Biological Characteristics of Lower Amur Grayling Thymallus tugarinae (Salmoniformes: Thymallidae):...

ISSN 0032�9452, Journal of Ichthyology, 2013, Vol. 53, No. 4, pp. 281–292. © Pleiades Publishing, Ltd., 2013.Original Russian Text © P.B. Mikheev, V.I. Ostrovskii, N.N. Semenchenko, G.V. Novomodnyi, A.P. Shmigirilov, E.I. Barabanshchikov, 2013, published in Voprosy Ikhtiologii,2013, Vol. 53, No. 3, pp. 315–326.

281

INTRODUCTION

Lower Amur grayling Thymallus tugarinae is one ofthe most abundant species of graylings inhabiting thebasins of middle and lower Amur River, the rivers ofthe southern coast of the Sea of Okhotsk, and thenorthwestern Sakhalin. Data on the reproductive biol�ogy of this species, as well as the other species of gray�lings inhabiting Amur River, are extremely scarce(Mikheev, 2008; Mikheev and Gul’, 2009) despitetheir primary importance.

This study aims to analyze the variability in sex�sizeand size�sex structure, fecundity, and gonad�somaticindex (GSI) in different subpopulations of the lowerAmur grayling, as well as to assess the reproductionpeculiarities of this species in the lower stream of theAnyui River.

MATERIALS AND METHODS

The sampling areas, study period, and samplingmethods are described in the first part of the articleseries (Mikheev et al., 2012a).

The body length of the fish was measured with0.1�mm accuracy according to Smitt (SL), and thebody weight was estimated with 0.1�g accuracy (totalweight and weight without intestines). The fish age was

determined by analyzing fish scale under an MBS�12stereomicroscope (Russia) with ×50 magnification byone operator; the age of large specimens was alsochecked by otolith and vertebrae analysis. The gonadstage was determined under Lapitskii (1949). The sexof juvenile specimens was determined under the MBS�12 stereomicroscope with ×50 magnification. Thegonads were weighed with 0.01�g accuracy. The femalefecundity was measured in the autumn and springcatches, when their gonads were at III–IV stages. Thegonads of mature females were analyzed in freshlycaught fish, weighed, and placed into 4% formalde�hyde solution. After the gonads were fixed, they weretransferred into the water, weighed again, and the eggswere taken for the analysis from the center of thegonad. The weight of the fixed gonads and eggs wasestimated with 0.01�g accuracy. The subsample of thegonad was 12.1 ± 5.2% of the total gonad weight. Theindividual absolute fecundity (AF) was assessed as thenumber of the eggs in the sample and their weight tothe total weight of the gonad. The relative fecundity(RF) and GSI (%) was calculated in relation to the fishweight without intestines.

Statistical methods were used for data processing(Student’s t�test at significance level p = 0.05). Thedata processing was performed using Statistica 6.0software.

Biological Characteristics of Lower Amur Grayling Thymallus tugarinae (Salmoniformes: Thymallidae): 3. Reproductive Biology

P. B. Mikheeva, V. I. Ostrovskiia, N. N. Semenchenkoa, G. V. Novomodnyia, A. P. Shmigirilova, and E. I. Barabanshchikovb

a Pacific Research Institute of Fisheries and Oceanography, Khabarovsk Branch, Khabarovsk, Russiab Pacific Research Institute of Fisheries and Oceanography (TINRO), Vladivostok, Russia

e�mail: [email protected] August 9, 2011

Abstract—We discuss peculiarities of the reproductive biology of lower Amur grayling Thymallus tugarinae.The sex ratio in most of the studied samples was close to 1 : 1, but sometimes it might differ due to variousreasons. Females dominated among the specimens entering the first reproduction period; the rate of femalesdecreased in the fish older than 5 years. Maturation was usual in fish that reached 20�cm body length, whichreferred to the age 3+. The males became mature a year after the females of the same age in a half of the stud�ied rivers. Absolute fecundity, egg size and weight, as well as gonad�somatic index, correlated positively to theage of the fish, its body weight, and length. The lower Amur grayling spawned from the end of April throughthe last decade of May at the water temperatures exceeding +6°C in the downwelling areas located upstreamthe riffles, on the small�size gravel bottom sediments, at the depths of 0.8 m and less, where the current veloc�ity was less than 0.7 m/s. The spawning grounds in the main riverbed and tributaries of the lower stream of theAnyui River comprised 426.3 ± 148.6 m2 per km2, or 0.32 ± 0.11% of the water�surface area.

DOI: 10.1134/S0032945213020100

Keywords: lower Amur grayling Thymallus tugarinae, Amur River basin, sex structure, size�sex structure, sex�size structure, fecundity, gonad�somatic index, spawning

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MIKHEEV et al.

RESULTS AND DISCUSSION

Sex Structure

Primary ratio of the sexes in the studied catches ofthe lower Amur grayling was not studied, so thepresent study comprised the results of the secondaryand tertiary “male : female” ratios (Table 1).

The sex ratio in most of the samples was close to 1 : 1,which was usual for the grayling species (Zinov’ev,2005). The prevalence of the males over the femaleswas found both for the mature and juvenile specimensof the fish inhabiting Bikin River (370 km upstreamthe estuary). The prevalence of females was observedin the samples obtained 70 km downstream this sam�pling site. Such a difference in sex ratio together withthe variability in growth rate (Mikheev et al., 2012b)evidenced to their remaining at the same growingareas, which was usual for this genus (Zakharchenko,1973; Buzby and Deegan, 2000; Reid et al., 2002;Nykaenen et al., 2004). We suppose that these differ�ences in the sex rate are mostly preconditioned by thefish population density at different sites but not by thevariability of the environmental conditions. Accordingto our assessment, the average catch per unit of fishing

effort was 0.31 ind./m of standard fixed net1 per day in

the upper stream and 0.22 ind./m per day at the sitelocated 300 km upstream the estuary. This may be aconsequence of overfishing after the sport fishingactivities in this area; the great number of fish with thetraumas of the upper jaw is the other evidence of thisanthropogenic load. Such traumatized specimenswere not found at the site located 370 km upstream,

1 “Chameleon” pound net, 30�m length, 1.2�m height, 30�mmmesh size

which evidenced to less anthropogenic load in thisarea together with higher average catch per unit offishing effort and fish population density. Probably, thegrayling population density in this area was regulatedby natural mechanisms when the male rate in the off�spring increased; on the other hand, the female rateincreased in the area affected by intensive catch, i.e.,the compensatory mechanism aimed to increase thereproductive potential of the population. Regard mustbe paid to the uniformity of such mechanisms in fish(Nikol’skii, 1974) and in terrestrial vertebrates (Bujal�ska, 1983; Odum, 1986).

The sex ratio dynamics in regard to the ontogeneticprocesses was studied in our previous publications(Mikheev et al., 2012a). Male prevalence was the fea�ture of the juveniles and the fish of 4+�years and olderinhabiting the lower stream of the Anyui River. At thesame time, females dominate in the group of maturingspecimens and the fish reaching their first spawning(2+ to 3+). Such contradiction is preconditioned bythe seasonal sampling of the fish and because the dataobtained during different seasons were pooledtogether. When the fish were sampled during the grow�ing period, males dominated (61%) in both juvenileand adult groups; however, females prevailed (59–61%) within the mature specimens caught during thespawning period. Regard must be paid to the adult fishsampled in Khor River during the spawning period, whenthe rate of females was as high as 70.5% (Table 1).

The prevalence of females in the spawning fish can�not be explained by the fishing gear selectivity. Thespring catch on Khor River was obtained by the haulseine on the shallow spawning ground; in the AnyuiRiver, the fish were caught by the floating 3�wall nets(mesh size 25 mm) and the seine net (mesh size 20 mm).

Table 1. Sex ratio in the catches of juvenile and mature specimens of lower Amur grayling Thymallus tugarinae

RiverJuveniles, ind. (%) Mature, ind. (%)

males females males females

Anyui River, stream:

– lower 95 (61.7) 59 (38.3) 83 (42.8) 111 (57.2)

– middle 28 (45.9) 33 (54.1) 22 (44.9) 27 (55.1)

Bikin River, km from estuary:

– 370 26 (57.8) 19 (42.2) 31 (68.9) 14 (31.1)

– 300 30 (44.1) 38 (55.9) 27 (41.5) 38 (58.5)

Kur River 50 (52.6) 45 (47.4) 47 (45.2) 57 (54.8)

Limuri River 36 (54.5) 30 (45.5) 20 (52.6) 18 (47.4)

Manoma River – – 20 (52.6) 18 (47.4)

Nizhnii Mel'gin River 18 (60.0) 12 (40.0) 17 (48.6) 18 (51.4)

Nizhnyaya Patkha River 48 (49.0) 50 (51.0) 17 (54.8) 14 (45.2)

Tarakanovka River 40 (55.6) 32 (44.4) – –

Khor River 71 (46.1) 83 (53.9) 18 (29.5) 43 (70.5)


BIOLOGICAL CHARACTERISTICS OF LOWER AMUR GRAYLING 283

We suppose that the domination of the females byabundance during the spawning period may beexplained by the combined effect of several factors.These factors include earlier maturation of females(Table 2; Fig. 1), decrease of the total fish abundancewith their aging, and the ability of the males to spawnintermittently. The last fact is proved by the results ofthe fish dissection; the mature specimens were sam�pled in the lower stream of the Anyui River in the endof April and early June 2010. Most of the males werecharacterized by leaky sperm in both cases (33% and62%, respectively). On the other hand, the females

were at IV stage in April, and already spawned in June.The ability of the males to spawn intermittently maycombine with their territory�related behavior and theparticipation of one male and several females in thespawning act. This was also observed for the Europeangrayling T. tugarinae inhabiting the water bodies ofSweden (Fabricius and Gustafson, 1955) and graylingT. arcticus inhabiting North America (Bishop, 1971;Tack, 1971; Kratt and Smith, 1980).

Regard must be paid to the absence of any differ�ences in the sex ratio of juvenile fish sampled in the

Table 2. Number of mature males and females and their rate from the total abundance of females (males) in different agegroups of lower Amur grayling Thymallus tugarinae in some studied rivers, ind./%

River Month of sampling

Age group

1–1+ 2–2+ 3–3+ 4–4+

females males females males females males females males

Anyui River, stream:

– lower IX–XI 1/3.5 – 37/52.1 12/27.3 26/89.6 12/52.2 5/100 14/100

– '' V–VI – – – 5/38.5 5/55.5 4/21.1 14/100 11/100

– middle VI–VII – – – – 11/84.6 9/90.0 2/100 3/100


– 370 VI 2/10.5 – 5/71.4 5/41.7 6/100 16/94.1

– 300 VI 1/12.5 – 22/91.7 4/40.0 14/100 17/100

Kur River X – – 13/28.9 12/31.6 14/100 10/100 7/100 5/100

Limuri River VI – – – 1/3.6 9/100 8/100 1/100 2/ 100

Nizhnii Mel'gin River X – – 1/25.0 1/ 14.3 9/81.8 7/58.3 2/100 4/100

Nizhnyaya Patkha River

VII–VIII – – – 2/9.1 4/80.0 5/83.3 6/100 8/100

Khor River V – – – – 20/90.9 7/100 4/100 2/100

Ibid IX–X 1/4.3 – 1/50 – 2/100 2/100 5/100 3/100

100

80

60

40

20

0

226�230

216�220

201�205

191�195

176�1

80

166�1

70

221�225

211�215

206�210

196�2

00

186�1

90

181�185

171�175

Size class, mm

Rat

e of

mat

ure

spec

imen

s, % (а)

(b)

171�173

162�1

64

159�161

153�155

146�1

49

174�176

168�170

165�167

156�158

150�152

Fig. 1. Frequency of occurrence of the (–�–) male and (� � � � �) female mature specimens of lower Amur grayling of differentsize classes: a—Anyui River (females—y = 46.61 ln(x) – 16.94, R2 = 0.89, n = 93 ind.; males—y = 0.79 х2 – 3.34 х + 8.11, R² =0.89, n = 83 ind.); b—Kur River (females— y = 52.73 ln(х) – 20.02, R² = 0.90, n = 43 ind.; males— y = 1.17 х2 – 0.67 ⎯ x +6.04, R² = 0.91, n = 44 ind.).

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MIKHEEV et al.

lower stream of the Anyui River in different years,which may evidence to the relative stability of theenvironmental conditions for grayling population sus�tainment in this area.

Age and Size of Maturing Fish

In most studied areas, maturation of the lowerAmur grayling occurred at the age of 3+ in most of thestudied populations, which was common for the gray�ling species characterized by middle life span(Zinov’ev, 2005). The development of the reproduc�tive functioning is mostly preconditioned by the fishsize than by their age. Particularly, the graylings inhab�iting the basin of the Anyui River have the most rapidgrowth (Mikheev et al., 2012b) and reach maturityearlier than the other subpopulations of this region, atthe age of 2+ (Table 2).

Opposite to the males, some fast�growing femalesmay reach maturation even at the age of 1+ and spawnthe next year at the age of 2 years. Particularly, adultmature female (2�age) sampled in autumn in the lowerstream of the Anyui River was the largest in its agegroup (SL = 198 mm, body weight 106 g). The otherexample is the female sampled in Khor River (SL =140 mm, body weight 31 g). Male maturation in mostof the grayling population usually occurs at the sameage as is observed for the females (Kur River, NizhnayaPatkha River, Limuri River) or a year later (AnyuiRiver, Nizhnii Mel’gin River, Bikin River) (Table 2).

The body length and weight of the adult specimensduring the period of the maturation in most of thegrayling population (in the representative samples)were linked to the growth peculiarities of the graylings.Higher average body weight and length were the char�acteristics of the fast�growing populations at theperiod of maturation in most of the grayling popula�

tion and vice versa (Table 3, Fig. 1) (Mikheev et al.,2012b).

The females usually reach maturity at a smallerbody weight and length compared to the males. This isapplicable for both the fish reaching the maturation atthe same age and for the males and females thatbecome mature at different ages that, in turn, may bepreconditioned by large energetic traits by the femalesfor vitellogenesis (Koshelev, 1971). Regard must bepaid to the significant differences in male and femalesbody size tracking already at gonad stage II (beginningof protoplasm growth), when the fish are maturing. Inthe Anyui River, the average body length, and weightof these females of 2+�age were 183.8 ± 3.9 mm and75.8 ± 5.2 g; males were 195.2 ± 2.4 mm and 88.8 ±2.7 g, respectively. Before the maturation started, thejuvenile males and females did not differ by their bodylength. The growing curves in maturing males of dif�ferent size groups were less sharp than for the females,since the development of the reproductive system inmales occurred in more size classes (Fig. 1). Togetherwith the later gonad maturation registered in a numberof cases, this may be concluded to be a feature of thesex dimorphism in grayling (Mikheev, 2009).

Assessing the age of gonad maturation in most ofthe grayling population, specific attention must bepaid to the analysis of the autumn not the springcatches. Definition of the first spawning of young fishby their gonad state (the next year or in a year after) isquite problematic when analyzing the material sam�pled in spring�early summer, since the fish are enteringthe early stages of gonad maturation during thisperiod. When analyzing the autumn catches, thereadiness of the fish for spawning the coming springmay be assessed easily and significantly. Probably, theage of gonad maturation in most of the grayling popu�

Table 3. Average body length (SL) and weight (M ± m) of males and females of lower Amur grayling Thymallus tugarinaeduring the maturation period

River Month and year of sampling

Males Females

SL, mm Body weight, g SL, mm Body weight, g

Anyui River X.2008 210.0 ± 2.3 114.7 ± 6.7 197.2 ± 2.7 101.9 ± 4.9

Ibid XI.2009 219.5 ± 2.9 138.8 ± 3.0 201.2 ± 1.8 111.7 ± 3.3

'' IV.2010 227.5 ± 7.0 134.4 ± 13.1 212.7 ± 5.9 118.3 ± 9.7


– 370 VI.2010 178.5 ± 4.9 77.8 ± 6.5 169.6 ± 5.1 66.4 ± 8.3

– 300 VI.2010 180.0 ± 2.7 79.7 ± 3.5 169.1 ± 9.8 56.5 ± 8.63

Kur River X.2006 172.6 ± 1.9 59.2 ± 1.8 156.6 ± 1.5 44.9 ± 1.6

Nizhnii Mel'gin River X.2006 200.0 ± 3.8 99.6 ± 3.3 189.3 ± 1.9 90.8 ± 3.7

Urmi River X.2008 203.2 ± 4.1 94.2 ± 5.7 189.5 ± 3.9 77.7 ± 4.9

Khor River V.2007 211.9 ± 7.0 109.4 ± 12.2 198.9 ± 2.7 96.8 ± 4.9

Note: Here and in Tables 4–7: M ± m are the arithmetical means and asymptotic standard errors.



lation may be overestimated if studied in the springsamples.

Fecundity

The individual absolute fecundity AF of lowerAmur grayling and its variability increased togetherwith the fish age (Table 4, Fig. 2), as was observed forthe other fish species. AF was closely linked to the bodylength and weight (Table 5), as was registered in theother graylings (Aganovic �, 1965; Tugarina, 1981;Zinov’ev, 2005). The linear relationship between thebody weight and fecundity was the most pronounced(Table 5, Fig. 2) when the coefficient of correlation (r)of these two parameters was 0.94. The dependence ofAF on the body length and age was better described bythe power function, which was in turn preconditionedby the close relationship between the AF and bodyweight. The overall tendency of AF dynamics in regardto the listed parameters was observed in every sample,but it might vary significantly for the fish sampled indifferent rivers (Fig. 2).

The most pronounced differences in AF betweenthe age groups of graylings were found for the popula�tions inhabiting the Kur River and the Anyui River; inthe last case, it exceeded the same parameter for theKur River population twofold in all the age groups.This was linked to the significant differences in thegrowth rate, and it was also observed for AF of the pop�ulations inhabiting the Anyui, Khor, and NizhniiMel’gin rivers (Table 4). Low AF was characteristic ofthe graylings inhabiting Sakhalin. The average AF of6+�age fish sampled from Langra River was 3118 eggs(2783–5005, n = 4 ind.) (Safronov et al., 2001);

meanwhile, fish of the same age sampled in the AnyuiRiver were characterized by higher AF (Table 4). Aswell, the fish from Sakhalin were significantly smaller(Mikheev et al., 2012b).

The average AF of grayling of the same size classinhabiting the lower stream of the Anyui River andsampled during the autumn period in different yearsdid not differ significantly, which allowed us to poolthese data as one dataset (Table 4). However, the com�parison of AF of the fish of 3+�age and 4+�age sam�pled in spring 2010 with the same fish caught inautumn 2009 (2+�age and 3+�age, respectively) evi�denced that the AF in the “autumn” fish was signifi�cantly lower than in the spring catches. This contra�dicted the earlier studies (Ivankov, 2001), when thenumber of ripe (yolk�carrying) oocytes decreased sig�nificantly during the gonad development (from stage

II–III to stage IV�B2 as was found for many fish spe�

cies. This contradiction may be linked with the sam�pling site, i.e., in spring 2010, the fish were caught15 km upstream the site used in autumn. Since therewas a close relationship between AF and fish growthrate, we have compared the calculated values of bodylength and weight for the graylings at the moment ofstarting the new year of life, i.e., the moment of devel�oping the second and the third annual scale rings forthe fish of 3(2+)�age and 4(3+)�age, respectively. Itwas found that the fish from spring catches differedfrom the “autumn” graylings by significantly highergrowth rate, which might evidence to better growingconditions for the fish inhabiting the areas 15�kmupstream the “autumn” sampling site. We suppose

2 Gonad stages are given according to Persov and Skakun (1962).

Table 4. Absolute and relative fecundity of lower Amur grayling Thymallus tugarinae

RiverMonth

and year of sampling

Age, years

1+ 2+ 3–3+ 4–4+ 5–5+ 6

Anyui River, lower stream

IX–XI.2007–2009

Ibid IV.2010

Kur River X.2006

Nizhnii Mel'gin River X.2006

Khor River X.2007

'' V.2007

Note: Absolute fecundity is above the line; relative fecundity (egg no./ind.) is below the line. Numbers in brackets indicate the numberof studied specimens.

162818.0 1( )�� 1446 65.7±

15.8 0.6 37( )±�� 2035 115.6±

17.7 0.6 25( )±�� 2659 19.2±

19.2 2.1 5( )±��

1806 254.5±

18.5 0.3 2( )±�� 2956 160.7±

20.0 0.8 11( )±�� 4120 606.6±

20.9 0.8 3( )±�� 4765 294.0±

22.1 1.4 6( )±��

803 83.4±

18.5 1.7 9( )±�� 986 62.8±

16.8 1.4 14( )±�� 1564 101.0±

17.8 0.9 7( )±��

1479 63.5±

19.0 0.5 14( )±�� 2685 1020.2±

24.6 5.0 2( )±�� 2453 287.8±

17.6 0.1 2( )±��

62625.5 1( )�� 895 112.0±

18.4 2.6 2( )±��

1413 102.9±

18.2 0.8 17( )±�� 1767 253.2±

16.3 1.7 4( )±��

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MIKHEEV et al.

5

4

3

2

1

064321 5

Age, years

5

4

3

2

1

0250210190170150 230

Body length, mm

5

4

3

2

1

01901007040 220

Body weight, g

130 160

(e) (f) (g)

5

4

3

2

1

034028016040

IX

220100

6

5

4

3

2

1

034028016040

X

220100

6

5

4

3

2

1

034028016040

XI

220100

6

5

4

3

2

1

034028016040

XII

220100

6

Body weight, g

5

4

3

2

1

0300270210150

VIII

240180

6

5

4

3

2

1

0300270210150

VII

240180

6

5

4

3

2

1

0300270210150

VI

240180

6

5

4

3

2

1

0300270210150

V

240180

6

Body length, mm

5

4

3

2

1

06531

I

42

6

5

4

3

2

1

06531

II

42

6

5

4

3

2

1

06531

III

42

6

5

4

3

2

1

06531

IV

42

6

Age, years

(а) (b) (c) (d)F

ecu

nd

ity,

th

ou

san

ds

eggs

Fig. 2. (a–d) empirical and (e–g) theoretical dependence of individual absolute fecundity on (aI, bII, cIII, DIV) age, (aV, bVI,cVII, DVII) body length, and (aIX, bX, cXI, DXII) body weight of females of lower Amur grayling Thymallus tugarinae inhabitingdifferent rivers: a—Anyui River (–�–); b—Kur River (–�–); c—Nizhnii Mel’gin River (–�–); d—Khor River (–×–).



that such difference may support the idea of sedentari�zation in lower Amur graylings, which may beobserved for the fish subpopulations inhabiting theareas that are situated close by each other.

It is known that AF depends on the egg diameterand weight. As well as AF, the egg diameter and weightincreased together with the fish growth, i.e., with itsage, body length, and body weight (Table 6). The rela�tionship of the egg size with these parameters was evenmore tight, i.e., the coefficients of correlation of theegg diameter with the fish age, body length, and bodyweight were 0.72, 0.66, and 0.73, respectively, for thefish sampled in the lower stream of the Anyui River.Because of high variability of the individual eggweight, this parameter depended less on the samecharacteristics of the fish, and the coefficients of cor�relation were 0.69, 0.45, and 0.65, respectively. Theegg diameter and weight of the graylings of differentpopulations varied greatly, which was preconditionedby the variability of the fish body length and weight inregard to the age classes. For example, when studyingthe fish of the same age group, the smallest eggs werefound in the slow�growing graylings sampled in theKur and Nizhnii Mel’gin rivers in October, and thebiggest ones were found in fast�growing graylings ofthe Anyui and Khor rivers (Table 6).

The relative fecundity, RF, in lower Amur graylingdepended differently on the fish age, length, andweight (Table 4) opposite to the common rulesobserved for AF, as well as for the egg size and weightparameters. The RF of the graylings inhabiting theAnyui River increased during the growth, but the

opposite pattern was observed for the populationinhabiting the Khor River, when RF decreased withinthe increase of fish age and weight. Relatively stableRF was registered for the graylings from the Kur River.

The RF in maturing young females from differentpopulations was similar, which might be evidence ofthe common mechanism of the reproductive systemdevelopment. However, during ontogenesis, the RF inthe females from different populations varied signifi�cantly. This may be linked with the conditions duringthe growing period that mostly affect the reproductivemetabolism of females but not their somatic growthrate, as it is found for many fish species (Spanovskayaand Grigorash, 1976; Krokhalevskii, 1980; Volodin,1983; Izyumov et al., 1983).

Interestingly, the slow�growing specimens of Euro�pean grayling (stream ecotype) are characterized byhigh RF (Zinov’ev, 2005). The opposite pattern wasobserved for lower Amur grayling. The maximal RFwas the characteristic of the fast�growing fish inhabit�ing the Anyui River, but low RF was observed for theslow�growing graylings from the Kur River that weresimilar to the European grayling by the growth rate,age structure, and AF. In addition, the graylings fromthe Kur River had other characteristics atypical for thestream graylings T. thymallus of short life span, partic�ularly, the maturity age (typical for the fish of middlelife span) and the egg size (similar to the egg size offast�growing graylings inhabiting the Anyui River). Wesuppose that primarily the graylings inhabiting the KurRiver are characterized by higher AF, relatively highgrowth rates, and their life span is longer. The decrease

Table 5. Parameters of equations describing the dependence of individual absolute fecundity (AF, egg no./ind.) in graylingThymallus tugarinae on the age (T, years), body length (L = SL, mm), and body weight (Q, g)

RiverEquation parameter Coefficient

of determinationa b

AF = aT b

Anyui River 384.70 ± 51.19 1.40 ± 0.09 0.82

Kur River 196.02 ± 53.12 1.35 ± 0.20 0.56

Nizhnii Mel'gin River 190.16 ± 94.76 1.67 ± 0.35 0.55

Khor River 176.19 ± 81.9 1.89 ± 0.37 0.53

AF = aL b

Anyui River 3.13 × 10–7 ± 0.33 4.18 ± 0.18 0.82

Kur River 7.53 × 10–5 ± 0.12 3.16 ± 0.30 0.74

Nizhnii Mel'gin River 1.79 × 10–5 ± 0.66 3.92 ± 0.67 0.64

Khor River 2.32 × 10–4 ± 0.32 2.94 ± 0.25 0.83

AF = a + bQ

Anyui River –544.27 ± 114.60 18.80 ± 0.74 0.88

Kur River 31.10 ± 13.24 14.41 ± 1.44 0.75

Nizhnii Mel'gin River –203.12 ± 35.96 19.43 ± 3.51 0.70

Khor River 113.29 ± 13.13 156.43 ± 1.29 0.81

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MIKHEEV et al.

in all the listed parameters led to high similarity of theKur River graylings to slow�growing fish with short lifespan; this event was recent, since there was a targetedelimination of fish of older ages and fast�growing spec�imens. In our opinion, the restoration of the naturalcharacteristics of this population is possible if uncon�trolled seine commercial fishing is stopped.

Gonad�Somatic Index

Average GSI in the juvenile specimens (1+�age)inhabiting the lower stream of Anyui River was 0.34 ±0.07 for females (0.20–0.43, n = 13) and 0.17 ± 0.05for males (0.12–0.22, n = 12). GSI increased accord�ing to the age of immature specimens and was signifi�cantly higher in the fish of 2+�age compared to thegraylings sampled in autumn (Table 7); this was mostpronounced in females because their oocytes enteredthe last stages of protoplasm growth. The beginning oftrophoplasmatic growth of oocytes led to rapidincrease of GSI (Ivankov, 2001), and the range of GSIin 3�year�old graylings (III stage of gonad develop�ment) inhabiting the lower stream of the Anyui Riverexceeded this parameter manifold compared to theimmature specimens. GSI increased also in accor�dance to the fish age and growth, particularly, inmature females, whose gonads were at the stage of tro�phoplasmatic growth of oocytes. The increase of GSIin regard to the fish age was pronounced in malesmuch less than in females (Fig. 3). Maximal GSI wereusually observed in the prespawning period, and min�imal was observed after the spawning, which was natu�ral (Table 7). As was observed for AF, GSI dependedmore on fish size than on age, which could be easilytracked by the coefficient of determination, i.e., 0.98

vs. 0.89 in females and 0.95 vs. 0.89 in males, respec�tively.

In addition, GSI correlated to the growth rate.Fast�growing females (gonad stage III) sampled in theAnyui River in October were characterized by signifi�cantly higher GSI than slow�growing fish caught inthe Kur and Nizhnii Mel’gin rivers. Average GSI infemales was 4.62 ± 0.16 (3�year�old), 6.47 ± 0.38, and7.91 ± 0.48 (5�year�old) in the Kur River; and 5.88 ±0.32 (4�year�old) and 7.32 ± 1.05 (5�year�old) in theNizhnii Mel’gin River, respectively. However, this ten�dency was not found in males. GSI was higher in3�year�old males from the Anyui River compared tothe specimens sampled in the Kur River, but the oppo�site pattern was observed for 4�year�old males. Thelowest GSI was a characteristic of the males inhabitingthe Nizhnii Mel’gin River. The absence of any rela�tionships between the growth rate and GSI in malesmay be explained by the priority of female reproduc�tive characteristics in population recruitment.

Spawning Grounds and Spawning

Lower Amur grayling starts to reproduce the earli�est among all the other salmonids spawning in spring.The spawning of lower Amur grayling in the basins ofAnyui River and Khor River usually starts in the end ofApril–the first decade of May, 2–3 weeks after the icestarts to melt. In 2010, the spawning started later(around May 14) because of the late spring. The watertemperature was +6°С. The spawning lasted until May23, when it was interrupted by flood. This led to rapidincrease of the water level and water turbidity. Regardmust be paid to the spawning habits of grayling, andthe reproduction occurs before or after the flood

Table 6. Individual weight and size of the eggs of lower Amur grayling Thymallus tugarinae of different age groups

RiverMonth

and year of sampling

Age, years

1+ 2+ 3–3+ 4–4+ 5 6

Anyui River, lower stream IX–XI.2007–2009

Ibid IV.2010

Kur River X.2006

Nizhnii Mel'gin River X.2006

Khor River X.2007

Ibid V.2007

Note: Individual weight of the egg (mg) is above the line; egg diameter (mm) is below the line. Numbers in brackets indicate the numberof studied specimens.

5.72.0 1( )�� 3.9 0.3±

1.6 0.1 34( )±�� 4.2 0.2±

1.7 0.1 24( )±�� 4.3 0.6±

1.9 0.1 5( )±��

7.1 0.5±

2.4 0.1 2( )±�� 8.8 0.2±

2.6 0.1 11( )±�� 9.8 0.3±

3.0 0.4 3( )±�� 9.5 0.5±

2.7 0.1 6( )±��

2.4 0.1±

1.6 0.1 9( )±�� 3.3 0.2±

1.8 0.1 14( )±�� 3.6 0.3±

2.0 0.1 7( )±��

3.0 0.1 13( )±

–�� 2.3 0.2 2( )±

–��

2.71.5 1( )�� 4.6 0.9±

1.9 0.1 2( )±��

8.3 0.4±

2.4 0.0 14( )±�� 9.7 1.3±

2.7 0.1 5( )±��



(rarely), but never in this combination. If the floodstarts at the beginning of the spawning and the flood islong lasting (until the water warms up to 12–15°С),most of the specimens do not reproduce, and thespawning effectiveness is extremely low. After that,most of the females sampled in June–July carry “full”gonads. Nonreleased oocytes of these females areresorbed and the gonads are dark red.

Several spawning grounds of lower Amur graylingwere studied in late May 2010 in the lower stream ofthe Anyui River (Fig. 4). The spawning grounds werelocated before the riffles (Fig. 4b), where the riverinewater infiltrated to the underflow (downwelling), and

this fact led to the identity of the temperature and gasregimes in the bottom sediments and on the surface.Approximately 70% of the spawning grounds werelocated in the tributaries (channels 5–20�m wide), theothers were in the mainstream of the Anyui River.Probably, lower Amur grayling preferred to spawn inthe small tributaries because of the earlier ice releasethere, especially in the lower stream of the AnyuiRiver. In the mainstream, lower Amur grayling alsospawned in the areas of water infiltration located alongthe shore (Fig. 4a).

The ecology of lower Amur grayling is similar to theother fish of Thymallidae family; they spawn usually in

Table 7. Dynamics of gonad�somatic index of lower Amur grayling Thymallus tugarinae sampled in the lower streamof the Anyui River

Age, yearsMonths

april july september october november

Females

2+–3

3+–4

4+–5

5+–6

Males

2+–3

3+–4

4+–5

5+–6

Note: Parameters of juveniles are above the line; those of mature specimens are below the line. Numbers in brackets indicate the numberof studied specimens.

0.39 0.02 3( )±

13.13 1.20 2( )±�� 0.31 0.02 7( )±

–�� 0.47 0.07 4( )±

4.93 0.18 8( )±�� –

6.22 0.53 4( )±�� 0.42 0.02 4( )±

7.65 0.23 24( )±��

–17.45 0.39 11( )±�� 0.35 0.01 3( )±

0.79 0.03 10( )±�� –

5.83 0.40 3( )±�� –

8.01 0.64 4( )±�� –

9.94 0.99 4( )±��

–20.49 0.85 3( )±�� –

0.88 0.01 2( )±�� –

7.20 0.51 2( )±�� –

10.58 1.15 2( )±��

–20.80 0.86 6( )±�� –

0.70 0.29 2( )±��

0.15 0.01 2( )±

1.95 0.35 2( )±�� 0.19 0.02 9( )±

–�� 0.19 0.03 6( )±

2.70 0.42 3( )±�� –

2.84 0.33 3( )±�� 0.21 0.01 2( )±

2.34 0.13 6( )±��

–2.42 0.14 10( )±�� –

0.22 0.02 9( )±�� –

3.71 0.11 2( )±�� –

2.30 0.13 3( )±��

–2.83 0.10 4( )±�� –

0.37 0.12 3( )±�� –

3.21 0.19 8( )±�� –

2.3 1( )��

–2.88 0.08 2( )±�� –

3.9 1( )�� –

2.63 0.18 3( )±��

25

20

15

10

5

0654321 271–300241–280211–240181–210150–180

(a) (b)

Fig. 3. Dependence of average gonad�somatic index (%) of ( ) males and ( ) females of lower Amur grayling Thymallus tugari�nae inhabiting the Anyui River on (a, years) age and (b, mm) body length. Females: a—y = 1.62 e0.47x, R2 = 0.89; b—y =0.72 x2.19, R2 = 0.98; males: a—y = 0.19 x1.70, R2 = 0.89; b—y = 0.27 x1.54, R2 = 0.95.

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MIKHEEV et al.

spring at the water temperatures of +4°+11.6°C, onthe bars built by small gravel, in the areas of slow cur�rents (up to 1 m/s), and at the depths of less than 1 m(Zinov’ev, 2005).

The average spawning depth of lower Amur graylingvaried from 25.1 ± 1.33 to 37.2 ± 0.93 cm. The spawningwas even registered at the depth of 10–15 cm. Thespawning on the shallow sites may be linked with earlystart of grayling reproduction, since these areas warmup first. The spawning substrate was the small gravel1–6�cm in size (3.73 ± 0.73 cm on average). Some�times, sand and stones (15–20 cm) were present, buttheir ratio did not exceed 10–15%. The average cur�rent velocity at the spawning ground (before the riffle)varied from 0.32 ± 0.09 up to 0.55 ± 0.02 m/s. Only atone site was the current velocity on the reach locatedbefore the spawning ground the same as before the rif�fle. Sometimes, it was lower, i.e., 0.25 ± 0.02 and0.43 ± 0.06 m/s, respectively. The current velocity onthe riffles located downstream the spawning groundvaried from 0.71 ± 0.03 up to 0.93 ± 0.01 m/s.

The lower Amur grayling forms compact nests,which are easily tracked by clean gravel (without foul�ing and silty sediments) upon them. The nests are theshallow hollows in the substrate. They are down to5�cm deep (2.8 ± 0.9 cm on average); the diametervaries from 18 to 35 cm (22.3 ± 2.1 cm). After some ofthe nests, small hillocks 3–4�cm in height are located.The eggs are laid on the sediment surface and in theupper layer of sediment, but not deeper than 5 cm.

The number of the nests on the spawning groundmay vary depending on the number of spawning fish.The minimal nest density was 1–3 per 10 m2 at thelowest spawning activity on the ground. When thenumber of reproducing graylings is high and the envi�

ronment is favorable for the spawning, the assessmentof the nest number may be incorrect due to failure indefining their margins. Such cases are quite usual inthe lower stream of the Anyui River, when the samenests may be used by several spawning specimens oneafter another.

The number and area of the sites favorable for lowerAmur grayling spawning were assessed in the lowerstream of the Anyui River. One to six (on average,4.3 ± 1.0) favorable sites were located per kilometer ofthe river (including the mainstream and the tributar�ies). The area of one spawning ground comprised from20 to 200 m2 (102.1 ± 32.3 m2). The multiplication ofthese two parameters resulted in 426.3 ± 148.6 m2/kmtotal coverage, or 0.32 ± 0.11% of the water surface forthe areas favorable for lower Amur grayling spawningin the lower stream of the Anyui River, including themainstream and the tributaries.

The population density of lower Amur grayling in thelower stream of the Anyui River is 191 ± 34 ind./hectareof water surface (Mikheev, 2010), or 3552 ± 328 ind./kmof river. If all these specimens are accounted to bemature, the “spawning density” is approximately 8.3 ±1.4 ind/m2 or 4 males per square meter of spawningground. This assessment is extremely high for the gray�ling species. According to other researchers (Fabriciusand Gustafson, 1955), the males of European graylingdefend their spawning grounds of the area of 0.8 up to16.0 m2. In North America, these areas are even larger,4.3–7.4 m2 (Tack, 1971), 6.6 m2 (Bishop, 1971), and6.1–15.5 m2 (Kratt and Smith, 1980). The males oflower Amur grayling also defend their spawninggrounds. We did not assess the area of the spawningground defended by a single male. However, takinginto account the population density of lower Amur

0.4 m/s

0.3 m

0.1 m/s

0.4–0.7 m0.3 m/s

0.25 m

0.25 m

0.2 m

0.2 m

0.8 m/s

0.7 m/s

0.6 m/s

0.5 m/s

0.1 m/s

10 m10 m

Island

Island

(а) (b)

Fig. 4. Location of the spawning grounds of lower Amur grayling Thymallus tugarinae in the main stream of the (a) Anyui Riverand the scheme of the spawning ground in (b) its tributary: ( )—spawning ground; ( )—alluvial gravel sediments (reaches);( )—margin of the undermined brae; ( )—vector of the current; bold font indicates the depths; italic font indicatesthe current velocity.



grayling in the Anyui River and the published range ofthe defended areas, we have to conclude on the insuf�ficiency of the spawning grounds for this species. Onthe other hand, the prevalence of females on thespawning grounds smoothes this insufficiency. Theprevalence of females may be linked with later matura�tion of males and significant mortality of lower Amurgrayling (instantaneous rate of total mortality offemales is 0.72 ± 0.25; males is 0.64 ± 0.18) and by theuse of the same spawning ground by the fish reproduc�ing in the following days. In addition, different behav�ior strategies employed by the males may optimize useof the spawning grounds. For example, the males ofEuropean grayling inhabiting water bodies of Belgiumare clearly divided by defending and nondefendingtheir spawning grounds. However, the spawning effec�tiveness of the males employing different behavior issimilar when their population density is high enough(Persat and Zakharia, 1992; Darchambeau and Pon�cin, 1997). Regard must be paid to similarities foundin other fish species, for example, for sockeye salmonOncorhynchus nerka (Parenskii, 1992).

CONCLUSIONS

(1) The sex ratio is close to 1 : 1 in most of the sam�ples. Females dominate in the group of the first�timematuring specimens; their ratio decreases in the groupof fish older than 5 years. This may be preconditionedby their higher mortality rates. We define lower Amurgrayling as the III type of the size�sex ratio in fish tak�ing into account male domination in older age groupsand their bigger weight compared to the females(Zamakhaev, 1959).

(2) Most of the population matures at the age of3+, when the body length reaches 20 cm; this is typicalfor the grayling species characterized by middle lifespan. Fast�growing specimens mature a year earlier,which also supports the idea that the maturation startswhen the fish reaches a particular body size. Rarely,females may start reproducing at the age of 1+, but themales mature a year later than females. Average bodysize and weight in immature females is usually lowerthan in males of the same age.

(3) Individual absolute fecundity and size�weightparameters of the eggs of lower Amur grayling corre�late positively with the fish age, body length andweight, and the growth rate. The most pronouncedrelationship was found between AF and size�weightparameters of fish. The highest AF is registered for thefast�growing lower Amur grayling inhabiting the AnyuiRiver and the lowest was found for slow�growing spec�imens of the Kur River. The AF depends on the size�weight parameters and the age of fish inhabiting dis�tinct water bodies differently.

(4) GSI depends more on the fish size than on thefish age. The highest GSI is registered for the fast�growing females inhabiting the Anyui River and thelowest is found for slow�growing specimens of the Kur

River. No such relationships are found for the males oflower Amur grayling.

(5) The spawning begins in the end of April andlasts through the last decade of May, when the watertemperature reaches +6°С. The fish use the down�welling area upstream the riffles and bends. Most ofthe spawning grounds locate in the tributaries. Smallgravel (1–5 cm), depths of less than 0.8 m, and currentvelocity up to 0.7 m/s are the limiting factors for thegrayling spawning. The spawning grounds in the mainriverbed and tributaries of the lower stream of theAnyui River cover 426.3 ± 148.6 m2 per 1 km2, or 0.32 ±0.11% of the water�surface area; we assume this as alimiting factor for the grayling population recruitmentin this area.

ACKNOWLEDGMENTS

We are grateful to A.K. Kyalundzyuga (local ofArsen’evo settlement, Nanaiskii District, KhabarovskKrai) for invaluable help in field sampling.

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Translated by D. Martynova

Biological Characteristics of Lower Amur Grayling Thymallus tugarinae (Salmoniformes: Thymallidae):...

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