Hydrobiologia (2018) 820:267–279 https://doi.org/10.1007/s10750-018-3664-2 PRIMARY RESEARCH PAPER Habitat selection and reproductive success of coot Fulica atra on ponds under different ﬁsh size and density conditions Marek Nieoczym Janusz Kloskowski Received: 16 January 2018 / Revised: 9 May 2018 / Accepted: 21 May 2018 / Published online: 31 May 2018 The Author(s) 2018 Abstract Fish may inﬂuence habitat selection and trophic impact of ﬁsh or ﬂedgling production was reproductive success in waterfowl. We investigated additionally limited by factors other than food. Carp the effects of common carp Cyprinus carpio on may adversely affect pond habitats of waterfowl both breeding coots Fulica atra along a gradient of ﬁsh via trophic interactions and through abiotic distur- size structure and density, created by separate stocking bance of ecosystem processes. In coots, however, the of age cohorts in ponds in eastern Poland. Coot effects can be mitigated by maintenance of abundant breeding densities were higher on ponds with low emergent vegetation and of submerged macrophytes biomass of small-sized, young-of-the-year ﬁsh than on resistant to ﬁsh. ponds with medium- or large-sized ﬁsh, stocked at high biomass densities; they also increased with Keywords Anthropogenic ponds Common carp increasing submerged vegetation biomass (an effect Fish–bird interactions Food supply Herbivory correlated with water transparency) and emergent Waterfowl vegetation cover. Densities of nektonic and epibenthic macroinvertebrates and of amphibian larvae were also negatively inﬂuenced by ﬁsh size/density gradient, while densities of emerging insects were not affected. Introduction However, coot breeding success per pair was similar among pond types, while positively related to sub- Interactions with ﬁsh can be crucial for habitat merged vegetation, indicating that either plant food selection and breeding success in many waterbird abundance was more important than the overall species. These interactions include food competition and reciprocal predation, but also a wide array of indirect ﬁsh effects, ranging from ecological engi- Handling editor: Stuart Halse neering to behavioural responses to ﬁsh by prey common to ﬁsh and aquatic birds (Hurlbert et al., M. Nieoczym (&) 1986; Giles, 1994; Hanson & Butler, 1994; Haas et al., Department of Zoology, Animal Ecology and Hunting, 2007; LeBourdais et al., 2009). The role of ﬁsh in University of Life Sciences, Akademicka 13, 20-033 Lublin, Poland structuring waterbird communities has grown in e-mail: firstname.lastname@example.org importance with increasing intensiﬁcation of ﬁsh- related management of inland waters, including J. Kloskowski world-wide ﬁsh introductions and conversion of Institute of Zoology, Poznan University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznan, Poland 123 268 Hydrobiologia (2018) 820:267–279 wetlands to aquaculture. Many waterfowl species have carp population characteristics (reviewed in Rahman, experienced population changes linked to increased 2015; Vilizzi et al., 2015). Consequently, ponds used ﬁsh presence (Musil, 2006; Bajer et al., 2009; Nummi for carp rearing differ in their suitability for breeding et al., 2016), probably because their roles in food webs birds, depending on culture conditions and intensity are similar to those of ﬁsh, but little is known about the (IUCN, 1997; Musil, 2006; Broyer & Calenge, 2010; relationships between ﬁsh and one of the most see also Lemmens et al., 2015). Differential pond common western Palearctic waterfowl species, the stocking practices provide an excellent opportunity to Eurasian Coot (Fulica atra Linnaeus, 1758). Owing to study the effects of ﬁsh on waterbirds, serving as a the often dominant position of coot in waterbird basis for large-scale whole-system natural experi- communities, particularly in shallow, eutrophic wet- ments, where ﬁsh populations (and their impact on lands (e.g. Nilsson, 1978; Paracuellos, 2006; Haas aquatic communities) are manipulated. Previous et al., 2007), its trophic impact via grazing pressure on research on carp ponds has shown strong effects of submerged macrophytes may have ecosystem-scale ﬁsh individual size and density on habitat selection by consequences, i.e. it may affect macrophyte abun- waterbirds (Haas et al., 2007; Kloskowski et al., 2010). dance and community structure and contribute to Typically, ponds with low ﬁsh biomass support the shifts between a macrophyte-dominated clear water highest diversity and abundance of macroinvertebrates state to a phytoplankton-dominated turbid state, and submerged vegetation (Broyer & Calenge, 2010; analogously to ﬁsh effects (Perrow et al., 1997; Nieoczym & Kloskowski, 2015) and offer the most Søndergaard et al., 1997; van Altena et al., 2016; but favourable conditions for many waterfowl, due to low see Hansson et al., 2010; Chaichana et al., 2011; competition for food during the chick stage (Hill et al., Marco-Mendez et al., 2015). Coot populations have 1987; Hanson & Butler, 1994; Haas et al., 2007). been shown to be sensitive to ﬁsh, presumably due to Other pond attributes, such as water area, nesting site negative ﬁsh impact on submerged macrophytes and availability and shelter from predators, can be impor- aquatic insects (Houdkova´ & Musil, 2003; Maceda- tant for bird habitat selection as well (e.g. Staicer et al., Veiga et al., 2017), i.e. food resources of coots. 1994; Paracuellos, 2006; Broyer & Calenge, 2010). Farming of carp species in open ponds, the However, in human-managed aquatic systems, bird principal component of freshwater aquaculture indus- habitat preferences may not match the actual habitat try in Central and Eastern Europe and Asia (Szu¨cs suitability due to unpredictable habitat dynamics, such et al., 2007), provides habitats for waterbirds, espe- as seasonal changes in food supplies or water-level cially in areas where natural wetlands are sparse or ﬂuctuations (Anteau et al., 2012; Kloskowski, 2012). have been converted to aquaculture (IUCN, 1997). Here we used separate stocking of ponds with carp age Waterbirds that are not piscivorous are typically not cohorts as the context for a natural experiment to deterred from ﬁsh ponds and may ﬁnd suitable breed- investigate coot habitat selection and breeding success ing conditions there. Coot densities have been reported in relation to the age structure of ﬁsh. Carp effects on to be considerably higher on carp ponds than on aquatic ecosystems are size-dependent, as prey cap- natural wetlands (Kozulin et al., 1998). On the other ture and ingestion are limited by gape size and because hand, cultured and widely stocked carp species are larger individuals tend to penetrate deeper into the capable of adversely affecting entire ecosystems, both sediments and to mobilise phosphorus through sedi- via trophic inﬂuences and habitat modiﬁcation (Pı´pa- ment suspension (Lammens & Hoogenboezem, 1991; lova´, 2006; Bajer et al., 2016; Collins & Wahl, 2017). Driver et al., 2005; Kloskowski, 2011). The species Common carp (Cyprinus carpio Linnaeus, 1758) is the has been reported to increase phytoplankton produc- most notorious for substantial top-down and bottom- tion and decrease water transparency and macrophyte up effects through omnivorous feeding, mainly on coverage, with effects generally increasing with ﬁsh detritus, benthic macroinvertebrates and zooplankton; density (Weber & Brown, 2015). Since under pond however, the foraging-related abiotic inﬂuence of carp conditions ﬁsh age corresponds to combined ﬁsh may create an even stronger disturbance pathway, with individual size and density, the carp age gradient was declines in water transparency and submerged macro- equivalent to a gradient of carp trophic pressure on phytes (Vilizzi et al., 2015; Kaemingk et al., 2017). pond communities. We considered habitat variables Variation in ecosystem responses can be attributed to related to the availability of animal and plant food, 123 Hydrobiologia (2018) 820:267–279 269 shelter, and nesting sites, all of which could be 2215–26 E). The ponds were of similar depth (mean potentially affected by ﬁsh. We expected ponds with values varying from 0.7 to 1.3 m over the study lower trophic pressure of ﬁsh to support higher levels period), ringed with emergent vegetation (mostly of animal and plant food for waterfowl (Lemmens reeds Phragmites australis (Cav.) Trin. ex Steud, et al., 2013), leading to positive habitat selection and 1841 or bulrush Typha spp.), and with surface areas higher breeding success in coots. ranging from 1 to 13 ha (with one pond of 23 ha). They were ﬁlled with water from nearby rivers and precipitation from February until the end of March, Materials and methods and drained between September and November. A gradient of ﬁsh impact was created by stocking 3 year Coot biology (size) cohorts of carp in separate ponds: young-of-the- year (0?) ﬁsh, individual total length 3–4 mm The coot is a semi-precocial species; chicks are (1.5–3.0 mg of weight), 1-year-old ﬁsh (1?), brooded on the nest for about 3–4 days and then the 110–160 mm (about 30–60 g) or 2-year-old (2?) ﬁsh, nest is abandoned, although it often remains used by 190–240 mm (about 140–300 g). The total biomass of the family for roosting. The young start diving for food 0? ﬁsh at stocking was practically negligible, but by at 3–5 weeks old and gradually become independent mid-July it had reached about 50 kg/ha. The 1? ﬁsh of their parents by 6–8 weeks of age. Coots rarely raise were stocked at densities of 98–390 kg/ha and the 2? two broods per season, but early clutch failure is ﬁsh at 149–308 kg/ha, respectively. We assumed that typically followed by a replacement clutch, which ﬁsh impact on pond ecosystems should increase with occasionally may be repeated (Taylor, 1998). Coots age, i.e. with increasing individual size (and correlated rely on the feeding conditions provided by the nesting biomass density) of stocked ﬁsh, although the 1? and pond because breeding pairs are strictly territorial and 2? ponds differed in ﬁsh size but did not, on average, family groups stay together in the same area of the differ in total biomass. Young-of-the-year carp from pond at least until the chicks are self-supporting July and older carp from May received broken cereal (Horsfall, 1984; Taylor, 1998; Varo, 2008). grains as supplemental feed, distributed in proportion Food is a substantial factor limiting reproductive to ﬁsh density, which could stimulate the productivity success in coots (Horsfall, 1984; Brinkhof & Cave, of the ponds and might be directly consumed by 1997). Coots rely on plant matter as the main food waterfowl; however, it was unlikely to contribute source during most of their life cycle (Hurter, 1972; signiﬁcantly to the coot diet during the breeding Metna et al., 2015). During the breeding period, season, since the grains were supplied in a limited area however, the share of animal food increases, because a of the pond, while breeding coots only feed within protein-rich diet is crucial for breeding females and their own territories (Horsfall, 1984). Hunting of young birds (Borowiec, 1975; Horsfall, 1984; Brin- waterfowl, including coots, was permitted at all study khof, 1997). Generally, the relative proportion of plant ponds from 15 August, i.e. after the assumed end of the and animal matter in the diet of the species is highly waterfowl breeding season, to 21 December. We dependent on available resources. The animal diet of collected data from 35 ponds altogether (12 ponds coots consists of a variety of macroinvertebrates, with 0? ﬁsh, 13 ponds with 1? ﬁsh and 10 ponds with including emerging aquatic insects, and to a lesser 2? ﬁsh); 12 ponds were sampled per year in 2005 and 2007 and 11 ponds in 2006. A more detailed descrip- extent vertebrates, such as amphibian larvae and small ﬁsh (Collinge, 1936; Borowiec, 1975; Horsfall, 1984; tion of the study system is given in Nieoczym & Taylor, 1998). Kloskowski (2015). Study system Coot surveys The research was conducted on semi-natural managed, Coot counts were conducted during the breeding drainable ponds, scattered in loose clusters in an season from April to the ﬁrst week of August at agricultural landscape north and west of the City of approximately weekly intervals. Coots were recorded Lublin in south-eastern Poland (5117–33 N, using binoculars and spotting scopes by an observer 123 270 Hydrobiologia (2018) 820:267–279 walking along levees around the ponds (round count the other hand, estimates of chick production based on method, Koskimies & Va¨isa¨nen, 1991). The numbers successfully hatched nests may omit early brood losses of breeding pairs were estimated based on observa- and include repeated broods of pairs not classiﬁed as tions of territorial birds using the maximum number double-brooded. observed per pond in April–May. When estimating the number of pairs, single adults observed close to each Habitat variables other, i.e. presumably within the same territory, were added for total pair count; ﬂocking birds were not Data on ﬁsh stocks (ﬁsh age, size structure and considered breeders. Nests were not searched for stocking density) were obtained from local ﬁsheries. systematically, but mainly along with other ﬁeldwork Submerged and ﬂoating vegetation (including activities in all pond types. Clutch size was determined macroalgae such as Charophyta) was sampled once in 89 nests for which the ﬁnal egg number was per breeding season during the maximum vegetation conﬁrmed during two visits at least 1 week apart. Pairs period, from 30 June and 2 July; eight samples were with broods were relatively easy to observe, as they collected using a Bernatowicz rake along two perpen- usually fed on open water; for each pond the number of dicular 30- to 45-m transects per pond. In the broods was estimated based on weekly surveys, laboratory, dead plant litter was removed and live eliminating from the records all repeated observations plants were identiﬁed to species, dried to constant weight and weighed to within 0.001 g (Nieoczym & of the same brood, as indicated by mapped locations of broods and brood-tending adults and by the age of Kloskowski, 2014). Water transparency was measured chicks. Broods hatched until the end of May were using a 12-cm Secchi disc concurrently with the classiﬁed as ‘early’ and those hatched in June–July as sampling of submerged vegetation. Nektonic and ‘late’ (with a distinct break in the seasonal hatching epibenthic macroinvertebrates and amphibian larvae pattern between 31 May and 8 June). Precise deter- were captured using submerged 1-l activity traps, at mination of hatching time was difﬁcult in the absence half-month intervals between 20 April and 15 July (six of regular nest checks; in most pairs, complete sampling sessions per pond, 10 traps per session) at the hatching could be inferred only from observations of interface between open water and emergent vegetation both parents with the brood off the nest. The hatching (for methodological details see Nieoczym & Klos- date of the clutch was backdated with accuracy of kowski, 2015). Macroinvertebrates, with the excep- about 1 week based on the date of the earliest brood tion of leeches Hirudinea, were identiﬁed to at least appearance and the colour characteristics of the order level, dried to constant weight and weighed. Of chicks’ plumage (Fjeldsa˚, 1977). the invertebrate taxa captured by the traps, those We deﬁned post-hatching breeding success as the known to be consumed by coots were included in the maximum number of [ 3-week-old juveniles analyses: Gastropoda, Hirudinea, Odonata, Hemi- observed with parents; chicks close to ﬂedging are ptera, and Coleoptera (Taylor, 1998). Amphibian difﬁcult to assign to a brood due to the decreasing larvae were wet-weighed after drip-drying and cohesiveness of family units. Coots 3 weeks and older released. differ in plumage characteristics from younger chicks Emerging insects (Ephemeroptera and Diptera) in that they develop white cheeks and breast (Fjeldsa, were sampled using vertically positioned emergence 1977). We assumed brood size at this age to be a traps between May and July in 2006 and 2007. In the reliable substitute for ﬂedging success because coot second week of each month, ten 4-l plastic traps chick mortality is concentrated within the ﬁrst (height 22 cm) were deployed per pond for 24 h. Each 2–3 weeks after hatching (Varo, 2008;Re˛k, 2010). trap had an inverted funnel covering an area of We used two measures of breeding success: per pair 200 cm and a 41-mm opening at the narrow end per season and per pair that successfully hatched at (construction similar to that used by Danell & Sjo¨berg, least one chick. We acknowledge the bias associated 1977). The greater part of the trap rested below the with each approach; as birds were not marked, when water surface. The traps were held in pairs by wooden assessing breeding success per pair per season we stakes more or less evenly distributed in the open could not ascertain whether any breeding pairs were water area. The locations of the traps were the same occasionally replaced by other pairs in the territory; on during each trapping event. Trap contents were 123 Hydrobiologia (2018) 820:267–279 271 preserved in 70% ethanol; the number of emerging size (all P [ 0.8). In the analyses of clutch size we insects caught by a trap was based on the maximum limited habitat variables to ﬁsh gradient. number of either imagines or pupae, depending on Prior to model construction, we used Pearson’s which were more numerous. Catches from both coefﬁcient to investigate relationships between pre- activity traps and emergence traps can be inﬂuenced dictor variables. Pond area was used in the analyses to by water temperature, which determines oxygen calculate pair/brood densities. Since breeding territo- solubility and affects invertebrate and larval amphib- ries on larger waterbodies may concentrate in the ian activity, as well as the diel emergence patterns of littoral zone near the shore, it could be argued that insects (Henrikson & Oscarson, 1978; Kureck, 1979; waterfowl numbers per unit of shoreline would be a but see Murkin et al., 1983). To reduce the effects of better measure of waterfowl abundance than numbers temperature differences between ponds during trap- per unit of water area (Nilsson, 1978). However, the ping sessions, traps were set in all ponds on the same ponds studied were uniformly shallow, often with day (exceptionally with a 1-day difference). Sampling scattered patches of emergent vegetation and coot was conducted on sunny and windless days. Water nests in the central part of the pond, the whole ﬂooded temperature was taken using a thermometer suspended area corresponding to the littoral zone of stratiﬁed midway in the water column on the day of trap lakes. Moreover, the ponds were of regular shape and deployment (9.00 a.m.–4.00 p.m.). the shoreline length was strictly correlated with water area size (r = 0.92, P \ 0.001). Since ﬁsh gradient We quantiﬁed pond area, shoreline length and proportional cover by emergent vegetation from was assumed to be the causative factor controlling digitised aerial photographs using the GIS-software abundance of macroinvertebrates and amphibians (see QGIS 2.8 Wien. Data on the surrounding habitat ‘‘Results’’ section), to mitigate collinearity issues, matrix were available from aerial images; however, nektonic macroinvertebrate and larval amphibian since our previous research on the local waterfowl biomass were omitted from the mixed models. Sim- communities indicated that landscape-level character- ilarly, submerged vegetation biomass was signiﬁ- istics were insigniﬁcant for selection of the breeding cantly correlated with Secchi depth (r = 0.36, pond (Kloskowski et al., 2010) and we were primarily P = 0.034); submerged vegetation was retained for interested in the effects of ﬁsh on breeding conditions, model selection since it yielded better univariate we focused on pond attributes. models and as a food source was assumed to be more important for breeding coots. Since the GLMMs Data analysis included only 2–4 predictor terms, for predictions we considered full models. However, minimal models Generalized linear mixed modelling (GLMM) with a (the subsets of signiﬁcant independent variables) log link and Poisson distribution was adopted to relate achieved by backward stepwise selection yielded the coot densities, clutch size and breeding success same patterns of results. measures to habitat variables. Pair/brood densities Densities of newly hatched broods on ponds and the were analysed at the pond level with year as a random relative biomass abundances of macroinvertebrates term to take account of the non-independence of known to be taken by coots and of amphibian larvae observations within years. An offset variable (the were compared between pond types using repeated natural log of the pond surface area) was speciﬁed in measures (RMs-)ANOVA with count/sampling ses- the models to account for differences in pond size. sion as the repeated factor. Year identity was included Clutch size and breeding success were analysed at the as a ﬁxed term in the RM-ANOVAs, but as it was not pair level, with timing of breeding (early vs. late signiﬁcant in any model (all P [ 0.5), it was omitted. broods) as an additional ﬁxed term and pond as a A Greenhouse–Geisser correction was used when random factor. Year was omitted to simplify the sphericity could not be assumed. models run at the level of individual pairs, as it was not When necessary, data were natural log transformed signiﬁcant when tested as a ﬁxed effect. We did not to reduce heteroscedasticity. Two-tailed statistical account for pair density on the pond in the analyses, signiﬁcance was deﬁned at the 0.05 level; means are because it was not correlated with clutch or ﬁnal brood given ± 1 SE. Post hoc comparisons were performed using the least signiﬁcant difference (LSD) test. The 123 272 Hydrobiologia (2018) 820:267–279 analyses were conducted in Statistica v. 13 (StatSoft, positively related to submerged vegetation abundance, Inc.) and GenStat v. 15 (VSN International Ltd.). while the model of breeding success per successful nesting attempt indicated the importance of brood phenology, with early broods producing more ﬂedg- Results lings than late broods (means 3.10 ± 0.22 vs. 2.47 ± 0.20, respectively; Table 1). Over the 3 years, the total number of coot breeding RM-ANOVA conﬁrmed that densities of newly pairs per year on the study ponds was estimated to be hatched broods throughout the breeding season -1 201 (range of densities per pond 0–4.00 ha , mean depended on the ﬁsh gradient; the time effect was 1.41 ± 0.17). The earliest newly hatched broods were signiﬁcant as well (Table 2). Fish gradient also had a observed towards the end of April each year, and the signiﬁcant inﬂuence on biomass abundance of latest in mid-July. Altogether we recorded 171 broods macroinvertebrates and amphibians in ponds (Table 2; (78 early and 93 late broods) at densities varying see also Fig. 3, where for the sake of illustration, data -1 between 0 and 3.6 ha (mean 1.10 ± 0.16). for all pond types were combined). In all RM- GLMM models showed that both breeding pair and ANOVAs, both on brood and on nektonic and brood densities of coots were related to the ﬁsh epibenthic prey densities, 0? ponds had signiﬁcantly gradient (Fig. 1) and increased with increasing higher means than ponds with older-age ﬁsh (LSD biomass of submerged and ﬂoating vegetation in the tests). During the trapping sessions, water tempera- pond (Table 1). Post hoc LSD tests indicated that 0? tures were similar between ponds and roughly consis- ponds supported higher numbers of pairs and broods tent between years, showing a gradual increase until than ponds with older-age ﬁsh. When Secchi trans- the end of June (Fig. 3A), with the exception of a cold parency was entered into the model, replacing sub- spell in late May 2006, when the temperature in the merged vegetation, it proved signiﬁcant as well (both ponds dropped to 13–15C. For the data pooled over P \ 0.05). Clutch size did not differ between pond pond types and the three study years, peak density of types (F = 1.44, P = 0.264) or between early and newly hatched broods coincided with peak abun- 2, 18 late nesting attempts (F = 0.72, P = 0.400). dances of macroinvertebrates and amphibians in early 1, 72 Similarly, models of breeding success showed no June. However, densities of newly hatched broods relationship with ﬁsh size structure/density (Fig. 2); recorded throughout the season were not correlated however, breeding success per pair per season was with the concurrent levels of macroinvertebrates and larval amphibians (Spearman r = 0.26, P = 0.623 and r = 0.60, P = 0.208, respectively, both N =6; Fig. 3B–D). Densities of emerging insects signiﬁ- cantly declined with time in all pond types (RM- ANOVA F = 3.86, P = 0.029) and were not 1,40 affected by the ﬁsh gradient (F = 1.41, 2,20 P = 0.268; Fig. 4). The emergence trap results may have been biased by the disproportionate occurrence of potential predators (leeches, Anisoptera nymphs, adult Dytiscidae and smooth newts Lissotriton vul- garis Linnaeus, 1758) that may consume insects as they emerge; in 0? ponds, mean fractions of traps with predators varied monthly between 20 and 41%, while in ponds with older/larger ﬁsh on average only 1–2% of the traps were invaded. Emerging insects were not Fig. 1 Densities of breeding coot pairs and broods on ponds recorded in emergence traps containing predators stocked separately with different-aged carp. The symbols and except for two traps invaded by dytiscids. error bars represent back-calculated means and 95% conﬁdence limits (original scale), respectively, from GLMM models. Log pond surface area was modelled as an offset variable to control for differences in pond size 123 Hydrobiologia (2018) 820:267–279 273 Table 1 Results of GLMM analyses (Poisson errors, log link and on (c) breeding success per pair per season and (d) per pair function) of the effects of habitat variables on (a) pair numbers with at least one chick hatched, with pond identity as a random and (b) brood numbers of coots on ﬁsh ponds, with year as a factor random factor and log pond surface area as an offset variable, Predictors Estimate ± SE F-ratio df P (a) Breeding pair number Fish age (0?,1?,2?) 0.00, -0.83, -1.15 (0.25) 11.28 2, 30 \ 0.001 Submerged vegetation 0.19 ± 0.07 7.12 1, 30 0.012 Emergent pond vegetation 1.41 ± 0.67 4.43 1, 30 0.044 (b) Brood number Fish age (0?,1?,2?) 0.00, -0.67, -0.98 (0.08) 6.02 2, 30 0.006 Submerged vegetation 0.24 ± 0.08 8.21 1, 30 0.008 Emergent pond vegetation 1.87 ± 0.75 6.30 1, 30 0.018 (c) Breeding success (number of juveniles/pair) Fish age (0?,1?,2?) 0.00, 0.15, -0.04 (0.17) 0.69 2, 15.4 0.517 Submerged vegetation 0.00 ± 0.01 5.23 1, 19.2 0.034 Emergent pond vegetation 0.47 ± 0.48 0.94 1, 28.1 0.341 (d) Breeding success (number of juveniles/brood) Fish age (0?,1?,2?) 0.00, -0.03, -0.19 (0.17) 0.64 2, 17.1 0.542 Submerged vegetation 0.00 ± 0.01 0.14 1, 14.1 0.711 Emergent pond vegetation -0.14 ± 0.42 0.11 1, 17.1 0.749 Early/late broods 0.00, -0.23 (0.11) 4.23 1, 154.6 0.041 Timing of breeding (early vs. late broods) was added as a ﬁxed term in the breeding success per brood analysis. For the categorical factors in the models (ﬁsh gradient, early vs. late broods), average standard errors of differences are shown in brackets Table 2 Repeated-measure ANOVA (with time as the repe- ated measure) for effects of ﬁsh gradient on the density of newly hatched coot broods and on the relative biomasses of macroinvertebrates and amphibian larvae Source of variation df FP Density of newly hatched broods/10 ha Fish gradient 2, 32 5.55 0.009 Time 5, 160 2.62 0.026 Time 9 ﬁsh gradient 10, 160 0.64 0.777 Dry biomass of invertebrates (g) Fish gradient 2, 32 11.43 \ 0.001 Time 5, 160 1.56 0.174 Time 9 ﬁsh gradient 10, 160 1.26 0.257 Wet biomass of tadpoles (g) Fig. 2 Coot breeding success per pair per season and per brood (only pairs that successfully hatched at least one chick were Fish gradient 2, 32 4.31 0.022 included) on ponds stocked separately with different-aged carp. Time 5, 160 1.86 0.105 The symbols and error bars represent back-calculated means and Time 9 ﬁsh gradient 10, 160 1.88 0.051 95% conﬁdence limits (original scale), respectively, from GLMM models. Sample sizes (numbers of broods) are shown above bars 123 274 Hydrobiologia (2018) 820:267–279 Fig. 3 Mean (± SE) water temperatures (A), densities of newly hatched broods of coot (B), relative abundances (dry biomass per 10 traps) of nektonic and epibenthic macroinvertebrates (C), and relative abundances (wet biomass per 10 traps) of amphibian larvae (D) throughout the breeding season (N = 35 ponds). X- axis numbers represent consecutive trapping events (at half-month intervals) and the concurrent coot counts. For clarity, data were pooled over pond types (0?,1? and 2? ﬁsh) and years (2005–2007) 123 Hydrobiologia (2018) 820:267–279 275 food availability between 1? and 2? ponds, suggest- ing that at similar density levels of relatively large- sized ﬁsh, the size structure of ﬁsh populations is of secondary importance. Carp may also exert substantial pressure on submerged vegetation via resuspension of sediments, herbivory and uprooting (e.g. Sidorkewicj et al., 1996; Kaemingk et al., 2017; Maceda-Veiga et al., 2017), and thus diminish food resources for coots and destroy refugia and oviposition sites for invertebrates and amphibians (Diehl & Kornijo´w, 1998). In our pond system, vegetation biomass was not signiﬁcantly related to the ﬁsh gradient, presumably because turbidity levels during the avian breeding season only Fig. 4 Mean (± SE) numbers of emerging insects (Ephe- exceptionally exceeded 20 NTU (Nieoczym & meroptera and Diptera) under different ﬁsh size and density conditions (ponds stocked with 0?,1? and 2? carp; N =7, 10 Kloskowski, 2014), a critical value over which plant and 6 ponds, respectively) in May–July 2006–2007. Means and development can be seriously hampered (Lougheed ranges of water temperatures at the time of trapping were 18C et al., 1998; see also Fischer et al., 2013). Carp impact (15–21C) in May, 21C (16–23C) in June and 21C (18–23C) on submerged vegetation and in turn on birds is likely in July to be more dramatic in warmer parts of the species’ Discussion introduced range, where carp remain active over most of the year due to higher annual water temperatures Coot habitat selection in relation to ﬁsh impact (Maceda-Veiga et al., 2017). Some pond macrophytes, on pond communities apparently more tolerant of turbid conditions and bottom stirring by benthivorous ﬁsh, persisted in the Our data show that pond selection by breeding coots presence of densely stocked larger carp. In some 1? was driven by ﬁsh population characteristics (size and 2? ponds, the only submerged macrophyte was structure combined with density) and abundance of sago pondweed (Stuckenia pectinata (L.) Bo¨rner, 1912) (Nieoczym & Kloskowski, 2015), an important emergent and submerged vegetation. Densities of breeding coots were considerably higher on low-ﬁsh foraging resource for coots (Allouche & Tamisier, 1984; Van Wijk, 1988; Hilt, 2006). Notably, carp have 0? ponds than on ponds containing high biomass densities of larger carp. This pattern was consistent been reported to impair the growth of sago pondweed under experimental conditions through herbivory, with ﬁsh effects on nektonic and epibenthic macroin- vertebrate and larval amphibian availability, indicat- increased water turbidity and stimulation of periphytic ing food competition (or competition-related cover shading the macrophytes (Sidorkewicj et al., interactions) between carp and coots. The coincidence 1996, 1999; but see Lougheed et al., 1998; Miller & of brood hatching peak with the seasonally highest Provenza, 2007). In our study system, coot breeding abundance of nektonic prey suggests that coots ﬁne- densities were related to both water transparency and tune egg-laying to the phenology of these prey abundance of submerged vegetation; these two habitat resources. The competitive impact of carp on birds variables are considerably interdependent (e.g. Crow- can be increased to a large degree by non-trophic der & Painter, 1991; Blindow et al., 1993; see also Kaemingk et al., 2017). Both submerged macrophytes (trait-mediated) interactions, since vagile adult insects and breeding amphibians avoid ponds with ﬁsh that as food resources and water transparency as a factor constraining prey detectability by diving birds (and pose a predation threat to their eggs and larvae (e.g. Resetaris & Wilbur, 1989; Trekels & Vanschoen- also growth of macrophytes and charophytes) could be winkel, 2017), and these effects may be contingent on important for breeding waterfowl (Hanson & Butler, ﬁsh size and density (Kloskowski, 2011). Overall, we 1994; Hargeby et al., 1994; Svingen & Anderson, did not ﬁnd differences in coot breeding parameters or 1998; Musil, 2006; Hansson et al., 2010). 123 276 Hydrobiologia (2018) 820:267–279 Emergent vegetation was another pond variable pair density was not correlated with clutch or ﬁnal important for habitat selection by coots, presumably brood size. because it provided nesting habitats and protection Given their high foraging plasticity and ability to against aerial predators (Salathe´, 1986). Luxuriance of use a wide array of plant and animal food (Perrow emergent vegetation may also reduce competition et al., 1997; Paracuellos, 2006), coots breeding under with ﬁsh because coots feed on the shoots and leaves conditions of high competition with ﬁsh may be of emergent macrophytes (Borowiec, 1975; Allouche expected to rely on food resources less affected by ﬁsh, & Tamisier, 1984; Metna et al., 2015). Adverse ﬁsh such as submerged macrophytes, as indicated by their effects on waterfowl may be to some extent mitigated positive effect on breeding success per pair per season. by high pond/lake productivity (e.g. Staicer et al., Macrophyte species able to tolerate the impact of ﬁsh 1994; Broyer & Calenge, 2010). Carp ponds are might be of special importance in providing the typically eutrophic and they receive additional nutri- quantities of food needed to meet the demands of ents from supplemental feeds, which are provided broods. Of the animal food, most nektonic and roughly in proportion to stock biomass. However, in epibenthic prey were obviously depressed by carp the ponds studied ﬁsh gradient and surrogates for pond (cf. Nieoczym & Kloskowski, 2015), so the only productivity were poorly correlated (Nieoczym & functional prey group unrelated to the ﬁsh gradient Kloskowski, 2014; see also Nilsson, 1978 for the was emerging insects. Brinkhof (1997) showed that interannual and within-season differences in chick absence of a relationship between lake productivity and coot abundance). survival can be explained by variation in the abun- dance of emerging insects during the early post- Coot breeding success hatching period (see also Horsfall, 1984), similarly to the pattern observed in dabbling ducks, with most The breeding response of coots to ﬁsh differed from ducklings hatching just after the peak of emerging those previously reported for waterbirds competitively chironomids (Danell & Sjo¨berg, 1977; Gardarsson & interacting with ﬁsh. Some duck species have been Einarsson, 2004; but see Dessborn et al., 2009). In our shown to select their habitats to avoid ﬁsh and, study, coot dependence on emerging insects appears consistently, despite greater breeding densities, their substantiated by the higher ﬂedging success of early reproductive success (expressed as brood size or broods, since abundance of emerging insects declined duckling growth) is higher on ﬁsh-free water bodies throughout the coot breeding season (cf. Brinkhof & (Eriksson, 1979; DesGranges & Rodrigue, 1986; Cave, 1997). Our emergence-trap data should be Giles, 1994). Another contrasting response to ﬁsh treated with caution, because in 0? ponds the traps was observed in facultatively piscivorous red-necked were frequently invaded by predaceous macroinver- grebes (Podiceps grisegena Boddaert, 1783) nesting tebrates and newts, readily feeding on emerging on carp ponds; breeding birds showed no habitat insects (Armitage, 1995). Studies using nektonic preference between 0? and 1? ponds and suffered invertebrate traps have not found any signiﬁcant heavy food-dependent mortality of chicks on the effects of predators in the traps on the catches (e.g. densely stocked 1? ponds, where ﬁsh proved unavail- Elmberg et al., 1992; Verdonschot, 2010). However, able to young birds due to size constraints and the disproportionate accumulation of predators in the suppressed the non-ﬁsh prey of grebes (Kloskowski, traps placed in low-ﬁsh ponds was likely to bias the 2012). In the present study, 0? ponds, supporting low emergence rate estimates. Activity and emergence densities of ﬁsh, were favoured by coots as nesting and trap results could be confounded by intraseasonal brood-rearing habitats over densely stocked ponds variation in water temperature. However, we assume with larger carp (see also Houdkova & Musil, 2003; that our results were not signiﬁcantly biased, because Maceda-Veiga et al., 2017), but breeding success both although water temperatures in the ponds progres- per breeding pair and per nesting attempt resulting in sively increased over most of the study period, they the successful hatch of at least one egg did not differ did not vary much from mid-May to July. Factors other among pond types. An adverse within-population than food could contribute to the similarity in survival density-dependent mechanism is unlikely, because rates of chicks between ponds, e.g. larger broods can attract predators and may be more difﬁcult for their 123 Hydrobiologia (2018) 820:267–279 277 References parents to protect (Re˛k, 2010). Also, early-season cold spells during the nestling period could lead to Allouche, L. & A. Tamisier, 1984. Feeding convergence of increased mortality independent of food (authors’ gadwall, coot and other herbivorous waterfowl species personal observations). wintering in the Camargue: a preliminary approach. Wildfowl 35: 135–142. Anteau, M. J., T. L. Shaffer, M. H. Sherfy, M. A. Sovada, J. H. Stacker, J. H. Stucker & M. T. Wiltermuth, 2012. Nest Conclusions survival of piping plovers at a dynamic reservoir indicates an ecological trap for a threatened population. Oecologia Fish proved an important factor in habitat selection by 170: 1167–1179. breeding coots, which should be considered in strate- Armitage, P. D., 1995. Chironomidae as food. In Armitage, P. D., P. S. Cranston & L. C. V. Pinder (eds), The Chirono- gies of wetland management for waterfowl. Ponds with midae. Biology and Ecology of Non-biting Midges. high ﬁsh impact (high ﬁsh densities, large individual Chapman and Hall, London: 423–435. size) supported the highest densities of coot broods. Bajer, P. G., G. Sullivan & P. W. 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