High temperature acclimation alters upper thermal limits and growth performance of Indian major carp, rohu, Labeo rohita (Hamilton, 1822)

Highlights

• Upper thermal limit of Labeo rohita decreased in increased acclimation temperature.

• Lowered Hb and RBC but higher WBC and blood glucose level were noticed at the CTmax in increased acclimation temperature.

• Higher frequencies of erythrocytic nuclear abnormalities (ENAs) and erythrocytic cellular abnormalities (ECAs) of erythrocytes were in the increased acclimation temperature.

• The growth performances were the highest at 33 °C and the lowest at 36 °C.

• High temperature (36 °C) is stressful for L. rohita.

Abstract

Increase in water temperature due to anthropogenic and climatic changes is expected to affect physiological functions of fish. In this study, we determined high temperature tolerance (CTmax) of a common aquacultured Indian major carp, rohu, Labeo rohita fingerlings (15.96 ± 0.72 g BW, 11.56 ± 0.42 cm TL) followed by acclimatization at three temperatures (30, 33, 36 °C). To determine the CTmax, we analyzed the major hemato-biochemical indices - hemoglobin (Hb), red blood cell (RBC), white blood cell (WBC), blood glucose levels, and erythrocytic nuclear abnormalities (ENAs) and erythrocytic cellular abnormalities (ECAs) of peripheral erythrocytes in the fish sampled at the start and end point at each acclimated temperature. Significantly decreased CTmax of the fish was found at 36 °C compared to 30 °C and 33 °C. The fish in the highest (36 °C) temperature were found with significantly lower Hb and RBC content and significantly higher WBC and blood glucose levels than that of the fishes in the lowest (30 °C) temperature both at the start and end points. The highest frequencies of ENAs and ECAs were found in the highest (36 °C) temperature group compared to the lowest (30 °C) temperature group at both the points. We also evaluated growth performance of the rohu fingerlings reared in the three temperatures for 60 days. The growth parameters - final weight gain, percent weight gain and specific growth rate were the highest at 33 °C and the lowest at 36 °C. The present study revealed that the highest temperature (36 °C) tested here may be hazardous to rohu and the temperature should be kept below 36 °C in the aquaculture setting to avoid physiological damage and growth and production loss to the fish.

Introduction

Temperature has gained a paramount importance among an array of environmental variables for the development and growth of aquatic organisms. Asymmetric fluctuations of atmospheric temperature, even a few degrees can affect the aquatic organisms including fish altering major hydrological properties (McGinn, 2002). For example, Cheung model depicts the projection that 1 °C temperature increase can reduce more than 3 million metric tons of prospective catches globally (Cheung et al., 2016). Evolutionarily fishes are adapted to live within a specific range of environmental variation, and beyond that range poses a threat for their physiology (Reynolds and Casterlin, 1980) and health (Barton et al., 2002). Almost all teleost species adopt their own special physiological and behavioral mechanisms that facilitate them to subsist against temperature associated stressful conditions (Prosser and Heath, 1991). In the tropics, most of the fishes are successfully adapted at a temperature range between 25 and 35 °C (Howerton, 2001). Though temperature increase to an optimum level can be favorable for aquaculture pertaining to better growth and early maturity, exceeding that limit may negatively affect the growth (Islam et al., 2019) and reproduction (Shahjahan et al., 2013, 2017). Moreover, high temperature can be stressful for fishes (Shahjahan et al., 2018; Ashaf-Ud-Doulah et al., 2019). Several studies underpin that in a condition of increased/increasing open water temperature, wild fishes can move to higher latitudes in a species-specific manner (Fogarty et al., 2017; Kleisner et al., 2017; Alabia et al., 2018). However, fish exist in confined aquatic conditions (ponds, lakes, cages etc.), especially the farmed fishes in captive condition are not capable of eluding them from daily or seasonal changes in water temperature. Therefore, to figure out the effect of temperature changes on fish species, thermal tolerance and acclimation studies have appeared a considerable tactics for scientists.

Acclimation temperature plays an important role in the thermal tolerance study. Acclimation can be defined as the total ability of fishes to adapt themselves to short or long-term changes in their surrounding environment. It has been observed that the organisms that show high physiological plasticity i.e., greater ability to adjust to the new thermal condition, are able to better survive in a thermal fluctuations or in a habitat that undergo abrupt thermal changes (Sandblom et al., 2014; Fu et al., 2018). Critical thermal methodology is extensively used to evaluate the higher and lower limits of temperatures tolerance in aquatic organisms where they are subjected to either continuous increase or decrease in temperature until temperature reaches the point of loss of equilibrium or lethal endpoint. The rate of oxygen consumption is another physiological response that can be integrated with the changes in environmental parameters due to its direct correlation to metabolic activities and energy flow that affects homeostasis of organisms (Salvato et al., 2001). Study suggests that subsequent decrease in dissolve oxygen concentration and increase in metabolic activity (resulting oxygen consumption) with the increase of environmental temperature, forces fish to try hard to adapt to this environmental condition by raising the level of the total hemoglobin content in their blood (Brix et al., 2004). Physiological stress response to intrinsic or extrinsic fluctuations by the fish have long been monitored using a number of hemato-biochemical parameters including the Hb and blood glucose levels as indicators (Cazenave et al., 2005; Elahee and Bhagwant, 2007; Hossain et al., 2015; Salam et al., 2015; Ahmed et al., 2016; Sharmin et al., 2016). Variation in the total white blood cell count induced by different stressors has also been used as a biochemical immunosuppressive indicator for fish (Kopp et al., 2010).

At the cellular level, erythrocyte abnormalities are used for qualitative and quantitative evaluation of cellular as well as nuclear damage caused by short or long term exposure to mutagenic agents (Montserrat et al., 2007). Consequently, this methodology has been found suitable for the measurement of thermal stress in fish because elevation of water temperature can result harmful effects on DNA (Shuey et al., 2006). In addition, increased temperature can also be accountable for DNA damage that may cause differential nuclear morphology in cells triggered by the release of DNase from lysosomes and the inactivation of DNA repair associated enzymes (Zafalon-Silva et al., 2017). Previous studies also observed the correlation of variable size and number of erythrocytes with ambient temperatures (Ytrestoyl et al., 2001; Shahjahan et al., 2018).

Rohu, Labeo rohita is a freshwater Indian major carp, commonly cultivated throughout Bangladesh and a number of other Asian countries – India, Laos, Myanmar, Nepal, Pakistan, and Viet Nam (FAO, 2020) and occupies a significant part of total fish production from aquaculture. The fish is very important to the aquaculturists for their rapid growth, high commercial importance and consumer preferences. Growth rate is regarded as the most important parameters that determine the economic aspects of commercial fish culture, which is impacted by various biotic and abiotic factors (Brett and Groves, 1979). Previously, the effect of acclimated temperatures for the growth (Das et al., 2005), metabolism, oxygen consumption (Das et al., 2004), a number of hematological parameters (Das et al., 2006) and metabolic responses to thermal acclimation (Das et al., 2009) of L. rohita have been studied. However, detailed information regarding the adaptive responses of this important species especially hemato-cytological changes during high temperature tolerance are yet to be thoroughly studied. Understanding the high temperature tolerance and growth performance of L. rohita in relation to different acclimation temperature will allow us to determine the level of stress response in a changing environment in modern aquaculture. Therefore, considering the increasing trend of global temperature and culture potential of this fish species, we investigated high temperature tolerance and growth performance of L. rohita fingerlings after acclimating at different temperatures. We analyzed the major hemato-biochemical indices, nuclear and cellular abnormalities of peripheral erythrocytes in the fish during determination of the high temperature tolerance.