The current anthropogenic global warming – estimated in an increment of sea temperature from 1 to 3°C for the next decades – is expected to generate profound metabolic alterations in marine ectotherm invertebrates, which can have consequences in the distribution and abundance of a wide number of species (Brown et al. 2004; Lefevre 2016; Madeira et al. 2016). Mobile species may tend to move to an environment where thermal conditions are more favorable but could provoke changes in the energetic relationship among the original components of the ecosystem (Cheung et al. 2008; Maharaj et al. 2018; Ángeles-González et al. 2021a, b). Although the physiological processes are enhanced under high temperatures and result in high energy production, they also provoke the increment of deleterious reactive oxygen species (ROS; Johnstone et al. 2019). The mitochondrial respiratory chain is one of the main ROS (e.g., hydroxyl and superoxide radicals, singlet oxygen, etc.) and reactive nitrogen species (RNS; e.g., nitric oxide, peroxynitrite, etc.) produced naturally through physiological and non-physiological processes (Fridovich 1986; Feidantsis et al. 2021).
Oxidative stress produced by ROS consists of deleterious cumulative biomolecular cell damage, mainly oxidation of lipids, proteins, and nucleic acids (Storey 1996; Hulbert et al. 2007). The progressive accumulation of these biomolecules in cells and tissues modifies the function of these structural elements and enzymatic activity, generating damage to the proteasomal system (Beckman and Ames 1998; Grune et al. 2001; Passos and Von Zglinicki 2006). The cell antioxidant defense mechanisms (ANTIOX) consist of a group of enzymes (e.g. catalase, glutathione peroxidase, peroxiredoxin; Di Giulio et al., 1989) complemented by some low-weight non-enzymatic molecules (e.g. vitamins A, C, and E, bilirubin, beta-carotene, uric acid, and flavonoids; Rahal et al., 2014) that progressively reduce ROS into safe compounds (e.g. O2 and H2O; Halliwell 2013) or break the autocatalytic chain of radical reactions (Cadenas 1989), respectively. However, in organisms subjected to heat stress, ROS production can surpass the ANTIOX system, producing a condition named pejus, in which the organism survival depends on the exposure time to heat stress or ability to reduce metabolism, and consequently, ROS production (Pörtner 2010; Pörtner et al. 2017; Rodríguez-Fuentes et al. 2017). Numerous theories have been related to the cumulative oxidative damage produced by ROS in cells with degenerative processes associated to senescence in the individuals (e.g. somatic mutational theory, mitochondrial-DNA mutational hypothesis of cell aging, and the free radical theory of aging; Harman 1956). However, the most worrying consequence of global warming might be the effect of thermal stress overpassing the capacity of individual generations to neutralize ROS with profound costs for the ecology of populations and communities (Parmesan 2006; Massamba-N´Siala et al. 2014). Moreover, increasing thermal stress length during the reproductive phases results even more in a stronger transgenerational response (Salinas and Munch 2012; Dupont et al. 2013). Therefore, to predict the way in which populations could react to changes in the environment -taking into account the transgenerational effect of thermal stress- is a milestone for understanding the full effects of global warming (Hendry et al. 2008).
Evidence has suggested that thermal tolerance between generations can be enhanced through thermal preconditioning of adults to trigger an epigenetic response that could increase the thermal tolerance of their offspring. To mention some, the process has been defined as cross-generation plasticity (CGP), when the environment experienced by parents influences offspring phenotype: F0–F1; multigenerational plasticity (MGP) when the environment experienced by previous generations is evident to the F2 and beyond: F1–F2+; and carry-over effects (COE) that occur within the development (e.g. embryo to larva; Byrne et al. 2020). Although thermal stress in parents has been suggested as an effective mechanism for coping with temperature increases, thereby enhancing progeny performance under thermal stress through epigenetic inheritance (Fellous et al. 2015, 2022; Eirin-Lopez and Putnam 2021), studies performed on the mussel Mytilus californicus and Octopus maya embryos have provided evidence for negative parental effects on offspring thermal tolerances (Dominguez-Castanedo et al. unpubl data; Waite and Sorte 2022).
Octopus maya supports one of the most important octopus fisheries at the world level, with an annual production of around 20,000 Tons and it is considered that their catch has reached the maximum sustainable yield. This species, endemic of the Yucatan Peninsula; is relatively sensitive to thermal stress (Ángeles-González et al. 2020, 2021b) as embryos (Caamal-Monsreal et al. 2016), juveniles (Noyola et al. 2013a) and adults (Juárez et al. 2015). When temperature was evaluated in adult O. maya females, the number of spawned and fertilized eggs was lower above 27ºC than in females maintained at 24ºC (Juárez et al. 2015). These results indicate that high temperature affects negatively, not only the capacity of females to produce eggs but also the way in which sperms fertilize them in the oviductal gland. In experiments with male octopus, temperatures of 28ºC or higher provoked testicular damage, reducing their parental contribution in progeny (López-Galindo et al. 2019). These results evidence that temperatures from 28°C to 30°C deeply affect the reproductive performance of this octopus species. Studies of temperature effects on gene expression of O. maya females (Juárez et al. 2019) showed that the white body (located in the brain) at high temperatures up-regulates the expression of genes related to nutrient transport, proteolysis, and response to temperature stimulus, probably associated with embryo development. Moreover, other studies have demonstrated that females invest additional energy during the reproductive process to maintain energy reserves for parental care (Roumbedakis et al. 2018; Juárez et al. 2019; Lin et al. 2019), which indicates that high temperatures could be affecting their ability to channel enough energy to all the events involved in reproduction (Meza-Buendía et al. 2021). Until now, our research group has identified that for O. maya an adverse parental carry-over of thermal effects exists, which may be associated with trade-offs between the female condition (less aerobic scope and energy for yolk synthesis at high temperatures) and the investment required (yolk quantity) to have a successful offspring (Dominguez-Castanedo et al. unpubl data). In a recent study, smaller sizes, less yolk, higher metabolic rates, and lower CAT activity and total glutathione (GSH) concentrations were observed in embryos from thermally stressed females than those observed in embryos from females maintained in optimal thermal conditions, indicating that maternal thermal stress exerts sever effects in the progeny of this octopus species.
Previous studies have also demonstrated that exposure time is another variable that should be considered when thermal sensibility is evaluated in ectotherm organisms (Pörtner 2017). Furthermore, metabolic and growth alterations have been observed in O. maya juveniles exposed to 30°C constant for more than 20 days when compared with animals exposed to temperature increments of 1°C d-1 until reaching 30°C (Juárez et al. 2016). To explain these results, the hypothesis is that octopuses exposed to a thermal ramp have the opportunity to make metabolic and energetic adjustments that allow them to maintain their homeostasis. On the contrary, octopuses kept in high constant temperatures were unable to maintain physiological stability, mainly because of ROS accumulation and the collapse of the ANTIOX defense mechanism.
The Yucatán peninsula has two well-differentiated oceanographic areas. One in the northern zone where a seasonal upwelling maintains the shelf floor temperature from 22 to 24°C in summer, while they can reach more than 30°C on the floor of the western zone temperatures (Fig. 1; Enriquez et al. 2013).
In consequence, oceanographic conditions drive the octopus population to have different biological cycles. In the northern zone, reproduction occurs year-round where the upwelling maintains the temperatures below 26°C even in summer (Fig. 1). In the western zone, the reproductive peak is concentrated in winter, when polar winds chill the platform (Angeles-Gonzalez et al. 2017; Juárez et al. 2018; Markaida et al. 2016). In such circumstances, females that spawn in the western zone incubate the embryos during the winter months (January to March) when temperatures are expected to be maintained from 22 to 26°C. Considering that in the western zone there is no influence of upwelling is highly probable that this zone, in warming scenarios, experiencing short and hard winters followed by high temperatures that could extend the summer season with high temperatures (IPCC 2021). In such a scenario, hatchlings could be exposed to fast temperature increments and sub-optimal thermal conditions that could affect their performance affecting at the end the population (Noyola et al. 2013a; Noyola et al. 2013b). In the past, variations in octopus landings were associated with thermal anomalies resulting from El Niño–Southern Oscillation (ENSO) events (Comisión Nacional de Pesca y Acuacultura, 2016). Using that information Ángeles-Gonzalez et al. (2017) found that the octopus fishery production is negatively affected in the western zone of the Yucatan Peninsula when temperature increases 2°C above average during an ENSO event. This effect has led to the hypothesis that the ENSO anomaly could be causing octopus migration from the western to eastern zone, where temperature increase is limited by seasonal upwelling. If this hypothesis is true, in warming scenarios or during the ENSO anomalies juveniles feel obligated to migrate to cooler environments before the thermal conditions affect their physiological condition irreversibly. The results obtained in early O. maya juveniles showed that 20 days at 30°C reduces their growth rate and survival because of the energetic costs associated to maintain the high metabolic rate in high temperatures (Noyola et al. 2013b), indicating that if juveniles do not migrate to low temperature environments their performance could be compromised.
Until now, evidence has demonstrated that high temperatures alter the physiological condition of O. maya embryos, juveniles, and adults and that time of exposure could have a key role in their thermal tolerance. This fact can be explained because animals depend on the duration of energetic reserves and the ability of antioxidant defense mechanisms to neutralize ROS when exposed to high temperature environments (Caamal-Monsreal et al. 2016; Meza-Buendia et al. 2021; Noyola et al. 2013b). Besides the time of exposure, thermal tolerance has also been observed to depend on the thermal history of the broodstock, which has a key role in the transgenerational thermal tolerance.
Until now, we know that in the scenario of thermal stress O. maya embryos, from thermally stressed females showed a reduction in their physiological performance and also in their survival (Domíngues-Castanedo et al unpublished data). Based on that, in the present study we design a series of experiments with the aim to evaluate the effects of thermal stress and time of exposure to optimal (25°C) and high temperatures (30°C) on O. maya juveniles obtained from thermal stressed and non-stressed females to provide an answer to the following question: i) Is there a relationship between maternal thermal condition and the ability of animals to make adjustments in their respiratory metabolism (Routine and high metabolic rate) and antioxidant defense mechanisms during conditioning time to optimal (25°C) and high temperatures (30°C), independently of the embryo physiological condition? ii) When the juveniles from embryos spawned by non-stressed females are exposed to thermal stress, what is the relationship between respiratory metabolism, the antioxidant defense mechanisms, and the exposure time allowing (or not) animals to survive?
In this sense, this study postulates the hypothesis that maternal thermal stress experienced by the embryos limited the physiological performance of juveniles, preventing animals from responding to thermal stress potentially present in warming scenarios.
In the case of animals from non-thermally stressed females, the limitations of the antioxidant system are expressed through ROS accumulation, which could explain the deterioration and mortality previously observed in juveniles exposed to temperatures above the optimal range (22 to 27°C) for more than 20 days (Noyola et al. 2013b).