1. Introduction
The disruptive effect of fish invasions is of particular conservation concern in the Iberian Peninsula, which is rich in endemisms. Indeed, >50% of native fish species are unique to this region [
1,
2], but the proportion of non-native fishes (>30%) continues to increase [
2,
3]. The bleak
Alburnus alburnus (L., 1758) is a cyprinid species native to most of Europe, from the northern Pyrenees to the Urals. In its native area, bleak inhabit lakes or still-waters in medium/large rivers and feed chiefly on zooplankton [
4,
5,
6]. In the Iberian Peninsula, this species was mainly introduced in reservoirs during the 1990s as a ‘forage fish’ for non-native piscivorous fishes, such as northern pike
Esox lucius L., 1758, largemouth bass
Micropterus salmoides (Lacepède, 1802) or pikeperch
Sander lucioperca (L., 1758) [
7]. Since its introduction, the bleak has displayed a strong invasive character throughout Spain and Portugal, taking advantage of anthropogenic disturbances on Mediterranean freshwater ecosystems [
8,
9,
10]. Moreover, this species threatens several Iberian fishes, mainly through hybridization, trophic competition and behavioral interference (i.e., aggression) [
3]. This is because Iberian fish communities have low diversity and are poorly adapted to a such invasion level of non-native fishes [
1], which usually displace native species from available resources. As an example, direct observations by snorkeling have clearly shown that foraging behavior of endemic Ebro nase
Parachondrostoma miegii (Steindachner, 1866) is disturbed by bleak [
11]. All this information on bleak traits (e.g., spread capacity, environmental impacts) allows to consider this species as a clear invasive fish of high ecological risk in Iberia [
2,
12]. However, the available information on bleak dietary traits in the Iberian Peninsula corresponds to a few particular sites only [
13,
14], with no study comparing data at the scale of this entire ecoregion. This would be of particular interest to reveal macroecological patterns (e.g., latitudinal gradients). Indeed, dietary traits of non-native fish can show wide variability under contrasting ecological conditions [
14,
15,
16] and this has implications from a conservation perspective. Thus, a better understanding of dietary data can be used by policy-makers and environmental managers to assist monitoring programs in identifying which other areas are likely to be colonized by this invasive species [
2]. Therefore, the information in the present paper is highly relevant to understand invasion features of this fish species throughout Iberian freshwaters.
Consequently, the aim of the present study was to assess the interpopulation variability in dietary traits of invasive bleak across the Iberian Peninsula. For this purpose, bleak populations were compared among the main rivers within this region, along with a native bleak population from France. Specifically, diet composition was analyzed by means of two overall indices: percentages of occurrence and ingested mass; and four dietary parameters were examined: ingested mass, prey richness, trophic diversity and trophic niche breadth.
3. Results
Diptera larvae (e.g., Chironomidae and Simuliidae), zooplankton (e.g., Cladocera water fleas) and detritus were the most frequent food categories for the reference native population (i.e., the River Saône), both in terms of occurrence and ingested mass (
Table 1). The Ebro population showed a similar diet composition as per native bleak, although Ephemeroptera and Plecoptera nymphs were also important prey items. For the rest of study rivers, percentages of food categories were highly variable (
Table 1). More in detail to be highlighted per river: vegetation and other benthic invertebrates (e.g., freshwater snails) were frequent in the River Tagus; flying insects (e.g., wasps, mosquitoes or butterflies) and Diptera larvae were important in the Guadiana and Segura populations, respectively; benthic invertebrates (e.g., Diptera larvae, insect nymphs, Mollusca) and nektonic insects (e.g., water boatmen or predatory beetles) were very important in terms of ingested mass (>40% and ≈20%, respectively) for the River Guadalquivir. Detritus was an important food category for all bleak populations: 21–42% in occurrence and 13–27% as ingested mass (
Table 1).
Regarding dietary parameters and after accounting for fish length, significant differences were found between bleak populations for ingested mass (F
5,812 = 32.94,
p < 0.001). Four distinct groups were found (from low to high adjusted mean): Saône/Segura (≈12 mg), Guadalquivir (≈25 mg), Guadiana (≈40 mg) and Tagus (almost 60 mg) (
Figure 1a). Differences were also found for prey richness (F
5,812 = 18.68,
p < 0.001). Two river groups were found: Ebro/Saône (
S ≈ 3–4 prey items) and Guadiana/Guadalquivir/Tagus (
S ≈ 5 prey) (
Figure 1b). Significant differences were found between populations for trophic diversity (F
5,812 = 19.76,
p < 0.001). Two river groups were found: Saône/Ebro/Guadalquivir (
H’ ≈ 1) and Guadiana/Tagus (
H’ > 1.5) (
Figure 1c). Significant differences were also observed between rivers for trophic niche breadth (F
5,812 = 20.49,
p < 0.001). Two distinct groups were found: Saône (
B ≈ 1.4) and Tagus/Guadiana (
B > 2); while the remaining three rivers showed intermediate
B values (1.6–1.7) (
Figure 1d).
4. Discussions
Given that the bleak mainly inhabits stillwaters in its native area, this species is well-adapted to play an ecological role as an openwater feeder, with diet being chiefly based on zooplankton [
4,
5]. Similarly, planktonic Crustacea were very important for native bleak in the River Saône. However, the main food categories were Diptera larvae and detritus (i.e., benthic food items) for this reference population. This discrepancy between scientific literature and the present results for the native area was probably because most studies on bleak have been performed in lakes and reservoirs (e.g., Vinni et al. [
4]; Vašek and Kubečka [
5]), whereas bleak diet has received less attention in flowing waters. However, even in lentic environments, bleak can modulate this zooplanktivorous strategy at each particular habitat patch to increase resource partitioning and consequently, reduce competition with coexisting cyprinid fishes, such as roach
Rutilus rutilus (L., 1758) or freshwater bream
Abramis brama (L., 1758) [
4,
5]. Dietary indices were more similar between the River Saône and the River Ebro, the (geographically) closest study area to the reference population. This was also observed by Latorre et al. [
26]) for other biologic traits (i.e., growth and reproduction), which was explained in terms of climatic and hydrological ‘proximity’. However, the intake of Diptera larvae and insect nymphs was different between the Saône and Ebro populations. In the River Saône, particle size was finer (see Methods section), with these bed conditions being very suitable for Diptera larvae (J. Cucherousset, pers. obs.), whereas substrate was coarser in the River Ebro (see Methods section), providing a high availability of nymphs (R. Miranda, pers. obs.). Other food items were prominent among the study populations, including a wide variety of trophic resources in terms of contrasting ecological features: vegetation, neuston, nekton and benthos. Thus, consumption of algae and plant material was higher in the River Tagus. In this respect, Vinni et al. [
4] demonstrated that intra- and mainly inter-specific competition were key causes to understand this result (i.e., high use of vegetation) in the native area. In relation to this finding, Tagus River showed the highest value for ingested mass, resulting in only one ‘statistical group’. This may compensate a higher proportion of vegetation in the diet (see Results above). As a support for this interpretation, Latorre et al. [
26] did not find any effect of this ‘low nutritious’ feeding type (vegetation) on the growth rate in the River Tagus, with this population showing the highest values. Particularly for detritus, bleak showed a high consumption in the study Iberian rivers, which was also found elsewhere within this ecoregion, from streams to reservoirs [
13,
14]. As a potential explanation, bleak may accidentally ingest plant material and detritus while feeding on sheltered invertebrates (D. Verdiell-Cubedo, pers. obs.). In the Guadiana population, bleak took advantage of prey from the water surface, such as fallen flying arthropods (D. Almeida, pers. obs.), which results in a low effort in terms of energy investment. Bleak caught prey from the water column in the River Guadalquivir, with this population displaying a ‘costlier’ foraging alternative, as nektonic insects (e.g., adult Dytiscidae beetles) require higher pursuit and capture efforts. However, more important, bleak fed on a great variety of benthic prey, from insect nymphs and larvae to mollusks and annelids, in all river populations. This finding indicates an elevated capacity of this fish to use food resources apparently less suitable to its morphologic adaptations (e.g., conspicuous superior mouth). Overall, these results suggest that bleak could deeply change the foraging strategy, from a ‘pelagic’ to a ‘benthic’ feeder, even within the same population (see Results for benthos and nekton in the River Guadalquivir). This capacity may aid bleak to better thrive in contrasting Iberian rivers, where zooplankton availability may be a more limited trophic resource [
14]. Such a significant dietary shift has been also observed in the Iberian Peninsula for other invasive fishes adapted to a more stable hydrological regime in their native ranges, although they are phylogenetically and geographically very ‘distant’ to the bleak (e.g., North American centrarchids, see Almeida et al. [
16]).
Regarding dietary parameters, variation ranges for the four examined predictors were similar as per other study areas in the Iberian Peninsula (Latorre et al. [
13] in the NE; Almeida et al. [
14] in the SW). The present data were obtained from large rivers and the just mentioned studies included streams and reservoirs. Thus, these overall results indicate that Iberian bleak populations possess a high capacity of adapting to the particular habitat conditions where this invasive fish inhabits. No clear pattern was observed for any dietary parameter in relation to the year of introduction, which was in accordance with Latorre et al. [
26] for growth and reproduction traits. This lack of relationship is probably because the establishment stage was reached in a few years after bleak introductions (e.g., Bøhn et al. [
27]). As an example, a rapid and wide establishment of this species has been recently demonstrated in the River Segura [
10]. Nevertheless, it must be clearly stated that data were limited (
n = five Iberian rivers). However, unlike the year of introduction, the foraging strategy appeared to show a slight relationship with the latitudinal gradient, specifically a unimodal response [
28], with Guadiana and mainly Tagus reaching the maximum values for all dietary parameters. In addition, the Tagus population showed the highest backcalculated lengths at all ages and growth index among the same study rivers (see Latorre et al. [
26]). A potential explanation is that bleak may be more favored by a moderate Mediterranean climate in central Iberia during the prespawning period (warmer) than temperate conditions in the native area (colder). Yet, bleak are affected by slightly more ‘severe’ ecological conditions in southern Iberia, e.g., oxygen level was lower because of higher temperature (physicochemical data not shown, but in accordance with the expected latitudinal gradient) [
29]. More in detail, these ‘benign’ conditions in central Iberia may improve the physiological status (e.g., metabolic rate) of bleak, which facilitates this fish species to use alternative prey and widen its diet, with the corresponding increase in the trophic variability. In contrast to this ‘generalist’ strategy, more northerly and southerly populations (i.e., distant from the optimum in terms of habitat quality, see theoretical aspects in Oksanen and Minchin [
28]) displayed a more ‘specialist’ strategy, reducing the complexity of diet composition. Nevertheless, these ecological interpretations must be understood with caution, as similarly to the previous statement, data were limited to a few locations (
n = five Iberian rivers) and moreover, the assessed latitudinal amplitude was relatively narrow (only 10° of Latitude, 37–47° N).
Ecological responses such as dietary traits usually show wide variability in non-native species when invading new habitats, with this being particularly clear in freshwater fishes [
13,
15,
16]. In the Iberian Peninsula, invasive fishes usually display wide trophic plasticity under contrasting environmental conditions, which contributes to improve their invasion process [
3,
13,
14]. Accordingly, dietary traits were clearly variable among the study rivers, indicating a wide ‘flexibility’ in bleak foraging strategies dependent on particular river conditions (i.e., habitat heterogeneity, food supply). Studies on bleak diet exist across Iberia in which resource availability were not assessed [
13,
14]). However, other studies on feeding habits of invasive fishes truly estimated food supply as a measure of trophic resources in this ecoregion (e.g., Almeida et al. [
16,
30]), comparing this availability to the use (i.e., bleak diet), and specifically calculating electivity indices (i.e., selection). The present study did not assess resource availability because of technical restrictions (in terms of materials and personnel) to properly quantify the biomass of plant, benthos and plankton in large rivers, which poses a strong study limitation. Thus, abundance of contrasting food items is a key factor to be analyzed for future research on bleak invasion. Similarly—as per other biologic attributes (e.g., growth and reproduction)—the high interpopulation variability is considered a mechanism for bleak to successfully invade novel Mediterranean freshwater ecosystems, from streams to large rivers [
8,
10,
26]. Indeed, Iberian endemic species are specialized to narrow trophic niches [
1] or alternatively, these fishes may display high plasticity to the natural variability in Mediterranean rivers. Irrespective of this specific mechanism, the low level of coevolutionary competition is a potential cause why Iberian fish fauna is not adapted to strong invasive competitors, such as bleak. This is one of the main reasons to consider this fish species as a bioinvader of high risk in the Iberian Peninsula (see
Table 1 in Almeida et al. [
2]). Consequently, environmental managers should apply urgent conservation measures to control bleak populations across Iberian freshwaters. First, these measures should focus on the target species (i.e., fish culling). Second—and according to other studies on bleak in Iberian waters [
9]—actions on aquatic habitats should be implemented to restore the ‘Mediterranean conditions’ of natural flow regimes that benefit native fish communities and hamper invasive species.