Temperature effects in single or combined with chemicals to the aquatic organisms: An overview of thermo-chemical stress

✅ 全文

温度效应单独或与化学物质联合作用对水生生物的影响:热化学胁迫综述

作者 Syed Shabi Ul Hassan Kazmi; Yolina Yu Lin Wang; Yan-Er Cai; Zhen Wang 期刊 Ecological Indicators 发表日期 2022 ISSN 1470-160X DOI 10.1016/j.ecolind.2022.109354 类型 原创研究 (Original Research)

📄 中文摘要 Chinese Abstract

中文
气候变化,特别是全球变暖,正通过水温升高和热极端事件频发显著改变水生环境。这些变化对水生生物,尤其是变温动物构成严重威胁,因为它们的生理机能、行为和生存能力与环境温度密切相关。温度变化影响广泛的生物响应——从热休克蛋白和代谢转换等分子机制,到生长、繁殖和适合度等整体生物表现。此外,温度可调节水体中化学污染物的毒性,这一现象被称为温度依赖性化学毒性(TDCT),使生态风险评估复杂化,并对现行水质基准(WQGs)的充分性提出挑战。

📋 英文结构化总结 English Structured Summary

全文整理

EN

Background:

Climate change, particularly global warming, is significantly altering aquatic environments through rising water temperatures and increased frequency of thermal extremes. These changes pose serious threats to aquatic organisms, especially ectotherms, whose physiology, behavior, and survival are tightly linked to ambient temperature. Temperature variations influence a wide range of biological responses—from molecular mechanisms like heat shock proteins and metabolic shifts to whole-organism performances such as growth, reproduction, and fitness. Moreover, temperature can modulate the toxicity of chemical contaminants in water, a phenomenon known as temperature-dependent chemical toxicity (TDCT), which complicates ecological risk assessments and challenges the adequacy of current water quality guidelines (WQGs).

Methods:

This paper is a comprehensive review synthesizing existing literature on the effects of temperature—both alone and in combination with chemical stressors—on aquatic organisms. The authors analyzed studies involving diverse aquatic species (e.g., fish, invertebrates like Daphnia and clams) and chemicals (e.g., heavy metals, pesticides) under varying thermal conditions. They evaluated physiological, biochemical, and ecological responses using frameworks such as thermal performance curves (TPCs), oxygen-limited thermal tolerance (OLTT), and species sensitivity distributions (SSD). Two primary models were examined for TDCT: Model-I (linear increase in toxicity with temperature) and Model-II (non-linear, inverted V-shape response), with emphasis on how these inform risk assessment across different temperature regimes.

Results:

Temperature fluctuations induce significant physiological and biochemical changes in aquatic organisms, including elevated cortisol levels, increased expression of heat shock proteins (e.g., HSP70), altered haemolymph parameters (e.g., glucose, hemoglobin, total haemocyte count), and disrupted immune function. Whole-organism performances such as feeding, growth, reproduction, and survivorship follow unimodal or inverted V-shaped responses to temperature, peaking at optimal ranges and declining sharply under thermal extremes. Chemical toxicity generally increases with temperature due to enhanced uptake and bioaccumulation driven by higher metabolic and ventilation rates, although non-linear patterns (Model-II) are observed under extreme conditions. Oxidative stress, DNA damage, and apoptosis are exacerbated at thermal limits, particularly when combined with chemical exposure.

Data Summary:

Studies show that chemical toxicity often follows an inverted V-shape relationship with temperature (Model-II), being lowest at optimal temperatures and highest near thermal tolerance limits. For example, cadmium accumulation in species like *Daphnia magna* and *Corbicula fluminea* increases with temperature due to higher metabolic rates. Temperature-dependent species sensitivity distributions (SSDs) reveal that aquatic organisms are more sensitive to chemicals at suboptimal temperatures. In marine systems, metals like Cd, Cu, and Zn exhibit heightened toxicity under thermal stress, with SSD curves shifting horizontally (temperature effect) and changing slope (salinity effect). Mortality rates increase monotonically at temperature extremes, while developmental and reproductive traits display left-skewed inverted V-shaped responses.

Conclusions:

Thermal stress profoundly impacts aquatic organisms at multiple biological levels, from molecular disruptions to population-level consequences. Elevated temperatures enhance chemical toxicity primarily by increasing contaminant uptake and metabolic demand, while simultaneously impairing physiological defenses. The integration of temperature into ecological risk assessment—through tools like temperature-dependent SSDs—is essential for accurate derivation of water quality guidelines. Current assessment factors may underestimate risks under climate change scenarios, necessitating refined models that account for thermo-chemical interactions across diverse ecosystems.

Practical Significance:

This review underscores the urgent need to incorporate temperature variability into environmental monitoring, chemical risk assessment, and policy-making for aquatic ecosystem protection. As climate change intensifies thermal extremes, traditional static water quality standards may fail to safeguard biodiversity. Adopting dynamic, temperature-informed frameworks—such as adjusted SSDs and updated WQGs—can improve the resilience of regulatory strategies and support sustainable management of both freshwater and marine environments under global warming.

📋 中文结构化总结 Chinese Structured Summary

中文

背景:

气候变化,特别是全球变暖,正通过水温升高和热极端事件频发显著改变水生环境。这些变化对水生生物,尤其是变温动物构成严重威胁,因为它们的生理机能、行为和生存能力与环境温度密切相关。温度变化影响广泛的生物响应——从热休克蛋白和代谢转换等分子机制,到生长、繁殖和适合度等整体生物表现。此外,温度可调节水体中化学污染物的毒性,这一现象被称为温度依赖性化学毒性(TDCT),使生态风险评估复杂化,并对现行水质基准(WQGs)的充分性提出挑战。

方法:

本文为一篇综合性综述,系统整合了关于温度单独作用及与化学胁迫因子共同作用对水生生物影响的现有文献。作者分析了涉及多种水生生物(如鱼类、水蚤和蛤蜊等无脊椎动物)和化学物质(如重金属、农药)在不同热条件下的研究。他们利用热性能曲线(TPC)、氧限制热耐受性(OLTT)和物种敏感性分布(SSD)等框架评估了生理、生化和生态响应。研究重点考察了两种TDCT模型:模型I(毒性随温度线性增加)和模型II(非线性倒V形响应),并着重探讨了这些模型如何在不同温度条件下为风险评估提供依据。

结果:

温度波动引起水生生物显著的生理和生化变化,包括皮质醇水平升高、热休克蛋白(如HSP70)表达增加、血淋巴参数(如葡萄糖、血红蛋白、血细胞总数)改变以及免疫功能紊乱。整体生物表现如摄食、生长、繁殖和存活率对温度呈单峰或倒V形响应,在最佳温度范围内达到峰值,在热极端条件下急剧下降。化学毒性通常随温度升高而增强,原因是代谢率和通气率增加导致污染物吸收和生物累积增加,但在极端条件下可观察到非线性模式(模型II)。氧化应激、DNA损伤和细胞凋亡在热极限条件下加剧,尤其是在与化学暴露共同作用时更为显著。

数据总结:

研究表明,化学毒性通常与温度呈倒V形关系(模型II),在最佳温度下最低,在接近热耐受极限时最高。例如,大型溞(*Daphnia magna*)和河蚬(*Corbicula fluminea*)等物种的镉累积随温度升高而增加,原因是代谢率升高。温度依赖性物种敏感性分布(SSD)表明,水生生物在次优温度下对化学物质更为敏感。在海洋系统中,镉、铜和锌等金属在热胁迫下毒性增强,SSD曲线发生水平移动(温度效应)和斜率变化(盐度效应)。死亡率在温度极端条件下单调递增,而发育和繁殖特征则呈现左偏的倒V形响应。

结论:

热胁迫在多个生物学层面对水生生物产生深远影响,从分子层面的紊乱到种群层面的后果。温度升高主要通过增加污染物吸收和代谢需求来增强化学毒性,同时削弱生理防御能力。将温度因素纳入生态风险评估——通过温度依赖性SSD等工具——对于准确推导水质基准至关重要。在气候变化情景下,现行评估因子可能低估风险,因此需要建立能够反映不同生态系统中热化学相互作用的精细化模型。

实践意义:

本综述强调亟需将温度变化纳入环境监测、化学风险评估和水生生态系统保护的政策制定中。随着气候变化加剧热极端事件,传统的静态水质标准可能无法有效保护生物多样性。采用动态的、温度信息框架——如调整后的SSD和更新的WQGs——可增强监管策略的韧性,支持全球变暖背景下淡水和海洋环境的可持续管理。

📖 英文全文 English Full Text

EN

Ecological Indicators 143 (2022) 109354 Available online 29 August 2022

1470-160X/© 2022 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/).

Temperature effects in single or combined with chemicals to the aquatic organisms: An overview of thermo-chemical stress

Syed Shabi Ul Hassan Kazmi , Yolina Yu Lin Wang , Yan-Er Cai , Zhen Wang *

Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, and Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou

University, Shantou 515063, China A R T I C L E I N F O

Keywords:

Climate change Thermal stress Aquatic ecosystem Temperature dependent chemical toxicity

Aquatic organisms A B S T R A C T Climatic change (global warming) not only limited to the terrestrial environmental variations but also trans­ forming the aquatic environments. Recent studies have reported that both coastal and freshwater bodies have experienced the progressive warming and will intensify (giant leap) during this century. Same time the bewil­ dering array of thermal stresses poses serious threats to the aquatic organisms. Although, there is a growing body of literature and scientific consensus regarding the effects of temperature to the aquatic biota. Hitherto, the extent to which the thermo-chemical stress on aquatic organisms intensifying is not fully elaborated. We have summarized following declarations:

• Temperature variations induce a range of physiological and biological responses in aquatic organisms including; corticosteroid response, metabolic response, immune responses, heat shock proteins, and wavering in haemolymph parameters.

• The observed responses due to temperature fluctuations are actually attributed to the whole organism level performances like, acclimation and adaptation, fitness, feeding and food conversion ratio, growth and development.

• Temperature dependent chemical toxicities are subjected to influence the chemical processes and underlying molecular/genetic mechanisms of aquatic organisms at individual population and community levels.

Additionally, this review outlined the series of mechanisms in aquatic organisms associated with temperature changes in single or combined with chemicals. These observations provide significant evidence that the climate change and temperature variations are critical and there is pressing need to carefully evaluate the conditions and responses at large geographical scales.

1. Introduction In this century, climate change (global warming) may be the largest anthropogenic disturbance ever placed on natural systems (Sala et al.,

2000; Thomas et al., 2004). Climatic changes not only rising the water temperature also leads to more frequent and long-lasting cold and heat waves. As postulated, global warming will result in climate change which is more unpredictable with increasing extreme weather events, including larger temperature fluctuations and more frequent extreme temperature events occurring in the future (IPCC, 2014).

Climate change induced by temperature variations can profoundly influence the ecology of ectotherms, including their physiological, biochemical and ecological responses (Calosi et al., 2008). The rela­ tionship between ectotherm life-history performances and temperature is typically characterized by an unimodal thermal performance curve (TPC) (Huey and Stevenson, 1979), defining the optimum temperature (To) and the operative temperature range between the critical minimum temperature (CTmin) and the critical maximum temperature (CTmax).

Currently, this unimodal TPC has been commonly used to assess the sensitivity of ectotherm species to climate warming (Amarasekare and

Savage, 2012), composite fitness metrics such as reproduction, devel­ opment, metabolic rate, fitness (Van der Have, 2002; P¨ortner and Knust,

2007; Kingsolver, 2009), and evolution (Huey and Kingsolver, 1989;

Huey et al., 2003; Frazier et al., 2006).

* Corresponding author.

E-mail address: zhenwang@stu.edu.cn (Z. Wang).

Contents lists available at ScienceDirect Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind https://doi.org/10.1016/j.ecolind.2022.109354

Received 21 July 2022; Received in revised form 15 August 2022; Accepted 18 August 2022

Ecological Indicators 143 (2022) 109354 2 Temperature variations caused by climate change, especially for thermal extremes, also have profound implications on chemical toxicity to individual organisms, and thus influences the size and structure of their population, the species composition of communities, and the structure and functioning of ecosystems (Cairns et al., 1975; Cairns et al., 1978; Lau et al., 2014; Zhou et al., 2014). Pioneer studies of the temperature-dependent chemical toxicity (TDCT) conducted on a wide range of aquatic organisms and chemicals have demonstrated that chemical toxicity and temperature varied from no relationship to negative or positive relationship which means that chemical toxicity partly, or fully dependent on temperature variations (Cairns et al., 1975;

Cairns et al., 1978). Although it is commonly reported that the chemical toxicity increases with increasing temperature (linear model, Model-I) within a range of temperatures (Leung et al., 2000; McConnachie and

Alexander, 2004; Kwok and Leung, 2005). As demonstrated in further comprehensive toxicity studies, non-linear function (e.g., inverted V- shape model, Model-II) tend to describe the relationship between tem­ perature and chemical toxicity more adequately, especially under extreme thermal conditions (Heugens et al., 2003; Bao et al., 2008).

Most recently, considering these two models (Model-I and Model-II) and natural temperature variations, the previous commonly used assessment factors (e.g. 10) were re-assessed to further validate whether or not the application of these factors in water quality guidelines (WQGs) can adequately protect freshwater and marine ecosystems, respectively (Lau et al., 2014; Zhou et al., 2014).

Because aquatic organisms are constantly exposed to environmental stimuli including both physical (temperature) and chemical stressors.

Temperature variations will not only alter the chemical toxicity to in­ dividual aquatic organisms, but also potentially introduce bias into the risk assessment of chemical contaminants or derivation of appropriate

WQGs for protecting the aquatic communities against chemicals. Thus, it is pertinent and essential to address the thermal effect on physico­ chemical properties of chemical contaminants and biological responses, and the combined influence of temperature and chemical exposure to biological responses. Therefore, this review emphasized the following three issues: 1) effects of temperature on physiological and biochemical responses to the aquatic organisms; 2) effects of tempeturure on chem­ ical preocess, including chemical speciation, accumulation, circulation and elimination; and 3) combined influence of temperature and chem­ ical to biological responses.

2. Temperature effects on aquatic organisms 2.1. Physiological and biological responses

2.1.1. Corticosteroid response Physiological stress responses such as cortisol release are simply autonomic responses that indicate activity and do not necessarily equate to suffering and diminished welfare (Ashley, 2007). The primary func­ tion of cortisol is to induce physiological changes that help animals either protect themselves from, or adapt to, the stressor. Cortisol release is a well-studied and sensitive indicator of cold stress. For instance, cortisol levels have been found to be positively correlated to the magnitude of temperature decreases for a number of fishes, including rainbow trout Oncorhynchus mykiss (Barton and Peter, 1982), salmon

Salmo salar (Skjervold et al., 2001; Hyv¨arinen et al., 2004), tilapia

Oreochromis aureus (Chen et al., 2002), and yellow perch Perca flavescens (Jentoft et al., 2002), and common carp Cyprinus carpio (Jaxion-Harm and Ladich, 2014). However, continuous high levels of cortisol can become maladaptive by regulating a diverse array of systems including metabolism, ion regulation, immune, growth and reproduction, which may ultimately affect the animal’s health (Houghton and Matthews,

1990). In certain instances, stress-modifying factors that are themselves chronically stressful, such as poor water quality or toxicants, can actu­ ally exacerbate (Barton and Peter, 1982) or attenuate the cortisol response to a second stressor. In rainbow trout (Salmo gairdneri), for instance, cortisol not only inhibits ovarian growth but also pushes the sex ratio in the male direction (van den Hurk and van Oordt, 1985).

2.1.2. Heat shock proteins (HSPs) One of the molecular responses that is activated in a cell under thermal stress is the heat shock proteins (HSPs) response, an event of genetic activation that occurs in the cells in response to abnormal, stressfully high or low temperatures (Hofmann, 2005). HSPs protect proteins, membranes, and other cellular components during heat-stress and facilitate repair or degradation of damaged proteins following a stressful event (Parsell and Lindquist, 1994). Importantly, while HSPs were so named because they are up-regulated by an acute increase in temperature (Lindquist, 1980). Extensive research has led to a detailed understanding of HSPs regulation and their mechanisms of action (Feder and Hofmann, 1999). There is a tendency of HSPs (e.g., HSP70) to in­ crease their expression with increasing levels of temperature variability (Arias et al., 2011; Folguera et al., 2011).At low temperatures, the synthesis and expression of HSP70 also occurs after the freezing point.

Because the depressed organism’s metabolism in such conditions can,t activate the physiological machinery which is necessary to start the synthesis of chaperone proteins, which occurs primarily in the recovery time. This indicating that there is a close relationship between the increased expression of HSP70 and the enhanced capacity of self- protection for subsequent extreme events (Krebs and Bettencourt,

1999; Chown and Nicholson, 2004).

2.1.3. Metabolic response Glucose concentration in the haemolymph increased during the exposure to the higher water temperatures (Lorenzon et al., 2007; Malev et al., 2010). This suggests that more glucose being made and available as energy supplement to meet increasing metabolic demand during stressful conditions of lower oxygen availability (Wendelaar Bonga,

1997) and is supported by the same temperature related response of lactate, which increases with increased energy usage with higher tem­ peratures (Durand et al., 2000; Ridgway et al., 2006; Lorenzon et al.,

2007). Results of haemolymph glucose in Maia squinado acclimated at different temperatures also indicated that the concentration of glucose in haemolymph reduced at low temperatures, while short acclimation periods at high temperature resulted higher glucose levels in the hae­ molymph (Durand et al., 2000).

2.1.4. Haemolymph parameters Hemocytes play an essential role in physiology and immune defense of aquatic organisms (Johansson et al., 2000). Loss and damage of circulating hemocytes would depress the immune ability, increase the susceptibility against pathogens, and even endanger the survival (Cheng et al., 2005). The total haemocyte count (THC) was found to be increased during exposure to the high temperatures so as to increase the immunity for thermal stress (Liu et al., 2010; Malev et al., 2010). Hae­ moglobin (Hb), as a direct link between ambient O2 availability and aerobic metabolism, also followed a temperature-dependent manner for aquatic invertebrates (Lamkemeyer et al., 2003; Seidl et al., 2005; Zeis et al., 2013). At temperatures below the critical thresholds, Hb induction in Daphnia is an example of a stressor-specific homeostasis response (Kültz, 2005). This second line of stress defense results in restored cellular oxygen conditions. However, such observations were not made by other authors for vertebrates (e.g., fishes), indicates that this attribute is not uniquely associated with heterothermy, but may have arisen in response to alternative evolutionary incentives (Clark et al., 2010;

Muyssen et al., 2010).

2.1.5. Immune responses The susceptibility of fish to disease is partly dependent on their environment, in particular on water temperature (Le Morvan et al.,

1998), because their entire physiology, including immune functions, is influenced by environmental temperature (Fry, 1967). For example,

S.S.U.H. Kazmi et al.

Ecological Indicators 143 (2022) 109354 3 most infectious diseases, such as the spring viraemia of carp (Cyprinus carpio), occur at lower environmental temperatures. Thus, the patho­ logical situation in fish depends both on temperature-dependent im­ mune system regulation and on pathogen growth (Le Morvan et al.,

1998). It is generally reported that lower temperatures adversely affected both cellular and humoral specific immune responses in various fish species (Bly and Clem, 1992). Lower temperatures can adversely affect specific immune responses mediated by T helper cells. In contrast, the secondary response can be elicited at low temperatures if immuno­ logical memory is established at high temperatures. The specific im­ mune responses, especially the humoural responses, are suppressed through the inhibition of the primary antibody responses at lower temperatures (Avtalion et al., 1970; Bly and Clem, 1992). In contrast, higher temperature could increase plasma IgM concentration, but a decreasing trend was observed in lysozyme activity and complement bacteriolytic activity in responses to thermal treatments (Jokinen et al.,

2011).

2.2. Whole-organism level performances 2.2.1. Acclimation and adaptations

Although physiological processes of aquatic ectotherms generally operate optimally within narrow temperature ranges, an extensive literature shows that most ectotherms can adjust or acclimate to changes in ambient temperature (Huey and Berrington, 1996; Stillman, 2003).

Within the genetic limits, sufficient acclimation of an organism can alleviate stress response to a novel thermal environment and thus extend thermal tolerant boundaries (Cairns et al., 1975; Cairns et al., 1978). As short-term exposure to either cold or warm extremes can be crucial to ectotherms (Bokhorst et al., 2008), they have to adjust their physio­ logical and biochemical responses so as to overcome such a stressful thermal scenario.

Stress proteins such as heat shock proteins (HSPs) can be induced to protect cellular structures (e.g., DNA) and to repair damaged compo­ nents, and in this way the ectotherm could extend its survivability even though in a time-limited manner (P¨ortner, 2002b). Liu et al. (2010) showed that anthraquinone extracts could improve haemolymph total protein contents, nitrogen monoxide concentrations, and lysozyme ac­ tivities, help shrimp resist high temperature stress. Additionally, Lub­ zens et al. (1995) found that the acclimation period of rotifers (Brachionus plicatilis) was associated with the synthesis of at least one specific protein (immunoisolation) and accumulation of lipids (eicosa­ pentaenoic acid), which supports the hypothesis of specific adaptations to survival at low temperatures during an acclimation period.

However, acclimation is generally considered to be only partial, so that physiological (and functional) processes are not completely de- coupled from temperature (Kingsolver and Huey, 1998). Fast and pro­ gressive temperature change could minimize acclimation phenomena (Burleson and Silva, 2011) and involved in a shift of thermal tolerant threshold (Frederich and P¨ortner, 2000). The common frog (Rana tem­ poraria) for instance did not show any behavioral adaptations in terms of breeding at lower temperatures (below 5 ◦C) (Muir et al., 2014).

2.2.2. Feeding and food conversion ratio (FCR) The influence of temperature-induced changes in water viscosity on the species activities (e.g., swimming) play an important role in deter­ mining the food uptake and feed conversion ratio (FCR) (Loiterton et al.,

2004), especially for small aquatic ectotherms. It is known that ambient temperature has mechanical effects on aquatic ectotherms by inversely affecting the dynamic viscosity of water (Vogel, 1994). For instance,

Bolton and Havenhand (1998) demonstrated that both physiological and viscosity-induced components of the reduction in water tempera­ ture could significantly reduce the number of microspheres ingested by

Galeolaria caespitosa. Likewise, Loiterton et al. (2004) demonstrated that the ingestion rate of D. galeata was found to be 50 % lower at 10 ◦C than at 25 ◦C due to the combined effects of increased viscosity and lower temperature, while viscosity alone accounted for 61 % of the decline in

FCR. Lagergren et al. (2000) also showed that hydrodynamic costs of predator defense in Eubosmina increased at low temperatures due to increased drag associated with higher viscosities.

Evidence also showed that growth of aquatic individuals were opti­ mized at the optimum temperature, in combination with maximum food intake and optimum FCR (Abbink et al., 2012; Vellinger et al., 2012). A reduction in feed utilization efficiency at extreme water temperatures has been reported for barramundi Lates calcarifer (Bermudes et al.,

2010), wolf fish Anarhichas lupus (Imsland et al., 2006) and European seabass Dicentrarchus labrax (Person-Le Ruyet et al., 2004). This is also consistent with another study on yellowtail kingfish in which FCR was significantly better in warm water (17 ◦C to 22 ◦C) compared with cool water (14 ◦C to 17 ◦C) (Moran et al., 2009). This can be explained that activities of digestive enzymes increase with within a certain tempera­ ture range but shortened passage time at higher temperatures may reduce exposure of food to enzymatic action (Harwood, 1979; McCarthy et al., 1999).

2.2.3. Reproduction Reproductive traits (e.g., eggs, hatching) are thought to be more sensitive to thermal stress than other traits and should therefore be included when estimating the fitness effects of thermal stress (Jørgensen et al., 2006). Moreover, reproductive processes are often affected by temperature change earlier, in other words by less severe conditions than those affecting development and survival (Fasolo and Krebs, 2004).

Previous studies also show a more symmetric temperature response on reproductive performances predicted by reaction rate theory (i.e., enzyme kinetics) (Carriere and Boivin, 1997; Dannon et al., 2010;

Amarasekare and Savage, 2012), in combination with the regulatory processes based on negative feedback pathways such as hormonal regulation (Nijhout, 1994). Several studies have investigated the nega­ tive effects of heat shock on the longevity and fecundity heat or cold shock processes (Rinehart et al., 2000). Heat or cold shock can also cause injury to oocytes and ovarian development in females that lead to the decrease in egg production (Rinehart et al., 2000; Castro-Longoria,

2003). In addition, heat shock can cut down on male fertility due to direct injury to the testes and sperm (Scott et al., 1997; Nguyen et al.,

2013). Moreover, the hatching success is also adversely influenced by extreme higher or lower temperatures (Holste and Peck, 2006; Hansen et al., 2010; Cruz et al., 2013), leading to lower survivor and hence lowering abundances of aquatic organisms. This probably due to decreased membrane permeability, disequilibria of coupled enzyme reactions and limits imposed by kinetics and inactivation of enzyme proteins (Rosa et al., 2012).

2.2.4. Growth and development Water temperature is one of the major environmental factors influ­ encing growth and development in aquatic ectotherms (Brett, 1979). A decreasing ontogenetic shift in optimum temperature is common for most ectotherms and has been described for a range of marine fishes including Atlantic cod (G. morhua) (Lafrance et al., 2005); turbot (Scophthalmus maximus) (Imsland et al., 1996); Atlantic halibut (Hippo­ glossus hippoglossus) (Hallaråker et al., 1995); plaice (Pleuronectes pla­ tessa) (Fonds et al., 1992); and yellowtail (Seriola lalandi) (Pirozzi and

Booth, 2009; Abbink et al., 2012). The growth of fishes were then reduced at the extreme temperature compared with the optimal tem­ perature (i.e., Inverted V-shape Model-II). This parabolic temperature response is typical of all species and can be explained by that the sig­ nificant reduction in food intake coupled with an increased demand for energy at such high temperatures is the likely major factor contributing to the poor growth performance of the fishes at extreme high tempera­ tures (Imsland et al., 1996; Peck et al., 2002; Bermudes et al., 2010). On the contraty, loss of appetite was suggested to be the direct reason for the growth inhibition at low temperatures (Ibarz et al., 2005). In addi­ tion, the fishes would have restricted heart rate and circulation of blood,

S.S.U.H. Kazmi et al.

Ecological Indicators 143 (2022) 109354 4 leading to limited supply of oxygen and energy to maintain essential cellular functions, and such conditions force the fish to switch to anaerobic respiration to acquire more energy (P¨ortner, 2002a), and hence, lower growth performances at extreme low temperatures.

Previous studies also showed that speices’ developmental rates exhibited temperature responses that were most consistent with the left- skewed inverted V-shape pattern (Sharpe and DeMichele, 1977; Huey and Berrigan, 2001; Gillooly et al., 2002; Savage et al., 2004). Typically, development ceases below a lower thermal threshold. Above it, the rate of development increases with temperature until an optimum is reached.

Above the optimal temperature, the rate rapidly decreases to zero (Campbell et al., 1974; Briere et al., 1999; Van der Have, 2002). This pattern has been attributed to the reaction rate and high temperature inactivation of a single major enzyme that drives the developmental process (Van der Have and de Jong, 1996; Van der Have, 2002; Rat­ kowsky et al., 2005); that is, the reaction rate increases monotonically with temperature while enzyme inactivation exhibits a unimodal response to temperature.

2.2.5. Survivorship and mortality The survivorship of free-living stages of auqatic organisms are likely to be affected by temperature effects on resource acquisition (Van der

Have, 2002). Thermal stress can become lethal to an aquatic organism when the temperature exceeds its thermal tolerance limit, which is determined by the interplay of its life stage, physiological condition, genetic history, and environmental influences (Cairns et al., 1975). The cumulative survivorship, especially embryonic viability, exhibits a temperature response that is inverted U-shaped rather than left skewed (Van der Have, 2002; Angilletta, 2009; Kingsolver, 2009), and per capita mortality rates exhibit a monotonic temperature response (Gillooly et al., 2001; Savage et al., 2004), this is supported by some studies that mortality rates can increase at very low or high temperatures (Morgan et al., 2001; Kyprianou et al., 2010; Wexler et al., 2011; Li et al., 2014a).

Extreme temperature-induced mortality can be explained by the oxygen limiting theory that fish have restricted ventilation rate at cold, resulting in a decline of oxygen supply to various organs, while the temperature- driven mismatch in energy demand and supply, and decrease of oxygen solubility in warm waters concomitantly challenge the survivability of the fish at extremely warm conditions (P¨ortner and Knust, 2007).

2.2.6. Fitness In ectotherms, fitness is also strongly temperature dependent: increasing temperature causes a rise in fitness up to a maximum, fol­ lowed by a rapid decline in fitness as temperature increases further (Kingsolver, 2009). This dependence provides a quantifiable metric for assessing the effects of climate warming on population viability. Since fitness is a composite trait consisting of individual components (e.g., fecundity, development, survivorship), Amarasekare and Savage (2012) also developed a mathematical framework that partitions the tempera­ ture dependence of fitness into its components of fecundity, develop­ ment, and mortality. Because the qualitative properties of the temperature responses of fitness components are robust to taxonomic and geographic variation (Gillooly et al., 2001; Gillooly et al., 2002;

Savage et al., 2004). The “hotter-is-better” hypothesis suggests a specific type of concerted change. Hotter-is-better proposes that genotypes or species with relatively high optimal temperatures (To) also have rela­ tively high maximal performance or fitness (rmax) at the optimum (Hamilton, 1973; Angilletta et al., 2010). This is based on the thermo­ dynamic argument that reaction rates of active enzymes increase with absolute temperatures, such that maximum reaction rates for species adapted to hot temperatures will be higher than those for species adapted to cold temperatures (measured at the optimal temperature for each) (Frazier et al., 2006; Kingsolver and Huey, 2008). As a result, the increase in fitness up to that optimum temperature is much slower than the decrease in fitness when environmental temperatures exceed the optimum (Deutsch et al., 2008), and the maximum potential fitnesses of adapted organisms will be greater in a warmer than in a cooler world (Kingsolver, 2009).

Temperature affects biochemical rates by altering the kinetic and free energies of biochemical reactions. For enzyme- mediated reactions, there are two components to the temperature dependence of reaction rates. First, increasing temperature increases the catalytic rate for an enzyme in its active state by increasing the kinetic energy of the system, as described by the Eyring (1935) model. The quantitative effect of temperature predicted by the Eyring model is best described using an

Arrhenius plot, relating the inverse of (absolute) temperature (T) to the reaction rate (Arrhenius 1889). The second component is the probability that the enzyme is in its active state. In general, this probability is maximal at some intermediate temperature and declines at higher and lower temperatures as a result of both reversible and irreversible enzyme inactivation (Ratkowsky et al., 2005). These two factors combine to give the thermal sensitivity of reaction rates a characteristic shape. At low temperatures, reaction rates increase linearly to geometrically with increasing temperature, reach a maximum at some “optimal” tempera­ ture, and then decrease rapidly at temperatures above the optimum. As a result, thermal sensitivity of reaction rates is strongly asymmetric at temperatures below versus above the optimum.

Remarkably, most biological rate processes at the whole-organism level, including rates of locomotion, growth, development, and fitness, exhibit the same basic form of thermal sensitivity as biochemical reac­ tion rates (Huey and Stevenson, 1979; Angilletta, 2009). As a result, models for the thermal sensitivity of biochemical reaction rates can be readily adapted to model the thermal sensitivity of organismal perfor­ mance and fitness (Ratkowsky et al., 2005). This common overall shape provides a useful means of identifying important patterns, or “modes,” of variation in thermal performance curves (TPCs) for organismal per­ formance or fitness among genotypes, populations, or species (Huey and

Kingsolver, 1989).

3. Temperature-dependent chemical toxicities (TDCT)

Climate change induced temperature variations, especially for ther­ mal extremes can have a profound implications on chemical toxicity to ectothermic organisms. Temperature-dependent chemical toxicity (TDCT) studies on wide ranges of aquatic organisms and chemicals have demonstrated that chemical toxicity and temperature varied from no relationship to negative or positive relationship (Cairns et al., 1975;

Cairns et al., 1978). Despite it is commonly reported that chemical toxicity increases with increasing temperature (i.e., Linear Model-I) (Leung et al., 2000; McConnachie and Alexander, 2004; Kwok and

Leung, 2005), non-linear function can describe the relationship between temperature and chemical toxicity more adequately with a wider range of temperatures (Angilletta, 2006; Bulte and Blouin-Demers, 2006; Bao et al., 2008). For example, chemical toxicity is found to follow a cumulated U-shape relationship and lowest at an optimal temperature (Topt) (Bao et al., 2008; Sangita et al., 2012). The inverse V-shape relationship (i.e., Model-II) between temperature and chemical toxic­ ities was also commonly observed in freshwater species (Lau et al.,

2014) and marine species (Zhou et al., 2014). Following the Model-II, chemical toxicity to aquatic organisms at a low temperature generally decreased with increasing temperature until it reached the optimal temperature, from which onwards it started to increase with rising temperature. In general, aquatic organisms living in optimal conditions are more tolerable to chemical toxicity than those living in the condi­ tions near to their thermal tolerance limits (Heugens et al., 2001; Bao et al., 2008; Li et al., 2014a).

3.1. Temperature-mediated chemical processes Chemical toxicity to aquatic organisms is not only associated with the concentration of the chemical in the water but also closely linked to its speciation and bioavailability (Bourgeault et al., 2013). Temperature

S.S.U.H. Kazmi et al.

Ecological Indicators 143 (2022) 109354 5 can also influence partition coefficient or diffusion rates chemicals (Heugens et al., 2001), leading to aggregation and precipitation, and then influences their speciation, solubility and bioavailability (Bour­ geault et al., 2013), resulting in significant alterations in their joint toxicities to an aquatic organism (Brocchi et al., 2013). The generally observed temperature-toxicity relationship was also partly thought to be related to changes in accumulation kinetics (Heugens et al., 2003).

Because the bioavailability of chemicals to aquatic species is controlled by chemical thermodynamics (i.e., chemical speciation) in the water, and then influenced by bonding interaction kinetics between ions or their complex species of the ions with the cell wall (Benda and Kouba,

1991).

It is generally accepted that a higher temperature increases the rate of uptake of chemical contaminants via increases of metabolic rate and ventilation rate of ectotherms and hence boosts bioaccumulation of the chemicals in the body tissue (Tsui and Wang, 2006; Cherkasov et al.,

2007; Schiedek et al., 2007), and ultimately leading to higher chemical toxicity at the higher temperature levels. Taken cadmium for an example, higher cadmium body concentrations at elevated temperature were reported for several species, such as Hexagenia rigida (Andres et al.,

1998), Asellus aquaticus (Vann Hattum et al., 1993), Corbicula fluminea (Graney et al., 1984), Anguilla japonica (Yang and Chen, 1996), Daphnia magna (Stuhlbacherl et al., 1993; Heugens et al., 2003), Perca fluviatilis (Edgren and Notter, 1980) and Chironomus riparius (Bervoets et al.,

1993). On the contraty, those fishes grown at lower temperatures had significantly lower osmolality than those grown at the optimum tem­ perature, which was due primarily to a significant reduction in plasma

Cl-, in combination of lower Na+/K+-ATPase activity at the extreme low temperatures. This is the expected response to the increased drinking and ion uptake rates associated with the increase in metabolism seen with increasing temperature (Ando et al., 2003). Moreover, the high test chemical concentrations could also inhibited the normal functioning of the the test speceis at the higher temperature levels, hampering a further increase in the cadmium uptake rate (Heugens et al., 2003).

Temperature may also affect physiological and biochemical state of an organism and thereby influence the partition of chemicals over the different compartments of the organism. Biochemical detoxification and elimination can also be increased with temperature, leading to a reduction of chemical toxicity. Additionally, ectotherms could enter dormancy (i.e., metabolic depression) at low temperatures leading to a reduced uptake of chemical and hence lowering toxicity (Bao et al.,

2008). In contrast to uptake rates, the temperature dependence of chemical (e.g., cadmium) elimination appears to be more complex. For instance, the depuration rates of Asiatic clams on cadmium were not altered by temperature (Inza et al., 1998). However, Burrowing mayfly nymphs eliminated cadmium rapidly when temperature was elevated (Odin et al., 1997), while a small but significant temperature effect on cadmium elimination was also reported in freshwater isopods since the metal was eliminated at 5 ◦C but not at 10 and 20 ◦C (Vann Hattum et al.,

1993). Generally, the temperature-toxicity relationship for chemicals demonstrates that elevated temperatures tend to enhance toxic effects of chemicals on organisms, which may be (partially) explained by the higher uptake rate of metals and a higher intrinsic sensitivity of organisms.

3.2. Temperature-mediated mechanisms Most freshwater creatures are ectothermic and their metabolism is highly temperature-dependent (Cherkasov et al., 2006), also making temperature a key environmental factor in controlling their physiolog­ ical performances, such as species inhabiting and acclimation (Burleson and Silva, 2011), resource acquisition (Van der Have, 2002), ventilation (Vellinger et al., 2012) and thus fitness (e.g., settlement, development, survivorship, reproduction) (Frazier et al., 2006; Angilletta, 2009;

Kingsolver, 2009; Amarasekare and Savage, 2012). Temperature can also affect various physical parameters in water bodies under different thermal dynamics. For example, the decreasing of gas solubility (e.g., oxygen) in aquatic organisms under the extreme high or low tempera­ tures would induce physiological and biological damages to aquatic ectotherms (P¨ortner, 2002a). Moreover, the lower temperature-induced changes in water viscosity can influence the swimming performance and kinematics of ectotherms (Fuiman and Batty, 1997), and then decline food ingestion (Bolton and Havenhand, 1998; Loiterton et al., 2004) and food conversion ratio (Liu et al., 2010; Abbink et al., 2012). Every aquatic organism has a thermal tolerance range (TTR), which is deter­ mined by interplay of developmental, genetic and environmental factors (Cairns et al., 1975). When temperature is higher or lower than the TTR of an organism, lethality may occur, and such a thermal stress at tem­ perature extremes may further increase the toxicity of a chemical.

Therefore, such an integrative inverted V-shape response (include

Model-I) can be typically explained by the temperature-regulated mechanisms.

Oxygen has long been known to play an important role in setting acute temperature limits of animals but characterizing the temperature limits of the physiological and biochemical pathways associated with the oxygen supply cascade. Oxygen-limited thermal tolerance (OLTT) model describes more details in physiological activities of ectotherms when exposed to various temperatures (Frederich and P¨ortner, 2000;

P¨ortner, 2001). The OLTT model suggests that aquatic ectotherms, like fishes, generally live within a confined range of temperatures where they function aerobically without displaying any sign of stress (e.g., behavioral disorder), beyond the confined range, however, the ecto­ therms would encounter a mismatch of energy demand and supply, and eventually shift to anaerobic respiration at the extreme high or low temperatures so as to increase energy supply for sustaining essential cellular and physiological functions (P¨ortner, 2010). Furthermore, thermal changes co-occurred progressive carbon dioxide accumulation would also exaggerate hypoxia due to the elevated oxygen demand on the one hand, and lower oxygen solubility at high temperatures on the other (Brewer and Peltzer, 2009; P¨ortner, 2010). When such changes in temperature and oxygen concentration are introduced, total meta­ bolism, basal metabolism and scope of activity of aquatic organisms decrease, while the frequency of locomotory acts and mechanical power decline (Svetlichny et al., 2000). Evidence showed that oxygen defi­ ciency could elicit (1) the transition to passive tolerance and associated systemic and cellular stress signals such as hormonal responses or oxidative stress; and (2) the activation of protection mechanisms (e.g., heat hock proteins) at thermal extremes (P¨ortner and Knust, 2007;

P¨ortner, 2010). Because reduction in oxygen consumption rates may be directly linked to chemical induced mucus production, structural dam­ age to gills and reduction in oxygen carrying capacity of haemocyanin (Leung et al., 2000; Morley et al., 2012). Therefore, it is easy to un­ derstand oxygen deficiency in the body tissue results in changes in growth, survival, reproduction and even population distribution and abundance under thermal stress (Perry et al., 2005; P¨ortner, 2010).

The increased bioaccumulation of chemical compounds is also bound to cause physiological discomfort or damage to organisms, and thus temperature can influence their susceptibility to chemical exposure (Cairns et al., 1975; Heugens et al., 2001). Reactive oxygen species (ROS) are normal byproducts of cellular respiration and have important roles in cell signalling and homeostasis (Cadenas, 1989). Nonetherless, during times of thermal stress, the oxygen mismatch may thus be due to physiological hypoxia (Cadenas, 1989; Matschak et al., 1995), which subsequently induces ROS and oxidative stress (Lesser, 2006; Vinagre et al., 2012; Vinagre et al., 2014). It has been well-documented that thermal stress is positively correlated with oxidative stress in aquatic ectotherms species (Dahlhoff et al., 1991; Paital and Chainy, 2014). This is further supported by the response of the oxidative stress biomarkers (e.g., SOD, CAT, GPX) which were commonly reported to be the lowest at the optimal temperature and it increased outside the speices upper and lower optimum thermal limits (Vinagre et al., 2012; Vinagre et al.,

2014), suggesting organisms suffer higher influences from high or low

S.S.U.H. Kazmi et al.

Ecological Indicators 143 (2022) 109354 6 temperatures than that from the optimum temperature. Thermal induced oxidative stress can also modify concentrations of lipid, protein and carbohydrate, leading to the changes of partition coefficients over membrane, storage lipid and body fluid (Heugens et al., 2001). Oxida­ tive stress is also known to be an important induction factor for cell apoptosis (Green and Reed, 1998; Orrenius, 2007). Previous researches demonstrated that water temperature decrease can induce ROS pro­ duction and hemocyte apoptosis (Qiu et al., 2001; Li et al., 2014b), in­ crease caspase-3 transcription and activity levels (Chang et al., 2009), cause DNA damage and lipid peroxidation (Malev et al., 2010; Vinagre et al., 2012), reduce the immune functions and resistance against pathogen infection (Le Morvan et al., 1998; Cheng et al., 2005; Chang et al., 2009). It is generally accepted that low temperatures adversely affect specific immune responses, especially the humoural response (Avtalion et al., 1970; Bly and Clem, 1992). Thus, the pathological sit­ uation in fish depends both on temperature dependent immune system regulation and on pathogen growth (Le Morvan et al., 1998).

4. Temperature dependent species sensitivity distribution (SSD)

Over the last twenty years, the chemical state of many water bodies have been improved due to the effective and precise risk mitigating strategies and measures. However, thermal stress and elevated tem­ perature have significant impacts on the aquatic environments. The elevated temperature most probably cause mortality of algal blooms or other aquatic species depends on the receiving water body (de Vries et al., 2008). Very earlier Carter et al. (1979) provided a rationale for evaluation of the biological responses induced by thermal stress. How­ ever, most of the times thermal stress coincide with various environ­ mental factors like antifouling agents, toxic biocides and hypoxia. Under these circumstances, it is problematic to evaluate the individual risk factor, thus integrating risk or multistress approach in overall one in­ dicator would be the more clear (De Zwart and Posthuma, 2005).

Therefore, the application of species sensitivity distribution (SSD) in combination with toxic and non-toxic stressors is more ideal indicator for ecological risk assessment.

Species sensitivity distribution describes the “mean sensitivity and range of sensitivity among biota” for specific type of the stressor (Aldenberg et al., 2002). This method is useful for the generic risk assessment, but also beneficial for location specific assessment if the local species incorporated (de Vries et al., 2008). Previously, the SSD was used by de Vries et al. (2008) to calculate the temperature induced mortality in aquatic environment as potential risk assessment tool of thermal stress. Their study summarized the acute exposure of organisms (50 aquatic species) that were capable of drift or swim in heated water.

Furthermore, the study revealed loss of the resident species that couldn’t sustain the warm temperature. Later on Zhou et al. (2014) focused on marine ecosystem and give a viewpoint to predict the temperature dependent chemical toxicity to marine organisms. Their study investi­ gated the temperature-acute toxicity correlation for variety of chemicals (e.g., chromium, cadmium, zinc, copper, nickel and TBT), on numerous marine ectotherms under various temperatures by two models (TDCT model I and II). However, the application of temperature dependent

SSDs on both models (TDCT model I and II), revealed that the marine water species were relatively more sensitive to the chemicals at high or low temperatures as compared to the optimal temperatures (Zhou et al.,

2014).

In the study of Mu et al. (2018) temperature and salinity based SSD was employed to predict the chemical toxicity of (i.e., Zn, Ni, Cd, Cu, Cr and Hg) on numerous communities of marine organisms. The sigmoidal logistic model on temperature-salinity based SSDs (represented by S type surfaces) demonstrated that the chemicals (metals) have high toxic potentials to the marine organisms. Furthermore, the physicochemical properties of the metals significantly affected their toxicities to the marine organisms. Both temperature and salinity actually affect the metals (chemicals) toxicities to the marine organisms and determine the slopes/shapes of SSD curves. In short, salinity affects the gradients of fitted curves while temperature influenced on horizontal positions (Mu et al., 2018). In an updated study on the application of temperature- dependent SSDs by Wang et al. (2019) reported that the thermal ex­ tremes can intensify the toxicity of chemicals (e.g., chlorpyrifos, carbaryl, mercury, copper, malathion, pentachlorophenol, and phenol) to freshwater biological communities. The temperature dependent SSDs generally showed the inverted V-shape (same as Model II) relationship along the temperature gradients. The application of temperature dependent SSDs however could be pivotal in refining the WQGs at various natural temperature ranges (Wang et al., 2019). Overall, SSD ascertain the logical standard to investigate the influence of numerous stressors or abiotic factors (e.g., temperature, salinity, pH etc.) on chemical toxicity to the aquatic organisms. However, rigorous studies combining the other stressors in one (aggregation of all stressors) would be more ideal choice to evaluate the chemical toxicity to aquatic biota and ecological risk assessment in both marine and freshwater environments.

5. Conclusion Thermal/temperature stress on aquatic organisms induce negative changes in their physiological and biochemical processes. The organ­ ism’s response to thermal extremes varies among different aquatic or­ ganisms at metabolic, hormonal and immunological levels. Higher temperature, disrupts the molecular and genetic mechanisms of organ­ isms, which leading toward abnormal individual performances. The negative biochemical responses (e.g., accumulation and release) signif­ icantly affect the organism’s adaptation, fitness, growth and develop­ ment, survivorship and reproduction activities. Furthermore, the thermal extremes can have profound implications on chemical toxicity to the aquatic organisms. Higher temperatures increases the rate of chemical contaminants uptake through increased metabolic and venti­ lation rate which subsequently boost the bioaccumulation of chemicals in the body tissues, ultimately leading to higher chemical toxicity.

Moreover, not the individual organisms are sensitive to the thermal stress, population, communities and whole ecosystem responds to the temperature extremes. This review, not only shed lights on temperature effects and temperature dependent chemical toxicity, it also provides a systematic approach to understand the drastic climate change scenario and combined thermo-chemical stress on aquatic ecosystems. However, extended and rigorous studies on domestic, regional and global levels are required to highlight the impacts of thermal stress, and devised advanced strategies to overcome this issue for sustainable aquatic environment.

CRediT authorship contribution statement Syed Shabi Ul Hassan Kazmi: Investigation, Methodology, Writing

– original draft. Yolina Yu Lin Wang: Writing – review & editing. Yan- Er Cai: Writing – review & editingZhen Wang: Conceptualization, Su­ pervision, Funding acquisition, Writing – review & editing.

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability Data will be made available on request.

S.S.U.H. Kazmi et al.

Ecological Indicators 143 (2022) 109354 7 Acknowledgements

This work research was supported by the National Natural Science

Foundation of China, China (42177264), 2020 Li Ka Shing Foundation

Cross-Disciplinary Research Grant, China (2020LKSFG03E), and Shan­ tou University Scientific Research Foundation for Talents, China (NTF19044).

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📖 中文全文 Chinese Full Text

中文

# 温度单独或联合化学物质对水生生物的影响:热化学胁迫综述

**Syed Shabi Ul Hassan Kazmi, Yolina Yu Lin Wang, Yan-Er Cai, Zhen Wang\***

广东省海洋灾害预测与防治重点实验室,广东省海洋生物技术重点实验室,汕头大学,汕头 515063,中国

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## 摘要

气候变化(全球变暖)不仅限于陆地环境的变化,也在改变着水生环境。近期研究表明,沿海水域和淡水水体均经历了持续变暖,且在本世纪内将加剧(巨大飞跃)。与此同时,错综复杂的热胁迫对水生生物构成了严重威胁。尽管关于温度对水生生物影响的文献日益丰富,科学界也逐步达成共识,但水生生物所承受的热化学胁迫在何种程度上加剧尚未得到充分阐述。本文总结了以下要点:

- 温度变化会引发生理和生物响应,包括皮质类固醇响应、代谢响应、免疫响应、热休克蛋白表达以及血淋巴参数波动。 - 温度波动引起的响应实际上归因于生物体整体水平的表现,如驯化与适应、适合度、摄食与食物转化率、生长与发育。 - 温度依赖性化学毒性(TDCT)会影响水生生物在个体、种群和群落层面的化学过程及潜在的分子/遗传机制。

此外,本综述概述了水生生物在温度单独或联合化学物质作用下的一系列响应机制。这些观察结果提供了重要证据,表明气候变化和温度变化至关重要,迫切需要在大地理尺度上仔细评估相关条件与响应。

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## 1. 引言

本世纪,气候变化(全球变暖)可能是人类对自然系统施加的最大人为干扰(Sala et al., 2000; Thomas et al., 2004)。气候变化不仅导致水温升高,还引发更频繁、更持久的寒潮和热浪。据推测,全球变暖将导致气候变化更加不可预测,极端天气事件增多,包括更大的温度波动和更频繁的极端温度事件(IPCC, 2014)。

气候变化引起的温度变化可深刻影响变温动物的生态学特征,包括其生理、生化和生态响应(Calosi et al., 2008)。变温动物的生活史表现与温度之间的关系通常以单峰热表现曲线(TPC)为特征(Huey and Stevenson, 1979),定义了最适温度(To)以及临界最低温度(CTmin)与临界最高温度(CTmax)之间的可操作温度范围。目前,这种单峰TPC已被广泛用于评估变温物种对气候变暖的敏感性(Amarasekare and Savage, 2012),以及综合适合度指标,如繁殖、发育、代谢率、适合度(Van der Have, 2002; Pörtner and Knust, 2007; Kingsolver, 2009)和进化(Huey and Kingsolver, 1989; Huey et al., 2003; Frazier et al., 2006)。

气候变化引起的温度变化,尤其是极端温度,还对个体生物的化学毒性产生深远影响,进而影响其种群大小与结构、群落的物种组成以及生态系统的结构与功能(Cairns et al., 1975; Cairns et al., 1978; Lau et al., 2014; Zhou et al., 2014)。针对多种水生生物和化学物质的温度依赖性化学毒性(TDCT)先驱研究表明,化学毒性与温度之间的关系从无相关到负相关或正相关不等,这意味着化学毒性部分或完全依赖于温度变化(Cairns et al., 1975; Cairns et al., 1978)。尽管通常报道化学毒性随温度升高而增加(线性模型,模型I)(Leung et al., 2000; McConnachie and Alexander, 2004; Kwok and Leung, 2005),但更全面的毒性研究表明,非线性函数(如倒V形模型,模型II)能更好地描述温度与化学毒性之间的关系,尤其是在极端热条件下(Heugens et al., 2003; Bao et al., 2008)。

最近,考虑到这两种模型(模型I和模型II)和自然温度变化,对以往常用的评估因子(如10)进行了重新评估,以进一步验证这些因子在水质基准(WQGs)中的应用是否能充分保护淡水和海洋生态系统(Lau et al., 2014; Zhou et al., 2014)。

由于水生生物持续暴露于包括物理(温度)和化学胁迫因子在内的环境刺激中,温度变化不仅会改变对个体水生生物的化学毒性,还可能给化学污染物的风险评估或保护水生群落的适当WQGs的推导带来偏差。因此,解决温度对化学污染物理化性质和生物响应的热效应,以及温度与化学暴露对生物响应的联合影响,具有重要性和必要性。因此,本综述重点阐述了以下三个问题:1)温度对水生生物生理和生化响应的影响;2)温度对化学过程的影响,包括化学形态、积累、循环和消除;3)温度与化学物质对生物响应的联合影响。

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## 2. 温度对水生生物的影响

### 2.1 生理和生物响应

#### 2.1.1 皮质类固醇响应

皮质醇释放等生理应激反应是简单的自主反应,仅表示活动状态,并不一定等同于痛苦和福利下降(Ashley, 2007)。皮质醇的主要功能是诱导生理变化,帮助动物保护自身免受胁迫或适应胁迫。皮质醇释放是冷应激的一个敏感指标。例如,已发现皮质醇水平与多种鱼类的温度下降幅度呈正相关,包括虹鳟(*Oncorhynchus mykiss*)(Barton and Peter, 1982)、鲑鱼(*Salmo salar*)(Skjervold et al., 2001; Hyvärinen et al., 2004)、罗非鱼(*Oreochromis aureus*)(Chen et al., 2002)、黄鲈(*Perca flavescens*)(Jentoft et al., 2002)和鲤鱼(*Cyprinus carpio*)(Jaxion-Harm and Ladich, 2014)。然而,持续高水平的皮质醇可能通过调节代谢、离子调节、免疫、生长和繁殖等多种系统而产生不利影响,最终影响动物健康(Houghton and Matthews, 1990)。在某些情况下,本身具有慢性胁迫性的应激修饰因子(如水质差或毒物)实际上会加剧(Barton and Peter, 1982)或减弱对应激源的皮质醇响应。例如,在虹鳟(*Salmo gairdneri*)中,皮质醇不仅抑制卵巢生长,还会使性别比偏向雄性方向(van den Hurk and van Oordt, 1985)。

#### 2.1.2 热休克蛋白(HSPs)

细胞在热胁迫下激活的分子响应之一是热休克蛋白(HSPs)响应,这是一种基因激活事件,发生在细胞应对异常、胁迫性的高温或低温时(Hofmann, 2005)。HSPs在热胁迫期间保护蛋白质、膜和其他细胞组分,并促进胁迫事件后受损蛋白质的修复或降解(Parsell and Lindquist, 1994)。重要的是,虽然HSPs因其在温度急性升高时上调而得名(Lindquist, 1980),但广泛的研究使人们对HSPs的调控和作用机制有了详细了解(Feder and Hofmann, 1999)。HSPs(如HSP70)的表达有随温度变异性增加而升高的趋势(Arias et al., 2011; Folguera et al., 2011)。在低温下,HSP70的合成和表达在冰点以下也会发生。因为在此条件下,生物体的新陈代谢受到抑制,无法激活合成伴侣蛋白所需的生理机制,这主要发生在恢复期。这表明HSP70表达增强与后续极端事件自我保护能力的提高之间存在密切关系(Krebs and Bettencourt, 1999; Chown and Nicholson, 2004)。

#### 2.1.3 代谢响应

暴露于较高水温期间,血淋巴中的葡萄糖浓度升高(Lorenzon et al., 2007; Malev et al., 2010)。这表明产生更多葡萄糖并作为能量补充,以满足在低氧可用性胁迫条件下增加的代谢需求(Wendelaar Bonga, 1997),乳酸的相同温度相关响应也支持这一点——乳酸随温度升高导致的能量使用增加而增加(Durand et al., 2000; Ridgway et al., 2006; Lorenzon et al., 2007)。在不同温度下驯化的*Maia squinado*血淋巴葡萄糖结果表明,低温下血淋巴中葡萄糖浓度降低,而在高温下短期驯化导致血淋巴中葡萄糖水平升高(Durand et al., 2000)。

#### 2.1.4 血淋巴参数

血细胞在水生生物的生理和免疫防御中发挥着重要作用(Johansson et al., 2000)。循环血细胞的损失和损伤会降低免疫力,增加对病原体的易感性,甚至危及生存(Cheng et al., 2005)。发现暴露于高温期间血细胞总数(THC)增加,以增强对热应激的免疫力(Liu et al., 2010; Malev et al., 2010)。血红蛋白(Hb)作为环境氧气可用性与有氧代谢之间的直接联系,在水生无脊椎动物中也遵循温度依赖性模式(Lamkemeyer et al., 2003; Seidl et al., 2005; Zeis et al., 2013)。在临界阈值以下,水蚤中Hb的诱导是胁迫特异性稳态响应的一个例子(Kültz, 2005)。这种第二道应激防线可恢复细胞氧条件。然而,其他作者未在脊椎动物(如鱼类)中观察到这一特征,表明这一属性并非异温动物所特有,而可能是对替代进化激励的响应(Clark et al., 2010; Muyssen et al., 2010)。

#### 2.1.5 免疫响应

鱼类对疾病的易感性部分取决于其环境,特别是水温(Le Morvan et al., 1998),因为其整个生理机能(包括免疫功能)都受环境温度影响(Fry, 1967)。例如,大多数传染性疾病,如鲤春病毒血症(*Cyprinus carpio*),发生在较低的环境温度下。因此,鱼类的病理状况取决于温度依赖性免疫系统调节和病原体生长(Le Morvan et al., 1998)。通常报道低温对多种鱼类的细胞和体液特异性免疫响应均产生不利影响(Bly and Clem, 1992)。低温可对T辅助细胞介导的特异性免疫响应产生不利影响。相反,如果在高温下建立了免疫记忆,则可在低温下引发二次响应。特异性免疫响应,特别是体液响应,在低温下通过抑制初级抗体响应而受到抑制(Avtalion et al., 1970; Bly and Clem, 1992)。相反,较高温度可增加血浆IgM浓度,但在热处理响应中溶菌酶活性和补体杀菌活性呈下降趋势(Jokinen et al., 2011)。

### 2.2 生物体整体水平表现

#### 2.2.1 驯化与适应

尽管水生变温动物的生理过程通常在狭窄的温度范围内最佳运行,但大量文献表明大多数变温动物可以调整或驯化以适应环境温度的变化(Huey and Berrington, 1996; Stillman, 2003)。在遗传限度内,生物体的充分驯化可以减轻对新热环境的应激反应,从而扩展耐热边界(Cairns et al., 1975; Cairns et al., 1978)。由于短期暴露于冷或热极端条件对变温动物至关重要(Bokhorst et al., 2008),它们必须调整其生理和生化响应以克服这种胁迫性热环境。

热休克蛋白(HSPs)等应激蛋白可被诱导以保护细胞结构(如DNA)并修复受损组分,通过这种方式,变温动物可以延长其存活时间,尽管是以时间限制的方式(Pörtner, 2002b)。Liu et al.(2010)表明,蒽醌提取物可提高血淋巴总蛋白含量、氮一氧化浓度和溶菌酶活性,帮助虾抵抗高温胁迫。此外,Lubzens et al.(1995)发现轮虫(*Brachionus plicatilis*)的驯化期与至少一种特异性蛋白(免疫隔离)的合成和脂质(二十碳五烯酸)的积累有关,这支持了在驯化期间对低温存活的特异性适应假说。

然而,驯化通常被认为只是部分的,因此生理(和功能)过程并未完全与温度解耦(Kingsolver and Huey, 1998)。快速和渐进的温度变化可使驯化现象最小化(Burleson and Silva, 2011),并涉及耐热阈值的移动(Frederich and Pörtner, 2000)。例如,普通蛙(*Rana temporaria*)在低温(低于5°C)下未表现出繁殖方面的行为适应(Muir et al., 2014)。

#### 2.2.2 摄食与食物转化率(FCR)

温度引起的水粘度变化对物种活动(如游泳)的影响在决定食物摄取和食物转化率(FCR)方面起着重要作用(Loiterton et al., 2004),特别是对于小型水生变温动物。已知环境温度通过反向影响水的动态粘度对水生变温动物产生机械效应(Vogel, 1994)。例如,Bolton and Havenhand(1998)证明,水温降低的生理和粘度诱导组分均可显著减少*Galeolaria caespitosa*摄入的微球数量。同样,Loiterton et al.(2004)证明,*D. galeata*的摄入率在10°C时比25°C时低50%,这是由于粘度增加和温度降低的综合效应,而仅粘度就占FCR下降的61%。Lagergren et al.(2000)还表明,由于与较高粘度相关的阻力增加,*Eubosmina*中捕食者防御的流体动力学成本在低温下增加。

证据还表明,水生个体的生长在最适温度下得到优化,结合最大食物摄入量和最佳FCR(Abbink et al., 2012; Vellinger et al., 2012)。已报道在极端水温下饲料利用效率降低,涉及澳洲尖吻鲈(*Lates calcarifer*)(Bermudes et al., 2010)、狼鱼(*Anarhichas lupus*)(Imsland et al., 2006)和欧洲海鲈(*Dicentrarchus labrax*)(Person-Le Ruyet et al., 2004)。这与另一项关于黄尾鰤的研究一致,该研究表明在温水(17°C至22°C)中FCR明显优于冷水(14°C至17°C)(Moran et al., 2009)。这可解释为消化酶活性在一定温度范围内随温度升高而增加,但在较高温度下通过时间缩短可能减少食物与酶作用的暴露(Harwood, 1979; McCarthy et al., 1999)。

#### 2.2.3 繁殖

繁殖性状(如卵、孵化)被认为比其他性状对应激更敏感,因此在估计热胁迫的适合度效应时应将其纳入(Jørgensen et al., 2006)。此外,繁殖过程通常更早地受到温度变化的影响,即以比影响发育和存活更轻度的条件受到影响(Fasolo and Krebs, 2004)。先前的研究还显示,由反应速率理论(即酶动力学)预测的繁殖表现具有更对称的温度响应(Carriere and Boivin, 1997; Dannon et al., 2010; Amarasekare and Savage, 2012),并结合基于负反馈途径(如激素调节)的调节过程(Nijhout, 1994)。多项研究调查了热休克对寿命和繁殖力的负面影响(Rinehart et al., 2000)。热或冷休克还可对雌性的卵母细胞和卵巢发育造成损伤,导致产卵量减少(Rinehart et al., 2000; Castro-Longoria, 2003)。此外,热休克可由于对睾丸和精子的直接损伤而降低雄性生育力(Scott et al., 1997; Nguyen et al., 2013)。此外,孵化成功率也受到极端高温或低温的不利影响(Holste and Peck, 2006; Hansen et al., 2010; Cruz et al., 2013),导致存活者减少,从而降低水生生物的丰度。这可能是由于膜通透性降低、偶联酶反应失衡以及酶蛋白质动力学和失活所施加的限制(Rosa et al., 2012)。

#### 2.2.4 生长与发育

水温是影响水生变温动物生长和发育的主要环境因子之一(Brett, 1979)。最适温度下降的个体发育转变在大多数变温动物中很常见,并已针对多种海洋鱼类进行了描述,包括大西洋鳕(*G. morhua*)(Lafrance et al., 2005)、大菱鲆(*Scophthalmus maximus*)(Imsland et al., 1996)、大西洋庸鲽(*Hippoglossus hippoglossus*)(Hallaråker et al., 1995)、欧鲽(*Pleuronectes platessa*)(Fonds et al., 1992)和黄尾鰤(*Seriola lalandi*)(Pirozzi and Booth, 2009; Abbink et al., 2012)。与最适温度相比,鱼类在极端温度下的生长降低(即倒V形模型II)。这种抛物线型温度响应是所有物种的典型特征,可以解释为在如此高温下食物摄入显著减少加上能量需求增加是导致鱼类在极端高温下生长表现差的主要因素(Imsland et al., 1996; Peck et al., 2002; Bermudes et al., 2010)。相反,食欲减退被认为是低温下生长抑制的直接原因(Ibarz et al., 2005)。此外,鱼类的心率和血液循环会受到限制,导致维持基本细胞功能的氧气和能量供应受限,这种条件迫使鱼类转向无氧呼吸以获取更多能量(Pörtner, 2002a),因此在极端低温下生长表现较低。

先前的研究还表明,物种的发育速率表现出与左偏倒V形模式最一致的温度响应(Sharpe and DeMichele, 1977; Huey and Berrigan, 2001; Gillooly et al., 2002; Savage et al., 2004)。通常,发育在较低热阈值以下停止。高于此阈值,发育速率随温度升高而增加,直到达到最适温度。在最适温度以上,速率迅速降至零(Campbell et al., 1974; Briere et al., 1999; Van der Have, 2002)。这种模式归因于驱动发育过程的单一主要酶的反应速率和高温失活(Van der Have and de Jong, 1996; Van der Have, 2002; Ratkowsky et al., 2005);即反应速率随温度单调增加,而酶失活对温度表现出单峰响应。

#### 2.2.5 存活与死亡

水生生物自由生活阶段的存活可能受到温度对资源获取的影响(Van der Have, 2002)。当温度超过其耐热极限时,热胁迫可能对水生生物致死,耐热极限由其生命阶段、生理状况、遗传历史和环境影响的相互作用决定(Cairns et al., 1975)。累积存活率,特别是胚胎活力,表现出倒U形而非左偏的温度响应(Van der Have, 2002; Angilletta, 2009; Kingsolver, 2009),而人均死亡率表现出单调温度响应(Gillooly et al., 2001; Savage et al., 2004),一些研究支持死亡率在极低或极高温度下可能增加(Morgan et al., 2001; Kyprianou et al., 2010; Wexler et al., 2011; Li et al., 2014a)。极端温度诱导的死亡可以用氧气限制理论来解释:鱼类在冷水中通气率受限,导致各器官氧气供应下降,而温度驱动的能量供需不匹配以及温暖水域中氧气溶解度降低同时挑战鱼类在极暖条件下的存活能力(Pörtner and Knust, 2007)。

#### 2.2.6 适合度

在变温动物中,适合度也强烈依赖于温度:温度升高导致适合度上升至最大值,随后随着温度进一步升高,适合度迅速下降(Kingsolver, 2009)。这种依赖性为评估气候变暖对种群活力的影响提供了可量化的指标。由于适合度是由个体组分(如繁殖力、发育、存活)组成的复合性状,Amarasekare and Savage(2012)还开发了一个数学框架,将适合度的温度依赖性分解为其繁殖力、发育和死亡率组分。由于适合度组分温度响应的稳健性质不受分类学和地理变异的影响(Gillooly et al., 2001; Gillooly et al., 2002; Savage et al., 2004)。"越热越好"假说提出了一种特定类型的协同变化。越热越好假说认为,具有相对较高最适温度(To)的基因型或物种在最适温度下也具有相对较高的最大表现或适合度(rmax)(Hamilton, 1973; Angilletta et al., 2010)。这是基于热力学论证:活性酶的反应速率随绝对温度增加而增加,因此适应高温的物种的最大反应速率将高于适应低温的物种(在每个物种的最适温度下测量)(Frazier et al., 2006; Kingsolver and Huey, 2008)。因此,适合度向该最适温度的上升速度远慢于环境温度超过最适温度时适合度的下降速度(Deutsch et al., 2008),且适应生物在较暖世界中的最大潜在适合度将大于在较冷世界中的最大潜在适合度(Kingsolver, 2009)。

温度通过改变生化反应的自由能来影响生化反应速率。对于酶介导的反应,反应速率的温度依赖性有两个组分。首先,温度升高通过增加系统的动能来提高活性状态酶的催化速率,如Eyring(1935)模型所述。Eyring模型预测的温度定量效应最好用Arrhenius图来描述,将(绝对)温度(T)的倒数与反应速率相关联(Arrhenius 1889)。第二个组分是酶处于活性状态的概率。通常,该概率在某个中间温度下最大,并在较高和较低温度下由于可逆和不可逆酶失活而降低(Ratkowsky et al., 2005)。这两个因素共同赋予反应速率的热敏感性以特征性形状。在低温下,反应速率随温度线性至几何增加,在某个"最适"温度下达到最大值,然后在最适温度以上迅速降低。因此,反应速率的热敏感性在最适温度以下与以上强烈不对称。

值得注意的是,在生物体整体水平上,大多数生物速率过程,包括运动、生长、发育和适合度的速率,表现出与生化反应速率基本相同的热敏感性形式(Huey and Stevenson, 1979; Angilletta, 2009)。因此,生化反应速率的热敏感性模型可以很容易地适用于模拟生物体表现和适合度的热敏感性(Ratkowsky et al., 2005)。这种共同的总体形状为识别基因型、种群或物种间生物体表现或适合度的热表现曲线(TPCs)变异的重要模式或"模式"提供了有用的手段(Huey and Kingsolver, 1989)。

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## 3. 温度依赖性化学毒性(TDCT)

气候变化引起的温度变化,尤其是极端温度,可对变温生物的化学毒性产生深远影响。针对多种水生生物和化学物质的温度依赖性化学毒性(TDCT)研究表明,化学毒性与温度之间的关系从无相关到负相关或正相关不等(Cairns et al., 1975; Cairns et al., 1978)。尽管通常报道化学毒性随温度升高而增加(即线性模型I)(Leung et al., 2000; McConnachie and Alexander, 2004; Kwok and Leung, 2005),但非线性函数能在更广泛的温度范围内更充分地描述温度与化学毒性之间的关系(Angilletta, 2006; Bulte and Blouin-Demers, 2006; Bao et al., 2008)。例如,发现化学毒性遵循累积U形关系,在最适温度(Topt)下最低(Bao et al., 2008; Sangita et al., 2012)。温度与化学毒性之间的倒V形关系(即模型II)在淡水物种(Lau et al., 2014)和海洋物种(Zhou et al., 2014)中也普遍观察到。根据模型II,在低温下水生生物的化学毒性通常随温度升高而降低,直到达到最适温度,此后开始随温度升高而增加。一般来说,生活在最适条件下的水生生物对化学毒性的耐受性高于生活在接近其耐热极限条件下的水生生物(Heugens et al., 2001; Bao et al., 2008; Li et al., 2014a)。

### 3.1 温度介导的化学过程

水生生物的化学毒性不仅与水中化学物质的浓度有关,还与其形态和生物利用度密切相关(Bourgeault et al., 2013)。温度还可影响化学物质的分配系数或扩散速率(Heugens et al., 2001),导致聚集和沉淀,进而影响其形态、溶解度和生物利用度(Bourgeault et al., 2013),从而显著改变其对水生生物的联合毒性(Brocchi et al., 2013)。通常观察到的温度-毒性关系也被认为部分与积累动力学的变化有关(Heugens et al., 2003)。因为化学物质对水生生物的生物利用度受水中化学热力学(即化学形态)控制,然后受离子或其复合物种与细胞壁之间的键合相互作用动力学影响(Benda and Kouba, 1991)。

人们普遍认为,较高的温度通过增加变温动物的代谢率和通气率来提高化学污染物的摄取速率,从而促进化学物质在身体组织中的生物累积(Tsui and Wang, 2006; Cherkasov et al., 2007; Schiedek et al., 2007),最终导致在较高温度水平下化学毒性更高。以镉为例,在升高的温度下,多种物种的体内镉浓度较高,如*Hexagenia rigida*(Andres et al., 1998)、*Asellus aquaticus*(Vann Hattum et al., 1993)、*Corbicula fluminea*(Graney et al., 1984)、*Anguilla japonica*(Yang and Chen, 1996)、*Daphnia magna*(Stuhlbacherl et al., 1993; Heugens et al., 2003)、*Perca fluviatilis*(Edgren and Notter, 1980)和*Chironomus riparius*(Bervoets et al., 1993)。相反,在较低温度下生长的鱼类的渗透压显著低于在最适温度下生长的鱼类,这主要是由于血浆Cl⁻显著减少,加上在极端低温下Na⁺/K⁺-ATP酶活性降低。这是对与代谢增加相关的饮水和离子摄取率增加的预期响应(Ando et al., 2003)。此外,高测试化学物质浓度也可能抑制测试物种在较高温度水平下的正常功能,阻碍镉摄取速率的进一步增加(Heugens et al., 2003)。

温度还可能影响生物体的生理和生化状态,从而影响化学物质在生物体不同区室中的分配。生化解毒和消除也可随温度增加而增加,导致化学毒性降低。此外,变温动物在低温下可能进入休眠(即代谢抑制),导致化学物质摄取减少,从而降低毒性(Bao et al., 2008)。与摄取速率相反,化学物质(如镉)消除的温度依赖性似乎更为复杂。例如,亚洲蛤的镉净化速率不受温度影响(Inza et al., 1998)。然而,穴居蜉蝣若虫在温度升高时迅速消除镉(Odin et al., 1997),而在淡水等足类动物中也报道了镉消除的微小但显著的温度效应,因为金属在5°C下被消除,但在10°C和20°C下未被消除(Vann Hattum et al., 1993)。通常,化学物质的温度-毒性关系表明,升高的温度往往会增强化学物质对生物的毒性效应,这可以(部分)用金属的较高摄取速率和生物体的较高内在敏感性来解释。

### 3.2 温度介导的机制

大多数淡水生物是变温动物,其代谢高度依赖于温度(Cherkasov et al., 2006),这也使温度成为控制其生理表现的关键环境因子,如物种栖息和驯化(Burleson and Silva, 2011)、资源获取(Van der Have, 2002)、通气(Vellinger et al., 2012)以及适合定殖、发育、存活、繁殖)(Frazier et al., 2006; Angilletta, 2009; Kingsolver, 2009; Amarasekare and Savage, 2012)。温度还可影响不同热动力学下水体中的各种物理参数。例如,在极端高温或低温下,水生生物中气体(如氧气)溶解度降低会引起水生变温动物的生理和生物损伤(Pörtner, 2002a)。此外,较低温度引起的水粘度变化可影响变温动物的运动性能和运动学(Fuiman and Batty, 1997),进而降低食物摄入(Bolton and Havenhand, 1998; Loiterton et al., 2004)和食物转化率(Liu et al., 2010; Abbink et al., 2012)。每种水生生物都有一个耐热范围(TTR),由发育、遗传和环境因子的相互作用决定(Cairns et al., 1975)。当温度高于或低于生物的TTR时,可能发生死亡,而这种极端温度下的热胁迫可能进一步增加化学物质的毒性。因此,这种综合倒V形响应(包括模型I)通常可以用温度调节机制来解释。

氧气长期以来被认为在设定动物的急性温度极限中起重要作用,但表征与氧气供应级联相关的生理和生化途径的温度极限。氧气限制热耐受(OLTT)模型更详细地描述了变温动物暴露于各种温度时的生理活动(Frederich and Pörtner, 2000; Pörtner, 2001)。OLTT模型表明,水生变温动物(如鱼类)通常生活在有限的温度范围内,在此范围内它们进行有氧功能而不显示任何应激迹象(如行为异常),然而,超出此有限范围,变温动物将遇到能量供需不匹配,最终在极端高温或低温下转向无氧呼吸,以增加能量供应来维持基本细胞和生理功能(Pörtner, 2010)。此外,热变化同时发生的渐进二氧化碳积累也会因一方面氧气需求增加另一方面高温下氧气溶解度降低而加剧缺氧(Brewer and Peltzer, 2009; Pörtner, 2010)。当引入温度和氧浓度的这些变化时,水生生物的总代谢、基础代谢和活动范围下降,而运动动作的频率和机械功率降低(Svetlichny et al., 2000)。证据表明,氧气缺乏可引发(1)向被动耐受的转变以及相关的系统和细胞应激信号,如激素响应或氧化应激;和(2)在热极端下保护机制(如热休克蛋白)的激活(Pörtner and Knust, 2007; Pörtner, 2010)。因为氧气消耗率的降低可能与化学物质诱导的粘液产生、鳃的结构损伤和血蓝蛋白携氧能力降低直接相关(Leung et al., 2000; Morley et al., 2012)。因此,很容易理解体内组织中的氧气缺乏会导致热胁迫下生长、存活、繁殖甚至种群分布和丰度的变化(Perry et al., 2005; Pörtner, 2010)。

化学化合物增加的生物累积也必然会对生物体造成生理不适或损伤,因此温度可影响其对化学暴露的易感性(Cairns et al., 1975; Heugens et al., 2001)。活性氧(ROS)是细胞呼吸的正常副产物,在细胞信号传导和稳态中发挥重要作用(Cadenas, 1989)。然而,在热胁迫期间,氧气不匹配可能是由于生理性缺氧(Cadenas, 1989; Matschak et al., 1995),随后诱导ROS和氧化应激(Lesser, 2006; Vinagre et al., 2012; Vinagre et al., 2014)。已有充分文献记载,在水生变温动物物种中,热胁迫与氧化应激呈正相关(Dahlhoff et al., 1991; Paital and Chainy, 2014)。氧化应激生物标志物(如SOD、CAT、GPX)的响应进一步支持了这一点,这些生物标志物通常在最适温度下最低,而在物种上下最适热限之外增加(Vinagre et al., 2012; Vinagre et al., 2014),表明生物体受到高温或低温的影响大于最适温度的影响。热诱导的氧化应激还可改变脂质、蛋白质和碳水化合物的浓度,导致膜、储存脂质和体液的分配系数发生变化(Heugens et al., 2001)。氧化应激也是细胞凋亡的重要诱导因子(Green and Reed, 1998; Orrenius, 2007)。先前的研究表明,水温降低可诱导ROS产生和血细胞凋亡(Qiu et al., 2001; Li et al., 2014b),增加caspase-3转录和活性水平(Chang et al., 2009),引起DNA损伤和脂质过氧化(Malev et al., 2010; Vinagre et al., 2012),降低免疫功能和对病原体感染的抵抗力(Le Morvan et al., 1998; Cheng et al., 2005; Chang et al., 2009)。人们普遍认为,低温对特异性免疫响应,特别是体液响应产生不利影响(Avtalion et al., 1970; Bly and Clem, 1992)。因此,鱼类的病理状况取决于温度依赖性免疫系统调节和病原体生长(Le Morvan et al., 1998)。

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## 4. 温度依赖性物种敏感性分布(SSD)

过去二十年来,由于有效和精确的风险缓解策略和措施,许多水体的化学状况得到了改善。然而,热胁迫和温度升高对水生环境有重大影响。温度升高最可能导致藻类或其他水生生物的死亡,具体取决于受纳水体(de Vries et al., 2008)。很早以前,Carter et al.(1979)为评估热胁迫诱导的生物响应提供了理论依据。然而,大多数时候热胁迫与各种环境因素同时发生,如防污剂、有毒杀菌剂和缺氧。在这些情况下,评估单个风险因子是有问题的,因此将风险或多胁迫方法整合到一个总体指标中会更加清晰(De Zwart and Posthuma, 2005)。因此,物种敏感性分布(SSD)与毒性和非毒性胁迫因子的结合是生态风险评估更理想的指标。

物种敏感性分布描述了"生物群对特定类型胁迫因子的平均敏感性和敏感性范围"(Aldenberg et al., 2002)。该方法对通用风险评估有用,但如果纳入本地物种,对特定地点的评估也有益(de Vries et al., 2008)。此前,de Vries et al.(2008)使用SSD计算水生环境中温度诱导的死亡率,作为热胁迫的潜在风险评估工具。他们的研究总结了能够漂流或游泳的生物(50种水生物种)的急性暴露。此外,研究揭示了无法维持温暖温度的本地物种的丧失。后来,Zhou et al.(2014)关注海洋生态系统,提出了预测温度依赖性化学毒性对海洋生物影响的观点。他们的研究通过两种模型(TDCT模型I和II)调查了多种化学物质(如铬、镉、锌、铜、镍和TBT)在多种海洋变温动物中在不同温度下的温度-急性毒性相关性。然而,温度依赖性SSD在两种模型(TDCT模型I和II)上的应用表明,与最适温度相比,海洋水生物种在高温或低温下对化学物质相对更敏感(Zhou et al., 2014)。

在Mu et al.(2018)的研究中,采用基于温度和盐度的SSD来预测化学物质(即Zn、Ni、Cd、Cu、Cr和Hg)对海洋生物群落的毒性。基于温度和盐度的SSD上的S形逻辑模型(由S型表面表示)表明,化学物质(金属)对海洋生物具有高毒性潜力。此外,金属的理化性质显著影响其对海洋生物的毒性。温度和盐度实际上影响金属(化学物质)对海洋生物的毒性,并决定SSD曲线的斜率/形状。简言之,盐度影响拟合曲线的梯度,而温度影响水平位置(Mu et al., 2018)。在Wang et al.(2019)关于温度依赖性SSD应用的更新研究中,报道了热极端可加剧化学物质(如毒死蜱、西维因、汞、铜、马拉硫磷、五氯苯酚和酚)对淡水生物群落的毒性。温度依赖性SSD通常沿温度梯度显示倒V形(与模型II相同)关系。然而,温度依赖性SSD的应用可能对于在各种自然温度范围内完善WQGs至关重要(Wang et al., 2019)。总体而言,SSD确定了一个逻辑标准,用于调查多种胁迫因子或非生物因子(如温度、盐度、pH等)对水生生物化学毒性的影响。然而,将其他胁迫因子结合在一个(所有胁迫因子的聚合)中的严格研究将是评估水生生物毒性和淡水和海洋环境中生态风险评估的更理想选择。

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## 5. 结论

水生生物的热/温度胁迫会诱导其生理和生化过程发生负面变化。生物体对热极端条件的响应在不同水生生物的新陈代谢、激素和免疫水平上存在差异。较高温度会破坏生物体的分子和遗传机制,导致个体表现异常。负面生化响应(如积累和释放)显著影响生物体的适应、适合度、生长和发育、存活和繁殖活动。此外,热极端可对水生生物的化学毒性产生深远影响。较高温度通过增加代谢和通气速率来提高化学污染物的摄取速率,从而促进化学物质在身体组织中的生物累积,最终导致更高的化学毒性。此外,不仅个体生物对热敏感,种群、群落和整个生态系统也对温度极端作出响应。本综述不仅阐明了温度效应和温度依赖性化学毒性,还提供了一种系统方法来理解剧烈气候变化情景和水生生态系统中的联合热化学胁迫。然而,需要在地方、区域和全球层面开展广泛而严格的研究,以突出热胁迫的影响,并制定先进策略来克服这一问题,实现可持续的水生环境。

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**作者贡献声明**

Syed Shabi Ul Hassan Kazmi:调查、方法论、撰写——初稿。Yolina Yu Lin Wang:撰写——审阅与编辑。Yan-Er Cai:撰写——审阅与编辑。Zhen Wang:概念化、监督、资金获取、撰写——审阅与编辑。

**利益冲突声明**

作者声明,他们没有已知的可能影响本文所述工作的竞争性财务利益或个人关系。

**数据可用性声明**

数据可根据要求提供。

**致谢**

本研究得到中国国家自然科学基金(42177264)、2020年李嘉诚基金会跨学科研究基金(2020LKSFG03E)和汕头大学科研人才基金(NTF19044)的支持。