Influences of environmental cues, migration history, and habitat familiarity on partial migration

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  • Behavioral Ecologydoi:10.1093/beheco/arq121

    Influences of environmental cues, migrationhistory, and habitat familiarity on partialmigration

    Christian Skov,a Kim Aarestrup,a Henrik Baktoft,a Jakob Brodersen,b Christer Bronmark,b

    Lars-Anders Hansson,b Einar E. Nielsen,c Tine Nielsena and P. Anders NilssonbaSection for Freshwater Fisheries Ecology, Technical University of Denmark, National Institute of AquaticResources (DTU Aqua), Vejlsvej 39, 8600 Silkeborg, Denmark, bDepartment of Ecology / Limnology,Ecology Building, Lund University, SE-223 62 Lund, Sweden, and cSection for Population Ecology and-Genetics, Technical University of Denmark, National Institute of Aquatic Resources (DTU Aqua),Vejlsvej 39, 8600 Silkeborg, Denmark

    The factors that drive partial migration in organisms are not fully understood. Roach (Rutilus rutilus), a freshwater fish, engage inpartial migration where parts of populations switch between summer habitats in lakes and winter habitats in connected streams.To test if the partial migration trait is phenotypically plastic or has genetic components, we translocated roach from 2 populationswith different opportunities for migration to a lake with migration opportunity, containing a local roach population. Thisenabled monitoring of partial migration of fish in 3 different situations: 1) previous opportunity for migration, migrating ina familiar environment (the local population); 2) previous opportunity for migration, migrating in an unfamiliar environment;and 3) no previous opportunity for seasonal migration, migrating in an unfamiliar environment. In addition, we evaluated themigration patterns of roach in the lake with migration opportunity wherefrom group 2 fish were translocated. Directionalmigration in and out of the lakes was monitored using Passive Integrated Transponder technology. Translocated fish withprevious migration opportunity showed migration patterns more similar to local fish than to their home lake population, andindividuals translocated from the lake without migration opportunity migrated when given the opportunity, suggesting thatpartial migration is phenotypically plastic and triggered by lake-specific environmental cues. We found temperature to bea proximate cue for migration decisions. Individuals without previous migration opportunity migrated at a lower proportionand with different small-scale migration patterns, suggesting that also genetic components are involved in the expression of thepartial migration trait. Key words: local adaptation, passive integrated transponders, phenotypic plasticity, proximate cues. Rutilusrutilus, translocation. [Behav Ecol]

    The spatio-temporal distribution of animals is of central im-portance for our understanding of dynamics and interac-tions within and between populations. Migration behavior iscommon across taxa and occurs regularly in all kinds of envi-ronments, terrestrial as well as aquatic (Swingland and Green-wood 1983; Dingle 1996; Nathan et al. 2008). The timing andextent of migrations may affect both population and trophicdynamics (e.g., Fryxell and Sinclair 1988; Lundberg 1988;Koyama et al. 2005; Brodersen, Adahl et al. 2008), and alteredmigration properties, for instance caused by environmentalchanges, could thereby impose effects on higher order pro-cesses. The understanding of migration behaviors should thusbe an integral part of the comprehension of such processes.Migratory differences between populations are common in

    nature. Well-known examples include migratory and residentpopulations of large herbivores of the Serengeti Plain andNgorongoro crater (Fryxell et al. 1988) and anadromousand landlocked populations of, for example, sockeye/kokanee salmon (e.g., Taylor 1999) and alewives in NorthAmerica (e.g., Post et al. 2008). Such differences in migrationpropensity are often due to physical barriers hindering

    migration. Migration variation has been shown to affect pop-ulation structure (Fryxell et al. 1988), ecosystem dynamics(Post et al. 2008), and evolution of foraging traits (Palkovacsand Post 2008).Many species show partial migration, in which less than

    100% of a population migrate, as found in, for example, birds,mammals, insects, and fish (review by Swingland 1983). Themechanisms involved in partial migration have been soughtafter using a number of approaches, including evaluation ofgenetic differences, evolutionary stable strategies or condi-tional differences, and the relative contribution of geneticand environmental components to partial migration (Lack1944; Lundberg 1988; Hindar et al. 1991; Jonsson and Jonsson1993; Kaitala et al. 1993; Brodersen, Nilsson et al. 2008). Stud-ies on birds have also suggested that all populations can beviewed as partially migratory, where totally resident or totallymigratory populations represent the extreme end points ofa partial migration continuum (Berthold 1996). This isbacked up by genetic evidence suggesting that frequency ofmigrants and migratory activity is 2 different aspects of 1 trait,migratoriness (Pulido et al. 1996). Differences between pop-ulations in frequency of migrants should therefore be due todifferences in selection pressure on this trait. Thus, if migra-tion behavior is at least partly under genetic control and thepartial migration patterns exhibited by a specific populationare a result of local adaptation to prevailing environmentalconditions, then migrating individuals should maintain their

    Address correspondence to C. Skov. E-mail: 18 January 2010; revised 29 June 2010; accepted 6

    July 2010.

    The Author 2010. Published by Oxford University Press on behalf ofthe International Society for Behavioral Ecology. All rights reserved.For permissions, please e-mail:

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  • migratory behavior in a new environment until natural selec-tion has restored local adaptation. In the extreme case, indi-viduals that have had no previous migration opportunity, forinstance due to physical barriers, should, according to thepopulation-property reasoning, remain nonmigratory if theopportunity to migrate should arise. If, on the other hand,migratory behavior is phenotypically plastic, migrants shouldalter their migration behavior in response to system-specificprerequisites and conditions in a new environment, regardlessof their migratory history. This latter alternative demands plas-ticity according to proximate cues that drive migration behav-ior. For example, it has been shown that altered opportunityfor growth can induce migratory or nonmigratory behavior(Olsson et al. 2006, Brodersen, Nilsson et al. 2008) and thatfood availability and population density influence partial mi-gration (Nilsson et al. 2006). These findings suggest that phe-notypic plasticity should be expected in the partial migrationtrait. We here investigate if partial migration is a completelyphenotypically plastic trait or if it has genetic components, byevaluating the timing and patterns of seasonal partial migra-tion in local and translocated populations of a partially mi-grating freshwater fish.Partial migration is a common phenomenon and occurs in

    many types of ecosystems. System-specific properties may,however, offer different opportunities to evaluate interpopu-lation differences in migration patterns. In terrestrial ecosys-tems, populations can have overlapping distributions, and itmay therefore be difficult to determine interpopulation dif-ferences in migration history (e.g., Bensch et al. 1999). Inaquatic systems, on the other hand, populations even withinsmall geographic areas may be clearly spatially separated, forinstance as for fish populations in different lakes. This studyuses the spatial distinctness of lake ecosystems to explore theimportance of environmental cues, environmental familiarity,and migration history, for partial migration timing and pat-terns, by studying 3 populations of roach (Rutilus rutilus) ina translocation experiment. As lakes often differ in growthand migration opportunities, as well as predation regimes,they represent suitable study systems for the questions athand. Earlier studies have shown that roach exhibit seasonalpartial migration from their home lakes to connected streamsduring winter in order to minimize risk of predation duringthe poor growthopportunity winter period (Hansson et al.2007, Bronmark et al. 2008; Skov et al. 2008). It was suggestedthat the migration is a response to seasonal changes in risk ofpredation P (cost) and growth potential G (benefit) in thelake versus the streams and that individuals trade off costsand benefits such that when the cost/benefit ratio (P/G) ina given habitat increases above a certain threshold, individualsshould migrate to either increase G or decrease P (Bronmarket al. 2008). As fish are ectothermal organisms, the predationrate by piscivorous fish and growth for roach are to a largeextent determined by temperature, and thus, changes in lakewater temperature during autumn are a potential proximatecue for roach out-migration from the lakes.We monitored and compared partial migration patterns of

    roach from 3 populations in different situations. We translo-cated individuals from 2 different lakes, 1 with and 1 withoutpossibilities for migration. Roach were translocated to a targetlake with connecting streams and hence migration possibili-ties. The target lake contained the third roach population thatwas monitored in its home system. Furthermore, we monitoredmigration patterns of roach in their home lake wherefrom wetranslocated fish with previous migration opportunity. Usingthis setup, we were able to evaluate partial migration behaviorsof fish in 3 different situations: 1) individuals with previousopportunity for seasonal migration migrating in an unfamiliarenvironment, 2) individuals with no previous opportunity for

    seasonal migration migrating in an unfamiliar environment,and 3) individuals with previous opportunity for seasonal mi-gration migrating in their familiar home environments in 2different lakes. If migration behavior is phenotypically plasticand influenced by system-specific environmental cues andproperties, we should expect fish in group 1 to migrate ina pattern more similar to local fish in the target lake than tofish in their lake of origin. We should also expect migrationamong group 2 fish when given migration opportunity in thetarget lake. If, on the other hand, the trait for partial migrationhas a large genetic component, fish from group 1 should showpartial migration patterns resembling those of their home pop-ulation, whereas fish from group 2 would not migrate at all.Hence, group 2 represents an extreme partial migration situa-tion evaluated to shed light on the relative importance of phe-notypic plasticity and genetic components as drivers of partialmigration patterns.Under the assumption that environmental factors govern

    partial migration behavior, we predicted that familiarity withthe migration environment would reveal small-scale differen-ces in migration timing and patterns between the 3 groups offish in the target lake, potentially originating from fish famil-iar with the environment being able to make more precisemigratory decisions from local experience. Furthermore, ifroach use water temperature as a proximate cue for migrationbehavior, we expected correlations between water tempera-ture and migration patterns in both lakes.


    Study systems

    The study took place in 3 lakes in Denmark. The target lake,Lake Sgard (lat 5525#N, long 919#E, Figure 1), to whichroach were translocated from 2 other lakes is a small,eutrophic, and shallow lake (area 0.26 km2, average depth1.6 m, and mean summer Secchi depth 0.55 m). The fishcommunity is numerically dominated by roach and small

    Figure 1.Schematic figure showing the experimental area in Lakes Sgard (A)and Loldrup (B). Arrows indicate flow direction of the water. The 2lines crossing the inlet and outlet, respectively, indicate positions ofthe 2 loop-shaped antennas, each covering the entire cross section ofthe stream.

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  • perch (Perca fluviatilis), but bream (Abramis brama), rudd(Scardinus erythrophthalmus), white bream (Blicca bjoerkna),pike (Esox lucius), and eel (Anguilla anguilla) also occur(Grunfeld 2003). There is no submerged vegetation present,and the lake is surrounded by a 3- to 4-m-wide reed margin(Phragmites australis) (Grunfeld 2003). Lake Sgard has well-defined inlet and outlet streams, and previous investigationshave shown that 4070% of the cyprinid fish, and especiallyroach, bream, and white bream, use the inlet and outlet streamsas overwintering habitats (unpublished data).Roach were translocated from 2 lakes, Lake Loldrup that

    has natural outlets/inlets providing opportunity for seasonalmigration and Lake Rnbk that does not provide opportu-nity for seasonal migration. Lake Loldrup (lat 5629#N, long926#E, Figure 1) is small, shallow, and slightly eutrophic(area 0.39 km2, average depth 1.2 m, and mean summer Sec-chi depth 1.1 m). The Lake Loldrup fish community is nu-merically dominated by roach and bream, but also includesperch, pike, and pikeperch (Sander lucioperca). Lake Loldruphas an inlet and an outlet and is comparable with Lake Sgardwith respect to size and average depth. The compositions ofthe fish communities differ slightly between the lakes withLake Loldrup having a higher numerical proportion of pisci-vores (0.034) than Lake Sgard (0.021, calculated from catchper unit effort data on perch, pike, and cyprinids in Grunfeld2003 and Viborg County 2002). Furthermore, after severalyears without submerged macrophytes, Lake Loldrup was in-vaded by submerged macrophytes (mainly Elodea canadensisMichx. and Potamogeton crispus L.) during 2006, and in Sep-tember 2006, these macrophytes covered more than 50% ofthe lake. Previous studies have shown that more than 70% ofthe cyprinid fish in Lake Loldrup reside in the inlet or outletstreams for prolonged periods during autumn and winter(Skov C, unpublished results). Lake Rnbk is small, shallow,and eutrophic (lat 5615#N, long 1003#E) (area 0.015 km2,average depth 0.8 m, and mean summer Secchi depth 0.55 m)and has no submerged macrophytes. The fish community isdominated by roach and also contains a few perch, pike, com-mon carp (Cyprinus carpio), and crucian carp (Carassius caras-sius). The lake was man made in the 1970s and is used asa rainwater drainage basin for an urbanized area; the waterto the lake is supplied from precipitation. The lake has noinlet stream, and the outlet consists of a surface spill situatedapproximately 20 m from the western shore. When excessrainwater enters the lake, the water level increases...