东方蝾螈幼体热耐受性和游泳表现的热驯化响应

陆洪良, 耿 军, 徐 卫, 平 骏, 张永普,*

1 杭州师范大学生命与环境科学学院, 杭州 310036 2 温州大学生命与环境科学学院, 温州 325035

东方蝾螈幼体热耐受性和游泳表现的热驯化响应

陆洪良1, 耿 军1, 徐 卫1, 平 骏2, 张永普2,*

1 杭州师范大学生命与环境科学学院, 杭州 310036 2 温州大学生命与环境科学学院, 温州 325035

特定物种的热驯化能力决定着其是否能成功耐受环境温度的改变,在应对未来气候变暖的趋势中扮演重要角色。为评估有尾类两栖动物的热驯化反应,在3个恒定水温(15、20℃和25℃)中驯化东方蝾螈(Cynopsorientalis)幼体4周,测定驯化后幼体在不同测试温度下的运动(游泳)表现、临界低温(CTMin)与临界高温(CTMax)。结果显示：驯化与测试温度均显著影响蝾螈的游泳速度；驯化温度亦影响蝾螈的CTMin和CTMax,但不影响可耐受温度范围(TRR)。驯化与测试温度的交互作用对蝾螈泳速的影响显著,表明驯化温度可改变其游泳表现的热敏感性。经某一温度驯化后蝾螈泳速似乎在相同测试温度下表现最好,该结果可能支持驯化有益假说。CTMin和CTMax随驯化温度的升高而增加,表明：低温驯化可提高动物抗低温能力,而高温驯化提高其抗高温能力。两栖类动物热耐受性与运动表现热驯化反应的种间变异可能与栖息地热环境的差异有关。

东方蝾螈；热驯化；热耐受能力；运动表现；驯化有益假说

在众多影响外温动物生理与行为表现的环境因子中,温度效应无疑是最明显的[1-2]。环境温度通过改变外温动物的体温可影响其生理与行为表现(例如,运动、摄食、同化、生长、免疫功能等)[2]。任何一种变温动物对外界环境温度的耐受能力有限。较长时间在过高或过低的热环境中暴露会使外温动物损伤甚至死亡[2-3]。使动物无法逃离致其死亡状态的极端温度上下限被分别定义为临界高温(CTMax)和临界低温 (CTMin)[2, 4]。在可耐受温度范围内,任何生理与行为表现随体温变化的趋势可用热功能曲线表示：体温从临界低温上升到最适水平,功能表现逐渐增加；从最适水平上升到临界高温,功能表现陡然下降[1]。外温动物的热耐受能力和功能表现的热敏感性存在显著的种内和种间差异,这种差异与其分布范围、扩散能力等方面相关联。例如,分布范围广的种类通常热耐受范围相对较大、热敏感性较低[2-3]。事实上,外温动物的热耐受能力和功能表现的热敏感性可以看成是长期适应热环境变异所做出的反应。当迁徙到新生境中,动物为适应当地热环境使某些生理表现(例如,肌肉收缩特性、酶代谢活性)逐渐发生变化,由此热耐受能力和功能表现的热敏感性也随之发生偏移。这一生理变化过程也被称为热驯化[5]。

外温动物的热驯化反应决定其应对周围环境热变异(包括未来气候变化等)的能力[6-8]。热驯化会改变变温动物的热耐受性,但其影响在不同种类中存在差异[9-12]。例如,有些种类在较低温度下驯化具有较大热耐受范围[13-14],而一些种类则在中等温度下驯化具有较大的热耐受范围[12,15-16]。动物的运动表现与其适合度紧密关联,在进化生物学研究中是被测量最为频繁的一个特征[17-18]。热驯化同样会影响外温动物的运动表现,并存在显著的种间差异[19-20]。例如,许多鱼类和蛙类的蝌蚪在不同水温下驯化,游泳速度的热敏感性发生显著变化,但是这种效应在发生变态后的蛙类中并不明显[20-23]。已有多种假说被提出来用于解释外温动物运动表现的热驯化反应。例如,驯化有益假说认为,经特定温度驯化的动物在该温度条件下会增强其功能表现或适合度[18,24]。虽然该假说获得了一些实验数据的支持,但其普遍适用性仍存在争议。一些研究表明：在低温、中等甚至高温下驯化的动物比在其它温度中驯化具有较好的功能表现或较高的适合度[24-26]。热驯化的生理与行为反应在鱼类及无尾两栖类中已有较多报道,但有尾两栖类及陆生脊椎动物并不多见[27-29]。

东方蝾螈(Cynopsorientalis)是一种分布于中国中部及东部的有尾两栖类动物,主要栖息于池塘、水田、流速较缓的山间溪流等水域。有关东方蝾螈的研究涉及胚胎发育、形态、繁殖等内容,但体温调节与功能表现方面未见报道。野外自然环境中,水温超过10℃东方蝾螈开始活动,3—7月雌体产卵,15—25℃是其适宜的生长温度[30]。本文以3个恒定驯化水温(15、20和25℃)代表适宜东方蝾螈生长的较低、中等以及较高水温,测定其临界高、低温以及不同体温下的运动表现,以评价热驯化对该种动物热生理特征的影响,旨在探讨热驯化是否会改变东方蝾螈的运动表现和热耐受能力？两栖类动物运动表现及热耐受能力的驯化反应是否存在种间差异？

1 材料与方法

1.1 动物收集与处理

实验用东方蝾螈为变态后幼体(N= 48),2014年6月中旬购自杭州钱江花鸟市场,随后运至杭州师范大学两栖爬行动物实验室。蝾螈随机放在3个塑料整理箱(60 cm × 45 cm × 35 cm)中,在实验室条件下适应性养殖3天。用数显游标卡尺(0.01mm)测定蝾螈体长(吻端至泄殖腔孔前缘间距),体长范围为32—43mm,随后将个体随机分为3组(15℃: (40.50.8) mm,N= 25; 20℃: (40.60.7) mm,N=9; 25℃: (38.90.9) mm,N=14)。将动物个体单独放入已标记的塑料盒(15 cm × 10 cm × 8 cm)中,盒底加入曝晒过自来水,水深约1.5cm,上覆打有小孔的盖子以保证空气流通。将装有蝾螈的塑料盒分别置于温度预先设置为(150.5)℃、(200.5)℃和(250.5)℃的人工气候箱(宁波莱福科技有限公司)中,每隔1d投喂食物(碎鱼肉)1次并换水。气候箱内光照周期设为13L∶11D,驯化时间为4周。

1.2 运动表现的测定

蝾螈热驯化4周后,选取无损伤、无病态的活跃个体用于随机测定3个测试温度(体温)条件下的运动表现(N= 44：15℃ 23条,20℃ 8条,25℃ 13条),不同测试温度间隔一天进行实验。运动表现测定前2h,将蝾螈放置于温度预先设定的人工气候箱内以控制其体温。将蝾螈放入盛有5cm水深的长方形玻璃槽(150 cm × 10 cm × 15 cm)中,玻璃槽的水温预先调整至相应的测试温度,一人用毛笔轻触蝾螈尾部以驱使其向前游动,另一人用松下HDC-HS900数码摄像机记录蝾螈在水中的游泳情况,每条蝾螈测定一个来回。摄像机记录的视频片段经MGI Video Wave III软件(MGI Software Co., Canada)分析读出游泳速度。游泳速度用蝾螈游过25 cm的最大速度表示。运动表现测定结束后,将蝾螈放回原来相应驯化温度的塑料盒。

1.3 热耐受性测定

运动表现测定结束,44条蝾螈在相应驯化温度再饲养一周后,用动态法测定其CTMin和CTMax[3, 31]。临界高、低温测定在人工气候箱内进行,为了消除不同时段对测定的影响,每日13:00—16:00进行实验。实验动物分批测定,单次4—6条蝾螈放入底部铺有湿润纱布的玻璃缸(35 cm × 30 cm × 25 cm),缸上覆以可透气塑料盖以防其逃脱,玻璃缸置于人工气候箱中。人工气候箱内温度从驯化温度以0.3℃ /min的速度下降或上升,当气候箱内低于5℃或高于35℃时按0.1℃ /min改变温度速率。当蝾螈在强烈刺激下出现反正反应(Righting response)时用UT- 325型电子温度计(优利德电子有限公司,上海)迅速测出泄殖腔温度,表示对应的CTMin或CTMax值。实验测定CTMin后,在相应驯化温度下继续驯养3d后测定CTMax。可耐受温度范围(TRR)用同个体CTMax与CTMin的差值表示。临界高低温测定结束后3d内,4条蝾螈死亡(15℃ 1条,20℃ 1条,25℃ 2条),相对应的CTMin、CTMax值以及可耐受温度范围未用于进一步统计分析。驯化反应速率(Acclimation response ratio, ARR)用驯化温度改变1℃时对应的CTMin或CTMax的变化值表示,即ARR=Δ CTM /Δ AT,式中Δ CTM 为CTMin或CTMax的改变量,Δ AT 为驯化温度(AT) 的改变量。

1.4 数据处理

用Statistica 6.0统计软件包(StatSoft, Tulsa, USA)处理相关数据。做进一步统计检验前, 用Kolmogorov-Smirnov检验和Bartlett分别检验数据正态性和方差同质性。用重复测量方差分析(Repeated measures ANOVA)检验驯化温度和测试体温对游泳速度的影响,单因子方差分析(One-way ANOVA)检验临界高低温以及耐受温度范围的组间差异,Tukey检验进行多重比较。描述性统计值用平均值±标准误表示,显著性水平设置为α=0.05。

2 结果

图1 不同热驯化条件下东方蝾螈幼体的游泳速度Fig.1 Swimming speed of juvenile Cynops orientalis acclimated to different temperatures

各实验组动物体长无显著的组间差异(F2, 45=1.04,P=0.363)。东方蝾螈幼体的游泳速度受驯化温度(F2, 41=3.28,P=0.048)、测试体温(F2, 82=4.31,P=0.017)以及两者交互作用(F4, 82=6.83,P<0.001)的影响显著(图1)。15、20℃驯化蝾螈泳速平均值分别在15、20℃测试温度下最大,但不同测试温度间统计上无显著差异(15℃驯化：F2, 44=1.22,P=0.306；20℃驯化：F2, 14=2.28,P=0.139)；25℃驯化蝾螈在25℃测试温度下的泳速显著大于15、20℃测试温度下泳速(F2, 24=14.40,P<0.001)。15℃测试温度下,低温(15℃)和中等温度(20℃)驯化蝾螈泳速快于高温(25℃)驯化个体(F2, 41=3.43,P=0.042)；20℃测试温度下,中等温度驯化蝾螈泳速快于低温及高温驯化个体(F2, 41=5.31,P<0.01)；而25℃测试温度下,高温及中等温度驯化蝾螈泳速快于低温驯化个体(F2, 41=6.94,P<0.01)(图1)。

驯化温度对东方蝾螈临界高、低温的影响均显著(CTMin：F2, 37=17.30,P<0.001；CTMax：F2, 37=5.92,P<0.01)。CTMin和CTMax均随驯化温度的升高而升高(图2)。20℃条件驯化蝾螈具稍宽的可耐受温度范围(TRR),但驯化温度对TRR的影响并不显著(F2, 37=0.74,P=0.483,图2)。15—20℃驯化温度,CTMin和CTMax的驯化反应速率(ARR)分别为0.09和0.26；而20-25℃驯化温度,CTMin和CTMax的ARR分别为0.21和0.16。

图2 不同热驯化条件下东方蝾螈幼体的临界高低温及可耐受温度范围(平均值带不同上标字母的表示差异显著)Fig.2 Critical thermal minimum and maximum, and thermal resistance range of juvenile Cynops orientalis acclimated to different temperatures (Means with different letters differ significantly, Tukey′s test, α=0.05, a>b)

3 讨论

3.1 热驯化对蝾螈运动表现的影响

虽然低温及中等温度驯化的东方蝾螈幼体在不同测试温度的游泳速度无显著差异,但总体上其游泳速度的热敏感性仍存在。外温动物运动表现的热功能曲线一般呈右倾的峰型曲线[2]。低温及中等温度驯化蝾螈泳速未表现明显的测试温度效应可能与热驯化改变泳速的热敏感性有关。运动表现随体温变化而变化在外温动物中是普遍的,但不同运动方式的热敏感性存在差异。一些研究表明：因水中运动能力的相对重要性,水生动物(如鱼类、两栖类等)水中运动表现的热敏感性显著低于陆地运动表现[27-29,32-33]。低温及中等温度驯化蝾螈在15—25℃测试温度范围内泳速无显著变化可能部分反映出这种趋势。当然与蝾螈陆地运动表现热敏感性的差异仍需进一步确定。

驯化温度显著影响蝾螈幼体的运动表现,这与许多其它外温动物的研究结果相类似。有意思的是,经某一温度驯化后蝾螈的游泳能力似乎在相同测试温度下表现最好。例如,25℃驯化蝾螈在25℃测试温度泳速最大；其余两驯化条件蝾螈在对应测试温度下泳速亦稍大。因此,这一结果可能支持驯化有益假说,即特定温度驯化的动物在该温度下具增强的功能表现和适合度[18,24]。

外温动物运动表现的热驯化效应在种间、种群间甚至不同发育阶段间存在差异[19-20]。两栖类动物运动表现热驯化效应的研究结果显示(表1)：许多两栖类动物幼体阶段水中运动表现的热驯化效应显著,但成年后陆地运动时该效应基本消失。两栖类运动表现的热驯化效应在不同个体阶段的转变被认为是与其生活环境的变迁有关。两栖类(特别是蛙类)幼体阶段主要在水体中生活,而成体阶段在陆地生活的时间会明显增加；水体的温度日波动通常远小于陆地上的温度日波动。成年后上陆活动的两栖类逐渐适应这种大幅度变化的陆地热环境,同时也削弱了热驯化对其运动表现以及其它生理行为特征的影响[19,24]。东方蝾螈生活于丘陵、山间或山边的水塘、沟渠、水田等静水水域中,此类水体环境的温度变异有限,因此,与其它水生动物相似[19-20],蝾螈幼体在水中的运动表现受热驯化的显著影响是可预测的。

表1 热驯化对几种两栖类动物运动表现的影响

3.2 热驯化对蝾螈热耐受性的影响

东方蝾螈幼体的临界低温(CTMin, 2.4—3.9℃)低于两种已研究蛙类蝌蚪的相应值(泽陆蛙Fejervaryalimnocharis：7.4—8.9℃；饰纹姬蛙Microhylaornata：8.7—11.7℃[11])；其临界高温(CTMax, 34.6—36.7℃)同样低于蛙类蝌蚪的相应值,如中国林蛙(Ranachensinensis)(35.8—39.8℃)[10],泽陆蛙(42.1—42.9℃)和饰纹姬蛙(39.8—40.9℃)[11],大蟾蜍(Bufogargarizans)(36.5—38.8℃)[39],与一些有尾类动物的相应值接近(34.1—38.4℃)[40-41]。东方蝾螈比一些蛙类蝌蚪具相对较低的CTMin和CTMax可能与其生境温度相对较低有关。

热驯化显著影响蝾螈幼体的热耐受能力,CTMin和CTMax随驯化温度的升高而上升,表明：低温驯化个体比高温驯化个体具较强抗低温能力,而高温驯化个体比低温驯化个体具较强抗高温能力。这与已报道的绝大多数两栖类动物种类的研究结果一致[1-11,39, 42]。仅在少数种类中,高温驯化个体的抗高温能力并不显著大于低温驯化个体。例如,即将发生变态的美洲林蛙(Ranasylvatica)[43]和牛蛙(Ranacatesbeiana)[44]蝌蚪在较高温度驯化的CTMax略低于较低温度驯化的相应值。本研究显示热驯化并不影响蝾螈幼体的可耐受温度范围(TRR)。该特征的热驯化效应在不同动物种类中存在较大差异。例如,泽陆蛙和饰纹姬蛙蝌蚪TRR随驯化温度的升高而降低[11],但在爬行类动物中并不存在一致的变化趋势[12-16,45-46]。稍凉或温和的环境温度可能最适于东方蝾螈幼体生长[29],本研究中中等温度驯化蝾螈显示稍宽的TRR可能反映出接近最适温度的驯化条件有利于表达其耐受能力。

驯化反应速率(ARR)代表外温动物对环境温度变化产生生理反应的能力。两栖类动物CTMin和CTMax的ARR值存在显著的种间差异(表2)。这种差异反映了在不同热环境中动物扩展其耐受能力的差别,并可能与它们栖息环境的温度条件有关。生活在短期内温度波动大的环境中的种类比生活在温度长期缓慢变化的环境中的种类通常具有较强抵抗快速温度变化的能力[47-48]。15—20℃驯化温度蝾螈幼体CTMax的ARR值(0.26)大于CTMin对应值(0.09),但20—25℃驯化温度CTMax的ARR值(0.16)小于CTMin对应值(0.21)。这一结果与泽陆蛙和饰纹姬蛙蝌蚪[11]和爬行类动物[12-14,45-46]的报道相似。Chatterjee等[49]预测CTMin或CTMax的变化幅度随着驯化温度接近对应热耐受临界值时逐渐减小至零,本文的研究结果与之相符合。然而,在一些种类中CTMin和CTMax(特别是CTMin)随驯化温度的变化趋势并不总是与上述预测相符。例如,10—20℃驯化温度美洲林蛙蝌蚪CTMin的ARR值大于CTMax的对应值[42]。

表2 几种两栖类动物临界高低温的驯化反应速率

Table 2 Acclimation response ratios (ARRs) of critical thermal minimum (CTMin) and maximum (CTMax) in some species of amphibians

物种Species发育阶段Developmentstage驯化温度/(℃)Acclimationtemperature临界低温驯化反应速率Acclimationresponseratioofcriticalthermalminimum临界高温驯化反应速率Acclimationresponseratioofcriticalthermalmaximum无尾类Anura Fejervaryalimnocharis[11]蝌蚪26—30期20—300．140．06 Microhylaornata[11]蝌蚪26—30期20—300．30．11 Ranachensinensis[10]蝌蚪？期10—25—0．27 R．sylvatica[43]蝌蚪27—29期10—30—0．11 R．catesbeiana[44]蝌蚪28—40期15—25—0．08 Bufoamericanus[43]蝌蚪32期10—30—0．06 B．woodhousei[43]蝌蚪27—32期10—30—0．02 B．marinus[42]蝌蚪26—30期25—350．10．25 B．gargarizans[39]蝌蚪？期10—25—0．39 Pseudacristriseriata[43]蝌蚪27期10—30—0．16 Gastrophrynecarolinensis[43]蝌蚪32期20—30—0．08有尾类Caudata Euryceamultiplicata[40]成体5—15—0．13 E．lucifuga[40]成体5—15—0．02 E．longicauda[40]成体5—15—0．08 Ambystomamaculatum[40]成体5—15—0．08 Cynopsorientalis(本研究)幼体15—250．150．21

综上所述,东方蝾螈幼体经不同温度驯化后其运动表现和热耐受能力会发生改变。经特定温度驯化后的蝾螈在对应测试体温下具有较好的运动表现,结果支持驯化有益假说；低温驯化有助于提升蝾螈的抗低温能力,而高温驯化能提升抗高温能力。两栖类动物的热驯化反应存在显著的种间差异。这些差异可能反映了不同种类个体发育过程中所经历热环境的变化。栖息生境温度变异幅度大,可能会削弱动物生理及功能表现的热驯化效应,但有助于提高其应对温度变化的能力。

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Physiological response and changes in swimming performance after thermal acclimation in juvenile chinese fire-belly newts,Cynopsorientalis

LU Hongliang1, GENG Jun1, XU Wei1, PING Jun2, ZHANG Yongpu2,*

1HangzhouKeyLaboratoryofAnimalAdaptationandEvolution,SchoolofLifeandEnvironmentalSciences,HangzhouNormalUniversity,Hangzhou310036,China2CollegeofLifeandEnvironmentalScience,WenzhouUniversity,Wenzhou325035,China

The thermal acclimatory capacity of a particular species determines its tolerance to environmental changes and affects its survival under future changing climatic conditions. Acclimation effects on physiological traits have been determined in many fish and frog species, but rarely in newts or salamanders. In the present study, we evaluated the physiological acclimatory response of newts. A total of 48 juvenile Chinese fire-belly newts (Cynopsorientalis) were collected and acclimated to 15℃, 20℃, and 25℃, which represented the low, intermediate, and high environmental temperatures experienced byC.orientalisduring their active period, respectively, over the course of 4 weeks. The locomotor (swimming) performances of individuals were measured at the same three test temperatures in a glass tank (150 cm × 10 cm × 15 cm) filled with water to a depth of 5 cm, and the critical thermal minimum (CTMin) and maximum (CTMax) were determined using a dynamic method. The thermal resistance range (TRR) was calculated as the difference between CTMaxand CTMin, and acclimation response ratio (ARR) of CTMinand CTMaxwas obtained by dividing the tolerance change by the change in acclimation temperature. The results from repeated-measures ANOVA analyses revealed that newt swimming speeds were significantly affected by the acclimation and test temperatures. Despite no statistically significant difference, low and intermediate temperature-acclimated newts had relatively high mean swimming speeds at 15℃ and 20℃, respectively, while the high-temperature-acclimated newts had superior swimming speeds at 25℃. Similarly, at 15℃, low temperature-acclimated newts swam faster than those acclimated to a high temperature. However, at 20℃, intermediate temperature-acclimated newts swam faster than low or high temperature-acclimated individuals, while at 25℃, high and intermediate temperature-acclimated newts swam faster than those acclimated to low temperature. Thus, our data supports the beneficial acclimation hypothesis, which predicts that acclimation to a particular temperature enhances the animal′s performance or fitness at that temperature. Our results also indicate that temperature acclimation shifts the thermal sensitivity of swimming performance inC.orientalissince low temperature-acclimated newts appear to have lower thermal sensitivity levels than those acclimated to high temperature. Both CTMinand CTMaxwere significantly enhanced at higher acclimation temperatures, suggesting that juvenile newts acclimated to low temperatures are more resistant to low temperatures and less resistant to high temperatures, whereas those acclimated to high temperatures are more resistant to high but less resistant to low temperatures. These results are consistent with previous studies focused on the various ectothermic vertebrate species analyzed to date. The TRR of newts was not affected by acclimation temperature, while the ARR of CTMax(0.26) was higher than that of CTMin(0.09) at acclimation temperatures between 15℃ and 20℃, but lower at acclimation temperatures between 20℃ and 25℃ (CTMax: 0.16vsCTMin: 0.21). These results are consistent with previous predictions that the magnitude of the change in CTMinor CTMaxslowly decreases and ultimately approaches zero as the acclimation temperature gradually reaches its thermal limits. Inter-species differences in thermal physiological response to acclimation in amphibians may be correlated with differences in thermal environments in their natural habitats.

Cynopsorientalis; thermal acclimation; thermal tolerance; locomotor performance; beneficial acclimation hypothesis

国家自然科学基金项目(31170376)；浙江省自然科学基金项目(LY15C030006,LY16C030001)

2015- 10- 06;

日期:2016- 07- 13

10.5846/stxb201510062006

*通讯作者Corresponding author.E-mail: zhangypu@126.com

陆洪良, 耿军, 徐卫, 平骏, 张永普.东方蝾螈幼体热耐受性和游泳表现的热驯化响应.生态学报,2017,37(5):1603- 1610.

Lu H L, Geng J, Xu W, Ping J, Zhang Y P.Physiological response and changes in swimming performance after thermal acclimation in juvenile chinese fire-belly newts,Cynopsorientalis.Acta Ecologica Sinica,2017,37(5):1603- 1610.