Habitat heterogeneity and fish behavior: Units of heterogeneity as a resource and as a source of information

ISSN 0032�9452, Journal of Ichthyology, 2010, Vol. 50, No. 5, pp. 386–395. © Pleiades Publishing, Ltd., 2010.Original Russian Text © V.N. Mikheev, M.O. Afonina, D.S. Pavlov, 2010, published in Voprosy Ikhtiologii, 2010, Vol. 50, No. 3, pp. 378–387.

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1Habitat heterogeneity is expressed as an uneven spa�tial distribution of resources and conditions. Effects ofheterogeneity are recognized on a broad scale—fromsimple laboratory microcosms with the size of tens ofcentimeters (Ivlev, 1955; Huffaker, 1958) to large�scale ecosystem variations of the size up to hundredkilometers (Wiens et al., 1993; Pinel�Alloul, 1995).Such effects were often taken into account by ecolo�gists, but behavior scientists, especially those who dealwith aquatic animals, and particularly, with fish, paidlittle attention to habitat heterogeneity. Developmentof underwater techniques, SCUBA observations andexperimental methods forced behavioral ecologiststook into consideration small�scale habitat structures

1 The article was translated by the authors.

that modify fish behavior (Pavlov, 1979; Mochek,1987; Hixon and Beets, 1993; Holbrook and Schmitt,2002; Mikheev, 2006).

Behavior is based on mechanisms of decision mak�ing (Stephens and Krebs, 1986; Blumstein andBouskila, 1996) that allow animals choosing suchkinds of activity, which increase their fitness (Milinski,1988; Lima and Dill, 1990). The most sophisticatedtasks of choice are those, which are related with trade�offs between the most important vital processes—feeding and defense from predators. In fish, like inmany other animals, these trade�offs are crucial inearly ontogeny when energy demands are high anddefensive mechanisms are poorly developed. Decisionmaking in juvenile fish is complicated by poor experi�ence, cryptic prey and predators, lack of landmarks

Habitat Heterogeneity and Fish Behavior: Units of Heterogeneity as a Resource and as a Source of Information1

V. N. Mikheev, M. O. Afonina, and D. S. PavlovSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 119071 Russia

e�mail: [email protected] June 16, 2009

Abstract—A review of studies, mainly experimental, on modifications of fish behavior caused by microscalehabitat heterogeneity. Elements or units of heterogeneity influence on decision making in fish either as con�testable physical resources, or as information cues or signals. Habitat heterogeneity arises from abiotic phys�ical objects, aggregations of prey, and grouping fish. Feeding behavior of fish including food search, choice,and consumption are significantly dependent on the structure of heterogeneity of the habitat, where fish areforaging. Depending on the parameters of heterogeneity, prey characteristics and a predator foraging mode,heterogeneous habitats can either facilitate feeding behavior, or makes it more difficult. Habitat heterogeneityplays significant and, as a rule, positive role providing various refuges for fish hiding from predators. Land�marks help fish to find the shortest route to shelters. If a habitat is rather homogeneous or in a novel habitat,which appears to be homogeneous, shoaling of fish makes surroundings of each individual in the school struc�tured providing fish with a substitute of shelters and landmarks. Recent experimental and field results con�vincingly demonstrate that the effects of main biotic and abiotic factors can be significantly modified by thestructure (level of spatial heterogeneity) of habitats. When a habitat is physically structured, tendencies to dis�perse and establish individual territories prevail. In uniform, poorly structured habitats, fish tend to gather inschools or shoals and maintain larger aggregations. Food is considered the major contestable resource, butfish often demonstrate interference competition not for food, but for heterogeneous sites in the habitat, wherethey vigorously fight either for a shelter or just for visually non�uniform area. Visually heterogeneous sites canbe used by fish as a template of a future individual territory, where fish can find not only food but also a refugefrom predators. Fish use individual territories for much longer period than food patches. Just the presence ofeither physical refuge or “social refuge” neutralized the inhibiting effect of kairomons and allowed fish to feedmore intensively despite the potential danger. We suggest that the decision�making was influenced only byavailable information of possibility to use a refuge. Habitat complexity is almost always accompanied by visualand other types of heterogeneity. Adaptive significance of fish attraction to the units of heterogeneity is prob�ably related to the fact that under natural situations vital for fish objects are often tightly coupled with heter�ogeneous sites. Thus, units of habitat heterogeneity can be reliable signals or information cues in uncertain,i.e. changeable and poorly predictable, habitats.

DOI: 10.1134/S0032945210050048

Key words: foraging, defense behavior, territoriality, shoaling, habitat complexity, exploration, aggressiveinteractions.

JOURNAL OF ICHTHYOLOGY Vol. 50 No. 5 2010

HABITAT HETEROGENEITY AND FISH BEHAVIOR 387

and shelters as well as energetically costly locomotion(Leshcheva and Zhuikov, 1989; Eklov and Persson,1996; Bystrom et al., 2004). When spatial distributionof resources and threats is variable, search, explorationand choice of objects should be done quickly and effi�ciently. Hypotheses of behavior optimization(Stephens and Krebs, 1986) are based on premises thatanimals are either sufficiently informed aboutresources and ambient conditions, or quickly and effi�ciently explore changing habitats. Both premises arehardly possible if an animal faces novel surroundings.Actively swimming fish juveniles often occur in novelhabitats, where decision�making is difficult due todeficiency of information (Dill, 1983, 1987).

Studying variability of behavior of juvenile fish, wefound that small�scale habitat heterogeneity, particu�larly visual heterogeneity, substantially influence vari�ous aspects of individual and social behavior (Mikheevand Pavlov, 2004; Mikheev, 2006). Small�scale habitatheterogeneity is usually considered as a factor thatmodifies patterns of prey spatial distribution, influ�ences prey vulnerability and efficiency of refuges.When prey spatial distribution is clumped, fish easierlocate aggregations that lead to higher intensity of for�aging (Ivlev, 1955; Mikheev et al., 1997a). Stream�dwelling fish often maintain stable position at a largeboulder, where they can find a shelter from predators,and a flow�gradient allows fish that hide in low�speedpart of the gradient intercept prey drifting in the fastflow (Fausch, 1984). In aquatic habitats with densevegetation, feeding rate planktivorous fish is lowerthan in open water areas (Crowder and Cooper, 1982;Gotceitas and Colgan, 1990). These examples demon�strate that habitat heterogeneity can operate as a phys�ical factor, which directly influence fish behavioreither facilitating, or inhibiting its activity at themoment. However, recently obtained results (Afoninaet al., 2005; Mikheev and Pavlov, 2005) suggest thathabitat heterogeneity can be considered as an infor�mation resource or signal factor that modifies fishbehavior and influences decision�making. Its effectcan be recognized not immediately, and it lasts evenwhen fish are not in perceptual contact with the sourceof signal.

The aim of the paper is to review and analyze orig�inal and published data on variations of foraging,defense and social behavior of fish under conditions ofsmall�scale habitat heterogeneity that influence phys�ical and information structure of the habitat. Morespecifically we will discuss situations of conflicts ofmotivations, and particularly those, in which fishshould compromise between feeding and anti�preda�tor activities.

MAIN APPROACHES TO STUDY EFFECTSOF THE HABITAT HETEROGENEITY

Modifications of behavior and small�scale spatialdistribution offish, which were related with habitat

heterogeneity, were observed in the field studies (Pav�lov, 1979; Mikheev, 1985; Mochek, 1987; Beukers andJones, 1997). These modifications were resulted frommulti�factorial impacts, and were described mainlyqualitatively that did not allow analysis of factorscaused observed variations. To study effects of separatefactors or combinations that are related with habitatheterogeneity, special laboratory experiments weredone (Mikheev et al., 1996; Afonina, 2002; Mikheev,2006). Large flow�through tanks with size more than20–30 fish body lengths were used in such experi�ments. The experiments were simultaneously carriedout in (1) visually heterogeneous aquaria (contrastedvisual objects on the walls and bottom, shelters on thebottom, areas with imitation of dense vegetation), and(2) control aquaria with relatively homogeneous inte�rior. Similar experimental design was used in experi�ments, where the role of hydraulic heterogeneity infeeding behavior and locomotion of juvenile fish wasstudied (Lupandin et al., 2004; Pavlov et al., 2008).

Clear effects of habitat heterogeneity on fishbehavior can be observed not only in laboratory exper�iments, but also under natural conditions. Howeversuch observations are possible only in rare suitable sit�uations. For example, when we had a possibility per�manently follow a small school of perch, Perca fluvia�tilis, juveniles foraging in a shallow water habitat withscattered patches of dense vegetation, we were able toobtain unbiased estimates of feeding selectivity in het�erogeneous habitats (Mikheev, 1985).

Use of mathematical models, which take intoaccount the heterogeneity of interacting objects (spa�tially explicit models), allows studying ecologicaleffects of fish behavior in heterogeneous habitats,when fragmentary experimental data are available(Mikheev et al., 1997b).

HETEROGENEOUS SITESAS A CONTESTABLE RESOURCE

AND HABITAT COMPLEXITY AS AN OBSTACLE IN TROPHIC RELATIONS

AMONG FISH

It is not always easy to discriminate between infor�mation effects and resource effects when analyzingmodifications of fish behavior caused by habitat heter�ogeneity. A large stone on the river bottom or a sepa�rate coral head could be a source of information avail�able to all swimming by fish. At the same time, suchphysical objects could be contestable and fish tend tokeep permanent perceptual contact with them. Avail�ability of information associated with units of hetero�geneity is restricted only by sensory capacities offish.When an object was embedded into an “internal map”(Olton et al., 1979; Mikheev, 1990), it can be usedthen distantly, without a real perceptual contact. Whenan object is used as a shelter or a territory landmark(Grant, 1997), it can be available only to one orrestricted number of fish.

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Marine and freshwater habitats with high densityand diversity of fish are also characterized by complexhabitat structure. The most impressive examples arerelated with coral reefs, coastal ecosystems of seas andlakes, fluvial habitats. No doubts that optical,mechanical, and hydrodynamic habitat heterogeneityof the scale comparable with fish body size and size oftheir home range should influence on the main kindsoffish activity. In this section, we will discuss effects ofhabitat heterogeneity that result in modifications offeeding, defense, and social behavior of fish.

Feeding Behavior

Fish foraging mode influence on the way in whichphysical habitat heterogeneity modifies main phasesof feeding behavior, prey search, choice, and con�sumption. Sit�and�wait or ambush searchers usuallylook for their prey hiding in topographically structuredareas, where they easily find a shelter, from which theyattack prey. Such foraging mode depends on the ratiobetween the predator size, prey size, and characteris�tics of the spatial structures located in a heterogeneoushabitat. Optimal conditions for ambush predators arethose in which spatially structured spots with sheltersare located among open areas. If dense vegetation,coral colonies, or abundant stones with narrow spac�ing are close to the hunting site of the predator, preycan easily find refuges and avoid predation (Endler,1991; Godin, 1997).

Another foraging mode that typical of sit�and�waitpredators is related to the water flow carrying fooditems nearby the fish, which maintain stable positionrelatively the bottom and river banks. In this case, therole of physical objects that shape heterogeneity (unitsof heterogeneity) is more diverse. For example, largesparsely distributed boulders can be used by foragingfish as landmarks, which help to maintain stable posi�tion in the stream. Stones, pieces of wood, densepatches of vegetation and other objects can be used asshelters. Such physical objects are also important asmodifiers of the hydraulic structure of the water flow.Sharp rheogradients allow fish to stay for a long time ina locality with low current velocity, “hydraulicshadow,” and monitor parts of the flow with highvelocity that carry more food items per time unit.Using burst speed, fish can intercept drifting preywithin the volume of water restricted by its visual reac�tion distance (Pavlov, 1979; Fausch, 1984; Lupandinet al., 2004).

Fish that use the mode of cruising searcher tend toforage in still�water conditions. Many fish, especiallyjuveniles, prey upon zooplankton, invertebrates dwell�ing in vegetation of littoral and sublittoral zones, dem�ersal organisms. Sparsely distributed patches of vege�tation of moderate density and size create suitable for�aging conditions for juvenile fish. We observed young�of�the�year perch, Perca fluviatilis, efficiently foragingin such patches located in the shallow�water zone of

the Sheksna Resrvoir (Mikheev, 1985). When fish werefeeding within the patches of vegetation, they did notkeep schooling but rather dense vegetation structureprevent them from being eaten by piscivores (Crowderand Cooper, 1982; Savino and Stein, 1989). Thepatches of vegetation that contain numerous inverte�brate prey play the role of landmarks facilitatingsearching for food in fish. In such a situation, movefrom one patch to another is the most risky and costlyphase of foraging. Moving among patches fish not onlyspend time and energy for costly locomotion, but alsoare vulnerable for predators. To compensate such arisk, fish maintain rather large schools.

Optimization of swimming paths is especiallyimportant for juvenile fish, for which lowering risk ofpredation and energy expenditures for locomotion iscrucial. In experiments with larvae of Carassius aura�tus we found that fish foraging in the habitat withpatchy food distribution eventually used more straighttrajectories while moving from one food patch toanother (Mikheev et al., 1992). Getting more familiarwith experimental surroundings, fish used both global(at the scale of an experimental tank) and local (stablefood patches on the bottom) landmarks (Mikheev andAndreev, 1993).

Using an individual�based model of fish searchingbehavior, we showed that a combination of directedmovement between food patches together with area�restricted search within the patches results in the mostefficient foraging in the patchy habitat (Mikheev et al.,1997b). When prey items and patches are cryptic,marked physical objects are used as landmarks facili�tating optimal swimming paths in foraging fish. In thisexample, young�of�the�year perch can use patches ofvegetation as reliable landmarks only when their dis�tribution is highly aggregated, i.e. relatively densepatches with clear cut edges were separated by areas ofopen water. Even or random distribution of vegetationmakes foraging of fish more difficult. The higher aver�age density of vegetation stands the lower food searchefficiency and ingestion rate of fish (Gotceitas, 1990;Bean and Winfield, 1995).

Characteristics of feeding behavior of fish includ�ing food search, choice, and consumption are signifi�cantly dependent on the structure of heterogeneity ofthe habitat, where fish are foraging. Depending on theparameters of heterogeneity, prey characteristics and apredator foraging mode heterogeneous habitat caneither hamper, or facilitate fish feeding behavior. Hab�itat heterogeneity arise from abiotic physical objects,aggregations of prey items, and grouping fish, whichinfluence on behavior of surrounding neighbors.

Defense Behavior

Evading and avoiding predators, fish use individualand cooperative tactics (Endler, 1991; Pitcher andParrish, 1993; Godin, 1997). In relatively uniformhabitats, cooperative tactics prevail in defense behav�



ior of fish, especially juvenile fish. These tactics areconnected with fish schools of different size, shape,and composition (Radakov, 1972; Pitcher and Parrish,1993; Pavlov and Kasumyan, 2003; Mikheev and Pav�lov, 2004). In heterogeneous habitats, individual tac�tics prevail. Use of shelters and camouflage are mostimportant among them (Endler, 1991; Godin, 1997).

In highly structured and stable habitats with strongpredation pressure that is typical of coral reef ecosys�tems (Hixon, Beets, 1993; Webster, 2002), shelters areexploited by fish not only individually, but also by fishgroups. According to our observations (our unpub�lished data), it is particularly true to small pomacen�trid fish like Dascillus spp., Chromis spp., small schoolsof which are permanently hovering over separate headsof corals Acropora and Pocillopora. When the threat ofpredation is rather low, schooling is quite efficientantipredator tool. Increased threat, like in the night,when schooling does not work against nocturnal pred�ators, or in the day, when predators are too abundantand active, force all the fish in the school synchro�nously hide among the coral branches. All the terri�tory, i.e. coral colony as refuge and the space over thecolony, where fish catch drifting food items, is usedcollectively. Despite the pronounced differences in thebody size among fish in such schools, no aggressiveinteractions between territory owners were observed.

Individual fish or small groups of fish often useobjects of complex shape as a refuge. In such refuges,fish are either hiding inside completely, or staying in itsshadow, or freezing over it. Search for and choosing aproper shelter is particularly important for juvenilefish, which are numerous and rather mobile. Whatcharacteristics of physical objects make them attrac�tive as shelters? Scanty experimental results are rathercontroversial. It has been shown in experiments with a3�D construction that bluegills, Lepomis macrochirus,chosen fragments, where vertical elements prevailed.Spacing, distance between bars played a significantrole as well. It was especially important for construc�tion composed of horizontal bars (Johnson, 1993). Nopreference for shelters with more spacious interiorwere found in experiments with goby, Neogobius mel�anostomus (Stammler and Corkum, 2005). Larger fishdid not prefer larger shelters. However, in experimentswith interference competition for shelters in theAtlantic salmon, Salmo salar, parrs, we observed thatlarger fish won contests for larger shelters (Mikheev,2000). The difference in the compared results areprobably related to different characteristics of sheltersused in experiments. In the experiments with N. mel�anostomus, the shelters were similar from outside anddiffered only by the volume of the interior. In theexperiments with S. salar, fish chosen among the shel�ters of different sizes. Internal and external sizes ofshelters were positively correlated. We suggest thatexternal parameters of physical structures are impor�tant for fish assessing and choosing the shelter. If theshelters are contestable, duration of the shelter explo�

ration and assessment should not be too long, becausethe competitors can occupy it before. Assessment ofthe habitat heterogeneity structure as potential refugesfrom predators should include not only characteristicsof separate physical objects, but also patterns of theirspatial distribution relatively to each other. Defensebehavior of territorial animals consists not only of thechoice of a suitable refuge, but also of highly stereo�typed motor patterns that facilitate finding the shortestway to the shelter from any point of the individual ter�ritory (Stamps, 1995).

In coastal habitats, where zones of dense vegetationalternate with areas of open water and sandy bottom,vegetation zones play role of refuge habitats (Orthet al., 1984; Linehan et al., 2001). Such refuge habitatsare preferred by young�of�the�year cods Gadusmorhua, which find safety and abundant food there(Laurel et al., 2004). Fish do not establish individualterritories in such habitats like salmon, S. salar, parrsdo over the stony bottom (Kalleberg, 1958; Mikheevet al., 1994b). Instead of using individual shelters,juvenile cods keep small shoals, freeze and camouflag�ing over suitable backgrounds. When the density of fishin the refuge habitat is too high, part of the populationis forced to areas of open water, where they keep largerand more dense shoals (Laurel et al., 2004).

Use of protective coloration is typical of fish livingin various habitats (Protasov, 1978; Donelly and Dill,1984). Ability to change coloration and be cryptic overthe chosen substrate is especially characteristic of bot�tom�dwelling fish. Protective coloration can be eitherrelatively stable, or quickly change depending on colorof the substrate. Juveniles of many fishes, for example,salmonids, are often occur in novel surroundings,where they have no information about shelters. Insuch a situation, they “freeze” over dark substratesthat makes them poorly visible for predators. Young�of�the�year rainbow trout, Oncorhynchus mykiss, canvigorously fight for dark spots over generally lightbackground even in familiar habitats, if there are noenough refuges. In experimental flow�through tankswith visually heterogeneous bottom, scared S. salarparr showed more pronounced preference for darkareas than did parr, which were not scared by predators(Mikheev, 2000).

Small�scale habitat heterogeneity plays significantand, as a rule, positive role providing various refugesfor fish hiding from predators. Landmarks help fish tofind the shortest route to shelters. If a habitat is ratherhomogeneous or in a novel habitat, which appears tobe homogeneous, shoaling of fish makes surroundingsof each individual in the school structured providingfish with a substitute of shelters and landmarks.

Social Behavior

Variability of social structure of fish groups andrelationships between fish are often caused by thestructure of their surroundings. The most impressive

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examples of such variability are related to the estab�lishment of individual territories within groups of fishthat occurred in a sparsely populated site in heteroge�neous habitats. After a rather long period of explora�tion of novel surroundings, fish begin competition forthe territory, which possess a shelter, well recognizablelandmarks, or a dark place on the bottom, over whichfish are cryptic (Mikheev, 2006). Competition isaccompanied by agonistic interactions, which resultedin establishment of the territory by one of the contes�tants, which is usually the largest fish. If a shelter islarge enough and a source of food is not far from it,more than one fish can establish the territory using thesame shelter. As a rule, the largest owner of the terri�tory allows the smallest fish to use the shelter and sur�rounding area (Mikheev, 2000).

If food is abundant, threat of predation is high, andcompeting fish are numerous, the shelter can beshared by several fish. When fish are out of the shelter,they maintain a compact group like a shoal. Fish insuch groups significantly differ by size that makesthem different from equipotential free�swimmingschools. Stable groups of small pomacentrid fishes,which are strongly associated with separate colonies ofscleractinian coral, are typical examples of such socialstructures. There are no aggressive interactions amongfish, which activity is well coordinated. All this makessuch groups similar to free swimming schools. Perma�nent relations with a particular site together withdiverse size structure make them similar to territorialstructures typical of near bottom fishes.

When the number of young�of�the�year cods,Gadus morhua, was high, a considerable part of itspopulation was forced out from densely vegetatedareas to open water areas, where they maintainedmuch larger shoals than in refuge habitats (eelgrassfields). This result is one of rare examples that showvariations of the spatial distribution pattern and socialstructure within a fish population depending on habi�tat heterogeneity (Laurel et al., 2004). Similar resultswere obtained in experiments with the minnow, Phox�inus phoxinus, where effects of various levels of habitatheterogeneity within a stream were studied (Orpwoodet al., 2008). Minnows shoaled and maintained largerschools when the predator, pike, Esox lucius, waspresent, but this effect was observed only in poorlystructured habitats. In highly structured habitats,frightened fish decreased their swimming velocity andstayed motionless at the units of heterogeneity.

Units of heterogeneity can be not only a contest�able resource. They can be used as markers of particu�lar sites, where fish interact. Such interactions couldbe the cleaning symbiosis, reproductive, shoaling rela�tionships. It is not an easy task to establish and main�tain a school in a habitat without landmarks. Schoolself�assembling seems to be much easier, when recog�nizable landmarks are within visual field. Fragments offish schools can play such a role in poorly structuredpelagial.

Type and characteristics of social interactionsamong fish with flexible social relations depend onvarious factors, among which biotic ones like thenumber and structure offish groups, predation pres�sure, food availability are considered to be the mostimportant. Recent experimental and field results con�vincingly demonstrate that the effects of these factorscan be significantly modified by the structure (level ofspatial heterogeneity) of habitats. When a habitat isphysically structured, tendencies to disperse andestablish individual territories prevail. In uniform,poorly structured habitats, fish tend to gather inschools or shoals and maintain larger aggregations.

HABITAT HETEROGENEITY AS A SOURCE OF INFORMATION CUES

MODIFYING FISH BEHAVIOR

In the previous section, we discussed modificationsof fish behavior caused by habitat heterogeneity in sit�uations when fish are permanently in the perceptivecontact with units of habitat heterogeneity. Ecologicalinteractions are usually accompanied by interference,and patterns of spatial distribution of fish are closelyrelated to characteristics of habitat heterogeneity.Recently discovered modifications of fish behavior, forwhich spatial relations between fish and units of heter�ogeneity are not clearly pronounced; their adaptivesignificance and functional interpretation are not evi�dent (Mikheev et al., 1997a; Mikheev, 2000; Afoninaet al., 2005; Mikheev, 2006; Pavlov et al., 2008). Wesuggest that units of habitat heterogeneity play in suchcases a role of signals or sources of information influ�encing fish behavior.

Exploratory Behavior

When occurred in novel habitats, scared fish, firstof all, habituate and begin exploration of their sur�roundings. Even very hungry fish do not start feedingbefore they are quiet and familiar to some extent withsurrounding structures (Mikheev et al., 1994a). Onlyabrupt appearance of a predator can interrupt the pro�cess of exploration. Exploration of a novel situationconsists of the two phases (Mikheev and Andreev,2003). Firstly, fish use global (on the scale of a habitat),and, secondly, local landmarks. Actively exploring anovel experimental tank fish are quickly swimmingalong the walls, and then they begin stops and turnsnear marked easily recognizable objects (Teyke, 1989;Nepomnyashchikh and Gremyachikh, 1996; Mikheevand Andreev, 1993).

Exploration of a novel habitat is energetically costly(in the beginning of exploration fish swimming veloc�ity is rather high) and dangerous activity, especially forjuvenile fish. In experiments with young cichlid fishCichlasoma octofasciatum, we discovered that fish wereswimming with lower velocity and completed theexploration of a novel aquarium much faster, if the



aquarium possessed contrast visual landmarks on thewalls. In the control aquarium, with visually uniformwalls, the period of exploration lasted 3 times longer,and swimming velocity of fish was 1.4 times higher. Weconsidered that the exploration was completed whenfish began feeding (Mikheev et al., 1997a). An abilityto efficiently use patterns of visual habitat heterogene�ity while exploring novel surroundings as shaped in thefish early ontogeny. Convict cichlids, Archocentrusnigrofasciatum, which were grown in visually hetero�geneous habitats, completed exploration of novel sur�roundings much faster and spending less energy thantheir conspecifics, which were grown in visuallydeprived habitats (Afonina, 2002).

Animals respond to changes in their surroundingsdepending on their life styles. Resident birdsresponded to the changes earlier and explored sur�roundings more actively and thoroughly than nomadicspecies (Mettke�Hofmann et al., 2005). We suggestthat similar differences could be observed in fish. Res�idents and nomads are known in fish both at withinspecies and between species levels (Grant and Noakes,1987). This suggestion is worth testing in experimentswith manipulation by physical structures within fishhome ranges.

Effects of Visual Heterogeneity

Taking into account the crucial role of vision in fishbehavior, we suggested that only visual cues couldmake a habitat heterogeneous and suitable for explo�ration and establishment a territory or home range(Mikheev, 2000; Mikheev and Pavlov, 2004). Thesecues can modify behavior that fish use while establish�ing an individual territory and competing forresources. Such suggestions are based on the results ofsome experimental studies, in which fish behavior wasmanipulated via visual perception. For example,males of the cichlid fish Hemichromis bimaculatus wonthe contest for the reproductive territory if they spenta certain period of time in an aquarium with visuallandmarks (vertical dark stripes on the walls). Males,which were not familiar with such an aquarium orspent there shorter time, lost a contest (Boer de andHeuts, 1973). There were no prior residency effects inaquaria without dark visual landmarks.

In experiments on the territory establishment insalmonid and cichlid fish, we found that the contestfor a potential territory could be provoked not only byvital essentials like a source of food or shelter, but alsoby marked visual landmarks (Mikheev et al., 1997a;Mikheev and Pavlov, 2004). These effects are mostprobable at the initial stages of the territory establish�ment. We observed that fish vigorously fought for anarea situated near dark vertical stripes on the walls ofaquarium. Smaller individuals were forced out eventu�ally by a larger fish from the area. Dominant, usually alarger fish, had significantly higher consumption ratethan a subordinate, when the contestable food patch

was near visual landmarks. If landmarks and the foodpatch were far from each other, both dominant andsubordinate fish had similar consumption rates. In thelatter case, activity of the dominant was directed pri�marily to guarding of the visually non�uniform that leftfor subordinate more chances to feed. These resultssuggest that “information resources' associated withheterogeneous sites are more contestable for fish thanenergy resources.

Ecological differences between fishes should betaken into account. For example, in juvenile salmo�nids, the differences take place both between speciesand within species. The benthic morph of the arcticcharr, Salvelinus alpinus, dwelling the near�shore zoneof lakes is rich of visually heterogeneous sitesresponded to the dark stripes on the light bottom, butjuvenile charr of the pelagic morph did not respond(Mikheev et al., 1996). Prey distribution and sheltersavailability are more predictable in the near�shorezone, and the resources there are often associated withunits of heterogeneity (Malmquist et al., 1992). It isalso true for stream�dwelling juveniles of the Atlanticsalmon, S. salar, which showed even more pro�nounced response to the visual heterogeneity than thebenthic morph of the Arctic charr. Juveniles of thepelagic morph of the Arctic charr live in the openwaters of lakes, where spatially fixed landmarks arevery rare, and zooplankton, the main food, forms tem�porary aggregations, which are usually not associatedwith landmarks.

Units of visual heterogeneity can be associated withstable structures of the home range like shelters, land�marks, and the response to such objects could be hardwired and more stable than to food patches. A darkpatch on the light bottom was very attractive to theyoung�of�the�year Atlantic salmon parrs and used byfish as a shelter (fish were less visible for predators overdark substrate) and a landmark that helped fish tomaintain the stable position in the flow and catchdrifting food particles (Mikheev, 2000).

Food is considered the major contestable resource,but fish often demonstrate interference competitionnot for food, but for heterogeneous sites in the habitat,where they vigorously fight either for a shelter or justfor visually non�uniform area (Mikheev et al., 1997a;Westerberg et al., 2004). Why contrasting geometricalfigures on the bottom or walls of aquarium occur to bemore attractive and valuable for fish than foodpatches? Food patches are usually ephemeral struc�tures and used by fish for a short period. Visually het�erogeneous sites can be used by fish inhabiting struc�tured habitats as a template of a future individual ter�ritory, where fish can find not only food but also arefuge from predators. Fish use individual territoriesfor much longer period than food patches.

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Habitat Heterogeneity and the Conflict of Motivations

One of the most complicated situations for deci�sion�making is when fish are hungry, surroundings areunfamiliar, and predation threat is high. The mainobstacle for choosing an optimal behavior is related tothe deficiency of information about the level of preda�tion threat, availability of food, and position of sheltersrelatively to sources of food. The safe solution for asolitary fish in a homogeneous habitat is to minimizeevery activity and stay quietly. What fish will do if thehabitat is heterogeneous? One of the most evidentalgorithms of fish behavior is to use a heterogeneoussite as a shelter, assess a degree of predation threat andresume feeding when the situation is safe enough. Fishoften assess the threat of predation estimating the con�centration of kairomones (Wisenden, 2000). However,such estimates provide no information about exactlocation of a predator, level and longevity of predationthreat. If fish, especially juveniles, is too cautious andcease foraging for a long period, their energy losseswould be too high. To study abilities offish to makedecisions under a conflict of motivations, we testedbehavior of hungry guppy, Poecilia reticulata, inaquaria with the mixture of large and small cladocer�ans Daphnia magna and kairomons of the cichlid fishAstronotus ocellatus (Afonina et al., 2005). Two typesof aquaria were used, one of them contained a patch ofplastic stripes in one of the corners that mimicked veg�etation, the other was free of physical structures. In theaquarium with uniform interior and added kairomons,the guppies in the groups of 3 fish had significantlylower consumption rate than had fish in the controlaquarium without kairomons. The reduction of therate was more pronounced in the case of large D.magna. No effects of kairomons were observed inaquaria with “vegetation” or in uniform aquaria whenthe size of fish group was increased up to 10 individu�als. Surprisingly, fish did not actually use the patch of“vegetation” as refuge. Just the presence of eitherphysical refuge or “social refuge” neutralized theinhibiting effect of kairomons and allowed fish to feedmore intensively despite the potential danger. We sug�gest that the decision�making was influenced only byavailable information of possibility to use a refuge.

Refuges as Modifiers of Fish Behavior

In one of the previous sections, we discussed howfish use units of the habitat heterogeneity as refugeswhen the direct threat of predation is anticipated. Itwas meant that both individual territory owners andgroups of fish sharing complex systems of refuges werefamiliar with surroundings. It is not like this, especiallyin the early ontogeny. In a novel habitat many fish usepredominantly shoaling, when predators suddenlyappear. Defense behavior and other aspects offishbehavior substantially change if physical structures

suitable as shelters were found during exploration of anovel area.

At the initial stage of exploration of a novel area, asuitable shelter can be used by all members of the fishgroup. Eventually, the shelter is getting a contestableresource (Mikheev et al., 2005). This transition isaccompanied by the change of all the system of socialrelations. First of all, equality of grouping fish disap�pears. The shelter is monopolized by the dominantfish, usually, it is the largest individual. Some of theother fish continue competition for the heterogeneoussite with the shelter for several hours—days, but even�tually cease the attempts. Sometimes, the dominantfish allows the smallest fish of the group to share thesame territory and shelter (Mikheev, 2000). Largercompetitors try to find empty sites with free refuges. Ifthere are no such sites nearby, failed fish shoal andmove to look for new habitats.

Contest for heterogeneous sites with shelters or justfor visually non�uniform areas is usually more proba�ble than contest for food patches (Mikheev et al.,1997a; Westerberg et al., 2004). However, we foundthat the social position of competing fish is correlatedwith their consumption rate (Mikheev et al., 2005).Feeding rate of dominants was much higher than thatof subordinates. Thus, behavioral relationships, whichoccur at the competition for free refuges, are relatednot only to the defense from predators. These relation�ships modify social interactions and allow revealing ofthe patterns of behavior that include contestability,defense and foraging activities. Such modifications ofbehavior take a long time (hours—days). This is whythe researchers discover and explore them ratherrarely.

CONCLUSIONS

Units of habitat heterogeneity as physical objectsare used by fish almost in all vital activities, feeding,defense, and social behavior. In a novel habitat, whenanimals are not familiar with such objects and theirspatial distribution, the behavioral responses to theunits of heterogeneity are not quite clear. In the courseof habitat exploration, the responses are getting moreclear�cut, easily recognizable, and tractable.

Habitat heterogeneity can be related to fixed sta�tionary objects with clear�cut margins (boulders, coralheads, dense patches of submerged vegetation etc.) aswell as to gradients of factors, which occur as a productof fixed objects. Most common gradients are rheogra�dients near obstacles in the water flow, photogradientsboth in the still and running waters. Fish use sites withphysical gradients as refuges, in which they continueother activities being poorly visible for predators. Stay�ing almost motionless in the hydrodynamical or opti�cal shadows, fish can guard their individual territoriesfrom intruders or catch prey drifting in the flow.

Objects that generate habitat heterogeneity can beeither clumped or dispersed. Separate boulders or



compact clusters of stones on the bottom of a river areexamples clumped objects, and continuous stands ofsubmerged vegetation or coral reefs with various den�sity of units are dispersed objects. There are many pat�terns of the spatial organization between these twoextremes. The role of habitat heterogeneity as modifi�ers of fish behavior depends on both characteristics ofseparate units and the pattern of their spatial distribu�tion. For example, an isolated object that possess saferefuge can be used as the shelter from predators, “ref�erence point” for establishment of an individual terri�tory, and landmark for fish feeding on drifting prey(Fausch, 1984). A bottom area covered with sub�merged vegetation can serve as a refuge from preda�tors. In such areas, foraging is often less efficient thanin open water sites, and guarded individual territoriesusually are not established. Fish as a rule keep shoals insuch habitats, but the shoals are less than in open waterareas.

A common term “habitat complexity,” or “habitatheterogeneity,” is usually applied to different types ofhabitats. One is an area with clumped sparsely distrib�uted objects, another �areas rather evenly covered withsubmerged vegetation. Both types of habitats are con�sidered “complex” or “heterogeneous,” and com�pared with open water relatively homogeneous habi�tats (Warburton, 1990; Bean and Winfield, 1995;Mikheev, 2000; Mikheev and Pavlov, 2004). Theresults of such comparisons are rather controversial.For example, structurally complex habitats can eitherfacilitate fish foraging or make it more difficult (Got�ceitas, 1990; Warburton, 1990; Bean and Winfield,1995); they can either help or prevent establishment ofindividual territories differently influencing agonisticbehavior of fish (Boer de and Heuts, 1973; Basquilland Grant, 1998; Mikheev and Pavlov, 2004). To avoidsuch logical problems, we have to take into account awide spectrum or continuum of levels of heterogeneity.This can include various types of habitats beginningfrom quite homogeneous habitats without any promi�nent objects, to moderately heterogeneous habitatswith rather rarely dispersed isolated objects or clustersof objects, and further on to highly heterogeneoushabitats densely filled with numerous units. Before wemake such “a scale of heterogeneities,” we have todevelop the indices of density of heterogeneity units,to learn how to assess diversity of the units (variabilityin size, shape, spacing) as well as their suitability asindividual or communal shelters.

What makes heterogeneous parts of the habitatattractive for fish, if there are no vital objects? It isknown that information about predators, food patchesavailable for fish is usually limited and unreliable. It isespecially true for juvenile fish. It is also known thatstructured habitats are characterized by high biologi�cal productivity, and there are plenty of potential ref�uges. Habitat heterogeneity or complexity is almostalways accompanied by visual and other types of het�erogeneity. Adaptive significance of fish attraction to

the units of heterogeneity is probably related to thefact that under natural situations vital for fish objectsare often tightly coupled with heterogeneous sites.Thus, units of habitat heterogeneity can be reliablesignals or information cues in uncertain, i.e. change�able and poorly predictable, habitats (McLinn andStephens, 2006).

We believe that taking into account of the effects ofsmall�scale habitat heterogeneity is important as oneof the determinants of biotic interactions in the spa�tially explicit models of the “predator�prey” and “tri�otroph” relationships. It is known that informationcues together with trophic relations substantiallyinfluence on characteristics and intensity of ecologicalinteractions (Wertheim, 2005).

ACKNOWLEDGMENTS

The study was supported by the Russian Founda�tion for Basic Research (projects no. 08�04�00893a,09�05�00736a, 08�04�00927a) and also by the grantfrom the President of the Russian Federation for theLeading Scientific Schools (contract no. NSH�2104.2008.4).

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Habitat heterogeneity and fish behavior: Units of heterogeneity as a resource and as a source of information