Trophic interactions in a lowland river fish community invaded by European barbel Barbus barbus (Actinopterygii, Cyprinidae)

Trophic interactions in a lowland river fish community invaded by European barbel Barbus barbus... Hydrobiologia (2018) 819:259–273 https://doi.org/10.1007/s10750-018-3644-6 PRIMARY RESEARCH PAPER Trophic interactions in a lowland river fish community invaded by European barbel Barbus barbus (Actinopterygii, Cyprinidae) Catherine Gutmann Roberts J. Robert Britton Received: 6 March 2018 / Revised: 2 May 2018 / Accepted: 8 May 2018 / Published online: 22 May 2018 The Author(s) 2018 Abstract Following their invasion, non-indigenous driven by inter-specific differences in functional fish can potentially exclude native fishes from their morphology and habitat use. original niches through competition, or can partition in their resource use with native species to facilitate co- Keywords Biological invasion  Isotopic niche existence. Here, using stable isotope analysis, the Non-indigenous  Stable isotope analysis  Trophic trophic interactions of invasive European barbel niche Barbus barbus and other fishes were tested in an invaded river of relatively low fish species diversity and where no other Barbus species were present. Testing was over three distinct life stages: age Introduction 0 ? (\ 38 mm), juveniles (86–231 mm) and adults ([ 386 mm). There were strong patterns of isotopic Invasions of non-indigenous fishes can result in niche partitioning between the juvenile fishes, with adverse impacts in native fish communities, including some inter-specific niche differences also apparent in competitive displacement and exclusion (Gozlan 0 ? fishes. For adult B. barbus and chub Squalius et al., 2010). Understanding how an invasive fish can cephalus, however, niche convergence was evident. impact native species requires knowledge on their Within the B. barbus population, the niches of the trophic interactions, such as whether they share prey adult fish differed significantly from the 0? and resources, resulting in niche convergence, or exploit juvenile fish, indicating considerable dietary changes different resources, resulting in niche partitioning with development. These results suggested that niche (Cucherousset et al., 2012; Tran et al., 2015; Copp partitioning at the most abundant life stages were et al., 2017). Quantifying the feeding relationships of facilitating the co-existence of invasive B. barbus with introduced and native fishes is thus important for other fishes in the community, with this most likely understanding their ecological risks to the native communities (Cucherousset & Olden, 2011) and facilitates assessment of the ecological impacts that might develop (Gozlan et al., 2010; Tran et al., 2015; Handling editor: Michael Power Copp et al., 2017). C. G. Roberts  J. R. Britton (&) European barbel Barbus barbus (Linneaus, 1758) Department of Life and Environmental Sciences, Faculty of the Cyprinidae family is now invasive in many of Science and Technology, Bournemouth University, European rivers outside of its native range, especially Poole BH12 5BB, Dorset, UK e-mail: rbritton@bournemouth.ac.uk 123 260 Hydrobiologia (2018) 819:259–273 rivers in Italy and Western Britain (Britton & Pegg, indigenous populations, with populations being rela- 2011). Attaining lengths to approximately 800 mm tively abundant and widespread through basins such as and weights in excess of 8 kg (Amat-Trigo et al., the River Severn (Amat-Trigo et al., 2017). Although 2017), they are generally valued for sport angling, knowledge of invasive B. barbus trophic interactions with this the primary driver of introductions (Britton & with indigenous fishes is limited in these rivers, both Pegg, 2011). A highly vagile species, they can disperse Basˇic´ et al. (2015) and Gutmann Roberts et al. (2017) relatively quickly through river systems (Hunt & revealed that in rivers in both their native and invasive Jones, 1974), often leading to rapid colonisation ranges, angling baits based on marine-derived nutri- (Carosi et al., 2017). In invaded rivers where they ents can provide a strong trophic subsidy. This results are sympatric with endemic Barbus fishes, such as in in some individual B. barbus and S. cephalus (gener- Italian rivers (e.g. the Tiber basin), long-term data ally [ 400 mm) specialising on this allochthonous suggest populations of endemic Barbus tyberinus resource. However, in rivers where angling is less Bonaparte, 1839 are being displaced by B. barbus, intense and so where this subsidy is lower, and in body with the mechanism suggested to involve asymmetric sizes that rarely consume these baits (\ 400 mm), competition between the fishes (Carosi et al., 2017). there remains a distinct knowledge gap on the trophic This displacement is in addition to genetic impacts relationships of invasive B. barbus with other species. caused by introgression that results in a loss of genetic Moreover, there is also minimal knowledge on how integrity in the endemic Barbus fishes (Meraner et al., their diet and trophic niche sizes change with increas- 2013; Zaccara et al., 2014). Elsewhere in Europe, ing body size, and in relation to these changes in the invasive B. barbus populations are often present in indigenous fishes. This is despite the diet of fish communities where other Barbus fishes are absent. usually being gape limited, where gape size is a Thus, whilst they are sympatric with indigenous function of body length (e.g. Persson et al., 1996), cyprinid fishes such as chub Squalius cephalus suggesting considerable dietary shifts will occur with (Linnaeus, 1758), they have lower functionally sim- increasing body length. Data on the inter- and intra- ilarity with these fishes than with congeners. Conse- specific trophic relationships of B. barbus are also quently, the strength of their interactions might be less missing in their invasive range more generally, where intense and their invasion might be less likely to incur competitive interactions between invasive and ende- negative ecological impacts. mic Barbus fishes have, to date, been inferred from Examples of systems invaded by B. barbus and relative body condition data (e.g. Carosi et al., 2017). where endemic Barbus fishes are absent are rivers in The aim of this study was to quantify the trophic Western England. In Britain, B. barbus is only interactions of a population of invasive B. barbus with indigenous to eastern flowing rivers in England due other fishes in a river where no other Barbus fishes to their previous connections with mainland Europe at were present. The focus was on determining the extent the end of the last glacial period (Wheeler & Jordan, of trophic niche sharing within and between species, 1990). Research on these indigenous B. barbus and how this altered across a range of life stages (as suggests many of these populations are imperilled inferred from body sizes). The River Teme, western due to losses of habitat and river connectivity (Basˇic´ England, was the study river, where non-indigenous B. et al., 2017). Consequently, enhancement stocking barbus have been present since the 1970s (Antognazza often supports these populations, with hatchery-reared et al., 2016). The objective was to determine the individuals released at lengths between 120 and trophic niche sizes and overlaps between invasive B. 250 mm and age 1? and 2? years (Britton et al., barbus and native fishes at three different life stages: 2004; Antognazza et al., 2016). Studies on the trophic age 0? (young-of-the-year), juveniles and adults. It interactions of these stocked fish suggest substantial was hypothesised that (1) due to the consistent patterns partitioning in their trophic niches with S. cephalus, of inter-specific trophic partitioning between B. bar- the species that has the most similar functional traits bus and native cyprinid fishes in their indigenous and body sizes as B. barbus in these rivers (Basˇic & range (Basˇic & Britton, 2016), these patterns of inter- Britton, 2016). specific partitioning are present in their non-indige- In their invasive range in Western England, pop- nous, invasive range; and (2) within the fishes, there ulations tend to be more successful than many were significant shifts in the position of the trophic 123 Hydrobiologia (2018) 819:259–273 261 niches across the three life stages, with populations occasionally present in samples but not included in having a relatively large niche comprising smaller analyses were bullhead Cottus gobio Linnaeus, 1758 sub-sets. and stone loach Barbatula barbatula (Linnaeus, As the B. barbus population of the River Teme (and 1758). Brown trout Salmo trutta Linnaeus, 1758 and the River Severn basin generally) is an important juvenile Atlantic salmon Salmo salar Linnaeus, 1758 angling resource (Amat-Trigo et al., 2017), the use of are also present in the river but are more prevalent stomach contents analysis via destructive sampling of upstream of the town of Ludlow, outside of the study the juvenile and adult fish was not possible. Conse- reach (Fig. 1). Compared with the area of river located quently, trophic analyses were based on stable isotope close to the confluence with the River Severn and that analysis (SIA), where the ecological application of was used by Gutmann Roberts et al. (2017), angling 13 15 carbon (as d C) and nitrogen (as d N) stable isotopes pressure was relatively light in the study reach, and is based on the predictable relationship between the thus inputs of angling baits containing high propor- isotope composition of a consumer and its prey. It thus tions of pelletized fishmeal were considered as rela- provides a temporally integrative and powerful tool to tively low. analyse trophic interactions between native and non- The 0? fish were sampled from a single area of native fishes (Cucherousset et al., 2012). For compar- nursery habitat located close to Bransford (Fig. 1). isons of SI data within and between the fishes, two They were sampled using a micromesh seine net metrics were used: the significance of differences in (25 9 2 m) on 12 September 2016. The fish were 15 13 d N-d C centroids, and core isotopic niche sizes (as euthanised via anaesthetic overdose (MS-222) and a proxy of the trophic niche) and overlaps calculated transported back to the laboratory on ice. In the using standard ellipse areas (Jackson et al., laboratory, they were identified to species, measured 2011, 2012). (standard length, nearest mm) and a sample of dorsal muscle tissue removed and dried to constant weight at 50C. The juvenile and adult fish samples were Methods collected using angling and electric fishing between July and September 2015 and 2016, with SIA based on Sampling details and stable isotope analysis scales (Busst & Britton, 2016, 2017). Correspond- ingly, for each captured fish, identification was to The study was conducted on the middle reaches of the species level, followed by measuring (fork length, River Teme, from the town of Tenbury Wells nearest mm) and the collection of between three and 0 0 (5219 N, - 224 W) to the village of Bransford five scales from the area between the base of the dorsal 0 0 (5210 N, - 216 W) (Fig. 1). Across the Teme fin and above the lateral line. As scales grow as fish catchment, altitude varies between 24.3 and 544.5 length increases, only the outer portion of scales mAOD, and land-use is primarily grassland (59%), reflects their most recent growth (Hutchinson & with some horticulture (24%) (CEH, 2018). In the Trueman, 2006; Basˇic´ et al., 2015). Consequently, study reach, the river generally comprised sequences only the very outer portion of the sampled scales was of pool and riffles, where maximum depths rarely used in SIA. One scale was prepared per fish, with this exceeded 2 m and widths rarely exceeded 15 m. A involving their thorough washing with distilled water, flow gauging station towards the downstream end of removal of the scale outer edge using dissection scissors and then drying to constant weight as per the the reach near Bransford had a long-term Q95 of 3 -1 3 -1 3 2.0 m s , Q50 of 10.2 m s and Q10 of 42.4 m 0? fish samples. The other scale samples were used to -1 s (CEH, 2018). In the study reach, the cyprinid fish age the fish (Amat-Trigo et al., 2017). Scale decalci- community had relatively limited diversity, with only fication was not performed prior to SIA, since the invasive B. barbus, and S. cephalus, dace Leuciscus removal of inorganic carbonates has no significant 13 15 leuciscus (Linnaeus, 1758) and minnow Phoxinus effect on scale d C and d N values (Sinnatamby phoxinus (Linnaeus, 1758) present. Grayling Thymal- et al., 2007, 2010; Woodcock & Walther, 2014). lus thymallus (Linnaeus, 1758) were also present in Concomitantly, qualitative samples for SIA of samples at the upper end of the reach and so were also macroinvertebrates were collected from two areas of 0 0 included in analyses. Other species that were the river, ‘Area 1 and ‘Area 2 . Samples in Area 1 123 262 Hydrobiologia (2018) 819:259–273 Fig. 1 Inset: location of the River Teme in Great Britain. Main study area was the stretch of the river between the two dashed map: The River Teme catchment showing its confluence with lines. Macroinvertebrates were collected at locations marked the River Severn. Arrows mark the direction of river flow. The with asterisks were collected from Tenbury Wells (5219 N, spp. larvae (n = 3 per Area) were also taken in 2016. 0 0 0 - 224 W) and Lindridge (5232 N, - 251 W), and All samples were taken back to the laboratory where 0 0 from Area 2 at Bransford (5210 N, - 216 W) in they were washed in distilled water and dried to June and September 2015 and 2016. Samples were constant weight as per the fish samples; note that in collected using kick sampling. Macro-invertebrate each case, one sample comprised between three and samples collected in 2015 contained very high six individuals. proportions of the amphipod Gammarus pulex (Lin- The dried muscle, scale and invertebrate samples naeus, 1758) in both sampling areas ([ 50%). Gam- were then submitted to the Cornell Isotope Laboratory marus spp. are common prey items for riverine fishes in New York, USA, for SIA. This involved the generally (e.g. MacNeil et al., 1999), as well as the samples being ground to powder, weighed in tin fishes analysed here more specifically (e.g. Mann, capsules (nearest 1,000 lg) and analysed on a Thermo 1974; Basˇic´ et al., 2015). Thus, samples were taken to Delta V isotope ratio mass spectrometer (Thermo describe the stable isotope data of fish putative prey in Scientific, USA) interfaced to a NC2500 elemental 2015. This sampling was repeated in 2016, with G. analyser (CE Elantach Inc. USA). Standards were pulex samples taken for SIA to enable consistent verified against international reference materials and temporal and spatial testing of differences in fish calibrated against the primary reference scales for 13 15 putative prey resources. However, to increase the d C and d N. The accuracy and precision were diversity of these baseline samples, samples of checked every ten samples using a standard animal Chironomid larvae (n = 6 per Area) and Trichoptera sample (mink). The outputs were values of d C and 123 Hydrobiologia (2018) 819:259–273 263 d N(%) for each sample. As C:N ratios were below correction on the stable isotope data, differences were 3.5, indicating low lipid content, there was no need for tested in the temporal data in the uncorrected and the d C to be lipid corrected (Post et al., 2007; Skinner corrected data of the juvenile fishes using ANOVA. et al., 2016). The juvenile fishes were used in preference to the adult fishes for this, as the diet of the latter was also likely to Data analysis have had some influence from angling baits containing ˇ ´ marine-derived fishmeal (Basic et al., 2015; Gutmann The 0? fish utilised in the analysis were all between Roberts et al., 2017). This testing was not completed 17 and 38 mm and in their first year of life. The for the 0? fishes, as their samples were taken from a juvenile fish were between 86 and 231 mm and single site in 2016. However, their data were also between ages 1? and 4? years; note that in this corrected to enable their results to be compared with length range, some L. leuciscus would have been the juvenile and adult fishes. The stable isotope sexually mature, but with B. barbus and S. cephalus correction equations were being immature. The adult fish, comprising only B. 15 15 d N  d N i base barbus and S. cephalus, were all C 386 mm TP ¼ þ 2 ð1Þ 3:4 (Table 2). The fish ages were derived by scale ageing using a projecting microscope and accounting annual 13 13 d C  d C i meaninv d C ¼ ð2Þ marks as per Amat-Trigo et al. (2017). For inter- corr CR inv specific data analyses, these length classes were considered separately. This was because the habitat where TP is the trophic position of the fish, d N is i i the isotopic ratio of the fish, d N is the isotopic use of these species tended to be quite different, with base the 0? fishes all sampled from marginal areas of the ratio of primary consumers, 3.4 is the fractionation between trophic levels and 2 is the trophic position of river where flows were minimal, the juvenile fishes were generally captured from relatively shallow and the baseline organism (Post, 2002); and d C is the corr corrected carbon isotope ratio of the fish, d C is the fast-flowing riffle habitats, and the adult fishes have uncorrected isotope ratio of the fish, d relatively large home ranges in the basin, often C is the meaninv mean invertebrate isotope ratio and CR is the exceeding 5 km (Hunt & Jones, 1974). By only inv 13 13 invertebrate carbon range (d C - d C ) (Ols- completing inter-specific analyses within these groups max min of lengths, then the data were being tested between son et al., 2009). The initial analyses using the corrected SI data tested fishes of relatively similar body sizes. This meant that these analyses would be more ecologically relevant for differences in TP and C between species and Corr between different life stages of the same species using testing the hypothesis than comparing data between species of very different length ranges (Basˇic & ANOVA or Welch’s test, with the latter used where the data were normally distributed but violated the assump- Britton, 2015). Prior to analysing the stable isotope analysis of the tion of homogeneity of variance. For each life stage, the corrected SI data were then used to test the significance fishes, the stable isotope data of the macro-inverte- 15 13 of differences in their d N-d C centroids, and differ- brate samples were tested for spatial (Area 1 versus ences in the positions and overlaps of their core trophic Area 2) and temporal (2015 vs. 2016) differences. 15 13 niches. For testing differences in the d N-d C Testing used generalized linear models (GLM) due to centroids per life stage and species, the SIA data were the relatively low sample sizes that were not normally normalised by square root transformation and a resem- distributed. The GLM revealed some significant differences (cf. Results). Thus, to enable the stable iso- blance matrix computed using Euclidean distances (Dethier et al., 2013). A PERMANOVA model was tope data of the juvenile and adult fish to be combined for use across the entire study reach, their isotopic data then fitted to this distance matrix using the adonis function in the vegan package in R. This calculated the required ‘correction’ (Jackson & Britton, 2014). 15 13 Correspondingly, the d N data were converted to significance of the differences in d N-d C centroids per group (Oksanen et al., 2007; R Core Team, 2017). trophic position (TP; Eq. 1) and the d C data were As the adonis function is similar to traditional corrected to C (Eq. 2) (Olsson et al., 2009; Jackson Corr ANOVA, it provided a pseudo F-statistic and P value & Britton, 2014). To identify the effect of this 123 264 Hydrobiologia (2018) 819:259–273 based on 999 permutations of the data (Dixon, 2003). revealed minimal differences in mean values, with Using the same method, it was then determined whether overlaps in their 95% confidence limits (Chironomid: different life stages within B. barbus and S. cephalus d C: Area 1: - 31.36 ± 0.39, Area 2: 15 13 15 had significant differences in theird N-d C centroids. 31.76 ± 0.42%; d N: Area 1: 9.88 ± 0.35, Area 2: With more than two life stages of fish being used per 9.74 ± 0.12%; Trichoptera: d C: Area 1: test, pairwise comparisons tested the significance of 32.36 ± 0.45, Area 2: 32.25 ± 0.38%; d N: Area differences between the groups, with Bonferroni 1: 9.20 ± 0.31, Area 2: 8.86 ± 0.42%). In G. pulex, adjustment for multiple comparisons. however, some spatial and temporal differences in To compare ‘core’ trophic niche size and overlaps their SI data were apparent that, when tested in GLMs, within and between species, the isotopic niche was revealed significant differences (d C: Wald 2 15 2 used, where the isotopic niche is an approximation of v = 12.05, P \ 0.01; d N: Wald v = 23.5, the trophic niche. It is acknowledged that the isotopic P \ 0.01; Table 1A). Pairwise comparisons of the niche varies slightly from the trophic niche due to it mean SI values from both models revealed these being influenced by factors other than diet (Jackson significant differences were both spatial and temporal et al., 2011), such as growth and metabolic rate of for both stable isotopes (Table 1B, C). Consequently, individuals (Busst & Britton, 2017). It was calculated the use of Eqs. 1 and 2 to correct the fish SI data used using the metric ‘standard ellipse area’ (SEA), a the G. pulex SI data only (Table 1A). Prior to data bivariate measure of the distribution of individuals in correction, there were significant differences in the isotopic space (Jackson et al., 2012). To examine the juvenile fish stable isotope data between years 13 15 size and overlap of the ‘core’ isotopic niches of each (ANOVA: d C F = 5.05, P = 0.03; d N 1,45 size group by species, ellipses were plotted that F = 11.56, P \ 0.01; Fig. 2A). However, these 1,45 enclosed 40% of the predicted data and thus the typical significant differences were no longer apparent fol- resource use of that life stage of fish. The ellipses were lowing isotopic correction (ANOVA: d C calculated within the R package SIBER v2.1.3 (Jack- F = 0.10, P = 0.75; d NF = 1.11, P = 0.30; 1,45 1,45 son et al., 2011, 2012) and, due to some relatively small Fig. 2B). Note that in the tests, SI data from L. sample sizes, a corrected Bayesian estimate of Stan- leuciscus were not included as they were only present dard Ellipse Area (SEA ) was calculated. This was in samples in 2016. followed by a calculation utilising a Markov chain Monte Carlo simulation with 10 iterations for each Intra- and inter-specific stable isotope analysed group that provided 95% confidence limits relationships (SEA ) of the isotopic niche size (Jackson et al., 2011; R Core Team, 2017). Using SEA , the extent of niche The lengths of each species were very similar across overlap (%) between species and life stages was then the 0? fishes. There was greater natural variation also estimated. This was determined using the maxi- between the lengths of fishes as juveniles (T. thymallus mum likelihood fitted standard ellipses, with the extent were smaller than other fishes) and adults (S. cephalus of the overlap between two groups thus represented by were generally smaller than B. barbus) (Table 2). The the overlap of their core niches. This was calculated only species with all life stages represented in analyses using Bayesian modelling in the SIBER package, with were B. barbus and S. cephalus. For B. barbus,C corr the denominator being the sum of non-overlapping was significantly higher in adults than the 0? fish and area of the two ellipses (Jackson et al., 2011). juveniles (P \ 0.01), whilst TP was significantly lower for adults versus the 0? fish (P \ 0.01) (Table 3). For S. cephalus, the 0? fish had signifi- Results cantly lower C than juveniles and adults (P \ 0.01) corr and significantly higher TP (P \ 0.01) (Table 3). Stable isotope correction for macro-invertebrate Between the species, differences in C between corr temporal and spatial differences 0? B. barbus and 0? S. cephalus were not signifi- cant, but was between both of these 0? fishes and Comparison of spatial differences in SI data of the 0? P. phoxinus (P \ 0.01; Table 3). The TP of 0? B. Chironomid larvae and Trichoptera spp. in 2016 barbus was significantly higher than both S. cephalus 123 Hydrobiologia (2018) 819:259–273 265 Table 1 (A) Mean stable isotope data of Gammarus pulex 14 (A) from the two sampled areas of the River Teme in 2015 and 2016, where values are estimates (± 95% CL) from the gen- eralized linear model (GLM), and their significance of differ- ences (as P values) according to pairwise comparisons with 13 15 Bonferroni adjustment in the GLM for (B) d C and (C) d N 12 (A) 13 15 Area Year n d C(%) d N(%) 1 2015 6 - 30.68 ± 0.58 10.78 ± 0.57 2016 4 - 29.44 ± 0.82 8.73 ± 0.71 2 2015 3 - 29.10 ± 0.82 10.22 ± 0.82 2016 6 - 29.86 ± 0.82 9.16 ± 0.82 (B) -31.0 -29.0 -27.0 -25.0 δ C(‰) d C Area 1, Area 1, Area 2, Area 2, 3.5 2015 2016 2015 2016 (B) Area 1, – 2015 3.0 Area 1, 0.05 – 2.5 Area 2, 0.01 1.00 – Area 2, 0.67 1.00 1.00 – 2.0 (C) 1.5 d N Area 1, Area 1, Area 2, Area 2, 2015 2016 2015 2016 1.0 -0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Area 1, – Ccorr Area 1, < 0.01 – Fig. 2 Uncorrected (A) and corrected (B) stable isotope data of ‘juvenile’ fish (except Leuciscus leuciscus) sampled in 2015 Area 2, 1.00 0.04 – (clear circle) and 2016 (filled circle) Area 2, < 0.01 1.00 0.43 – differences in C and TP between adult B. barbus corr and S. cephalus (P [ 0.05; Table 3). Sample number (n) represents the number of samples analysed, 15 13 where one sample = 3–6 individual gammarids Differences in d N-d C centroids Values in bold are significant at P B 0.05 The overall test for differences in the positions of the 15 13 d N-d C centroids of the 0? fishes was significant and P. phoxinus (P \ 0.01), although it was not (F = 15.72, P \ 0.01); pairwise comparisons indi- 2,58 significantly different between S. cephalus and P. cated the significant differences were between P. phoxinus (P [ 0.05; Table 3). In juveniles, C of B. corr phoxinus and the other fishes (P \ 0.01 in both cases), barbus was significantly lower than all other fishes but with differences between B. barbus and S. (P \ 0.01; Table 3). The TP of juvenile B. barbus was cephalus being not significant (P [ 0.05; Table 4). significantly higher than T. thymallus, significantly For the juvenile fishes, the overall model was signif- lower than L. leuciscus, but not significantly different icant (F = 18.41, P \ 0.01), with significant dif- 3,76 to S. cephalus (Table 3). There were no significant ferences between all species (P \ 0.01; Table 4). This TP δ N (‰) 266 Hydrobiologia (2018) 819:259–273 Table 2 The number, fish length ranges, mean lengths (95% CL) and measurement type (SL standard length, FL fork length) of each life stage of fish analysed for their stable isotopes across the two sampling areas Species n Length range (mm) Mean length (mm) (± 95% CL) Length measurement 0? B. barbus 30 18–34 25.2 ± 1.8 SL 0? S. cephalus 15 17–36 27.3 ± 2.4 SL 0? P. phoxinus 16 17–38 27.3 ± 2.8 SL Juvenile B. barbus 16 105–231 158 ± 15 FL Juvenile S. cephalus 16 112–207 153 ± 11 FL Juvenile L. leuciscus 30 102–214 167 ± 11 FL Juvenile T. thymallus 15 86–205 122 ± 16 FL Adult B. barbus 21 540–690 584 ± 17 FL Adult S. cephalus 21 386–570 466 ± 22 FL Table 3 Outputs of Species Test Testing df FP ANOVA/Welch’s test of corrected carbon (C ) and corr C corr trophic position (TP) for Barbus barbus ANOVA Life stage 2,64 32.76 \0.01 comparisons between life Squalius cephalus Welch’s Life stage 2,31 17.66 \0.01 stages and species for Barbus barbus and Squalius 0? ANOVA Species 3,60 10.01 \0.01 cephalus Juvenile Welch’s Species 3,36 16.61 \0.01 Adult ANOVA Species 1,40 2.09 0.16 Species/ life stage Test Testing df FP TP Barbus barbus ANOVA Life stage 2,64 47.17 \0.01 Squalius cephalus ANOVA Life stage 2,49 6.52 \0.01 0? ANOVA Species 3,60 12.36 \0.01 Juvenile Welch’s Species 3,30 60.53 \0.01 Note data for all sites and Adult ANOVA Species 1,40 0.02 0.90 years are combined was in contrast to the adult B. barbus and S. cephalus, Core isotopic niches (standard ellipse areas) which were not significantly different (F = 1.77, 1,41 The 95% confidence intervals of the core isotopic P = 0.18). 15 13 The model testing differences in d N-d C cen- niches (as standard ellipse areas) at each life stage suggested they were similar in size between the troids between the different life stages of B. barbus was significant (F = 28.89, P \ 0.01), with pair- species (Table 5). In general, the core isotopic niches 2,64 of the 0? fishes had low overlap (maximum 7% wise comparisons indicating the significant differ- ences were between adults and the other life stages between B. barbus and S. cephalus), the juvenile fishes (P \ 0.01; Table 4). Whilst the overall model was had no niche overlap, but in adult B. barbus and S. also significant in S. cephalus (F = 17.31, cephalus, their niches overlapped by 55% (Fig. 3). 2,49 P \ 0.01), pairwise comparisons indicated the signif- Within B. barbus, there was no overlap in their core icant differences were only between the 0? fishes and niches between the 0?, juvenile and adult fish (Fig. 3). the other life stages (P \ 0.01; Table 4). In S. cephalus, there was no niche overlap between 0? and juveniles, with this increasing to 2% between 123 Hydrobiologia (2018) 819:259–273 267 15 13 Table 4 The significance of differences in d N-d C centroids between the different life stages of the fishes, as represented by P values (with Bonferroni adjustment for multiple comparisons) derived in PERMANOVA 0? B. 0? S. 0? P. J B. J S. J L. J T. A B. A S. barbus cephalus phoxinus barbus cephalus leuciscus thymallus barbus cephalus 0? B. barbus - 0? S. cephalus 0.74 – 0? P. phoxinus \ 0.01* \ 0.01* – J B. barbus 0.22 – – – J S. cephalus – \ 0.01* – 0.01* – J L. leuciscus – – – 0.02* 0.01* – J T. thymallus – – – 0.01* 0.01* 0.02* – A B. barbus \ 0.01* – – \ 0.01* – – – – A S. cephalus – \ 0.01* – – 0.62 – – 0.18 – Table 5 Mean Lifestage and species C TP SEAc (± 95% CL) corr stable isotope data (± 95% CL) and standard ellipse 0? B. barbus 0.06 ± 0.38 3.30 ± 0.08 0.77 ± 0.28 areas (as SEAc; ± 95% CI 0? S. cephalus 0.49 ± 0.65 2.92 ± 0.13 0.96 ± 0.51 SEAb) for the sampled 0? P. phoxinus - 1.49 ± 0.49 3.02 ± 0.11 0.73 ± 0.36 fishes in the study river and across the three life stages Juvenile B. barbus 0.39 ± 0.58 2.70 ± 0.13 0.54 ± 0.28 (0?, juvenile and adult) Juvenile S. cephalus 2.57 ± 0.75 2.63 ± 0.14 0.59 ± 0.30 Juvenile L. leuciscus 1.42 ± 0.39 3.03 ± 0.05 0.44 ± 0.16 Juvenile T. thymallus 1.57 ± 0.20 2.13 ± 0.14 0.28 ± 0.14 Adult B. barbus 2.52 ± 0.40 2.62 ± 0.15 1.34 ± 0.58 Adult S. cephalus 3.22 ± 0.45 2.61 ± 0.15 1.89 ± 0.83 0 ? and adults, and then the juvenile niche sitting and core isotopic niches. The centroids were calcu- entirely within the adult niche (Fig. 4). lated using all SI data per life stage and species, whereas cores niches are based on a predicted 40% of the SI data to indicate typical resource use (Jackson Discussion et al., 2011, 2012). There were some consistent results from these analyses that aligned with Hypothesis 1, Hypothesis 1 tested whether there were consistent especially in the juvenile fishes where there were 15 13 inter-specific patterns of trophic partitioning between significant differences in d N-d C centroids between B. barbus and the other fishes. It was formulated due to all species and no overlaps in their core niches. In the these patterns of niche partitioning being evident 0? fishes, there was less consistency in the results of between the fishes in the B. barbus indigenous range both analyses, with isotopic niches showing low inter- 15 13 (Basic & Britton, 2016). An alternative to this specific overlap, but with d N-d C centroids show- hypothesis would be the fishes having high niche ing significant differences only between P. phoxinus overlap, as has been suggested between invasive and and the other fishes. Whilst there was poor alignment endemic Barbus fishes in Italian rivers, where it of the results in the adult fishes with Hypothesis 1, both 15 13 appears to have resulted in the competitive displace- analyses provided consistent results; the d N-d C ment of the endemics (Carosi et al., 2017). Hypothesis centroids of the adult B. barbus and S. cephalus were 15 13 1 was tested using two analyses, d N-d C centroids not significantly different and their core niches had 123 268 Hydrobiologia (2018) 819:259–273 This pattern was evident in rivers that had been (a) 4.0 stocked with hatchery-reared B. barbus at sizes below 3.5 ˇ ´ 250 mm and remained evident in adult fishes (Basic 3.0 and Britton, 2016). In contrast, Gutmann Roberts et al. 2.5 (2017) revealed that in the lower reaches of the study 2.0 river, there was high overlap in the core isotopic 1.5 niches of adult B. barbus and S. cephalus, primarily 1.0 the result of individual fishes specialising in the -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 consumption of pelletized marine fishmeal utilised by (b) 4.0 anglers. This niche overlap was also evident in the 3.5 adult fishes here, where inter-specific niche differ- 3.0 ences were only significant in the 0? and juvenile fishes. In B. barbus, there were strong and significant 2.5 patterns in niche partitioning between their different 2.0 life stages, suggesting considerable ontogenetic shifts 1.5 in their diet that resulted in their population having a 1.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 relatively large core isotopic niche that was composed of at least three distinct sub-sets. This was consistent (c) 4.0 15 13 with Hypothesis 2, although the d N-d C centroids 3.5 suggested differences were not significant between the 3.0 0? and juvenile fish. In contrast, the isotopic niches of 2.5 S. cephalus were more similar over their three studied 2.0 life stages, with only the niche of the 0? fish being 1.5 distinct from the other life stages, with the juvenile and 1.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 adult niches overlapping completely, contrary to Ccorr Hypothesis 2. Fig. 3 Corrected Carbon (C ) versus trophic position (TP) Stable isotope data of 0? fishes can be confounded corr for Barbus barbus (filled triangle), Squalius cephalus (filled by issues of their data still showing a strong parental square), Leuciscus leuciscus (delta) and Thymallus thymallus signal. For example, in anadromous brown trout Salmo (open square), and the positions of their core isotopic niches (as trutta, newly emerged fry retained a strong parental, SEA ), where solid line: B. barbus, small dashed line: S. marine-based isotopic signal that enabled their differ- cephalus, long dashed line: L. leuciscus, and dash/dot line: T. thymallus.(a)0? fishes; (b) juvenile fishes; and (c) adult fishes entiation from fry produced from non-anadromous parents, but this difference was much reduced after relatively high overlap (55%). Across all life stages four months of feeding in freshwater (Briers et al., and analyses, there was no evidence to support the 2013). In 0? smallmouth bass Micropterus dolomieu, alternative hypothesis that invasion by B. barbus had post-hatch embryos had elevated d N values that resulted in competitive displacement of native fishes, were associated with their parental origin, but these as suggested by Carosi et al. (2017) for endemic values subsequently decreased rapidly due to their Barbus. It is, however, acknowledged that this was not exogenous feeding during their metamorphosis from tested implicitly here, given the absence of data from larvae into juveniles (Vander Zanden et al., 1998). the pre-invaded period or from sites with B. barbus Here, the 0? fishes utilised were all of lengths above absent. 17 mm, were all fully formed juveniles rather than The pattern of isotopic niche partitioning between larvae, and were up to 10 weeks old. Their stable iso- B. barbus and other fishes was thus consistent with a tope data were very distinct from those of the adult number of isotopic studies completed on populations fishes; in terms of uncorrected data, the 0? fishes were in their indigenous range (Basˇic´ et al., 2015;Basˇic´ and depleted in d Cbyupto8% compared to adult Britton, 2015, 2016). These studies all suggested that conspecifics. Consequently, the strong patterns of core B. barbus and S. cephalus have distinct core isotopic isotopic niche partitioning detected in these 0? fishes niches, with minimal inter-specific resource sharing. were interpreted as resulting from their dietary TP Hydrobiologia (2018) 819:259–273 269 Fig. 4 Intra-specific (a) 4.0 comparisons of Corrected Carbon (C ) versus corr trophic position (TP) and 3.6 positions of core isotopic niches (as SEA ) for (a) Barbus barbus and (b) Squalius cephalus, and 3.2 where filled diamond, solid line: 0? fish; open circles, dashed line: juvenile fish; 2.8 filled triangle, dotted line: adult fish 2.4 2.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 4.0 (b) 3.6 3.2 2.8 2.4 2.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 Ccorr differences formed by their exogenous feeding within all samples from all areas sampled (in contrast to other the river, rather than being a legacy of their parental macro-invertebrate taxa), there were significant dif- isotopes. ferences in their isotopic data between years and sites In this study, the fish SI data were ‘corrected’ to (whereas data from other macro-invertebrate taxa enable data to be combined across two sampling years revealed similar values, at least spatially), and liter- and relatively long stretch of river. The use of standard ature suggests Gammarus spp. are an important prey equations to ‘correct’ SI data in this manner is well item for many fishes (e.g. MacNeil et al., 1999). established (e.g. Olsson et al., 2009; Jackson & Correction of the juvenile fish SI data using the G. Britton, 2014). However, this correction relies upon pulex data was also demonstrated as removing signif- an adequate description of the SI data of the fish prey icant temporal differences. To enable the SI data of the resources. Here, correction focused on use of G. pulex 0? fishes to be comparable to the other fishes, they SI data. The rationale for this was they were present in were also corrected using the G. pulex data, although TP 270 Hydrobiologia (2018) 819:259–273 stomach contents analyses (SCA) for the 0? fishes barbus presence, it is acknowledged that this is had suggested that these amphipods were a minor prey speculative given that isotopic niche sizes of the item (Gutmann Roberts & Britton, 2018). However, native fishes were unable to be measured in B. barbus individuals of [ 20 mm standard length in all the absence. Notwithstanding, the inter-specific isotopic 0? fish species analysed had infections of the intesti- niche partitioning evident in the study suggests that nal parasite Pomphorhynchus tereticollis (C. Gutmann despite their similar ecological guilds and sharing Roberts, unpublished data). This parasite has gam- similar habitats (especially the 0? fishes), there were marids as its intermediate host (Kaldonski et al., sufficient differences between the fishes in their 2008), suggesting G. pulex might have been consumed functional traits and/or habitat utilisation to enable in greater proportions in the 0? fishes than suggested substantial differentiation in their core isotopic niches by SCA. Moreover, in the River Severn basin, to occur (Robinson et al., 1993; Borcherding et al., Pomphorhynchus spp. has been reported as prevalent 2013; Negus & Hoffman, 2013). in all the fishes studied here (Brown 1984), suggesting On one hand, the results here could suggest that the gammarids are a common and important prey item of ecological impacts of invasive B. barbus are relatively fish in the river. Therefore, although it is acknowl- minor in the river, as there was little evidence to edged that the macro-invertebrate baseline SI data suggest there was high diet similarity in the fishes at used to correct the data here could have utilised a their most abundant life stages (0? and juveniles). wider range of taxa, especially in 2015, it is strongly This inference is supported by other recent studies on argued that the use of G. pulex SI data to correct the native B. barbus that have revealed strong patterns of fish SI data was justified and appropriate. inter-specific core isotopic niche partitioning (e.g. Following introductions of non-native fishes, Basic & Britton, 2015, 2016). However, these studies adverse ecological impacts often develop through were all limited to assessing trophic interactions via increased inter-specific competition for food resources stable isotope analysis, with studies suggesting that between invasive and sympatric native fishes (Gozlan when compared with other dietary analysis methods, et al., 2010; Cucherousset et al., 2012). Given the such as stomach contents analyses, different results relatively similar size ranges of the invasive B. barbus can occur, resulting from differences between items with other cyprinid fishes across the different life ingested (stomach contents) and assimilated (SIA) stages (albeit with some inter-specific length differ- (e.g. Locke et al., 2013). Consequently, some caution ences within life stages), this suggests there was is necessary if isotopic niche overlaps are to be used to considerable potential for inter-specific competitive infer the strength of competitive interactions. More- interactions, especially given the fishes were from over, invasive B. barbus can potentially result in other relatively similar functional guilds (Basic & Britton, ecological concerns, such as causing habitat alter- 2016). However, the lack of overlap in the isotopic ations, given recent work has demonstrated that in niches of the 0? and juvenile fishes—the life stages their native range, B. barbus act as ‘zoogeomorphic when their abundances tend to be highest—suggested agents’ (Pledger et al., 2014, 2016). This is where their low dietary overlap, with only the isotopic niches of benthic foraging activities can reduce bed material the adult fishes indicating some dietary overlap. stability, increase bedload transport, and impact Schulze et al. (2012) suggested that species within microtopographic roughness and sediment structure the same ecological guild can only coexist when they (Pledger et al., 2014, 2016). This benthic foraging respond differently to limited resource availability could then also impact upon aspects of the macro- with, for example, specialised species only persisting invertebrate communities, such as decreased abun- if their competitors are generalists. Evidence in dance via predation or reduced species richness via literature supports this, with reduced trophic niche disturbance. However, these aspects were beyond the sizes in many co-existing fishes when compared to scope of this study and so further research is required allopatry (Bolnick et al., 2010; Tran et al., 2015). In to provide increased understandings of how B. barbus the study river, however, even where the isotopic invasions affect macro-invertebrate communities and niches of the fishes were partitioned, the niches were sediment structure. Finally, it should also be noted that similarly sized. Although this suggests there had not the study river was low in fish species richness, with a been any niche constriction in the native fishes in B. cyprinid fish community comprising only four species 123 Hydrobiologia (2018) 819:259–273 271 assessments of trophic relationships in riverine fish com- (including B. barbus), with other fish taxa being very munities. Journal of Applied Ichthyology 31: 296–300. limited in diversity and abundance in the study reach, Basˇic´, T. & J. R. Britton, 2016. Characterizing the trophic niches and with no other Barbus species present. Conse- of stocked and resident cyprinid fishes: consistency in quently, if B. barbus are introduced into a river with partitioning over time, space and body sizes. Ecology and Evolution 6: 5093–5104. considerably higher native fish species richness, Basˇic´, T., J. R. Britton, M. C. Jackson, P. Reading & J. Grey, irrespective of the presence of any other Barbus 2015. Angling baits and invasive crayfish as important species, there is the possibility that there will be a trophic subsidies for a large cyprinid fish. Aquatic Sciences greater probability of higher niche overlaps within 77: 153–160. Basˇic´, T., J. R. Britton, S. P. Rice & A. G. Pledger, 2017. species in the fish community and thus higher potential Impacts of gravel jetting on the composition of fish for ecological impacts to result. It is therefore spawning substrates: Implications for river restoration and recommended that such introductions proceed only fisheries management. Ecological Engineering 107: 71–81. with caution and full risk assessment (Roy et al., Bolnick, D. I., T. Ingram, W. E. Stutz, L. K. Snowberg, O. L. Lau & J. S. Paull, 2010. Ecological release from inter- 2018). specific competition leads to decoupled changes in popu- In summary, across three life stages of invasive B. lation and individual niche width. 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Trophic interactions in a lowland river fish community invaded by European barbel Barbus barbus (Actinopterygii, Cyprinidae)

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Life Sciences; Freshwater & Marine Ecology; Ecology; Zoology
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Abstract

Hydrobiologia (2018) 819:259–273 https://doi.org/10.1007/s10750-018-3644-6 PRIMARY RESEARCH PAPER Trophic interactions in a lowland river fish community invaded by European barbel Barbus barbus (Actinopterygii, Cyprinidae) Catherine Gutmann Roberts J. Robert Britton Received: 6 March 2018 / Revised: 2 May 2018 / Accepted: 8 May 2018 / Published online: 22 May 2018 The Author(s) 2018 Abstract Following their invasion, non-indigenous driven by inter-specific differences in functional fish can potentially exclude native fishes from their morphology and habitat use. original niches through competition, or can partition in their resource use with native species to facilitate co- Keywords Biological invasion  Isotopic niche existence. Here, using stable isotope analysis, the Non-indigenous  Stable isotope analysis  Trophic trophic interactions of invasive European barbel niche Barbus barbus and other fishes were tested in an invaded river of relatively low fish species diversity and where no other Barbus species were present. Testing was over three distinct life stages: age Introduction 0 ? (\ 38 mm), juveniles (86–231 mm) and adults ([ 386 mm). There were strong patterns of isotopic Invasions of non-indigenous fishes can result in niche partitioning between the juvenile fishes, with adverse impacts in native fish communities, including some inter-specific niche differences also apparent in competitive displacement and exclusion (Gozlan 0 ? fishes. For adult B. barbus and chub Squalius et al., 2010). Understanding how an invasive fish can cephalus, however, niche convergence was evident. impact native species requires knowledge on their Within the B. barbus population, the niches of the trophic interactions, such as whether they share prey adult fish differed significantly from the 0? and resources, resulting in niche convergence, or exploit juvenile fish, indicating considerable dietary changes different resources, resulting in niche partitioning with development. These results suggested that niche (Cucherousset et al., 2012; Tran et al., 2015; Copp partitioning at the most abundant life stages were et al., 2017). Quantifying the feeding relationships of facilitating the co-existence of invasive B. barbus with introduced and native fishes is thus important for other fishes in the community, with this most likely understanding their ecological risks to the native communities (Cucherousset & Olden, 2011) and facilitates assessment of the ecological impacts that might develop (Gozlan et al., 2010; Tran et al., 2015; Handling editor: Michael Power Copp et al., 2017). C. G. Roberts  J. R. Britton (&) European barbel Barbus barbus (Linneaus, 1758) Department of Life and Environmental Sciences, Faculty of the Cyprinidae family is now invasive in many of Science and Technology, Bournemouth University, European rivers outside of its native range, especially Poole BH12 5BB, Dorset, UK e-mail: rbritton@bournemouth.ac.uk 123 260 Hydrobiologia (2018) 819:259–273 rivers in Italy and Western Britain (Britton & Pegg, indigenous populations, with populations being rela- 2011). Attaining lengths to approximately 800 mm tively abundant and widespread through basins such as and weights in excess of 8 kg (Amat-Trigo et al., the River Severn (Amat-Trigo et al., 2017). Although 2017), they are generally valued for sport angling, knowledge of invasive B. barbus trophic interactions with this the primary driver of introductions (Britton & with indigenous fishes is limited in these rivers, both Pegg, 2011). A highly vagile species, they can disperse Basˇic´ et al. (2015) and Gutmann Roberts et al. (2017) relatively quickly through river systems (Hunt & revealed that in rivers in both their native and invasive Jones, 1974), often leading to rapid colonisation ranges, angling baits based on marine-derived nutri- (Carosi et al., 2017). In invaded rivers where they ents can provide a strong trophic subsidy. This results are sympatric with endemic Barbus fishes, such as in in some individual B. barbus and S. cephalus (gener- Italian rivers (e.g. the Tiber basin), long-term data ally [ 400 mm) specialising on this allochthonous suggest populations of endemic Barbus tyberinus resource. However, in rivers where angling is less Bonaparte, 1839 are being displaced by B. barbus, intense and so where this subsidy is lower, and in body with the mechanism suggested to involve asymmetric sizes that rarely consume these baits (\ 400 mm), competition between the fishes (Carosi et al., 2017). there remains a distinct knowledge gap on the trophic This displacement is in addition to genetic impacts relationships of invasive B. barbus with other species. caused by introgression that results in a loss of genetic Moreover, there is also minimal knowledge on how integrity in the endemic Barbus fishes (Meraner et al., their diet and trophic niche sizes change with increas- 2013; Zaccara et al., 2014). Elsewhere in Europe, ing body size, and in relation to these changes in the invasive B. barbus populations are often present in indigenous fishes. This is despite the diet of fish communities where other Barbus fishes are absent. usually being gape limited, where gape size is a Thus, whilst they are sympatric with indigenous function of body length (e.g. Persson et al., 1996), cyprinid fishes such as chub Squalius cephalus suggesting considerable dietary shifts will occur with (Linnaeus, 1758), they have lower functionally sim- increasing body length. Data on the inter- and intra- ilarity with these fishes than with congeners. Conse- specific trophic relationships of B. barbus are also quently, the strength of their interactions might be less missing in their invasive range more generally, where intense and their invasion might be less likely to incur competitive interactions between invasive and ende- negative ecological impacts. mic Barbus fishes have, to date, been inferred from Examples of systems invaded by B. barbus and relative body condition data (e.g. Carosi et al., 2017). where endemic Barbus fishes are absent are rivers in The aim of this study was to quantify the trophic Western England. In Britain, B. barbus is only interactions of a population of invasive B. barbus with indigenous to eastern flowing rivers in England due other fishes in a river where no other Barbus fishes to their previous connections with mainland Europe at were present. The focus was on determining the extent the end of the last glacial period (Wheeler & Jordan, of trophic niche sharing within and between species, 1990). Research on these indigenous B. barbus and how this altered across a range of life stages (as suggests many of these populations are imperilled inferred from body sizes). The River Teme, western due to losses of habitat and river connectivity (Basˇic´ England, was the study river, where non-indigenous B. et al., 2017). Consequently, enhancement stocking barbus have been present since the 1970s (Antognazza often supports these populations, with hatchery-reared et al., 2016). The objective was to determine the individuals released at lengths between 120 and trophic niche sizes and overlaps between invasive B. 250 mm and age 1? and 2? years (Britton et al., barbus and native fishes at three different life stages: 2004; Antognazza et al., 2016). Studies on the trophic age 0? (young-of-the-year), juveniles and adults. It interactions of these stocked fish suggest substantial was hypothesised that (1) due to the consistent patterns partitioning in their trophic niches with S. cephalus, of inter-specific trophic partitioning between B. bar- the species that has the most similar functional traits bus and native cyprinid fishes in their indigenous and body sizes as B. barbus in these rivers (Basˇic & range (Basˇic & Britton, 2016), these patterns of inter- Britton, 2016). specific partitioning are present in their non-indige- In their invasive range in Western England, pop- nous, invasive range; and (2) within the fishes, there ulations tend to be more successful than many were significant shifts in the position of the trophic 123 Hydrobiologia (2018) 819:259–273 261 niches across the three life stages, with populations occasionally present in samples but not included in having a relatively large niche comprising smaller analyses were bullhead Cottus gobio Linnaeus, 1758 sub-sets. and stone loach Barbatula barbatula (Linnaeus, As the B. barbus population of the River Teme (and 1758). Brown trout Salmo trutta Linnaeus, 1758 and the River Severn basin generally) is an important juvenile Atlantic salmon Salmo salar Linnaeus, 1758 angling resource (Amat-Trigo et al., 2017), the use of are also present in the river but are more prevalent stomach contents analysis via destructive sampling of upstream of the town of Ludlow, outside of the study the juvenile and adult fish was not possible. Conse- reach (Fig. 1). Compared with the area of river located quently, trophic analyses were based on stable isotope close to the confluence with the River Severn and that analysis (SIA), where the ecological application of was used by Gutmann Roberts et al. (2017), angling 13 15 carbon (as d C) and nitrogen (as d N) stable isotopes pressure was relatively light in the study reach, and is based on the predictable relationship between the thus inputs of angling baits containing high propor- isotope composition of a consumer and its prey. It thus tions of pelletized fishmeal were considered as rela- provides a temporally integrative and powerful tool to tively low. analyse trophic interactions between native and non- The 0? fish were sampled from a single area of native fishes (Cucherousset et al., 2012). For compar- nursery habitat located close to Bransford (Fig. 1). isons of SI data within and between the fishes, two They were sampled using a micromesh seine net metrics were used: the significance of differences in (25 9 2 m) on 12 September 2016. The fish were 15 13 d N-d C centroids, and core isotopic niche sizes (as euthanised via anaesthetic overdose (MS-222) and a proxy of the trophic niche) and overlaps calculated transported back to the laboratory on ice. In the using standard ellipse areas (Jackson et al., laboratory, they were identified to species, measured 2011, 2012). (standard length, nearest mm) and a sample of dorsal muscle tissue removed and dried to constant weight at 50C. The juvenile and adult fish samples were Methods collected using angling and electric fishing between July and September 2015 and 2016, with SIA based on Sampling details and stable isotope analysis scales (Busst & Britton, 2016, 2017). Correspond- ingly, for each captured fish, identification was to The study was conducted on the middle reaches of the species level, followed by measuring (fork length, River Teme, from the town of Tenbury Wells nearest mm) and the collection of between three and 0 0 (5219 N, - 224 W) to the village of Bransford five scales from the area between the base of the dorsal 0 0 (5210 N, - 216 W) (Fig. 1). Across the Teme fin and above the lateral line. As scales grow as fish catchment, altitude varies between 24.3 and 544.5 length increases, only the outer portion of scales mAOD, and land-use is primarily grassland (59%), reflects their most recent growth (Hutchinson & with some horticulture (24%) (CEH, 2018). In the Trueman, 2006; Basˇic´ et al., 2015). Consequently, study reach, the river generally comprised sequences only the very outer portion of the sampled scales was of pool and riffles, where maximum depths rarely used in SIA. One scale was prepared per fish, with this exceeded 2 m and widths rarely exceeded 15 m. A involving their thorough washing with distilled water, flow gauging station towards the downstream end of removal of the scale outer edge using dissection scissors and then drying to constant weight as per the the reach near Bransford had a long-term Q95 of 3 -1 3 -1 3 2.0 m s , Q50 of 10.2 m s and Q10 of 42.4 m 0? fish samples. The other scale samples were used to -1 s (CEH, 2018). In the study reach, the cyprinid fish age the fish (Amat-Trigo et al., 2017). Scale decalci- community had relatively limited diversity, with only fication was not performed prior to SIA, since the invasive B. barbus, and S. cephalus, dace Leuciscus removal of inorganic carbonates has no significant 13 15 leuciscus (Linnaeus, 1758) and minnow Phoxinus effect on scale d C and d N values (Sinnatamby phoxinus (Linnaeus, 1758) present. Grayling Thymal- et al., 2007, 2010; Woodcock & Walther, 2014). lus thymallus (Linnaeus, 1758) were also present in Concomitantly, qualitative samples for SIA of samples at the upper end of the reach and so were also macroinvertebrates were collected from two areas of 0 0 included in analyses. Other species that were the river, ‘Area 1 and ‘Area 2 . Samples in Area 1 123 262 Hydrobiologia (2018) 819:259–273 Fig. 1 Inset: location of the River Teme in Great Britain. Main study area was the stretch of the river between the two dashed map: The River Teme catchment showing its confluence with lines. Macroinvertebrates were collected at locations marked the River Severn. Arrows mark the direction of river flow. The with asterisks were collected from Tenbury Wells (5219 N, spp. larvae (n = 3 per Area) were also taken in 2016. 0 0 0 - 224 W) and Lindridge (5232 N, - 251 W), and All samples were taken back to the laboratory where 0 0 from Area 2 at Bransford (5210 N, - 216 W) in they were washed in distilled water and dried to June and September 2015 and 2016. Samples were constant weight as per the fish samples; note that in collected using kick sampling. Macro-invertebrate each case, one sample comprised between three and samples collected in 2015 contained very high six individuals. proportions of the amphipod Gammarus pulex (Lin- The dried muscle, scale and invertebrate samples naeus, 1758) in both sampling areas ([ 50%). Gam- were then submitted to the Cornell Isotope Laboratory marus spp. are common prey items for riverine fishes in New York, USA, for SIA. This involved the generally (e.g. MacNeil et al., 1999), as well as the samples being ground to powder, weighed in tin fishes analysed here more specifically (e.g. Mann, capsules (nearest 1,000 lg) and analysed on a Thermo 1974; Basˇic´ et al., 2015). Thus, samples were taken to Delta V isotope ratio mass spectrometer (Thermo describe the stable isotope data of fish putative prey in Scientific, USA) interfaced to a NC2500 elemental 2015. This sampling was repeated in 2016, with G. analyser (CE Elantach Inc. USA). Standards were pulex samples taken for SIA to enable consistent verified against international reference materials and temporal and spatial testing of differences in fish calibrated against the primary reference scales for 13 15 putative prey resources. However, to increase the d C and d N. The accuracy and precision were diversity of these baseline samples, samples of checked every ten samples using a standard animal Chironomid larvae (n = 6 per Area) and Trichoptera sample (mink). The outputs were values of d C and 123 Hydrobiologia (2018) 819:259–273 263 d N(%) for each sample. As C:N ratios were below correction on the stable isotope data, differences were 3.5, indicating low lipid content, there was no need for tested in the temporal data in the uncorrected and the d C to be lipid corrected (Post et al., 2007; Skinner corrected data of the juvenile fishes using ANOVA. et al., 2016). The juvenile fishes were used in preference to the adult fishes for this, as the diet of the latter was also likely to Data analysis have had some influence from angling baits containing ˇ ´ marine-derived fishmeal (Basic et al., 2015; Gutmann The 0? fish utilised in the analysis were all between Roberts et al., 2017). This testing was not completed 17 and 38 mm and in their first year of life. The for the 0? fishes, as their samples were taken from a juvenile fish were between 86 and 231 mm and single site in 2016. However, their data were also between ages 1? and 4? years; note that in this corrected to enable their results to be compared with length range, some L. leuciscus would have been the juvenile and adult fishes. The stable isotope sexually mature, but with B. barbus and S. cephalus correction equations were being immature. The adult fish, comprising only B. 15 15 d N  d N i base barbus and S. cephalus, were all C 386 mm TP ¼ þ 2 ð1Þ 3:4 (Table 2). The fish ages were derived by scale ageing using a projecting microscope and accounting annual 13 13 d C  d C i meaninv d C ¼ ð2Þ marks as per Amat-Trigo et al. (2017). For inter- corr CR inv specific data analyses, these length classes were considered separately. This was because the habitat where TP is the trophic position of the fish, d N is i i the isotopic ratio of the fish, d N is the isotopic use of these species tended to be quite different, with base the 0? fishes all sampled from marginal areas of the ratio of primary consumers, 3.4 is the fractionation between trophic levels and 2 is the trophic position of river where flows were minimal, the juvenile fishes were generally captured from relatively shallow and the baseline organism (Post, 2002); and d C is the corr corrected carbon isotope ratio of the fish, d C is the fast-flowing riffle habitats, and the adult fishes have uncorrected isotope ratio of the fish, d relatively large home ranges in the basin, often C is the meaninv mean invertebrate isotope ratio and CR is the exceeding 5 km (Hunt & Jones, 1974). By only inv 13 13 invertebrate carbon range (d C - d C ) (Ols- completing inter-specific analyses within these groups max min of lengths, then the data were being tested between son et al., 2009). The initial analyses using the corrected SI data tested fishes of relatively similar body sizes. This meant that these analyses would be more ecologically relevant for differences in TP and C between species and Corr between different life stages of the same species using testing the hypothesis than comparing data between species of very different length ranges (Basˇic & ANOVA or Welch’s test, with the latter used where the data were normally distributed but violated the assump- Britton, 2015). Prior to analysing the stable isotope analysis of the tion of homogeneity of variance. For each life stage, the corrected SI data were then used to test the significance fishes, the stable isotope data of the macro-inverte- 15 13 of differences in their d N-d C centroids, and differ- brate samples were tested for spatial (Area 1 versus ences in the positions and overlaps of their core trophic Area 2) and temporal (2015 vs. 2016) differences. 15 13 niches. For testing differences in the d N-d C Testing used generalized linear models (GLM) due to centroids per life stage and species, the SIA data were the relatively low sample sizes that were not normally normalised by square root transformation and a resem- distributed. The GLM revealed some significant differences (cf. Results). Thus, to enable the stable iso- blance matrix computed using Euclidean distances (Dethier et al., 2013). A PERMANOVA model was tope data of the juvenile and adult fish to be combined for use across the entire study reach, their isotopic data then fitted to this distance matrix using the adonis function in the vegan package in R. This calculated the required ‘correction’ (Jackson & Britton, 2014). 15 13 Correspondingly, the d N data were converted to significance of the differences in d N-d C centroids per group (Oksanen et al., 2007; R Core Team, 2017). trophic position (TP; Eq. 1) and the d C data were As the adonis function is similar to traditional corrected to C (Eq. 2) (Olsson et al., 2009; Jackson Corr ANOVA, it provided a pseudo F-statistic and P value & Britton, 2014). To identify the effect of this 123 264 Hydrobiologia (2018) 819:259–273 based on 999 permutations of the data (Dixon, 2003). revealed minimal differences in mean values, with Using the same method, it was then determined whether overlaps in their 95% confidence limits (Chironomid: different life stages within B. barbus and S. cephalus d C: Area 1: - 31.36 ± 0.39, Area 2: 15 13 15 had significant differences in theird N-d C centroids. 31.76 ± 0.42%; d N: Area 1: 9.88 ± 0.35, Area 2: With more than two life stages of fish being used per 9.74 ± 0.12%; Trichoptera: d C: Area 1: test, pairwise comparisons tested the significance of 32.36 ± 0.45, Area 2: 32.25 ± 0.38%; d N: Area differences between the groups, with Bonferroni 1: 9.20 ± 0.31, Area 2: 8.86 ± 0.42%). In G. pulex, adjustment for multiple comparisons. however, some spatial and temporal differences in To compare ‘core’ trophic niche size and overlaps their SI data were apparent that, when tested in GLMs, within and between species, the isotopic niche was revealed significant differences (d C: Wald 2 15 2 used, where the isotopic niche is an approximation of v = 12.05, P \ 0.01; d N: Wald v = 23.5, the trophic niche. It is acknowledged that the isotopic P \ 0.01; Table 1A). Pairwise comparisons of the niche varies slightly from the trophic niche due to it mean SI values from both models revealed these being influenced by factors other than diet (Jackson significant differences were both spatial and temporal et al., 2011), such as growth and metabolic rate of for both stable isotopes (Table 1B, C). Consequently, individuals (Busst & Britton, 2017). It was calculated the use of Eqs. 1 and 2 to correct the fish SI data used using the metric ‘standard ellipse area’ (SEA), a the G. pulex SI data only (Table 1A). Prior to data bivariate measure of the distribution of individuals in correction, there were significant differences in the isotopic space (Jackson et al., 2012). To examine the juvenile fish stable isotope data between years 13 15 size and overlap of the ‘core’ isotopic niches of each (ANOVA: d C F = 5.05, P = 0.03; d N 1,45 size group by species, ellipses were plotted that F = 11.56, P \ 0.01; Fig. 2A). However, these 1,45 enclosed 40% of the predicted data and thus the typical significant differences were no longer apparent fol- resource use of that life stage of fish. The ellipses were lowing isotopic correction (ANOVA: d C calculated within the R package SIBER v2.1.3 (Jack- F = 0.10, P = 0.75; d NF = 1.11, P = 0.30; 1,45 1,45 son et al., 2011, 2012) and, due to some relatively small Fig. 2B). Note that in the tests, SI data from L. sample sizes, a corrected Bayesian estimate of Stan- leuciscus were not included as they were only present dard Ellipse Area (SEA ) was calculated. This was in samples in 2016. followed by a calculation utilising a Markov chain Monte Carlo simulation with 10 iterations for each Intra- and inter-specific stable isotope analysed group that provided 95% confidence limits relationships (SEA ) of the isotopic niche size (Jackson et al., 2011; R Core Team, 2017). Using SEA , the extent of niche The lengths of each species were very similar across overlap (%) between species and life stages was then the 0? fishes. There was greater natural variation also estimated. This was determined using the maxi- between the lengths of fishes as juveniles (T. thymallus mum likelihood fitted standard ellipses, with the extent were smaller than other fishes) and adults (S. cephalus of the overlap between two groups thus represented by were generally smaller than B. barbus) (Table 2). The the overlap of their core niches. This was calculated only species with all life stages represented in analyses using Bayesian modelling in the SIBER package, with were B. barbus and S. cephalus. For B. barbus,C corr the denominator being the sum of non-overlapping was significantly higher in adults than the 0? fish and area of the two ellipses (Jackson et al., 2011). juveniles (P \ 0.01), whilst TP was significantly lower for adults versus the 0? fish (P \ 0.01) (Table 3). For S. cephalus, the 0? fish had signifi- Results cantly lower C than juveniles and adults (P \ 0.01) corr and significantly higher TP (P \ 0.01) (Table 3). Stable isotope correction for macro-invertebrate Between the species, differences in C between corr temporal and spatial differences 0? B. barbus and 0? S. cephalus were not signifi- cant, but was between both of these 0? fishes and Comparison of spatial differences in SI data of the 0? P. phoxinus (P \ 0.01; Table 3). The TP of 0? B. Chironomid larvae and Trichoptera spp. in 2016 barbus was significantly higher than both S. cephalus 123 Hydrobiologia (2018) 819:259–273 265 Table 1 (A) Mean stable isotope data of Gammarus pulex 14 (A) from the two sampled areas of the River Teme in 2015 and 2016, where values are estimates (± 95% CL) from the gen- eralized linear model (GLM), and their significance of differ- ences (as P values) according to pairwise comparisons with 13 15 Bonferroni adjustment in the GLM for (B) d C and (C) d N 12 (A) 13 15 Area Year n d C(%) d N(%) 1 2015 6 - 30.68 ± 0.58 10.78 ± 0.57 2016 4 - 29.44 ± 0.82 8.73 ± 0.71 2 2015 3 - 29.10 ± 0.82 10.22 ± 0.82 2016 6 - 29.86 ± 0.82 9.16 ± 0.82 (B) -31.0 -29.0 -27.0 -25.0 δ C(‰) d C Area 1, Area 1, Area 2, Area 2, 3.5 2015 2016 2015 2016 (B) Area 1, – 2015 3.0 Area 1, 0.05 – 2.5 Area 2, 0.01 1.00 – Area 2, 0.67 1.00 1.00 – 2.0 (C) 1.5 d N Area 1, Area 1, Area 2, Area 2, 2015 2016 2015 2016 1.0 -0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Area 1, – Ccorr Area 1, < 0.01 – Fig. 2 Uncorrected (A) and corrected (B) stable isotope data of ‘juvenile’ fish (except Leuciscus leuciscus) sampled in 2015 Area 2, 1.00 0.04 – (clear circle) and 2016 (filled circle) Area 2, < 0.01 1.00 0.43 – differences in C and TP between adult B. barbus corr and S. cephalus (P [ 0.05; Table 3). Sample number (n) represents the number of samples analysed, 15 13 where one sample = 3–6 individual gammarids Differences in d N-d C centroids Values in bold are significant at P B 0.05 The overall test for differences in the positions of the 15 13 d N-d C centroids of the 0? fishes was significant and P. phoxinus (P \ 0.01), although it was not (F = 15.72, P \ 0.01); pairwise comparisons indi- 2,58 significantly different between S. cephalus and P. cated the significant differences were between P. phoxinus (P [ 0.05; Table 3). In juveniles, C of B. corr phoxinus and the other fishes (P \ 0.01 in both cases), barbus was significantly lower than all other fishes but with differences between B. barbus and S. (P \ 0.01; Table 3). The TP of juvenile B. barbus was cephalus being not significant (P [ 0.05; Table 4). significantly higher than T. thymallus, significantly For the juvenile fishes, the overall model was signif- lower than L. leuciscus, but not significantly different icant (F = 18.41, P \ 0.01), with significant dif- 3,76 to S. cephalus (Table 3). There were no significant ferences between all species (P \ 0.01; Table 4). This TP δ N (‰) 266 Hydrobiologia (2018) 819:259–273 Table 2 The number, fish length ranges, mean lengths (95% CL) and measurement type (SL standard length, FL fork length) of each life stage of fish analysed for their stable isotopes across the two sampling areas Species n Length range (mm) Mean length (mm) (± 95% CL) Length measurement 0? B. barbus 30 18–34 25.2 ± 1.8 SL 0? S. cephalus 15 17–36 27.3 ± 2.4 SL 0? P. phoxinus 16 17–38 27.3 ± 2.8 SL Juvenile B. barbus 16 105–231 158 ± 15 FL Juvenile S. cephalus 16 112–207 153 ± 11 FL Juvenile L. leuciscus 30 102–214 167 ± 11 FL Juvenile T. thymallus 15 86–205 122 ± 16 FL Adult B. barbus 21 540–690 584 ± 17 FL Adult S. cephalus 21 386–570 466 ± 22 FL Table 3 Outputs of Species Test Testing df FP ANOVA/Welch’s test of corrected carbon (C ) and corr C corr trophic position (TP) for Barbus barbus ANOVA Life stage 2,64 32.76 \0.01 comparisons between life Squalius cephalus Welch’s Life stage 2,31 17.66 \0.01 stages and species for Barbus barbus and Squalius 0? ANOVA Species 3,60 10.01 \0.01 cephalus Juvenile Welch’s Species 3,36 16.61 \0.01 Adult ANOVA Species 1,40 2.09 0.16 Species/ life stage Test Testing df FP TP Barbus barbus ANOVA Life stage 2,64 47.17 \0.01 Squalius cephalus ANOVA Life stage 2,49 6.52 \0.01 0? ANOVA Species 3,60 12.36 \0.01 Juvenile Welch’s Species 3,30 60.53 \0.01 Note data for all sites and Adult ANOVA Species 1,40 0.02 0.90 years are combined was in contrast to the adult B. barbus and S. cephalus, Core isotopic niches (standard ellipse areas) which were not significantly different (F = 1.77, 1,41 The 95% confidence intervals of the core isotopic P = 0.18). 15 13 The model testing differences in d N-d C cen- niches (as standard ellipse areas) at each life stage suggested they were similar in size between the troids between the different life stages of B. barbus was significant (F = 28.89, P \ 0.01), with pair- species (Table 5). In general, the core isotopic niches 2,64 of the 0? fishes had low overlap (maximum 7% wise comparisons indicating the significant differ- ences were between adults and the other life stages between B. barbus and S. cephalus), the juvenile fishes (P \ 0.01; Table 4). Whilst the overall model was had no niche overlap, but in adult B. barbus and S. also significant in S. cephalus (F = 17.31, cephalus, their niches overlapped by 55% (Fig. 3). 2,49 P \ 0.01), pairwise comparisons indicated the signif- Within B. barbus, there was no overlap in their core icant differences were only between the 0? fishes and niches between the 0?, juvenile and adult fish (Fig. 3). the other life stages (P \ 0.01; Table 4). In S. cephalus, there was no niche overlap between 0? and juveniles, with this increasing to 2% between 123 Hydrobiologia (2018) 819:259–273 267 15 13 Table 4 The significance of differences in d N-d C centroids between the different life stages of the fishes, as represented by P values (with Bonferroni adjustment for multiple comparisons) derived in PERMANOVA 0? B. 0? S. 0? P. J B. J S. J L. J T. A B. A S. barbus cephalus phoxinus barbus cephalus leuciscus thymallus barbus cephalus 0? B. barbus - 0? S. cephalus 0.74 – 0? P. phoxinus \ 0.01* \ 0.01* – J B. barbus 0.22 – – – J S. cephalus – \ 0.01* – 0.01* – J L. leuciscus – – – 0.02* 0.01* – J T. thymallus – – – 0.01* 0.01* 0.02* – A B. barbus \ 0.01* – – \ 0.01* – – – – A S. cephalus – \ 0.01* – – 0.62 – – 0.18 – Table 5 Mean Lifestage and species C TP SEAc (± 95% CL) corr stable isotope data (± 95% CL) and standard ellipse 0? B. barbus 0.06 ± 0.38 3.30 ± 0.08 0.77 ± 0.28 areas (as SEAc; ± 95% CI 0? S. cephalus 0.49 ± 0.65 2.92 ± 0.13 0.96 ± 0.51 SEAb) for the sampled 0? P. phoxinus - 1.49 ± 0.49 3.02 ± 0.11 0.73 ± 0.36 fishes in the study river and across the three life stages Juvenile B. barbus 0.39 ± 0.58 2.70 ± 0.13 0.54 ± 0.28 (0?, juvenile and adult) Juvenile S. cephalus 2.57 ± 0.75 2.63 ± 0.14 0.59 ± 0.30 Juvenile L. leuciscus 1.42 ± 0.39 3.03 ± 0.05 0.44 ± 0.16 Juvenile T. thymallus 1.57 ± 0.20 2.13 ± 0.14 0.28 ± 0.14 Adult B. barbus 2.52 ± 0.40 2.62 ± 0.15 1.34 ± 0.58 Adult S. cephalus 3.22 ± 0.45 2.61 ± 0.15 1.89 ± 0.83 0 ? and adults, and then the juvenile niche sitting and core isotopic niches. The centroids were calcu- entirely within the adult niche (Fig. 4). lated using all SI data per life stage and species, whereas cores niches are based on a predicted 40% of the SI data to indicate typical resource use (Jackson Discussion et al., 2011, 2012). There were some consistent results from these analyses that aligned with Hypothesis 1, Hypothesis 1 tested whether there were consistent especially in the juvenile fishes where there were 15 13 inter-specific patterns of trophic partitioning between significant differences in d N-d C centroids between B. barbus and the other fishes. It was formulated due to all species and no overlaps in their core niches. In the these patterns of niche partitioning being evident 0? fishes, there was less consistency in the results of between the fishes in the B. barbus indigenous range both analyses, with isotopic niches showing low inter- 15 13 (Basic & Britton, 2016). An alternative to this specific overlap, but with d N-d C centroids show- hypothesis would be the fishes having high niche ing significant differences only between P. phoxinus overlap, as has been suggested between invasive and and the other fishes. Whilst there was poor alignment endemic Barbus fishes in Italian rivers, where it of the results in the adult fishes with Hypothesis 1, both 15 13 appears to have resulted in the competitive displace- analyses provided consistent results; the d N-d C ment of the endemics (Carosi et al., 2017). Hypothesis centroids of the adult B. barbus and S. cephalus were 15 13 1 was tested using two analyses, d N-d C centroids not significantly different and their core niches had 123 268 Hydrobiologia (2018) 819:259–273 This pattern was evident in rivers that had been (a) 4.0 stocked with hatchery-reared B. barbus at sizes below 3.5 ˇ ´ 250 mm and remained evident in adult fishes (Basic 3.0 and Britton, 2016). In contrast, Gutmann Roberts et al. 2.5 (2017) revealed that in the lower reaches of the study 2.0 river, there was high overlap in the core isotopic 1.5 niches of adult B. barbus and S. cephalus, primarily 1.0 the result of individual fishes specialising in the -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 consumption of pelletized marine fishmeal utilised by (b) 4.0 anglers. This niche overlap was also evident in the 3.5 adult fishes here, where inter-specific niche differ- 3.0 ences were only significant in the 0? and juvenile fishes. In B. barbus, there were strong and significant 2.5 patterns in niche partitioning between their different 2.0 life stages, suggesting considerable ontogenetic shifts 1.5 in their diet that resulted in their population having a 1.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 relatively large core isotopic niche that was composed of at least three distinct sub-sets. This was consistent (c) 4.0 15 13 with Hypothesis 2, although the d N-d C centroids 3.5 suggested differences were not significant between the 3.0 0? and juvenile fish. In contrast, the isotopic niches of 2.5 S. cephalus were more similar over their three studied 2.0 life stages, with only the niche of the 0? fish being 1.5 distinct from the other life stages, with the juvenile and 1.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 adult niches overlapping completely, contrary to Ccorr Hypothesis 2. Fig. 3 Corrected Carbon (C ) versus trophic position (TP) Stable isotope data of 0? fishes can be confounded corr for Barbus barbus (filled triangle), Squalius cephalus (filled by issues of their data still showing a strong parental square), Leuciscus leuciscus (delta) and Thymallus thymallus signal. For example, in anadromous brown trout Salmo (open square), and the positions of their core isotopic niches (as trutta, newly emerged fry retained a strong parental, SEA ), where solid line: B. barbus, small dashed line: S. marine-based isotopic signal that enabled their differ- cephalus, long dashed line: L. leuciscus, and dash/dot line: T. thymallus.(a)0? fishes; (b) juvenile fishes; and (c) adult fishes entiation from fry produced from non-anadromous parents, but this difference was much reduced after relatively high overlap (55%). Across all life stages four months of feeding in freshwater (Briers et al., and analyses, there was no evidence to support the 2013). In 0? smallmouth bass Micropterus dolomieu, alternative hypothesis that invasion by B. barbus had post-hatch embryos had elevated d N values that resulted in competitive displacement of native fishes, were associated with their parental origin, but these as suggested by Carosi et al. (2017) for endemic values subsequently decreased rapidly due to their Barbus. It is, however, acknowledged that this was not exogenous feeding during their metamorphosis from tested implicitly here, given the absence of data from larvae into juveniles (Vander Zanden et al., 1998). the pre-invaded period or from sites with B. barbus Here, the 0? fishes utilised were all of lengths above absent. 17 mm, were all fully formed juveniles rather than The pattern of isotopic niche partitioning between larvae, and were up to 10 weeks old. Their stable iso- B. barbus and other fishes was thus consistent with a tope data were very distinct from those of the adult number of isotopic studies completed on populations fishes; in terms of uncorrected data, the 0? fishes were in their indigenous range (Basˇic´ et al., 2015;Basˇic´ and depleted in d Cbyupto8% compared to adult Britton, 2015, 2016). These studies all suggested that conspecifics. Consequently, the strong patterns of core B. barbus and S. cephalus have distinct core isotopic isotopic niche partitioning detected in these 0? fishes niches, with minimal inter-specific resource sharing. were interpreted as resulting from their dietary TP Hydrobiologia (2018) 819:259–273 269 Fig. 4 Intra-specific (a) 4.0 comparisons of Corrected Carbon (C ) versus corr trophic position (TP) and 3.6 positions of core isotopic niches (as SEA ) for (a) Barbus barbus and (b) Squalius cephalus, and 3.2 where filled diamond, solid line: 0? fish; open circles, dashed line: juvenile fish; 2.8 filled triangle, dotted line: adult fish 2.4 2.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 4.0 (b) 3.6 3.2 2.8 2.4 2.0 -3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 Ccorr differences formed by their exogenous feeding within all samples from all areas sampled (in contrast to other the river, rather than being a legacy of their parental macro-invertebrate taxa), there were significant dif- isotopes. ferences in their isotopic data between years and sites In this study, the fish SI data were ‘corrected’ to (whereas data from other macro-invertebrate taxa enable data to be combined across two sampling years revealed similar values, at least spatially), and liter- and relatively long stretch of river. The use of standard ature suggests Gammarus spp. are an important prey equations to ‘correct’ SI data in this manner is well item for many fishes (e.g. MacNeil et al., 1999). established (e.g. Olsson et al., 2009; Jackson & Correction of the juvenile fish SI data using the G. Britton, 2014). However, this correction relies upon pulex data was also demonstrated as removing signif- an adequate description of the SI data of the fish prey icant temporal differences. To enable the SI data of the resources. Here, correction focused on use of G. pulex 0? fishes to be comparable to the other fishes, they SI data. The rationale for this was they were present in were also corrected using the G. pulex data, although TP 270 Hydrobiologia (2018) 819:259–273 stomach contents analyses (SCA) for the 0? fishes barbus presence, it is acknowledged that this is had suggested that these amphipods were a minor prey speculative given that isotopic niche sizes of the item (Gutmann Roberts & Britton, 2018). However, native fishes were unable to be measured in B. barbus individuals of [ 20 mm standard length in all the absence. Notwithstanding, the inter-specific isotopic 0? fish species analysed had infections of the intesti- niche partitioning evident in the study suggests that nal parasite Pomphorhynchus tereticollis (C. Gutmann despite their similar ecological guilds and sharing Roberts, unpublished data). This parasite has gam- similar habitats (especially the 0? fishes), there were marids as its intermediate host (Kaldonski et al., sufficient differences between the fishes in their 2008), suggesting G. pulex might have been consumed functional traits and/or habitat utilisation to enable in greater proportions in the 0? fishes than suggested substantial differentiation in their core isotopic niches by SCA. Moreover, in the River Severn basin, to occur (Robinson et al., 1993; Borcherding et al., Pomphorhynchus spp. has been reported as prevalent 2013; Negus & Hoffman, 2013). in all the fishes studied here (Brown 1984), suggesting On one hand, the results here could suggest that the gammarids are a common and important prey item of ecological impacts of invasive B. barbus are relatively fish in the river. Therefore, although it is acknowl- minor in the river, as there was little evidence to edged that the macro-invertebrate baseline SI data suggest there was high diet similarity in the fishes at used to correct the data here could have utilised a their most abundant life stages (0? and juveniles). wider range of taxa, especially in 2015, it is strongly This inference is supported by other recent studies on argued that the use of G. pulex SI data to correct the native B. barbus that have revealed strong patterns of fish SI data was justified and appropriate. inter-specific core isotopic niche partitioning (e.g. Following introductions of non-native fishes, Basic & Britton, 2015, 2016). However, these studies adverse ecological impacts often develop through were all limited to assessing trophic interactions via increased inter-specific competition for food resources stable isotope analysis, with studies suggesting that between invasive and sympatric native fishes (Gozlan when compared with other dietary analysis methods, et al., 2010; Cucherousset et al., 2012). Given the such as stomach contents analyses, different results relatively similar size ranges of the invasive B. barbus can occur, resulting from differences between items with other cyprinid fishes across the different life ingested (stomach contents) and assimilated (SIA) stages (albeit with some inter-specific length differ- (e.g. Locke et al., 2013). Consequently, some caution ences within life stages), this suggests there was is necessary if isotopic niche overlaps are to be used to considerable potential for inter-specific competitive infer the strength of competitive interactions. More- interactions, especially given the fishes were from over, invasive B. barbus can potentially result in other relatively similar functional guilds (Basic & Britton, ecological concerns, such as causing habitat alter- 2016). However, the lack of overlap in the isotopic ations, given recent work has demonstrated that in niches of the 0? and juvenile fishes—the life stages their native range, B. barbus act as ‘zoogeomorphic when their abundances tend to be highest—suggested agents’ (Pledger et al., 2014, 2016). This is where their low dietary overlap, with only the isotopic niches of benthic foraging activities can reduce bed material the adult fishes indicating some dietary overlap. stability, increase bedload transport, and impact Schulze et al. (2012) suggested that species within microtopographic roughness and sediment structure the same ecological guild can only coexist when they (Pledger et al., 2014, 2016). This benthic foraging respond differently to limited resource availability could then also impact upon aspects of the macro- with, for example, specialised species only persisting invertebrate communities, such as decreased abun- if their competitors are generalists. Evidence in dance via predation or reduced species richness via literature supports this, with reduced trophic niche disturbance. However, these aspects were beyond the sizes in many co-existing fishes when compared to scope of this study and so further research is required allopatry (Bolnick et al., 2010; Tran et al., 2015). In to provide increased understandings of how B. barbus the study river, however, even where the isotopic invasions affect macro-invertebrate communities and niches of the fishes were partitioned, the niches were sediment structure. Finally, it should also be noted that similarly sized. Although this suggests there had not the study river was low in fish species richness, with a been any niche constriction in the native fishes in B. cyprinid fish community comprising only four species 123 Hydrobiologia (2018) 819:259–273 271 assessments of trophic relationships in riverine fish com- (including B. barbus), with other fish taxa being very munities. Journal of Applied Ichthyology 31: 296–300. limited in diversity and abundance in the study reach, Basˇic´, T. & J. R. Britton, 2016. Characterizing the trophic niches and with no other Barbus species present. Conse- of stocked and resident cyprinid fishes: consistency in quently, if B. barbus are introduced into a river with partitioning over time, space and body sizes. Ecology and Evolution 6: 5093–5104. considerably higher native fish species richness, Basˇic´, T., J. R. Britton, M. C. Jackson, P. Reading & J. Grey, irrespective of the presence of any other Barbus 2015. Angling baits and invasive crayfish as important species, there is the possibility that there will be a trophic subsidies for a large cyprinid fish. Aquatic Sciences greater probability of higher niche overlaps within 77: 153–160. Basˇic´, T., J. R. Britton, S. P. Rice & A. G. Pledger, 2017. species in the fish community and thus higher potential Impacts of gravel jetting on the composition of fish for ecological impacts to result. It is therefore spawning substrates: Implications for river restoration and recommended that such introductions proceed only fisheries management. Ecological Engineering 107: 71–81. with caution and full risk assessment (Roy et al., Bolnick, D. I., T. Ingram, W. E. Stutz, L. K. Snowberg, O. L. Lau & J. S. Paull, 2010. Ecological release from inter- 2018). specific competition leads to decoupled changes in popu- In summary, across three life stages of invasive B. lation and individual niche width. Proceedings of the Royal barbus, there were some strong patterns of isotopic Society—Biological Sciences 277: 1789–1797. niche partitioning with native fishes, with this parti- Borcherding, J., M. Dolina, L. Heermann, P. Knutzen, S. Kru- ger, S. Matern, R. van Treeck & S. Gertsen, 2013. Feeding tioning initially evident between some fishes during and niche differentiation in three invasive gobies in the their first year of life that became strongly apparent at Lower Rhine, Germany. Limnologica 43: 49–58. juvenile life stages. These invasive B. barbus thus Briers, R. A., J. O. Waterman, K. Galt & R. N. Campbell, 2013. integrated into this riverine food web via exploiting Population differentiation and temporal changes of car- otenoid pigments and stable isotope ratios in the offspring different food resources to the native fishes that of anadromous and non-anadromous trout Salmo trutta. facilitated their co-existence. Ecology of Freshwater Fish 22: 137–144. Britton, J. R. & J. 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