shock caused by adding NaCl during immersion, water and also therefore marking dye penetrates easier into the fry and the mark quality increases. During marking with antibiotics, in which the transport of the fluorochrome dye was promoted by osmotic shock (50 g L−1 NaCl), an improvement of the readability of the marks was also shown (Rojas-Beltran et al., 1995). To avoid high mortality, attention must be given to the ARS concentration and the pH value. In the present study as well as in the findings of Blom et al. (1994), Beckman and Schulz (1996) and Eckmann et al. (1998) mortality was highest at concentrations with or above 300 mg L−1. Special care must be taken with regard to the pH stability during immersion. Otherwise there is a risk of high mortality during or after immersion (Eckmann et al., 1998). Beckman and Schulz (1996) observed that the pH stabilizes after maintaining the solutions through aeration overnight or by adding sodium bicarbonate. In the present study, 1 g L−1 NaOH was used to raise the pH; this had no negative effects on the fish; therefore, use of NaOH is recommended. The best life stage for mass-marking with ARS appears to be after hatching (Nagiec et al., 1995; Beckman and Schulz, 1996; Eckmann et al., 1998; Champigneulle and Rojas-Beltran, 2001). Other studies demonstrated that fish otoliths can be marked with ARS during embryonic development: cod Gadus morhua L. (Blom et al., 1994), turbot Scophthalmus maximus (L.) (Iglesias and Rodriguez-Ojea, 1997) and whitefish Coregonus lavaretus (L.) (Eckmann, 2003) respectively. However, to the knowledge of the authors, a technique for marking brown trout embryos (eggs) with ARS did not exist at the time. Evaluation of stocking efficiency The summer of 2003 was the warmest on record since 1870 (German Meteorological Service). As one consequence, growth rates of different fish species increased markedly, for example, in perch (Perca fluviatilis L.) in Upper Lake Constance (Eckmann et al., 2006). In 2003, in one trout river in the Black Forest approx. 50 km northwest from the study area, a higher growth rate than in 2002 or 2001 was also observed in trout (J. Baer and A. Brinker, in preparation). It is assumed that in the Radolfzeller Aach River the growth rate for trout in 2003 was also higher than in years with normal weather conditions. This fact in combination with the longer time between stocking and recapture in 2003 (80 days) compared with 2002 (60 days) would explain the different size distribution of young-of-the-year trout between the years. Survival of juvenile trout is influenced by many factors (McRea and Diana, 2005) causing varying survival rates (Kelly-Quinn and Bracken, 1989; Berg and Jørgensen, 1991; Ward and Slaney, 1993; Näslund, 1998; Lund et al., 2003). In the present study, a total of only 12 out of 20 000 stocked fish could be recaptured, but the exact survival rate of the stocked fish is unclear. Young trout are sensitive to increased water velocity (Daufresne et al., 2005), which may have caused a downstream displacement of the stocked fry. However, the Radolfzeller Aach River is spring-fed and with a small catchment area, thus the water velocity is relatively constant. Flood events, which presumably should have caused displacement of all stocked trout, were not observed during the study period. One reason for the high mortality might be predation by predatory fish. During the electrofishing surveys, a few trout between 20 and 35 cm were observed. In the studies of Henderson and Letcher (2003), between 4.3% and 48.6% of stocked salmon (Salmo salar L.) fry were consumed by older salmon and trout within the first days after stocking, and total fry mortality due to predation varied from 4.3% to 60.7%. In other studies (Kelly-Quinn and Bracken, 1989; Berg and Jørgensen, 1991), the worst survival rates of stocked trout were recorded when wild fry densities were high. Brown trout fry begin to defend feeding territories shortly after hatching and emerging. Competition during this period is often intense, and failure to obtain territories is likely to reduce survival considerably (Elliot, 1994). Johnsson et al. (1999) showed in studies about territorial competition among brown trout fry that the territory owner could displace the invader in 85% of contests, and that 30% size advantage was required to balance the advantage of ownership. In the present study, in both years more than 90% of all caught young-of-the-year trout were offspring of wild trout. Therefore, it can be assumed that Radolfzeller Aach River brown trout spawn naturally and recruit, and that at the time of stocking most likely the territories suitable for fry were already occupied by wild trout. In addition, mortality from predation might have been high. Hence, stocked trout had low survival chances and/or find free territory or displace wild fry. Therefore, they were either eaten or forced to leave the stocking area, likely the reason for the low number of recaptured stocked trout. However, even if the low number of marked fish during the electric fishing survey could not be clarified in detail, the benefits of stocking fry in the study period were strongly questionable. In the unstocked area, the density of juvenile trout was comparable to the density in the stocked areas or, viewed the other way around, intensive stocking could not remarkably increase the population density. This suggests for the study period that the carrying capacity (Mills, 1971) was reached. Artificial stocking is therefore unnecessary. Consequently, it was recommended to discontinue stocking. Fisheries managers had discussed brown trout stocking in this part of the river several years prior to the present study, as natural spawning was regularly observed. However, the angling clubs worried about a decreasing fisheries yield if stocking were discontinued, especially under increasing predation by nearby cormorants. Without the data on stocking efficiency, the stocking was not stopped. However, based on the present data, as from 2004 stocking was given up. So far, no decrease in the abundance of young-of-the-year brown trout has been found (J. Baer, unpubl. data). In conclusion, marking larval trout by immersion in an ARS 150 mg L−1 concentrated solution is a simple and inexpensive method. Use of this method allows fishery managers to evaluate the effectiveness of stocking programmes with young brown trout. Acknowledgements This project was funded by the Fischereiabgabe Baden-Württemberg. Permission to use the study sites for electrofishing were kindly granted by the fishermen's organization, Hegegemeinschaft Radolfzeller Aach. We thank D. Dzuiba, H. Katzwinkel and W. Martin and our colleagues from the Fisheries Research Station for their assistance in field operations. We also thank K. Baer for reading the manuscript and P. 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