Effect of maternal temperature stress before spawning over the energetic balance of Octopus maya juveniles exposed to a gradual temperature change

Journal of Experimental Marine Biology and Ecology 474 (2016) 39–45

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Effect of maternal temperature stress before spawning over the energetic balance of Octopus maya juveniles exposed to a gradual temperature change Oscar E. Juárez a, Verónica Hau b, Claudia Caamal-Monsreal c, Clara E. Galindo-Sánchez a, Fernando Díaz d, Denisse Re d, Carlos Rosas c,⁎ a Laboratorio de Genómica Funcional de Organismos Marinos, Departamento de Biotecnología Marina, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada–Tijuana # 3918, Ensenada, Baja California, México b Instituto Tecnológico de Tizimín, Tizimín Yucatán, México c Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Puerto de Abrigo s/n, Sisal, Yucatán, México d Laboratorio de Ecofisiología de Organismos Acuáticos, Departamento de Biotecnología Marina, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada–Tijuana # 3918, Ensenada, Baja California, México

a r t i c l e

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Article history: Received 16 February 2015 Received in revised form 30 September 2015 Accepted 1 October 2015 Available online xxxx Keywords: Phenotypic plasticity Energetic balance O. maya Temperature change

a b s t r a c t Octopus maya supports an important fishery in Yucatan Peninsula (YP) where this species is highly abundant. Considering that temperatures in the tropics are increasing (IPCC, 2013), there are several scenarios that can modify the dynamic of the O. maya population in YP: i) prolonged summer and short winter seasons, and/or ii) fast temperature increases and high temperatures after a winter season, both affecting the survival of hatchlings and the performance of juveniles. The present study was designed to evaluate the effect of maternal temperature stress over hatchling and juvenile performance in terms of their energetic plasticity and thermoregulatory behaviour, when they were exposed to a gradual temperature increase (TI) from 24 to 30 °C and compared with hatchlings maintained at preferred and constant temperature (24 °C). Hatchlings from stressed females were smaller, and had a lower growth rate compared to those from unstressed females providing evidence that temperature stress experienced by females has consequences on the performance of hatchlings, with effects on the biomass production and survival. Results also demonstrated that hatchlings exposed to TI (24–30 °C) had a growth rate and oxygen consumption similar to those maintained at preferred temperature (24 °C), in both female groups indicating that a gradual temperature increase of 1 °C every 5 days is probably enough to allow the organisms to make physiological adjustments without an excessive energetic cost. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Cephalopods are strongly influenced by temperature, as it play an important role in the regulation of embryo development, growth patterns and reproduction (Katsanevakis et al., 2005a, 2005b; André et al., 2009; Uriarte et al., 2012; Zuñiga et al., 2013). In cephalopods, respiratory metabolism has a central role in the survival and physiological performance, due to the high demand of energy that those organisms have for growth (Petza et al., 2011; Semmens et al., 2011) and locomotion activity (Wells and Clark, 1996). Temperature is the main environmental factor that controls the respiratory metabolism in cephalopods; therefore, it is considered the most important factor controlling the energy turnover and the fitness of cephalopods (Mangold, 1983; Farías et al., 2009; Noyola et al., 2013b).

⁎ Corresponding author. E-mail address: [email protected] (C. Rosas).

http://dx.doi.org/10.1016/j.jembe.2015.10.002 0022-0981/© 2015 Elsevier B.V. All rights reserved.

Temperature defines the distribution limits of marine animals and determines how they perform in the ecosystem (Clarke, 1996; Stillman and Somero, 2000; Somero, 2010; Tepolt and Somero, 2014); beyond these limits, growth and reproductive capacity decrease, thereby increasing vulnerability both in vertebrates and invertebrates (Pörtner and Knust, 2007; Sokolova et al., 2012; Magozzi and Calosi, 2015). These limits and their relationship with phenotypical plasticity (Pigliucci et al., 2006) allow us to know how possible climate changes could negatively affect marine populations in their natural distribution zones; those results are of particular interest when experiments are designed to resemble the temperature variations of the environment where the species inhabits (Clarke, 1996; Pörtner, 2002). Angilletta et al. (2002) proposed that the evolution of thermal sensitivity in ectothermic organisms relates body temperature with the environmental temperature. This relationship is not a coincidence, as the environment has selected organisms which performance is maximal at those temperatures. Therefore when the temperature chosen by the animal matches the naturally occurring temperature in an experimental

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gradient, it can be considered as the optimum temperature (Brett, 1971; Beitinger and Fitzpatrick, 1979; Magnuson et al., 1979; Hochachka and Somero, 1984; Angilletta et al., 2002; Noyola et al., 2013a). In Octopus maya juveniles a preferred temperature of 23.4 °C was identified (Noyola et al., 2013a). Results of growth and energetic balance indicate that, juveniles of O. maya maximise their efficiency to transform the ingested energy into body biomass in a temperature range of 22–26 °C, confirming that the theoretical value of final preferred temperature coincides with the range of temperatures in which the juveniles exhibit their maximum performance (Noyola et al., 2013b). These results provide evidence and relevant information related to the adaptive mechanism involved in the temperature tolerance of this species; however their interpretation is limited, because the animals were acclimated at constant temperatures that are far to those occurring in cultured or wild conditions. According to Pigliucci et al. (2006), the genotype generates phenotypes that are capable of responding to environmental changes, due to the fixation of characters during the evolutionary history of an organism, shaping its phenotypic plasticity. Examining the effects of temperature on the variation of a phenotype allows us to explore the interaction between an environmental change rate, performance scope and genetic variation within a population (Clarke, 1996). The Yucatan Peninsula (YP), located in the northern hemisphere of the American continent, is a transition site between the Caribbean Sea and the Gulf of Mexico. Oceanographic studies performed in this region show that the temperature of the adjacent continental shelf is regulated, at least partially, by the presence of a seasonal upwelling in summer. According to Enriquez et al. (2013), the upwelling arises in pulses, provoking temperature fluctuations between 22 and 26 °C. Although this upwelling has an influence on wide zones of the Gulf of Mexico, at the western edge of the continental shelf of YP, benthic temperatures can reach 30 °C during the summer, including areas where O. maya inhabits (Zavala-Hidalgo et al., 2006; Enriquez et al., 2013; Centre for Atmospheric Science, 2014). Juárez et al. (2015) demonstrated that the temperature is the stimulus that triggers the onset of spawning in O. maya. In their study, fertilised females were exposed to different possible thermal scenarios: a) high summer temperature (31 °C), b) winter temperature (24 °C) and c) a temperature decrease (TD) at a rate of 1 °C every 5 days from 31 to 24 °C, which resembles the summer-winter transition in the continental shelf of YP at the beginning of the O. maya spawning season. Juárez et al. (2015) observed that a temperature of 31 °C is enough to inhibit the spawning of O. maya females (only 13% of females spawned). The few fertilised eggs spawned died 2 weeks later, indicating that the high temperature was also deleterious to embryos. Females exposed to TD only spawned after the temperature was 27 °C and below (86% of females spawned). At the end of the experiment, a mean value of 530 eggs per spawn was observed in these females. They also observed that all females maintained at 24 °C spawned, with a mean value of 1208 eggs/spawn. From such results, it was evident that 27 °C is the threshold temperature that determines the O. maya spawning and that those higher temperatures provoke enough stress in the females to reduce the reproductive success. Their results suggest that O. maya females are adapted to avoid spawning at high temperatures because of the low survival of the embryos and hatchlings (Juárez et al., 2015). Considering that temperatures in the tropics are increasing (IPCC, 2013), there are possible scenarios that can affect the dynamics of O. maya population: i) prolonged summer and short winter seasons that reduce the time of low temperatures in the continental shelf, allowing the spawning of octopus females, but exposing them to temperature stress during maturation process; ii) fast temperature increases after the winter season, as a consequence of atmospheric elevation of temperature, affecting the benthic temperatures early in the year, and exposing hatchlings to gradual increases of temperature in their distribution zone; iii) reduction of the upwelling pulses, provoking higher temperatures

(i.e., 30 °C; Centre for Atmospheric Science, 2014) than observed when regular upwelling pulses arise (i.e., 24 °C; Enriquez et al., 2013). The strongest ocean warming is projected for the surface in tropical and northern Hemisphere subtropical regions, with an increase between 0.6 and 2.0 °C by the end of the 21st century, with scenarios where the atmosphere will be warming (IPCC, 2013). In such circumstances, a reduction on cold days could be expected, besides an increase in the number of hot days, generating gradual temperature increases in the O. maya hatchling zone. The present study was designed to evaluate if hatchlings spawned by females that experienced a thermal stress (after being exposed to TD), are affected in terms of their energetic physiology and thermoregulatory behaviour when they are exposed to a gradual temperature increase. 2. Method 2.1. Origin and acclimation of animals The study was carried out in the Experimental Cephalopod Production Unit (ECPU) at the UMDI-UNAM, Sisal, Yucatan, Mexico, following the procedures of Rosas et al. (2008) and Moguel et al. (2010) for collecting and maintaining egg-laying females of O. maya. Octopuses were caught using artisan lines, with live crabs as bait, in front of Sisal harbour (Yucatán, Mexico). The octopuses were transported from the port to the laboratory, which is situated 300 m inland, in a 120 L circular tank containing seawater. A total of 50 octopuses were used for the experiments. For all treatments, octopuses were acclimated outdoors during 14 days, in a semi-open aquaculture system consisting of 22 m3 circular liner tanks (maximum 30 animals per tank), keeping a 1:1 sex ratio. The system temperature ranged from 20 to 29 °C; with salinity of 36 psu and dissolved oxygen (DO) concentration around 5 mg L−1. Each octopus was fed fresh Callinectes sapidus (half of crab at the morning and half at the afternoon) with a mean weight of 130 g. Uneaten food and faeces were removed daily. During acclimation octopuses paired freely. Fertilised females (15 per treatment) were individually reared in 80 L tanks in a recirculating aquaculture system. Each tank included a fibreglass box that served as a refuge for the female and for spawn settlement. For stressed females, the initial system temperature was 31 °C, which was maintained for 10 days, and then the temperature dropped 1 °C every 5 days until the system reached 24 °C for a total of 40 days treatment. These conditions were selected because 24 °C is the preferred temperature and has been recommended as the best condition for the spawn (Noyola et al., 2013a; Rosas et al., 2014). The water was heated by a 1200 W titanium immersion heater connected to a digital temperature sensor, both at a system reservoir. The water was cooled using air conditioning, according to the temperature required. Salinity, aeration, diet and cleaning were kept the same as the conditions used during the acclimation for all treatments. Unstressed females (n = 15) were kept at 24 °C for 40 days with the same salinity, aeration, diet and cleaning as used in the treatment of stressed females. Spawns of both stressed and unstressed females were incubated at 24 ± 1 °C until hatching. Hatchlings from three females of each group were mixed and used in the experiment (48 hatchlings from stressed females and 48 from unstressed females); they were separated in four groups, each group with 24 hatchlings, such that hatchlings with the same thermal history were maintained at 24 ± 1 °C or exposed at a temperature ramp (Ramp) of 24–30 °C with increment of 1 °C every 5 days. Hatchlings were individualised in 500 mL containers and fed ad libitum with fresh crab–squid paste (Martinez et al., 2014) for 45–46 days. Every day, the food was added by opening the cap of the container without disturbing the animals. A clean Megalongena corona bispinosa shell was placed in each container as a refuge. The containers included windows covered with mesh and were placed into 40 L tanks connected to a flow-through seawater system

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and coupled to a skimmer and anthracite earth filter. Fifty percent of the seawater in the flow-through system was renewed daily. Eight 500 mL containers were placed in each tank, connected to a recirculation seawater system. A set of three 40 L tanks (each set with 24 hatchlings) with a specific experimental temperature (24 ± 1 °C or Ramp) was assigned to animals from different thermal histories (from stressed or unstressed females). A total of 96 hatchlings were maintained in twelve tanks with salinity of 38 psu, DO N 5.0 mg L−1 and pH ranging from 7.9 to 8.1. The temperature in all tanks was maintained using titanium heaters and chillers (1 HP) connected to temperature controllers. 2.2. Growth, feed intake and absorption efficiency Specific growth rate (SGR) was calculated as SGR = [(LnW2 − LnW1) / t] ∗ 100, where W2 and W1 are the octopuses' final and initial wet weights, respectively, Ln is the natural logarithm and t is the number of experimental days. Growth (g) in milligrammes per day (mg animal−1day−1) was calculated as g = (W2 − W1) / t. Survival was calculated as the difference between the number of animals at the beginning and at the end of the experiment. Phenotypic plasticity of the growth rate was calculated as the difference between growth rate obtained of animals exposed to Ramp and those maintained at 24 °C, from both stressed and unstressed females. 2.3. Energetic balance The effect of the experimental conditions on oxygen consumption was measured in organisms from each treatment (at 24 °C or at 30 °C for animals maintained in Ramp). The oxygen consumption (VO2) was measured using a continuous flow respirometer where respirometric chambers were connected to a well-aerated, recirculating seawater system (Rosas et al., 2008). Juveniles were placed in 90 mL chambers with an approximate flow rate of 0.1 L min−1. All animals were allowed to acclimatise to the chambers for 1–1.5 h before measurements were made. A Melongena corona bispinosa shell was offered as a shelter in each chamber. A chamber without an octopus (with a shelter) was used as a control, both during routine metabolism and feeding metabolism measurements. To do that, a similar ration used to feed each octopus was added to the control chamber. Measurements of DO were recorded for each chamber (at entrance and exit) every minute using oxygen sensors attached to flow cells, which were connected by an optical fibre to an Oxy 10 mini-amplifier (PreSens©, Germany). The sensors were calibrated for each experimental temperature using saturated seawater (100% DO) and a 5% sodium sulphate solution (0% DO). The fasting metabolism was obtained from measurements taken every minute for 60 min after the conditioning period. Afterwards, octopuses were fed, providing half of the ration (15% ww day− 1 ) two times a day, to complete a total ration of 30% ww day−1 (Quintana et al., 2011). Oxygen consumption measurements during the feeding phase were taken every minute until the oxygen consumption returned to pre-feeding values. Octopuses were weighed at the end of the experiment. The oxygen consumption was calculated as the difference in DO concentrations between the input and output of each chamber, with the water flow being timed. Routine metabolism (Rrout) was estimated from the VO2 (mg h− 1 g− 1 ww) values of fasting octopuses. The apparent heat increase (RAHI; J h−1 g− 1 dw) was estimated from the difference between VO 2 of fasting octopuses and the maximum value attained after feeding, taking into account the time needed to reach the oxygen consumption peak after feeding. The partial energy budget was estimated using the following equation (Lucas, 1993): AS = Rtot + Pg where AS is the assimilated energy, Rtot indicates respiration (Rtot = Rrout + RAHI) and Pg is the energy invested in growth, all of which are expressed as J g−1 dw day−1. Pg was obtained using the actual growth rate of all octopuses during the experimental time (45 days). A value of 10.1 kJ g− 1 was used to

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transform the growth data into energy production units of J g−1 day−1 dry weight (Rosas et al., 2004, 2008). Respiratory (R) and production net efficiency (Pg E) values were calculated as R / AS × 100 and Pg / AS × 100, respectively. The Phenotypic plasticity of production (PhPPg) was calculated using data of biomass production obtained for juveniles of O. maya maintained at 22 and 30 °C (Noyola et al., 2013b). 2.4. Preferred temperature The thermal preference of the octopuses was determined by the acute method described by Reynolds and Casterlin (1979), for which a horizontal gradient was generated, as described by Díaz et al. (2006), which consisted in a PVC pipe with 400 cm long and 20 cm in diameter, comprising 20 virtual segments of 20 cm each. The water column with 9 cm depth was heated by placing a 1000 W heater at one end of the pipe, whereas at the other extreme, water was cooled by using a chiller to set the gradient, which temperature ranged from 9 to 35 °C. In each segment, an air stone was placed to maintain a DO concentration range of 5–9 mg O2 L−1, and to avoid stratification in the water column. The temperature was measured in each virtual segment with an infrared digital thermometer (Steren model HER-425). Juveniles were not fed 24 h before testing in order to avoid interference caused by diet (Nelson et al., 1985; Beamish and Trippel, 1990). Early juveniles with different thermal histories and maintained at 24 °C or Ramp were randomly selected from each set of experimental conditions. One octopus at once was placed into the virtual segment of the gradient which temperature matched the octopus' provenance temperature (24 or 30 °C). The location of the organisms and the temperature of each segment were recorded every 10 min for 120 min. Twelve repetitions were performed for each set of experimental conditions. A control experiment was performed to evaluate the distribution of octopuses in the gradient when a homogenous temperature of 24 or 30 °C was maintained. The control evaluation was repeated with ten octopuses from each set of experimental conditions. The thermal optimal deviation (TOD) was calculated as the difference between optimum temperature of O. maya (Topt = 23.4 °C = final preferred temperature; Noyola et al., 2013a) and the preferred temperature observed in animals exposed to the different experimental conditions (TPexp, °C) and from different thermal histories: TOD, °C = 23.4 − PTexp. 2.5. Statistical analysis A one-way analysis of variance (ANOVA) was used to evaluate the effect of thermal history on growth, oxygen consumption and thermal preference. Tests for homogeneity of variance (Levene test) and normality (Kolmogorov–Smirnov) were performed to check if the data set fulfilled the ANOVA assumptions; when the data did not meet these assumptions, differences among the groups were assessed using a Kruskal–Wallis test (for oxygen consumption). Multiple comparisons were carried out with a Student–Newman–Keuls test (SNK). A T-test was performed to evaluate the differences between the provenance temperatures and those selected by the octopuses. Differences were considered significant at P b 0.05 (Zar, 1999). 3. Results The maternal thermal history (stressed or unstressed) significantly affected the wet weight of O. maya hatchlings (Table 1; P b 0.05). The initial wet weight and growth rate of hatchlings from unstressed females was almost double than those obtained in hatchlings from stressed females (Table 1). Survival of the hatchlings was also affected by the maternal thermal history. Animals from stressed females had a lower survival than animals from unstressed females (Table 1). The SGR of the juveniles was also affected by the maternal thermal history. Animals from stressed females had a significant lower growth rate than octopuses from unstressed females. However, the Ramp did

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Table 1 Initial and final weight (g), growth rate coefficient (DGC % day−1) and survival (%) of early O. maya juveniles from stressed and unstressed females, exposed to different experimental temperatures for 45 days. Values are the mean ± SD; the number of individuals (n) is indicated in each case. Different letters means statistical differences between rows. Origin

Stressed females

Unstressed females

Stressed females

Unstressed females

Juveniles

24 °C

24 °C

Ramp: 24 to 30 °C

Ramp: 24 to 30 °C

Initial weight, g Final weight, g SGR, % day−1 n Time, days Survival, %

0.073 + 0.014a 0.18 + 0.07a 1.96 + 0.042a 24 46 75

0.14 + 0.02b 0.8 + 0.2b 3.88 + 0.11b 24 45 100

0.081 + 0.017a 0.21 + 0.063a 2.07 + 0.04a 24 46 58

0.12 + 0.013b 0.61 + 0.13b 3.62 + 0.072b 24 45 100

not affect the growth rate of juveniles with the same maternal thermal history (Table 1, P N 0.05). Routine oxygen consumption was affected by the thermal history of organisms, with lower values in animals from unstressed females and exposed to Ramp (1.71 mg O2 g− 1 h− 1) and higher in animals from stressed females maintained at 24 °C and in Ramp (mean value of 8.4 mg O2 h−1 g−1, P b 0.05; Table 2). Postprandial oxygen consumption of juveniles increased from 13 to 100% of routine oxygen consumption, depending on the thermal history and experimental treatment, with lower values in animals from stressed females and maintained in Ramp (13%), followed by animals from stressed and unstressed females and maintained at 24 °C (27%) and animals from unstressed females maintained Ramp (100%). The maximum postprandial oxygen consumption was reached 0.2–0.5 h after feeding. The maximum postprandial oxygen consumption was recorded in animals from stressed females, independently of the experimental temperatures at which juveniles were exposed (mean value of 10.1 mg O2 g−1 h−1); this value was three times higher than that showed by juveniles from unstressed females and maintained at both experimental temperatures (mean value of 3.3 mg O2 h− 1 g−1 ww) (Table 2; P b 0.05). Post-prandial oxygen consumption, calculated as the difference between routine and maximum metabolic rate, was affected by maternal history and experimental temperatures over the juveniles, with higher values for juveniles from unstressed females and lower values in juveniles from stressed females (Table 2; P b 0.05). The energy spent in respiratory metabolism (RTot) was affected by the maternal thermal history and by the experimental temperature over the juveniles, with higher values in animals from stressed females (mean value of 540 J g− 1 day− 1) and lower values in animals from unstressed females and exposed to Ramp (112 J g−1 day−1) (Table 2; P b 0.05). Energy invested in the production of biomass was only affected by the maternal thermal history of animals (P b 0.05; Table 2), with higher values in octopuses from unstressed females (76 J g−1 day−1) and lower values in juveniles from stressed females (41 J g−1 day−1);

animals from unstressed females invested 33–40% of the assimilated energy to biomass production, whereas animals from stressed females invested only 6–8% of the assimilated energy (Table 2). Hatchlings' PhPPg showed values of 2.2 J g−1 dw day−1 for animals from stressed females and − 5.09 J g−1 dw day−1 for octopuses from unstressed females. Using data of biomass production obtained for juveniles of O. maya maintained at 22 and 30 °C (Noyola et al., 2013b), the PhPPg showed a negative value of −932 J g−1 dw day−1. The preferred temperature was not affected by either the experimental temperature or the thermal history of the organisms. A mean value of 24 ± 2 °C was calculated (Fig. 1). A higher but moderate TOD value was obtained in animals from stressed females that were maintained in Ramp, and in octopuses from unstressed females in both experimental thermal conditions (mean TOD value of 0.9 °C; Fig. 2). A lower TOD value of 0.3 °C was obtained in octopuses from stressed females and maintained at 24 °C (Fig. 2). 4. Discussion Results showed that hatchlings from stressed females were not only smallest, but had a lower growth rate compared to hatchlings from unstressed females. These results provide evidence that the temperature stress during the last part of the maturation process of O. maya females has a dramatic consequence on the performance of hatchlings, with serious effects on the biomass production and survival. Although, there are no other studies that relate temperature stress during maturation to the next-generation performance, results here obtained suggest that probably yolk synthesis and other factors involved in embryos size could be affected by temperature, determining egg size, embryonic development and hatchling characteristics. To date, how temperature modulates yolk synthesis remains unclear, but it has been observed that yolk volume in cephalopods has a negative correlation with egg incubation temperature (Bouchaud, 1991; Juárez et al., 2015); these

Table 2 Effect of temperature on partial energetic balance of O. maya juveniles from stressed and unstressed females exposed to different experimental temperatures. Values as kJ day−1 g−1 dw. Mean ± SE. Different letters means statistical differences, P b 0.05. Origin

Stressed females

Unstressed females

Stressed females

Unstressed females

Juveniles

24 °C

24 °C

Ramp: 24 to 30 °C

Ramp: 24 to 30 °C

Oxygen consumption, mgO2 h−1 g−1 ww Routine Maximum post prandial Post prandial Time to reach the pike, h

9.03 + 1.4 c 11.5 + 2.4 b 2.49 + 0.07 d 0.4

2.5 + 0.40 b 3.16 + 0.10 a 0.66 + 0.09 a 0.3

7.76+ 1.13 c 8.82 + 2.77 b 1.05 + 0.09 b 0.48

1.71 + 0.04 a 3.44 + 1.90 a 1.73 + 0.08 c 0.23

Respiratory metabolism, J day−1 g−1 dw RRout RAHI RTotal Production (Pg), J day−1 g−1 dw AS = R + Pg R/As, % Pg/AS, %

580 + 90 c 3 + 0.1 d 582 + 47 c 40 + 0.8 a 622 94 6

161 + 26 b 1 + 0.1 a 162+ 18 b 78+ 2.3 b 240 67 33

496 + 72 c 1 + 0.1 c 498 + 65 c 42 + 0.8 a 540 92 8

111 + 3 a 1 + 0.1 b 112 + 13 a 73 + 1.4 b 185 60 40

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Fig. 1. Preferred temperature of O. maya juveniles from stressed and unstressed females exposed to different experimental temperatures. Values as the mean ± SD.

results may imply that temperature have a fundamental role in the regulation of yolk synthesis. Other studies should be performed to know what kind of biochemical characteristics of the yolk are modified when females are exposed to high temperatures and their consequences on the embryo and hatchling characteristics, for a better understanding of the relationship between temperature and offspring performance. Previous studies demonstrated that octopuses of different sizes have similar growth rates; in cephalopods, this is an adaptive characteristic that allows the animals to recruit a broodstock population throughout the year (Leporati et al., 2007; Briceño-Jacques et al., 2010). However, in the present study, we observed that hatchlings from stressed females had a lower growth rate than juveniles from unstressed females. Results of energetic balance indicate that animals from stressed females showed a 2.5–3.5 fold change higher in their respiratory metabolism (RTot) than those from unstressed females, suggesting that maternal thermal stress can drastically affect the physiological mechanisms of the juveniles. Strong differences were observed in RRout, suggesting that physiological unbalance observed in RTot was at a maintenance metabolism level, where animals from stressed females showed higher metabolic rate than octopuses from unstressed females. To date, we do not have data to explain what kind of physiological alteration was produced during embryo development in order to understand such anomalies, however results here obtained put in evidence that juvenile octopuses from stressed females experienced a parental effect probably induced by changes in parental germ cells; affecting the size, growth and metabolism of those juveniles. According to Badyaev and Uller (2009) these could be epigenetic effects which are result of selection pressures during adult stages with serious repercussions over offspring, showing that O. maya population is highly sensible to high temperatures. Although epigenetic effect does not imply changes in the genome, in a scenario of high temperatures within the

Fig. 2. Thermal optimal deviation (TOD, °C = final preferred temperature of O. maya [23.4 °C; Noyola et al., 2013a] — preferred temperature of experimental animals [PTexp]). Values obtained by Noyola et al. (2013a) at 30 °C for of O. maya juveniles.

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O. maya spawning zone, it is possible to predict that the next generation will have lower growth rates than the offspring from breeding adults that spawn at low temperatures. It is important to consider that those hatchlings from stressed females did not show physiological limitations against progressive temperature increments (at least until 30 °C with a Ramp of 1 °C every 5 days) indicating that, independently of the parental effects, these offspring maintained their thermal adaptations in a similar manner to the offspring from unstressed females. Based on the concept of oxygen-limiting thermal tolerance, Pörtner (2010) and Sokolova et al. (2012) proposed that, when ectotherms are exposed to a moderate stress (i.e., increment of temperature) beyond the optimal conditions (namely “Pejus range”), the costs of maintenance are increased in order to cover additional energy demands derived from cellular protection and cellular damage repair. In such circumstances, the energy available for growth is reduced. The results obtained in the present study indicate that the effects of high temperature experienced by females had an effect at a cellular level in the embryos, which provoked an increase in the basal metabolic rate in hatchlings that, in the end, affected the growth rate. There is evidence indicating that octopus embryos have limited mechanisms to protect and repair cells when exposed to temperature stress. Repolho et al. (2014) showed that O. vulgaris embryos incubated at 21 °C did not have the physiological mechanisms to compensate this high temperature (when compared with embryos maintained at 18 °C), resulting in increasing percentages of smaller premature paralarvae. These authors also observed that the metabolic costs of the transition from embryo to planktonic paralarvae significantly increased with warming, and HSP70 concentrations and glutathione S-transferase activity levels were significantly magnified from the late embryonic to paralarval stages. Despite of the presence of effective antioxidant defence mechanisms, high temperatures led to the augmentation of malondialdehyde levels, which is an indicator of cellular injury. These effects could be experienced also by O. maya embryos resulting in smaller hatchlings. One of the critical factors related to thermal tolerance of ectotherms is related to the time that the organisms need to make physiological adjustments to temperature changes. In the present study, hatchlings were maintained close to the optimum temperature (24 °C) and exposed to temperature increments of 1 °C every 5 days. Results demonstrated that, independently of the thermal history, the growth rate and oxygen consumption were not affected by this temperature increase; there were no statistical differences in each experimental group for any physiological response between the animals maintained at 24 °C and exposed to Ramp. In fact, when the plasticity of O. maya hatchlings (calculated between 24 °C and the Ramp) was compared with the plasticity calculated of O. maya juveniles maintained at 22 and 30 °C for 20 days (Noyola et al., 2013a), we observed that animals from stressed or unstressed females did not really modify their growth rate as a function of temperature, showing low values of plasticity. In octopuses maintained at constant temperatures by Noyola et al. (2013a), a negative plasticity was observed, indicating that the high and constant temperature induced a significant reduction in the growth rate. According to Pigliucci et al. (2006) and Magozzi and Calosi (2015), positive values of plasticity indicate that temperature changes promoted the activation of genetically assimilated physiological mechanisms, meaning a better condition (i.e., a higher growth rate, less time to reach reproductive maturity, etc.). If a negative plasticity is reversible, it is possible that this response is adaptive, because organisms have a mechanism to revert the negative conditions that produced the physiological impairment (i.e., when thermal stress is reverted, due to a cellular mechanism to protect or repair cells; Pörtner 2010; Sokolova et al., 2012). If plasticity is negative and not reversible, it is possible that such a response is not adaptive, because, under such conditions, the animals cannot survive any longer. This is the case of O. maya juveniles maintained at 30 °C under constant conditions, where it was observed that those animals cannot

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be maintained for more than 60 days, because after that time, they began to die. In other hand if the plasticity does not change, it means that the physiological mechanisms were not altered by environmental changes, indicating that thermal variation was genetically assimilated during an adaptive process of the species; this is the case for O. maya hatchlings exposed to a gradual temperature increase, even when maternal thermal stress was present. In this context, we can conclude that a gradual temperature increase of 1 °C every 5 days is probably imprinted into the O. maya genome, allowing the organisms to make physiological adjustments without an excessive energetic cost. This was also evident when the effect of Ramp on the preferred temperature of the juveniles with different maternal thermal histories was evaluated. Results demonstrate that the Ramp did not modify the temperature preference of the animals when placed within a thermal gradient. In fact, a TOD lower than 1 °C was observed in all experimental animals, indicating that octopuses maintained at a constant temperature of 24 °C or exposed to a Ramp preferred the theoretical optimum temperature. In contrast, animals acclimated for 20 days at 30 °C (Noyola et al., 2013a) had a TOD of 3.5 °C, indicating that a constant temperature of 30 °C induced some alterations that affected the identification of the temperature in the horizontal gradient, where the performance is maximum. This study demonstrates that females exposed for few days (25 days) at temperatures between 31 to 28 °C were affected in such magnitude that their offspring where smaller than the offspring coming from unstressed females. These results highlight the sensitivity of this species to temperature and the possible consequences of temperature increases in the continental shelf of Yucatan Peninsula. In a warming scenario O. maya could be a key species for monitoring temperature changes in the Gulf of Mexico. Analysing the size of individuals captured in fisheries may help to identify if females are experiencing temperature stress in the spawning zones, making possible an early prediction of ecological alterations in other aquatic resources of this ecosystem. Acknowledgments This study was possible thanks to financing of the PAPIIT IN 212012 programme. We would like to thank CONACYT for the scholarship granted to Oscar Juárez Valdez, studying the graduate programme at CICESE. We also thank CONACYT for funding the CB 241690 and CONACYT infrastructure I010/186/2014. We thank CONACYT for the scholarship granted to FDH, number 232 974, for being able to perform the national sabbatical stay. [SS] References André, J., Grist, E.P.M., Semmens, J.M., Pecl, G., Segawa, S., 2009. Effects of temperature on energetics and the growth pattern of benthic octopuses. J. Exp. Mar. Biol. Ecol. 374, 167–179. Angilletta, M.J., Niewiarowski, P.H., Navas, C.A., 2002. The evolution of thermal physiology in ectotherms. J. Therm. Biol. 27, 249–268. Badyaev, A.V., Uller, T., 2009. Parental effects in ecology and evolution: mechanisms, processes and implications Philos. Trans. R. Soc. B. 364, 1169–1177. Beamish, F.W.H., Trippel, E.A., 1990. Heat Increment: a static dynamic dimension in bioenergetic models? Trans. Am. Fish. Soc. 119, 649–661. Beitinger, T.L., Fitzpatrick, L.C., 1979. Physiological and ecological correlates of preferred temperature in fish. Am. Zool. 19, 319–330. Brett, J.R., 1971. Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am. Zool. 11, 99–113. Briceño-Jacques, F., Mascaró, M., Rosas, C., 2010. GLMM-based modelling of growth in juvenile Octopus maya siblings: does growth depend on initial size? ICES J. Mar. Sci. 67, 1509–1516. Bouchaud, O., 1991. Energy consumption of the cuttlefish Sepia officinalis during embryonic development preliminary results. Bull. Mar. Sci. 49, 333–340. Centro de Ciencias de la Atmósfera, 2014. Atlas climático digital de México. Universidad Nacional Autónoma de Méixco, México (http://uniatmos.atmosfera.unam.mx/ ACDM/). Clarke, A., 1996. The influence of climate change on the distribution and evolution of organisms. In: Johnston, I.A., Benett, A.F. (Eds.), Animals and Temperatures: Phenotipic and Evolutionary Adaptations. Cambridge University Press, New York, pp. 379–408.

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