Can octopus embryos and juveniles contend with heatwaves?

Abstract

Heatwaves are emerging climatological threats intensifying by climate change, that pose unprecedented challenges to thermally sensitive marine species. This study investigated the physiological and metabolic responses of O. maya offspring to heatwave conditions, focusing on oxidative stress, mitochondrial function, and survival. We simulated a critical scenario where females with an optimal thermal history (24°C) laid eggs at the onset of a heatwave, exposing the offspring to optimal (24°C), intermediate (26°C), or high (30°C) temperatures for the entire embryonic development (~45 days) and 30 days post-hatching. Embryos incubated at 30°C showed altered morphometry (reduced mantle and arm lengths) and suppressed routine metabolic rates by the end of embryonic development. Among antioxidants analyzed, total glutathione (GSH) emerged as a key factor in mitigating oxidative stress, supporting previous observations suggesting a key role in reactive oxygen species (ROS) protection. We hypothesized that energy reallocation to stress defense mechanisms compromised developmental processes, resulting in smaller hatchlings with reduced survival and diminished factorial metabolic scope. High-resolution respirometry revealed mitochondrial dysfunction, including increased proton leak and reduced respiratory efficiency, exacerbating oxidative damage and impairing oxygen transport. While some juveniles exhibited metabolic plasticity and elevated ATP production, these responses were insufficient to counteract the long-term costs of thermal stress. These findings suggest that although optimal thermal history, as seen in upwelling zones, may offer temporary protection, prolonged exposure to elevated temperatures could severely compromise reproductive success and population sustainability.

Fig 1. Sea bottom temperatures at Campeche (19.97°N, 90.87°W; black line) and Sisal (21.28°N, 90.05°W; red line) during the period 2016–2019.

Daily average temperatures were derived from hourly time series recorded by thermometers installed on two Acoustic Doppler Current Profilers (ADCPs).

Fig 2. Experimental design and number of replicates for each experimental group.

TIMR = Temperature-Induced Metabolic Rate (maximum: max; minimum: min); TMS = Thermal Metabolic Scope; ANTIOX = Antioxidant Defense System; dph = days post-hatching; dps = days post-spawning. Org, Act, and Gro represent the organogenesis, activation, and growth stages of embryo development, respectively. Females were maintained at 24°C, and their embryos were incubated at either 24°C, 26°C, or 30°C throughout development. After hatching, juveniles remained at the same temperature they experienced as embryos. The downward arrows indicate that all juveniles originated from females kept at 24°C and continued in their respective temperature treatments (24°C, 26°C, or 30°C) after hatching.

Fig 3. Morphological characteristics of Octopus maya embryos incubated at 24°C, 26°C, or 30°C.

Panels show data for the activation (A) and growth (B) stages of development. WW = Wet weight; TL = Total length; ML = Mantle length; AL = Arm length; ED = Eye diameter; YV = Yolk volume. Individual data points are shown for each treatment.

Fig 4. Routine oxygen consumption rates (RMR) of Octopus maya embryos incubated at 24°C, 26°C, and 30°C.

Values are expressed as mg O₂ g ⁻ ¹ h ⁻ ¹. Org, Act, and Gro correspond to the organogenesis, activation, and growth stages of development, respectively. Data are shown as mean ± SD, with individual data points included.

Fig 5. Antioxidant enzyme activity and oxidative damage markers in Octopus maya embryos incubated at 24°C, 26°C, and 30°C.

Antioxidant components include the enzyme superoxide dismutase (SOD), the tripeptide total glutathione (GSH), and the enzyme glutathione-S-transferase (GST). Oxidative damage markers include lipid peroxidation (LPO) and oxidized proteins (PO). Panels represent the organogenesis (A), activation (B), and growth (C) stages of development. Each panel includes a 2-D ordination plot showing the relative distances and group centroids. Individual data points are shown for each treatment.

Fig 6. Respiratory metabolism of juvenile Octopus maya chronically exposed to 24°C, 26°C, and 30°C, with thermal stress histories matching their embryonic incubation temperatures.

(A) Routine metabolic rate (RMR); (B) temperature-induced metabolic rate minimum (TIMR min); (C) temperature-induced metabolic rate maximum (TIMR max); (D) thermal metabolic scope (TMS) and factorial metabolic scope (FMS). Data are presented as mean ± SD, with individual data points shown for each group. Different lowercase letters indicate statistically significant differences among groups (P < 0.05).

Fig 7. Mitochondrial respiratory metabolism of juvenile Octopus maya chronically exposed to 24°C, 26°C, and 30°C, with thermal stress histories matching their embryonic incubation temperatures.

Parameters evaluated include State 3 respiration (A), State 4′o respiration (B), oxidative phosphorylation (OXPHOS) capacity (C), and the respiratory control ratio (RCR; D). State 3: Oxygen consumption in the presence of exogenous substrates (proline) and ADP, representing active mitochondrial respiration. State 4′o: Oligomycin-induced oxygen consumption, reflecting proton leakage and electron transport chain activity. OXPHOS capacity: Calculated as State 3 – State 4′o, representing ATP synthase activity. RCR: The ratio of State 3 to State 4′o, indicating mitochondrial coupling efficiency. Data are presented as mean ± SD, with raw data points represented as colored circles. Different lowercase letters denote statistically significant differences (P < 0.05).

Fig 8. Antioxidant enzyme activity and oxidative damage markers in juvenile Octopus maya chronically exposed to 24°C, 26°C, and 30°C, with thermal stress histories matching their embryonic incubation temperatures.

Antioxidant enzymes include superoxide dismutase (SOD), catalase (CAT), the tripeptide total glutathione (GSH), and glutathione-s-transferase (GST). Oxidative damage markers include lipid peroxidation (LPO) and oxidized proteins (PO). The embedded 2-D ordination plot shows the relative distances and centroids for each treatment group, highlighting clustering patterns and variability in antioxidant responses. Individual data points are shown for each treatment.