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Declining Coastal Piscivore Populations in the Baltic Sea: Where and When Do Sticklebacks Matter?

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Declining Coastal Piscivore Populations in the Baltic Sea: Where and When Do Sticklebacks Matter? http://www.diva-portal.org This is the published version of a paper published in Ambio. Citation for the original published paper (version of record): Byström, P., Bergström, U., Hjälten, A., Ståhl, S., Jonsson, D. et al. (2015) Declining coastal piscivore populations in the Baltic Sea: where and when do sticklebacks matter?. Ambio, 44(Suppl 3): S462-S471 http://dx.doi.org/10.1007/s13280-015-0665-5 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-110599 AMBIO 2015, 44(Suppl. 3):S462–S471 DOI 10.1007/s13280-015-0665-5 Declining coastal piscivore populations in the Baltic Sea: Where and when do sticklebacks matter? Pa¨r Bystro¨m, Ulf Bergstro¨m, Alexander Hja¨lten, Sofie Sta˚hl, David Jonsson, Jens Olsson Abstract Intraguild predation interactions make fish predation (IGP) (Werner and Gilliam 1984; Irigoien and de communities prone to exhibit alternative stable states Roos 2011). IGP in fish communities is strongly dependent with either piscivore or prey fish dominance. In the Baltic on size relationships between interacting species and in- Sea, local declines of coastal piscivores like perch (Perca cludes interactions where juvenile predators compete with fluviatilis) have been observed to coincide with high their future prey for shared resources to interactions where densities of sticklebacks (Gasterosteus aculeatus). prey feed on juvenile predators, i.e., reciprocal IGP (Pers- Mechanisms behind this shift between piscivore and son et al. 2007a; Fauchald 2010; van der Hammen et al. stickleback dominance were studied both experimentally 2010; Hin et al. 2011). In the former case, competition from and in field. Results showed that predation by sticklebacks prey for shared resources may result in a juvenile com- has a strong negative effect on perch larvae survival, but petitive bottleneck in the predator which limits recruitment this effect rapidly decreases with increasing perch size, to the adult predator stage (Werner and Gilliam 1984; likely due to gape limitations and digestion constraints in Bystro¨m et al. 1998). In the latter case, prey may impose sticklebacks. Large spatial and temporal variations in high mortality on juvenile predators through predation and patterns of stickleback migration into perch spawning sites thereby reduce the recruitment of predators (Fauchald were observed. Whether or not high density of sticklebacks 2010). Based on either or both of above mechanisms, will cause declines in coastal piscivore populations is Walters and Kitchell (2001) suggested the presence of two suggested to depend on the availability of spawning sites in alternative stable community states (ASS), a high predator which sticklebacks do not migrate into or arrive late in the density state where predators control the prey population reproduction season of coastal piscivores. such that they increase the growth and survival of their own offspring, or a high prey population density state were prey Keywords Intraguild predation Á Ecosystem coupling Á limit predator population growth and density. The potential Recruitment Á Coastal piscivores Á for both competition and reciprocal predation control in IGP Three-spined stickleback Á Alternative stable states systems is especially challenging in a management context. This is due to that these systems may initially respond to exploitation of predators or gradual environmental change INTRODUCTION similar to traditional linear food chains until reaching thresholds where sudden regime shifts occur (Hin et al. Life history omnivory (shifts in resource use from inverte- 2011;Ga˚rdmark et al. 2015). Thus, in a high prey popula- brates to fish over ontogeny) is common in fish and may tion density state, a recovery of a predator population may involve both habitat shifts and interactions where species be hampered by the strong negative effects from the prey both prey on and compete with each other, i.e., intraguild population on predator recruitment (Walters and Kitchell 2001; Fauchald 2010;Ga˚rdmark et al. 2015). Ecosystems or habitats are in many cases coupled Electronic supplementary material The online version of this article (doi:10.1007/s13280-015-0665-5) contains supplementary through fluxes of organisms (Massol et al. 2011) and in material, which is available to authorized users. spatially linked systems with IGP, the likelihood for ASS Ó The Author(s) 2015. This article is published with open access at Springerlink.com 123 www.kva.se/en AMBIO 2015, 44(Suppl. 3):S462–S471 S463 has been shown to depend on the degree of spatial if sticklebacks can have a negative impact on the survival of separation (van der Hammen et al. 2010) or on the relative perch recruits, and under which conditions this may be im- productivity of the coupled systems (Schreiber and Rudolf portant for recruitment success of coastal piscivores. More 2008). In marine ecosystems, migrating fish that over their specifically, we studied what sizes of YOY perch are vul- life cycle use different habitats for growth and reproduc- nerable to stickleback predation in laboratory and estimated tion, link processes in offshore, and coastal and/or fresh- mortality rates of differently sized YOY perch in the absence water ecosystems (Schindler et al. 2005; Eriksson et al. or presence of sticklebacks in a large-scale pond experiment. 2011). Moreover, ecosystem-specific anthropogenic im- The results from these studies were then contrasted to field pacts like fishing or eutrophication may cause strong ef- data on temporal variation in stickleback migration into fects in the adjacent ecosystems through changes in piscivore spawning sites and mortality patterns of YOY densities of migrating fish (Eriksson et al. 2011; Casini perch in relation to stickleback densities. Finally, in a coastal et al. 2012). Consequently, in offshore–coastal IGP sys- area with high densities of stickleback we estimated (a) the tems, the potential for both cross-ecosystem migration of number of perch migrating from the sea up to a small fish and variation in habitat-specific productivity could freshwater lake for spawning, (b) the YOY perch densities in cause ASS in either of the systems. that lake, and (c) the proportion of perch that have been Eutrophication and depletion of large piscivores have recruited from freshwater systems in that area. resulted in dramatic changes in the Baltic Sea ecosystem (O¨ sterblom et al. 2007;Mo¨llmann et al. 2009). The collapse of cod (Gadus morhua) has resulted in predation release of MATERIALS AND METHODS small planktivores, and a planktivore dominated offshore ecosystem (Casini et al. 2009; Eriksson et al. 2011). Along Detailed descriptions of methods for all approaches can be with this shift in the offshore ecosystem, local declines in found in Supplementary Material S1. the Baltic Proper have been observed of the coastal key- stone piscivorous fish species: perch (Perca fluviatilis) and Laboratory experiment and gape size limitation pike (Esox lucius) (Ljunggren et al. 2010; Eriksson et al. 2011). This decline has coincided with increasing densities In order to estimate gape limitations of three-spined stick- of sticklebacks which migrate into coastal areas for repro- lebacks when feeding on differently sized YOY perch, we duction (Nilsson et al. 2004; Ljunggren et al. 2010; Eriksson measured stickleback gape sizes and conducted feeding et al. 2011; Appelberg et al. 2013). This shift from piscivore experiments in aquarium using different size combinations dominance to a coastal fish community dominated by of sticklebacks as predators and perch as prey. Gape sizes of sticklebacks has been suggested to be due to competition a random sample of sticklebacks were measured to the and/or predation from increasing densities of three-spined nearest 0.1 mm as the distance between the upper and lower sticklebacks on young piscivores. However, evidence for jaw at a gape angle of 90°, using a stereo microscope. To this is circumstantial and based mainly on negative corre- estimate theoretical maximum length of a YOY perch that lations between stickleback and young-of-the-year (YOY) sticklebacks can consume, we combined our estimate of perch abundance in field data (Nilsson 2006; Ljunggren stickleback gape size relationship with published relation- et al. 2010; Eriksson et al. 2011). Decreased top–down ships between YOY perch body height and length. For the control of sticklebacks from declining coastal piscivore feeding experiments, we used three size classes of stickle- populations has also been suggested to increase eu- back: small (30–40 mm), medium (45–55 mm), and large trophication symptoms, i.e., algal blooms in shallow bays, (65–75 mm) placed individually in aquarium and six size as sticklebacks feed on grazers which in turn controls algal classes of YOY perch as prey (11, 14, 19, 21, 25, and biomass (Eriksson et al. 2011; Sieben et al. 2011). Hence, in 31 mm, total length). Prior to experiments, sticklebacks addition to their importance for recreational and commer- were starved for 24 h, and thereafter either ten YOY perch cial small-scale fisheries, coastal piscivore populations (size classes 11 and 14 mm) or five YOY perch (size classes provide important regulating ecosystem services in being 19, 21, 25, and 31 mm) were introduced to each aquarium. key species for the function and structure of coastal food Number of consumed perch was recorded after 4 h. webs (HELCOM 2007; Bergstro¨m et al. 2013). The cascading effects of high densities of sticklebacks on Pond experiment lower trophic levels in the Baltic Sea coastal ecosystem are well known (Eriksson et al. 2011, and references therein), but We conducted a large-scale pond experiment to examine whether or not sticklebacks have negative impacts on coastal whether or not survival of YOY perch is dependent on their piscivore population densities and what mechanisms may be size when three-spined sticklebacks migrate into perch operating is still an open question.
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