Extreme reduction in nutritional value of a key forage fish during the Pacific marine heatwave of 2014-2016

Abstract

Pacific sand lance Ammodytes personatus are a key forage fish in the North Pacific for many species of salmon, groundfish, seabirds, and marine mammals and have historically been important to predators in relatively warm years. However, extreme declines in the nutritional value of sand lance in Prince William Sound, Alaska, USA, during 2012−2016 indicate that energy transfer from lower trophic levels to predators via sand lance may have been disrupted during the North Pacific marine heatwave in 2015 and 2016. Nutritional value (length, energy density, and whole-body energy) was measured in age-0 and age-1 sand lance collected during July in cool (2012−2013) and increasingly warm (2014−2016) years. The value of age-0 fish was relatively stable, with only minor differences among years for length and whole-body energy. By contrast, the value of age-1 fish significantly declined in 2015, and by 2016 they were 38% shorter and 13% lower in energy density compared to cooler years. This contributed to significant declines in whole-body energy of 44% in 2015 and 89% in 2016 compared to cooler years (2012−2014). The 2015 sand lance cohort experienced little growth or lipid accumulation from July 2015 at age-0 to July 2016 at age-1. This effective disruption of energy flow through pelagic food webs probably contributed to population declines and/or breeding failures observed among several predators in the Gulf of Alaska and suggests that tipping points were reached during the heatwave.

Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016

“…In addition to shifts in latitudinal abundance of specific taxa, warm water conditions diminished body condition and somatic growth of ectothermic forage fish. Body condition of capelin and sand lance in the GOA and CCS was reduced during the heatwave, resulting in smaller, less energy-dense prey for murres [107,[111][112][113]. Whole-body energy content of age-1 sand lance declined by 44% in 2015 and 89% in 2016 in Alaska [114], and body condition of sand lance in the northern CCS declined markedly in 2014-2015 [113].…”

“…Consequently, the flow of energy to forage fish was disrupted, even as their own metabolic demand increased. This likely led to reduced somatic growth and fat storage [69,107]. In turn, this reduced survival in some forage fish (or age-classes) and lowered the nutritional quality of forage fish for seabirds ( Fig 6).…”

The role of sand lances (Ammodytes sp.) in the Northwest Atlantic Ecosystem: A synthesis of current knowledge with implications for conservation and management

“…Indeed, Ammodytes populations that are in close proximity (<60 km) to each other but experience different ocean temperature regimes can exhibit markedly different age compositions or growth rates (Robards, Rose, & Piatt, 2002). Growth rates can also vary markedly among just a few years with strong temperature fluctuations (von Biela et al, 2019). During the 1980s, NWA Ammodytes populations in Northeast U.S. continental shelf waters were generally ≤5 years of age, primarily age 1–3 (Nelson & Ross, 1991).…”

“…A winter dormancy period has been suggested for A. dubius , yet no rigorous study of dormancy timing currently exists in the NWA region (Gilman, 1994). In each case, vigorous feeding prior to dormancy appears to contribute to maturation and survival, thus making this genus potentially vulnerable to changes in the spatio‐temporal dynamics of their zooplankton prey (Kuzuhara et al, 2019; Nishikawa, Nakamura, Okamoto, & Ueda, 2019; Van Deurs, Christensen, Frisk, & Mosegaard, 2010; van Deurs, Hartvig, & Steffensen, 2011; von Biela et al, 2019;).…”

“…In addition, climate change is altering the availability of key Ammodytes prey in the North Sea where C. finmarchicus is being replaced by a warmer water conspecific, C. helgolandicus (Calanidae). Calanus helgolandicus differs in phenology, size, and nutrition (Frederiksen et al 2011, van Deurs et al, 2009; van Deurs et al, 2015), which has implications for energy flow to higher‐level predators (von Biela et al, 2019). Examples from the Northeast Atlantic presented here and throughout this synthesis show how the competing demands from the commercial fishery relative to fish, marine mammal and seabird predators can be managed (Furness, 2002) when Ammodytes are explicitly considered.…”