ISSN 0032�9452, Journal of Ichthyology, 2010, Vol. 50, No. 6, pp. 483–488. © Pleiades Publishing, Ltd., 2010.Original Russian Text © D.S. Pavlov, V.Yu. Ponomareva, A.E. Veselov, V.V. Kostin, 2010, published in Voprosy Ikhtiologii, 2010, Vol. 50, No. 4, pp. 548–553.

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The juveniles of samonids (Salmonidae), similarlyto some other fishes, are differentiated into groups bymorphological and physiologo�biochemical parame�ters (Thorpe, 1977; Metcalfe et al., 1992; Pavlov et al.,2007b; etc.). Such intrapopulational heterogeneity isformed under the influence of environmental condi�tions and occurs even in the progeny of one pair ofspawners (Pavlov et al., 2007a). Its adaptive signifi�cance is the enhancement of survival of juveniles.

Previously (Pavlov et al., 2007b, 2008), it wasshown for the Atlantic salmon Salmo salar from theVarzuga River that, in the process of primary distribu�tion from the mainstream spawning grounds, theunderyearlings occupy the parts of the river differing inhydrology. One part of fish is distributed in the coastalareas of the cataract reaches of the Varzuga andanother part is distributed in tributaries. With refer�ence to the Arenga tributary, it was found that theunderyearlings from the tributary in comparison withindividuals from the coastal zone had, by some param�eters, an increased level of energy metabolism andlater on in increased level of lipid metabolism, as wellas a higher growth rate. The revealed differences indi�cate the presence of phenotypic groups in underyear�lings of the Atlantic salmon (Pavlov et al., 2007b,2008, 2009). However, behavioral mechanisms of theirformation remained unknown.

As the habitats of fry from the aforementionedgroups differ, first of all, in flow rate (it is higher in thetributary) it was assumed that the rheoreaction of fishshould have a direct relation to their differentiation.

The present study is aimed at investigation of therheoreaction as a behavioral mechanism of formationof phenotypic groups of underyearlings of the Atlanticsalmon. The type of rheoraction, rheopreferendum,and critical current velocity in fry of Atlantic salmondistributing from their redds are studied.

MATERIAL AND METHODS

The subject of the present investigation was juve�niles of the Atlantic salmon at the age 0+ of two phe�notypic groups, from the coastal zone and from tribu�taries, in the period of its primary distribution fromredds. The fish were caught from the coastal zone atthe Varzuga cataract (the coastal group), at the dis�tance up to 2 m from the edge of water, and in theArenga tributary, up to 15 m upstream from themouth (the group from the tributary). The conditionsin these biotopes were described previously (Pavlovet al., 2009). The density of fry in the Varzuga at thecatching site was 5–12 and that in the Arenga was 1–7 specimens/m2. The fish were captured by two elec�trofishing passes of FA�2 on July 24–27, 2008.

Rheoreaction as a Mechanism of Formation of Phenotypic Groups of Underyearlings of the Atlantic Salmon Salmo salar

D. S. Pavlova, V. Yu. Ponomarevaa, A. E. Veselovb, and V. V. Kostina

a Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow 119071 ae�mail: Pavlov@sevin.ru

b Institute of Biology, Karelian Research Center, Russian Academy of Sciences,ul. Pushkinskaya 11, Petrozavodsk, 185910 Russia

Received February 9, 2010

Abstract—Experimental investigation on rheoreaction as a behavioral mechanism in the formation of phe�notypic groups of underyearlings of the Atlantic salmon Salmo salar is performed. Juveniles of the Atlanticsalmon are investigated at the age 0+ from the coastal group and from the tributary group in the period of itsprimary distribution from redds. The underyearlings from the tributary group differ from the coastal fish inincreased critical current velocity, the fact that among them the most portion of individuals have a positivetype of rheoreacrtion, and the fact that they prefer currents more often. The behavioral mechanism of spatialseparation of the spreading juveniles at confluence of two currents is revealed: stronger individuals with thepositive type of rheoreaction and the expressed rheopreferendum mainly move against the flow at a higherspeed and manage to get into a tributary. The weaker fish with static and negative dynamic types of rheoreac�tion, having no expressed rheopreferendum, prefer the flow with lower current rate and turn out to be in thecoastal zone of the mainstream.

DOI: 10.1134/S003294521006007X

Key words: Atlantic salmon, type of rheoreaction, underyearlings, spatial separation, phenotypic groups,rheopreferendum, critical current velocity.

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After 24 hours acclimation in mainstream cages,the following parameters of rheoreaction were deter�mined in the experimental fish: the type of rheoreac�tion, rheopreferendum, and critical current velocity.

The type of rheoreaction shows the direction ofmovement of fish in the water flow in relation toimmovable landmarks. The following types of rheore�action were discerned: the positive dynamic type ofrheoreaction (PDTR)—the fish move upstream inrelation to immovable landmarks; the static type ofrheoreaction (STR)—the fish almost do not move inrelation to immovable landmarks; and the negativedynamic type of rheoreaction (NDTR)—the fishmove downstream in relation to immovable land�marks.

The type of rheoreaction was determined in theinstallation “fishway” analogous to one used previ�ously (Hensleigh and Hendry, 1998; Pavlov et al.,2010). The installation is a tray 165 × 20 cm in size,separated by transverse walls into 11 sections. Thewidth of an opening from section to section is approx�imately 5 cm. The flow rate in openings between sec�tions exceeded the threshold value for the investigatedfish and was 3 cm/s. The experiments were made ongroups by 15–20 fish. Each group was placed into thecentral start section (no. 6) with a protective net onboth sides. The fish were acclimated to the conditionsof the experiment during 20 min in presence of theflow in the installation. Then the nets were removed.At the first and the 20th minute of the experiment, thenumber of individuals in each section of the fishwaywas recorded. The individuals moved upstream againstthe flow to sections 1–5 were recorded as demon�strated PDTR, the fish remaining in the initial sectionno. 6 were recorded as STR, and the individuals moveddownstream to sections 7–11 were recorded asNDTR. After the experiment, the fry with differenttype of rheoreaction were placed into different trapsfor further investigation of their rheopreferendum.

The rheopreferendum of fish was determined indi�vidually in a hydrodynamic tray 75 × 20 cm in size withtwo channels. In one of the channels (20 × 10 cm) theflow rate was 10 cm/s; in another (similar) channelthere was no flow (Pavlov et al., 2007a). In the down�stream part of the installation, there was the start sec�tion occupying the whole width of the tray. The lengthof the working part of the tray (from the start section tochannels) was 40 cm.

A fry was placed in a start section of the installationwith a protective net preventing its leaving. During3 min it was acclimated to the experimental condi�tions then the net was removed. The experiment con�tinued either until the first arrival of the fish to one ofthe channels or not longer than 5 min from themoment of removing the net. One of two possibleresults of the experiment was recorded: a choicebetween the channel with flow and without flow madeby the fry, or its refusal to choose (during the experi�ment the fish did not swim to neither of the channels).

In calculation of the value of rheopreferendum (theportion of individuals that chose the channel withflow) the fish which made no choice were notincluded. After determination of rheopreferendum,the fish were used for estimation of critical currentvelocity.

The critical current velocity for fish is the mini�mum value of the flow rate at which the fish cannotresist the current and it is taken by the flow. This flowrate was measured individually in a modified hydrody�namic installation for determination of critical currentvelocity in fish (Pavlov, 1979). The working cell is a 1 mlong glass tube, 20 mm in diameter. To decrease turbu�lence, additional nets were placed in front of the work�ing cell.

The fish was placed to the working cell previouslyfilled with water. After 1.5–2.0 min of acclimation toconditions of the installation, the flow rate in the tubewas gradually increased to the flow rate level at whichthe fish could not resist the current and were driftedonto the protecting net. The flow rate in the tube wasdetermined by the discharge method (Pavlov et al.,2007a).

After experiments, the standard body length (fromthe snout tip to the end of scale cover, SL) of each fishwas determined.

Altogether, 167 experiments were made on163 salmon fry SL 24–30 mm. Critical current veloci�ties were recorded in 60 experiments, by 30 fry in eachgroup. For determination of the type of rheoreactionby three experiments were made on fish from thecoastal group and tributary group (52 and 51 speci�mens, respectively). Rheopreferendum was investi�gated in 50 experiments on underyearlings from thecoastal zone (50 specimens) and in 51 experiments onunderyearlings from the tributary (51 specimens).

RESULTS

Kind of rheoreaction type. The salmon underyear�lings started movement in the installation from the firstminute of the experiment both to upstream and down�stream sections. To the downstream sections, the juve�niles moved both passively and actively. The fry fromthe tributary were characterized by higher activity andtheir movements were more abrupt in comparisonwith underyearlings from the coastal zone. In 3–5 minafter the beginning of the experiment some fishchanged the direction of movement—they returned tosections where they were previously. Most frequently,the direction was changed in marginal sections as itwas not possible to move in the previous direction.

In the first minute of the experiment, 56% of fishfrom the coastal group remained in the start sectionand 65% of individuals from the tributary group left it(Fig. 1a). The underyearlings from tributaries movedmore frequently and farther against the flow than thejuveniles from the coastal zone; in the first–fifth sec�tions, 42 and 30% of fish ascended, respectively.

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Up to the 20th minute of the experiment, most ofunderyearlings left the start section. The fish from thetributary moved mainly upstream and those from thecoastal zone moved downstream (Fig. 1b). Differencesin the sum distribution of fish from the investigatedgroups by sections of the fishway are significant both atthe first minute and at the 20th minute of the experi�ment (χ2 test, p < 0.001 and p = 0.05, respectively).

The type of rheoreaction was different in the fishfrom the investigated groups (Fig. 2). Most individualsfrom the tributary demonstrated PDTR and the part offry with STR was minimum and differed significantlyfrom the portion of fish both with PDTR and NDTR(Student’s test for the parts, p < 0.001). In the fish fromthe coastal zone, the number of individuals withPDTR was maximum and the minimum was withNDTR. The level of significance of differences ofthese portions was 0.06 by the Student’s test. Insalmon fry from the tributary group, in comparisonwith the coastal group, there were almost twofoldmore individuals with PDTR and fivefold times lessindividuals with STR (Student’s test for parts, p =0.006 and p = 0.002, respectively).

Rheopreferendum. After removal of the protectivenets, some fish immediately moved to one of the chan�nels of the installation; they moved almost withoutdarts against the flow. Other individuals stayed forsome time at the downstream net not reacting to the

removal of the protective net and moved to one of thechannels only to the middle or even to the end of theexperiment. Similarly to the fishway, the fish from thetributary group were more timid, made more abruptand rapid movements than the individuals from thecoastal group.

Some few of the tested fish during 5 min (durationof the experiment) remained in the start section. Theystayed in the flow near the center of the start section,or leaned with their tail against the protective net, orwere pressed to it by the flow.

Most fish from the tributary group (60%) preferredthe flow (Fig. 3). Among them, individuals withPDTR were significantly more numerous than oneswith other rheoreaction type (Student’s test for parts,p < 0.005).

In the underyearlings from the coastal group, therheopreferendum was not expressed: they almostidentically chose the channels with flow or without it.

5

01

No. of section of fishway

15

2

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35

30

10

20

15

1

2

2

1

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sh in

a s

ecti

on,

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imen

s

Fig. 1. Distribution of underyearlings of the Atlanticsalmon Salmo salar from (1) the coastal group and (2) thetributary group by sections of the installation at the (a) firstand the (b) 20th minute of the experiment (103 speci�mens). The arrow shows the flow direction.

30

25

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0

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2

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ber

of fi

sh,

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imen

s

Rheoreaction typePDTR STR NDTR

Fig. 2. The rheoreaction type in underyearlings of theAtlantic salmon Salmo salar from (1) the coastal group and(2) the tributary group (103 specimens). Designations ofrheoreaction types: PDTR—positive dynamic, SRT—static, and NDTR—negative dynamic.

60

50

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Por

tion

of f

ish

th

at c

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eth

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ann

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tributary coastal

PDTR

Fish groups

STR

NDTR

Fig. 3. The rheopreferendum of underyearlings of theAtlantic salmon Salmo salar from the coastal group(43 specimens) and the tributary group (45 specimens).Designations as in Fig. 2.

(a)

(b)

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The ratio of individuals with PDTR and NDTR in frychose the channel with flow was also identical.

Generally, rheopreferendum turned out to be dif�ferent in fish from the investigated groups. Simulta�neously, its dependence on the type of rheorteractionin fish was revealed. This dependence differs on tenfish from the coastal zone and from the tributary. Thegroup, type of rheoreraction, and combination ofthese factors significantly influenced the choice madeby the fish in the installation (two�factor analysis ofvariance, p < 0.001).

Absolute critical current velocity for fry was higherthan in the tributary group, 34.3 ± 12.2 cm/s, than inthe coastal group, 26.2 ± 6.4 cm/s (Fig. 4a). Thelength of fish from the tributary (27.3 ± 0.12 mm) wasgreater than the length of individuals from the coastalzone of the mainstream (26.5 ± 0.09 mm). The relativecritical current velocity (Fig. 4b) in the fish from thetributary group (12.6 ± 4.54 SL/s) also was higher thanthat in fish from the coastal group (9.9 ± 2.39 SL/s).Differences by critical current velocity and bodylength between the groups are significant (Student’stest, p < 0.01).

DISCUSSION

The eggs of salmonids, in particular of the Atlanticsalmon, differ from each other by the size, weight, andvolume of the stock substances (Kazakov, 1982). Later,these initial differences influence the intensity ofgrowth and development of early juveniles, and alsoinfluence the results of primary distribution of under�yearlings of the Atlantic salmon from redds (Veselovand Kalyuzhin, 2001). During distribution from redds,some few salmon fry remain in the central part of theVarzuga mainstream. Mainly, they distribute in itscoastal zone and in the Arenga tributary. The biotopesof tributaries, of the Arenga in particular, differ fromthe coastal biotopes of the Varzuga in richer foodresources for salmons of age 0+ (Shustov, 1983; Bary�shev, 2004). It is important that in the Arenga tributarythe flow rates are higher—0.98 (0.82–1.28) m/s—than in the Varzuga—0.74 (0.70–0.95) m/s (Pavlovet al., 2009). Under different life conditions, the dif�ferences between the fish from the tributary and thecoastal zone of the Varzuga increase. This leads to theformation of two phenotypic groups of the Atlanticsalmon at age 0+ differing in body size and weight, inlevels of energy and lipid metabolism (Pavlov et al.,2007b, 2008). Thus, the principal cause of origin ofphenotypic groups of salmon under the consideredconditions is the spatial separation of distributing juve�niles. This separation is realized due to different rela�tion to flow (rheoreaction type, rheopreferendum) inthe fish with initially different locomotor capacities(the critical current velocity).

For understanding the mechanisms of spatial dis�tribution of fry of the Atlantic salmon, let us considerthe scheme of their primary distribution (Fig. 5). Afterbrief active�passive downstream migration from reddsto the lower boundary of the cataract, the juvenilesbegin actively swimming along the gradient line offlows and depths to the coastal zone of the river. At theconfluence of the Arenga and the Varzuga shown inthe scheme as the area of choice, the fry enter flowswith different intensity. Here, they have to make achoice: either to move against the more rapid flow ofthe Arenga or to move to the coastal zone of the Var�zuga where the flow is weaker. Stronger individualswith a higher probability of manifestation of PDTRmore often chose a strong flow, move to the tributary,and form the tributary spatial group. Weaker fish withSTR and NDTR and not expressed rheopreferendumprefer the coast of the Varzuga mainstream.

It should be stressed that our investigations weremade during the first days of appearance of salmon fryin the tributary. Before this time, all individuals stayedunder hydraulically similar conditions of the Varzugamainstream. Therefore, training little influences thevalue of the investigated parameters of rheoreaction offish. Thus, different attitude to flow (rheoreaction)and different locomotor capacities are related not so

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Fig. 4. (a) Absolute and (b) relative flow rates in underyear�lings of the Atlantic salmon Salmo salar from (1) thecoastal group and (2) the tributary group (60 specimens).

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RHEOREACTION AS A MECHANISM OF FORMATION OF PHENOTYPIC GROUPS 487

much to environmental conditions of fry as to the ini�tial differences of salmon eggs and larvae.

In rheogradient conditions (at confluence of thetributary to the mainstream), these individuals of thesame generation differed by their initial parametersand chose different directions of their movements.Such choice leads to spatial separation of the distrib�uting juveniles and to the life of these fish in differentbiotic and abiotic conditions. This results in the for�mation of phenotypic groups of juveniles. Thus, rheo�reaction (attitude to flow) is a behavioral mechanismof differentiation of juveniles of the Atlantic salmon.There are many sites with similar rheogradient condi�tions both in the Varzuga and in other rivers (Pavlovet al., 2009). Therefore, the possibility of realization ofsuch mechanism of differentiation of juveniles israther frequent.

CONCLUSIONS

(1) The individuals from the investigated groupsdiffer in parameters of rheoreaction. The salmon fryfrom the tributary group, in comparison with the

coastal group, are characterized by a higher criticalcurrent velocity for their rheoreaction, among themthe portion of individuals with the positive rheoreac�tion type is more numerous; they prefer the water flowmore often.

(2) The behavioral mechanism of spatial separationof distributing juveniles of the Atlantic salmon at theconfluence of two flows is revealed: strong individualswith the positive type of rheoreaction and theexpressed rheopreferendum move against the waterflow at a higher speed and get in the tributary. Theweaker fish with static and negative dynamic types ofrheoreaction and not expressed rheopreferendum pre�fer the flow of a lower rate and attain to the coastalzone of the mainstream.

REFERENCES

1. I. A. Baryshev, “Amphibiotic Insects of Rearing Sites ofJuvenile Atlantic Salmon in the Varzuga River Basin,”in Materials of II All�Russia Symposium on Amphibioticand Aquatic Insects (Voronezh, 2004), pp. 7–13.

2. J. E. Hensleigh and A. P. Hendry, “RheotacticResponse of Fry from Beach�Spawning Populations of

Flowdirection

Coastal zon

e

Directionof distribution

of salmon

Spawning grounds

Selectionarea

Flowdirection

Cataract

Tributary

juveniles

Fig. 5. Scheme of primary distribution of juveniles and formation of spatial groups of the Atlantic salmon Salmo salar in the areaof confluence of the Varzuga River and the Arenga River (after Pavlov et al., 2007b).

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