Population traits of invasive bleak Alburnus alburnus between different habitats in Iberian fresh waters

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Limnologica 46 (2014) 70–76

Contents lists available at ScienceDirect

Limnologica

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opulation traits of invasive bleak Alburnus alburnus betweenifferent habitats in Iberian fresh waters

avid Almeidaa,∗, Paris V. Stefanoudisb, David H. Fletchera, Carlos Rangelc,duardo da Silvac

Centre for Conservation Ecology & Environmental Change, Bournemouth University, Poole, Dorset BH12 5BB, UKSchool of Ocean and Earth Sciences, University of Southampton, Southampton SO14 3ZH, UKDepartment of Anatomy, Cell Biology and Zoology, University of Extremadura, Badajoz 06071, Spain

r t i c l e i n f o

rticle history:eceived 10 July 2013eceived in revised form 29 October 2013ccepted 15 December 2013vailable online 25 December 2013

eywords:quatic conservationioinvasionreshwater fishediterranean ecosystems

eservoiriverpain

a b s t r a c t

The bleak Alburnus alburnus (L.) is a cyprinid native to most of Europe, mainly inhabiting lentic environ-ments. This fish species is a successful invader in the Iberian Peninsula, where it was first introducedto reservoirs as forage fish during the 1990s. Bleaks threaten the highly endemic Iberian fish fauna bymeans of trophic competition and hybridization. Yet, little is known about the environmental biologyof bleaks in the Iberian Peninsula, particularly far from impounded waters. Thus, the aim of this workwas to compare seasonal and gender variation of size structure, body condition and reproductive invest-ment of bleaks between different habitats. Only sexually mature bleaks were seasonally collected andexamined from the River Gévora and the Sierra Brava Reservoir (southwestern Spain) to assess morein-depth the adaptive capacity at the population level and the subsequent invasiveness. Bleak was anabundant species in the fish assemblages of both habitat types (i.e. river and reservoir). The proportion ofsmaller mature bleaks was lower in the river than the reservoir during spring and the opposite patternwas observed during winter. Both male and females were larger in the river during the breeding sea-son in the study areas (i.e. spring), as well as with higher body condition and reproductive investment.

These findings suggest that bleaks enhance their reproduction rate in the river to compensate for highermortality in this habitat, where environmental conditions may be harsher due to the winter floods andsummer droughts typical of Mediterranean water courses. Overall results highlight the high degree ofplasticity in population traits of the bleak in the Iberian Peninsula, which will surely aid its ability to adaptto a wide variety of Mediterranean ecosystems, including lentic and lotic environments. Consequently,this invasive fish may pose a serious risk for the highly valuable fauna of Mediterranean Europe.

ntroduction

Biological invasions are a major driver of biodiversity loss athe global scale (Mooney and Hobbs, 2000; Genovesi, 2005). Inarticular, fish have been introduced worldwide, with adverseffects reported on freshwater ecosystems (Welcomme, 1992;owx, 1998; Rahel, 2002). Several studies have highlighted a vari-ty of serious impacts on native communities by invasive fishia hybridization, disease vector, competition or predation (e.g.eunda, 2010; Ribeiro and Leunda, 2012). This conservation con-ern is especially relevant in the Iberian Peninsula (Almeida et al.,

013a), as fish fauna is highly endemic, with >30% of the nativesh species being confined to this region (Reyjol et al., 2007). Yet,he number of non-native fishes continues to increase in Iberian

∗ Corresponding author. Tel.: +44 01202965384; fax: +44 01202965530.E-mail address: [email protected] (D. Almeida).

075-9511/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.ttp://dx.doi.org/10.1016/j.limno.2013.12.003

© 2013 Elsevier GmbH. All rights reserved.

fresh waters, i.e. >25% of the total fish species (Leunda, 2010), whichare consequently considered a hotspot for fish invasions (Clavero,2011; Almeida et al., 2013a).

The bleak Alburnus alburnus (L.) is a cyprinid native to most ofEurope, mainly inhabiting lentic environments, such as lakes orstill waters in medium-large rivers, where it feeds on invertebratesfrom the water-column or the surface (Freyhof and Kottelat, 2008).In the Iberian Peninsula, reservoirs are important spots for intro-duction of non-native fish, chiefly for species displaying limnophilicrequirements (Godinho et al., 1998; Almeida et al., 2012a,b), asbleaks (Vinyoles et al., 2007). This species was introduced in sev-eral Spanish reservoirs from France in the 1990s as a forage fish forpiscivorous species such as largemouth bass Micropterus salmoides(Lacépède), northern pike Esox lucius L. or pike-perch Sander lucio-

perca (L.) (Elvira and Almodóvar, 2001; Vinyoles et al., 2007), whichare target species for recreational angling. Consequently, bleaks arenow widespread across several Iberian drainages. The main poten-tial cause to explain the success of the bleak in the Iberian rivers

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s the lack of competition from endemic cyprinids, as these fishpecies are well adapted to local conditions and consequently theiriches are rather narrow (Ferreira et al., 2007). Therefore, they cane easily displaced by the opportunistic bleak. As an example, theecline of several populations of the endemic Ebro nase Parachon-rostoma miegii (Steindachner) has been related to bleak presence,s observational experiments demonstrated that overall activityevels and aggression of the Ebro nase is decreased when it cohab-ts with bleak, while an analogous behaviour shift in the bleaks wasot found (Almeida and Grossman, 2012). Moreover, hybridizationhreatens the genetic integrity of Iberian fishes, with a well-knownxample in the endemic Squalius complex, which is disrupted byleak introgression (Almodóvar et al., 2012).

Data on bleak distribution is the only relevant information avail-ble for this fish in the Iberian Peninsula (Vinyoles et al., 2007).owever, specific research on the environmental biology of theleak may contribute to manage this bioinvasion and control thepread throughout Spain and Portugal. In particular, the assessmentf non-native species status between different habitats is crucial torovide accurate insights into their invasiveness in the introducedanges (e.g. Almeida et al., 2012b), with population traits being ofarticular concern to understand how invasive species adapt toative ecosystems (Sakai et al., 2001). However, to our knowledgeo data on population structure of bleaks have been provided for

berian fresh waters and, particularly for this region, such informa-ion would be novel and valuable from habitats clearly differentrom those reservoir-like environments.

In light of the dearth of research on autoecology of invasiveleaks in the Iberian Peninsula, the aim of this work was to compareopulation traits of this fish species between different habitats forhis region. Specifically, we analyzed seasonal and gender varia-ion of size structure, body condition and reproductive investmentn bleak populations from a river and a reservoir located within theuadiana River Basin (southwestern Spain). We hypothesized that:

1) the proportion of smaller size intervals will be lower in the riveruring spring, where environmental conditions (i.e. lower wateremperature and trophic availability, as well as higher predatoryressure and effort due to the current) may promote stronger win-er mortality on the youngest/smallest fish (Hurst, 2007); (2) theroportion, size and reproductive investment of females (i.e. gonadeight) will be greater in the river during spring to better enhance

he reproduction rate and thus compensate for the population’sinter loss (e.g. Rose et al., 2001; Ali et al., 2003); and (3) bleaks willisplay better body condition in the reservoir, where energy expen-iture by fish may be lower due to the lack of current (Almeida et al.,012b) and suitable food resources (i.e. zooplankton) may be moreeadily available for this species.

aterials and methods

tudy areas

The River Gévora (length: 74 km; catchment surface: 983 km2;ltitude range: 1027–170 m.a.s.l.) is a small right-margin trib-tary (wetted width: 3–10 m; water depth: 0.5–2.0 m; annualischarge: 0.5–0.9 m3 s−1) to the River Guadiana (southwesternpain). Bleaks were collected from a 10 km section of the Riverévora: 38◦59′23′′ N–06◦56′02′′ W and 38◦55′14′′ N–06◦57′29′′ W

or the upstream and downstream boundaries of the section,espectively. The Sierra Brava Reservoir (surface: 2005 ha; volume:32 hm3; water depth: 10–20 m; altitude range: 352–303 m.a.s.l.)

s located on the River Ruecas (39◦13′36′′ N–05◦38′06′′ W), a right-argin tributary to the Guadiana River. These two study areas were

elected because bleak abundances were high enough to achieveepresentative sampling sizes, while avoiding the effect of fish

ica 46 (2014) 70–76 71

removal on the population traits throughout the study period. Also,the accessibility to the sampling sites was easy with all the samplingequipment. Moreover, bleaks were virtually confined to each par-ticular habitat type (i.e. no water impoundments nearby the studyriver section, and the dam and unsuitable tributaries for bleaks inthe study reservoir). Thus, the effect of each habitat type (i.e. eitherriver or reservoir) on bleak population traits was more integrallyassessed by controlling the effect of fish movements/migrationsfrom other different habitats adjacent to the study areas. Despitethe distance between the river section and the reservoir (around100 km), all these above advantages justified the selection of thesetwo study areas. Furthermore, the assessment of population traitsbetween selected different habitats have previously been shown asappropriate to reveal wide ranges of phenotypic plasticity in otherinvasive fish species, although the study areas were not spatiallyclose (e.g. Almeida et al., 2009, 2012a,b).

Substratum in the study areas is siliceous, with Precambric andPalaeozoic slates and quartzites. The climate in this region is con-tinental Mediterranean, with rainfall concentrated in autumn andwinter (800–1000 mm) and intense summer drought (<500 mm).The average annual temperature ranges between 10 and 15 ◦C. Thelowest temperatures occur in winter (−5 ◦C) and the highest insummer (45 ◦C). Riparian vegetation mainly consists of narrow-leafed ash Fraxinus angustifolia Vahl, willow Salix spp., commonalder Alnus glutinosa (L.), poplar Populus spp. and bramble Rubusspp. Aquatic vegetation consists of macrophytes such as watercrowfoot Ranunculus spp., rushes Juncus spp. and Scirpus spp., aswell as freshwater weeds of the genera Chara and Spyrogira. Theland use is mainly for agriculture and cattle rearing.

The River Gévora and the Sierra Brava Reservoir were locatedin the middle part of the same catchment (Guadiana RiverBasin) and consequently fish assemblage composition was sim-ilar (Table 1). Specifically, potential competitors for the bleak inboth study areas are endemic cyprinids, such as calandino Squaliusalburnoides (Steindachner) and Iberian arched-mouth nase Ibe-rochondrostoma lemmingii (Steindachner), and most importantlyother abundant non-native species, eastern mosquitofish Gambusiaholbrooki Girard and pumpkinseed Lepomis gibbosus (L.). Predatorsfor the bleak are northern pike and largemouth bass, with thislatter species being the most abundant piscivorous fish in bothhabitats (Table 1). Non-fish species that can potentially exert pre-dation pressure on bleak are grey heron Ardea cinerea L., little egretEgretta garzetta (L.) and the Eurasian otter Lutra lutra (L.), althoughall these predators are much more abundant in the river habitat (D.Almeida, pers. observ.). Regarding trophic availability for the bleak,the annual mean abundance of zooplankton is 32 mg m−3 in theriver and 53 mg m−3 in the reservoir; and the annual mean abun-dance of benthic invertebrates is 7 g m−2 in the river and 3 g m−2 inthe reservoir (Fletcher et al., 2013).

Field sampling and laboratory procedures

Fish were collected from April 2007 to February 2008. This wasa hydrologically average period for the study areas (Ministry ofEnvironment Spain, 2013), which avoids the effects of particular dryor wet years and allows data to be considered as representative forthis species in the Mediterranean region of the Iberian Peninsula.To achieve an accurate assessment of the seasonal effect on popu-lation traits, surveys were carried out at each habitat in April–May2007 for spring, July–August 2007 for summer, October–November2007 for autumn and January–February 2008 for winter. Also, sur-veys were evenly distributed across the study areas. Specifically,

a total of 44 surveys (11 sites × 4 seasons) were carried out inthe river and 32 (8 × 4) in the reservoir. Moreover, surveys wereundertaken in the morning, when bleak activity is at its maximum(Prchalová et al., 2010). To encompass the existing environmental

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72 D. Almeida et al. / Limnologica 46 (2014) 70–76

Table 1Fish abundances per species and by habitat type. Species richness is also shown. Results are means ± SE. Species in grey are non-native.

Fish abundances (CPUE, ind. 100 m−2) Habitat type

River Reservoir

Allis shad Alosa alosa (L.) 0.07 ± 0.07 –Northern pike Esox lucius L. 0.09 ± 0.07 0.23 ± 0.09Iberian long-snout barbel Luciobarbus comizo (Steindachner) 1.44 ± 0.72 0.38 ± 0.19Iberian small-head barbel Luciobarbus microcephalus (Almac a) 0.60 ± 0.17 0.06 ± 0.04Southern Iberian barbel Luciobarbus sclaterii (Günther) 0.07 ± 0.05 0.23 ± 0.14Unidentified barbel Luciobarbus spp. 3.26 ± 1.67 3.58 ± 2.00Goldfish Carassius auratus (L.) 0.40 ± 0.21 0.29 ± 0.19Common carp Cyprinus carpio L. 0.51 ± 0.18 3.55 ± 1.59Gudgeon Gobio gobio (L.) 0.37 ± 0.31 –Jarabugo Anaecypris hispanica (Steindachner) – –Calandino Squalius alburnoides (Steindachner) 1.33 ± 0.90 1.06 ± 0.83Southern Iberian chub Squalius pyrenaicus (Günther) 0.14 ± 0.10 0.03 ± 0.03Iberian arched-mouth nase Iberochondrostoma lemmingii (Steindachner) 1.33 ± 0.89 1.35 ± 1.29Southern straight-mouth nase Pseudochondrostoma willkommii (Steindachner) 0.26 ± 0.23 2.90 ± 1.93Southern Iberian spined-loach Cobitis paludica (de Buen) 0.51 ± 0.31 0.19 ± 0.14Black bullhead Ameiurus melas (Rafinesque) 0.21 ± 0.09 0.77 ± 0.55Eastern mosquitofish Gambusia holbrooki Girard 17.30 ± 3.45 25.35 ± 9.79Pumpkinseed Lepomis gibbosus (L.) 13.84 ± 2.90 24.71 ± 6.9Largemouth bass Micropterus salmoides (Lacepède) 2.88 ± 1.10 4.13 ± 1.91

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Freshwater blenny Salaria fluviatilis (Asso)

Bleak Alburnus alburnus (L.)

Fish richness

ariability at each site, fish were collected from all mesohabitatsresent in both river (runs, riffles and pools) and reservoir (lit-oral and limnetic zones), thus obtaining a representative samplef bleaks along a wide size range from the two habitat types. Theost appropriate catch methods were used to thoroughly sam-

le every habitat. We used electrofishing (2000 W DC generatort 200–250 V, 2–3 A) along with dip nets (1.5 m long pole, 30 cmiameter net, 10 mm mesh size) in the river, following a zigzagingnd upstream direction at each site (25–30 m river long, 30–40 miner site). We sampled the reservoir using two boats to seine net30 m × 5 m, 10 mm mesh size) in the limnetic zone and electrofish-ng for the littoral zone (the same procedure and equipment asescribed above for the river sampling). At each sampling site, theotal area surveyed was recorded for subsequent abundance calcu-ations.

After each survey was concluded, bleaks were immediatelymmersed in an overdose solution of anaesthetic (MS-222) for5 min followed by severance of the spinal cord. The individualsere stored in ice during transport to the laboratory. Individuals of

he remaining fish species were counted and kept in a tank withupplied oxygen (2 aerators Aera, portable battery pump) untilully recovered before being released. All field procedures compliedith animal use and care regulations of Europe and Spain (specific

icences were granted for Scientific Field Research in Extremadura,pain). Fish were collected by trained personnel (i.e. the holder ofhe Licences, E. da Silva). Thus, no adverse effects were caused onhe wildlife in the study habitats and all non-target fish recoveredully from the anaesthetic.

On the arrival at the laboratory, the bleaks were frozen (−20 ◦C)ntil processing and then measured for standard length (SL,1 mm). This particular fish length was the only measure of sizesed for data analyses, as it avoids noise given by variation ofaudal fin length not related to body size (e.g. wounds and cutsn the fin skin and rays). Only sexually mature individuals weresed for data analyses, as traits of this (mature) population fractionre potentially more related to the adaptive capacity of non-nativesh, as well as their subsequent invasiveness and ecological impactVila-Gispert et al., 2005). Thus, fish were dissected to examine

he gender and sexual maturity. To decide the minimum size ofexual maturity within each gender, smaller fish from the spawn-ng period (i.e. from April to May in the study areas, E. da Silva,ers. observ.) were classified as mature males by detecting nuptial

0.10 ± 0.10 –9.67 ± 1.93 19.58 ± 6.294.12 ± 1.95 4.23 ± 2.09

tubercles on the skin. We had previously checked in the field thatseveral small males with tubercles could expel milt under slightabdominal pressure. Regarding females, small individuals of thisgender were classified as mature if their ovaries contained yolkedeggs (e.g. Tarkan et al., 2009). After examinations, a total of 1096mature individuals (n = 373 from the river and n = 723 from thereservoir, >80 mm SL) were also measured for eviscerated weight(We, ±0.01 g) and gonad weight (Wg, ±0.1 mg) by using electronicbalances.

Data analyses

Data were transformed by using ln (x + 1). Assumptions of nor-mality of distributions and homogeneity of variances were verifiedthrough Shapiro–Wilk and Levene’s tests, respectively. All statisti-cal analyses were performed with SPSS v.19 (SYSTAT Software Inc.,Chicago, USA). The significance level was set at = 0.05.

For descriptive purposes, abundances of fish assemblages werecalculated as Catch Per Unit Effort (CPUE, ind. 100 m−2) for eachsampling site and then averaged for every habitat (Table 1). Fishcommunity species richness was also calculated per sampling siteand averaged for every habitat. Size structure was examined bymeans of frequency distributions using 10 mm SL intervals, startingwith the smaller size interval for which shorter mature individualswere found (i.e. 81–90 mm SL). Differences in size structure wereassessed between habitats by using chi-squared (�2) tests for everyseason. Log-linear analysis was used to test male-to-female devia-tions from parity across habitats and seasons, as well as to assessthe interaction of these two factors on sex-ratio. Two-way anal-ysis of variance (ANOVA) was performed to compare the size ofbleaks between habitats, seasons and their interaction, with thedependent variable being the SL. Post hoc Tukey–Kramer honestlysignificant difference (HSD) tests were used to compare mean SLamong groups per habitat or season. Gender was not consideredas a factor within this analysis to avoid unnecessary complexityof the model (i.e. a three-way ANOVA) and thus increase the sta-tistical power of the remaining sources of variation, which wouldotherwise be seriously compromised. Consequently, results from

two-way ANOVAs on SL were shown for each gender separately.Body condition and reproductive investment were assessed byusing data from spring in order to include only the spawning periodand thus reveal clearer variation patterns of these population traits

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reproductive investment (F1,323 = 0.22, P = 0.64). Thus, the patternsof variation showed a similar rate (i.e. the slope) between gendersat each habitat for every parameter, with males and females dis-playing higher We and Wg in the river (Fig. 3). Remarkably, females

Table 2Sex-ratio (males/females) of bleak by habitat type for every season.

Habitat type Season

SL (mm)

Fig. 1. Size structure of bleak by habitat type for every season. River: open b

etween habitats. Specifically, two-way ANCOVAs (covariate: SL)nd subsequent Tukey–Kramer HSD tests were used, with habi-at type and gender as the factors. To provide a more integratedmpression of true body condition, the dependent variable was

e to avoid bias from the weight of gonads and gut contentse.g. Godard et al., 2013). The dependent variable for reproductivenvestment was Wg. In both cases (i.e. condition and reproduction),he effect of fish size was controlled by using SL as the covariate. Thispproach, i.e. the use of fish length as the covariate, is statisticallyreferable to control the effect of size, instead of using the residualsrom linear regressions between the body/gonad mass and the sizeGarcía-Berthou, 2001) or computing indices/ratios (e.g. Fulton’sondition factor, Gonadosomatic index) (Packard and Boardman,999; García-Berthou, 2001).

esults

Fish community species richness was similar between the rivernd the reservoir, with several non-native species in both habitatsTable 1). Bleak was an important species among the fish assem-lages from the river and the reservoir, with only pumpkinseed L.ibbosus (L.) and mosquitofish G. holbrooki Girard, both invasives,eing more abundant (Table 1). Significant differences in size struc-ure were found between habitats in all seasons. In particular, theroportion of smaller size intervals was lower in the river thanhe reservoir during spring (�2

6 = 134.22, P < 0.001) and the oppo-

ite pattern was observed during winter (�2

7 = 103.74, P < 0.001)Fig. 1). A bimodal distribution (i.e. two mature cohorts) was foundn the bleak size structure from the reservoir during autumn and

inter. This bimodal distribution was also observed in the river

SL (mm)

eservoir: full bars. Chi-squared statistics and significance levels are shown.

population, although less apparent in winter, with a likely secondmode on the 121–130 mm SL interval, corresponding to the cohortof larger individuals (Fig. 1). The final model obtained from the log-linear analysis included the interactions gender × habitat (partialassociation: G1 = 8.74, P = 0.003) and gender × season (partial asso-ciation: G3 = 76.38, P < 0.001). Specifically, sex-ratio was stronglybiased to the males in both habitats during spring and the riverduring winter (Table 2). Females were more abundant than malesin the river during autumn (Table 2). Significant interactions werefound between the factors habitat and season for the size of bleaksin both males (F3,645 = 51.93, P < 0.001) and females (F3,435 = 44.87,P < 0.001). Males were larger in the river during spring, but smallerthan in the reservoir in winter. Females were larger in the river dur-ing spring and summer, but smaller than in the reservoir in winter(Fig. 2). In the river, both males and females were smaller duringwinter than the rest of seasons, whereas SL was lower in the reser-voir during spring (Fig. 2). No interactions between habitats andgenders were found for body condition (F1,323 = 0.47, P = 0.49) and

Spring Summer Autumn Winter

River 3.1 0.9 0.6 2.2Reservoir 3.3 1.1 1.1 0.8

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74 D. Almeida et al. / Limnologica 46 (2014) 70–76

90

100

110

120

130

winterautumnsummerspring

90

100

110

120

130

winterautumnsummerspring

SL (

mm

)

males

females

a

a

1 1

a

a a

1 1

2

Fig. 2. Bleak size (SL, mm) between habitat types and seasons. River: open cir-cles and dashed lines; Reservoir: full circles and solid lines. Each gender is shownseparately. Results are means ± SE, after two-way ANOVAs. Significant differences(Tukey–Kramer HSD tests) are indicated by: (a) river > reservoir in spring for males;(a) reservoir > river in winter for males; (1) spring < summer, autumn, winter in thereservoir for males; (1) winter < autumn, summer, spring in the river for males; (a)river > reservoir in spring for females; (a) river > reservoir in summer for females;(tf

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Fig. 3. Eviscerated weight (We) and gonad weight (Wg) between habitat types andgenders. River: open circles and dashed lines; Reservoir: full circles and solid lines.Results are adjusted means ± SE, after two-way ANCOVAs (covariate: SL). Signif-icant differences (Tukey–Kramer HSD tests) are indicated by: (a) river > reservoirmales for We; (a) river > reservoir females for We; (1) females > males in the riverfor We; (1) females > males in the reservoir for We; (a) river > reservoir males for

a) reservoir > river in winter for females; (1) spring < summer, autumn, winter inhe reservoir for females; (1–2) winter < autumn < summer, spring in the river foremales.

howed higher body condition and reproductive investment thanales did in both habitats (Fig. 3).

iscussion

Since its introduction 20–25 years ago in the Iberian Penin-ula, the bleak has proven to be very invasive, displaying a highpread rate and displacing native species (Vinyoles et al., 2007;ibeiro et al., 2008). Consequently, it is currently a typical species

n the fish assemblages of this region (Carol et al., 2006; Maceda-eiga et al., 2010). This was also observed in the present study,here only other two successful invaders, eastern mosquitofish

nd pumpkinseed, were more abundant, probably because of aigher colonizing potential (García-Berthou et al., 2005; Copp andox, 2007). Regarding the environmental biology of bleaks, resultshowed that this species can reach high abundances under differ-nt conditions of the habitat features, with this ecological aspecteing similar to other invasive fishes in the Iberian Peninsula, ashown by Almeida et al. (2009, 2012a,b). Thus, despite bleak beingonsidered as a limnophylic species (e.g. inhabiting reservoir-likeabitats), the present study showed that bleak also develop well in

otic environments (e.g. streams), where they may diversify theiriet and change prey items from zooplankton in still-waters to

enthic invertebrates in flowing-waters (Fletcher et al., 2013). Thisarticular dietary shift has been shown as advantageous for thestablishment of other invasive fish (see Almeida and Grossman,013 for an example in largemouth bass). These findings confirm

Wg; (a) river > reservoir females for Wg; (1) females > males in the river for Wg; (1)females > males in the reservoir for Wg.

the wide phenotypic plasticity of habitat requirements displayed bybleak in novel habitats, which is a common trait of invasive speciesand surely facilitates the invasion process (Agrawal, 2001).

We found support for our first hypothesis on a higher effect ofwinter mortality in the bleak population from the river. However,a more accurate analysis of results indicated that smaller individ-uals, within the mature fraction of the bleak population, were notthe main size intervals vulnerable to winter mortality in both habi-tats. Despite Hurst’s (2007) assertion that most sources of wintermortality (e.g. thermal stress, starvation) tend to select against thesmallest members of the cohort and population, larger individualsmay be more prone to die during winter due to a higher reproduc-tive effort, with the subsequent expenditure of reserves (Hutchingset al., 1999). Thus, this seasonal effect may occur on the bleakpopulation from the study reservoir, as two cohorts were appar-ent in winter, whereas only one cohort was observed in spring,probably as a result from high winter mortality on larger/older indi-viduals. This seasonal variation in the size structure has also beenobserved in lakes across the native range of the bleak (Bíró andMuskó, 1995). In the river, the larger cohort was less obvious duringwinter, which indicates a stronger effect of early winter mortal-ity on this mature cohort than in the reservoir, suggesting moresevere environmental conditions in the river (e.g. lower tempera-tures, higher floods) and/or weaker individuals (survivors from theharsh summer drought, see Magalhães et al. (2007) for some exam-ples). In spring, similar to the reservoir, the smaller cohort grew andeventually resulted in the only cohort during the breeding season.However, growth rate appeared to be higher during late winter andearly spring in the river, as the mode increased two size intervals

from winter (i.e. mode on 91–100 mm SL) to spring (i.e. mode on111–120 mm SL), instead of only one size interval in the reservoir(from 91–100 to 101–110 mm SL). Indeed, the present results alsoshowed greater eviscerated and gonad weights in the river during

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pring. This overall higher development of mature individuals maye a physiological response at the population level to enhance theeproduction rate and thus compensate for the higher mortality inhe river, which has been observed in several fish species, includingyprinids, under adverse environmental conditions (e.g. Rose et al.,001; Ali et al., 2003). This may explain the mismatch of the resultsith our third hypothesis, which predicted a better body condition

f bleaks in the reservoir. Furthermore, we expected a larger sizend reproductive investment only in females from the river duringpring, according to our second hypothesis, but this was also trueor males in the same habitat, highlighting a combined response ofoth genders to withstand poor environmental conditions (Innesnd Metcalfe, 2008).

Thus, these findings could be related to two well-defined pop-lation strategies, adjusted to the higher (i.e. in the river) or loweri.e. in the reservoir) effects of ecological filters during cold, rainyinters and summer droughts in Mediterranean fluvial ecosystems

Gasith and Resh, 1999; Boix et al., 2010). In particular, reservoirsave stable hydrological conditions and are warmer in winter andooler in summer than Mediterranean rivers because of their highater volume (Wetzel, 2001). Indeed, these more stable condi-

ions usually result in higher zooplankton production than in riverabitats (see data on these abundances in the Methods section).pecifically, zooplankton is a major food resource for bleaks, givenhe morphological adaptations of this fish species to feed from theater column and the surface (Vøllestad, 1985). As a consequence,

he survivorship of bleaks may be better in reservoirs compared tohe high winter and summer mortalities of rivers, caused by thenvironmentally harsher conditions. Especially in summer, habitatoss (i.e. by the decrease of water level), oxygen depletion and pre-ation are the main causes of fish mortality in Mediterranean riversMagalhães et al., 2002). For example, herons and otters can exert atrong predatory pressure on endemic fishes of Iberian rivers dur-ng summer (Peris et al., 1995; Ruiz-Olmo et al., 2007; Almeida et al.,012c). However, this pressure specifically for the bleak may be

argely exerted by one of its main predators in the Iberian Peninsula,he largemouth bass (e.g. Almeida and Grossman, 2013), which isell represented in both the river and the reservoir. Consequently,

his piscivorous species could act as a leading factor influencinghe traits of the study bleak populations, as shown elsewhere forimilar predator–prey relationships (e.g. Brönmark et al., 1995).

Regarding sex-ratio, we did not find support for our secondypothesis, with males being much more abundant than femalesere in spring for both habitats. Females may be a preferential prey

or piscivorous predators in spring due to eggs being a valuablenergy source (e.g. Lee et al., 2009) and females may be also easyargets while they are searching for spawning sites (Britton and

oser, 1982; Cunningham et al., 2002). Moreover, Hutchings et al.1999) observed differences between genders in the energy allo-ated to fish reproduction, to the detriment of post-reproductiveurvival, which could be modulated by existing habitat featuresBartelt et al., 2004; Almeida et al., 2013b). Thus, males, exhibitingower body condition than females, may undergo higher mortalityust after summer drought in the river, with female bleaks dying

ore intensely than males later during early winter.In conclusion, the present study highlights the wide plasticity in

opulation traits of the bleak in the Iberian Peninsula, as shown forther invasive fishes in this region (Almeida et al., 2009, 2012a,b).his flexibility provides bleaks with a clear advantage to adapt to

wide variety of Mediterranean ecosystems, including lentic andotic environments. Overall results suggest that the invasivenesss potentially high throughout other Iberian catchments, as this

pecies also develops well under conditions far from reservoirs,ore than expected according to previous data (Vinyoles et al.,

007). This, along with the great range of impacts exerted by theleak, may mean that this bioinvasion poses a serious risk to the

ica 46 (2014) 70–76 75

highly valuable fauna of the Mediterranean Europe (Ferreira et al.,2007; Reyjol et al., 2007).

Acknowledgements

This project was funded by the FEDER programme throughthe Junta de Extremadura (project code: 045/06, 2006–2007). D.Almeida held a postdoctoral grant from the European Commission(Marie Curie IEF, PIEF-GA-2011-298998).

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