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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 Nilssonb

aSection for Freshwater Fisheries Ecology, Technical University of Denmark, National Institute of AquaticResources (DTU Aqua), Vejlsøvej 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),Vejlsøvej 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: [email protected] 18 January 2010; revised 29 June 2010; accepted 6

July 2010.

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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 growth–opportunity 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.

METHODS

Study systems

The study took place in 3 lakes in Denmark. The target lake,Lake Søgard (lat 55�25#N, long 9�19#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 Søgard (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 Søgard has well-defined inlet and outlet streams, and previous investigationshave shown that 40–70% 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 Rønbæk that does not provide opportu-nity for seasonal migration. Lake Loldrup (lat 56�29#N, long9�26#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 Søgardwith 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 Søgard (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 Rønbæk is small, shallow,and eutrophic (lat 56�15#N, long 10�03#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 and even-tually runs over the spill and drops 2.5 m through pipelines toa nearby river. The 2.5-m drop prevents return migration tothe lake if fish actively or by chance enters the surface spill.Lake water temperatures in the outlets of Lakes Loldrup andSøgard were measured with Tidbit storage loggers, loggingtemperature once every hour throughout the study period.

Treatments, fish capture, and tagging

Roach from Lake Loldrup were translocated to the target LakeSøgard and represented a population with a history of oppor-tunity (O) of migration translocated to a new unfamiliar (U)environment (henceforth referred to as OU fish). Translo-cated fish from Lake Rønbæk represented a population withno (N) previous opportunity for migration translocated to anunfamiliar (U) environment (NU fish). The original roachpopulation in the target lake (Lake Søgard) representeda population with previous opportunity for migration to bemonitored in its familiar (F) environment (OF fish).NU fish from Lake Rønbæk and OU fish from Lake Loldrup

were sampled by electrofishing in the litoral zone on 10 Sep-tember 2006 and transferred to Lake Søgard where they werestocked in separate holding pens to acclimatize to the new

environmental conditions. Similarly, OF fish were sampledby electrofishing in Lake Søgard and transferred to a holdingpen in order to standardize treatments between the 3 groupsof fish. Eighty-three fish from each holding pen and popula-tion were individually weighed to the nearest 0.1 g, measuredto the nearest millimeter (total length, Table 1), andtagged according to Skov et al. (2005) by surgically implantinga TIRIS Passive Integrated Transponder (PIT) tag (Texas In-struments, RI-TRP-RRHP, half duplex, 134 kHz, 23.1-mmlong, 3.85-mm diameter, 0.6 g in air) into the stomach cavityof the fish. After recovery from tagging, all fish were releasedin the centre of Lake Søgard. In order to compare the migra-tory behavior of OU fish with that of fish migrating in theirnatal Lake Loldrup (henceforth referred to as OUorigin fish),282 individuals were captured in Lake Loldrup, PIT tagged,and released. An evaluation of PIT-tag marking techniqueshas shown that the method causes no significant effect on fishwell-being, including body condition (Skov et al. 2005). Ex-perimental animal treatment was performed under permis-sion from the Danish Animal Experiments Inspectorate.

Fish migration

Migrations of roach between the lake and the inlet and outletstreams in lakes Loldrup and Søgard weremonitored by passivebiotelemetry using a modified PIT-tag antenna system (Skovet al. 2005; Skov et al. 2008; Figure 1). When a tagged fishswims by an antenna, the PIT-tag is energized and emitsa unique code that can be recorded and stored together withdate and time on a memory card. Two loop-shaped antennas,each covering the entire cross section of the stream, wereplaced 3–5 m apart along the inlet (15 m upstream the lake)and the outlet streams (150 m downstream the lake, as outlettopography did not allow installation of antennas closer to thelake). The use of 2 sequential antennas enables determinationof fish swimming direction. The antenna recording frequencywas 5 energize/receive cycles s21 (Castro-Santos et al. 1996).Migration data presented are based on data from time oftagging until 1 June 2007, when return migration to the lakehad ended.

Data treatment and analysis

Individual fish were defined as migrants if they were recordedby any antenna in the streams during the study period, and in-dividual fish were defined as residing in the stream as long astheir latest record was on the antenna farthest away from the

Table 1

Mean 6 SE length, body condition, and migration characteristics ofindividual roach with different backgrounds: individuals withprevious opportunity for migration migrating in a familiarenvironment (OF), individuals without previous opportunity formigration migrating in an unfamiliar environment (NU), andindividuals with previous opportunity for migration migrating in anunfamiliar environment (OU)

NU OU OF

Length (mm) 141 6 1 168 6 2 159 6 2Condition(weightresidual)

0.003 6 0.004 0.014 6 0.003 20.022 6 0.003

Days to firstmigration

34 6 5 51 6 3 67 6 2

Days in stream 82 6 16 122 6 7 114 6 8Number ofmigrations

18 6 2 15 6 4 9 6 2

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lake. The proportion of migrants was summarized for eachpopulation and day of investigation. Individual roach bodycondition and length can influence individual migratory be-haviors (Brodersen, Nilsson et al. 2008). In order to elucidatethe influence of such pre-experimental conditions on migra-tion propensity within and between our study populations, weperformed a 3-way logistic regression with individual migra-tion (yes or no) as dependent variable and population origin,individual body condition, and individual body length at timeof tagging as independent factors. Body conditions were mea-sured as the individual residuals from a log total length—logweight regression at tagging for all fish released in LakeSøgard. In order to further explore population differencesin migration patterns, individual cumulative time spent inthe stream (stream residence time) over the migration periodwas calculated for each individual and population. Also, thenumber of migrations in and out of the lake was calculated foreach individual and compared between populations, givinga proxy for differences in individual activity. Migration inci-dents are here defined as events where a fish had passed bothantennas and then been away from the antennas for at least30 min. This was done to avoid inclusion of local movement offish arising from the fish swimming back and forth by theantennas several times during a migration incident.In order to evaluate the role of temperature as a proximate

cue for migration out of the lake, Lake Søgard outlet dailymean temperature was correlated to daily proportions ofOF, OU, and NU fish migrated and Lake Loldrup outlet tem-perature to proportion migrated of the OUorigin fish, usingSpearman Rank Correlations as normality of data could notbe achieved. We focused on autumn migration out of the lakeand analysed data from migration initiation until 31 Decem-ber 2006 in order to avoid effects of, for example, fish mor-tality on migration patterns later in the season. Furthermore,we evaluated overall out-migration patterns between thegroups of fish over the seasonal temperature trends in thelakes. Here, proportions of migrants were summarized intothe dates at which the first individual migrated and the dateswhen 10%, 25%, 50%, 75%, and 100% of the migrants of eachgroup of fish had migrated. Next, the seasonal trend temper-atures at these dates were obtained from a nonlinear regres-sion of temperature decreases between 1 September and 31December. Daily mean temperatures for Lake Søgard andLake Loldrup were regressed over the period-day numbersaccording to the sigmoidal function

Ts ¼ uT

�ezdi

ezdi 1 ezTd

�1 lT ; ð1Þ

where Ts is the overall seasonal temperature trend, z is a pa-rameter estimating the deviation from the null step function,di is a parameter estimating the day number for the functionpoint of inflection (maximum rate of change in Ts), Td is daynumber–specific average temperature, and constants uT and lTrestrict the Ts function to an upper (uT 1 lT) early-season anda lower (lT) late-season temperature level. As 1 of the OF fishmigrated after 31 December , we used the date when 58 of the59 (98%) OF migrants had left the lake (29 December) toenable comparisons during the general out-migration period.

RESULTS

The NU fish from Lake Rønbæk (that lacks opportunity forseasonal migration) showed partial migration when translo-cated to Lake Søgard (Figure 2a), with up to 40% of the fishleaving the lake for the streams during the winter season. TheOU fish translocated from Lake Loldrup showed a migration

pattern more similar to fish originating from Lake Søgard(OF fish) with up to 81% OU fish and 71% OF fish migrating(Figure 2a). Overall, there was a high resemblance in theseasonal migration pattern between OF, OU, and NU fishmigrating in Lake Søgard (Figure 2a). However, the migrationpattern of translocated fish from Lake Loldrup (OU) differedsubstantially from the pattern displayed by the fish migratingin Lake Loldrup (OUorigin) (Figure 2b). More specifically,OUorigin fish migrated out of the lake much earlier in theseason, in a remarkably synchronized fashion, and with a lowerproportion (51%) compared with the translocated OU fish(Figure 2b).The correlation between temperature and proportion of

individuals migrating was high in Lake Søgard (OU fish:Spearman rank correlation rs ¼ 20.91, P , 0.001; NU fish:rs ¼ 20.86, P , 0.001; and OF fish: rs ¼ 20.91, P , 0.001),whereas showing a much lower, but still significant, correlationcoefficient in Lake Loldrup (OUorigin fish: rs ¼ 20.24, P ¼0.008). The seasonal temperature trends were well describedby the nonlinear regression (Equation 1) for both Lake Søgard(di ¼ 50.887 6 0.761, z ¼ 0.072 6 0.004, R2 ¼ 0.949) and LakeLoldrup (di ¼ 43.914 6 0.905, z ¼ 0.073 6 0.004, R2 ¼ 0.925;uT ¼ 12 and lT ¼ 6 for both lakes; Figure 2). The seasonaltrend temperatures, calculated according to Equation 1, at firstoccurrence of migration varied between 14 and 18�C amongthe 4 groups of fish. The OF fish from Lake Søgard, migrating

Figure 2Seasonal patterns of partial migration from Lake Søgard (a) andLake Loldrup (b) related to lake-specific temperatures (thin solidlines). Grey solid curves are seasonal temperature trendsapproximated by nonlinear regression. (a) Percentage of roach fromOU (dotted line), NU (solid line) and OF (dashed line) fish inconnected streams during the migratory period. (b) Percentage ofroach from OUorigin (solid line) fish in connected streams, with themigration pattern of OU fish migrating in Lake Søgard (dotted line)for comparison.


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in their home environment, started and continued their mi-gration at lower trend temperatures (on later dates) than theother groups of fish (Figure 2a and Figure 3). OU, NU, andOUorigin fish initiated migration at very similar seasonal trendtemperatures, whereas the seasonal-trend temperatures fortheir following migrations differed (Figure 3). The majority(75%) of OUorigin migrants migrated at temperatures.14�C, whereas 75% of migrants in Lake Søgard migrated attemperatures below 8�C.When comparing fish with different origins migrating in

Lake Søgard, OF fish migrated later in the autumn than theOU and NU fish (Table 1 and Figure 2a; Kruskal–Wallis teston number of days between day of tagging until first migra-tion for individuals [v2 ¼ 42.2, n ¼ 172; P , 0.001]), in linewith the temperature differences in Figure 3. In the 3-waylogistic regression, the probability of migration was signifi-cantly different between the groups migrating in Lake Søgard(Wald2 ¼ 8.808, P ¼ 0.012), where a maximum of 80.7% ofthe OU fish, 71.1% of the OF fish, and 39.8% of the NU fishwere out of the lake. Individual body condition of the fish atthe time of tagging had no significant influence on the prob-ability for migration (Wald1 ¼ 1.785, P ¼ 0.182) but smallerfish showed a lower migration probability than larger fish(Wald1 ¼ 7.220, P ¼ 0.007). The interactions group 3condition 3 length (Wald2 ¼ 2.317, P ¼ 0.314), group 3condition (Wald2 ¼ 0.947, P ¼ 0.623), and group 3 length(Wald2 ¼ 3.505, P ¼ 0.173) were all nonsignificant and wereremoved from the model.The small-scale temporal changes in proportion of migrants

in Figure 2 are caused by individual fish moving in and out ofthe streams, and this migration activity differed betweenthe Lake Søgard fish groups (analysis of variance [ANOVA],F2,84 ¼ 3.38, P ¼ 0.039). NU fish migrated in and out of thestreams nearly twice as often as the OF fish (Table 1). Streamresidence time (total number of days registered in thestreams) varied among individuals, from less than a day upto 202 days (an OF individual), and also differed between theLake Søgard fish groups (ANOVA, F2,84 ¼ 3.68, P ¼ 0.029;Table 1). NU fish had shorter residence times compared withOU and OF fish (Table 1). The corresponding comparisons

between Lake Loldrup fish migrating in Lake Loldrup (OUor-igin) and Lake Søgard (OU) showed that neither stream ac-tivity (ANOVA, F1,118 ¼ 1.11, P ¼ 0.291) nor stream residencetime (ANOVA, F1,118 ¼ 2.33, p ¼ 0.129) differed betweenOUorigin and OU fish.

DISCUSSION

There was a clear evidence that the overall trait for partialmigration was driven by phenotypic plasticity. The migratorybehavior of the Lake Loldrup fish translocated to Lake Søgard(OU fish) was more similar to the migration behavior of thelocal Lake Søgard OF fish than to the source population inLake Loldrup (OUorigin). Moreover, the NU fish with noprevious migration opportunity did indeed migrate and didso in an overall pattern resembling the other 2 groups. Therewere some differences between local and translocated fish insmall-scale migration patterns, potentially suggesting a geneticinfluence on migration behaviors, but with a minor role forthe expression of the migration trait. Our results thusoverall suggest that the trait for partial migration was plasticand mainly influenced by environmental parameters (e.g.,Lundberg 1988; Olsson et al. 2006).Despite the fact that fish from Lake Rønbæk (NU fish) un-

likely had any experience from seasonal migration before therelease into Lake Søgard, nearly half of the NU fish migratedwhen given the opportunity, albeit with a lower proportioncompared with OU and OF fish. The lower proportion ofNU migrants could potentially be explained by NU fish beingslightly smaller (Table 1) as the probability of migration in-creases with fish size (Brodersen, Nilsson et al. 2008). How-ever, differences in migrating proportions between fishgroups in Lake Søgard remained significant when comparingfish ,15 cm (post hoc; NU ¼ 46%, OU ¼ 77%, OF ¼ 60%;Pearson chi square, v2 ¼ 7.2, n ¼ 122; P ¼ 0.044), excludingthe influence of fish size on this result. The migration of LakeRønbæk fish shows that the trait for partial migration is notlost in populations without a history of migration opportunity.Moreover, the lower proportion of migrating NU fish couldindicate that selection against propensity to migrate may havetaken place in Lake Rønbæk, either due to selection againstmaladaptive trait expression or through random genetic driftrelated to the founding of the Lake Rønbæk population. Thiswould suggest the occurrence of genetic variation behind thepartial migration trait in roach. It should be noted, though,that the origin of the roach that were introduced to LakeRønbæk is unknown and that they could potentially havecome from a lake with migration opportunity. Although evo-lution in fish populations can occur on a contemporary timescale (e.g., 80–120 years, Koskinen et al. 2002), Lake Rønbækis only about 30 years old, and the number of generationsavailable for evolutionary processes to proceed is relativelyrestricted (i.e., for fixation of a nonmigratory genotype). Itis nevertheless clear that the NU fish from Lake Rønbækcould not have migrated before but were still able to migratewhen given the opportunity. However, the NU fish from LakeRønbæk seemed to respond with lower precision to tempera-ture as a proximate cue than the other 2 fish groups migratingin Lake Søgard, as they produced the weakest correlationbetween autumn temperature and migration. This is despitethe fact that NU fish showed a migration pattern strikinglysimilar to the OU fish at the start of the migration period(Figure 2). The striking similarities, however, ended aroundthe start of November when NU fish had lower migrationproportions than OU fish, and further dissimilarities ap-peared towards the end of 2006 (Figure 2). Interestingly,the period November to December showed a relatively highvariation in lake temperatures, without the marked decreasing

Figure 3Seasonal trend temperatures at dates where the first individualmigrated and when 0%, 10%, 25%, 50%, 75%, and 100% of themigrants of each group of fish had migrated. Seasonal trendtemperatures are given via a nonlinear regression of date-specifictemperature decreases between 1 September and 31 December inLake Søgard and Lake Loldrup (see text for further elaboration).


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trend seen during the previous autumn period (Figure 2).This suggests that albeit fish without previous opportunityfor migration are able to track seasonal trends of decreasingtemperatures when migrating, they seem less able to makeprecise migratory decisions during periods with temperaturevariation without overall trends.The onset and extent of partial migration is most likely trig-

gered by 1 or more environmental cues. Our correlation anal-yses show that temperature is involved as a proximate cue forthe migration patterns observed during fall when roach mi-grated out of the lakes, but the importance of the tempera-ture cue appears to be lake specific. Fish migrating from LakeSøgard (both local and translocated) seemed to track andrespond to daily and seasonal temperature changes to a highdegree, whereas fish in Lake Loldrup responded to tempera-ture changes in a synchronized fashion by performing most ofthe migration within a narrow temperature span (just above14�C) in early October (Figures 2 and 3). A somewhat similarbut less pronounced burst of out-migration appeared in LakeSøgard at around 7�C, when the gross remainder of migrantsof the 3 fish groups left the lake. Roach seasonal partial mi-gration patterns hereby differ between lakes with comparableseasonal temperature patterns (Figure 2), and although tem-perature is a likely proximate cue initiating and influencingmigration, it cannot by itself explain the patterns found. Theoriginal approach to explain the phenomenon of roach par-tial migration (Bronmark et al. 2008) identified seasonal tem-perature-dependent changes in roach growth opportunity (G)and predation risk (P) as the ultimate causes. Roach werefound to shift habitat so as to minimize the P/G ratio (cf.Werner and Gilliam 1984). Decreasing lake temperatures dur-ing autumn decreased G more rapidly than P for roach, gen-erating an incentive for roach to leave the lake habitat duringwinter and migrate to connected streams that contain fewerpredators. Temperature is hence a proximate cue that drivesroach partial migration, and different background levels ofG and P should influence temperature-dependent timingand pattern of migration. We propose that this is what causedthe differences in out-migration patterns between LakesSøgard and Loldrup in our study. The theoretical predationpressure in Lake Loldrup is higher than Lake Søgard, whichsuggests that the P/G ratio should reach migration-inducinglevels at higher temperatures assuming that interlake levels ofG are comparable. It should be noted in this context that theimportance of temperature as a proximate cue for partialmigration should be stronger for ectothermal compared withendothermal organisms. Growth potential and predation riskshould be only indirectly affected by temperature in endo-therms, and, hence, migration patterns should be less clearlyrelated to temperature regime.Although a higher density of predators and consequently

P/G ratio could explain the earlier out-migration from LakeLoldrup, it cannot explain the percentages of partial migra-tion displayed in the lakes. About 50% of the tagged fish inLake Loldrup were simultaneously out of the lake shortlyafter the early-November rapid burst of out-migration,whereas about 80% of the translocated Lake Loldrup OU fishwere simultaneously out of Lake Søgard (Figure 2). This iscounterintuitive considering the higher predator densities inLake Loldrup that should stimulate migration. We have noconclusive explanation to this result but suggest that combi-nations of, for example, predation regime, vegetation struc-tural complexity, as well as individual body conditions(Brodersen, Nilsson et al. 2008) could act in different direc-tions on individual migratory decisions, a topic that deservesattention in future studies. Both timing and magnitude ofpartial migration have been shown to have potential impactson lake ecosystem state by affecting spring succession dynam-

ics on roach return migration (Brodersen, Adahl et al. 2008),making our interlake differences interesting above the anec-dotal level.The NU fish translocated from Lake Rønbæk and the OU

fish translocated from Lake Loldrup migrated in the unfamil-iar Lake Søgard environment. Although the NU and OU mi-grants showed early-season migration patterns very similar toeach other, they differed from the local OF fish that initiatedmigration about a month later (Figure 2). This reveals thatinitiation of migration in the translocated fish was not a resultof them simply joining the local fish migration, implying a lowinfluence of social interactions and/or shoal belonging onmigration patterns. The migration patterns of the fish in LakeSøgard furthermore differed at the more detailed level. Theresidence time in the streams as well as the number of migra-tions between the streams and the lake were different betweenthe local OF and the translocated NU fish. We suggest thatthese differences may reflect a more beneficial and perhapsmore optimal migration behavior in the OF fish, originatingfrom experience of migration in the familiar environment.For instance, the lower number of antenna recordings suggesta more deliberate migration behavior of the local OF fish andthereby plausibly reduced exposure to potential predators(e.g., Jacobsen and Perrow 1998). Similarly, by migrating laterin season, the local fish would have been able to forage fora longer period in the lake habitat, which should providemore food compared with the stream habitat (Bronmarket al. 2008) and build up energy stores before migrating. Thisargument assumes that local familiarity involves better knowl-edge of predation risk and foraging opportunity. This couldallow a more fine-tuned departure migration that could ben-efit individuals and in its extension be viewed as a selectivecomponent possibly contributing to local adaptation in migra-tory behavioral decisions. Interestingly, the small-scale migra-tion behaviors did not differ between OU and OUoriginmigrants, potentially supporting the reasoning that thesetraits are at least partially under genetic control. Local adap-tation is defined as genetically based traits that confer higherfitness of local individuals in their native environment com-pared with nonnative individuals in the same environment(Kawecki and Ebert 2004). Local adaptation has been demon-strated in other freshwater and anadromous fish (see reviewsby Taylor 1991 and Adkison 1995), for a number of differentphysiological as well as life history traits, including migrationpatterns (e.g., Adkison 1995; Aarestrup et al. 1999). It is, how-ever, evident that local adaptation is not influencing overallpopulation-specific partial migration patterns in our study.Instead, we observe high plasticity in overall migration behav-iors among populations. This is likely to be a plastic-adaptiveresponse to high between-year variability in temperature, P/Gratios, and other cues within lakes, apparently overriding po-tential costs of maintaining phenotypic plasticity in the migra-tion trait. Nevertheless, the different small-scale migrationbehaviors of the local roach in Lake Søgard suggest that localadaptation could play a role, but if so only minor, in theexpression of the migration trait.Individuals that successfully perform seasonal partial migra-

tion should benefit from their migratory behavior by increasedprobability of survival and reproduction. As our results showhigh plasticity in migration behavior according to environ-mental circumstances, there is great scope for adjustment ofroach migratory behavior to retain these fitness componentsin varying environments. Temperature is 1 major proximatecue for roach partial migration, and the plasticity in responseto temperature and predation/growth conditions suggeststhat partial migration, with its effects on individuals, popula-tions, and potentially systems, will prevail in future scenariosof changing climate.


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FUNDING

Danish Angling License funds.

We thank 2 anonymous referees for useful comments on previousdrafts and Mercy Lard for language proof reading.

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