ISSN 00329452, Journal of Ichthyology, 2014, Vol. 54, No. 2, pp. 186–194. © Pleiades Publishing, Ltd., 2014. Original Russian Text © D.S. Pavlov, V.V. Kostin, V.Yu. Ponomareva, 2014, published in Voprosy Ikhtiologii, 2014, Vol. 54, No. 2, pp. 216–224.
Aggressive Behavior as a Mechanism of Spatial Differentiation of Juvenile Salmonid Fishes (Based on Black Sea Brown Trout Salmo trutta labrax (Salmonidae)) D. S. Pavlov, V. V. Kostin, and V. Yu. Ponomareva Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 117071 Russia email:
[email protected] Received May 16, 2013
Abstract—Aggressive behavior of hatcheryreared juvenile Black Sea brown trout Salmo trutta labrax at the age of 5.5–6.0 months is investigated. Shortage of suitable territory leads to the separation of the fish into two spatial groups: demersal and pelagic. During the process of spatial differentiation of the fish, the individuals that have not selected permanent habitats (demersal or pelagic) are characterized by the highest aggression level. The duration of the formation of stable spatial differentiation of the fish depends on the stocking den sity. At a low stocking density (10–45 fish/m2), spatial differentiation is established by the beginning of the second day after the transfer of the fish to new conditions; at a high stocking density (182 fish/m2), it is estab lished approximately by the seventh day. Following the establishment of the (secondary) spatial groups, aggressive acts are registered mainly between the individuals from the same spatial group. A role of aggressive behavior in intrapopulation differentiation of brown trout is discussed. DOI: 10.1134/S0032945214020064 Keywords: Black Sea brown trout Salmo trutta labrax, salmonid fishes (Salmonidae), behavior, differentia tion, phenotypic groups, aggression
As is known, intrapopulation spatial differentiation into the groups characterized by different probabilities of the appearance of anadromous or resident life strat egies is usual for salmonid fishes (Salmonidae). This differentiation evolves under the effect of development of juveniles at restricted environmental resources, such as food and territory (available demersal habitats) (Pavlov and Savvaitova, 2008; Pavlov et al., 2010a, 2010b). The investigations of the mechanisms of smol tification and differentiation of juvenile Atlantic salmon Salmo salar, brown trout S. trutta, coho salmon Oncorhynchus kisutch, sockeye salmon O. nerka, and mikizha Parasalmo mykiss into migrants and residents have been conducted over many years (Thorpe, 1977; Thorpe et al., 1989; Metcalfe et al., 1992; Kirillov et al., 2007; Pavlov et al., 2008a, 2008b). The main attention has been directed to physiological and ecological mechanisms, but a role of behavioral mechanisms of differentiation of the population into the groups with different life strategies is studied at a lower degree. The investigation of such behavioral mechanism as aggressive behavior is conducted during the period of smoltification (Faush, 1984; Pavlov et al., 2008b). In particular, mainly the juveniles of Atlantic salmon displaced by the competitors into the water mass are subjected to smoltification (Pavlov et al., 2008b). In addition, ecological mechanisms of differentiation of the fishes at the age of 0+ and their rheoreaction are studied (Zorbidi, 1998; Zorbidi and
Polyntsev, 2000; Kirillova and Kirillov, 2007; Kirillova, 2008; Pavlov et al., 2010b). Based on our previous investigations (Pavlov et al., 2010a), the differentiation into two spatial groups (demersal and pelagic) is observed in hatcheryreared Black Sea brown trout Salmo trutta labrax during the first year of its life. A probability of the transition to a certain life strategy is connected with different possi bilities of access of the fish to food resources and avail able sites at the bottom. A probability of the formation of a resident life strategy is larger in the individuals, which have an access to food resources and sites at the bottom, and a probability of the appearance of anadromous life strategy is larger in pelagic individuals characterized by restricted food resources and restricted access to the bottom (Pavlov et al., 2010a, 2012). This behavioral differentiation is registered in the hatcheryreared fishes at the age of 5.5–6.0 months, i.e., seven months before the appearance of visual charac teristics of smoltification. The role of aggressive behavior in the intrapopulation differentiation of the fishes at this age is not studied. The goal of this study is the experimental investiga tion of aggressive behavior as a possible mechanism of spatial differentiation in juvenile Black Sea brown trout. The juveniles used in this study represent the third generation of a progeny obtained from wild spawners. During the culture of the fish at the hatch ery, genetic changes of the population are minimal,
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and a high level of genetic variation remains (Kholod et al., 2004). Therefore, the results of this study can reflect the situation usual for natural populations of the brown trout. MATERIALS AND METHODS The investigations were conducted from July to August 2009 and from April to May 2010 at the Adler trout hatchery (northern Caucasus). After hatching (in late March and early April), the larvae and juve niles of Black Sea brown trout were kept in the tanks (7.0 × 0.55 m, water level up to 0.5 m) at stocking den sity of 80000–90000 fish/m2 (15000–17000 fish/m3). Artesian water supply with water renewal of 0.5 h and a narrow temperature range (11–12°С) were used at the hatchery. The juveniles at the age of 2 or 3 weeks were fed dry pellets by hand from 10 to 15 times a day; the juveniles at the age of 3 months and older were fed from 7 to 9 times a day. The pellets sank for 15–30 s and remained on the bottom of the tanks for at least 1 h. The juveniles of the two age groups were investi gated. These groups were as follows: the fishes at the age of 2–3 weeks after hatching (onset of their spatial differentiation was registered by this age) and the fishes at the age between 5.5 and 6.0 months. Standard length (from the snout origin to the end of scale cover, SL) reached 26–35 and 32–69 mm, respectively. To study the dynamics of the formation of spatial groups and a role of aggressive behavior in the spatial differentiation of the fish, the individuals of a primary group (demersal or pelagic) were transferred into the cages or aquariums. In this paper, the primary group means the group of individuals that was formed before the start of the experiment. In addition to the pattern of spatial distribution, the individuals of the primary groups differed in coloration of the body (the bodies of demersal fishes were lighter due to light bottoms of the tanks) and startle response (demersal individuals were less frightened). Followed by the transfer of the fish to the experimental cages or aquariums, a new spatial differentiation was registered both in primary demer sal and primary pelagic individuals, and secondary spatial groups appeared. The following designations were used for the latter groups. Secondary pelagic group (SPG): individuals that spent 0–33.3% of the observation time at the bottom (and more than 66.7% of the observation time in the water mass). Secondary undefined group (SUG): individuals that spent 33.3– 66.7% of the observation time at the bottom. Second ary demersal group (SDG): individuals that spent 66.7–100% of the observation time at the bottom. The experiments were conducted on the fishes of the primary demersal and primary pelagic groups at the same time, and the pairs of similar aquariums or cages were used. The fishes from the primary demersal and primary pelagic groups were kept separately in each pair of aquariums or cages. The juveniles at the age of 2–3 weeks were kept in three pairs of experi JOURNAL OF ICHTHYOLOGY
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mental aquariums (12 × 20, 12 × 20, and 34 × 20 cm; water level 15 cm), and the numbers of fishes from the primary groups were 10, 15, and 40 fishes. The stock ing densities were 417, 625, and 588 fish/m2. The juve niles at the age between 5.5 and 6.0 months were kept in five pairs of the cages installed in the tanks. The bot tom sizes of the cages were as follows: 90 × 55 cm (the first and second pairs) and 40 × 55 cm (the third, fourth, and fifth pairs). The water level in the cages reached 50 cm. Five individuals were kept in each cage of the first and second pairs of the cages, and 5, 10, and 40 individuals were kept in each cage of other three pairs of the cages, respectively. Thus, the behavior was investigated at four stocking densities of the brown trout: 10, 23, 45, and 182 fish/m2 (or 20, 45, 91, and 364 fish/m3). During the experiments, water tempera ture, water current speed, and feeding regime were similar to those in the tanks of the hatchery. In total, 130 individuals of brown trout at the age between 2 and 3 weeks and 130 individuals at the age between 5.5 and 6.0 months were used for the experiments. The fishes subsequently used in the experiments were caught with a hand net from the water mass (pri mary pelagic group) and from the bottom (primary demersal group) of the tanks. The behavior and distri bution of the fishes in the experimental groups were registered on the following day after the transfer of the fish, and the observations continued for 6 days (for the fish at the age 2–3 weeks) or 10–13 days (for the fish at the age 5.5–6.0 months). The behavior was regis tered using daily videotaping for 10–20 minutes each. The videotaping was conducted approximately at noon followed by at least 1 h after feeding of the fish at illumination between 3000 and 7000 lx. The video camera captured the image of the whole cage or aquar ium with all fishes inside. Total duration of the video tapes reached 30 h. Fish behavior was analyzed for each individual based on the videotapes. On the first frame, all fishes from the cage were numbered, and the positions of each fish were followed from the whole videotape. The numbers of observations were equal to the number of individuals in the cage. The following parameters were registered every second: position of the fish (in the water mass or at the bottom, i.e., in the contact with the bottom of the cage), presence or absence of aggres sion acts (attack, push, or chase), and their direction 1
(offensive or attacked individuals) . Based on these data, the following indices were calculated: average density of the fish at the bottom during the observation (for 10–20 min), fish/m2; aggression (a ratio between all aggression acts and number of fishes in the cage for observation period), act/(fish/min); time that individ ual spent at the bottom during the observation, % of 1 In
the calculations, chasing events with a duration exceeding 1 s were regarded as single aggressive acts.
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Density, fish/m2
60 50 40 30 20 10 0
1
2
3
4
5 6 7 8 Time, days
9 10 11 12 13
Fig. 1. Dynamics of the density of juvenile Black Sea brown trout Salmo trutta labrax at the bottom of the cage at a stocking density of 182 fish/m2: (–䊊–) primary pelagic group; (–䊉–) primary demersal group.
total observation time; and aggression direction (num bers of offensive and attacked individuals). Aggression of the fishes increased during the exper iments. Therefore, the following equations were used for correct comparison of aggression between the indi viduals at different stocking densities during the entire experiment: ai bi Σ Σ ai + bi ai + bi Y a = , Y b = , n n where Ya and Yb are normalized aggression of the fishes from the primary pelagic and primary demersal groups, respectively; ai and bi are aggression of the fishes from the primary pelagic and primary demersal groups during the day i, act/(fish/min); i is day num ber after the transfer of the fish; and n is number of components. Based on our criterion, the hierarchy established when the stability of fish density at the bottom was maintained for 3 days (based on Student’s ttest for fractions). Statistical treatment of the data was conducted according to Lakin (1990). RESULTS Features of Aggressive Behavior in Juvenile Brown Trout of Different Age A part of brown trout juveniles appears in the water mass for the first time at the age between 2 and 3 weeks. Followed by the transfer to the aquariums, only 20% of the fishes collected in the water mass and 60% of the fishes collected at the bottom of the tank choose the sites at the bottom of the aquarium, and aggression level is minimal reaching 0.026 act/(fish/min). Terri torial behavior and aggression are registered only in single individuals.
By the age 5.5–6.0 months, the juveniles from the tanks of the hatchery are separated into the spatial groups (demersal and pelagic), and this separation is connected with the appearance of territorial behav ior. Just after the transfer to the cage, the fishes from both groups (primary demersal and primary pelagic) stay at the bottom, where they spend almost all their time (94–100%). Aggression of the fish reaches 0.45 act/(fish/min). The features of aggressive behav ior as a mechanism of spatial differentiation of brown trout at this age are described below. Formation of spatial distribution. Based on the dynamics of fish density at the bottom of the cage, two steps of the formation of the secondary demersal group (SDG) characterized by unstable (variable) and stable densities are revealed. At the first step, the fish density is significantly different in various days of the experi ment, and this density is larger in the fishes from the primary demersal group than in the fishes from the primary pelagic group. At the second step (of the sta ble density), the number of fishes at the bottom does not differ in various days, and this number is similar in the representatives of both primary groups. The dura tion of each step depends on the stocking density of the fish. At low and middle stocking densities (10, 23, and 45 fish/m2), the duration of the step of unstable den sity is between 1 and 2 days. During this step, the den sity at the bottom reaches 6, 4, and 9 fish/m2 in pri mary demersal fishes, respectively, and 3, 2, and 2 fish/m2 in primary pelagic fishes, respectively. Within 2 or 3 days after the start of the experiment, the step of the stable density is registered. During this step, the relationship between the fish density at the bottom (у) and duration of the experiment (х, days) is approxi mated by the following equations. The fishes from the primary pelagic group at the stocking densities of 10, 23, and 45 fish/m2: у = –0.19х + 5.26, у = 0.49х + 15.0, and у = –0.68х + 9.49, respectively. The fishes from the primary demersal group at the same stocking densities: у = ⎯0.24х + 7.41, у = –0.17х + 12.4, and у = 0.99х + 4.70, respectively. As is shown from the regres sion coefficients, the fish density at the bottom is com paratively stable over the experiment. At the highest stocking density (182 fish/m2), the number of fishes (from both primary groups) at the bottom changes during 4, 5, or 6 days, and this number becomes stable only on the fifth, sixth, or seventh day, indicating onset of the second (stable) step of the for mation of the SDG (Fig. 1). Aggression. Aggression (on average) of the primary pelagic fishes is larger than that of the primary demer sal individuals (Table 1). Based on the regression anal ysis, aggression of the representatives of the experi mental groups depends on the stocking density, aver age time that the fishes spend at the bottom, and duration of their life in new conditions. The regression equations are as follows: all investigated individuals, Y = ⎯0.000023t2 + 0.002t + 0.0002b2 – 0.0004c – 0.01m + JOURNAL OF ICHTHYOLOGY
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Table 1. Aggression (act/(fish/min)) of juvenile Black Sea brown trout Salmo trutta labrax from the primary pelagic and primary demersal groups at different stocking densities during the experiment Stocking density, fish/m2
Time, days 1
2
3
4
5
6
7
8
9
10
11
12
13
10
0.17 0.06
0.13 0.00
0.39 0.20
0.21 0.01
0.72 0.09
0.13 0.10
0.44 0.15
0.06 0.12
0.25 0.03
0.72 0.00
0.24 0.62
0.93 0.24
0.35 0.08
23
– 0.05
0.12 0.03
0.14 0.15
0.19 0.1
0.25 0.02
0.19 0.01
0.08 0.52
0.04 0.06
0.21 0.22
0.08 0.16
0.16 0.74
0.39 0.15
0.09 0.75
45
0.01 0.02
0.23 0.49
0.23 0.49
1.04 0.29
0.7 0.03
0.91 0.16
0.08 0
0.08 0.54
0.2 0.48
0.07 0.25
0.03 –
0.79 –
4.8 –
182
0.03 0.06
0.25 0.00
0.21 0.03
0.22 0.35
0.16 0.15
0.26 0.50
0.07 0.06
0.23 0.13
0.26 0.17
0.57 0.07
– 0.16
– 0.38
– 0.12
Above the line, primary pelagic group; below the line, primary demersal group; (–) absence of data.
0.09; fishes from the primary pelagic group, Y = ⎯0.000022t2 + 0.002t + 0.0002b + 0.0007c2 – 0.0021c + 0.13; and fishes from the primary demersal group, Y = –0.000022t2 + 0.002t + 0.003b – 0.0002c2 + 0.05, where Y is aggression of the experimental group, act/(fish/min); t is average time that individuals spend at the bottom, %; b is number of days after the transfer of the fish into new conditions; с is stocking density, fish/m2; and m is belonging to a primary group (1, pelagic; 2, demersal). All coefficients of the equa tions are significant (р < 0.001). Despite the established spatial differentiation of the fish, aggression of the individuals from both pri mary groups increases during the experiment (Fig. 2). Based on the values of regression coefficients, aggres sion in the primary demersal individuals increases slightly rapidly than that in the primary pelagic fishes. Aggression of the representatives of both primary groups depends significantly on the stocking density, but the relationships are different (Fig. 3). In the pri mary pelagic fishes, aggression is larger at low and maximum stocking densities than at middle stocking densities. In primary demersal fishes, the inverse situ ation is registered: aggression is the largest at middle stocking densities, and it is lower at low and maximum stocking densities. At middle stocking densities, aggression values for the fishes from both primary groups are not significantly different. Relationship between aggression and time of stay at the bottom. Different individuals are characterized by variable aggression during the experiment. In the most aggressive fishes, the time of their stay at the bottom and in the water mass is approximately equal (Fig. 4). Minimum aggression is registered in the individuals that spend all the time in the water mass and do not compete with other fishes for the sites at the bottom or in the individuals that stay all the time at certain sites of the bottom and do not participate in the competi tion. This relationship between a degree of aggression JOURNAL OF ICHTHYOLOGY
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and spatial choice is observed both in the primary pelagic and primary demersal individuals at all stock ing densities used in the experiments. Direction of aggression. After the transfer of the fish into the cages, a new spatial differentiation estab lishes independently on the initial belonging of the fish to a demersal or pelagic group, and secondary spatial groups are formed. In the representatives of both sec ondary groups, a certain pattern of the choice of the object for aggression is registered (Table 2). The observation of the direction of aggression (i.e., offensive or attacked individuals) shows that the majority of aggressive acts occur between the individ uals from the same secondary group, with the exclu sion of the SUG formed from the primary pelagic fishes, in all variants of the experiment (Table 2: all stocking densities). The analysis of the data for differ ent stocking densities shows that the individuals from the SPG attack mainly pelagic fishes (maximum pro portion of the attacks: six of eight cases), sometimes they attack the fishes from the SUG (one case, at a stocking density of 10 fish/m2, primary pelagic group), or they are do participate in the competition (one case, at a stocking density of 23 fish/m2, primary pelagic group). The individuals from the SUG (characterized by uncertain spatial differentiation) attack the fishes from the same group (four of eight cases), from the SDG (three cases), and from the SPG (one case). The individuals from the SDG attack mainly the fishes from the same group (at a stocking density of 10–45 fish/m2) or exclusively the competitors from the SPG or SUG (at a stocking density of 182 fish/m2). DISCUSSION Spatial differentiation of the Black Sea brown trout during half of the first year of its life is observed twice. The first differentiation is registered at the age between 2 and 3 weeks, and the majority of individuals (80% of
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0.4
0.3
0.2
Aggression, act/(fish/min)
0.1
0
1
2
3
4
5
8
9 10 11 12 13
6 7 8 Time, days
9 10 11 12 13
6
7
0.6 (b) 0.5
0.4
0.3
0.2
0.1
0
1
2
3
4
5
Fig. 2. Aggression dynamics of juvenile Black Sea brown trout Salmo trutta labrax from two groups at different stocking densities: (a) primary pelagic group (on average, у = 0.0121х + 0.1972, R2 = 0.0729); (b) primary demersal group (on average, у = 0.0193х + 0.0696, R2 = 0.4182); (–) 10, (⋅⋅⋅⋅) 23, () 45, (–⋅⋅–) 182 fish/m2, (—), on average, all densities.
primary pelagic fishes and 40% of primary demersal fishes) do not stay at the bottom sites even if these sites are free. Thus, the territorial behavior is not expressed at this age. In natural environment, emergence of salmonid larvae from the ground is observed; the swim bladder is filled by air; and initial distribution of larvae is associated with their rise into the water mass (Pavlov et al., 2010b). Temporal occurrence in the pelagic environment is usual for all larvae at a certain ontoge netic step, but onset of this step is variable in different larvae. At the hatchery, a temporal rise of the larvae into the water mass is also observed, but this rise is not
accompanied by their spatial distribution, and it does not lead to subsequent intrapopulation differentiation. In natural conditions (after initial distribution), the juveniles transit to the territorial mode of life accom panied by increasing aggression (Thorpe, 1977; Faush, 1984; Metcalfe et al., 1992). Strong individuals occupy the most suitable sites at the bottom, and weak individuals, which are unable to defend suitable areas at the bottom, move downstream and search for avail able spaces. As a result, secondary spatial distribution is observed, and the range of the generation becomes wider. At hatchery conditions, available sites at the JOURNAL OF ICHTHYOLOGY
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0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 10
23
45
182
Fig. 3. Relationship between normalized aggression (Yaxis) and stocking density (Xaxis) in juvenile Black Sea brown trout Salmo trutta labrax from the ( ) primary pelagic and ( ) primary demersal groups.
0.5
0.4
0.3
0.2
0.1
0
20
60
40
80
100
Fig. 4. Relationship between individual aggression (Yaxis, act/min) and time spent at the bottom (Xaxis, %) in juvenile Black Sea brown trout Salmo trutta labrax from the primary pelagic and primary demersal groups (on average, at all stocking densities over the entire period of the experiments); see designations in Fig. 1.
bottom of the tank are restricted, and aggressive behavior represents a mechanism of the displacement of a part of individuals into the water mass. Therefore, a large number of fishes are distributed in the water mass by the age between 5.5 and 6.0 months. Without a possibility to escape from the tank, these fishes should be adapted to pelagic life. However, a pelagic mode of life is not usual for juvenile brown trout of this age, which is connected with their growth rate, feeding (Pavlov et al., 2012), and behavior. According to Pav lov et al. (2010a), during the transition of the young to a migratory state, the behavior of pelagic fishes is sim ilar to that in smolts (anadromous life strategy), and the behavior of demersal fishes is similar to that in the JOURNAL OF ICHTHYOLOGY
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representatives of a resident form (resident life strat egy). Followed by the transfer of the fish into the cage (during the first day), their density at the bottom is larger in the primary demersal group than in the pri mary pelagic group. Thus, the experience accumu lated during ontogeny, as well as inherent program (stereotype) of territorial behavior, could have an effect on spatial differentiation of the fish. Then the number of the fishes at the bottom becomes stable, and the differences between the primary demersal and pri mary pelagic individuals disappear, i.e., the role of accumulated experience is minimal, and the density of the fish at the bottom is determined by inherent
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Table 2. Direction of aggression (%) in juvenile Black Sea brown trout Salmo trutta labrax from the primary pelagic and primary demersal groups at different stocking densities Primary pelagic group Offensive fishes
Y100, act/(fish/min)
Primary demersal group
attacked fishes SDG
SUG
SDG SUG SPG
0.0320 0.0610 0.1100
67 49 16
25 38 25
SDG SUG SPG
0.0060 0.0150 0.0280
44 41 28
41 45 40
SDG SUG SPG
0.0120 0.0100 0
89 20 0
10 80 0
SDG SUG SPG
0.0080 0.0060 0.0330
70 52 3
26 16 14
SDG SUG SPG
0.0003 0.0130 0.0210
0 86 4
0 0 4
SPG
Y100, act/(fish/min)
All stocking densities 8 0.027 14 0.092 59 0.075 Stocking density 10 fish/m2 15 0.009 14 0.021 32 0.008 Stocking density 23 fish/m2 2 0.006 0 0.009 0 0.018 Stocking density 45 fish/m2 4 0.001 32 0.038 83 0.029 Stocking density 182 fish/m2 100 0.002 14 0.002 92 0.013
attacked fishes SDG
SUG
SPG
49 16 19
15 62 11
36 22 70
49 22 36
14 49 6
37 29 57
66 38 30
4 0 19
30 62 51
39 4 10
28 90 13
33 6 77
0 0 3
61 89 2
39 11 95
(Y100) aggression of the secondary group accepted as 100%; (SDG, SUG, and SPG) secondary demersal, secondary undefined, and secondary pelagic groups, respectively.
behavior of individuals. The analysis of dynamics of fish density at the bottom for 10–13 days shows that the spatial differentiation of the fishes is established already on the second day at small and middle stocking densities (10, 23, and 45 fish/m2). At a high stocking density (182 fish/m2), more time is required for the stable spatial differentiation: the number of secondary demersal individuals becomes constant only by the seventh day. It is connected, most likely, with a large number of competitors for the space at the bottom.
ipate in the active struggle. The latter individuals, most likely, protect their sites using the acts of demonstra tions (which are not taken into consideration in this study), and the number of direct aggression acts decreases. This feature is registered in the individuals from both primary demersal and primary pelagic groups.
Thus, the spatial differentiation establishes com paratively rapidly. It could be suggested that aggression becomes stable by the same time. Nevertheless, aggression increases in all investigated fishes during the experiment (for 10–13 days), and aggression is not equal among the individuals from different secondary groups. The fishes from the secondary undefined group (SUG) are most aggressive. At the same time, the fishes that continuously occur in the water mass (SPG) do not compete for the space at the bottom, and the fishes that stay at the bottom (SDG) already “have proved their superiority” and also do not partic
Step 1. Fish behavior is directed mainly to search ing for and occupation of a space at the bottom of the cage. Spatial distribution of the fish is not stable. Pre vious experience has an impact on their behavior. During the first day of the experiment, the number of fishes at the bottom of the cage from the primary de mersal group is larger than that from the primary pelagic group. Some individuals from the latter group are displaced from the bottom by the fishes from the former group. The duration of the step depends on the stocking density, reaching 1 or 2 days at lower densities and a higher number of days at higher densities.
Thus, two steps of the spatial differentiation of brown trout in the new conditions can be defined in this study.
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Step 2. Previous experience of the fishes is not sig nificantly important for their spatial distribution, and the density of the fishes at the bottom (on average) is equal for the representatives from the primary demer sal and primary pelagic groups. Spatial distribution of the fishes becomes stable, and (on average) aggression increases. At the same time, the direction of aggressive acts has changed: the number of interferences between the representatives of the secondary spatial groups decreases, and the proportion of interactions between the individuals within each secondary group increases. The possible explanations of aggression prevalence between the individuals from a secondary spatial group are as follows. At a high stocking density in the cage (182 fish/m2), more than 90% of aggressive acts are registered within the group of the secondary pelagic fishes, and, most likely, the demersal and pelagic fishes do not represent a single hierarchical structure. The appearance of a separate (intrinsic) hierarchical struc ture in hatcheryreared salmonid fishes forced to occur in pelagic environment is described in several papers (Fenderson et al., 1968; Moyle, 1969; Noakes and Leatherland, 1977; Metcalfe et al., 1989). Forma tion of two independent hierarchical groups was previ ously registered in Atlantic salmon (Pavlov et al., 2008b). The interruption of aggressive relationships between the demersal and pelagic individuals is observed by the beginning of smoltification in pelagic fishes, i.e., during their transition to anadromous life strategy. As is shown in Black Sea brown trout (Pavlov et al., 2010a), a probability of the transition to anadro mous life strategy reaches a high level in the pelagic individuals at the age between 5.5 and 6.0 months. Thus, aggressive interactions between the individuals that have chosen different life strategies (anadromous or resident) become less frequent both in the Black Sea brown trout and Atlantic salmon. A mechanism of the substantial decrease of aggressive interactions between the individuals from different secondary groups can be connected with their spatial distribution. Both in demersal and pelagic fish, aggressive behavior is regis tered when the individual reaches an “aggression dis tance.” The individuals from the secondary demersal group are distributed mainly at the bottom, and, there fore, they contact with the fishes from the same group more frequently. Similar to this situation, the individ uals from the water mass contact mainly with their pelagic counterparts. CONCLUSIONS (1) Aggressive behavior of brown trout connected with the territorial mode of life represents a mecha nism of differentiation of the juveniles into spatial groups in the conditions of restricted space. (2) The duration of the appearance of spatial differ entiation depends on the stocking density of the fish: at low stocking densities (10–45 fish/m2), the spatial differentiation establishes by the second day after the JOURNAL OF ICHTHYOLOGY
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transfer of the fish to new conditions; and at a high stocking density (182 fish/m2), it establishes approxi mately by the seventh day. (3) During the formation of the spatial differentia tion, the individuals that have not chosen the site for subsequent life (at the bottom or in the water mass) are more aggressive. (4) Followed by the appearance of the (secondary) spatial groups, the main proportion of aggressive acts are registered between the individuals within each group. In addition, a high stocking density leads to abrupt decrease of aggressive interactions between the individuals from different spatial groups. ACKNOWLEDGMENTS This work was supported by the Russian Founda tion for Basic Research (projects nos. 110400686a and 120431103mol_a), the Program of the Presid ium of the Russian Academy of Sciences “Live Nature” of the Federal Agency for Science and Inno vations (State contracts nos. 02.740.11.0280, 14.740.11.0165, and 16.740.11.0174), and the Pro gram of the President of the Russian Federation “Leading Scientific Schools” (no. NSh719.2012.4). REFERENCES Faush, K.D., Profitable stream positions for salmonids; relating specific growth rate to net energy gain, Can. J. Zool., 1984, vol. 62, pp. 441–451. Fenderson, O.C., Everhart, W.H., and Muth, K.M., Com parative agonistic and feeding behavior of hatcheryreared and wild salmon in aquaria, J. Fish. Res. Board Can., 1968, vol. 25, pp. 1–14. Kholod, O.N., Makhrov, A.A., Kulyan, S.A., et al., Genetic features of the Black Sea brown trout (Salmo trutta labrax) broodstocks from the hatcheries of Russian Federation, Tsi tologiya, 2004, vol. 46, no. 10, pp. 875–876. Kirillov, P.I., Kirillova, E.A., and Pavlov, D.S., Some fea tures of biology of early young of mikizha Parasalmo mykiss in the Utkholok River (northwestern Kamchatka), Mater. VIII Mezhdunar. nauch. konf. “Sokhranenie biorazno obraziya Kamchatki i prilegayushchikh morei” (Proc. VIII Int. Conf. “Conservation of Biodiversity of Resources of Kamchatka and Adjacent Seas”), PetropavlovskKam chatsky, 2007, pp. 51–55. Kirillova, E.A., Some features of biology of coho salmon Oncorhynchus kisutch at the first year of life in the Utkholok and Kalkaveem rivers (northwestern Kamchatka), Chteniya Pamyati V.Ya. Levanidova, 2008, no. 4, pp. 292–301. Kirillova, E.A. and Kirillov, P.I., Feeding of the young of coho salmon and mikizha during downstream migration, Tez. IV Vseros. konf. po povedeniyu zhivotnykh (IV All Union Conf. on Fish Behavior Abstracts of Papers), Mos cow, 2007, pp. 268–269. Lakin, G.F., Biometriya (Biometrics), Moscow: Vysshaya Shkola, 1990. Metcalfe, N.B., Huntingford, F.A., Graham, W.D., and Thorpe, J.E., Early social status and the development of
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Translated by D.A. Pavlov
JOURNAL OF ICHTHYOLOGY
Vol. 54
No. 2
2014
