Variable forage fish biomass and phenology influence marine predator diet, foraging behavior, and species interactions in coastal Newfoundland, Canada

ICES Journal of Marine Science, 2024, Vol. 81, Issue 4, 629–642 https://doi.org/10.1093/icesjms/fsae021 Received: 30 June 2023; revised: 5 February 2024; accepted: 6 February 2024 Advance access publication date: 7 March 2024 Review Article Variable forage fish biomass and phenology influence marine predator diet, foraging behavior, and species interactions in coastal Newfoundland, Canada Gail K. Davoren * Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada Corresponding author. Department of Biological Sciences, University of Manitoba, 50 Sifton Road, Winnipeg, Manitoba, R3T 2N2, Canada. E-mail: Abstract Forage fish species provide essential linkages for energy transfer within pelagic marine food webs. Capelin (Mallotus villosus), the focal forage fish in coastal Newfoundland, Canada, suffered a stock collapse in 1991 and has not recovered. Despite this collapse, capelin continue to provide locally abundant prey aggregations. Here, I synthesize the lessons learned from a long-term capelin-predator research program (2004–2022) on the northeast Newfoundland coast during the postcollapse period. I highlight the importance of simultaneously estimating forage fish biomass and predator responses in a multispecies and multiyear context. High interannual variation in capelin spawning timing and biomass was observed. Lower capelin biomass consistently resulted in predator species- and assemblage-level dietary shifts toward a higher diversity of lower trophic level, alternative prey. Energetic foraging costs of seabirds also increased under lower capelin biomass, but responses differed among species. Summer capelin consumption by dominant seabirds (9389 tonnes) and whales (778 tonnes) indicated predator energetic requirements and revealed higher natural mortality relative to fishery-based (1289 tonnes) mortality. Overall, this case study illustrated that, despite high observed behavioural plasticity, varying species-specific predator responses to changing capelin biomass integrated to increase potential competitive interactions under low capelin biomass, providing a basis for ecosystem-level change. Keywords: stable isotope analysis; bird-borne tracking devices; at-sea experiments; seabirds; humpback whales; consumption estimates; capelin (Mallotus villosus) Introduction Pelagic marine food webs are under wasp-waist control, where energy is funneled through a few forage fish species (e.g. herring, capelin, anchovy), making them critical to energy flow (Cury et al. 2000, Pikitch et al. 2012). Forage fish convert energy at lower trophic levels into food for top vertebrate predators, thereby regulating energy flow through marine food webs (Pikitch et al. 2012). Despite the critical role of forage fish in marine ecosystems, these species comprise approximately onethird of the global marine fish catch (Smith et al. 2011, Pikitch et al. 2012), with increasing proportions used as feed in the aquaculture industry (Alder et al. 2008, Tacon and Metian 2009). Although fishing makes forage fish populations more vulnerable to collapse (Essington et al. 2015), demonstrating the impact of forage fish exploitation rates on predator abundance can be difficult (Hilborn et al. 2017). This difficulty may result from predators being adapted to the high natural population size fluctuations (∼±40%) of forage fish species (Hilborn et al. 2017), often referred to as “boom and bust cycles” (Pikitch et al. 2012), or due to varying life-history traits of predators (Koehn et al. 2021). Nevertheless, even modest declines in forage fish biomass have been predicted (Cairns 1987) and shown to impact higher trophic levels (Piatt et al. 2007, Cury et al. 2011, Smith et al. 2011) and marine ecosystems (Pikitch et al. 2014). Therefore, researchers have argued the need to develop precautionary ecosystem-based harvest strategies for forage fish species (Pikitch et al. 2004, Pikitch 2015). One advocated strategy is to maintain biomass above traditional fisheries targets (e.g. maximum sustainable yield) based on energetic requirements of predators (Cury et al. 2011, Smith et al. 2011, Pikitch et al. 2012). This management strategy, however, requires quantifying these predator requirements through multiyear research programs that simultaneously quantify fisheries-independent forage fish biomass and the foraging behaviour, diet, and reproductive success of multiple predator species (e.g. Piatt and Methven 1992, Boyd and Murray 2001, Piatt et al. 2007, Cury et al. 2011). Unfortunately, such long-term research programs are rare. Capelin (Mallotus villosus) is an important forage fish species throughout its circumpolar range (Carscadden and Vilhjálmsson 2002) and is the dominant forage fish that many top predators, including marine birds, mammals, and large predatory fish (e.g. Atlantic cod, Gadus morhua), rely on as prey on the Newfoundland and Labrador Shelf. In this region, capelin are considered a single stock complex (Northwest Atlantic Fisheries Organization (NAFO) Divisions 2J3KL; DFO 2021), where fish undergo extensive migrations (>250 km) during the spring from offshore regions to inshore regions to spawn (Carscadden et al. 2013) at intertidal and subtidal sites (Nakashima and Wheeler 2002, Davoren et al. 2008). The arrival of spawning capelin in coastal regions acts as a pulsed resource (Ostfeld and Keesing 2000, Yang et al. 2008, 2010), whereby prey for coastal marine predators become temporarily super-abundant during the spawning season relative to © The Author(s) 2024. Published by Oxford University Press on behalf of International Council for the Exploration of the Sea. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. ∗ 630 During the summer, seabird species of the family Alcidae (hereafter, “alcids”) comprise most of the seabird biomass in this area (>90%; Table 1), including murres (88%), puffins (3.4%), and razorbills (0.5%). Owing to the numerical dominance of alcids in the bay and their reliance on capelin as prey (Davoren and Montevecchi 2003, Montevecchi et al. 2019, Jenkins and Davoren 2021, Lescure 2021), research has focused on these species. Alcids are wing-propelled, pursuit diving birds that capture prey underwater. Their wing design is a compromise between underwater propulsion and aerial flight, whereby high amounts of energy are expended during flight compared to other avian species (Thaxter et al. 2010, Elliott et al. 2013). Therefore, factors that increase distances flown to foraging locations substantially increase foraging costs, or foraging effort, and are predicted to influence the survival of offspring and, ultimately, adults (Cairns 1987). For these alcid species breeding in the bay, each pair raises a single eg (...truncated)