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Thermopreference, tolerance and metabolic rate of early stages juvenile Octopus maya acclimated to different temperatures
Journal of Thermal Biology 38 (2013) 14–19
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Thermopreference, tolerance and metabolic rate of early stages juvenile Octopus maya acclimated to different temperatures Javier Noyola a, Claudia Caamal-Monsreal b, Fernando Dı´az c,n, Denisse Re c, Adolfo Sa´nchez b, Carlos Rosas b a
´noma de Me ´xico, Circuito exterior Cd. Universitaria, Mexico 04510 Departamento de Biologı´a, Facultad de Ciencias, Universidad Nacional Auto ´n, Mexico ´n, Facultad de Ciencias, Universidad Nacional Auto ´noma de Me´xico, Puerto de abrigo s/n, Sisal, Yucata Unidad Multidisciplinaria de Docencia e Investigacio c ´n Cientı´fica y de Educacio ´n Superior de Ensenada, Carretera Ensenada-Tijuana # 3918, Baja California, Ensenada Departamento de Biotecnologı´a Marina, Centro de Investigacio B.C., Mexico b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2012 Accepted 24 September 2012 Available online 29 September 2012
Thermopreference, tolerance and oxygen consumption rates of early juveniles Octopus maya (O. maya; weight range 0.38–0.78 g) were determined after acclimating the octopuses to temperatures (18, 22, 26, and 30 1C) for 20 days. The results indicated a direct relationship between preferred temperature (PT) and acclimated temperature, the PT was 23.4 1C. Critical Thermal Maxima, (CTMax; 31.8 7 1.2, 32.7 7 0.9, 34.8 7 1.4 and 36.5 7 1.0) and Critical Thermal Minima, (CTMin; 11.6 7 0.2, 12.8 7 0.6, 13.7 7 1.0, 19.00 7 0.9) increased significantly (P o 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 1C resulted in a calculated area of 210.0 1C2. The oxygen consumption rate increased significantly a ¼0.05 with increasing acclimation temperatures between 18 and 30 1C. Maximum and minimum temperature quotients (Q10) were observed between 26–30 1C and 22–26 1C 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 Me´xico. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Thermal preference Critical thermal tolerance polygon Oxygen consumption rate Early stage juveniles
1. Introduction In nature, aquatic organisms use their ability to adapt in order to persist in a particular habitat responding to changes in the environment through metabolic or behavioral adjustments (Pigliucci, 1996). These adjustments provide the organisms with a physiological plasticity, which is particularly important in ectotherms that regularly experience wide fluctuations in temperature (Buckley et al., 2001). Environmental temperature is a critical variable to all organisms but specifically to ectotherms because it has been linked to their rate of metabolic processes and ultimately to growth and fitness (Tepler et al., 2011). In a thermally heterogeneous environment, ectotherms can apply considerable behavioral control over their body temperature by actively tracking areas that are thermally favorable and/or avoiding those are not, these temperature intervals in which the organism congregates or spends time in are operationally defined
n Corresponding author at: Departamento de Biotecnologı´a Marina (CICESE), P.O. Box 430222, San Diego, CA 92143-0222, USA. Fax: þ 1 52 646 175 05 69. E-mail address: [email protected] (F. Dı´az).
0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2012.09.001
as the preferred temperature or thermal preference (Reynolds and Casterlin, 1979). The thermal preference of an individual is a species-specific response which can vary according to age, weight, food availability, season, water quality, light intensity or by density dependent factors such as competition or the presence of pathogens (Wedemeyer et al., 1999), even throughout the day (Giattina and Garton, 1982). In addition, it has been mentioned by Beitinger and Fitzpatrick (1979) and McCauley and Casselman (1981) that the temperature that a organism prefer, commonly coincide with the optimum temperature that requires to move, grow or reproduce, because it allows the organism to maximize its energy efficiency (Kelsch, 1996). In the past critical thermal methodology has been used to determine thermal tolerance in aquatic organisms (Lutterschmidt and Hutchison, 1997; Beitinger et al., 2000); the methodology is due in part to logistical and animal care concerns. Critical thermal testing requires relatively few organisms and, less equipment and provides a rapid non-lethal assessment of thermal tolerance (Fry, 1967; Beitinger et al., 2000). Bennett and Beitinger, (1997) used thermal tolerance values to build the first CTMax polygon. Attributes of thermal tolerance polygons provide important insights into the ecology of aquatic organisms, and their distributions have been used
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to identify temperatures-related to survival tactics, predict the spread of exotic species, quantify the thermal niche of endangered species, and determine optimal culture conditions as well as assess the thermal biology of organisms in habitats sensitive to global climate change (Bennett and Beitinger, 1997; Walsh et al., 1998; Das et al., 2004; Eme and Bennett, 2009). Metabolism data in aquatic organisms has been used as a tool to determine the impact that several environmental factors could have, such as the temperature, salinity or exposure to pollutants, allowing us to determine the energetic costs that this combinations have on the organism (Stern et al., 1984; Lemos et al., 2001; Altinok and Grizzle, 2003; Manush et al., 2004; Brougher et al., 2005; Frisk et al., 2012). The oxygen consumption (VO2) is intimately associated with the metabolic work and the energy flow that the organism can use for the homeostatic control mechanisms (Salvato et al., 2001; Das et al., 2005). Octopus species have a temperature range in which individuals do not exhibit any signs of stress and/or odd behavior. The ability of octopuses to respond to thermal change is dependent on a number of factors, including thermal history or acclimation temperature (Berger, 2010). According to Somero (2005), each species will exhibit different capacities for acclimation based on how close in proximity they are to their thermal tolerance limits. O. maya is an octopus species endemic to the Yucatan peninsula, with a distribution range from the Campeche Bay, in the north of the Yucatan peninsula, to Isla Mujeres (Solis, 1967). Recently, the range has expanded polewards at its northern limit to Ciudad del Carmen, Campeche (Solis, 1997). O. maya is one of the most important commercially exploited species in Mexican fisheries. During the last several decades, this species has been studied from a variety of perspectives, including general physiology, embryonic development, feeding physiology, growth, gonad development, amino acid mobilization and growth and culture of juveniles in outdoor tanks (Segawa and Hanlon, 1988; CazaresSimental, 2006; Caamal-Monsreal, 2006; Aguila et al., 2007; Domingues et al., 2007; Rosas et al., 2007, 2008; Nepita-Villanueva and Defeo, 2001; Avila-Poveda et al., 2009; George-Zamora et al., ˜o et al., 2010 Domingues et al., 2012). Despite the great 2011; Bricen number of studies on this species, none, to date, has focused on thermal physiology. This study is the first to evaluate the effect of different acclimation temperatures on thermal preference, by including a description of the thermal stress response, use of a thermal tolerance polygon and evaluation of respiratory metabolism in O. maya early juveniles.
2. Materials and methods The experimental organisms were 260 early juveniles of red octopus O. maya with a wet weight range of 0.38–0.78 g; they were obtained from a brood stock in the maturation area Unidad Multidisciplinaria de Docencia e Investigacio´n, Facultad de Ciencias, UNAM, Sisal, Yucata´n, Me´xico. All octopuses used were weighed on a digital semi-analytical balance (OHAUS Scout SC2020, 70.01 g) and were individually to placed in a numbered PVC refuge. The reservoirs were 56 L and were connected to a recirculation system with constant conditions of a temperature of 25 1C, a salinity of 35.0% and dissolved oxygen of 6.70 mg L 1. Once the octopus reached an age of 30 days the acclimation period began at temperatures of 18, 22, 26 and 30 71 1C. Briefly each O. maya early juvenile was placed in a plastic container (500 mL). The containers had two windows covered with plastic mesh (5 mm) on each side and was placed into the recirculatory seawater system (32% O2 higher than 5 mg L 1; pH 48); a clean Melongena corona bispinosa shell was placed in each container to provide refuge. To maintain the sea water at 18 71 1C we used a
15
Prime Chiller Model 268. To maintain the water at 22 71 1C and 2671.5 1C an immersion heater of 300 W was used. The temperature of 3071 1C was maintained using a titanium immersion heater Clepco of 1800 W. During the experimental period the animals were fed twice a day with a shrimp–squid paste (30–70%) bounded with gelatin ad libitum and the food which was not consumed was removed daily (Rosas et al., 2008). The acclimation period totaled 20 days. The thermal preference of each octopus was determined by the acute method, described by Reynolds and Casterlin (1979) in which a horizontal gradient was used as described by Dı´az et al. (2006). The apparatus consisted of a PVC pipe 400 cm long and 20 cm in diameter, with 20 virtual segments of 20 cm each. The depth of the water column was 9 cm, and a gradient was formed by placing a 1000 W heater at one end, while at the other, extreme cold water was cooling in a chiller. The gradient had a temperature range of 9–35 1C. In each virtual segment, a tube diffuser was placed along to the gradient keeping a very gently aeration to maintain a concentration of dissolved oxygen from 5 to 9 mg O2 L 1, and avoid stratification in the water column. Temperature was measured in each virtual segment with an infrared digital thermometer (Steren model HER-425). Juveniles of octopuses were not fed 24 h before testing to avoid interference from their diet (Nelson et al., 1985; Beamish and Trippel, 1990). At the end of the acclimation period octopuses were selected from each acclimation temperature. Inside the formed gradient, five organisms were introduced at the virtual segment which contained the acclimation temperature and previous early juveniles. The location of the organisms and the temperature of each segment were recorded every 10 min, for a total of 120 min. We performed four repetitions for each experimental condition. The final preferendum was determined graphically by the intersection of the preferred temperatures by the organisms from each temperature acclimation and with the equality line. The system used to determine the endpoint for CTMax and CTMin in early juveniles of O. maya was a 40 L aquarium used as a thermoregulated bath. Within this bath, four experimental chambers of 350 mL cylindrical shape were placed with a 1000 W immersion heater attached to an aeration stone to maintain a uniform temperature. To determined CTMin, this bath was conditioned as a recirculation systems connected to an Isotemp Refrigerated Circulator Model 900 (Fisher Scientific). Each chamber contained a thermometer for measuring temperature and an aeration system to avoid stratification in water column. Determinations of CTMax and CTMin were performed between 9:00 and 14:00 h. The heating and cooling rate was 1 1C min 1 (Lutterschmidt and Hutchison, 1997). Visual monitoring was performed to describe the behavioral stress responses shown by red octopuses exposed increases and decreases in temperature. When the early juveniles reached this point they were returned to their acclimation temperature. The organisms were used only once and the data from the animals that did not recover after 96 h (3% to 5%) after returning to their acclimation temperature were discarded from statistical analysis. A thermal tolerance polygon was constructed from the CTMax and CTMin values using a modified version of the methods described by Bennett and Beitinger, (1997). Oxygen consumption (VO2) was measured using a continuous flow respirometer comprised of a respirometric chamber connected to a recirculating system (Rosas et al., 2008). Fifteen organisms from each acclimation temperature (18, 22, 26, and 30 71 1C) were placed in 90 mL chambers with an approximate flow rate of 0.1 L min 1. All animals were allowed to acclimate to the chambers for 1–1.5 h before measurements were made. Octopuses were offered a Melongena corona bispinosa shell as a refuge. A chamber without any octopus but containing a shell was
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used as a control. Every minute measurements of dissolved oxygen (DO) were recorded for each chamber (input and output) with oxygen sensors attached to flow-cells connected by optical fiber to an Oxy 10 mini-amplifier (PreSens&, Germany). The sensors were calibrated at each experimental temperature with saturated seawater 100% (DO) and with a 5% sodium sulphate solution (0% DO). The oxygen consumption (VO2) of early juveniles exposed to different acclimation temperatures was determined using the difference between the oxygen concentration at input and output of each experimental chamber, and was corrected by the time and flow of the water, expressed as mg O2 kg 1 h 1. Temperature quotients, Q10, were calculated to assess the effect of acclimation on oxygen consumption rate (OCR) using Eq. (1) (Schmidt-Nielsen, 1997) where R2 and R1 are the OCRs at temperatures T2 and T1, respectively. Q 10 ¼
Rate2 Rate1
ð10=Temp2 Temp1 Þ ð1Þ
A Kruskall–Wallis test was used to examine differences in the preferred temperature between repetitions for each acclimation temperatures when was using the acute methodology. Once this was confirmed, we pooled the data of preferred temperature of juveniles and used a one-way analysis of variance (ANOVA) by ranks (Kruskall–Wallis test). The one-way (ANOVA) was used previously as a determination of normality (Shapiro–Wilk test)
and homoscedasticity (Bartlett test) of the data, as well as to examine the effect of acclimation temperature on the thermal tolerance and oxygen consumption of the early juveniles of red octopus. Sigma Stat version 3.1. was used for statistical analysis.
3. Results The preferred temperature of O. maya was significantly affected by the acclimation temperature obtained a direct relationship (Po0.05); the preferred temperature was increased in the octopuses acclimated to 18, 22 and 30 1C and was observed a plateau on the preferred temperature in the organisms acclimated at 22 to 26 1C. The median that intersected the acute method equality line resulted in a final preferendum of 23.4 1C (Fig. 1). The CTMax and CTMin of O. maya were significantly affected as increasing acclimation temperatures (Po0.05) (Table 1). When early juveniles were exposed to rising thermal stress and experienced ink release, they were immediately returned to the baseline acclimation temperature which result in 95% survival after 96 h. Those octopuses that were exposed to decreasing thermal stress and that experienced tentacles curled, globular mantle, ink release, and chromatophore changes, all of them maintained a 97% survival rate. The scope for thermal tolerance for early juveniles was between 17.5 and 21.1 1C. The thermal tolerance polygon delimited by the CTMin and CTMax for the each acclimation temperature exposed to O. maya early juveniles had an area of 210.0 1C2 (Fig. 2). The rate of oxygen consumption increased significantly (Po 0.05), as the acclimation temperature increased from 18 to 30 1C and reached a maximum of 90.5 mg O2 kg 1 h 1w.w. (Fig. 3). Maximum and minimum temperature quotients (Q10) were observed between 26–30 1C and 22–26 1C as 3.03 and 1.71, respectively.
4. Discussion
Fig. 1. Preferred temperature of early juveniles of O. maya acclimated to different temperatures. Median 7 95% confidence interval. The bars include 50% of the organism’s distribution. The 451 construction line represents the point at which the preferred and acclimation temperature are equal.
The zone of distribution of the octopus endemic species O. maya in the Yucata´n Peninsula in Me´xico is a transition site, between the Caribbean Ocean and the Gulf of Me´xico, characterized for an upwelling that reduces the temperatures on summer, maintaining a relatively low temperature, therefore O. maya niche is characterized by a temperature that fluctuates between 21 and 26 1C. (Zavala-Hidalgo et al., 2003, 2006). The preferred temperature found, 23.4 1C is inside of the thermal interval which these organisms experimented in natural conditions. According to Nichelmann (1983), at this temperature interval they are exposed to minimum thermal stress and their physiological functions are
Table 1 Critical thermal maximum (CTMax) and critical thermal minimum (CTMin) of early juvenile O. maya acclimated at four temperatures (N ¼ 128) data into brackets represent 7 confidence interval to 95% of the median. Stress response
Acclimation temperature (1C) 18.0
22.0
26.0
30.0
CTMax
Ink release
31.8 (30.6, 33.0)
32.7 (31.8, 33.6)
34.8 (33.4, 35.0)
36.5a (35.5, 37.5)
CTMin
Tentacles curled
11.6b (11.4–12.0)
12.8 (12.2–13.4)
13.7 (12.7–14.7)
19.0b (18.1–19.9)
The underline between groups indicates a similar effect of acclimation temperature (P 40.05). Ink release, tentacles curled. Median values and confidence interval (95%) in parenthesis. a b
Significant difference in CTMax early juveniles of O. maya between acclimation temperatures (Po 0.05). Significant difference in CTMin early juveniles of O. maya between acclimation temperatures (Po 0.05).
a
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Fig. 3. Oxygen consumption rate in early juveniles of O. maya acclimated to four temperatures. Median 7 95% confidence interval.
Fig. 2. Thermal tolerance polygon of early juveniles of O. maya acclimated to different temperatures.
optimized, which is reflected in maximum growth. The amplitude of this temperature zone has important ecological and aquacultural implications (Huey and Stevenson, 1979). The plateau obtained from preferred temperature between 22 and 26 1C probably is the adaptative responses that reduce the impact of temporal and spatial variation in environmental temperatures on body temperature that allows of this specie maintains a physiologically stable state. Consequently, the cultivation of O. maya in the southeastern zone of Me´xico can be carried out with success in regions where the temperature of the water is closest to the preferred temperature. Although the CTMax and CTMin may occur at different temperatures in different species, the behavioral response is the same across of diverse taxa (Lutterschmidt and Hutchison, 1997). For this reason, CTMax and CTMin are an excellent index for evaluating the thermal requirements and physiology of O. maya. As the temperature increases during the CTMax test, organisms usually display a sequence of responses such as stable (active swimming, coordinated chromatophore flashes and arms movements) globular mantle
(increased the volume mantle), curled tentacles (slower swimming), erect mantle (pinched shape), spasm and suddenly contraction mantle and massive expulsion of ink (chromatophore flashes uncoordinated and inactive). In O. huttoni paralarvae Higgins et al. (2012) described similar responses and terms; when increasing temperature namely as healthy, twitch (the mantle shape changed from redounded at pinched similarly to erect mantle described for O. maya), spasms, and rigor. As the temperature decreases during the CTMin test, organisms usually display a sequence of responses such as stable (active swimming, chromatophore flashes coordinated and arms movements), globular mantle (volume mantle increased), tentacles curled, (twisting arms from the tips to the mantle base, progressing slower swimming until total immobility). Therefore we considered the end point for CTMax and CTMin in early juveniles of O. maya as ink release due to the mainly contraction mantle and tentacles curled. According to White (1983) and Beitinger et al. (2000), this points represented the pre-death thermal point due these responses precede heat coma and death, at which locomotory responses become disorganized due to neuromuscular blockade and presynaptic failure, and octopus loses the ability to escape the conditions which may ultimately lead to his death. Valencia (2006) reported the same behavioral responses in O. bocki that were used as primary defense mechanisms for protection from predators. Alternatively sudden ink release in early juveniles may be due to spasmodic contraction of the mantle and the muscles around the gland as a result from thermal stress rather than a response as an apparent defensive tactic to avoid a predator (Bush and Robison, 2007). The scope for thermal tolerance reported in postlarvae and juveniles of M. rosenbergii by Dı´az-Herrera et al. (1998) had values of 24.8–27.3 1C; in Prochilodus scrofa Barrionuevo and Fernandes (1995) obtained a thermal range of 26.7–28.2 1C; and for M. acanthurus Dı´az et al. (2002) obtained values between 22.9 and 23.6 1C. The scope for thermal tolerance for O. maya (17.5 and 21.1 1C) was higher than that obtained for M. rosenbergii, Prochilodus scrofa and M. acanthurus which indicate that these species have the capacity for enduring marked seasonal thermal fluctuations. The amplitude of the scope for the acclimation temperature reveals the degree of thermal adaptation of the aquatic species that can be correlated with the thermal stability of their habitat (Brett, 1970). The area of the thermal tolerance polygon obtained for O. maya was slightly lower than that reported in Manush et al. (2004) in
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freshwater prawn Macrobrachium rosenbergii in which the obtained thermal tolerance polygon had an area of 255.0 1C2; for Indian carp Labeo rohita Chatterjee et al. (2004) reported an area of the polygon of 275.5 1C2. The CTM temperature polygon reflects a thermal tolerance strategy suited to the thermal habitat of early juveniles. Additionally attributes of the thermal tolerance polygon provide important insights into aquatic organism’s ecology and distribution, and have been used to identify temperature-related survival tactics, quantify the thermal niche and determine optimal culture conditions. Overall the polygon area provides a convenient and useful comparative index of eurythermality in species such as freshwater prawn, Indian carp and O. maya which show an intermediate degree of eurythermality. The zone of distribution of the octopus in the Yucata´n Peninsula in Me´xico is a transition site the characterized for an upwelling, which reduces the temperatures on summer, maintaining a relatively low temperature which fluctuates between 21 and 26 1C. (Zavala-Hidalgo et al.,2003; Zavala-Hidalgo et al., 2006). Regarding the routine metabolism of early juveniles of O. maya, we found that as the acclimation temperature increased, the oxygen consumption also increased. Similar results were obtained in different species of squids and octopuses in which oxygen consumption increases continuously with increased temperature (Borer and Lane, 1971; O’Dor, 1982; DeMont and O’Dor, 1984; Segawa, 1995; Segawa and Nomoto, 2002; Katsanevakis et al., 2005; Higgins et al., 2012). The temperature coefficient (Q10) calculated for several species of squid and octopus were 2.18 for Octopus briareus between 20 and 30 1C, 2.7 for Loligo opalescens between 10 and 15 1C, 5.6 for Illex illecebrosus, 8.3–18.2 1C, 1.44–4.47 for different body weight class of Sepioteuthis lessoniana, 10–30 1C, 0.89 for Octopus ocellatus, 20–25 1C, 2.4 for Octopus vulgaris, 13–28 1C, 1.68–1.31; and for older larvae of O. huttoni, 10–25 1C (Borer and Lane, 1971; O’Dor, 1982; Demont and O’Dor, 1984; Segawa, 1995; Segawa and Nomoto, 2002; Katsanevakis et al., 2005; Higgins et al., 2012). In early juveniles of O. maya we obtained the lowest Q10 values (1.71) in the range of 22–26 1C, indicating that within this temperature range, organisms had better adapted to maintain homeostasis. (Dent and Lutterschmidt, 2003; Chatterjee et al., 2004; Gonzalez et al., 2010). Studies by Kita et al. (1996), Chatterjee et al. (2004), Das et al. (2004, 2005) and Debnath et al. (2006) suggest that the point where the Q10 is lowest compared to the acclimation temperatures, corresponds to the optimum temperature for growth. This is due to, the decrease in the Q10 which suggest that metabolism was reduced and that more energy was available for growth processes. The interval that coincided with the thermal preferendum of the early juveniles of O. maya (23.4 1C) was reported in this work. The metabolic rate of octopuses can be indirectly measured by the oxygen consumption rate; furthermore the optimum temperature for growth can be estimated through the determination of the Q10. The observation that the optimum temperature coincides with the temperature range at which early juveniles of O. maya had a smaller Q10 value, can be explained by the fact that molluscs have enzymatic and physiological systems that work better when they are close to their optimal temperature (Vernberg, 1983). The results of this study are vital in determining the suitability and survival in different geographic areas for the culture of octopus species, the environmental requirements for keeping them in captivity and the understanding of their distribution ranges. Finally these results are functional in better understanding the effects of global climate change for this species.
Acknowledgements We thank Jose M. Dominguez and Francisco Javier Ponce from the Drawing Department of CICESE for preparing the figures.
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Reynolds, W.W., Casterlin, M.E., 1979. Behavioral thermoregulation and the final preferendum paradigm. Am. Zool. 19, 211–224. Rosas, C., Cuzon, G., Pascual, C., Gaxiola, G., Chay, D., Lopez, N., Maldonado, T., Domingues, P.M., 2007. Energy balance of Octopus maya fed crab or an artificial diet. Mar. Biol. 152, 371–381. Rosas, C., Tut, J., Baeza, J., Sanchez, A., Sosa, V., Pascual, C., Arena, L., Domingues, P.M., Cuzon, G., 2008. Effect of type of binder on growth, digestibility, and energetic balance of Octopus maya. Aquaculture 275, 291–297. Salvato, B., Cuomo, V., Di Muro, R., Beltramini, M., 2001. Effects of environmental parameters on the oxygen consumption of four marine invertebrates: a comparative factorial study. Mar. Biol. 138, 659–668. Schmidt-Nielsen, K., 1997. Animal Physiology: Adaptation and Environment. Cambridge University Press, UK. Segawa, S., Hanlon, R.T., 1988. Oxygen consumption and ammonia excretion rates in Octopus maya, Loligo forbes and Llolliguncula brevis (Mollusca: Cephalopoda). Mar. Behav. Physiol. 13, 389–400. Segawa, S., 1995. Effect of temperature on oxygen consumption of juvenile oval squid Sepioteuthis lessoniana. Fish. Sci. 61, 734–746. Segawa, S., Nomoto, A., 2002. Laboratory growth, feeding, oxygen consumption and ammonia excretion of Octopus ocellatus. Bull. Mar. Sci. 71, 801–813. Solis, M., 1967. Aspectos biolo´gicos del pulpo Octopus maya Voss y Solis. Inst. Nal. Inv. Biol. Pesq. 18, 1–90. Solis, M., 1997. The Octopus maya fishery of the Yucata´n Peninsula. The fishery and market potential of octopus in California CMSC 10, 1–10. Somero, G., 2005. Linking biogeography to physiology: evolutionary and acclimatory adjustments to thermal limits. Front. Zool. 2, 1–9. Stern, S., Borut, A., Cohen, D., 1984. The effect of salinity and ion composition on oxygen consumption and nitrogen excretion of Macrobrachium rosenbergii. Comp. Biochem. Physiol. 79A, 271–274. Tepler, S., Mach, K., Denny, M., 2011. Preference versus performance: body temperature of intertidal snail Chlorostoma funebralis. Biol. Bull. 220, 107–117. Valencia, N., 2006. Differences in the diurnal and nocturnal defense mechanisms of Octopus bocki (Adams, 1941). Student Res. Papers. University of California 1–7. Vernberg, F.J., 1983. Respiratory adaptations. The Biology of Crustacea: Environmental Adaptations, vol. 8. Academic Press, New York, pp. 1–44. Walsh, S.J., Haney, D.C., Timmerman, C.M., Dorazio, R.M., 1998. Physiological tolerance of juvenile reobust redhorse Moxostoma robustum: conservation implications for an imperiled species. Environ. Biol. Fishes 51, 429–444. Wedemeyer, G.R., Meyer, F.P., Smith, L., 1999. Environmental Stress and Fish Diseases. Narendra Publishing House, Delhi, India p: 107. White, R., 1983. Effects of acute temperature change and acclimation temperature on neuromuscular function and lethality in crayfish. Physiol. Zool. 56, 174–194. Zavala-Hidalgo, J., Morey, S.L., OBrien, J.J., 2003. Seasonal circulation on the western shelf of the Gulf of Mexico using a high-resolution numerical model. J. Geophys. Res. 108, 1–19. Zavala-Hidalgo, J., Gallegos-Garcı´a, A., Martı´nez-Lo´pez, B., Morey, S.L., OBrien, J.J., 2006. Seasonal upwelling on the western and southern shelves of the Gulf of Mexico. Ocean Dyn. 56, 333–338.
Contents lists available at SciVerse ScienceDirect
Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio
Thermopreference, tolerance and metabolic rate of early stages juvenile Octopus maya acclimated to different temperatures Javier Noyola a, Claudia Caamal-Monsreal b, Fernando Dı´az c,n, Denisse Re c, Adolfo Sa´nchez b, Carlos Rosas b a
´noma de Me ´xico, Circuito exterior Cd. Universitaria, Mexico 04510 Departamento de Biologı´a, Facultad de Ciencias, Universidad Nacional Auto ´n, Mexico ´n, Facultad de Ciencias, Universidad Nacional Auto ´noma de Me´xico, Puerto de abrigo s/n, Sisal, Yucata Unidad Multidisciplinaria de Docencia e Investigacio c ´n Cientı´fica y de Educacio ´n Superior de Ensenada, Carretera Ensenada-Tijuana # 3918, Baja California, Ensenada Departamento de Biotecnologı´a Marina, Centro de Investigacio B.C., Mexico b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2012 Accepted 24 September 2012 Available online 29 September 2012
Thermopreference, tolerance and oxygen consumption rates of early juveniles Octopus maya (O. maya; weight range 0.38–0.78 g) were determined after acclimating the octopuses to temperatures (18, 22, 26, and 30 1C) for 20 days. The results indicated a direct relationship between preferred temperature (PT) and acclimated temperature, the PT was 23.4 1C. Critical Thermal Maxima, (CTMax; 31.8 7 1.2, 32.7 7 0.9, 34.8 7 1.4 and 36.5 7 1.0) and Critical Thermal Minima, (CTMin; 11.6 7 0.2, 12.8 7 0.6, 13.7 7 1.0, 19.00 7 0.9) increased significantly (P o 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 1C resulted in a calculated area of 210.0 1C2. The oxygen consumption rate increased significantly a ¼0.05 with increasing acclimation temperatures between 18 and 30 1C. Maximum and minimum temperature quotients (Q10) were observed between 26–30 1C and 22–26 1C 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 Me´xico. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Thermal preference Critical thermal tolerance polygon Oxygen consumption rate Early stage juveniles
1. Introduction In nature, aquatic organisms use their ability to adapt in order to persist in a particular habitat responding to changes in the environment through metabolic or behavioral adjustments (Pigliucci, 1996). These adjustments provide the organisms with a physiological plasticity, which is particularly important in ectotherms that regularly experience wide fluctuations in temperature (Buckley et al., 2001). Environmental temperature is a critical variable to all organisms but specifically to ectotherms because it has been linked to their rate of metabolic processes and ultimately to growth and fitness (Tepler et al., 2011). In a thermally heterogeneous environment, ectotherms can apply considerable behavioral control over their body temperature by actively tracking areas that are thermally favorable and/or avoiding those are not, these temperature intervals in which the organism congregates or spends time in are operationally defined
n Corresponding author at: Departamento de Biotecnologı´a Marina (CICESE), P.O. Box 430222, San Diego, CA 92143-0222, USA. Fax: þ 1 52 646 175 05 69. E-mail address: [email protected] (F. Dı´az).
0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2012.09.001
as the preferred temperature or thermal preference (Reynolds and Casterlin, 1979). The thermal preference of an individual is a species-specific response which can vary according to age, weight, food availability, season, water quality, light intensity or by density dependent factors such as competition or the presence of pathogens (Wedemeyer et al., 1999), even throughout the day (Giattina and Garton, 1982). In addition, it has been mentioned by Beitinger and Fitzpatrick (1979) and McCauley and Casselman (1981) that the temperature that a organism prefer, commonly coincide with the optimum temperature that requires to move, grow or reproduce, because it allows the organism to maximize its energy efficiency (Kelsch, 1996). In the past critical thermal methodology has been used to determine thermal tolerance in aquatic organisms (Lutterschmidt and Hutchison, 1997; Beitinger et al., 2000); the methodology is due in part to logistical and animal care concerns. Critical thermal testing requires relatively few organisms and, less equipment and provides a rapid non-lethal assessment of thermal tolerance (Fry, 1967; Beitinger et al., 2000). Bennett and Beitinger, (1997) used thermal tolerance values to build the first CTMax polygon. Attributes of thermal tolerance polygons provide important insights into the ecology of aquatic organisms, and their distributions have been used
J. Noyola et al. / Journal of Thermal Biology 38 (2013) 14–19
to identify temperatures-related to survival tactics, predict the spread of exotic species, quantify the thermal niche of endangered species, and determine optimal culture conditions as well as assess the thermal biology of organisms in habitats sensitive to global climate change (Bennett and Beitinger, 1997; Walsh et al., 1998; Das et al., 2004; Eme and Bennett, 2009). Metabolism data in aquatic organisms has been used as a tool to determine the impact that several environmental factors could have, such as the temperature, salinity or exposure to pollutants, allowing us to determine the energetic costs that this combinations have on the organism (Stern et al., 1984; Lemos et al., 2001; Altinok and Grizzle, 2003; Manush et al., 2004; Brougher et al., 2005; Frisk et al., 2012). The oxygen consumption (VO2) is intimately associated with the metabolic work and the energy flow that the organism can use for the homeostatic control mechanisms (Salvato et al., 2001; Das et al., 2005). Octopus species have a temperature range in which individuals do not exhibit any signs of stress and/or odd behavior. The ability of octopuses to respond to thermal change is dependent on a number of factors, including thermal history or acclimation temperature (Berger, 2010). According to Somero (2005), each species will exhibit different capacities for acclimation based on how close in proximity they are to their thermal tolerance limits. O. maya is an octopus species endemic to the Yucatan peninsula, with a distribution range from the Campeche Bay, in the north of the Yucatan peninsula, to Isla Mujeres (Solis, 1967). Recently, the range has expanded polewards at its northern limit to Ciudad del Carmen, Campeche (Solis, 1997). O. maya is one of the most important commercially exploited species in Mexican fisheries. During the last several decades, this species has been studied from a variety of perspectives, including general physiology, embryonic development, feeding physiology, growth, gonad development, amino acid mobilization and growth and culture of juveniles in outdoor tanks (Segawa and Hanlon, 1988; CazaresSimental, 2006; Caamal-Monsreal, 2006; Aguila et al., 2007; Domingues et al., 2007; Rosas et al., 2007, 2008; Nepita-Villanueva and Defeo, 2001; Avila-Poveda et al., 2009; George-Zamora et al., ˜o et al., 2010 Domingues et al., 2012). Despite the great 2011; Bricen number of studies on this species, none, to date, has focused on thermal physiology. This study is the first to evaluate the effect of different acclimation temperatures on thermal preference, by including a description of the thermal stress response, use of a thermal tolerance polygon and evaluation of respiratory metabolism in O. maya early juveniles.
2. Materials and methods The experimental organisms were 260 early juveniles of red octopus O. maya with a wet weight range of 0.38–0.78 g; they were obtained from a brood stock in the maturation area Unidad Multidisciplinaria de Docencia e Investigacio´n, Facultad de Ciencias, UNAM, Sisal, Yucata´n, Me´xico. All octopuses used were weighed on a digital semi-analytical balance (OHAUS Scout SC2020, 70.01 g) and were individually to placed in a numbered PVC refuge. The reservoirs were 56 L and were connected to a recirculation system with constant conditions of a temperature of 25 1C, a salinity of 35.0% and dissolved oxygen of 6.70 mg L 1. Once the octopus reached an age of 30 days the acclimation period began at temperatures of 18, 22, 26 and 30 71 1C. Briefly each O. maya early juvenile was placed in a plastic container (500 mL). The containers had two windows covered with plastic mesh (5 mm) on each side and was placed into the recirculatory seawater system (32% O2 higher than 5 mg L 1; pH 48); a clean Melongena corona bispinosa shell was placed in each container to provide refuge. To maintain the sea water at 18 71 1C we used a
15
Prime Chiller Model 268. To maintain the water at 22 71 1C and 2671.5 1C an immersion heater of 300 W was used. The temperature of 3071 1C was maintained using a titanium immersion heater Clepco of 1800 W. During the experimental period the animals were fed twice a day with a shrimp–squid paste (30–70%) bounded with gelatin ad libitum and the food which was not consumed was removed daily (Rosas et al., 2008). The acclimation period totaled 20 days. The thermal preference of each octopus was determined by the acute method, described by Reynolds and Casterlin (1979) in which a horizontal gradient was used as described by Dı´az et al. (2006). The apparatus consisted of a PVC pipe 400 cm long and 20 cm in diameter, with 20 virtual segments of 20 cm each. The depth of the water column was 9 cm, and a gradient was formed by placing a 1000 W heater at one end, while at the other, extreme cold water was cooling in a chiller. The gradient had a temperature range of 9–35 1C. In each virtual segment, a tube diffuser was placed along to the gradient keeping a very gently aeration to maintain a concentration of dissolved oxygen from 5 to 9 mg O2 L 1, and avoid stratification in the water column. Temperature was measured in each virtual segment with an infrared digital thermometer (Steren model HER-425). Juveniles of octopuses were not fed 24 h before testing to avoid interference from their diet (Nelson et al., 1985; Beamish and Trippel, 1990). At the end of the acclimation period octopuses were selected from each acclimation temperature. Inside the formed gradient, five organisms were introduced at the virtual segment which contained the acclimation temperature and previous early juveniles. The location of the organisms and the temperature of each segment were recorded every 10 min, for a total of 120 min. We performed four repetitions for each experimental condition. The final preferendum was determined graphically by the intersection of the preferred temperatures by the organisms from each temperature acclimation and with the equality line. The system used to determine the endpoint for CTMax and CTMin in early juveniles of O. maya was a 40 L aquarium used as a thermoregulated bath. Within this bath, four experimental chambers of 350 mL cylindrical shape were placed with a 1000 W immersion heater attached to an aeration stone to maintain a uniform temperature. To determined CTMin, this bath was conditioned as a recirculation systems connected to an Isotemp Refrigerated Circulator Model 900 (Fisher Scientific). Each chamber contained a thermometer for measuring temperature and an aeration system to avoid stratification in water column. Determinations of CTMax and CTMin were performed between 9:00 and 14:00 h. The heating and cooling rate was 1 1C min 1 (Lutterschmidt and Hutchison, 1997). Visual monitoring was performed to describe the behavioral stress responses shown by red octopuses exposed increases and decreases in temperature. When the early juveniles reached this point they were returned to their acclimation temperature. The organisms were used only once and the data from the animals that did not recover after 96 h (3% to 5%) after returning to their acclimation temperature were discarded from statistical analysis. A thermal tolerance polygon was constructed from the CTMax and CTMin values using a modified version of the methods described by Bennett and Beitinger, (1997). Oxygen consumption (VO2) was measured using a continuous flow respirometer comprised of a respirometric chamber connected to a recirculating system (Rosas et al., 2008). Fifteen organisms from each acclimation temperature (18, 22, 26, and 30 71 1C) were placed in 90 mL chambers with an approximate flow rate of 0.1 L min 1. All animals were allowed to acclimate to the chambers for 1–1.5 h before measurements were made. Octopuses were offered a Melongena corona bispinosa shell as a refuge. A chamber without any octopus but containing a shell was
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used as a control. Every minute measurements of dissolved oxygen (DO) were recorded for each chamber (input and output) with oxygen sensors attached to flow-cells connected by optical fiber to an Oxy 10 mini-amplifier (PreSens&, Germany). The sensors were calibrated at each experimental temperature with saturated seawater 100% (DO) and with a 5% sodium sulphate solution (0% DO). The oxygen consumption (VO2) of early juveniles exposed to different acclimation temperatures was determined using the difference between the oxygen concentration at input and output of each experimental chamber, and was corrected by the time and flow of the water, expressed as mg O2 kg 1 h 1. Temperature quotients, Q10, were calculated to assess the effect of acclimation on oxygen consumption rate (OCR) using Eq. (1) (Schmidt-Nielsen, 1997) where R2 and R1 are the OCRs at temperatures T2 and T1, respectively. Q 10 ¼
Rate2 Rate1
ð10=Temp2 Temp1 Þ ð1Þ
A Kruskall–Wallis test was used to examine differences in the preferred temperature between repetitions for each acclimation temperatures when was using the acute methodology. Once this was confirmed, we pooled the data of preferred temperature of juveniles and used a one-way analysis of variance (ANOVA) by ranks (Kruskall–Wallis test). The one-way (ANOVA) was used previously as a determination of normality (Shapiro–Wilk test)
and homoscedasticity (Bartlett test) of the data, as well as to examine the effect of acclimation temperature on the thermal tolerance and oxygen consumption of the early juveniles of red octopus. Sigma Stat version 3.1. was used for statistical analysis.
3. Results The preferred temperature of O. maya was significantly affected by the acclimation temperature obtained a direct relationship (Po0.05); the preferred temperature was increased in the octopuses acclimated to 18, 22 and 30 1C and was observed a plateau on the preferred temperature in the organisms acclimated at 22 to 26 1C. The median that intersected the acute method equality line resulted in a final preferendum of 23.4 1C (Fig. 1). The CTMax and CTMin of O. maya were significantly affected as increasing acclimation temperatures (Po0.05) (Table 1). When early juveniles were exposed to rising thermal stress and experienced ink release, they were immediately returned to the baseline acclimation temperature which result in 95% survival after 96 h. Those octopuses that were exposed to decreasing thermal stress and that experienced tentacles curled, globular mantle, ink release, and chromatophore changes, all of them maintained a 97% survival rate. The scope for thermal tolerance for early juveniles was between 17.5 and 21.1 1C. The thermal tolerance polygon delimited by the CTMin and CTMax for the each acclimation temperature exposed to O. maya early juveniles had an area of 210.0 1C2 (Fig. 2). The rate of oxygen consumption increased significantly (Po 0.05), as the acclimation temperature increased from 18 to 30 1C and reached a maximum of 90.5 mg O2 kg 1 h 1w.w. (Fig. 3). Maximum and minimum temperature quotients (Q10) were observed between 26–30 1C and 22–26 1C as 3.03 and 1.71, respectively.
4. Discussion
Fig. 1. Preferred temperature of early juveniles of O. maya acclimated to different temperatures. Median 7 95% confidence interval. The bars include 50% of the organism’s distribution. The 451 construction line represents the point at which the preferred and acclimation temperature are equal.
The zone of distribution of the octopus endemic species O. maya in the Yucata´n Peninsula in Me´xico is a transition site, between the Caribbean Ocean and the Gulf of Me´xico, characterized for an upwelling that reduces the temperatures on summer, maintaining a relatively low temperature, therefore O. maya niche is characterized by a temperature that fluctuates between 21 and 26 1C. (Zavala-Hidalgo et al., 2003, 2006). The preferred temperature found, 23.4 1C is inside of the thermal interval which these organisms experimented in natural conditions. According to Nichelmann (1983), at this temperature interval they are exposed to minimum thermal stress and their physiological functions are
Table 1 Critical thermal maximum (CTMax) and critical thermal minimum (CTMin) of early juvenile O. maya acclimated at four temperatures (N ¼ 128) data into brackets represent 7 confidence interval to 95% of the median. Stress response
Acclimation temperature (1C) 18.0
22.0
26.0
30.0
CTMax
Ink release
31.8 (30.6, 33.0)
32.7 (31.8, 33.6)
34.8 (33.4, 35.0)
36.5a (35.5, 37.5)
CTMin
Tentacles curled
11.6b (11.4–12.0)
12.8 (12.2–13.4)
13.7 (12.7–14.7)
19.0b (18.1–19.9)
The underline between groups indicates a similar effect of acclimation temperature (P 40.05). Ink release, tentacles curled. Median values and confidence interval (95%) in parenthesis. a b
Significant difference in CTMax early juveniles of O. maya between acclimation temperatures (Po 0.05). Significant difference in CTMin early juveniles of O. maya between acclimation temperatures (Po 0.05).
a
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Fig. 3. Oxygen consumption rate in early juveniles of O. maya acclimated to four temperatures. Median 7 95% confidence interval.
Fig. 2. Thermal tolerance polygon of early juveniles of O. maya acclimated to different temperatures.
optimized, which is reflected in maximum growth. The amplitude of this temperature zone has important ecological and aquacultural implications (Huey and Stevenson, 1979). The plateau obtained from preferred temperature between 22 and 26 1C probably is the adaptative responses that reduce the impact of temporal and spatial variation in environmental temperatures on body temperature that allows of this specie maintains a physiologically stable state. Consequently, the cultivation of O. maya in the southeastern zone of Me´xico can be carried out with success in regions where the temperature of the water is closest to the preferred temperature. Although the CTMax and CTMin may occur at different temperatures in different species, the behavioral response is the same across of diverse taxa (Lutterschmidt and Hutchison, 1997). For this reason, CTMax and CTMin are an excellent index for evaluating the thermal requirements and physiology of O. maya. As the temperature increases during the CTMax test, organisms usually display a sequence of responses such as stable (active swimming, coordinated chromatophore flashes and arms movements) globular mantle
(increased the volume mantle), curled tentacles (slower swimming), erect mantle (pinched shape), spasm and suddenly contraction mantle and massive expulsion of ink (chromatophore flashes uncoordinated and inactive). In O. huttoni paralarvae Higgins et al. (2012) described similar responses and terms; when increasing temperature namely as healthy, twitch (the mantle shape changed from redounded at pinched similarly to erect mantle described for O. maya), spasms, and rigor. As the temperature decreases during the CTMin test, organisms usually display a sequence of responses such as stable (active swimming, chromatophore flashes coordinated and arms movements), globular mantle (volume mantle increased), tentacles curled, (twisting arms from the tips to the mantle base, progressing slower swimming until total immobility). Therefore we considered the end point for CTMax and CTMin in early juveniles of O. maya as ink release due to the mainly contraction mantle and tentacles curled. According to White (1983) and Beitinger et al. (2000), this points represented the pre-death thermal point due these responses precede heat coma and death, at which locomotory responses become disorganized due to neuromuscular blockade and presynaptic failure, and octopus loses the ability to escape the conditions which may ultimately lead to his death. Valencia (2006) reported the same behavioral responses in O. bocki that were used as primary defense mechanisms for protection from predators. Alternatively sudden ink release in early juveniles may be due to spasmodic contraction of the mantle and the muscles around the gland as a result from thermal stress rather than a response as an apparent defensive tactic to avoid a predator (Bush and Robison, 2007). The scope for thermal tolerance reported in postlarvae and juveniles of M. rosenbergii by Dı´az-Herrera et al. (1998) had values of 24.8–27.3 1C; in Prochilodus scrofa Barrionuevo and Fernandes (1995) obtained a thermal range of 26.7–28.2 1C; and for M. acanthurus Dı´az et al. (2002) obtained values between 22.9 and 23.6 1C. The scope for thermal tolerance for O. maya (17.5 and 21.1 1C) was higher than that obtained for M. rosenbergii, Prochilodus scrofa and M. acanthurus which indicate that these species have the capacity for enduring marked seasonal thermal fluctuations. The amplitude of the scope for the acclimation temperature reveals the degree of thermal adaptation of the aquatic species that can be correlated with the thermal stability of their habitat (Brett, 1970). The area of the thermal tolerance polygon obtained for O. maya was slightly lower than that reported in Manush et al. (2004) in
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freshwater prawn Macrobrachium rosenbergii in which the obtained thermal tolerance polygon had an area of 255.0 1C2; for Indian carp Labeo rohita Chatterjee et al. (2004) reported an area of the polygon of 275.5 1C2. The CTM temperature polygon reflects a thermal tolerance strategy suited to the thermal habitat of early juveniles. Additionally attributes of the thermal tolerance polygon provide important insights into aquatic organism’s ecology and distribution, and have been used to identify temperature-related survival tactics, quantify the thermal niche and determine optimal culture conditions. Overall the polygon area provides a convenient and useful comparative index of eurythermality in species such as freshwater prawn, Indian carp and O. maya which show an intermediate degree of eurythermality. The zone of distribution of the octopus in the Yucata´n Peninsula in Me´xico is a transition site the characterized for an upwelling, which reduces the temperatures on summer, maintaining a relatively low temperature which fluctuates between 21 and 26 1C. (Zavala-Hidalgo et al.,2003; Zavala-Hidalgo et al., 2006). Regarding the routine metabolism of early juveniles of O. maya, we found that as the acclimation temperature increased, the oxygen consumption also increased. Similar results were obtained in different species of squids and octopuses in which oxygen consumption increases continuously with increased temperature (Borer and Lane, 1971; O’Dor, 1982; DeMont and O’Dor, 1984; Segawa, 1995; Segawa and Nomoto, 2002; Katsanevakis et al., 2005; Higgins et al., 2012). The temperature coefficient (Q10) calculated for several species of squid and octopus were 2.18 for Octopus briareus between 20 and 30 1C, 2.7 for Loligo opalescens between 10 and 15 1C, 5.6 for Illex illecebrosus, 8.3–18.2 1C, 1.44–4.47 for different body weight class of Sepioteuthis lessoniana, 10–30 1C, 0.89 for Octopus ocellatus, 20–25 1C, 2.4 for Octopus vulgaris, 13–28 1C, 1.68–1.31; and for older larvae of O. huttoni, 10–25 1C (Borer and Lane, 1971; O’Dor, 1982; Demont and O’Dor, 1984; Segawa, 1995; Segawa and Nomoto, 2002; Katsanevakis et al., 2005; Higgins et al., 2012). In early juveniles of O. maya we obtained the lowest Q10 values (1.71) in the range of 22–26 1C, indicating that within this temperature range, organisms had better adapted to maintain homeostasis. (Dent and Lutterschmidt, 2003; Chatterjee et al., 2004; Gonzalez et al., 2010). Studies by Kita et al. (1996), Chatterjee et al. (2004), Das et al. (2004, 2005) and Debnath et al. (2006) suggest that the point where the Q10 is lowest compared to the acclimation temperatures, corresponds to the optimum temperature for growth. This is due to, the decrease in the Q10 which suggest that metabolism was reduced and that more energy was available for growth processes. The interval that coincided with the thermal preferendum of the early juveniles of O. maya (23.4 1C) was reported in this work. The metabolic rate of octopuses can be indirectly measured by the oxygen consumption rate; furthermore the optimum temperature for growth can be estimated through the determination of the Q10. The observation that the optimum temperature coincides with the temperature range at which early juveniles of O. maya had a smaller Q10 value, can be explained by the fact that molluscs have enzymatic and physiological systems that work better when they are close to their optimal temperature (Vernberg, 1983). The results of this study are vital in determining the suitability and survival in different geographic areas for the culture of octopus species, the environmental requirements for keeping them in captivity and the understanding of their distribution ranges. Finally these results are functional in better understanding the effects of global climate change for this species.
Acknowledgements We thank Jose M. Dominguez and Francisco Javier Ponce from the Drawing Department of CICESE for preparing the figures.
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