通河林区黄鼬(Mustelasibirica)冬季被毛形态结构的功能适应性

王 颖, 孙长虹, 张 伟

东北林业大学野生动物资源学院, 哈尔滨 150040

通河林区黄鼬(Mustelasibirica)冬季被毛形态结构的功能适应性

王 颖, 孙长虹, 张 伟*

东北林业大学野生动物资源学院, 哈尔滨 150040

被毛在哺乳动物适应性进化过程中执行保温和保护两个重要功能，其形态结构上存在的功能适应性特征因所处的部位不同而表现出适应性分化现象，由动物体躯干至四肢末端呈显著的梯度变化。以黑龙江省通河林区黄鼬东北亚种(Mustelasibiricamanchurica)冬季雌雄成体各10只完整毛皮对象，研究了背中部、腹中部和后肢下部3个部位的直针毛、披针毛、绒针毛、绒毛，以及后趾部硬毛的被毛性状因子，统计分析表明：通河林区黄鼬相同身体部位4种类型毛的长度和细度指标均为直针毛>披针毛>绒针毛>绒毛，相同部位4种类型毛长度的相关性极显著，直针毛细度与披针毛细度相关性极显著(P<0.01)，绒针毛细度与绒毛细度相关性极显著(P<0.01)，这种特征使得被毛在整体结构上为实施保温和保护功能奠定基础；同时，黄鼬被毛各性状的保温功能从背部向后趾部呈递减趋势，而保护功能则呈现递增趋势，被毛形态结构性状上的分化与动物机体异温性充分结合，对于黄鼬适应寒冷的森林生态环境具有重要意义。

黄鼬; 被毛; 形态结构; 功能适应

动物机体的形态结构特征与其所处的环境及所要发挥的功能密不可分。哺乳动物被毛是发挥相关功能以使其适应环境的重要部分[1- 6]，如一些动物被毛的颜色和斑纹对动物的隐蔽、求偶展示、吸收太阳能等起着重要作用[7- 10]；同时，被毛的形态结构性状与所处环境也紧密相关，栖息于不同生境中的动物在被毛微观结构上的差异十分显著[11- 15]，即使生活在特定生境中的动物也通过被毛的季节性脱换[2,16-17]和身体不同部位被毛的性状差异[18- 22]来适应所处的生态环境。比较动物不同身体部位的被毛特征，能够反映出不同部位的毛对适应环境的功能分化，也可以反映出动物对其生存环境的适应[23]。但以往的研究多是探索动物被毛对高寒环境的适应策略，事实上动物被毛除了用于防御严寒之外[24- 26]，还要保护机体免受伤害[27-28]，并且动物被毛在生态类型复杂、恶劣气候环境下的适应性特征和分化更加明显；同时，以往研究也多以毛被类型简单的动物为对象，代表性不突出。本实验选取生态类型复杂，冬季漫长严寒的黑龙江省通河林区为研究地，以分布性广、适应性强、毛被类型复杂(含直针毛、披针毛、绒针毛、绒毛、硬毛等多种类型毛)的黄鼬(Mustelasibirica)为研究对象，探讨动物被毛在形态结构上普遍存在的功能适应性特征和适应性分化现象。

黑龙江省通河龙口林场为低山丘陵地貌，属温带大陆性季风气候区，全年平均气温1.9 ℃，1月极端最低气温达-46.2 ℃，10月下旬到翌年5月下旬为结冻期。主要的森林类型为以阔叶红松林为主的针阔混交林和以桦树林、杨树林、栎树林组成的阔叶林，其次为榛子灌丛和胡枝子灌丛。在严寒而漫长的冬季，动物首先要解决保温问题，同时由于植被类型复杂，又要强化对机体的保护以避免外界环境刮伤身体和避免被毛过长阻碍其运动[29]。通河龙口林场的特殊的环境气候特征极适于开展动物被毛的生态适应性及功能适应性分化的研究。

1 材料与方法

1.1 材料

将2005年12月—2006年2月在黑龙江省通河龙口林场采集的黄鼬东北亚种雌雄成体各10只的完整毛皮作为实验材料，分别在每只个体的背中部(dorsal back)、腹中部(belly)、后肢下部(lower hindleg)采集直针毛(unbent awn)、披针毛(sub-awn)、绒针毛(vellus awn)、绒毛(undercoat hair)各5根，在每只个体的后趾部(hind claw)采集硬毛(bristle)各5根。因同部位的同类型的单根毛即可进行形态学的物种鉴定[30]，5根毛的统计数据可以有效避免测量误差[23]。

1.2 方法

1.2.1 光镜样本制备

将完整的毛样本置于培养皿中，用乙醚和95%的乙醇按1∶1组成的脱脂液脱脂20min；将脱脂后的毛置于30%的过氧化氢中脱色30 min，用无水乙醇清洗10 min。将处理后的毛放到2—3 mm厚的无色有机玻璃载片上，在其上下覆以无机玻璃载片，并用铁夹固定。放到120 ℃的DGG- 9053A型电热恒温干燥箱中加热2 h；待玻璃冷却后卸下铁夹及无机载片，此时毛附着于有机玻璃载片上；用窄透明胶带将整根毛粘起并平行贴于距毛鳞片印痕1—2 mm处，即制成可同时用光镜观察鳞片和髓质的装片[30]。

1.2.2 数据测量

应用H6303i生物显微镜及配套的图片处理、测量软件系统(重光数码显微系统)对毛长度、髓质长度、毛尖无髓段长度、毛细度、髓质细度等指标进行测量，其中毛细度和髓质细度以毛最粗部位为标准，测量部位见图1。在测量前先用台微尺对显微镜进行校正，测定屏幕测量值与实物真实值之间的系数，所有测量指标乘以校正系数即为所测量的真实值。

图1 毛的测量部位示意图(a: 毛尖无髓段长度；b: 髓质长度；c: 毛根无髓段长度；d: 毛细度；e: 髓质细度)Fig.1 Measurement of different hair parameters (a: Non-medulla tip length, b: Medulla length, c: Non-medulla root length, d: Hair diameter, e: Medulla diameter)

1.2.3 相对指标的计算

髓质长度所占比例=b/(a+b+c)

毛尖无髓段长度所占比例=a/(a+b+c)

髓质指数=e/d

1.2.4 统计分析

应用SPSS15.0软件处理，先用Kolmogorov-Smirnov分别检验背中部、腹中部、后肢下部的直针毛、披针毛、绒针毛、绒毛及后趾部硬毛等五种类型毛的长度、髓质长度、髓质长度比例、毛尖无髓段长度比例、细度、髓质指数等6个被毛性状因子是否呈正态分布，经检验数据均符合正态分布(P>0.05)。

针对同种类型毛的长度、髓质长度、髓质长度比例、毛尖无髓段长度比例、细度、髓质指数等指标是否由于身体部位的不同而产生显著差异，先经方差齐性检验，P值均大于0.05，方差齐。因此，采用单因素方差分析中的最小显著差数法(LSD)对所测指标进行差异显著性检验[31]；并应用皮尔森(Pearson)双变量相关性统计法对相同部位四种类型毛的长度、细度进行相关性分析。

2 结果与分析

2.1 相同身体部位四种类型毛的长度、细度比较

由表1可知，相同身体部位四种类型毛的长度和细度变化趋势均为：直针毛﹥披针毛﹥绒针毛﹥绒毛；由表2可知，四种类型毛长度之间的相关性均极显著。

由表1可知，相同身体部位的直针毛细度与披针毛细度相差不大，且直针毛细度是绒针毛细度的2倍左右，是绒毛细度的6—8倍。由表3可知，直针毛细度与披针毛、绒针毛的细度均呈显著正相关，但与绒毛细度不相关(r=0.176,P>0.05)；披针毛细度与绒针毛、绒毛的细度均显著正相关，绒针毛细度与绒毛细度显著正相关(r=0.340，P<0.05)。表明黄鼬直针毛细度可能左右着披针毛和绒针毛的细度，而绒毛细度与直针毛细度无关，披针毛、绒针毛和绒毛之间的细度密切相关。

2.2 不同身体部位被毛性状之间的比较

由表1可知，雄性直针毛的长度和细度表现为：背中部﹥腹中部﹥后趾部﹥后肢下部，而直针毛的其他性状指标(如雌性直针毛的长度和细度、雌雄性直针毛的髓质长度、髓质长度所占比例、髓质指数)则都表现为：背中部﹥腹中部﹥后肢下部﹥后趾部，毛尖无髓段长度所占比例则都表现为：背中部﹤腹中部﹤后肢下部﹤后趾部。虽然后肢下部直针毛与后趾部硬毛的长度、细度因黄鼬性别不同呈相反的变化趋势，但后肢下部与后趾部在毛长度(P雄∶后肢下部—后趾部=0.124>0.05,P雌∶后肢下部—后趾部=0.773>0.05)和毛细度(P雄∶后肢下部—后趾部=0. 229>0.05,P雌∶后肢下部—后趾部=0.589>0.05)上并无显著差异。这表明在总体上直针毛和硬毛的长度、细度、髓质长度、髓质长度所占比例和髓质指数由躯干向四肢末端递减，毛尖无髓段长度所占比例则正好相反(注：为了便于说明问题，将后趾部的硬毛与直针毛统一进行比较) 。

无论雌雄，披针毛的长度、髓质长度、髓质长度所占比例、细度、髓质指数都表现为：背中部﹥腹中部﹥后肢下部，披针毛的毛尖无髓段长度所占比例则都表现为：背中部﹤腹中部﹤后肢下部。表明披针毛的长度、细度、髓质长度、髓质长度所占比例和髓质指数由躯干向四肢末端递减，毛尖无髓段长度所占比例则正好相反。

对于绒针毛，除了雌性的髓质指数表现为：腹中部﹥背中部﹥后肢下部外，毛长度、髓质长度、髓质长度所占比例、毛细度、雄性绒针毛髓质指数都表现为：背中部﹥腹中部﹥后肢下部；毛尖无髓段长度所占比例为：背中部﹤腹中部﹤后肢下部。这表明在总体上绒针毛的长度、细度、髓质长度、髓质长度所占比例和髓质指数由躯干向四肢末端递减，毛尖无髓段长度所占比例则正好相反。

除了绒毛细度、雄性绒毛的髓质指数表现为：腹中部﹥背中部﹥后肢下部外，毛长度、髓质长度、髓质长度所占比例、雌性绒毛的髓质指数都表现为：背中部﹥腹中部﹥后肢下部，毛尖无髓段长度所占比例则为：背中部﹤腹中部﹤后肢下部。绒毛相应性状的身体部位差异不明显，只有毛尖无髓段长度由躯干向四肢末端明显增大。

雄性直针毛和披针毛的髓质长度所占比例、雄性直针毛的毛尖无髓段长度所占比例、雌雄性直针毛及雄性披针毛的毛细度、雄性直针毛及雌雄性披针毛的髓质指数等指标在背中部与腹中部之间无显著差异(P背中部—腹中部>0.05)，以及腹中部与后肢下部直针毛的髓质指数无显著差异外(P腹中部—后肢下部>0.05)，其他性状指标之间都存在显著差异。表明背中部与腹中部的绒针毛和绒毛的相应性状无明显差异。

表2 雌雄黄鼬四种类型毛长度相关性(n=400)

表3 雌雄黄鼬四种类型毛细度相关性 (n=400)

3 讨论

被毛作为哺乳动物身体最外层的部分，对机体的保温和抗机械损伤起着重要作用。在宏观性状上，动物通过增加被毛的长度和密度来适应寒冷环境[22,24,29,32]。在微观结构上，动物被毛的性状指标也同样具备一定的保温和抗机械损伤功能，如通过扩大髓质的比例来加强保温[6,21,24]或者调节髓质发达程度、鳞片的排列方式和密集程度实现保温和保护功能[33]。但毛长度过长不利于动物的奔跑[29,34]；髓质占据毛空间的比例过大，降低了毛的弹性、强度和韧性[30],同时也影响被毛的抗机械损伤功能[35-36]；毛尖无髓段比例越大，动物身体上被毛的耐磨性越强[37]。所以动物要增强被毛的保温功能，就会弱化其保护功能，同一部位被毛在微观性状上的保温和保护功能不可能同时得到最好的表达。但是动物机体存在异温性，这对于动物在被毛微观结构上解决保温和保护功能的矛盾发挥了重大作用。故在长期的进化过程中，动物被毛的功能分化与动物机体的异温性相结合，使得被毛在微观性状上很好地解决了保温和保护功能上的矛盾[21]。

黄鼬被毛在整体上明显分化为直针毛、披针毛、绒针毛、绒毛4种类型的毛，它们呈4层分布，构成错落有致的防护层，绒毛细度与直针毛细度无关且长度远远小于直针毛，可以充分填充直针毛、披针毛间的空隙，从而增加毛密度；而且绒针毛下部及绒毛整体的弯曲结构，使动物被毛之间可容纳较多的静止空气，可降低冷空气进入被毛内的速度，从而加强了保温作用。同时，由于直针毛和披针毛位于毛被的最上层，先与环境接触，对毛被的整体结构起支撑作用，它们的纺锤形结构，使得毛头部位相对较粗、也较绒针毛和绒毛结实，且毛头部位皮质层发达，抗机械损伤性能强，有效地保护了下部的绒针毛和绒毛。

研究表明，背中部被毛的长度最大，增加了背部保温层的厚度；同时髓质长度最长、髓质长度所占比例、毛细度及髓质指数最大、毛尖无髓段所占比例最小，由此多方面地增加了背中部被毛髓质所占的比例，使单根毛能够容纳更多的静止空气。因为背部接近体核且直接暴露，需要具有极强保温功能的被毛来阻止身体热量的流失[20,38]。

后趾部由于与外环境直接接触多，需要强化保护功能。其硬毛最短，有利于动物的活动，倘若通过增加毛长度来加强缓冲能力，则不利于黄鼬的穿行，也易造成被毛与植被缠结。但硬毛的髓质指数最小，则皮质层最发达，同时髓质长度及髓质长度所占比例最小、毛尖无髓段所占比例最大，这避免了由于髓质比例过大导致的毛脆、易折断等不利情况，增加了毛的弹性和强度，使毛的抗机械损伤功能加强[34-35]。但后趾部被毛的这些特点势必降低其保温功能，动物体的异温性恰好弥补了这一不足。

腹中部被毛的诸多性状与背中部被毛的相关性状接近，这是由于腹部位于体核需要加强保温，同时又处于体核下部，处于保温向保护的过渡阶段。在后肢下部的上毛中，除雄性黄鼬在直针毛的髓质指数上与腹中部直针毛无显著差异外，其他性状均与腹中部存在显著差异，而雌雄黄鼬后肢下部直针毛的长度、细度与后趾部硬毛更加接近(P后肢下部—后趾部>0.05)，由此可见，后肢下部直针毛的功能更趋向于接近后趾部硬毛，主要实施保护。

进而，由表1可知，黄鼬被毛各形态结构性状从背部向肢体末端的保温功能呈逐渐下降趋势，而抗机械损伤功能呈逐渐上升趋势，并在腹中部和后肢下部表现出过渡特征。背中部被毛与后趾部上毛的形态结构性状处于保温与保护功能的两个极端，而腹中部与后肢下部则处于中间状态。Underwood[19]和Moen[20]研究发现北极狐和黑熊的被毛厚度由背部向四肢末端逐渐降低，这与本文的研究结果相一致。被毛长度越短，热量散失得越快，保温性能则越低，动物体的异温性特征正好弥补了保温功能由躯干至四肢末端梯度降低的不足[17]。许多学者的研究也表明被毛因部位的不同分化出分别执行保温功能和保护功能的结构特征，马鹿东北亚种冬季从臀部向蹄部被毛保温功能逐渐降低，保护功能逐渐增加[21]。狍冬季采食较困难，需要大量运动，为适应积雪和草木干枯所增大的磨损作用，其被毛的保护功能由躯干向四肢逐渐增大[6]。白唇鹿在被毛性状的保温和保护功能上的表现也是如此，这与其需要在高寒草原和灌丛中快速奔跑相适应[39-40]。生活于通河林区的黄鼬冬季食物主要是鼠类，通河林区植被类型复杂[41-42]，需要在布满榛子灌丛和胡枝子灌丛的厚雪地上猎食鼠类，对腹部和四肢的被毛造成巨大的机械磨损作用，黄鼬的腹部和四肢的抗机械损伤功能增强后，对防止动物被植物伤害显得极其重要[42]，因此其被毛的保温功能和保护功能由躯干至四肢出现了适应性的变化。

综上所述，被毛分化为四种类型，使得毛被在整体结构上对于黄鼬具备一定的保温和缓冲功能，在此基础上，被毛微观结构上的分化又满足了黄鼬身体不同部位对保温和保护功能的需要，这一特性与动物机体的异温性结合，使得肢体末端、趾部等与外环境接触较多的部位的被毛在微观上强化了保护功能，从而在降低了保温功能的情况下不至冻伤机体。这对于黄鼬适应残酷寒冷的森林环境具有重要意义。

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Hair morphology as functional adaptation in winterMustelasibiricain Tonghe forest area

WANG Ying, SUN Changhong, ZHANG Wei*

CollegeofWildlifeResources,NortheastForestryUniversity,Harbin150040,China

The body function and external morphology of animals with long life span are affected by the environment. Changes in environmental factors, such as temperature, humidity, and illumination, affect the animal′s appearance and its internal functions through changes in physiological mechanisms. Many species of mammals are characterized by a layer of hair on the skin. Hair, being constantly exposed to the outside environment, directly indicates functional adaptations to the environment. Adaptation to the environment is caused by a long-lasting selection pressure on a trait as a result of natural selection. To fit the environment, animal can change a series of traits, such as color and body shape. The hairs, which serve for thermal insulation and protection, are the result of a long adaptive evolution. As a result of geographic isolation, populations of one species that are isolated from each other for a long time undergo speciation, resulting in subspecies or new species. Morphological structure of hairs covering different body regions is the result of different functional adaptations. Often there is a gradient in hair variation from the body to the end of the limbs in many mammals. Siberian weasel is a valuable fur animal and a subject of various studies in China. The animal molts seasonally starting from tail to hips, back, and neck, and lastly head and limbs in the fall, and in the opposite direction in the spring. The hair type in Siberian weasel is complex. On the basis of its shape and structure, hair is divided into guard hair, sub-awn, vellus awn, undercoat hair, and bristles. In this study, we measured the length and diameter of guard hair, sub-awn, vellus awn, and undercoat hair, all of which were sampled from the center of the back and venter, the lower end of hind limb, and bristles from the upper side of the hind toe. These hairs were collected from winter pelage of 20 adult Siberian weasels located in Tonghe forest area of Heilongjiang Province. Results showed that the length and diameter of the four types of hair always decreased at the same position. We detected significant correlation between the length of the four hair types (P< 0.01) and significant positive correlation between the diameter of guard hairs and sub-awns (P< 0.01) as well as between vellus awns and undercoat hairs (P< 0.01). The character of each hair type provided the potential to properly insulate and protect animal body as a whole. Thus, the insulation provided by the hair decreased from the back to the hind toe, whereas the protection increased. The hair traits differed among body regions in relation to different temperatures at those parts. We collected and analyzed morphological characters of the guard hair including its length and width, cuticular scale pattern, and medulla. We found significant difference in hair density between the winter and summer coat, hair length, and proportion of absent medulla in guard hair, and we discuss the adaptive mechanism of this variation. Pelage is found only in mammals, where during the course of evolution, its primary role became insulation and protection from the elements. The morphology of the pelage related to the insulation and protection function differed significantly between body regions, resulting from the differentiation of the characteristics during the course of adaptation of pelage. There is a visible gradient in its morphology from the trunk to the limbs. This study reported functional adaptability of the morphological structure of winter pelage of Siberian weasel. The fur was sampled from 20 Siberian weasels (10 males and 10 females) from Longkou Forest Farm of Tonghe in Xiaoxingan Mountain, Heilongjiang Province, in winter from December 2005 to February 2006. Five hairs of each of the four hair types (unbent awn, sub-awn, vellus awn, undercoat hair) were sampled from different parts of the body including dorsal back, venter, and lower hind leg, and five bristles were sampled from upper side of hind claw. The length of the hair, medulla, and non-medulla tip as well as the diameter of the hair and medulla were measured in all sampled hairs and the measurements were used to calculate the proportion of the length of medulla, non-medulla tip, and indexes of medulla (proportion of medulla diameter to hair diameter). All the measurements were carried out by using microscope photography and its supporting software for photo processing and measuring. The analyses indicated a significant correlation between the length of the four hair types and a significant positive correlation between the diameter of unbent awn and sub-awn (P< 0.01) and between vellus awn and undercoat hair (P< 0.01); the hair length played a very important role in the insulation and protection properties of the pelage. Furthermore, the morphological properties of the Siberian weasel winter pelage showed a gradual change from the trunk to the limbs, indicating that the gradient in the insulation and protection function of the pelage corresponds to the heterothermy. Observed polarization of winter pelage in Siberian weasel is the result of adaptation to cold environment in winter. This study provided insights into the strategies of Siberian weasel to adapt to cold climate in the Tonghe forest area.

Siberian weasel; pelage hairs; morphological structure; functional adaptation

国家自然科学基金(30570272)

2013- 11- 27;

日期:2014- 11- 03

10.5846/stxb201311272833

*通讯作者Corresponding author.E-mail: zwfur@aliyun.com

王颖, 孙长虹, 张伟.通河林区黄鼬 (Mustelasibirica)冬季被毛形态结构的功能适应性.生态学报,2015,35(17):5623- 5631.

Wang Y, Sun C H, Zhang W.Hair morphology as functional adaptation in winterMustelasibiricain Tonghe forest area.Acta Ecologica Sinica,2015,35(17):5623- 5631.