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ISSN 1062 3590, Biology Bulletin, 2011, Vol. 38, No. 2, pp. 138­145. © Pleiades Publishing, Inc., 2011. Original Russian Text © A.A. Makhrov, V.S. Artamonova, V.S. Sumarokov, A.N. Pashkov, S.I. Reshetnikov, M.V. Ganchenko, S.A. Kulyan, 2011, published in Izvestiya Aka demii Nauk, Seriya Biologicheskaya, 2011, No. 2, pp. 178­186.

ZOOLOGY

Variation in the Timing of Spawning of the Black Sea Brown Trout Salmo trutta labrax Pallas under Artificial and Natural Conditions
A. A. Makhrova, V. S. Artamonovaa, V. S. Sumarokovb, A. N. Pashkovb, S. I. Reshetnikovb, M. V. Ganchenkoc, and S. A. Kulyand
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 119071 Russia e mail: makhrov12@mail.ru b Kuban State University, ul. Stavropol'skaya 149, Krasnodar, 350040 Russia Department of Agriculture and Processing Industry of Krasnodar Krai, ul. Rashpilevskaya 36, Krasnodar, 350000 Russia d Adler Experimental Production Salmon Breeding Hatchery, ul. Partizanskaya, Monastyr' village, Sochi, Krasnodar krai, 354386 Russia
Received April 16, 2010
a

c

Abstract--Analysis of the maturation and spawning times of the Black Sea brown trout bred at the fish farm ing plants and inhabiting natural waterways of the Northwestern Caucasus has demonstrated a considerable variation depending on environmental conditions, first and foremost, temperature. This fact, as well as the analysis of literature data, suggests that the duration and timing of the spawning season cannot be used as self sufficient criteria for identifying species of the genus Salmo. DOI: 10.1134/S1062359011020075

The fish belonging to the genus Salmo display a high ecological plasticity: several intraspecific forms can coexist even in a small aquatic system. Some of them were described as separate species (Gunther, 1866); however, further studies confirmed the species status of only the Atlantic salmon (Salmo salar) and brown trout (S. trutta) as well as several endemic spe cies (S. marmoratus, S. letnica, S. ischchan, S. carpio, and S. platycephalis) (Berg, 1962; Frost and Brown, 1967; Behnke, 1968; Dorofeeva, 1998). Just recently, this list was supplemented with a number of endemic species (Zerunian and Gandolfi, 1990; Delling, 2003). Nonetheless, Kottelat and Freyhof (2007) without any additional studies separated several other species of the genus Salmo. In particular, based only on the differences in spawning ground and time, they pro posed to regard sympatric forms of the brown trout from Lake Ohrid (Balkan Peninsula) as the separate species S. aphelios, S. balcanicus, and S. letnica. It is demonstrative that any genetic distinctions between these species were undetectable even by such a sensi tive method as microsatellite analysis (Susnik et al., 2006, 2007); thus, the authors believe that prezygotic reproductive isolation can serve as an independent cri terion of species. The goal of the work was to analyze the maturation and spawning times of one of the brown trout subspe cies--the Black Sea brown trout Salmo trutta labrax--bred at fish farming plants and inhabiting rivers of the Northwestern Caucasus and to study the appropriateness of this trait as a criterion for identify ing salmon species.

MATERIALS AND METHODS The background for this work was data on the mat uration and spawning times of the Black Sea brown trout obtained at the Adler Experimental Production Salmon Breeding Hatchery (hereinafter, AEPSB hatchery) as well as for the fish inhabiting several rivers on the Black Sea coast of the Northwestern Caucasus, namely, the Mzymta River and its tributary, the Chvizhepse River, and Shakhe, Psezuapse, Psakho, and Pshada (Fig. 1). The AEPSB hatchery is located on the bank of the Mzymta River 35 km from Adler. Characteristics of this hatchery are listed in the paper by Kulyan (1999). The hatchery has a captive broodstock of the Black Sea brown trout, which has been formed for several years of the fingerlings obtained from anadromous breeders caught in the Mzymta River. These breeders were kept to spawning in cages in the river and released after reproduction. Currently, the AEPSB hatchery has both captive and replacement broodstocks of the Black Sea brown trout as well as the raised fingerlings. The fingerlings are raised in a closed room in direct flow tanks with a volume of about 640 l until an age of 1 year and then are either transferred into ITsA 2 (Russia) shed tanks with a circular flow and a volume of 1900 l or released into the Mzymta and Shakhe rivers. Granulated combined feeds (according to the fish age and weight) are used when raising the replacement broodstock; during the maturation period, the feeding is ceased, and males are kept separately from females.

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VARIATION IN THE TIMING OF SPAWNING
Gelendzhik r Rive ada Psh
Goryachii Klyuch Apsheronsk

139
Maikop

Azov Sea

Tuapse
Ps e

zupse R.
. m it R Chi Sha khe R.

Krasnodar

Sochi

Mz ym ta R.

Blac kS ea

Maikop

Bla ck Sea

Chvizheps

. eR

Fig. 1. Sites of sample collection. The inset shows the location of study areas on the territory of Krasnodar krai.

o akh R. Ps

AEPSB plant

Lake Ritsa

In our work, we recorded the dates of spawning of the females of generation of 1999 and 2000 bred at the AEPSB hatchery and their mothers, wild females that spawned in 1999 and 2000. In addition, biological analysis of 29 individuals (10 males and 19 females) of the generation of 2000 was performed on September 27­28, 2003. In addition to the artificially bred fish, we also ana lyzed wild fish caught in rivers running into the Black Sea. The hydrological characteristics of these rivers are described by Borisov (2005) and Reshetnikov and Pashkov (2009). The caught underyearlings and the individuals originating from breeding facilities were discarded from analysis. The latter individuals were distinguished from the wild ones according to the fin rays bent as a result of necrosis (Dombrovsky and Usik, 2001). The age of wild fish was determined by the same person according to scales. The main biological characteristics of the studied wild and artificially bred Black sea brown trout indi viduals, the volumes of studied samples, and catching dates are listed in Table 1. Black Sea brown trout fish ing is limited because this form is rare; therefore, we examined the samples of a rather small volume. The body length to the caudal fin fork was measured in the majority of fish according to Smith (AC). In the case of individuals with a damaged caudal fin, AC was not measured; the body length to the end of the scale cov ering (AD) was used instead. The degree of gonad maturation was assessed according to the scale pro posed by Murza and Khristoforov (1991). The stage of maturation was determined by one person for all indi viduals.
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RESULTS AND DISCUSSION The females of generation 1999 obtained from wild breeders but raised at the AEPSB hatchery spawned for the first time in the winter of 2002­2003, i.e., dur ing the third year of their life. The spawning campaign extended to the end of spring (Table 2). In January­ March of 2003, the spawn was not taken from part of the mature females; thus, the number of individuals that reached maturity during this period was even larger than is shown in Table 2. In early June 2003, we necropsied a dead female at the fifth stage of gonad maturity. In September 2003, the females of generation 2000 from the AEPSB hatchery population were at the sec ond­third to fourth stages of gonad maturity and the males, at the second and fourth stages (Table 3). From December 2003 to June 2004, the fish from both stud ied generations (1999 and 2000) matured; the spawn ing peak was observed in January. Because of insuffi cient number of tanks, the breeders were mixed, pre venting us from recording the spawning dates for each generation individually. In September­October, the gonads of wild fish from the Mzymta, Shakhe, Chvizhepse, Psezuapse, and Psakho were at the second, third­fourth, fourth, and fifth stages of maturation (Table 3). The "wild" breeders of the anadromous brown trout form caught in the Mzymta River for further breeding reached maturity in November­December (Table 2). The wild fish caught in September 2005 in the Pshada River were least developed (Table 3). Note that this was an abnormal year, since the water in the Pshada River was very low due to a dry summer and the brown trout residential form localized to a deep pool near the entry of a spring fed brook.


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Table 1. Characterization of the studied samples of the Black Sea brown trout Sampling site and date AEPSB plant; Septem ber 27­28, 2003 Mzymta River; Septem ber 25, 2003 Sex Males Females Males Males Same site; October 5, 2004 Chvizhepse River; Sep tember 24, 2006 Male Males Females Psakho River; Septem ber 8, 2006 Shakhe River; Septem ber 29, 2003 Same site; October 6, 2004 Psezuapse River; Sep tember 14, 2006 Males Males Females Males Age 2+ 2+ 1+ 2+ 1+ 2+ 3+ 2+ 3+ 2+ 3+ 1+ 1+ 1+ 1+ 2+ 2+ 3+ 2+ 3+ 1+ 1+ n 10 19 2 1 3 6 1 4 5 4 9 2 4 5 1 2 9 1 2 3 3 6 AC length, mm ­ ­ 92­103 (97.5) 138 91­114 (103.3) 129­158 (143.3) 246 142­169 176­213 150­161 175­230 136­146 (153.8) (200.6) (155) (197.4) (141) AD length, mm 380­442 (409) 387­456 (424.4) 84­94 (89) 128 84­106 (95.7) 119­147 (133.2) 227 130­156 162­196 139­149 160­212 126­134 (141.8) (184.8) (143.8) (181.4) (130) Weight, g 765­1265 (976) 855­1320 (1060.6) 7.9­10.8 (9.35) 26.2 8.2­14.6 (11.53) 20.5­39.5 (30.33) 154.7 34.1­52.2 (41) 64.7­111.4 (87.7) 35.4­43.8 (39.2) 59.4­130.9 (86.9) 27.1­32.5 (29.8) 34.7­70.6 (52.2) 41.7­65.6 (50.36) 12.7 40.6­72.1 (56.35) 44.8­70.8 (59.39) 93.3 64.2­85 (74.6) 75.5­114.4 (89.6) 35.3­58.3(47.8) 35.6­50.6 (43.52)

153­200 (172.8) 162­196 (177) 104 168­197 162­192 212 181­198 190­213 153­183 (182.5) (178.1) (189.5) (201.7) (167.7)

142­186 (159.8) 150­181 (164.2) 96 157­184 149­178 195 167­183 176­198 142­171 (170.5) (164.4) (175) (187.3) (156)

Males Females

Pshada River; Septem ber 21, 2005

Males Females

154­175 (165.3)

144­164 (154.2)

Note: The minimal and maximal values and the mean (parenthesized) are given for length and weight; n is the sample volume, individuals (for Tables 1 and 3).

Table 2. Maturation time and the number of mature wild females of the Black Sea brown trout from the Mzymta River (1999 and 2000) and the females bred at the AEPSB hatchery (2002­2003) Group Wild females Females bred at the AEPSB hatchery November 1 0 December 6 13 March 0 5 April 0 6 May 0 6

What are the possible reasons for the differences in the maturation and spawning times of the artificially bred and wild Black Sea brown trout as well as of indi viduals from different populations? The brown trout has several intraspecific forms; the most widespread of them are migratory (anadromous) and residential. The latter one (especially males) is actively involved in the spawning of migratory individ uals of the same species, i.e., both forms can constitute a single population. The self reproducing populations of the brown trout residential form are found only in the regions of aquatic systems that are not visited due

to some reasons by the anadromous fish (Barach, 1962; Kuzishchin, 1997; Klementsen et al., 2003; Pav lov and Savvaitova, 2008; Tuniev, 2008). Autumn spawning is characteristic of both anadro mous and residential forms of the brown trout. The autumn spawning period only occasionally extends to January (Menzies, 1936). Some males retain the sperm fertilizing ability until spring; however, the spawn of the females that had not spawned by the fall is unable to develop in spring (Scrochowska, 1969). According to our data (Tables 2, 3) and the litera ture data (Murza and Khristoforov, 1988; etc.), the
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VARIATION IN THE TIMING OF SPAWNING Table 3. Distribution of the studied fish according to maturation stages Fish distribution according to maturation stages, % Sex Date Catching site Age, years n Second Males September 2003 Mzymta River October 2003 September 2003 Shakhe River October 2003 September 2006 Chvizhepse River September 2006 Psezuapse River September 2006 Psakho River September 2005 Pshada River September 2003 AEPSB plant Females September 2003 Mzymta River September 2003 Shakhe River September 2006 Chvizhepse River September 2006 Psezuapse River September 2005 Pshada River September 2003 AEPSB plant 1+ 2+ 3+ 1+ 1+ 2+ 2+ 3+ 2+ 3+ 1+ 1+ 2+ 1+ 2+ 1+ 2+ 3+ 2+ 3+ 1+ 2+ 2 1 1 4 1 2 4 5 9 1 2 3 10 3 6 5 4 9 2 3 6 19 100 100 0 50 0 100 0 0 33 0 0 0 60 100 100 100 50 0 0 0 66 0 Second­ third 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 17 5 Third 0 0 0 0 0 0 0 0 0 0 0 67 0 0 0 0 0 0 0 0 17 47 Third­ fourth 0 0 0 25 0 0 0 0 11 0 0 33 0 0 0 0 0 0 0 33 0 32 Fourth 0 0 100 25 0 0 100 100 56 100 100 0 40 0 0 0 50 100 100 67 0 16

141

Fifth 0 0 0 0 100 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

timing of spawning for the anadromous and residential Black Sea brown trout individuals in the Mzymta River and the majority of other rivers of the Russian Black Sea shore does not differ from that typical of the species. These data are also confirmed by the informa tion obtained from local residents, although one of the experienced fishermen mentioned a form of brown trout in the Mzymta River that spawned in August. However, the maturation of the females from the Pshada River is somewhat delayed as compared with the females of other waterways. The period when breeders from the captive broodstock of the AEPSB hatchery became ready to spawn considerably expands towards the spring season (Table 2). This fact was noticed in two generations of the brown trout raised at this hatchery. The extension of maturation and spawn ing periods of the Black Sea brown trout towards the spring months is annually recorded at the other fish farming facility, the Adler federal state hatchery. The spawning there is recorded from November to early April (Babii et al., 2002; Nikandrov and Shindavina,
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2007; V.A. Yankovskaya, personal communication) (Fig. 2). Analysis of the published data demonstrates that the spawning time is inherited in some salmon species (Heggberget, 1988; Nikandrov et al., 2002). On the other hand, it has been shown that the genes control ling the spawning time had formed before the genome duplication accompanying the origination of salmon fish (O'Malley et al., 2002). Thus, it is most likely that such genes regulating maturation are present in all the salmon species. However, in some cases that we stud ied (AEPSB hatchery), the extension in the matura tion period and spawning time took place almost dur ing one generation in the majority of individuals of a certain group; therefore, we cannot speak about the genetic nature of this phenomenon--the effect of the environment is evident. As is known, several environmental factors influ ence the time of fish spawning in addition to the gen otype (Lam, 1983; Koshelev, 1984). For example, the spawning commencement in salmonids is to a consid


142 t , °C 15 10 5
VI VII VIII IX X XI XII I (b) II III IV V ()

MAKHROV et al.

VI

15 10 5

VI VII VIII IX X XI XII I

II III IV V

VI

15 10 5

(c)

VI VII VIII IX X XI XII

I

II III IV V

VI

Month
Fig. 2. Annual temperature variations in (a) Mzymta River, (b) tanks of the Adler plant (Nikandrov et al, 2002), and (c) the AEPSB plant. The abscissa shows the spawning period of brown trout (Murza and Khristoforov, 1988; Babii et al., 2002; Nikandrov and Shindavina, 2007).

erable degree determined by the photoperiod (Brom age et al., 1989). However, extension of the spawning period and its advance towards spring was also observed in the Black Sea brown trout breeders from the Adler hatchery. The fish at this facility are kept in unshaded tanks, so the photoperiod does not differ from the natural conditions. The extension of the spawning period and its advance towards spring in the brown trout breeders raised at the AEPSB hatchery is likely to be connected with the water supply from springs. As for the Adler hatchery, the fish there are kept in the water taken from under the riverbed of the Mzymta River. Correspond ingly, the temperatures necessary for activation of sex product maturation at these facilities are reached later than in rivers, while the seasonal changes in tempera ture are less pronounced than in nature (Fig. 2). Most likely, these particular specific features of the temperature regimen to a considerable degree deter mine the slowed and less concurrent maturation of the breeders from both artificial populations. The temper ature changes at the AEPSB hatchery more consider ably differ from the natural conditions as compared with the Adler hatchery (Fig. 2); correspondingly, the change in the timing of spawning is more distinctly

pronounced. Presumably, a certain delay in the gonad development of the wild fish from the Pshada River was also connected with the fact that they spent the summer in cold spring water. Our conclusion agrees well with the literature data. For example, it has been shown that the brown trout spawns earlier in the upper reaches of rivers, where water cools faster, as compared with the lower reaches (Turyanin, 1982; Yakimov and Khatukhov, 2002). The spawning of the resident brown trout commences in January­March in the Russian spring fed rivers (Vre mya neresta..., 1893; Selegenenko, 1964). The brown trout reproduces in early spring in cold brooks of the Taurus Mountains, Turkey (Whittal, 1967). In an arte sian fed mountain brook in Spain, the spawning period of brown trout is extended from December to April (Gortazar et al., 2007), which is almost com pletely analogous to the spawning period of the brown trout at the AEPSB hatchery. The spawning of the brown trout inhabiting cold mountain lakes of the Caucasus is also delayed. In par ticular, some individuals in Lake Tabistskhuri spawn in February (Kavraisky, 1896), as well as the brown trout S. t. ezenami in Lake Eizenam (Saidov and Magome dov, 1989). The brown trout of Lake Paravani spawns from the end of November to the beginning of Febru ary (Barach, 1964). The brown trout of Lake Viso vacko in the Balkan Peninsula (described as an endemic species, S. visovacensis) spawns at the inflow and outflow of the Krka River, passing through the lake, in December and January and in the lake itself, according to survey data, in March and April (Taler, 1948). A spring spawning of the May trout S. schiffermul leri, living in mountain lakes in the upper reaches of the Danube River, was described (Heckel and Kner, 1858). The carpione S. carpio, inhabiting mountain Lake Garda (Italy), spawns in winter and spring; moreover, some individuals maturate twice a year (Melotto and Alessio, 1990). The forms of the Sevan trout S. ischchan (Savvaitova et al., 1989) and Ohrid trout S. letnica (Soric, 1990) with winter and spring­ summer spawning are described. The spawning season of bojak, a race of the Sevan trout, advanced from October­November to January­February and even March, when the spawning grounds dried making the fish move to deeper sites for spawning (Smolei, 1966). Of special interest are the trout from the mountain lake Posta Fibreno (Italy). The water temperature there is almost constant over the year, amounting to about 10°C (Zerunian, 2002). Two forms of trout inhabit the lake: one spawns in December­January and the other, in February­March (Gibertini et al., 1990). The former is described as an endemic species S. fibreni (Zerunian and Gandolfi, 1990). Data on the dependence of spawning time on water temperature are also available for other salmonids, in particular, the Atlantic salmon (Vladimirskaya, 1960; Johnston et al., 1992; Pankhurst and King, 2010). This
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species also spawns at different times in the upper and lower reaches of rivers (Webb and McLay, 1996), and a gradual, without any pronounced peaks, seasonal change in water temperature delays the spawning of the breeders of this species (Dikhnich, 2004). The rainbow trout grown in warmer water commences spawning earlier and in colder water, delays its spawn ing (Khristoforov and Murza, 1988; Scott, 1990; Pankhurst and King, 2010). Our studies and analysis of the published data dem onstrate that the spawning period of the representa tives of the genus Salmo can considerably vary being influenced by environmental conditions. Spawning in different seasons (twice a year) is possible even during the ontogenesis of one individual, as was observed in carpione (Melotto and Alessio, 1990). According to the observations of the authors, spawning of the Black Sea brown trout can extend from November to April (for a half year) due to pheno typic plasticity, and the offspring is quite viable. The spawning period of these individuals overlaps the spawning periods of all three "novel" species of the Ohrid trout, which spawn from October to January, from January to February, and from May to July (Soric, 1990). Thus, there are grounds to assume that the matura tion period of the Ohrid trout forms described as sep arate species--S. aphelios, S. balcanicus, and S. letnica--is to a considerable degree determined by temperature conditions, while the discreteness of their spawning periods results from the availability of only a few spawning grounds differing in their abiotic condi tions. It is likely that the maturation of the Ohrid trout forms is not discrete, since a characteristic of each form is numerous individuals reaching maturity by the end of the normal spawning season or even later (Soric, 1990). Presumably, these individuals do not "fit" the conditions of a particular spawning ground. The presence of such individuals is anticipated, if the spawning period is determined by the environment rather than genetic adaptation to a particular spawn ing ground. The spawning grounds of some salmonids are also subject to high variation, since, as experiments have shown, the site for future spawning of salmonids is usually determined by remembering a site in the aquatic body from which juveniles leave for feeding (Stabell, 1984). For example, it was demonstrated that although a form of the Sevan trout, the winter bakhtak, spawned in Lake Sevan, its fingerlings released into a tributary of the lake returned for spawning to this particular waterway (Vladimirov, 1942). As was mentioned above, another form of the Sevan trout, bojak, commenced spawning at deep sites when its spawning grounds were dried (Smolei, 1966). Note that homing in the brown trout is not so strict as compared with the other salmonids, and spawning migration to a nonnatal river (straying) is regularly observed (Makhrov et al., 1999).
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The differences in spawning periods or grounds of some Salmo forms alone are insufficient to regard them as separate species, especially when these differ ences are not confirmed by the most important criteria of species--genetic and morphological traits. For example, a diagnostic trait for S. aphelios (a form from Lake Orchid that spawns in May­June) according to Kottelat and Freyhof (2007) is an orange meat color. As is known, the fish meat color is to a considerable degree determined by the food objects, and it is difficult to imagine a less stable trait. The data on the differences in the frequencies of mitochondrial DNA haplotypes between the winter and summer spawning forms of the Ohrid trout described as S. letnica and S. aphelios, respectively, were obtained when studying a hypervariable region in mtDNA (control region 3' end) and should not be taken into account in evolutionary and population studies (Susnik et al., 2006, 2007). Some small distinc tions between the winter and summer spawning forms in the allelic frequencies of an allozyme locus (Wilson, 2004) may be a result of selection. Thus, it is likely that neither the duration nor the timing of the spanning period is an appropriate self sufficient criteria for species identification of the rep resentatives of the genus Salmo. ACKNOWLEDGMENTS The authors are grateful to the staff of the Sochi National Park for their assistance in sampling as well as to A.V. Dikhnich, E.A. Dorofeeva, K.V. Kuzish chin, M.V. Mina, I.G. Murza, V.Ya. Nikandrov, D.S. Pavlov, O.L. Khristoforov, N.I. Shindavina, and V.A. Yankovskaya for discussion of the issues covered in this paper. This work was supported by the Presidium of the Russian Academy of Sciences under the program "Biodiversity: Inventory, Functions, and Preserva tion" (projects nos. 2.3.1 and 23 P) and the Russian Foundation for Basic Research and the Administra tion of Krasnodar krai (project nos. 05 04 49232, 06 04 96735, and 11 04 00 69 7 a). REFERENCES
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