Within the twilight of the oceanic mesopelagic realm, 200–1000 m below sea level, are potentially vast resources of fish. Collectively, these mesopelagic fishes are the most abundant vertebrates on Earth, and this global fish community plays a vital role in the function of oceanic ecosystems. The biomass of these fishes has recently been estimated using acoustic survey methods, which rely on echosounder-generated signals being reflected from gas-filled swimbladders and detected by transducers on vessels. Here, we use X-ray computed tomography scans to demonstrate that several of the most abundant species of mesopelagic fish in the Southern Ocean lack gas-filled swimbladders. We also show using catch data from survey trawls that the fish community switches from fish possessing gas-filled swimbladders to those lacking swimbladders as latitude increases towards the Antarctic continent. Thus, the acoustic surveys that repeatedly show a decrease in mesopelagic fish biomass towards polar environments systematically overlook a large proportion of fish species that dominate polar seas. Importantly, this includes lanternfish species that are key prey items for top predators in the region, including king penguins and elephant seals. This latitudinal community switch, from gas to non-gas dominance, has considerable implications for acoustic biomass estimation, ecosystem modelling and long-term monitoring of species at risk from climate change and potential exploitation.

Southern Ocean ecosystems are globally important and vulnerable to global drivers of change, yet they remain challenging to study. Fish and squid make up a significant portion of the biomass within the Southern Ocean, filling key roles in food webs from forage to mid-trophic species and top predators. They comprise a diverse array of species uniquely adapted to the extreme habitats of the region. Adaptations such as antifreeze glycoproteins, lipid-retention, extended larval phases, delayed senescence, and energy-conserving life strategies equip Antarctic fish and squid to withstand the dark winters and yearlong subzero temperatures experienced in much of the Southern Ocean. In addition to krill exploitation, the comparatively high commercial value of Antarctic fish, particularly the lucrative toothfish, drives fisheries interests, which has included illegal fishing. Uncertainty about the population dynamics of target species and ecosystem structure and function more broadly has necessitated a precautionary, ecosystem approach to managing these stocks and enabling the recovery of depleted species. Fisheries currently remain the major local driver of change in Southern Ocean fish productivity, but global climate change presents an even greater challenge to assessing future changes. Parts of the Southern Ocean are experiencing ocean-warming, such as the West Antarctic Peninsula, while other areas, such as the Ross Sea shelf, have undergone cooling in recent years. These trends are expected to result in a redistribution of species based on their tolerances to different temperature regimes. Climate variability may impair the migratory response of these species to environmental change, while imposing increased pressures on recruitment. Fisheries and climate change, coupled with related local and global drivers such as pollution and sea ice change, have the potential to produce synergistic impacts that compound the risks to Antarctic fish and squid species. The uncertainty surrounding how different species will respond to these challenges, given their varying life histories, environmental dependencies, and resiliencies, necessitates regular assessment to inform conservation and management decisions. Urgent attention is needed to determine whether the current management strategies are suitably precautionary to achieve conservation objectives in light of the impending changes to the ecosystem.

The oceanic mesopelagic zone, 200–1000 m below sea level, holds abundant small fishes that play central roles in ecosystem function. Global mesopelagic fish biomass estimates are increasingly derived using active acoustics, where echosounder-generated signals are emitted, reflected by pelagic organisms and detected by transducers on vessels. Previous studies have interpreted a ubiquitous decline in acoustic reflectance towards the Antarctic continent as a reduction in mesopelagic fish biomass. Here, we use empirical data to estimate species-specific acoustic target strength for the dominant mesopelagic fish of the Scotia Sea in the Southern Ocean. We use these data, alongside estimates of fish relative abundance from net surveys, to interpret signals received in acoustic surveys and calculate mesopelagic biomass of the broader Southern Ocean. We estimate the Southern Ocean mesopelagic fish biomass to be approximately 274 million tonnes if Antarctic krill contribute to the acoustic signal, or 570 million tonnes if mesopelagic fish alone are responsible. These quantities are approximately 1.8 and 3.8 times greater than previous net-based biomass estimates. We also show a peak in fish biomass towards the seasonal ice-edge, corresponding to the preferred feeding grounds of penguins and seals, which may be at risk under future climate change scenarios. Our study provides new insights into the abundance and distributions of ecologically significant mesopelagic fish stocks across the Southern Ocean ecosystem.