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Prey Or Predator—Expanding the Food Web Role of Sandeel Ammodytes Marinus

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Prey Or Predator—Expanding the Food Web Role of Sandeel Ammodytes Marinus Vol. 516: 267–273, 2014 MARINE ECOLOGY PROGRESS SERIES Published December 3 doi: 10.3354/meps11064 Mar Ecol Prog Ser OPENPEN ACCESSCCESS NOTE Prey or predator — expanding the food web role of sandeel Ammodytes marinus Ole Ritzau Eigaard*,**, Mikael van Deurs**, Jane W. Behrens, Dorte Bekkevold, Keith Brander, Marie Plambech, Kristian Schreiber Plet-Hansen, Henrik Mosegaard National Institute of Aquatic Resources (DTU Aqua), Charlottenlund Castle, 2920 Charlottenlund, Denmark ABSTRACT: We report an unexpected observation of lesser sandeel Ammodytes marinus foraging on juveniles and late larval stages of the same species. This recording sheds new light on the can- nibalistic and piscivorous capacity of forage fish and raises a number of questions about the role of forage fish in marine food webs. In 2012 and 2013, the stomachs of 748 sandeels from 36 differ- ent commercial sandeel hauls in the central North Sea were opened, and 9% of these contained late-stage sandeel larvae. In order to better understand the cannibalistic nature of sandeels, we made a detailed analysis of another 450 sandeels from a single haul with a high frequency of apparent cannibals. One-third of the stomachs contained a minimum of 1 young sandeel (mean length 2.7 cm; max. length 4.9 cm), 10% contained 5 or more, and 1 stomach contained 18. Analy- ses of sample DNA confirmed that predator and prey were conspecifics. Larger specimens were more likely to be cannibals. Among cannibals, however, the specific sandeel larvae consumption was independent of cannibal size. We argue that this piscivorous cannibalistic behaviour may not only be a key factor in explaining recruitment fluctuations in North Sea sandeel stocks, but it may also add a new element to the complexity of energy flow in marine food chains. KEY WORDS: Cannibalism · Energy flow · Forage fish · Food web · Piscivory · Population dynamics · Trophic control INTRODUCTION ecological and socio-economic consequences and poses a challenge to sustainable fisheries manage- Forage fish transfer energy from plankton to larger ment (Dickey-Collas et al. 2014). Several external predators in marine food webs (Pikitch et al. 2014). drivers of these fluctuations have been identified, These planktivorous, fast-growing, small to medium - typically defined in relation to their impact points in sized schooling forage fish species are vital to many the trophodynamic processes of the marine environ- larger marine predators, including mammals and sea ment as either bottom-up, e.g. changing climate birds (Thompson et al. 2007, Cury et al. 2011), and (Arnott & Ruxton 2002) and cyclic changes in envi- they also sustain a number of large commercial fish- ronmental conditions (Tourre et al. 2007), or top- eries worldwide, accounting for more than 30% of down, i.e. predator−prey interactions at higher global landings (Smith et al. 2011). trophic levels (Frederiksen et al. 2007) and commer- Most forage fish populations display large fluctua- cial fishing (Smith et al. 2011). Hence, the general tions in biomass on both decadal and inter-annual perception is that forage fish abundance is controlled time scales (Pikitch et al. 2014). This has pronounced by food availability, physical-chemical conditions, © The authors 2014. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - **These authors contributed equally to this work restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 268 Mar Ecol Prog Ser 516: 267–273, 2014 fishing mortality and predation pressure from higher tral North Sea (54° 8’ N, 2° 3’ E). This haul had a rela- trophic levels (Frank et al. 2007, van Deurs et al. tively high prevalence of cannibals and was there- 2009), and the prevailing biological trait being as- fore suitable for analysing the predator to prey ratio signed to these species is that of prey to higher and the allometry of the apparent cannibalistic be - trophic levels and grazers on the secondary produc- haviour. Total length of individual fish (from the tip of tion. the snout to the tip of the longer lobe of the caudal Internal drivers of the so-called rollercoaster stock fin) was measured to the nearest cm and weighed to dynamics of forage fishes (Dickey-Collas et al. 2014) nearest mg. Individual stomach contents of the sam- seem to be overlooked in the bottom-up versus top- pled sandeel were subsequently sorted into 2 groups, down paradigm for investigating population dynam- fish larvae and non-fish larvae, and weighed. Indi- ics and interactions in the marine ecosystem de- vidual fish larvae were counted and, if well enough scribed above. Cannibalism is widespread among preserved, the total length was also measured to the teleosts (Smith & Reay 1991), and theory predicts that nearest mm. Based on these data, we related preda- cannibalism in general can have profound effects on tor size to cannibalism prevalence and size of the population structure and dynamics (Kohlmeier & eaten conspecifics. Ebenhöh 1995, Magnússon 1999); cannibalism could thus potentially be a hitherto overlooked co-driver of forage fish population dynamics. In support, sandeel Genetic analyses cannibalism has been suggested by Lynam et al. (2013) as an explanation for the weak relationship DNA sequence analysis (bar coding) was applied between spawning stock biomass and recruitment in to determine prey species, using a standardized ap - the North Sea sand eel stocks. However, reports of proach (Ratnasingham & Hebert 2013). Total geno- forage fish cannibalism are almost absent from the mic DNA was extracted from 8 adult sandeel and 2 literature. larval prey per gut (16 prey in total) using an Omega Here we report the unexpected finding of sandeel tissue DNA extraction kit (Omega Biotech). DNA Ammodytes marinus cannibalizing large quantities concentrations were measured using a NanoDrop of late larval stages and juveniles of their own spe- Fluorospectrometer (Thermo Fisher Scientific). Mito- cies. These findings challenge the traditional percep- chondrial cytochrome c oxidase subunit I (COI) gene tion of forage fish ecology and population dynamics PCR amplifications were undertaken using the by demonstrating that forage fishes are not only primers FishF1 and FishR23 (Ward et al. 2005), am - planktivorous, feeding on zooplankton (including pli fying a ~650 base pair fragment of the COI gene. fish eggs and small fish larvae; Macer 1966, Engel- PCR reactions included 0.5 µl genomic DNA, 6.25 µl hard et al. 2014) but are also cannibals, feeding on Qiagen Multiplex PCR Master Mix (Qiagen) and relatively large conspecifics, i.e. juveniles and late 1.25 µl of each 3.2 pmol primer, with 4.5 µl water stage larvae. bringing the total volume of the reaction to 12.5 µl. The PCR cycling regime was as follows: initial denat- uration at 95°C for 15 min followed by 30 cycles of MATERIALS AND METHODS 94°C for 30 s, 57°C for 90 s and 72°C for 60 s, and a fi- nal elongation for 15 min at 60°C. PCR products were Sampling and stomach analyses visualized under UV on an ethidium bromide-stained 2% agarose gel. Then 8 µl samples of PCR products In 2012 and 2013, the stomachs of 748 sandeels were cleaned using 1.2 µl phosphat ase buffer, 0.3 µl from 36 different commercial sandeel hauls (10 to 40 phosphatase enzyme, 0.3 µl Exonuclease I (Exo I) and stomachs from each haul) in the central North Sea 2.2 µl water. Samples were incubated for 1 h at 37°C were opened. Of these, 9% contained at least 1 late followed by 20 min at 80°C. Sequencing reactions stage sandeel larvae, and these were distributed over were performed using the BigDyeTerminator v3.1 17 hauls (between April 16 and June 7). In order to Cycle Sequencing Kit (Ap plied Biosystems) with the better understand the cannibalistic nature of individ- forward primer. PCR conditions were 1 min at 96°C, ual sandeels, we made a detailed analysis of another followed by 40 cycles of 10 s at 96°C, 5 s at 50°C and 450 sandeel randomly sampled from a commercial 4 min at 60°C. PCR products were purified using 5 µl haul (April 21, 2012) of the Danish industrial trawler EDTA, precipitated using 100% ethanol, and then ‘L455 Lotte Vohnsen’, taken from the primary Danish dried, re-suspended in HighDye (Applied Biosys- sandeel fishing grounds on Dogger Bank in the cen- tems) and sequenced using an ABI 3130 Genetic An- Eigaard et al.: Food web role of forage fishes 269 alyzer (Applied Biosystems). Sequence quality was Larval sandeels co-occurred with copepods, checked by visual inspection, and specimens for amphipods and mysiids in the cannibal stomachs. which >300 base pairs high- quality sequence was Notably, however, sandeel larvae were often found obtained were matched against the BOLD data clumped together in the stomachs rather than mixed repository (Ratnasingham & Hebert 2007). up with the other gut content. This feeding pattern resulted in the presence of very distinct planktivory and piscivory diet bands in adult sandeel stomachs RESULTS (Fig. 2a). Stomach analysis Cannibalism allometry The 450 sampled sandeels ranged from 10 to 17 cm (12.2 ± 1 cm; mean ± SD) in total length. More than The number of sandeel larvae per stomach fol- one-third (165) of the fish had 1 or more larval lowed a zero-inflated distribution. Analyses based on sandeels or juveniles in their stomach, 41 stomachs size groups (1 cm intervals, and only size groups con- contained 5 or more, and the maximum number of taining 10 or more sandeels) revealed a highly signif- ingested offspring was 18 (Fig. 1a). In total, 580 late icant and clearly linear relationship between fish stage larvae or juveniles were found in the 165 stom- length and the proportion of fish being cannibals (p < achs.
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