Unique thermal sensitivity imposes a cold-water energetic barrier for vertical migrators

Many oceanic animals (for example, krill to jumbo squids) undertake diel vertical migrations across steep gradients in light, temperature, and oxygen, contributing to biogeochemical fluxes and interacting with oxygen minimum zones. While climate change has driven latitudinal range shifts in marine fauna, the mechanisms controlling the distributions of vertical migrators remain unclear. Some tropical zooplankton and the jumbo squid Dosidicus gigas have expanded poleward during warming events, reshaping food webs. Conventional explanations often emphasize oxygen limitation in warming waters, but vertical migrators appear to tolerate broad temperature ranges between surface and depth. This study asks how temperature and oxygen jointly shape the aerobic performance of vertical migrators and whether thermal sensitivity of metabolic traits imposes energetic barriers that govern their native ranges and potential climate-driven expansions. Using the Metabolic Index framework, the authors hypothesize that cold, rather than warm, waters impose an energetic (aerobic scope) barrier to poleward range expansion due to ecological selection for high activity in warm surface waters and relaxed selection at cold, hypoxic depths.

Prior work links climate warming to marine range shifts at species and community levels, with notable tropicalization events in the North Pacific. Studies have invoked multiple drivers, including productivity, life-history, circulation, and physicochemical changes. The Metabolic Index framework has been used to connect oxygen supply capacity and environmental oxygen to habitat constraints, generally finding Pmax near air saturation in coastal species and declining aerobic scope with warming. Mesopelagic and OMZ-adapted species show enhanced hypoxia tolerance and metabolic suppression at depth. However, temperature sensitivities of metabolic traits in vertical migrators have been undercharacterized, particularly regarding how selection for activity in light-rich surface waters versus low-light mesopelagic refuges shapes oxygen supply capacity and aerobic scope across temperatures.

The study integrates laboratory respirometry and environmental mapping within the Metabolic Index framework to quantify oxygen supply capacity (α), standard metabolic rate (SMR), critical PO2 (PcSMR), maximum metabolic rate (MMR), and factorial aerobic scope (FAS). Temperature sensitivity of traits was expressed as Arrhenius slopes (E). Key components:

• Species and traits: Six vertically migrating euphausiids (krill) and the jumbo squid Dosidicus gigas; comparative dataset of diverse coastal species. For D. gigas, both SMR and MMR were compiled from literature; for euphausiids, new SMR and PcSMR measurements at 10 and 20 °C were made, along with α.
• Animal capture and respirometry (euphausiids): Live krill collected with a modified Tucker trawl (insulated cod end) during R/V Sikuliaq cruise SKQ2017015 (Jan–Feb 2017) in an Eastern Pacific OMZ region. After 6–12 h acclimation at target temperature in air-saturated water, individuals were sealed in darkened chambers (2–50 ml; chamber volume:mass ~10–100) with filtered seawater plus antibiotics. PO2 was monitored optically (Loligo Witrox 4 or PyroScience FireSting O2) as it declined to the level insufficient to support respiration (trial duration 6–48 h). Temperature control via water baths; oxygen meters calibrated to air-saturated seawater and Na2SO4 solutions; stirring provided. Post-trial, animals were frozen and weighed.
• Determining oxygen supply capacity α: For species with published SMR and PcSMR, α = SMR / PcSMR. For four euphausiids, α was directly estimated within trials by dividing MR by concurrent PO2 across time bins; the average of the highest three α values per trial defined α.
• Temperature coefficients (E): Derived from Arrhenius plots (slope of ln(metric) vs 1/kBT). Because metrics are related, E values satisfy Ea = EMMR − EPcmax = ESMR − EPcSMR.
• Environmental mapping: World Ocean Atlas 2018 fields for temperature and oxygen were extracted for a 500–2,000 km offshore band along the eastern Pacific (55°S–55°N), across 0–500 m depth in 37 bins. Measured SMR, PcSMR, α, and their temperature dependencies (E) were adjusted to any given T using respirometry R package adj_by_temp(). For all non-squid species, PO2max at 25 °C was assumed 21 kPa; MMR at 25 °C estimated as 21 kPa × α; EMMR assumed either 0.3 eV (coastal mean) or 1.0 eV (minimum avoiding oxygen limitation). Derived metrics per grid cell included: MMRPO2 = PO2 × SMR / PcSMR; MMRT = SMR × PO2max / PcSMR; FASPO2 = MMRPO2 / SMR; FAST = MMRT / SMR; MMRmin = min(MMRPO2, MMRT); FASmin = min(FASPO2, FAST); Pcmax = FAST × PcSMR. Averages were computed for each 0.25° latitude bin and depth.
• Dosidicus gigas mapping: Used measured MMR and EMMR. MMR showed low temperature sensitivity between 10–20 °C (EMMR = 0.21) and very high sensitivity between 20–25 °C (EMMR = 1.65). These piecewise E values were used in mapping.
• El Niño and climate projections: Sea-surface temperatures from NOAA DOISST v2.1 (monthly, Jun 1997–Jun 1998) for El Niño and CMIP6 SSP5-8.5 periods (2021–2040, 2041–2060, 2081–2100) were used; surface PO2 assumed 21 kPa. FAS under these conditions was compared to WOA-based surface FAS.
• Monte Carlo sensitivity: For D. gigas, 5,000 iterations drew SMR, MMR, and PcSMR from normal distributions parameterized by means and SEs; complete mapping recomputed each iteration to produce 95% CIs for derived metrics (e.g., FAS, Pcmax) per latitude-depth bin. Additional sensitivity runs used fixed E values.
• Scaling: Where needed (D. gigas), metabolic rates were normalized to 100 g body mass using measured scaling exponents (e.g., SMR = 13.03 M^−0.117; Pc ≈ 2.44 M^−0.03).

• Vertical migrators possess high, temperature-invariant oxygen supply capacity (α) across their day-night depth-temperature gradient, unlike coastal species. Mean α for Eastern Pacific migrators was ~3.84 µmol O2 g−1 h−1 kPa−1, much higher than coastal species (0.64 ± 0.45 µmol O2 g−1 h−1 kPa−1).
• In migrators, SMR and PcSMR exhibit similar temperature sensitivities (relationship: y = 0.94X + 0.21; n = 7 species; P = 0.06), yielding α that is relatively insensitive to temperature (α higher: P = 1.76 × 10−2; temperature insensitivity: P = 3.06 × 10−10) compared with coastal taxa where SMR is more temperature sensitive than PcSMR (y = 0.62X − 0.06; n = 20; P = 4.3 × 10−7).
• Enhanced thermal sensitivity of active metabolism: For D. gigas, MMR is weakly temperature sensitive between 10–20 °C (EMMR = 0.21) but extremely sensitive between 20–25 °C (EMMR = 1.65). A temperature coefficient for MMR <1.0 eV in tropical settings implies oxygen limitation at depth; >1.0 eV would depress capacity at cold temperatures.
• Cold-water aerobic barrier: Aerobic scope (FAS) is low in cold waters, even at air-saturated PO2, due to ecological selection patterns. For D. gigas, surface FAS falls below ~2–3 at native poleward range edges; higher latitudes are metabolically unavailable (FAS < 3) because persistent cold restricts MMR relative to SMR.
• Oxygen versus temperature limitation: In temperate waters, oxygen levels typically do not limit FAS; deoxygenation would need to reduce PO2 by >50% to significantly limit FAS. Even if PO2 < Pcmax, FAS would decline only by ~5% per kPa in surface waters, far less impactful than temperature-driven constraints.
• Range dynamics with warming: Warmer conditions (e.g., 1997–1998 El Niño and projected SST increases under SSP5-8.5) expand metabolically available habitat (FAS > 3) poleward by ~10–20° latitude in both hemispheres for D. gigas. Similar cold-water barriers likely exist for euphausiids; model outputs show highest FAS in native warm ranges and reduced FAS at higher latitudes, especially when EMMR is high (1.0 eV).
• Robustness: Monte Carlo simulations indicate that while absolute values vary, the qualitative pattern of surface FAS ≥ 3 in the tropical-subtropical core and < 3 at higher latitudes persists across 95% confidence intervals.

Findings support the hypothesis that cold waters impose an energetic (aerobic scope) barrier to poleward range expansion in vertical migrators. Selection for high metabolic capacity in warm, well-lit surface waters (predator–prey interactions) and relaxed selection at cold, low-light mesopelagic depths have yielded a physiology characterized by high, temperature-invariant oxygen supply capacity but enhanced thermal sensitivity of active metabolism. Consequently, aerobic scope is disproportionately depressed at cold temperatures beyond what thermodynamic expectations alone would predict, even when oxygen is not limiting, thereby constraining distributions. This framework reconciles observations of tropical migrator range expansions during warm anomalies and suggests that climate warming will relax cold-water barriers, enabling further poleward expansion. Oxygen declines, in contrast, are unlikely to substantially limit aerobic scope in temperate surface waters under plausible scenarios, though some compression of tropical habitats may occur due to warming at the surface and OMZ shoaling at depth. Overall, temperature operates as a metabolic regulator in vertical migrators due to ecological context, and the Metabolic Index mapping links individual physiological traits to biogeographic patterns and future shifts.

The study identifies a unique thermal sensitivity in vertical migrators: a high, temperature-invariant oxygen supply capacity paired with an enhanced temperature sensitivity of active metabolism. This physiology produces a cold-water energetic barrier that limits poleward distributions despite ample oxygen, explaining native tropical ranges and observed warm-event expansions. Climate warming is predicted to alleviate this barrier, expanding metabolically available habitat, whereas deoxygenation alone will have limited impact on aerobic scope in temperate surface waters. Contributions include: new euphausiid respirometry data, explicit temperature–oxygen mapping of aerobic scope across latitude and depth, and evidence that ecological selection shapes thermal responses of metabolic traits. Future research should directly measure MMR and temperature coefficients across more migrators, refine parameterizations of α and Pc across sizes and life stages, incorporate behavior and diel activity patterns into scope mapping, and integrate more realistic oxygen scenarios (including future OMZ dynamics) to assess habitat compression and ecosystem consequences.

• Extrapolation beyond measured temperature ranges (notably >25 °C) when projecting climate-change effects and El Niño scenarios.
• For all species except Dosidicus gigas, MMR and EMMR were not directly measured; EMMR values (0.3 or 1.0 eV) were assumed for mapping.
• Assumed PO2max = 21 kPa at the surface; for El Niño and CMIP6 SST mappings, oxygen data were not available and were assumed to be 21 kPa.
• Most species were measured over narrow body-size ranges, limiting robust scaling analyses; mapping used normalization and literature scaling where available.
• Model focuses on temperature and oxygen; other ecological and physiological factors (e.g., food availability, behavior, life history, circulation) may also influence range limits but were not explicitly modeled.
• Piecewise EMMR for D. gigas may introduce uncertainties outside the 10–25 °C range.