Journal of Fish Biology (2014) 84, 1195–1201 doi:10.1111/jfb.12328, available online at wileyonlinelibrary.com
Feeding efficiency of planktivores under disturbance, the effect of water colour, predation threat and shoal composition L. Nurminen*†, S. Estlander*‡, M. Olin* and H. Lehtonen* *Department of Environmental Sciences/Aquatic Sciences, University of Helsinki, P. O. Box 65, Helsinki 00014, Finland and ‡Biological Centre, Academy of Sciences of the Czech ˇ Republic, Hydrobiological Institute, Na Sádkách 7, 370 05 Ceské Budˇejovice, Czech Republic
(Received 10 October 2013, Accepted 21 December 2013) The consumption of phantom midge Chaoborus flavicans larvae by Perca fluviatilis showed clear response to water colour, predation threat and shoal composition with the most significant negative effect for water colour. In the case of Rutilus rutilus, no similar combined response was observed and the total prey consumption was significantly negatively affected by predation threat of Esox lucius. The results suggest that differences in life-history traits may result in disparity in species-specific responses to disturbance. © 2014 The Fisheries Society of the British Isles
Key words: interspecific competition; intraspecific competition; optical properties; trait-related response.
Disturbance is a major driver in the structure and dynamics of communities and ecosystem-level processes (Sousa, 1984). In aquatic ecosystems, the question of disturbance is very timely, since aquatic habitats are in a rapid state of change, and disturbance is often of anthropogenic origin. Different species respond in diverse ways to disturbances depending on their life-history traits and extent of trophic interactions (Sousa, 1984; Dodd & Dreslik, 2008). Species that change habitat or prey during ontogeny are often subjected to selection pressures and competition, drivers which are affected by disturbance (Werner, 1988). Between-species differences in disturbance responses may alter interactions among co-occurring species with different life-history traits. For example, the perch Perca fluviatilis L. 1758 shows morphological pre-adaptation to three major environment-driven niche shifts during its life history from planktivory, through consuming a macroinvertabrate diet, to piscivory (Eklöv & Persson, 1995; Hjelm et al., 2000), whereas the roach Rutilus rutilus (L. 1758) is a generalist omnivore that lacks an ontogenic diet shift and remains more susceptible to †Author to whom correspondence should be addressed. Tel.: + 358 9 191 58990; email: [email protected]
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predation throughout its life (Horppila & Nurminen, 2009). These differences during ontogeny should be detectable in early species-specific behaviour-related traits in response to disturbance. Visibility in aquatic ecosystems is decreasing due to increasing runoff of dissolved organic carbon and nutrients from catchments causing brownification and eutrophication (Kirk, 1994; Monteith et al., 2007). This fundamental change in light environment has consequences on species interactions and ecosystem functioning through top–down control (Lind, 2003). Earlier studies have shown that decreased visibility severely disturbs prey detection of visually dependent fishes (Vinyard & O’Brien, 1976; Estlander et al., 2010, 2012). Cyprinids, such as R. rutilus, are known for efficient zooplanktivory in low visibility (Bohl, 1980), whereas percids, such as P. fluviatilis, are vision-oriented selective particulate feeders at the plankton-feeding stage (Helfman, 1979) and therefore more susceptible to decreasing visibility (Nurminen et al., 2010a). Thus, when juvenile R. rutilus compete with juvenile P. fluviatilis (Persson et al., 1999; Estlander et al., 2010), R. rutilus is claimed to be a more efficient planktivore (Persson, 1987). Pike Esox lucius L. 1758, as the top predator in many aquatic ecosystems, is the main threat for planktivorous P. fluviatilis and R. rutilus (Craig, 1996). When attempting to predict between-species interactions, it is essential to compare these species with different life-history traits as they are key species in many lakes in Europe (Lehtonen et al., 2008; Olin et al., 2010). Disturbance caused by different abiotic and biotic factors can affect prey consumption of planktivores, resulting in different growth patterns (Estlander et al., 2012). To define species-specific effects of disturbance on prey consumption, a full-factorial experimental design including pure and mixed P. fluviatilis and R. rutilus shoals, two levels of water colour, with and without predator were used. It was expected that (1) degraded visibility would affect the feeding rate of P. fluviatilis more than that of R. rutilus, (2) predation threat would decrease the feeding rate of both species, being a more important factor in determining the prey consumption of R. rutilus and (3) the presence of R. rutilus would disrupt the feeding rate of P. fluviatilis more than the presence of P. fluviatilis would affect prey consumption by R. rutilus. The experiments were conducted in 1000 l tanks in controlled laboratory facilities, used previously by Estlander et al. (2012). Fishes were caught from nearby lakes (P. fluviatilis = 108, Lake Majajärvi, wire traps; R. rutilus = 108, Lake Rahtijärvi, seine; E. lucius = 3, Lake Majajärvi, angling). A shoal of six fishes (2 week acclimation, 48 h starvation) was used in each experiment (P. fluviatilis or R. rutilus pure shoals; 3 + 3 P. fluviatilis and R. rutilus mixed shoals) in clear and highly humic water and with and without predation threat (three replicates of each treatment; total of 36 experiments; 24 replications for each species). The water colour treatments were conducted in clear ( 0⋅05) (Fig. 1). Additionally, no significant effect of decreasing visibility (water colour, P > 0⋅05) was observed. Esox lucius presence (predation threat, F 1,16 = 25⋅0, P < 0⋅001) and the interaction of E. lucius presence and visibility (predation threat × water colour, F 1,16 = 7⋅5, P < 0⋅05) had significant effects on the feeding rate of R. rutilus indicated by the negative effect of E. lucius presence on prey consumption in clear water [Fig. 1(a), (b)] but a less distinct effect in humic water [Fig. 1(c), (d)]. No significance was observed for the presence of P. fluviatilis (shoal composition, P > 0⋅05) on the feeding rate of R. rutilus. Fish LT had no significant effect on feeding rate in either species (P > 0⋅05). As expected, the feeding rate of P. fluviatilis was significantly affected by water colour regardless of shoal composition or predation threat. The response of R. rutilus to water colour was not as distinct. Perca fluviatilis is an efficient feeder dependent on prey detection and more vulnerable to degraded visibility than R. rutilus (Nurminen et al., 2010a, b; Estlander et al., 2012). This phenomenon may be partly explained by the different trait-related feeding strategies of the species (Peterka & Matena, 2011). Perca fluviatilis is a discontinuous swimmer with intensive prey search tactics and requires a visual stimulus to react to prey movement, detecting and attacking the prey items from a greater distance than R. rutilus (Peterka & Matena, 2011). Rutilus rutilus, however, displays tight school formation and is a less-selective feeder, with a prey search tactic of continuous swimming (Eklöv & Persson, 1995; Peterka & Matena, 2011) and, therefore, is less affected by visibility (Nurminen et al., 2010a). Perca fluviatilis
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Fig. 1. Mean ± 95% c.l. feeding rate on Chaoborus flavicans by Perca fluviatilis ( ) and Rutilus rutilus ( ) in different treatments: pure and mixed shoals, two levels of water colour, with and without predation threat by Esox lucius. (a, b) Clear water and (c, d) humic water treatments; (a, c) pure shoal and (b, d) mixed shoal treatments.
eventually becomes a cannibalistic piscivore (Byström et al., 1998), and is known to form loose schools showing intraspecific aggression (Christensen & Persson, 1993), resulting in higher variation in the feeding rate of individuals compared to R. rutilus (Nurminen et al., 2010a). As expected, predation threat provided by the presence of E. lucius decreased prey consumption of both planktivores in clear water, with predator visual cues combined with chemical cues (Mikheev et al., 2006; Ranåker, 2012). In contrast, in humic water where visual cues were limited, the overall low consumption of prey resulted in no additional effect of predation threat in either species. In clear water with no predation threat, the feeding rate of P. fluviatilis in mixed shoals was slightly lower than in pure shoals, indicating a disturbing effect on P. fluviatilis by the more active R. rutilus (Estlander, 2011). This is in line with suggestions that the competitive interaction between the species in open water habitats is in favour of R. rutilus (Persson, 1987; Persson & Greenberg, 1988). In mixed shoals, it appeared that in humic water and in clear water under predation threat, the feeding rate of P. fluviatilis was slightly higher than in pure shoals. This may be due to the presence of continuously moving R. rutilus which activated the otherwise more passive P. fluviatilis when combined with disturbance from visual deterioration or predation threat (Ranåker, 2012; L. Nurminen, pers. obs.). Corroborating this hypothesis, when considering the feeding rate of R. rutilus, the presence of P. fluviatilis did not appear to have any additional disruptive or enhancing effect (Persson, 1987). In R. rutilus, the
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presence of predation threat by E. lucius appeared to be the primary factor affecting the feeding efficiency. This may be due to the overall lower prey consumption and the predator avoidance strategy displayed by R. rutilus by forming tighter schools and actively avoiding the vicinity of the predator by aggregating close to the centre of the experimental unit (Ranåker, 2012). In prey consumption by P. fluviatilis, degrading visibility which affects movement, hunting activity and prey search of a visual hunter (Vinyard & O’Brien, 1976), appeared to be the ultimate regulating factor. It has been debated whether intraspecific or interspecific competition is the primary factor shaping fish communities, especially among coexisting species with common resources such as P. fluviatilis and R. rutilus (Persson, 1986; Svanbäck & Eklöv, 2002; Hjelm et al., 2003; Svanbäck et al., 2008). This study suggests that species-specific life-history traits and the origin of disturbance may affect the role of interspecific competition in species showing resource partitioning. Changing aquatic ecosystems, disturbance originating from different sources may contribute to population-, community- and ecosystem-level changes through diverse species-specific effects and responses. The experiments conducted comply with the regulations of Finnish Animal Welfare Commission (ESAVI-2010-04859). The study was financially supported by the R. Erik Serlachius Stiftelse Foundation, Bergsrådet Bror Serlachius Stiftelse Foundation and research grants of the University of Helsinki. Evo Fisheries Research Station of Finnish Game and Fisheries Research Institute provided excellent facilities and M. S. V. Lösönen helped with the experiments.
References Bohl, E. (1980). Diel pattern of pelagic distribution and feeding in planktivorous fish. Oecologia 44, 368–375. Byström, P., Persson, L. & Wahsltröm, E. (1998). Competing predators and prey: juvenile bottlenecks in whole-lake experiments. Ecology 2, 2154–2167. Carter, T. R., Fronzek, S. & Bärlund, I. (2004). FINSKEN: a framework for developing consistent global change scenarios for Finland in the 21st century. Boreal Environment Research 9, 91–107. Christensen, B. & Persson, L. (1993). Species-specific antipredatory behaviours: effect on prey choice in different habitats. Behavioural and Ecological Sociobiology 32, 1–9. Craig, J. F. (1996). Pike: Biology and Exploitation. London: Chapman & Hall. Dodd, C. K. Jr. & Dreslik, M. J. (2008). Habitat disturbances differentially affect individual growth rates in a long-lived turtle. Journal of Zoology 275, 18–25. Eklöv, P. & Persson, L. (1995). Species-specific antipredator capacities and prey refuges: interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). Behavioural and Ecological Sociobiology 37, 169–178. Estlander, S. (2011). Fishes of the darkness. Water colour-regulated competitive interactions in humic lakes. PhD Thesis. Department of Environmental Sciences, University of Helsinki, Finland. Available at http://urn.fi/URN:ISBN:978-952-10-7058-7/ Estlander, S., Nurminen, L., Olin, M., Vinni, M. & Horppila, J. (2009). Seasonal fluctuations in macrophyte cover and water transparency of four brown-water lakes: implications for crustacean zooplankton in littoral and pelagic habitats. Hydrobiologia 620, 109–120. Estlander, S., Nurminen, L., Olin, M., Vinni, M., Immonen, S., Rask, M., Ruuhijärvi, J., Horppila, J. & Lehtonen, H. (2010). Diet shifts and food selection of perch (Perca fluviatilis) and roach (Rutilus rutilus (L.)) in humic lakes of varying water colour. Journal of Fish Biology 77, 241–256. Estlander, S., Horppila, J., Olin, M., Vinni, M., Lehtonen, H., Rask, M. & Nurminen, L. (2012). Troubled by the humics – effects of water colour and interspecific competition on the feeding efficiency of planktivorous perch. Boreal Environment Research 17, 305–312. Helfman, G. S. (1979). Twilight activities of yellow perch Perca flavescens. Journal of the Fisheries Research Board of Canada 36, 173–179.
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Hjelm, J., Persson, L. & Christensen, B. (2000). Growth, morphological variation and ontogenetic niche shifts in perch (Perca fluviatilis) in relation to resource availability. Oecologia 122, 190–199. Hjelm, J., van de Weerd, G. H. & Sibbing, F. A. (2003). Functional link between foraging performance, functional morphology, and diet shifts in roach (Rutilus rutilus). Canadian Journal of Fisheries and Aquatic Sciences 60, 700–709. Horppila, J. & Nurminen, L. (2009). Food niche segregation between two herbivorous cyprinid species in a turbid lake. Journal of Fish Biology 75, 1230–1243. Horppila, J., Estlander, S., Olin, M., Pihlajamäki, J., Vinni, M. & Nurminen, L. (2011). Gender–dependent effects of water quality and conspecific density on the feeding rate of fish – factors behind sexual growth dimorphism. Oikos 120, 855–861. Kirk, J. T. O. (1994). Light and Photosynthesis in Aquatic Ecosystems. Cambridge: Cambridge University Press. Lehtonen, H., Rask, M., Pakkasmaa, S. & Hesthagen, T. (2008). Freshwater fishes, their biodiversity, habitats and fisheries in the Nordic countries. Aquatic Ecosystem Health and Management 11, 298–309. Lind, O. T. (2003). Suspended clay’s effect on lake and reservoir limnology. Archiv für Hydrobiologie 139, 327–360. Mikheev, V. N., Wanzenbock, J. & Pasternak, A. F. (2006). Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behaviour. Ecology of Freshwater Fish 15, 111–117. Monteith, D. T., Stoddard, J. L., Evans, C. D., de Wit, H. A., Forsius, M., Høgåsen, T., Wilander, A., Skjelkvåle, B. L., Jeffries, D. S., Vuorenmaa, J., Keller, B., Kopácek, J. & Vesely, J. (2007). Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537–541. Nurminen, L., Pekcan-Hekim, Z. & Horppila, J. (2010a). Feeding efficiency of planktivorous perch Perca fluviatilis and roach Rutilus rutilus in varying turbidity: an individual-based approach. Journal of Fish Biology 76, 1848–1855. Nurminen, L., Pekcan-Hekim, Z., Repka, S. & Horppila, J. (2010b). Effect of prey type and inorganic turbidity on littoral predator-prey interactions in a shallow lake: an experimental approach. Hydrobiologia 646, 209–214. Olin, M., Vinni, M., Lehtonen, H., Rask, M., Ruuhijärvi, J., Saulamo, K. & Ala–Opas, P. (2010). Environmental factors regulate the effects of roach Rutilus rutilus and pike Esox lucius on Perca fluviatilis populations in small boreal forest lakes. Journal of Fish Biology 76, 1277–1293. Pekcan-Hekim, Z., Horppila, J., Nurminen, L. & Niemistö, J. (2005). Diel changes in habitat preferences and diet of perch (Perca fluviatilis), roach (Rutilus rutilus) and white bream (Abramis björkna). Archiv für Hydrobiologie Special Issues Advances in Limnology 59, 173–187. Persson, L. (1986). Effects of reduced interspecific competition on resource utilization in perch (Perca fluviatilis). Ecology 67, 355–364. Persson, L. (1987). Effects of habitat and season on competitive interactions between roach (Rutilus rutilus) and perch (Perca fluviatilis). Oecologia 73, 170–177. Persson, L. & Greenberg, L. A. (1988). Juvenile competitive bottlenecks: the perch (Perca fluviatilis) – roach (Rutilus rutilus) interaction. Ecology 71, 44–56. Persson, L., Byström, P., Wahlström, E., Andersson, J. & Hjelm, J. (1999). Interactions among size-structured populations in a whole-lake experiment: size- and scale-dependent processes. Oikos 87, 139–156. Peterka, J. & Matena, J. (2011). Feeding behaviour determining differential capture success of evasive prey in underyearling Eurpean perch (Perca fluviatilis L.) and roach (Rutilus rutilus (L.)). Hydrobiologia 661, 113–121. Ranåker, L. (2012). Piscivore-prey interactions. Consequences of changing optical environments. PhD Thesis. Department of Biology, University of Lund, Sweden. Available at http://www.lu.se/lup/publication/2520947/ Sousa, W. P. (1984). The role of disturbance in natural communities. Annual Review of Ecology and Systematics 15, 353–391. Svanbäck, R. & Eklöv, P. (2002). Effects of habitat and food resources on morphology and ontogenic trajectories in perch. Oecologia 131, 61–70.
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Svanbäck, R., Eklöv, P., Fransson, R. & Holmgren, K. (2008). Intraspecific competition drives multiple species resource polymorphism in fish communities. Oikos 117, 114–124. Vinyard, G. L. & O’Brien, J. (1976). Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). Journal of the Fisheries Research Board of Canada 33, 2845–2849. Werner, E. (1988). Size, scaling and the evolution of complex life cycles. In Size-Structured Populations – Ecology and Evolution (Eberman, B. & Persson, L., eds), pp. 60–81. New York, NY: Springer.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 1195–1201
Feeding efficiency of planktivores under disturbance, the effect of water colour, predation threat and shoal composition L. Nurminen*†, S. Estlander*‡, M. Olin* and H. Lehtonen* *Department of Environmental Sciences/Aquatic Sciences, University of Helsinki, P. O. Box 65, Helsinki 00014, Finland and ‡Biological Centre, Academy of Sciences of the Czech ˇ Republic, Hydrobiological Institute, Na Sádkách 7, 370 05 Ceské Budˇejovice, Czech Republic
(Received 10 October 2013, Accepted 21 December 2013) The consumption of phantom midge Chaoborus flavicans larvae by Perca fluviatilis showed clear response to water colour, predation threat and shoal composition with the most significant negative effect for water colour. In the case of Rutilus rutilus, no similar combined response was observed and the total prey consumption was significantly negatively affected by predation threat of Esox lucius. The results suggest that differences in life-history traits may result in disparity in species-specific responses to disturbance. © 2014 The Fisheries Society of the British Isles
Key words: interspecific competition; intraspecific competition; optical properties; trait-related response.
Disturbance is a major driver in the structure and dynamics of communities and ecosystem-level processes (Sousa, 1984). In aquatic ecosystems, the question of disturbance is very timely, since aquatic habitats are in a rapid state of change, and disturbance is often of anthropogenic origin. Different species respond in diverse ways to disturbances depending on their life-history traits and extent of trophic interactions (Sousa, 1984; Dodd & Dreslik, 2008). Species that change habitat or prey during ontogeny are often subjected to selection pressures and competition, drivers which are affected by disturbance (Werner, 1988). Between-species differences in disturbance responses may alter interactions among co-occurring species with different life-history traits. For example, the perch Perca fluviatilis L. 1758 shows morphological pre-adaptation to three major environment-driven niche shifts during its life history from planktivory, through consuming a macroinvertabrate diet, to piscivory (Eklöv & Persson, 1995; Hjelm et al., 2000), whereas the roach Rutilus rutilus (L. 1758) is a generalist omnivore that lacks an ontogenic diet shift and remains more susceptible to †Author to whom correspondence should be addressed. Tel.: + 358 9 191 58990; email: [email protected]
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predation throughout its life (Horppila & Nurminen, 2009). These differences during ontogeny should be detectable in early species-specific behaviour-related traits in response to disturbance. Visibility in aquatic ecosystems is decreasing due to increasing runoff of dissolved organic carbon and nutrients from catchments causing brownification and eutrophication (Kirk, 1994; Monteith et al., 2007). This fundamental change in light environment has consequences on species interactions and ecosystem functioning through top–down control (Lind, 2003). Earlier studies have shown that decreased visibility severely disturbs prey detection of visually dependent fishes (Vinyard & O’Brien, 1976; Estlander et al., 2010, 2012). Cyprinids, such as R. rutilus, are known for efficient zooplanktivory in low visibility (Bohl, 1980), whereas percids, such as P. fluviatilis, are vision-oriented selective particulate feeders at the plankton-feeding stage (Helfman, 1979) and therefore more susceptible to decreasing visibility (Nurminen et al., 2010a). Thus, when juvenile R. rutilus compete with juvenile P. fluviatilis (Persson et al., 1999; Estlander et al., 2010), R. rutilus is claimed to be a more efficient planktivore (Persson, 1987). Pike Esox lucius L. 1758, as the top predator in many aquatic ecosystems, is the main threat for planktivorous P. fluviatilis and R. rutilus (Craig, 1996). When attempting to predict between-species interactions, it is essential to compare these species with different life-history traits as they are key species in many lakes in Europe (Lehtonen et al., 2008; Olin et al., 2010). Disturbance caused by different abiotic and biotic factors can affect prey consumption of planktivores, resulting in different growth patterns (Estlander et al., 2012). To define species-specific effects of disturbance on prey consumption, a full-factorial experimental design including pure and mixed P. fluviatilis and R. rutilus shoals, two levels of water colour, with and without predator were used. It was expected that (1) degraded visibility would affect the feeding rate of P. fluviatilis more than that of R. rutilus, (2) predation threat would decrease the feeding rate of both species, being a more important factor in determining the prey consumption of R. rutilus and (3) the presence of R. rutilus would disrupt the feeding rate of P. fluviatilis more than the presence of P. fluviatilis would affect prey consumption by R. rutilus. The experiments were conducted in 1000 l tanks in controlled laboratory facilities, used previously by Estlander et al. (2012). Fishes were caught from nearby lakes (P. fluviatilis = 108, Lake Majajärvi, wire traps; R. rutilus = 108, Lake Rahtijärvi, seine; E. lucius = 3, Lake Majajärvi, angling). A shoal of six fishes (2 week acclimation, 48 h starvation) was used in each experiment (P. fluviatilis or R. rutilus pure shoals; 3 + 3 P. fluviatilis and R. rutilus mixed shoals) in clear and highly humic water and with and without predation threat (three replicates of each treatment; total of 36 experiments; 24 replications for each species). The water colour treatments were conducted in clear ( 0⋅05) (Fig. 1). Additionally, no significant effect of decreasing visibility (water colour, P > 0⋅05) was observed. Esox lucius presence (predation threat, F 1,16 = 25⋅0, P < 0⋅001) and the interaction of E. lucius presence and visibility (predation threat × water colour, F 1,16 = 7⋅5, P < 0⋅05) had significant effects on the feeding rate of R. rutilus indicated by the negative effect of E. lucius presence on prey consumption in clear water [Fig. 1(a), (b)] but a less distinct effect in humic water [Fig. 1(c), (d)]. No significance was observed for the presence of P. fluviatilis (shoal composition, P > 0⋅05) on the feeding rate of R. rutilus. Fish LT had no significant effect on feeding rate in either species (P > 0⋅05). As expected, the feeding rate of P. fluviatilis was significantly affected by water colour regardless of shoal composition or predation threat. The response of R. rutilus to water colour was not as distinct. Perca fluviatilis is an efficient feeder dependent on prey detection and more vulnerable to degraded visibility than R. rutilus (Nurminen et al., 2010a, b; Estlander et al., 2012). This phenomenon may be partly explained by the different trait-related feeding strategies of the species (Peterka & Matena, 2011). Perca fluviatilis is a discontinuous swimmer with intensive prey search tactics and requires a visual stimulus to react to prey movement, detecting and attacking the prey items from a greater distance than R. rutilus (Peterka & Matena, 2011). Rutilus rutilus, however, displays tight school formation and is a less-selective feeder, with a prey search tactic of continuous swimming (Eklöv & Persson, 1995; Peterka & Matena, 2011) and, therefore, is less affected by visibility (Nurminen et al., 2010a). Perca fluviatilis
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Fig. 1. Mean ± 95% c.l. feeding rate on Chaoborus flavicans by Perca fluviatilis ( ) and Rutilus rutilus ( ) in different treatments: pure and mixed shoals, two levels of water colour, with and without predation threat by Esox lucius. (a, b) Clear water and (c, d) humic water treatments; (a, c) pure shoal and (b, d) mixed shoal treatments.
eventually becomes a cannibalistic piscivore (Byström et al., 1998), and is known to form loose schools showing intraspecific aggression (Christensen & Persson, 1993), resulting in higher variation in the feeding rate of individuals compared to R. rutilus (Nurminen et al., 2010a). As expected, predation threat provided by the presence of E. lucius decreased prey consumption of both planktivores in clear water, with predator visual cues combined with chemical cues (Mikheev et al., 2006; Ranåker, 2012). In contrast, in humic water where visual cues were limited, the overall low consumption of prey resulted in no additional effect of predation threat in either species. In clear water with no predation threat, the feeding rate of P. fluviatilis in mixed shoals was slightly lower than in pure shoals, indicating a disturbing effect on P. fluviatilis by the more active R. rutilus (Estlander, 2011). This is in line with suggestions that the competitive interaction between the species in open water habitats is in favour of R. rutilus (Persson, 1987; Persson & Greenberg, 1988). In mixed shoals, it appeared that in humic water and in clear water under predation threat, the feeding rate of P. fluviatilis was slightly higher than in pure shoals. This may be due to the presence of continuously moving R. rutilus which activated the otherwise more passive P. fluviatilis when combined with disturbance from visual deterioration or predation threat (Ranåker, 2012; L. Nurminen, pers. obs.). Corroborating this hypothesis, when considering the feeding rate of R. rutilus, the presence of P. fluviatilis did not appear to have any additional disruptive or enhancing effect (Persson, 1987). In R. rutilus, the
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presence of predation threat by E. lucius appeared to be the primary factor affecting the feeding efficiency. This may be due to the overall lower prey consumption and the predator avoidance strategy displayed by R. rutilus by forming tighter schools and actively avoiding the vicinity of the predator by aggregating close to the centre of the experimental unit (Ranåker, 2012). In prey consumption by P. fluviatilis, degrading visibility which affects movement, hunting activity and prey search of a visual hunter (Vinyard & O’Brien, 1976), appeared to be the ultimate regulating factor. It has been debated whether intraspecific or interspecific competition is the primary factor shaping fish communities, especially among coexisting species with common resources such as P. fluviatilis and R. rutilus (Persson, 1986; Svanbäck & Eklöv, 2002; Hjelm et al., 2003; Svanbäck et al., 2008). This study suggests that species-specific life-history traits and the origin of disturbance may affect the role of interspecific competition in species showing resource partitioning. Changing aquatic ecosystems, disturbance originating from different sources may contribute to population-, community- and ecosystem-level changes through diverse species-specific effects and responses. The experiments conducted comply with the regulations of Finnish Animal Welfare Commission (ESAVI-2010-04859). The study was financially supported by the R. Erik Serlachius Stiftelse Foundation, Bergsrådet Bror Serlachius Stiftelse Foundation and research grants of the University of Helsinki. Evo Fisheries Research Station of Finnish Game and Fisheries Research Institute provided excellent facilities and M. S. V. Lösönen helped with the experiments.
References Bohl, E. (1980). Diel pattern of pelagic distribution and feeding in planktivorous fish. Oecologia 44, 368–375. Byström, P., Persson, L. & Wahsltröm, E. (1998). Competing predators and prey: juvenile bottlenecks in whole-lake experiments. Ecology 2, 2154–2167. Carter, T. R., Fronzek, S. & Bärlund, I. (2004). FINSKEN: a framework for developing consistent global change scenarios for Finland in the 21st century. Boreal Environment Research 9, 91–107. Christensen, B. & Persson, L. (1993). Species-specific antipredatory behaviours: effect on prey choice in different habitats. Behavioural and Ecological Sociobiology 32, 1–9. Craig, J. F. (1996). Pike: Biology and Exploitation. London: Chapman & Hall. Dodd, C. K. Jr. & Dreslik, M. J. (2008). Habitat disturbances differentially affect individual growth rates in a long-lived turtle. Journal of Zoology 275, 18–25. Eklöv, P. & Persson, L. (1995). Species-specific antipredator capacities and prey refuges: interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). Behavioural and Ecological Sociobiology 37, 169–178. Estlander, S. (2011). Fishes of the darkness. Water colour-regulated competitive interactions in humic lakes. PhD Thesis. Department of Environmental Sciences, University of Helsinki, Finland. Available at http://urn.fi/URN:ISBN:978-952-10-7058-7/ Estlander, S., Nurminen, L., Olin, M., Vinni, M. & Horppila, J. (2009). Seasonal fluctuations in macrophyte cover and water transparency of four brown-water lakes: implications for crustacean zooplankton in littoral and pelagic habitats. Hydrobiologia 620, 109–120. Estlander, S., Nurminen, L., Olin, M., Vinni, M., Immonen, S., Rask, M., Ruuhijärvi, J., Horppila, J. & Lehtonen, H. (2010). Diet shifts and food selection of perch (Perca fluviatilis) and roach (Rutilus rutilus (L.)) in humic lakes of varying water colour. Journal of Fish Biology 77, 241–256. Estlander, S., Horppila, J., Olin, M., Vinni, M., Lehtonen, H., Rask, M. & Nurminen, L. (2012). Troubled by the humics – effects of water colour and interspecific competition on the feeding efficiency of planktivorous perch. Boreal Environment Research 17, 305–312. Helfman, G. S. (1979). Twilight activities of yellow perch Perca flavescens. Journal of the Fisheries Research Board of Canada 36, 173–179.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 1195–1201
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L . N U R M I N E N E T A L.
Hjelm, J., Persson, L. & Christensen, B. (2000). Growth, morphological variation and ontogenetic niche shifts in perch (Perca fluviatilis) in relation to resource availability. Oecologia 122, 190–199. Hjelm, J., van de Weerd, G. H. & Sibbing, F. A. (2003). Functional link between foraging performance, functional morphology, and diet shifts in roach (Rutilus rutilus). Canadian Journal of Fisheries and Aquatic Sciences 60, 700–709. Horppila, J. & Nurminen, L. (2009). Food niche segregation between two herbivorous cyprinid species in a turbid lake. Journal of Fish Biology 75, 1230–1243. Horppila, J., Estlander, S., Olin, M., Pihlajamäki, J., Vinni, M. & Nurminen, L. (2011). Gender–dependent effects of water quality and conspecific density on the feeding rate of fish – factors behind sexual growth dimorphism. Oikos 120, 855–861. Kirk, J. T. O. (1994). Light and Photosynthesis in Aquatic Ecosystems. Cambridge: Cambridge University Press. Lehtonen, H., Rask, M., Pakkasmaa, S. & Hesthagen, T. (2008). Freshwater fishes, their biodiversity, habitats and fisheries in the Nordic countries. Aquatic Ecosystem Health and Management 11, 298–309. Lind, O. T. (2003). Suspended clay’s effect on lake and reservoir limnology. Archiv für Hydrobiologie 139, 327–360. Mikheev, V. N., Wanzenbock, J. & Pasternak, A. F. (2006). Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behaviour. Ecology of Freshwater Fish 15, 111–117. Monteith, D. T., Stoddard, J. L., Evans, C. D., de Wit, H. A., Forsius, M., Høgåsen, T., Wilander, A., Skjelkvåle, B. L., Jeffries, D. S., Vuorenmaa, J., Keller, B., Kopácek, J. & Vesely, J. (2007). Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537–541. Nurminen, L., Pekcan-Hekim, Z. & Horppila, J. (2010a). Feeding efficiency of planktivorous perch Perca fluviatilis and roach Rutilus rutilus in varying turbidity: an individual-based approach. Journal of Fish Biology 76, 1848–1855. Nurminen, L., Pekcan-Hekim, Z., Repka, S. & Horppila, J. (2010b). Effect of prey type and inorganic turbidity on littoral predator-prey interactions in a shallow lake: an experimental approach. Hydrobiologia 646, 209–214. Olin, M., Vinni, M., Lehtonen, H., Rask, M., Ruuhijärvi, J., Saulamo, K. & Ala–Opas, P. (2010). Environmental factors regulate the effects of roach Rutilus rutilus and pike Esox lucius on Perca fluviatilis populations in small boreal forest lakes. Journal of Fish Biology 76, 1277–1293. Pekcan-Hekim, Z., Horppila, J., Nurminen, L. & Niemistö, J. (2005). Diel changes in habitat preferences and diet of perch (Perca fluviatilis), roach (Rutilus rutilus) and white bream (Abramis björkna). Archiv für Hydrobiologie Special Issues Advances in Limnology 59, 173–187. Persson, L. (1986). Effects of reduced interspecific competition on resource utilization in perch (Perca fluviatilis). Ecology 67, 355–364. Persson, L. (1987). Effects of habitat and season on competitive interactions between roach (Rutilus rutilus) and perch (Perca fluviatilis). Oecologia 73, 170–177. Persson, L. & Greenberg, L. A. (1988). Juvenile competitive bottlenecks: the perch (Perca fluviatilis) – roach (Rutilus rutilus) interaction. Ecology 71, 44–56. Persson, L., Byström, P., Wahlström, E., Andersson, J. & Hjelm, J. (1999). Interactions among size-structured populations in a whole-lake experiment: size- and scale-dependent processes. Oikos 87, 139–156. Peterka, J. & Matena, J. (2011). Feeding behaviour determining differential capture success of evasive prey in underyearling Eurpean perch (Perca fluviatilis L.) and roach (Rutilus rutilus (L.)). Hydrobiologia 661, 113–121. Ranåker, L. (2012). Piscivore-prey interactions. Consequences of changing optical environments. PhD Thesis. Department of Biology, University of Lund, Sweden. Available at http://www.lu.se/lup/publication/2520947/ Sousa, W. P. (1984). The role of disturbance in natural communities. Annual Review of Ecology and Systematics 15, 353–391. Svanbäck, R. & Eklöv, P. (2002). Effects of habitat and food resources on morphology and ontogenic trajectories in perch. Oecologia 131, 61–70.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 1195–1201
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Svanbäck, R., Eklöv, P., Fransson, R. & Holmgren, K. (2008). Intraspecific competition drives multiple species resource polymorphism in fish communities. Oikos 117, 114–124. Vinyard, G. L. & O’Brien, J. (1976). Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). Journal of the Fisheries Research Board of Canada 33, 2845–2849. Werner, E. (1988). Size, scaling and the evolution of complex life cycles. In Size-Structured Populations – Ecology and Evolution (Eberman, B. & Persson, L., eds), pp. 60–81. New York, NY: Springer.
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