Open Access
Knowl. Manag. Aquat. Ecosyst.
Number 417, 2016
Article Number 36
Number of page(s) 7
Published online 14 October 2016

© N. Top et al., Published by EDP Sciences 2016

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1 Introduction

Freshwaters are amongst the most impacted ecosystems in the world and are being continuously affected by increased rates of introduction of non-native fish (Marr et al., 2013). These introductions can occur either intentionally or accidentally, and are mainly the result of fisheries establishment, release of ornamental and bait fishes, or biomanipulation (Jackson and Grey, 2013; Tarkan et al., 2015). Although impacts of introduced non-native fish to the native fauna can occur in several ways, species-specific competition for habitat and food resources in the recipient environment is quite common (Cucherousset and Olden, 2011; Vilizzi et al., 2012; Paterson et al., 2015). For this reason, studies on habitat interactions of non-native species with native faunas can provide crucial insight into the long-term dynamics of species interactions within ecosystems (Lodge, 1993). Also, the invasion success of an introduced species in a new environment depends on its ability to adapt and use local resources (Fausch et al., 2001; Guo, 2006), and non-native fish species may cause a shift in local species community structure (Werner, 1984). Clearly, all of these aspects make the understanding of fish–habitat relationships a crucial requirement (Yamazaki et al., 2006).

An introduced species of particular interest is the North American pumpkinseed Lepomis gibbosus. Following its introduction to Europe in the late 1900s as an ornamental fish for estate ponds, it was first found in Turkish inland waters of the Thrace Region (European part of Turkey) in the early 1980s (Erk'akan, 1983; Baran and Ongan, 1988). In the 2000s, the species was introduced to Anatolia (Asian part of Turkey: Özcan, 2007; Ağdamar et al., 2015), and more recently the number of L. gibbosus populations in Turkish waters was reported to have increased (Tarkan et al., 2015). Whilst in southern Europe L. gibbosus has become a successful invader responsible for detrimental effects on the native fish fauna (Cucherousset et al., 2009), for Turkish inland waters it is still regarded as a ‘potential’ invader (Tarkan et al., 2015). This is because little information is available on its (putative) impacts on the native biota in a country characterised by a very rich endemic freshwater fish fauna (≈322 species in total, of which 215 or 66.8% endemic: Freyhof et al., 2014).

In general, pond-dwelling populations of L. gibbosus have been studied more frequently whereas studies of stream-dwelling populations remain scarce. The latter studies have usually provided contrasting conclusions suggesting either potential ecological consequences or relatively harmless impacts (Godinho et al., 1997; Gutiérrez-Estrada et al., 2000; Villeneuve et al., 2005; Cucherousset et al., 2009; Almeida et al., 2014). However, despite the species' long-time presence in Europe and its fast spread across Anatolia, there have been only few studies on its habitat interactions in this area and virtually none in southern Europe (Gkenas et al., 2016).

Although early studies suggested that L. gibbosus displaced native Eurasian perch Perca fluvatilis in France (Roule, 1928, 1935), these were not quantitatively substantiated and later research has not provided support to this hypothesis (e.g. Copp, 1989a, 1993). The first detailed study on the habitat use of L. gibbosus and its interactions with native fish species was undertaken in a small river catchment of southern England (Klaar et al., 2004), where escapee L. gibbosus from floodplain ponds and reservoirs have become established. This and follow-up studies (Vilizzi et al., 2012; Stakėnas et al., 2013) revealed strong habitat associations between L. gibbosus and native brown trout Salmo trutta, but suggested little or no impact (Gkenas et al., 2016). Although these reports are usually from lentic systems (Cucherousset et al., 2009), a recent study from a stream system in Spain revealed adverse aggressive impacts by L. gibbosus on non-native crayfish and especially endemic fishes and frogs (Almeida et al., 2014). However, except for circumstantial evidence on the displacement of native Iberian stream fish by L. gibbosus (Prenda et al., 2006; Ferreira et al., 2007), there has been no direct and detailed study on the habitat use and interactions of L. gibbosus with native or endemic species in the southern Mediterranean Region and particularly in Anatolia, where successful reproduction of L. gibbosus as a result of high water temperatures in streams is known to occur.

To fill this knowledge gap, the aim of the present study was to assess the habitat use of L. gibbosus in association with other fish species in a temperate stream characterised by a Mediterranean climate and high fish diversity with several non-native and endemic species. It was hypothesised that the high water temperatures and rich biodiversity of the stream would result in strong habitat interactions between L. gibbosus and the native species. The present findings will also contribute to identify the preferred habitat structure of L. gibbosus that allows for nest creation, which favours the species' successful reproduction and likely interactions with the recipient native fish (Copp et al., 2010).

2 Materials and methods

2.1 Study area and sampling

Sarıçay Stream flows into the Gulf of Güllük through the Muğla-Milas region in south-west Anatolia (Fig. 1). The stream is ≈80 km long, the average width of the river bed is ≈10 m, and it hosts different habitat types (predominantly sand, gravel, mud and stone, and rock). Mean water temperatures change seasonally from an average of 25.2 °C in summer, 20.2 °C in autumn, 9.8 °C in winter, and 13.3 °C in spring. Two large reservoirs have been constructed along the stream's course and there are also small ponds formed by disused sandpits. The stream fish fauna includes both endemic (i.e. loach Oxynoemacheilus sp., Smyrna chub Petroleuciscus smyrnaeus, Aegean chub Squalius fellowesii) and non-native fish species (i.e. gibel carp Carassius gibelio, common carp Cyprinus carpio, eastern mosquitofish Gambusia holbrooki, topmouth gudgeon Pseudorasbora parva).

Sampling was conducted between June 2009 and May 2010, with samples collected at locations selected haphazardly by Point Abundance Sampling (PAS: Nelva et al., 1979) by Electrofishing (SAMUS-725MP, anode diameter of 2 m). This method provides reproduceable and quantifiable samples and is efficient along the entire range of catchable fish sizes (Copp, 1989b). Sampling was carried out over a ≈300 m stream stretch (37°20′35.2″ N, 27°43′38.0″ E) in summer (78 point samples), winter (25), autumn (100) and spring (50), for a total of 253 random points. Maximum depth was ≈130 cm and electrofishing was effective even in the deeper parts of the river, where small and bottom-dwelling fish species were successfully captured. Juvenile L. gibbosus individuals were distinguished from adults based on a total length at maturity of 77.5 mm for the species in Sarıçay Stream (Top, 2012). Measurements of microhabitat variables included: (i) depth (cm), (ii) substratum composition (visually estimated as: mud, <50 µm; silty sand, >50 µm to 0.06 cm; sand, >0.06–0.2 cm; gravel, >0.2–2.0 cm; mud + stone, >2.0–20.0 cm; rock, >20 cm as described in Beyer et al. (2007)), (iii) distance from bank (cm), (iv) distance from vegetation (cm), (v) submersed aquatic vegetation, (vi) submersed woody structure (roots or other ligneous material), (vii) plant cover (all in % of point area), (viii) water velocity (determined semi-quantitatively as described in Beyer et al. (2007), using a pole as: none, no ripple effect around the pole; medium fast: gentle ripple effect around the pole (>0 but <5 cm s−1); fast: elevated ripple effect around the pole (5–10 cm s−1), (ix) turbidity (estimated visually as: low, medium and high blurry), and (x) light intensity (at the water surface and categorised as: shady, sunny-shady, and sunny). Catch per Unit Effort (CPUE) was recorded simultaneously during electrofishing and expressed as number of fish specimens captured by cumulative time of electrofishing operations.

thumbnail Fig. 1

Study area (Sarıçay Stream: south-west Anatolia, Turkey).

2.2 Data analysis

Constrained Quadratic Ordination (CQO) was used to analyse fish–habitat relationships (Yee, 2004). Compared to Canonical Correspondence Analysis (CCA), CQO overcomes the (unrealistic) assumptions of equal tolerances, equal maxima and uniformly distributed optima and site scores over the range of the environmental gradient (Yee, 2004), and has been recently applied successfully to the study of fish–habitat relationships (Vilizzi et al., 2012). Briefly, in CQO a sample × species data matrix is related to a sample × microhabitat variables data matrix, and the output is an ordination diagram. In the latter, the x-axis represents the ‘latent variable’ (sensu Bollen, 2002), which in the present study is a vector consisting of a linear combination of the microhabitat variables, whereas the y-axis plots the presence/absence of the species on the latent variable axis. CQO estimates an optimal linear combination of the microhabitat variables (which are ‘condensed’ into the latent variable) and regresses the species' data upon the latent variable axis using a quadratic curve fitted across the species' scores. For the purposes of this study, each response curve (or profile) in the ordination diagram represents the distributional range of the species across the microhabitat gradient (i.e. the latent variable), so that the relative position of the curve along the gradient indicates the use/preference of the species for certain values of the microhabitat variables summarised into the microhabitat gradient, and as determined by the species' probability of occurrence. The optimum is the value along the microhabitat gradient at which the highest probability of occurrence for that species is recorded (Yee, 2004).

Using the entire set of 253 point samples, CQO models were fitted to presence/absence data for adult and juvenile L. gibbosus and P. parva as introduced species and for S. fellowesii and P. smyrnaeus as endemic species (note that because of the relatively large sample sizes required by the statistical procedure to ensure convergence, no season-wise analysis of the data was possible: see also Vilizzi et al., 2012). Depth, substratum composition, distance from bank, distance from vegetation, submersed aquatic vegetation, submersed woody structure, plant cover, velocity, turbidity and light intensity (defined as above) were the ten descriptors identifying the microhabitat latent variable. Fitting of CQO was under a binomial model of rank 1, with three non-linear degrees of freedom and unequal tolerances and after choice of the ‘best’ 100 models (Yee, 2006). Implementation of models was in R ×64 v3.0.3 (R Development Core Team, 2015) using library VGAM v0.9-7 and following guidelines in Yee (2006).

3 Results

In total, 2341 fish in seven species were sampled. S. fellowesii (n = 765) and juvenile (306) and adult L. gibbosus (514) were the most abundant, followed by P. smyrnaeus (234) and P. smyrnaeus (234). Gambusia holbrooki (232), albeit abundant, was found only in a few locations and mostly as 0+ juveniles, and was therefore removed from the dataset for CQO analysis. Similarly, C. gibelio (6), C. carpio (3) and Oxynoemacheilus sp. (21) occurred too infrequently in samples to permit microhabitat analysis.

The relative abundances of the five fish species retained for the study of fish–microhabitat relationships indicated seasonal variability. Thus, S. fellowesii was the most abundant species in all seasons, followed by juvenile L. gibbosus. P. parva was the least abundant species in spring but relatively more abundant in autumn. Finally, adult L. gibbosus were the least abundant species only in winter, whereas this was true of P. smyrnaeus in all seasons except spring (Fig. 2).

Based on CQO, turbidity (−0.941), substratum composition (−0.422), light intensity (−0.345), distance from bank (−0.295), submersed woody structure (−0.182) and plant cover (−0.174), in that order, were the descriptors with negative loadings on the microhabitat latent variable axis; whereas, depth (0.339), submersed aquatic vegetation (0.336), distance from vegetation (0.297) and velocity (0.122) had positive loadings (Fig. 3). Turbidity was the major microhabitat driver with by far the largest loading. Unimodal, bell-shaped curves were fitted to P. parva (optimum = −6.264; tolerance = 1.47) and L. gibbosus (−4.804; 1, as reference value), which showed a preference for less turbid waters, whereas the opposite was true for P. smyrnaeus (−5.406; 2.99), which also preferred higher depths. The lack of any optima for S. fellowesii and L. gibbosus juveniles and the presence of an ‘inverse’ bell-shaped curve within the negative range of values of the latent variable indicated avoidance of the microhabitats preferred by P. parva and adult L. gibbosus (Fig. 3). Overall, adult L. gibbosus in Sarıçay Stream preferred locations closer to the bank with less turbid water, plant cover, light intensity and woody structure and with sandy substratum whilst avoiding riffle habitats with coarser debris, deeper water, dense submersed aquatic vegetation and higher velocities. Except for the other non-native P. parva, these preferences were not shared by either the endemic species or juvenile L. gibbosus, with the latter demonstrating a partial habitat overlap with one of the two endemic species under study (i.e. S. fellowesii).

thumbnail Fig. 2

Abundance of the most common fish species sampled from Sarıçay Stream according to season.

thumbnail Fig. 3

Constrained Quadratic Ordination (CQO) plots for the most abundant fish species sampled from Sarıçay Stream. A summary indication of the main microhabitat features is provided on the negative and positive boundaries of the microhabitat (latent) variable axis.

4 Discussion

L. gibbosus have been reported to prefer generally sandy and slow-flowing river branches and oxbows, and to inhabit mainly still waters, reservoirs, floodplain lakes, ponds and marshes with avoidance of deeper areas (e.g. Balon, 1959; Crivelli and Mestre 1988; Copp et al., 2002). Although these habitat preferences were overall in accordance with the findings of the present study, the lack of a habitat overlap with the native species disagrees with previous studies on habitat association with native brown trout in a small river in England, where water temperatures may not reach the necessary levels for the species' optimal reproduction (Vilizzi et al., 2012; Stakėnas et al., 2013). In this regard, all previous studies conducted in England have shown that L. gibbosus occur randomly in river systems of the region and are generally found as small individuals (<40 cm TL) escaped from closed still water sources (e.g. ponds, lakes, reservoirs: Copp and Fox, 2007). However, the present results also do not corroborate the findings from Almeida et al. (2014) of negative impacts, hence do not support the hypothesis of increased habitat affinity with native and endemic species under elevated water temperatures (suitable for successful reproduction and establishment of L. gibbosus).

The observed similarity in habitat preferences between adult L. gibbosus and P. parva and dissimilarity with the native species can be interpreted in two ways. Firstly, these two non-native species could have replaced local species in the stream, even though this contention would be hard to support in the absence of pre-introduction or isotope-based analysis studies able to unravel trophic changes over time (e.g. Jackson et al., 2016). Secondly, the two non-native species may be using different trophic levels to avoid habitat overlap with the resident native species. In this regard, a recent study suggested that P. parva invasion resulted in niche differentiation, with the species being found at a lower trophic position relative to some native species (Tran et al., 2015). Declerck et al. (2002) found a moderate overlap between P. parva and L. gibbosus, which can shift their niche for different food sizes. However, niche overlap can be difficult to interpret because species may modify their niche according to competition for resources. Werner (1984) suggested that an introduced species able to utilise resources efficiently may lead to an expansion in the native species' diet. Both of the non-native species examined in the present study prefer habitats with increased complexity with plant cover and woody structure (e.g. branches, roots), and this habitat complexity could provide variable feeding opportunities by spatial segregation for both species (Declerck et al., 2002) as well as shelter for competitors (Fisher Huckins et al., 1999). Also, rich food and nutrient availability in Sarıçay Stream (Top, 2012) may lead to reduce competition. Indeed, results of Karakuş (2014), who investigated feeding interactions of the fish species in Sarıçay Stream, support this contention, with P. parva showing limited interactions with the native species but a significant one with L. gibbosus. On the contrary, in a turbid shallow lake of Central Europe, L. gibbosus and P. parva were reported to occur in large numbers within reeds, but no significant overlap for diet was found (Wolfram-Wais et al., 1999).

Although no significant habitat overlap was detected between adult L. gibbosus and the endemic species of Sarıçay Stream, a constant decline in the abundance of P. smyrnaeus was still observed (Fig. 2). This was regardless of the large microhabitat loading of P. smyrnaeus, which does not imply that the species was abundantly captured, as only presence/absence relationships were investigated in the present study. Thus, the decline in abundance was likely due to the low environmental tolerance of the species as a result of worsening habitat conditions (Özdemir et al., 2015). However, given the overall pronounced niche differentiation observed in the present study, non-native L. gibbosus and P. parva at this stage may be considered not to pose a threat to the endemic species of Sarıçay Stream. Indeed, endemic S. fellowesii was found in high abundance, similar to other streams and lakes of the Aegean region (Özdemir et al., 2015; Top et al., 2016).

Overall, the present results support recent findings on feeding interactions between native and non-native fishes (Karakuş, 2014; Jackson et al., 2016) and suggest that the potential for adult L. gibbosus to cause adverse impacts through habitat competition with the native species is not apparent in Sarıçay Stream. This is at variance with other studies carried out using different methodologies (e.g. snorkelling) and investigating different effects (e.g. aggression) under similar climate and environmental conditions (e.g. Almeida et al., 2014). Notably, the present outcome would invalidate prediction that climate change could favour L. gibbosus reproduction and subsequent establishment and impact on the native fauna (as is the case for the UK: Copp et al., 2010), and this is especially true should habitat complexity and food resources be high enough. In this regard, the tenet that invasive species differ from non-native species by exerting impacts on the recipient ecosystem was not supported for L. gibbosus and P. parva in Sarıçay Stream. However, support to this conclusion may be eventually provided through e.g. food-web analyses (Cucherousset and Olden, 2011; Tran et al., 2015; Jackson et al., 2016) and/or by more studies on habitat associations from different stream systems, especially Mediterranean-type ones in southern Europe. Finally, the results of the present study could have benefited from the sampling of ‘control’ sites where L. gibbosus does not occur. Pending further investigations, the present results should be regarded as preliminary.

As was the case with the present study, the importance of reporting on instances where non-native fishes exert negligible (or no) impacts on the native biota should be emphasised, as most of the literature tends to prioritise the existence of negative effects (e.g. Gozlan, 2008). Indeed, this practice would provide for a more comprehensive approach to the understanding of the ecology of non-native fishes introductions and related management (Britton et al., 2011).

Conflict of interest

The authors declare that they have no conflict of interest.


This study was supported by the Research Fund of Muğla Sıtkı Koçman University (Project No: 09/28). We thank the General Directorate of Protection and Control, Ministry of Agriculture and Rural Affairs, Republic of Turkey for providing permission to carry out sampling for the present study.


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Cite this article as: Top N, Tarkan AS, Vilizzi L, Karakuş U. 2016. Microhabitat interactions of non-native pumpkinseed Lepomis gibbosus in a Mediterranean-type stream suggest no evidence for impact on endemic fishes. Knowl. Manag. Aquat. Ecosyst., 417, 36.

All Figures

thumbnail Fig. 1

Study area (Sarıçay Stream: south-west Anatolia, Turkey).

In the text
thumbnail Fig. 2

Abundance of the most common fish species sampled from Sarıçay Stream according to season.

In the text
thumbnail Fig. 3

Constrained Quadratic Ordination (CQO) plots for the most abundant fish species sampled from Sarıçay Stream. A summary indication of the main microhabitat features is provided on the negative and positive boundaries of the microhabitat (latent) variable axis.

In the text