卫万荣,麻安卫,何凯,张卫国*
(1.草地农业生态系统国家重点实验室,兰州大学草地农业科技学院,甘肃 兰州 730020; 2.秦安县农村能源开发站,甘肃 秦安 741600)
啮齿类动物群居起源研究假说
卫万荣1,麻安卫1,何凯2,张卫国1*
(1.草地农业生态系统国家重点实验室,兰州大学草地农业科技学院,甘肃 兰州 730020; 2.秦安县农村能源开发站,甘肃 秦安 741600)
摘要:文章阐述了有关啮齿类动物群居起源相关的7个假说。资源防卫假说认为当资源(食物、水、庇护所)在时空上呈斑块状聚集分布时,群居有利于获取和保护资源。捕食风险假说认为群居能降低啮齿类被捕食的风险,因此在高风险栖境中群居较为普遍。社群温度调节假说认为在寒带和气候寒冷的地区群居有利于啮齿类减少能量消耗。旱区食物分布假说认为处于干旱生境中的啮齿类为减少挖掘洞道所需的能耗和弱化无收益觅食风险不得不形成群居。生活史约束假说认为体型小、脂肪贮存能力低、生长速率慢的啮齿类为能成功抚育后代而不得不形成群居。由于构建洞穴耗能巨大,因此窝巢共享假说认为啮齿类为减少能耗被迫共享洞系进而形成群居。亲代投资假说认为由于亲本对后代的持续性投资,因而群居的形成是由子代推迟扩散导致的。最后,本文对啮齿类群居未来研究的热点进行了探讨。
关键词:群居;资源防卫假说;捕食风险假说;社群温度调节假说;旱区食物分布假说;生活史约束假说;窝巢共享假说;亲代投资假说
群居(社会性)动物是指以群体为生活方式,无论觅食、休憩、迁移等行为都以集体为单位,彼此间相互关照,相互协助的动物[1]。影响动物群居的因素一直是动物社会生物学和行为生态学的研究热点。动物群居可能由某种自然因素或同一外部刺激对个体吸引而致,也可能是动物个体间相互吸引造成的[2],亦可能是动物本身的扩散受到外部环境限制导致的[3]。栖息适合度是判定是否有利于动物群居的综合指标,包括捕食风险、觅食效率、寄生虫和疾病传播、攻击性、资源竞争、杀婴和通奸行为等诸多因素[4-8]。只有降低这些弊端和约束产生的影响,栖息适合度适宜,动物才会形成群居生活[9]。
啮齿类是哺乳动物中种类最多的一个类群,也是分布范围最广的哺乳动物,全世界约有2000多种。其生活方式独居、临时聚群和群居均有[3,10]。群居啮齿类是指个体间联系频繁,有共同的摄食区域、领地,共享一个窝巢和洞系[11-13]。有关啮齿类群居理论论述研究我国学者还未曾有过评述,国外亦不多见[14-15]。因此本文在国内外现有文献的基础上,介绍影响啮齿类群居起源的主要观点及相关研究,如资源防卫假说(the resource-defense hypothesis)、捕食风险假说(the predatory risk hypothesis)、温度调节假说(the social thermoregulation hypothesis)、旱区食物分布假说(the aridity food-distribution hypothesis)、生活史限制假说(the life-history constraint hypothesis)、亲代投资假说(the parental investment hypothesis)、窝巢共享假说(the burrow-sharing hypothesis),对相关研究进行总结评价,并对未来的研究热点进行探讨,为我国学者提供参考。
1资源防卫假说
资源防卫假说又称资源分散假说(the resource dispersion hypothesis):当资源(食物、水、庇护所、配偶)在时空上呈斑块状分布,群居有利于啮齿类获取和保护资源[15]。简明而言,个体所能获取的资源随种群数量增加而增加,啮齿类种群密度随资源聚集程度的增加而增加;反之,资源稀疏且均匀分布时,保护资源所需代价巨大,栖息适合度降低,群居就显得不切实际[16]。
许多实验性研究结果与该假说相符。例如,人为控制甘尼森土拨鼠(Cynomysgunnisoni)食物后其种群与社群结构发生改变[16]。当食物聚集度增加后土拨鼠摄食区域减小,种群密度增加;反之食物减少且分布均匀时其摄食区域扩大,种群密度降低。野外观测实验也得到了相同结果[17-19]。在食物集中分布的区域,土拨鼠种群密度较大;但在食物聚集度低并均匀分布的区域,种群密度较小;增加雌性棕背鼠平[17](Clethrionomysrufocanus)和雌性加利福尼亚小田鼠[18](Microtuscalifornicus)食物资源后二者活动范围的重叠度显著增加;实验性增加雌性棕背鼠平数量后聚群现象明显增加[19]。除此而外,摄食领域亦随种群大小而变,如长爪沙鼠[20](Merionesunguiculatus)和水豚[21](Hydrochaerishydrochaeris)个体所能获取的资源随领地增大而增加。由于食物对鼠类能否生存和成功繁殖至关重要,增加尾林鼠[22](Neotomacinerea)和岩豚鼠[23](Kerodonrupestis)的食物后,其种群内有更多的个体参与到储存和保护食物资源的过程中,亦从侧面验证了该假说。
尽管许多研究支持该假说,但亦有研究与该假说相矛盾,如阿根廷长耳豚鼠(Dolichotispatagonum),其群居的形成仅仅是由于旱季食物资源短暂性聚集分布导致的,其他季节食物资源零星分布时并不形成群居[24];人为增加雌性或雄性黑田鼠[25](Microtusagrestis)后其社群结构并不改变;旱獭[26](Marmotacaudata)的种群大小与可利用食物资源无相关性。
2捕食风险假说
捕食风险指动物为躲避捕食者而改变其行为方式和生理状态付出的代价[27]。行为改变包括:活动模式和时间分配格局的改变[28-29];具体表现为选择相对安全但食物质量低的栖境[30-31]、减少取食频率和时间而相应地增加警觉时间[32-36]、增加对环境条件的敏感性[37]、增加间断性移动模式、食物选择及食谱改变[38]。啮齿类降低捕食风险主要通过以下几种机制:1、多眼效应(the‘many eyes effect’);2、自私的兽群效应(the‘selfish herd effect’);3、增加种群防御;4、稀释效应(the dilution effect)。多眼效应认为密度大的种群更易发现捕食者;自私的兽群效应认为捕食风险与其所处种群的位置相关(通常栖境外围的个体被捕食的风险较高);稀释效应最为简单,捕食风险随种群密度增加而降低(因种群数量增加每个个体被捕食的概率下降);种群防御机制(尤其对于攻击性强的啮齿类而言)认为能否成功击退捕食者与参与到防御中的个体数量相关。因此,捕食风险假说认为在高风险栖境中啮齿类群居普遍,同时捕食风险与栖境中植被高度、盖度密切相关[39]。
多眼效应认为捕食风险随种群大小而变。许多啮齿类行为学相关研究验证了这一点,如随着灌丛八齿鼠(Octodondegus)种群密度的增加,其发现人类捕食者的时间越早[40];高原鼠兔觅食时间随种群数量增加而上升,相反,其警戒和洞内时间却随种群密度增加而减少[35];除此而外,群居的田鼠(Microtusepiroticus)、棕背鼠平(Clethrionomysglareolus)和黄姬鼠(Apodemusflavicollis)被鼬袭击和猎杀的概率要低于独居个体[41];种群密度大的黑尾草原犬鼠(Cynomysludovicianus)和白尾草原犬鼠(Cynomysleucurus)相比小种群而言能够较早发现天敌从而进行有效躲避[42]。但亦有研究结果并不支持捕食风险假说,如Hayes等[43]发现灌丛八齿鼠种群大小与其存活率并无明显相关性。
黑尾草原犬鼠[44]、旱獭[45]和水豚[46]的行为研究验证了自私的兽群效应,相比核心区域的个体而言,领域外围的个体通常所需的警戒时间较长、警戒频率更高;另外,降低草原犬鼠密度后发现中央区域位置附近觅食的个体数明显增加,外围个体数减少[47]。
捕食风险与种群内的个体数量紧密相关,种群密度大时个体活动区域扩大[48]。草原犬鼠觅食区域与洞口距离的远近和种群密度密切相关,从一定程度上验证了稀释效应。这是因为捕食风险随种群密度增加而降低,相应的其活动范围就会扩大。
种群防御机制在野外观察中得到了证实。群居能减少被天敌袭击的概率,如水豚群居可减少野狗侵袭其幼崽[49];除此而外,还能有效地阻止同类入侵者,如雌性小家鼠[50](Musmusculus)和贝尔丁地松鼠[51](Spermophilusbeldingi)群居可降低同类入侵引起的杀婴行为。
啮齿类行为学和生态学相关研究表明植被盖度与捕食风险显著相关。自然生境中,有些啮齿类如长爪沙鼠[20](Merionesunguiculatus)、高原鼠兔[52](Ochotonacurzoniae)和豚鼠[53](Caviaaperea)在植被稀疏低矮的生境密度大,而另一些如布氏田鼠[54](Microtusbrandti)、白尾草原犬鼠[42]多栖息于植被盖度大的生境,造成这种生境的差异是啮齿类长期与自然环境相适应的结果。白足鼠(Peromyscusleucopus)、灰松鼠(Sciuruscarolinensis)和花栗鼠(Tamiasstriatus)在开阔生境中觅食时间减少,警戒时间显著增加[15]。捕食风险与植被盖度的关系在人为控制实验中也得到了验证。相比植被盖度低的生境而言,加氏鹿鼠[55](Clethrionomysgapperi)和小沙鼠[56](Gerbilluspyramidum)在植被盖度大的生境中受到袭击的概率较低;降低草原犬鼠密度后其会尽量避免栖息于开阔生境[57]。
虽然植被盖度与捕食风险的关系得到了验证,但仍受到许多不可控制因素的影响。首先,植被能在视觉上阻碍天敌发现猎物的几率[58];其次,与植被盖度相关的安全性与天敌类型有关[59]。如增加植被盖度会减少被飞禽类天敌发现的几率,但被爬行类捕食者发现的几率增加[60];再者,许多啮齿动物用鸣声和视觉(竖起尾巴)信号向同类传递风险信号,植被是否有利于声音和视觉信号传递取决于植被高度和声音的频率[42]。关于捕食风险对啮齿类种群的研究表明,捕食风险效应不但是影响猎物种群动态的一个重要因素,其对猎物种群动态的调控作用可能要大于直接捕杀[27]。
3社群温度调节假说
社群温度调节假说又称为能耗调节假说:在寒带和气候寒冷的地区,啮齿类为减少能耗、增加生存几率就会形成群居[61-62],个体的能量耗损与群居的数量呈负相关性[62]。有3种机制能解释小型动物蜷缩挤在一起降低能耗:1)减少暴露在空气中的体表面积有利于减少新陈代谢速率进而利于保存能量[63];2)洞穴中湿度和温度的增加会减少动物热量和水分损耗[40],因此环境湿度和温度的增加[64]利于体温调节;3)某些生理过程能调节体温[62]。
在室内条件下证实了动物紧紧拥簇可降低能耗、增加生存概率这一点,如裸鼢鼠[65](Heterocephalusglaber)、长爪沙鼠[66]、麝鼠[67](Ondatrazibethicus)、八齿鼠[64]、达马拉兰鼹鼠[68](Cryptomysdamarensis)、纳塔尔摩尔鼠[68](Cryptomyshottentotusnatalensis)和家兔[69](Oryctolaguscuniculus)等。野外观察结果也得出相同结论,当冬季来临时,南部飞鼠[70](Glaucomysvolans)、灰松鼠[71]、草原田鼠[72](Microtuspennsylvanicus)和纹鼠[73](Rhabdomyspumilio)单位洞系中的个体数明显增加;除此而外,鼠类的冬季存活率随窝巢内个体数量增加而增大、体重损耗量下降[74-75]亦从侧面验证了该点。
但也有一些室内和野外试验并不支持该假说,如草原犬鼠的能耗与季节变化无关,无显著差异[76];低温环境下独居的西伯利亚仓鼠(Phodopussungorus)和群居相比,尽管群居个体脂肪量较高、体况较好,但二者能耗并无明显区别[77];另外,冬眠性的黄腹土拨鼠(M.flaviventris)其群居性的亚成体平均日损耗量要大于独居个体也与该假说相矛盾[78]。
4旱区食物分布假说
Jarvis和Sherman[79]提出了旱区食物分布假说,该假说能够很好地解释干旱地区地下鼠形成群居的机制。由于地下鼠所处生境降水量小,土壤硬度大、食物呈簇状分布,因而地下鼠易形成群居。干旱生境中地下鼠群居有利于降低觅食成本,觅食成本包括挖掘洞道所耗能量和无收益觅食风险[80]。无收益觅食风险指到达食物分布区域过程中可能面临无任何食物获取而必须承担的风险[81]。干旱生境中食物资源呈斑块状聚集分布,由于地下鼠觅食无方向性,再加上地下觅食是高耗能活动[79-80,82-83],独居地下鼠常会因为不能及时发现足够维持自身生存的食物而导致无收益觅食风险增加,合作觅食有2个好处:1)发现食物的几率增加,2)减少单位个体能耗。
干旱生境会限制地下鼠的扩散,影响种群形成以及觅食的有效性。如干旱生境中隐鼠[84](Cryptomyshottentotushottentotus)种群的迁入率和迁出率要低于湿润地区,种群结构稳定;食物资源与洞系分形维数正相关,非洲鼹鼠[83](Fukomysmechowii)雨季洞系的分形维数和所能获取的食物资源要高于旱季,并且同一季节大种群的分形维数要大于小种群,说明大种群能增加觅食有效性;达马拉兰鼹鼠(Cryptomysdamarensis)的小种群生存下来的概率要低于大种群[82];除此而外,计算机模拟发现食物的簇状分布与土壤硬度紧密相关,干旱生境中独居物种觅食效率低下,而群居形成的合作觅食可降低无收益觅食风险[85]。
另外,还能从生理学角度解释该假说。群居形成的前提条件是个体的社会容忍度(宽容度)高,这对于那些攻击性强的物种尤为重要[86],由于攻击行为极其耗能和耗水[87],因此处于旱区啮齿类的群居很有可能是其为防止水分和能量损耗而减少攻击行为的副产物。攻击性程度与糖皮质激素水平正相关,对鼹鼠和豚鼠生物学、生态学和行为学方面的研究亦能解释该点[87-88]。
亦有研究与该假说相矛盾,如栖息于干旱生境中独居的霜鼠[89](Heliophobiusargenteocinereus)在食物质量低的栖境中亦能生存。
5生活史约束假说
Burda和Kawalika[90]提出了生活史约束假说,又有学者将其称为“共同抚养后代受益”假说[43](‘benefits of communal care’hypothesis)。该假说认为那些体型小、脂肪贮存能力低、生长速率慢的啮齿类为能成功繁衍后代不得不形成群居。体型小的独居啮齿类不能成功抚育后代[90]主要是因为体型小的物种发育速率缓慢,性成熟周期长,哺乳期雌性没有足够的脂肪抚养后代,因此需要很多成体参与抚育后代。达马拉兰鼹鼠和裸鼹鼠是滨属科体型最小的物种,它们的发育时间很长就验证了该假说[82,91-92]。共同抚育后代有诸多优点,如增强后代免疫功能[93]、减少寄生虫和病菌的感染几率[94],增强个体调控体温的能力[72]。
然而,Bennett等[95]活捕解剖哺乳期独居的雌性岬鼠(Georychuscapensis)和4种社会性的雌性隐鼠,发现均有脂肪堆积的现象,这与生活史约束假说矛盾。
6窝巢共享假说
群居与动物的生命周期、领域扩张及栖境的安全紧密相关[96],大多数啮齿类将洞系和窝巢作为规避极端天气、储存食物和冬眠的场所[97],因而洞系对啮齿类而言是一种极为关键重要的资源。由于天然避难所有限,而建造洞系对个体而言代价巨大,因而动物被迫共享洞系进而形成群居[98-99]。该假说认为构建洞穴的啮齿类更易形成群居。
自King[100]发现洞系资源与啮齿类社会制度紧密相关后,许多学者对此做了大量研究。如匈牙利小家鼠(Musspicilegus)在秋季建造土冢时(繁殖场所),由于建造土冢耗能巨大,个体并不能单独完成,因此需要很多个体参与,最后共享洞系形成群居[101];洞系亦是决定八齿鼠群居的关键因素[7,101];相比小种群而言,较大种群的八齿鼠能利用更多洞系资源[90];草原犬鼠独居和群居均有,但群居的洞系构造要比独居的复杂[76]。
尽管很多研究结果支持该假说,但亦有很多实验结论与之相悖。如相比独居的灌丛八齿鼠,群居并不会减少洞系建造的时间,这与洞系共享假说不符[99],但相比独居而言,群居个体平均推至地表的土壤要多,从长远来看,群居有利于其减少建造洞系所付出的代价;除此而外,亦有研究表明洞系资源并非是限制灌丛八齿鼠群居形成的真正原因[102];构筑洞系的豚鼠比不构筑洞系的更易形成较大的种群[103];水鼠平(Arvicolaterrestris)严重依赖洞道作为逃避捕食者的场所,尽管洞系建造成本较高,水鼠平也不会为分享洞道而形成群居[104];小豚鼠[105](Microcaviaaustralis)群居形成的真正原因并不是为减少能耗;还有许多独居地下鼠行为学研究结果与该假说相矛盾[12-13,106]。
7亲代投资假说
该假说认为群居是断奶后亲本持续性投资[107]致使子代推迟扩散导致的[108-110]。因而体型大的物种扩散延迟的可能性更大,因为即使食物充足,也要很长时间才能发育完全[107,109]。
群居啮齿类发育成熟所需的时间和扩散的时间呈正相关,而与生长季长短负相关。如温带地区松鼠生长周期的长短与积雪消融时间呈负相关。北美松鼠的生物学研究验证了亲代投资假说[111];生长周期长的土拨鼠发育成熟的时间早,扩散时间早[112]。也有实验结论与之矛盾,如北美土拨鼠(Marmotamonax)的社会性并不随生长季的长短发生变化[75];高山土拨鼠在亚成体阶段因食物因素不得不扩散[91]。
8小结
许多假说均能一定程度上解释啮齿类群居的原因,同时它们之间也并不相互排斥。例如,啮齿类群居既能够减少捕食风险,也能通过体温调节减少能耗。因此,在未来研究啮齿类群居因素时须考虑各个假说。例如,有些学者研究的焦点可能限制于旱区食物分布假说和生活史约束假说,然而,捕食风险假说和资源防卫假说有时却可能更为恰当。
啮齿类群居是综合考虑环境和自身因素利弊权衡后的结果。首先,群居并非是某个因素单独引起的,可能是很多因素综合作用导致的;其次,影响动物群居的决定性因素是随动物不断适应环境而变的,并非是一成不变;第三,与种群相关的其他社会属性如数量、社群关系的稳定性仍不清楚。以上3点需更复杂、精细、长周期的实验来验证。
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The evolutionary causes of rodent group-living: Hypotheses
WEI Wan-Rong1, MA An-Wei1, HE Kai2, ZHANG Wei-Guo1*
1.StateKeyLaboratoryofGrasslandAgro-ecosystems,CollegeofPastoralAgriculturalScienceandTechnology,LanzhouUniversity,Lanzhou730020,China; 2.RuralEnergyDevelopmentStationofQin’an,Qin’an741600,China
Abstract:This paper describes 7 hypotheses concerning group-living rodents which are accepted by most researchers. The resource-defense hypothesis believes that group-living individuals may become more efficient in obtaining and protecting resources than solitary-living conspecifics when resources (food, water, shelter) are non-uniformly distributed. The predatory risk hypothesis states that sociality should prevail in riskier habitats because group-living can reduce the risk of predation. The social thermoregulation hypothesis suggests that group-living could reduce the energy consumption in relatively cold habitats. The aridity food-distribution hypothesis believes that rodents living in arid habitats live in groups to share burrows or minimize the cost of burrow construction. The life-history constraint hypothesis thinks that rodents with smaller size, lower fat reserves, and low rate of postnatal growth are forced to live in groups to be able to successfully foster offspring. The burrow-sharing hypothesis states that rodents are forced to live in groups to share burrow use or minimize the cost of burrow construction. The parental investment hypothesis believes that, because of the continuing investment in offspring, group-living resulted from delay dispersion of offspring. Finally the paper discusses the future research focus on rodent group-living.
Key words:group-living; the resource-defense hypothesis; the predatory risk hypothesis; the social thermoregulation hypothesis; the aridity food-distribution hypothesis; the life-history constraint hypothesis; the burrow-sharing hypothesis; the parental investment hypothesis
*通信作者
Corresponding author. E-mail: wgzhang@lzu.edu.cn
作者简介:卫万荣(1988-),男,甘肃皋兰人,在读博士。E-mail:weiwr07@lzu.edu.cn
基金项目:公益性行业项目(201203041)资助。
*收稿日期:2015-11-17;改回日期:2015-12-28
DOI:10.11686/cyxb2015520
http://cyxb.lzu.edu.cn
卫万荣, 麻安卫, 何凯, 张卫国. 啮齿类动物群居起源研究假说. 草业学报, 2016, 25(4): 212-221.
WEI Wan-Rong, MA An-Wei, HE Kai, ZHANG Wei-Guo. The evolutionary causes of rodent group-living: Hypotheses. Acta Prataculturae Sinica, 2016, 25(4): 212-221.