Effect of Temperature Stress on the Survival of Juvenile Chinese Mitten Crab (Eriocheir Sinensis)

Iranian Journal of Fisheries Sciences 18(4) 763-774 2019 DOI: 10.22092/ijfs.2019.118594 Effect of temperature stress on the survival of juvenile Chinese mitten crab (Eriocheir sinensis)

Peng J.1,2; Zhao Y.L.1,2*; Xu Z.G. 2,3*; Liu B.Q.2; Duan C.C.1,2; Tang Y.C.1

Received: January 2017 Accepted: May 2017

Abstract Eriocheir sinensis, which is an important aquaculture species, belongs to the class Crustacea. To discuss the temperature tolerance of E. sinensis, the survival rates of juvenile crabs of E. sinensis were determined in this paper using a series of temperature settings (normal temperature, 25°C, 30°C, 32°C, 34°C, 35°C, 36°C, 38°C, 40 °C). The results indicated that except the normal temperature level, mortality rate almost reached 100% at other temperatures. The time of death of all crabs at 30℃, 35℃, and 40℃ was different. All the crabs died in only 10 minutes at 40℃, while they died after 3 days and 7 days at 35 ℃ and 30℃, respectively. In addition to normal temperature conditions, minimum survival time of the juvenile crabs of E. sinensis at other temperature condition was no more than 24 h. Before the 8th day, the death rate at 30℃ and normal

temperature was different, change of turning slope for concentration of NH3-N and TN was contrary. Under normal temperature, the behavior of abdomen extension was not observed in juvenile crabs but the percentage time of abdomen extension was relatively long at 25℃. This research studied the influence of temperature stress on the survival of juvenile crabs of E. sinensis to provide information reference for the production and Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 transportation of juvenile crab of E. sinensis.

Keywords: Eriocheir sinensis, Temperature stress, Survival, Behavior response

1- Key Laboratory of Forestry Remote Sensing Based Big Data & Ecological Security for Hunan Province, Central South University of Forestry and Technology, Changsha 410004, China 2- Engineering Research Center for Internet of Animals, Changsha 410128, China 3- Hunan Urban and Rural Ecological Planning and Restoration Engineering Research Center, Hunan City University, Yiyang 413000, China *Corresponding author's Email: [email protected]; [email protected] 764 Peng et al., Effect of temperature stress on the survival of…

Introduction the survival mechanism of economic The Chinese mitten crab (Eriocheir species under extreme weather, such as sinensis) is considered to be one of the temperature, is particularly important. specific aquaculture species in China, Temperature is one of the most which belongs to Crustacea, Decapoda, important environmental factors Crapsida, Eriocheir (Pan, 2002). affecting crabs, which can affect Normally Chinese mitten crab were neuromuscular activity, respiration, cultured for two years, in the first year blood circulation and lipid metabolism it is cultured from crab larvae to button and other physiological activities (Aardt, size, and in the other year it is cultured 1993). The relationship between North to market size in ponds, reservoirs or America dungeness crab (Cancer other waters fields. So the juvenile magister) (Kondzela and Shirley, 1993; crabs of E. sinensis are also known as Sulkin and Mckeen, 1996), Red king buttony crab. Chinese mitten crabs can crab (Kamchatka cancer) in the North survive in various environments, such Pacific (Shirley and Shirley 1989; as estuarine waters, freshwater lakes Kittaka and Onoda 2002), North and ponds. In addition to China, the American blue crab (Callinectes Chinese mitten crab is also distributed sapidus) (Leffler, 1972; Fisher, 1999), in Europe and the Americas (Zou and Mud crab (Scylla serrata) (Hamasaki, Si-Fa, 2002). Chinese mitten crabs are 2003; Ruscoe et al., 2004), Distant sea widely distributed in the Yangtze River, crab (Portunus pelagicus) (Bryars and Liaohe, Oujiang and other waters in Havenhand, 2006) and temperature has China, of which Yangtze River is the been reported in a large number of most excellent quality. Due to its high literature. While, at present there is little nutritional value and market demand, research on temperature tolerance of Chinese mitten crab has increasingly Chinese mitten crab, (Bo Huang et al., Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 become a promising commercial 2001) focused on the effects of species. The aquaculture industry has temperature on the E. sinensis larval been rapidly developing in many parts growth and development. The results with Chinese mitten crab aquaculture as suggested that the survival rate a pillar industry of aquaculture (Wang increases with temperature. et al., 2016). In order to know more details on the Average water temperature in the biology of Chinese mitten crab and middle and lower Yangtze River is 31- provide references for aquaculture to 35℃ in summer and 0-4℃ in winter. ensure the sustainable development of Crab grow from early March to early Chinese mitten crab industry, the November, for up to about 240 days. juvenile crab was employed as the This temperature range is very suitable research object to study the impact of for the growth of Chinese mitten crabs high temperature stress on its survival. (Zhang, 2000). With the global climate change, extreme weather is becoming Materials and methods more and more frequent. To understand 254 juvenile crabs of E. sinensis, with Iranian Journal of Fisheries Sciences 18(4) 2019 765

an average weight of 6-10 g, were juvenile crabs of E. sinensis to captured from Dongting Lake region in temperature precisely, an experiment China, where the crab culture was with fewer intervals of temperature was common and the crab was the main designed. Glass aquaria (44 cm×28 cm economic resource. Sampling was done ×28cm) with paving pebbles at the in April, when water temperature in bottom and 24 cm of water column was Dongting Lake is 15-23 °C. Normal used. The following temperature were body color, lively and healthy tested: normal temperature, 25℃, 30℃, individuals were chosen and reared in 32℃, 34℃, 35℃, 36℃, 38℃, 40℃. freshwater lake (112.37°E ， 29.07°N) Three female crabs and three male crabs were reared in each temperature to adapt to laboratory conditions. level. Death time of every crab was 2 weeks later, 200 juvenile crabs of E. recorded for all the levels. Besides the sinensis were divided randomly into death time, behavior response to five groups (n=40 for each group, half temperature was explored. The behavior male and half female), and transferred of the juvenile crabs of E. sinensis to five water tanks (80 cm×58 cm×40 under different temperatures was cm) for rearing. The following recorded with a Panasonic video camera temperatures were tested: 25°C, 30°C, (HDC-HS900) after 5 min for adaption. 35°C, 40°C, normal temperature (<25°C) Behavioral indicators, locomotor as the control group. Weight, carapace activity, movement of mouthparts, length, carapace width and height were cleaning of antennae, antennule measured for each crab before retraction, flicking of antennae, experiment (Montu et al., 1996). percentage time of abdomen, eyestalk Pebbles, at a diameter of 2 cm, were extension movement, and percentage placed at the bottom of the tanks time of closure behavior were Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 serving as a crab refuge. The depth of distinguished (McGaw and McMahon., the water was set at 30 cm, which was 1999). The behavior number or in accordance with field culture sustained time of above behaviors were environment. 5 g food was fed at 22:00 counted from the video. Because the every day during the experiment. At the living time was different, statistic was same time, an oxygen pump worked 8 only carried out 1 min. hours every day to supply dissolved Temperature control device (Kedibo oxygen. Water temperature was WK-SM3) was used in the experient to measured every day for normal ensure the temperatures were as temperature level and dead crabs were expected. Dissolved oxygen was also recorded for all levels. At the same measured with a portable dissolved time, pH, ammonia nitrogen (NH3-N), oxygen device (Shanghai Leici JPB- total nitrogen (TN) and total 607A). pH was measured with a phosphorus (TP) were also measured portable pH device (Shanghai Leici every three days. PHS-3E). NH -N, TN, TP were checked In order to determine the threshold of 3 by standard method (Wei et al., 2008). 766 Peng et al., Effect of temperature stress on the survival of…

An independent sample test was crabs was 2.409±0.270 cm, the average employed to analyze the role of sex and carapace width of female crabs was temperature in the survival process. 2.617±0.284 cm, and the average height Temperature control study using model at withers of female crabs was behavior analysis. 1.262±0.144 cm; the average carapace length of male crabs was 2.465±0.265 Result cm, the average carapace width of male Morphology of juvenile crabs of crabs was 2.617±0.284 cm, and the Eriocheir sinensis average height at withers of male crabs The morphological indexes of all was 1.269±0.162 cm. There were no experimental crabs were counted. The significant differences in mean carapace mean body weights of the crabs were length, width and height between the measured to be 8.543±2.555 g for females and the males (p>0.05). (Table females and 9.304±2.977 g for males, 1). the difference was significant (p<0.05). The average carapace length of female

Table 1: Morphology of juvenile of Eriocheir sinensis. Carapace length(cm) Carapace width(cm) Carapace height(cm) Weight(g) Mean±SD Mean±SD Mean±SD Mean±SD Females 2.409±0.270 2.617±0.284 1.262±0.144 8.543±2.555 Males 2.465±0.265 2.628±0.291 1.269±0.162 9.304±2.977 T-test p>0.05 p>0.05 p>0.05 p<0.05* * indicates significant difference (p<0.05).

Mortality rates of the juvenile crabs of At 40℃ all crabs died in only 10 E. sinensis at different temperatures minutes, while they died in 3 days and 7 Normal temperature fluctuated between days at 35 ℃ and 30℃, respectively.

Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 20℃ ~ 25℃ during the experiental There was an obvious tendency that period and was lower than the lowest high temperature meant the crabs would temperature level, 25℃ (Fig. 1). die in a shorter time. In accordance with Combined with the control temperature the above tendency, mortality rate of level, there was a successive crab reached 92.5% under 25℃ on the temperature gradient to explore 16th day. When all the crabs almost relationship between survival and died for all control temperature levels, temperature of juvenile crabs of E. 50% of crabs in the normal temperature sinensis. With the increase of level, survived. Besides the mortality temperature, from normal temperature, rate, there was also a huge difference in to 25℃, 30℃, 35℃ and 40℃, mortality the death process. The death happened rate of crabs increased (Fig. 2). Except in such a short time that the mortality in the normal temperature level, rate suddenly rose and reached 100% mortality rate almost reached 100% for for the high temperature level, such as other temperatures. Time of death of all 30 ℃ or higher temperature. The crabs crabs at 30℃, 35℃, 40℃ was different. died gradually at temperature of 25℃ Iranian Journal of Fisheries Sciences 18(4) 2019 767

and normal temperature level. Basing sinensis. 25℃ may be the threshold on the above analysis, temperature temperature for juvenile crabs of E. played an important role in the sinensis. development of juvenile crabs of E.

Figure 1: Fluctuations of normal temperature during the experience. Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021

Figure 2: Mortality rate of juvenile of Eriocheir sinensis under different temperatures.

Survival time of the juvenile crabs of E. Maximum survival time of the juvenile sinensis at different temperatures crabs of E. sinensis at normal There was a more direct evidence to temperature, 25℃, 30℃, 32℃, 34℃, show that at higher temperature, 35℃, 36℃, 38℃, 40℃ were 555 h, 423 survival time was shorter. In addition to h, 170.50 h, 168 h, 0.21h, 75h, 36h, normal temperature condition, 0.3h, 0.1h, respectively. Mean of minimum survival time of the juvenile survival time were 394.50±130.60 h, crabs of E. sinensis at other temperature 281.44±103.41 h, 163.34±26.96 h, conditions were no more than 24 h. 84.28±91.71 h, 3.86±4.71 h, 768 Peng et al., Effect of temperature stress on the survival of…

72.05±13.18 h, 23.67±6.08 h, 0.09±0.10 would not be changed. The tolerance of h, 0.08±0.03 h, respectively at the series individuals was variable and the less of temperature gradient. Although there test-crabs led to the result. was a peak at 35℃, 36℃, the tendency

Figure 3: Survival time of juvenile of Eriocheir sinensis at different temperatures.

Change of water quality factors Combined with the mortality rate of Because crabs died in short time at different temperature levels, the 8th day temperatures of 35℃ and 40℃, only was an important node for 30℃ because change of water quality at normal all crabs died and number of dead crabs temperature, 25℃ (threshold was more than the other days. There temperature) and 30℃ are shown (Fig. was no jumping point for normal

3). The concentration of NH3-N for the temperature and 25℃. Focusing on the

Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 above temperature levels increased, change of water quality, especially the although the gradient for different key node, mechanism might be levels were variable (Fig. 4A). The explored. TP should not be the key regular pattern of concentration of TN factor to affect crab survival because

was different from NH3-N. For the first there were no signification differences four days of the experiment, the for different temperature levels. A

concentration of TN increased quickly common feature for NH3-N and TN and reached about 6 mg L-1, after which have been gotten, that the the concentration of TN fluctuated at concentrations of both at 30℃ were 0.6 mg L-1 (Fig. 4B). pH of water was higher than normal temperature and alkalescence and ranged from 7.15 to 25℃ level. After 100% death, the

7.62 (Fig. 4C). Similar to the concentration of NH3-N and TN at 30℃ concentration of NH3-N, concentration decreased. A steep increase of pH also of TP was also growing and gradient of revealed the clue, that there might be a

normal temperature, 25℃ and 30℃ was close relationship between both NH3-N similar (Fig. 4D). and TN and crab survival. The Iranian Journal of Fisheries Sciences 18(4) 2019 769

concentrations of NH3-N and TN were declined. The concentration of NH3-N not the highest nor the lowest, so there and TN at normal temperature always was no threshold value for Chinese rose, but the gradient was different. No mitten crab, but there was accumulation matter the death rate of crabs or th effect. Before the 8 day, the death rate concentrations of NH3-N and TN at at 30℃ and normal temperature were 25℃ was intergrade. Basing on the different, change of turning slopes for above analysis, change in concentration

concentrations of NH3-N and TN were of NH3-N and TN might affect survival

contrary. The concentration of NH3-N of the juvenile crabs of E. sinensis. and TN at 30℃ rose first and then Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021

Figure 4: Water quality factor changes at different temperatures.

Behavioral responses to temperature male crabs (p＞0.05). The movement of change mouth parts and flicking of antennae The E. sinensis died quickly in were the two main behaviors of juvenile conditions when temperature were over crabs under two temperature gradients. 25℃, so this paper only collects the Under different temperatures, there was statistics of behavior activities of E. no significant difference between the sinensis under normal temperature or frequency of movement of mouth parts below 25℃ (Table 2). No matter under of female and male crabs (p ＞ 0.05); normal temperature or below 25℃, there was no significant difference there were no significant differences between the frequencies of flicking of between the behaviors of female and antennae for female crabs under 770 Peng et al., Effect of temperature stress on the survival of…

different temperatures. However, the crabs and it was 41.33±9.87 seconds frequency of flicking of antennae for within one minute for male crabs. male crabs was 100.67±2.52 under Significant differences could be normal temperature and it was observed in terms of the percentage 77.33±2.08 at 25℃. The frequency of time of abdomen extension under two flicking of antennae under normal temperature conditions between female temperature was significantly higher crabs and male crabs (p＜0.05). The than that at 25℃ (p ＜ 0.01). Under frequency of locomotor activity, normal temperature, the behavior of cleaning of antennae, antennule abdomen extension was not observed in retraction and eyestalk movement was juvenile crabs but the percentage time low and the difference was not obvious of abdomen extension was relatively under two temperature gradients (p＞ long at 25℃. The percentage time of 0.05). Closure reaction was not abdomen extension was 27.67±6.81 observed during the observation. seconds within one minute for female

Table 2: Behavioral comparison between Eriocheir sinensis under different temperature.

Normal 25℃ p temperature

Female 1.00±1.00 1.67±0.58 p>0.05 Locomotor activity(n) Male 3.33±1.53 1.33±2.31 p>0.05 Female 117±11.53 103.00±20.95 p>0.05 Movement of mouth parts(n) Male 81.33±19.09 94.00±14.18 p>0.05 Female 1.33±0.58 1.33±0.58 p>0.05 Cleaning of antennae/antennules(n) Male 3.67±2.08 0.67±0.58 p>0.05 Female 2.33±0.58 1.67±1.53 p>0.05 Antennule retraction(n) Male 2.00±2.00 2.67±0.58 p>0.05 Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 Female 113±18.74 84.33±14.3 p>0.05 Flicking of antennae(s) Male 100.67±2.52 77.33±2.08 p<0.01** Female 0 27.67±6.81 p<0.05* Percentage time of abdomen extension(s) Male 0 41.33±9.87 p<0.05* Female 1.00±1.00 1.33±1.53 p>0.05 Eyestalk movement(n) Male 2.67±0.58 1.33±1.16 p>0.05 Female 0 0 — Percentage time of closure behavior(s) Male 0 0 — ** represents highly significant difference; * represents significant difference

Discussion the water temperature is over 30℃, it The range between 20 to 25℃ might be may lead to the death of juvenile crabs, the suitable temperature for the growth which should be noted in artificial of juvenile crabs of E. sinensis, which breeding practices. From existing conformed to the temperature of the reports of larval cultivation of E. season in which large number of sinensis, the most suitable cultivation juvenile crabs of E. sinensis appear. If temperature in the experiment of Chang Iranian Journal of Fisheries Sciences 18(4) 2019 771

and Sang (1995) is 25℃. The environment for the growth of E. appearance of juvenile crabs in Yangtze sinensis and the optimal range was 7.0 River Delta region was between April to 9.1. The respiratory activity of 15th to May 15th and the range of water crustacean will be changed no matter temperature was between 20 to 25°C whether it was lower of higher than this (Zhang 2002), which was roughly range. The ability to absorb oxygen consistent with the results of this from outside through gills will be experiment. influenced, thus affecting the oxygen The optimal survival temperature consumption rate (Lin et al., 2000). The required by the E. sinensis at different pH change during the course of this growth periods is different. In the experiment was within the appropriate breeding season, the temperature range range and thus the pH change was not was 10℃ to 20℃ (Herrgesell et al., the primary cause of the death of crabs 1983). The survival rate of megalopa in this experiment. Although the TP larva was the highest between 12 to concentration during the course of this 18℃ and megalopa larva has relatively experiment was higher than normal strong tolerance to low temperature. aquatic water, the change node of TP Afterwards, the optimal survival concentration was not consistent with temperature gradually rises with the the death time pf crabs. Therefore, the growth of larva (Anger, 1991). The high TP concentration was also not the optimal culture condition for adult E. primary cause of the death of crabs in sinensis was that the pH value was 6.8 this experiment. No fresh water was and the water temperature was 28°C poured during the course of this (Hong et al., 2013). This trend experiment, so the excreta of E. sinensis conforms to the real situation where and the residue of feed led to the water temperature at the beginning of increase of ammonia concentration in Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 the breeding peak of E. sinensis is low the water. The increase of ammonia but gradually rises with the progress of stress concentration and the extension time. of stress time led to the damage of non- The temperature required during the specific immune defense system of E. shelling period of E. sinensis was sinensis, thus accelerating the death of relatively low. Although the mechanism E. sinensis (Wang et al., 2006; Hong et in this aspect remains to be further al., 2007; Huang et al., 2006). However, investigated, the situation in the initial conditions in this experiment experiments and cultivation bases were consistent except the temperature, indicates the shelling of larva of E. so the increase of ammonia sinensis often occurs late at night or concentration was the possible cause early in the morning when the water but not the primary cause of the death temperature was low, which reflects the acceleration of E. sinensis. Hong-Zhu choice of low temperature of larva of E. Wang proposed that TN concentration is sinensis. negatively correlated with crab yield in Alkaline pH was the suitable studying the stocking model of E. 772 Peng et al., Effect of temperature stress on the survival of…

sinensis in Yangtze River basin (Wang and salinity on the larval et al., 2006), which is consistent with development of the Chinese mitten the views of this paper. crab Eriocheir Sinensis (decapoda, In conclusion, temperature exerted grapsidae). Marine Ecology Progress great influence on the survival of Series, 72, 103-110. juvenile crabs of E. sinensis. Obviously, Bo Huang, H., Nan-shan, D. and Wei, temperature needs to be L., 2001. Effects of temperature and comprehensively considered in the Ca2+ on the larval development of production practice. Meanwhile, we the decapoda crustacean: Eriocheir should attach great significance to water sinensis. Chinese Journal of quality monitoring and make Oceanology and Limnology, 19, 228- adjustments to abnormal conditions. To 232. guarantee high survival rate of juvenile Bryars, S.R. and Havenhand, J.N., crabs of E. sinensis in breeding, 2006. Effects of constant and transportation and other activities, the varying temperatures on the temperature should be controlled no development of blue swimmer crab higher than 30℃. (Portunus pelagicus) larvae: Laboratory observations and field Acknowledgments predictions for temperate coastal The authors greatly appreciate Lei waters. Journal of Experimental FENG and Huimin HUANG for Marine Biology and Ecology, 329, assistance with the field investigation. 218-229. The authors also greatly appreciate Fisher, M.R., 1999. Effect of Qing ZHANG who provided temperature and salinity on size at experiment samples. This research was maturity of female blue crabs. supported by the National Key Transactions of the American Downloaded from jifro.ir at 9:56 +0330 on Thursday September 30th 2021 Research and Development Program of Fisheries Society, 128, 499-506. China (2014BAC09B03), International Hamasaki, K., 2003. Effects of Science and Technology Cooperation temperature on the egg incubation Program of China (2015DFA90450), period, survival and developmental and Key Technology R&D Program of period of larvae of the mud crab Hunan Province (2016TP1014). Scylla serrata (Forskål) (Brachyura: Portunidae) reared in the laboratory. References Aquaculture, 219, 561-572. Aardt, W.J.V., 1993. The influence of Herrgesell, P.L., Schaffter, R.G. and temperature on the haemocyanin Larsen, C.J., 1983. Effects of function and oxygen uptake of the freshwater outflow on San Francisco freshwater crab Potamonautes Bay biological resources. warreni calman. Comparative Interagency Ecological Study Biochemistry and Physiology Part A Program for the Sacramento–San Physiology, 106, 31-35. Joaquin Estuary, Technical Report Anger, K., 1991. Effects of temperature No. 7. July Iranian Journal of Fisheries Sciences 18(4) 2019 773

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