Thermal optimality and physiological parameters inferred from experimental studies scale latitudinally with marine species occurrences.

Ocean warming is expected to occur due to anthropogenic climate change bringing a spatial shift of marine communities. Experimental data that characterize the aerobic power budget via an aerobic scope, thermal metabolic scope, or thermal preferences have been proposed as tools that can describe species distribution since they characterize species fitness or performance under different temperatures. This study tested the potential relationship between observed occurrences and different physiological studies in the Americas for 11 commercially important species in Mexico. Projections were also developed for Mexico's exclusive economic zone under different climate warming scenarios. The physiological data were fitted from optimum up to pejus temperatures and projected to sea surface temperatures for present (2003-2014) and Representative Concentration Pathway (RCP) scenarios (RCP 2.6, RCP 4.5, RCP 6.0, and RCP 8.5) for the period 2040-2050 and 2090-2100. For species with wide distributions in the Americas, the number of occurrences reported decreases at higher latitudes related to the decrease in species performance calculated from laboratory experiments. In addition, higher species occurrences are usually reported around optimum temperatures. Overall, the results suggest that pejus temperatures likely restrict latitudinal distribution, at least for widely distributed taxons. Regarding Mexican projections, the results varied widely by species. For example, in the Atlantic Ocean, Octopus maya and Panulirus argus are vulnerable to warming scenarios, while Centropomus undecimalis is not. Interestingly, northern Campeche Bank, the Gulf of California, and Western Baja California may act as thermal refugia for marine species indicating they could be assigned as protected areas to support fisheries throughout the Mexican exclusive economic zone. This research adds to the increasing evidence of the relationship between thermal niche and wild population distribution.

Benzophenone-3 does not Cause Oxidative Stress or B-esterase Inhibition During Embryo Development of Octopus maya (Voss and Solís Ramírez, 1966).

Benzophenone-3 (BP-3) is an active ingredient in sunscreen lotions and personal-care products that protects against the damaging effects of ultraviolet rays. Given its worldwide dissemination, it has been linked with harmful effects on aquatic biota; however, its impact is not fully understood calling for further studies. To understand the impacts on an important economically and ecologically species, we evaluated the toxicity of BP-3 during the embryonic development of Octopus maya. Embryos were exposed to increasing concentrations of up to 500 µg BP-3/L until hatching. Antioxidant enzyme activities, oxidative-stress indicators, and B-esterases activities were measured at different developmental phases (organogenesis, activation, and growth). There were no significant differences between treatments, suggesting the lack of production of toxic metabolites that may be related to a protective chorion, an underdeveloped detoxification system, and the experimental conditions that limited phototoxicity.

Effects of Phenanthrene Exposure on the B-esterases Activities of Octopus maya (Voss and Solís Ramírez, 1996) Embryos.

No ecotoxicological information exists on phenanthrene (Phe) exposure in cephalopods, animals of commercial and ecological importance. This study investigated the effect of Phe on two B-esterases, Acetylcholinesterase (AChE) and Carboxylesterases (CbE), in Octopus maya embryos. Octopus embryos were exposed to different treatments: control (seawater), solvent control (seawater and DMSO 0.01%), 10 and 100 µg/L of Phe. AChE and CbE activities were measured at different developmental stages (blastula, organogenesis, and growth). B-esterase activities increased in control and solvent control as the embryos developed, showing no statistically significant differences between them. On the other hand, the embryos exposed to Phe had significant differences from controls, and between the high and low concentrations. Our results indicate that B-esterases are sensitive biomarkers of exposure to Phe in O. maya. Still, complementary studies are needed to unravel the toxicodynamics of Phe and the implications of the found inhibitory effect in hatched organisms.

The thermal tolerance of a tropical population of blue crab (Callinectes sapidus) modulates aerobic metabolism during hypoxia.

The blue crab Callinectes sapidus is a widespread ectothermic species that supports large fisheries. Physiology of temperate and subtropical populations of blue crabs are well studied; however, a lack of information exists on tropical populations. Given the low locomotion capabilities of C. sapidus adult blue crabs, natural selection should favor traits that shape a particular thermal niche reflected through tolerance modulation to dissolved oxygen (DO). This study was designed to evaluate the thermal window and hypoxia sensitivity of the blue crab population in the southern Gulf of Mexico. The effect of acclimation temperatures from 20 °C to 34 °C on thermal preference (TP), critical thermal limits (CT), and thermal metabolic scope (TMS) was assessed in normoxia. Metabolic rate regulation over oxygen partial pressure (pO2) gradient was evaluated through oxygen consumption measurements at different degrees of acute hypoxia. Callinectes sapidus was observed tending to specialize towards higher temperatures, showing a mean TP from 26 °C to 33 °C. The lowest performance of aerobic pathways was observed at the coldest regimes and the highest at the warmest ones with mean TMS value being 35 % greater at 34 °C than 20 °C. Patterns for metabolic regulation were dependent on the interaction between environmental temperature and DO, in which the interval from 29 °C to 34 °C provoked a 50 % reduction in oxygen consumption when exposed to ∼20% air saturation levels. The results obtained showed that blue crabs distributed in the southern Gulf of Mexico could be close to their oxygen-temperature tolerance limits, which has important implications when climate change effects on species re-distribution is considered.

Exploring the effects of warming seas by using the optimal and pejus temperatures of the embryo of three Octopoda species in the Gulf of Mexico.

Using data related to thermal optimal and pejus of the embryos of Octopus americanus from Brazil and O. insularis and O. maya from Mexico, this study aimed to project the potential distribution areas in the Gulf of Mexico and predict distribution shifts under different Representative Concentration Pathway scenarios (RCP 6 and 8.5) for the years 2050 and 2100. The different thermal tolerances elicited different responses to current and future scenarios. In this sense, O. insularis and O. maya thermal niches stretch from the Caribbean to Florida. Nevertheless, O. insularis may inhabit warmer areas than O. maya. Surprisingly, no area was considered thermally habitable for O. americanus, which could have been associated with the use of data of populations thermally adapted to temperate conditions south of Brazil. According to models, a warming scenario would cause a restriction of the available thermal niche of O. maya, while O. insularis could expand under RCP 6 scenarios. This restriction was more substantial in the RCP 8.5 scenario. Nevertheless, under the RCP 8.5 scenario, the temperature in 2100 may negatively affect even O. insularis, the species most thermal tolerant. If our results are accurate, the fishing yield of O. insularis will increase in the future, replacing the heavily exploited O. maya in the coasts of the southern Gulf of Mexico. Regarding O. americanus, no inference might be made until thermal tolerances of locally adapted populations can be studied.

Thermal biology of prey (Melongena corona bispinosa, Strombus pugilis, Callinectes similis, Libinia dubia) and predators (Ocyurus chrysurus, Centropomus undecimalis) of Octopus maya from the Yucatan Peninsula.

On the Yucatan Peninsula there is an upwelling which allows access to a body of cold water that controls temperature in this area. This modulates the ecology and distribution of organisms that inhabit the continental shelf. The objective of this study was to determine the effect of different acclimation temperatures on the thermal biology of prey as mollusc, crustacean (Melongena corona bispinosa, Strombus pugilis, Callinectes similis, Libinia dubia) and predators as fish (Ocyurus chrysurus, Centropomus undecimalis) of Octopus maya. Octopus prey preferred temperatures between 23.5°C and 26.0°C, while predators preferred temperatures 26.4-28.5°C. The species with largest thermal windows were M. corona bispinosa (328.8°C(2)), C. similis (322.8°C(2)), L. dubia (319.2°C(2)), C. undecimalis (288.6°C(2)), O. chrysurus (237.5°C(2)), while the smallest thermal window was for S. pugilis (202.0°C(2)). The acclimation response ratios (ARR) estimated for prey ranged from 0.24-0.55 in animals exposed to CTMax and 0.21-0.65 in those exposed to CTMin. Amongst predators, ARR ranged from 0.30 to 0.60 and 0.41 to 0.53 for animals exposed to CTMax and CTMin, respectively. Correlating the optimal temperature limits of prey and predators with surface temperatures on the continental shelf and those 4m deep showed that the main prey, Callinectes similis and L. dubia, shared a thermal niche and that an increase in temperature could force these species to migrate to other sites to find optimal temperatures for their physiological functions. As a consequence the continental shelf community would undergo a structural change. Predators were found to be near their optimal temperatures in surface temperatures on the continental shelf. We conclude that they would remain in the area in a warming scenario. The size of the thermal window was related to the type of ecosystem inhabited by these species. These ARR intervals allowed us to categorize the species as temperate or tropical, according to the oceanographic conditions that prevail on the Yucatan Peninsula.

Cephalopod culture: current status of main biological models and research priorities.

A recent revival in using cephalopods as experimental animals has rekindled interest in their biology and life cycles, information with direct applications also in the rapidly growing ornamental aquarium species trade and in commercial aquaculture production for human consumption. Cephalopods have high rates of growth and food conversion, which for aquaculture translates into short culture cycles, high ratios of production to biomass and high cost-effectiveness. However, at present, only small-scale culture is possible and only for a few species: the cuttlefish Sepia officinalis, the loliginid squid Sepioteuthis lessoniana and the octopuses Octopus maya and O. vulgaris. These four species are the focus of this chapter, the aims of which are as follows: (1) to provide an overview of the culture requirements of cephalopods, (2) to highlight the physical and nutritional requirements at each phase of the life cycle regarded as essential for successful full-scale culture and (3) to identify current limitations and the topics on which further research is required. Knowledge of cephalopod culture methods is advanced, but commercialization is still constrained by the highly selective feeding habits of cephalopods and their requirement for large quantities of high-quality (preferably live) feed, particularly in the early stages of development. Future research should focus on problems related to the consistent production of viable numbers of juveniles, the resolution of which requires a better understanding of nutrition at all phases of the life cycle and better broodstock management, particularly regarding developments in genetic selection, control of reproduction and quality of eggs and offspring.

Evaluation of Octopus maya enzyme activity of the digestive gland and gastric juice.

As the demand for Octopus maya grows, sustainable farming practices become essential to prevent overexploitation, so that farming can be developed as a sustainable alternative to traditional fishing. Understanding the digestive dynamics of the octopus is essential for devising optimal dietary formulations in aquaculture. Despite the progress in understanding cephalopod digestion, little is known about the specific functioning of the digestive enzymes responsible for breaking down protein substrates. This knowledge gap underscores the need for further research to support sustainable O. maya population management. In this paper, dietary formulations are identified for cephalopods by characterizing O. maya digestive enzymes present in the digestive gland and gastric juice. The investigation revealed that acidic proteases showed a peak activity at higher temperatures than alkaline proteases. Inhibitors confirmed the presence of H, L, and D cathepsins. The lower activation energy of alkaline enzymes compared to acidic ones observed highlights an intriguing aspect of O. maya's digestive physiology. This research provides valuable insights into O. maya digestive enzyme functions, representing a significant advancement in formulating diets crucial for successful octopus farming that may help to fully understand its physiology.

The hard life of an octopus embryo is seen through gene expression, energy metabolism, and its ability to neutralize radical oxygen species.

The reproductive process in Octopus maya was analyzed to establish the amount of reactive oxygen species that the embryos inherit from females, during yolk synthesis. At the same time, respiratory metabolism, ROS production, and the expression of some genes of the antioxidant system were monitored to understand the ability of embryos to neutralize maternal ROS and those produced during development. The results indicate that carbonylated proteins and peroxidized lipids (LPO) were transferred from females to the embryos, presumably derived from the metabolic processes carried out during yolk synthesis in the ovary. Along with ROS, females also transferred to embryos glutathione (GSH), a key element of the antioxidant defense system, thus facilitating the neutralization of inherited ROS and those produced during development. Embryos are capable of neutralizing ROS thanks to the early expression of genes such as catalase (CAT) and superoxide dismutase (SOD), which give rise to the synthesis of enzymes when the circulatory system is activated. Also, it was observed that the levels of the routine metabolic rate of embryos are almost as high as those of the maximum activity metabolism, which leads, on the one hand, to the elevated production of ROS and suggests that, at this stage of the life cycle in octopuses, energy production is maximum and is physically limited by the biological properties inherent to the structure of embryonic life (oxygen transfer through the chorion, gill surface, pumping capacity, etc.). Due to its role in regulating vascularization, a high expression of HIf-1A during organogenesis suggests that circulatory system development has begun in this phase of embryo development. The results indicate that the routine metabolic rate and the ability of O. maya embryos to neutralize the ROS are probably the maximum possible. Under such circumstances, embryos cannot generate more energy to combat the free radicals produced by their metabolism, even when environmental factors such as high temperatures or contaminants could demand excess energy.

The impact of settleable atmospheric particulate on the energy metabolism, biochemical processes, and behavior of a sentinel mangrove crab.

We use the sentinel mangrove crab, Minuca rapax, as a model to investigate the effects of metallic settleable particulate matter (SePM) on wetland. Multiple levels of energetic responses, including (i) metabolic rate and energy budget, (ii) oxidative stress, and (iii) behavioral response by righting time, were assessed as well as the metal and metalloid content in crabs exposed to 0, 0.1 and 1 g.L-1 of SePM, under emerged and submerged conditions over five days, simulating the rigors of the intertidal habitat. Al, Fe, Mn, Cr, and Y exhibited a concentration-dependent increase. Metal concentrations were higher in submerged crabs due to the continuous ingestion of SePM and direct exposure through gills. Exposure concentration up to 1 g.L-1 decreased metabolic rate and enzymatic activities, reduced assimilation efficiency and energy for maintenance, and induces a slower response to righting time, probably by metal effects on nervous system and energy deficits. In conclusion, SePM exposure affects the redox status and physiology of M. rapax depending on he submersion regime and SePM concentration. The disruption to the energy budget and the lethargic behavior in M. rapax exposed to SePM implies potential ecological alterations in the mangrove ecosystem with unknown consequences for the local population.

Are haloclines distributional barriers in anchialine ecosystems? Physiological response of cave shrimps to salinity.

Anchialine systems are coastal groundwater habitats around the world which host a unique community of cave adapted species (stygobionts). Such communities are expected to be separated by haloclines into either fresh or saline groundwater communities, hence climate changes (e.g., eustatic sea level shifts) and anthropic driven changes (e.g., salinization) may have a great impact on these stygobiont communities. Here we used cave-restricted species of Typhlatya from the Yucatan Peninsula as models to identify physiological capacities that enable the different species to thrive in marine groundwater (T. dzilamensis) or fresh groundwater (T. mitchelli and T. pearsei), and test if their distribution is limited by their salinity tolerance capacity. We used behavior, metabolic rates, indicators of the antioxidant system and cellular damage, and lactate content to evaluate the response of individuals to acute changes in salinity, as a recreation of crossing a halocline in the anchialine systems of the Yucatan Peninsula. Our results show that despite being sister species, some are restricted to the freshwater portion of the groundwater, while others appear to be euryhaline.

Thermopreference, tolerance and metabolic rate of early stages juvenile Octopus maya acclimated to different temperatures.

Thermopreference, tolerance and oxygen consumption rates of early juveniles Octopus maya (O. maya; weight range 0.38-0.78g) were determined after acclimating the octopuses to temperatures (18, 22, 26, and 30°C) for 20 days. The results indicated a direct relationship between preferred temperature (PT) and acclimated temperature, the PT was 23.4°C. Critical Thermal Maxima, (CTMax; 31.8±1.2, 32.7±0.9, 34.8±1.4 and 36.5±1.0) and Critical Thermal Minima, (CTMin; 11.6±0.2, 12.8±0.6, 13.7±1.0, 19.00±0.9) increased significantly (P<0.05) with increasing acclimation temperatures. The endpoint for CTMax was ink release and for CTMin was tentacles curled, respectively. A thermal tolerance polygon over the range of 18-30°C resulted in a calculated area of 210.0°C(2). The oxygen consumption rate increased significantly α=0.05 with increasing acclimation temperatures between 18 and 30°C. Maximum and minimum temperature quotients (Q10) were observed between 26-30°C and 22-26°C as 3.03 and 1.71, respectively. These results suggest that O. maya has an increased capability for adapting to moderate temperatures, and suggest increased culture potential in subtropical regions southeast of México.

Moderate hypoxia mitigates the physiological effects of high temperature on the tropical blue crab Callinectes sapidus.

Dissolved oxygen (DO) and water temperature vary in coastal environments. In tropical regions, the ability of aquatic ectotherms to cope with hypoxia and high-temperature interactive effects is fundamental for their survival. The mechanisms underlying both hypoxia and thermal tolerance are known to be interconnected, therefore, the idea of cross-tolerance between both environmental stressors has been put forward. We investigated the combined role of hypoxia and temperature changes on the physiological responses of blue crab Callinectes sapidus living in the southern Gulf of Mexico. We measured oxygen consumption, plasmatic biochemical indicators, total hemocyte count (THC), and antioxidant activity biomarkers in muscle and gill tissues of blue crab acclimated to moderate hypoxia or normoxia and exposed to a thermal fluctuation or a constant temperature, the former including a temperature beyond the optimum range. Animals recovered their routine metabolic rate (RMR) after experiencing thermal stress in normoxia, reflecting physiological plasticity to temperature changes. In hypoxia, the effect of increasing temperature was modulated as reflected in the RMR and plasmatic biochemical indicators concentration, and the THC did not suggest significant alterations in the health status. In both DO, the antioxidant defense system was active against oxidative (OX) damage to lipids and proteins. However, hypoxia was associated with an increase in the amelioration of OX damage. These results show that C. sapidus can modulate its thermal response in a stringent dependency with DO, supporting the idea of local acclimatization to tropical conditions, and providing insights into its potential as invasive species.

High resolution respirometry of isolated mitochondria from adult Octopus maya (Class: Cephalopoda) systemic heart.

Mitochondrial respirometry is key to understand how environmental factors model energetic cellular process. In the case of ectotherms, thermal tolerance has been hypothesized to be intimately linked with mitochondria capability to produce enough adenosine triphosphate (ATP) to respond to the energetic demands of animals in high temperatures. In a recent study made in Octopus maya was proposed the hypothesis postulating that high temperatures could restrain female reproduction due to the limited capacity of the animals' heart to sustain oxygen flow to the body, affecting in this manner energy production in the rest of the organs, including the ovarium Meza-Buendia AK et al. (2021). Unfortunately, until now, no reports have shown temperature effects and other environmental variables on cephalopod mitochondria activity because of the lack of a method to evaluate mitochondrial respiratory parameters in those species' groups. In this sense and for the first time, this study developed a method to obtain mitochondrial respirometry data of adult Octopus maya's heart. This protocol illustrates a step-by-step procedure to get high yield and functional mitochondria of cephalopod heart and procedure for determining the corresponding respiratory parameters. The procedure described in this paper takes approximately 3 to 4 hours from isolation of intact mitochondria to measurement of mitochondrial oxygen consumption.

Maturation trade-offs in octopus females and their progeny: energy, digestion and defence indicators.

Sexual maturation and reproduction influence the status of a number of physiological processes and consequently the ecology and behaviour of cephalopods. Using Octopus mimus as a study model, the present work was focused in the changes in biochemical compound and activity that take place during gonadal maturation of females and its consequences in embryo and hatchlings characteristics. To do that, a total of 31 adult females of O. mimus were sampled to follow metabolites (ovaries and digestive gland) and digestive enzyme activities (alkaline and acidic proteases) during physiological and functional maturation. Levels of protein (Prot), triacylglyceride (TG), cholesterol (Chol), glucose (Glu), and glycogen (Gly) were evaluated. Groups of eggs coming from mature females were also sampled along development and after hatching (paralarvae of 1 and 3 days old) to track metabolites (Prot, TG, Glu, Gly, TG, Chol), digestive enzymes activity (Lipase, alkaline proteases, and acidic proteases), and antioxidant/detoxification defence indicators with embryos development. Based on the data obtained, we hypothesized that immature females store Chol in their ovaries, probably from the food they ingested, but switch to TG reserves at the beginning of the maturation processes. At the same time, results suggest that these processes were energetically supported by Glu, obtained probably from Gly breakdown by gluconeogenic pathways. Also, was observed that embryos metabolites and enzyme activities (digestive and antioxidant/detoxification enzymes) where maintained without significant changes and in a low activity during the whole organogenesis, meaning that organogenesis is relatively not energetically costly. In contrast, after organogenesis, a mobilization of nutrients and activation of the metabolic and digestive enzymes was observed, together with increments in consumption of yolk and Gly, and reduction in lipid peroxidation. Derived from our results, we also have the hypothesis that reactive oxygen species (ROS) were produced during the metabolic processes that occurs in ovarian maturation. Those ROS may be in part transferred to the egg provoking a ROS charge to the embryos. The elimination of ROS in embryos started when the activity of the heart and the absorption of the yolk around stages XIV and XV were evident. Altogether, these processes allowed the paralarvae to hatch with buffered levels of ROS and with the antioxidant defence mechanisms ready to support further ROS production derived from paralarvae higher life stage requirements (feeding and metabolic demands).

Comparison of Aerobic Scope for Metabolic Activity in Aquatic Ectotherms With Temperature Related Metabolic Stimulation: A Novel Approach for Aerobic Power Budget.

Considering that swim-flume or chasing methods fail in the estimation of maximum metabolic rate and in the estimation of Aerobic Scope (AS) of sedentary or sluggish aquatic ectotherms, we propose a novel conceptual approach in which high metabolic rates can be obtained through stimulation of organism metabolic activity using high and low non-lethal temperatures that induce high (HMR) and low metabolic rates (LMR), This method was defined as TIMR: Temperature Induced Metabolic Rate, designed to obtain an aerobic power budget based on temperature-induced metabolic scope which may mirror thermal metabolic scope (TMS = HMR-LMR). Prior to use, the researcher should know the critical thermal maximum (CT max) and minimum (CT min) of animals, and calculate temperature TIMR max (at temperatures -5-10% below CT max) and TIMR min (at temperatures +5-10% above CT min), or choose a high and low non-lethal temperature that provoke a higher and lower metabolic rate than observed in routine conditions. Two sets of experiments were carried out. The first compared swim-flume open respirometry and the TIMR protocol using Centropomus undecimalis (snook), an endurance swimmer, acclimated at different temperatures. Results showed that independent of the method used and of the magnitude of the metabolic response, a similar relationship between maximum metabolic budget and acclimation temperature was observed, demonstrating that the TIMR method allows the identification of TMS. The second evaluated the effect of acclimation temperature in snook, semi-sedentary yellow tail (Ocyurus chrysurus), and sedentary clownfish (Amphiprion ocellaris), using TIMR and the chasing method. Both methods produced similar maximum metabolic rates in snook and yellowtail fish, but strong differences became visible in clownfish. In clownfish, the TIMR method led to a significantly higher TMS than the chasing method indicating that chasing may not fully exploit the aerobic power budget in sedentary species. Thus, the TIMR method provides an alternative way to estimate the difference between high and low metabolic activity under different acclimation conditions that, although not equivalent to AS may allow the standardized estimation of TMS that is relevant for sedentary species where measurement of AS via maximal swimming is inappropriate.

Digestive Physiology of Octopus maya and O. mimus: Temporality of Digestion and Assimilation Processes.

Digestive physiology is one of the bottlenecks of octopus aquaculture. Although, there are successful experimentally formulated feeds, knowledge of the digestive physiology of cephalopods is fragmented, and focused mainly on Octopus vulgaris. Considering that the digestive physiology could vary in tropical and sub-tropical species through temperature modulations of the digestive dynamics and nutritional requirements of different organisms, the present review was focused on the digestive physiology timing of Octopus maya and Octopus mimus, two promising aquaculture species living in tropical (22-30°C) and sub-tropical (15-24°C) ecosystems, respectively. We provide a detailed description of how soluble and complex nutrients are digested, absorbed, and assimilated in these species, describing the digestive process and providing insight into how the environment can modulate the digestion and final use of nutrients for these and presumably other octopus species. To date, research on these octopus species has demonstrated that soluble protein and other nutrients flow through the digestive tract to the digestive gland in a similar manner in both species. However, differences in the use of nutrients were noted: in O. mimus, lipids were mobilized faster than protein, while in O. maya, the inverse process was observed, suggesting that lipid mobilization in species that live in relatively colder environments occurs differently to those in tropical ecosystems. Those differences are related to the particular adaptations of animals to their habitat, and indicate that this knowledge is important when formulating feed for octopus species.