2022, Vol. 29 
印记是动物对早期特定时期生活经历的一种终身难忘的记忆形式[1]。印记研究起始于鸟类。1930年，奥地利动物行为学家Lorenz[1]发现经人工孵化并由他养大的灰鹅会将他认为母亲，首次将这种生命早期经历的无条件习得记忆且对未来行为产生显著影响的过程定义为“印记”。Svåsand等[2]也论证了在哺乳动物中同样存在印记现象。随着印记的广泛研究，国内外学者相继在鸡、孔雀、小鼠等动物中均证实有印记现象，并发现印记具有不同的类型[3-5]。如崔勇华等[6]和耿慧等[7]研究发现仅雏鸡的印记就有嗅觉印记、视觉印记及听觉印记3种类型。
嗅觉印记是指通过嗅觉感知而产生的印记，是一种在早期生活史特殊阶段对特定嗅觉信息的学习记忆形式，且在以后生活中的某些特定情境中展现出的典型行为特征。嗅觉印记在一些鱼类的生殖洄游、归巢产卵中表现尤其明显。1978年Hasler等[8]通过对鲑科鱼类归巢(homing)行为的实验研究，首次提出鱼类嗅觉印记假说。随后在更多的鱼类中证实了嗅觉印记的存在[9-10]。国际上对嗅觉印记的生理基础、发生机制等方面的研究已逐渐系统深入，而国内相关研究仍十分有限。嗅觉印记与鱼类特定的生殖洄游、敌害预警、繁殖求偶等活动密切相关，对于珍稀濒危鱼类保护、资源养护及养殖生产均有重要的指导作用。因此，本文对鱼类嗅觉印记的相关研究进展进行简要综述，以期引起国内学者的关注，特别是在新时期渔业资源增殖养护及濒危水生动物保护中应注重嗅觉印记的潜在影响，为渔业资源保护与产业发展的科学管理决策提供参考。
1 鱼类嗅觉印记现象 1.1 生殖洄游中的归巢行为鱼类嗅觉印记最早在解释鲑科鱼类生殖洄游的归巢问题中提出。鲑科鱼类如太平洋鲑(Oncorhynchus spp.)[11]、大西洋鲑(Salmo salar)[12]普遍具有在繁殖时期准确地洄游至出生地溪流进行产卵的生殖洄游现象。Hasler等[8]针对这种鲑生殖洄游精准回归出生地的归巢(homing)行为提出嗅觉印记假说，即鲑在敏感时期对出生溪流中的氨基酸等嗅觉信息通过嗅觉产生印记(嗅觉印记)，这种印记一直保留并伴随鲑成长，待鲑成年后，这种印记会引导成年鲑探寻记忆中的氨基酸味道，从而准确地回归到自己的出生地。随后，相似的嗅觉印记行为现象在白亚口鱼(Cutostomus commersoni)[13]、虹鳟(Oncorhynchus mykiss)[14]等鱼类中得到验证。
1.2 回归定居行为和洄游性鱼类回归产卵场的行为类似，研究发现非洄游性的珊瑚礁鱼类中也存在嗅觉印记介导的回归定居行为[15-17]。珊瑚礁鱼类的幼鱼在进入成年栖息地之前，有一段浮游生活时期。浮游时期结束之后，大多数珊瑚礁鱼类选择定居于幼鱼时期生活的珊瑚礁，如对红小丑鱼(Amphiprion melanopus)研究发现，幼鱼浮游期结束后会选择孵化时期的同一个奶嘴海葵(Entacmaea quadricolor)作为栖息地[18-21]。这种行为表现为明显的回归定居行为。Arvedlund等[21]和Paris等[22-23]首次通过原位气味选择实验发现，雀鲷科(Pomacentridae)和天竺鲷科(Apogonidae)幼鱼能够在离海岸几公里的地方，从众多不同的珊瑚礁中识别出自己曾经栖息的珊瑚礁的气味，以气味作为导航信息改变自身的游泳速度和方向，实现回归定居。以上研究表明了嗅觉在珊瑚礁幼鱼选择栖息珊瑚礁的重要性，证明珊瑚礁幼鱼在出生时或者出生后不久形成了嗅觉印记，这种嗅觉印记控制珊瑚礁鱼类的回归定居行为。
1.3 亲缘识别鱼类能够对亲缘关系的特定信息产生印记。遇到其他鱼类时，将印记信息与其他鱼类的表达信息进行对比，可以在庞大的种群中识别具有血缘关系的亲属，从而实现与同种个体捕食协作或在繁殖中避免近亲繁殖[24-26]。鱼类亲缘识别的研究始于20世纪末，首先在鲑科鱼类的种群研究中发现。鲑科鱼类能够识别自身种群释放的化学信号，且研究证明幼鱼对本种群的气味信息表现出明显偏好，显示出对自身种群的特异性亲近行为[27]。随后，又有研究表明鱼类种群内个体的血缘关系也影响亲近行为。随后，研究表明鱼类种群内个体具有血缘关系，并非随机组成。鲑科鱼类[28]、三刺鱼[29](Gasterosteus aculeatus)以及其他鱼类都有排斥种内非亲属关系的行为表现，表明鱼类中存在亲缘识别行为。斑马鱼[30-31]能够在发育早期将亲属关系信息通过嗅觉进行印记，形成长期记忆，这属于亲属识别中的嗅觉印记行为。
2 嗅觉印记行为的发生时期鱼类嗅觉印记发生于鱼类早期生活阶段特定的短暂时期，以保证嗅觉印记的准确性。鲑科鱼类在胚胎期和幼鱼期的转化期间(parr-smolt transformation, PST)这两个时期是印记发生的主要时期，但不同鱼类嗅觉印记发生的具体时期不同。Havey等[32], Nevitt等[33]和Bett等[34]通过对实验鲑成鱼在两种气味选择的迷宫中进行测试，发现与对照组的鱼相比，在幼鱼期经历有氨基酸气味暴露6周后的成年鲑鱼在同种氨基酸的迷宫格中停留的时间比在幼鱼期经历只暴露1周或1天的成年鲑停留的时间明显更多。表明随着气味印记时间的增加，印记保真度越好。Quinn等[35]最近发现红鲑(Oncorhynchus gorbuscha)嗅觉印记发生在胚胎期的卵黄囊完全吸收至孵化前。对斑马鱼亲属印记机制研究发现，斑马鱼的嗅觉印记时间为胚胎受精6 d后的24 h内，过早或过晚的给予信息物质暴露，都不能形成嗅觉印记。
3 鱼类嗅觉印记的信号物质 3.1 氨基酸氨基酸是引发归巢行为嗅觉印记的主要信号物质。Hasler等[8]1978年提出的嗅觉印记假说认为鲑幼鱼将原出生溪流中的氨基酸作为嗅觉印记的信号分子，鲑成鱼则依赖于这种氨基酸信号分子进行长距离生殖洄游的归巢行为。Yamamoto等[36-37]通过测定日本北海道大马哈鱼(Oncorhynchus keta)生长河流中的氨基酸浓度随季节和年份的变化验证了这一猜想。研究发现河流中丙氨酸、天冬氨酸、谷氨酸、甘氨酸、亮氨酸、丝氨酸和缬氨酸等7种氨基酸浓度比较稳定，因此推测溪流中游离氨基酸组成的长期稳定性可能对鲑的嗅觉印记行为至关重要。嗅觉系统对氨基酸敏感性的研究从生理基础上加深了氨基酸可以作为嗅觉印记信号物质的可能性。Cole等[38]和Schmachtenbery等[39]研究发现大多数鱼类均能通过嗅觉系统检测到所有类型氨基酸；通过嗅觉电生理技术已证实嗅觉神经元对氨基酸十分敏感[40-41]。在分子层面已经发现鱼类嗅觉上皮中含有L-氨基酸结合蛋白[42]和基因受体，直接证实这一猜想。在大马哈鱼鱼脑中的鉴定发现了构成N-甲基-D-天门冬氨酸受体(N-methyl-D-aspartate recepto)必需亚基NR1的基因。Hinz等[43]通过实验证明，N-甲基-D-天门冬氨酸受体作为谷氨酸受体的一种亚型，能够影响嗅觉印记的功能开关。
3.2 MHC多肽MHC多肽是气味的一种成分，在鱼类体内由MHC基因表达。MHC II基因已经在斑马鱼中鉴定得到[44]。研究斑马鱼亲缘识别行为中的嗅觉印记时期和机制时，幼鱼在与其拥有MHC II类等位基因的兄弟姐妹身上留下印记，对兄弟姐妹的嗅觉偏好在斑马鱼还处于性发育未成熟阶段，已表现出亲近行为[45]。但成鱼阶段，雌性会避开亲缘雄性的气味，用人工合成的MHC II类肽作为印记敏感期的信息物质，不仅证明斑马鱼对MHC II类肽有行为偏好，也可以引发亲缘识别现象的发生，表明MHC II类肽是亲缘识别中的信息物质[46]。除了MHC II类肽，在鱼类和其他水生物种的亲缘识别中发现，尿液、黏液和鳃释放的信息物质在亲缘识别嗅觉印记中也发挥着重要作用[47]。
3.3 其他可能引发嗅觉印记的信号分子水环境中存在的鱼类性信息素，如类固醇，前列腺素等，均是由性腺分泌的脂质物质，能够引起同种鱼类产生繁殖反应。1988年Sorensen等[48]首次描述了排卵雌性金鱼释放前列腺素F2α及其代谢物15-酮-前列腺素F2α，并激活雄性金鱼的嗅觉感觉神经元诱导吸引和求偶行为。研究发现前列腺素F2α特异性地激活斑马鱼体内的两种不同敏感度的嗅觉受体，并在不同群体的纤毛嗅觉神经元中表达[49-50]。Sato等[51]发现雄性金鱼成鱼的嗅觉神经元对性激素敏感。嗅上皮嗅觉神经元中存在性信息素受体，能与水中的性信息素物质结合，利用GPCRs，使cAMP增加，激活环核苷酸门控通道(cyclicnucleotidegated, CNG)的开启，产生动作电位，将信息传至大脑，通过下丘脑-脑垂体-性腺轴的反馈调控作用于鱼的生殖生理过程。能够引起鱼类嗅觉反应的性信息素是否可以作为嗅觉印记的信息物质，仍然需要进一步研究。另外，更广泛的嗅觉行为，如在鱼类摄食偏好、防御敌害等表现出的典型行为是否被归类为嗅觉印记行为仍需要进一步研究验证；能够引起鱼类嗅觉反应的警报信息素，是否可以作为嗅觉印记的信息物质，也需要进一步研究。
4 鱼类嗅觉印记的发生与调控 4.1 嗅觉印记的发生嗅觉印记的发生与嗅觉器官发生密切相关，嗅觉上皮中嗅觉感受神经元是一种具有高度灵敏性的双极神经元细胞。迄今为止，已经发现了5种类型的嗅觉感受神经元(olfactory receptor neurons, OSNs)：纤毛OSNs、微绒毛OSNs、梨形OSNs、隐窝OSNs和Kappe OSNs[52]。不同的嗅觉感受神经元中存在不同的嗅觉受体蛋白。研究发现，气味分子，如氨基酸、胆汁酸盐、核苷、多胺和信息素等水溶性分子均能与嗅觉感受神经元上的嗅觉受体蛋白结合。嗅觉受体蛋白多为G蛋白耦连受体(G protein-coupledreceptors, GPCRs)，与溶于水中的信号分子，如氨基酸结合后，引起细胞内cAMP浓度增加，促使环核苷酸门控通道(cyclic nucleotide gated, CNG)开启，引起Na+、Ca2+向细胞内流动，Cl-向细胞外流动，使细胞膜产生去极化[53-55]。通过嗅觉感受神经元将感官知觉转化为电信号，转导至紧连于嗅囊后方呈橄榄状的嗅球，再经过嗅束将信息传递至端脑进行处理[56-57]。Gerlach等[58]通过荧光染色的方式发现气味分子MHC多肽相关的钙调蛋白激酶在鱼脑的背侧嗅球高表达，证实斑马鱼嗅觉印记形成可能由此途径发生。同时也提出MHC多肽气味分子会与OSN中隐窝细胞嗅觉受体进行结合。Biechl等[59]在研究斑马鱼亲缘识别行为中的嗅觉印记机制时发现，嗅觉印记形成后的斑马鱼幼鱼和对照组相比，隐窝细胞的总数虽然没有差异，但印记形成后的斑马鱼幼鱼在气味刺激后激活的隐窝细胞数量明显高于对照组，说明在产生嗅觉印记幼鱼的特定嗅觉感受神经元OSN中观察到的较高的神经元活动与这些OSN数量的增加无关，因此嗅觉印记可能与气味感受器本身的结合敏感性有关。
4.2 嗅觉印记的调控鱼类嗅觉印记发生于幼年时期，成鱼需要对嗅觉印记回忆(retrieval)才能准确地进行洄游归巢、回归定居地以及种内和种间识别等行为。Hasler等[8]首先提出鱼类嗅觉印记的敏感发育时期与甲状腺激素的调控有关。在红鲑[60-61]等鱼类的研究中发现胚胎期至幼鱼期转化时期时期，血浆甲状腺激素水平会增加。随着研究的深入，鱼类PST时期甲状腺激素水平升高这一结果已经得到广泛认可。Lema等[62]通过测定鲑PST时期甲状腺激素水平和嗅觉上皮细胞的细胞密度变化，证实在PST时期，甲状腺激素可以诱导鲑嗅觉神经元细胞增殖，甚至微小的甲状腺素浓度变化都与嗅觉细胞增殖有关，从而证明了鱼类嗅觉印记的发生与甲状腺激素的调节有关。
嗅觉印记和洄游归巢行为的激素调控过程在大马哈鱼中得到了较清晰的解答。Ueda等[42]于2015年在大马哈鱼脑中克隆并鉴定出表达N-甲基-D-天门冬氨酸受体(N-methyl-D-aspartate recepto)必需亚基NR1基因。研究发现在大马哈鱼嗅觉印记发生时期，幼鱼脑中NR1和促甲状腺素释放激素(thyrotropin-releasing hormone, TRH)的基因表达上调，而NR1和促性腺激素释放激素(gonadotropin-releasing hormone, GnRH)基因在成鱼归巢到洄游过程中的表达上调。并且用甲状腺激素处理幼鱼能够提高了NR1基因的活性，用GnRH处理成鱼处理提高了大马哈鱼对溪流气味的辨别能力。这表明NR1基因在嗅觉印记行为发生过程中有着关键作用，这种作用在幼鱼时期受到促甲状腺素释放激素TRH调节，在成鱼时期受到促性腺激素释放激素GnRH的调节。但是NR1基因的具体作用以及调节机制尚待进一步解答[63-64]。
5 环境变化对鱼类嗅觉印记的影响人类活动污染，例如，农业面源污染、城市污水、工业废水、医疗化学物质导致的环境污染是对鱼类嗅觉及嗅觉印记产生影响的主要因素。研究发现，广泛应用于渔业生产中的有机磷杀虫剂二嗪磷能造成波斯鲟(Acipenser persicus)嗅上皮细胞损伤以及降低其全身甲状腺素和三碘甲状腺原氨酸，进而影响波斯鲟嗅觉印记的发生[65]。一种用于防治海鳗的农药杀鳗酚(3-trifluoromethyl-4-nitrophenol, TFM)也被发现对湖鲟(Acipenser fulvescens)幼鱼嗅觉神经元有抑制作用，导致湖鲟的嗅觉敏感度降低[66]，影响湖鲟嗅觉印记行为中的信号转导过程。
全球变暖导致的二氧化碳水平升高和海洋酸化(H+升高，pH降低)同样影响鱼类嗅觉印记。研究表明，海洋环境酸化会影响珊瑚鱼的回归定居行为[67]。Porteus等[68]研究发现，溶解有高浓度二氧化碳的海水会降低欧洲鲈(Dicentrarchus labrax)嗅觉系统敏感性，嗅觉上皮和嗅球中细胞组织的转录水平差异表明造成敏感性降低的原因是海洋酸化导致嗅觉神经的信号传导受到影响。
6 鱼类嗅觉印记行为研究展望与应用前景鱼类的嗅觉印记在国际上已有较多深入研究，特别是嗅觉电生理技术的发展与应用提高了嗅觉感应能力和灵敏度的测量精度，从而提高了嗅觉印记的测试验证水平；目前已开展细胞水平神经元的信号转导过程研究，并试图从分子层面揭示嗅觉印记产生的机制，相关内容已成为研究热点。如在大马哈鱼中鉴定得到的鱼类嗅觉印记关键基因NR1基因，其表达产物NR1亚基是N-甲基-D-天冬氨酸受体(NMDAR)的必需亚基。而在脊椎动物中，NMDAR是谷氨酸受体通道的一种亚型，可以介导中枢神经系统的大部分快速兴奋性突触传递[69]。因此，谷氨酸是否是大马哈鱼和其他鱼类嗅觉印记发生过程中神经传导的神经递质，需要进一步验证。NR1基因是嗅觉印记发生的开关，而TRH和GnRH是打开开关的关键激素，激素如何调节NR1基因的表达仍未清晰解答[42]。
国内关于鱼类嗅觉印记的研究还很少，关注度不够，尚属起步阶段，有关研究聚焦在嗅觉器官对于信号分子氨基酸的敏感性筛选等基础研究阶段[70]。例如，我国在刀鲚(Coilia nasus)嗅觉基因表达方面获得新的进展[71]，研究发现刀鲚性腺和嗅囊中主嗅觉受体基因MORs基因表达量明显高于其他组织，且洄游型刀鲚比定居型刀鲚嗅囊的MOR-4K13和MOR-51I2表达量高，基因层面揭示了主嗅觉受体基因MORs在嗅觉印记中有重要作用；刀鲚性腺中MORs基因高表达是否与刀鲚洄游归巢行为密切关联尚无明确答案。
嗅觉印记的研究可以为鱼类保护和渔业生产提供新思路。近年来增殖放流的鲑在洄游过程中会出现迷途问题，致使其不能回到产卵场产卵，严重影响了增殖放流效果[72]。我国增殖放流效果也存在同样问题。基于嗅觉印记的研究，Dittman等[73]提出促进放流鲑形成嗅觉印记的方法。他们通过将胚胎期鲑移到产卵场附近的繁育初孵场，建立不同的实验组，发现经过胚胎期的环境改善，促进了印记的形成，从而提高了人工繁育放流鲑的归巢精度，显著提升了增殖放流效果。这一成功案例提示针对洄游性鱼类的保护中注重嗅觉印记的重要性。针对目前内陆流域渔业资源衰退的现状以及增殖放流效果不佳的问题，在开展鱼类保护研究中不仅要考虑洄游通道、栖息地的物理环境要素变迁问题，还要考虑水质污染等环境变化对河流化学环境因素的影响。对于江海洄游性鱼类，如中华鲟(Acipenser sinensis)，不仅关注产卵场本身的栖息环境状况，还要考虑水体污染等可能对鱼类回归产卵场本能的影响。以资源养护为目标的增殖放流应该充分评估苗种繁育基地的水源、放流位点和放流时间，以提高放流回归率。随着对嗅觉印记的深入理解，一些名贵经济鱼类的开口饵料、摄食驯化、食性转换等问题的解决对于产业技术突破有重要的借鉴意义，其在渔业中的应用研究值得重视。
| [1] |
Lorenz K. Der kumpan in der umwelt des vogels[J]. Journal für Ornithologie, 1935, 83(3): 289-413..》Google Scholar
|
| [2] |
Svåsand T, Skilbrei O T, van der Meeren G I, et al. Review of morphological and behavioural differences between reared and wild individuals: Implications for sea-ranching of Atlantic salmon, Salmo salar L., Atlantic cod, Gadus morhua L., and European lobster, Homarus gammarus L.[J]. Fisheries Management and Ecology, 1998, 5(6): 473-490..》Google Scholar
|
| [3] |
McCabe B J. Visual imprinting in birds: Behavior, models, and neural mechanisms[J]. Frontiers in Physiology, 2019, 10: 658..》Google Scholar
|
| [4] |
Liu B X. An analysis of the imprint behavior of several birds[J]. Shangdong Poultry, 1995(4): 34-35 [刘冰许. 试析几种鸟类的印记行为[J]. 山东家禽，1995(4) : 34-35.].》Google Scholar
|
| [5] |
SanMiguel J M, Bartolomei M S. DNA methylation dynamics of genomic imprinting in mouse development[J]. Biology of Reproduction, 2018, 99(1): 252-262..》Google Scholar
|
| [6] |
Cui Y H, Zhu Y H. The filial imprinting of young chick as A model system for memory studies[J]. Laboratory Animal Science and Administration, 2004, 21(4): 40-42. [崔勇华，朱玉华. 利用小鸡印记行为建立学习记忆模型[J]. 实验动物科学与管理，2004, 21(4): 40-42.].》Google Scholar
|
| [7] |
Geng H, Li D F. Neural mechanism of the early memory formation in chicks[J]. Life Science Research, 2005, 9(3): 196-201. [耿慧，李东风. 小鸡早期记忆形成的神经机制[J]. 生命科学研究，2005, 9(3): 196-201.].》Google Scholar
|
| [8] |
Hasler A D, Scholz A T. Olfactory Imprinting and Homing in Salmon: Investigations into the Mechanism of the Imprinting Process[M]. Berlin: Springer-Verlag, 1983..》Google Scholar
|
| [9] |
Dixson D L, Jones G P, Munday P L, et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish[J]. Oecologia, 2014, 174(1): 99-107..》Google Scholar
|
| [10] |
Gerlach G, Hodgins-Davis A, Avolio C, et al. Kin recognition in zebrafish: A 24-hour window for olfactory imprinting[J]. Proceedings Biological Sciences, 2008, 275(1647): 2165-2170..》Google Scholar
|
| [11] |
Ueda H. Physiological mechanisms of imprinting and homing migration in Pacific salmon Oncorhynchus spp.[J]. Journal of Fish Biology, 2012, 81(2): 543-558..》Google Scholar
|
| [12] |
Svåsand T, Skilbrei O T, van der Meeren G I, et al. Review of morphological and behavioural differences between reared and wild individuals: Implications for sea-ranching of Atlantic salmon, Salmo salar L., Atlantic cod, Gadus morhua L., and European lobster, Homarus Gammarus L.[J]. Fisheries Management and Ecology, 1998, 5(6): 473-490..》Google Scholar
|
| [13] |
Werner R G, Lannoo M J. Development of the olfactory system of the white sucker, Catostomus commersoni, in relation to imprinting and homing: A comparison to the salmonid model[J]. Environmental Biology of Fishes, 1994, 40(2): 125-140..》Google Scholar
|
| [14] |
Keefer M L, Peery C A, High B. Behavioral thermoregulation and associated mortality trade-offs in migrating adult steelhead (Oncorhynchus mykiss): Variability among sympatric populations[J]. Canadian Journal of Fisheries and Aquatic Sciences, 2009, 66(10): 1734-1747..》Google Scholar
|
| [15] |
Swearer S E, Caselle J E, Lea D W, et al. Larval retention and recruitment in an island population of a coral-reef fish[J]. Nature, 1999, 402(6763): 799-802..》Google Scholar
|
| [16] |
Dixson D L, Jones G P, Munday P L, et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish[J]. Oecologia, 2014, 174(1): 99-107..》Google Scholar
|
| [17] |
Coppock A G, Gardiner N M, Jones G P. Olfactory discrimination in juvenile coral reef fishes: Response to conspecifics and corals[J]. Journal of Experimental Marine Biology and Ecology, 2013, 443: 21-26..》Google Scholar
|
| [18] |
Swearer S E, Caselle J E, Lea D W, et al. Larval retention and recruitment in an island population of a coral-reef fish[J]. Nature, 1999, 402(6763): 799-802..》Google Scholar
|
| [19] |
Dixson D L, Jones G P, Munday P L, et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish[J]. Oecologia, 2014, 174(1): 99-107..》Google Scholar
|
| [20] |
Coppock A G, Gardiner N M, Jones G P. Olfactory discrimination in juvenile coral reef fishes: Response to conspecifics and corals[J]. Journal of Experimental Marine Biology and Ecology, 2013, 443: 21-26..》Google Scholar
|
| [21] |
Arvedlund M, McCormick M I, Fautin D G, et al. Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae)[J]. Marine Ecology Progress Series, 1999, 188: 207-218..》Google Scholar
|
| [22] |
Paris C B, Cowen R K. Direct evidence of a biophysical retention mechanism for coral reef fish larvae[J]. Limnology and Oceanography, 2004, 49(6): 1964-1979..》Google Scholar
|
| [23] |
Paris C B, Atema J, Irisson J O, et al. Reef odor: A wake up call for navigation in reef fish larvae[J]. PLoS ONE, 2013, 8(8): e72808..》Google Scholar
|
| [24] |
Hepper P G. Kin recognition: Functions and mechanisms. A review[J]. Biological Reviews of the Cambridge Philosophical Society, 1986, 61(1): 63-93..》Google Scholar
|
| [25] |
Tang-Martinez Z. The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: A critical re-evaluation[J]. Behavioural Processes, 2001, 53(1-2): 21-40..》Google Scholar
|
| [26] |
Groot C, Quinn T P, Hara T J. Responses of migrating adult sockeye salmon (Oncorhynchus nerka) to population-specific odours[J]. Canadian Journal of Zoology, 1986, 64(4): 926-932..》Google Scholar
|
| [27] |
Courtenay S C, Quinn T P, Dupuis H M C, et al. Factors affecting the recognition of population-specific odours by juvenile coho salmon[J]. Journal of Fish Biology, 1997, 50(5): 1042-1060..》Google Scholar
|
| [28] |
Folke C, Olsén H, Winberg S, et al. Differences inrheotactic response and attraction to population-specific odours in Baltic salmon (Salmo salar L.) parr[J]. Nordic Journal of Freshwater Research, 1997, 67: 45-51..》Google Scholar
|
| [29] |
Van Havre N, Fitzgerald G J. Shoaling and kin recognition in the threespine stickleback (Gasterosteus aculeatus L.)[J]. Biology of Behaviour, 1988, 13: 190-201..》Google Scholar
|
| [30] |
Bakker T, Frommen J. Adult three-spined sticklebacks prefer to shoal with familiar kin[J]. Behaviour, 2004, 141(11-12): 1401-1409..》Google Scholar
|
| [31] |
Khodaei L, Long T A F. Kin recognition and co-operative foraging in Drosophila melanogaster larvae[J]. Journal of Evolutionary Biology, 2019, 32(12): 1352-1361..》Google Scholar
|
| [32] |
Havey M A, Dittman A H, Quinn T P, et al. Experimental evidence for olfactory imprinting by sockeye salmon at embryonic and smolt stages[J]. Transactions of the American Fisheries Society, 2017, 146(1): 74-83..》Google Scholar
|
| [33] |
Nevitt G A, Dittman A H, Quinn T P, et al. Evidence for a peripheral olfactory memory in imprinted salmon[J]. Proceedings of the National Academy of Sciences of the United States of America, 1994, 91(10): 4288-4292..》Google Scholar
|
| [34] |
Bett N N, Hinch S G, Dittman A H, et al. Evidence of olfactory imprinting at an early life stage in pink salmon (Oncorhynchus gorbuscha)[J]. Scientific Reports, 2016, 6: 36393..》Google Scholar
|
| [35] |
Quinn T P, Stewart I J, Boatright C P. Experimental evidence of homing to site of incubation by mature sockeye salmon, Oncorhynchus nerka[J]. Animal Behaviour, 2006, 72(4): 941-949..》Google Scholar
|
| [36] |
Yamamoto Y, Ueda H. Behavioral responses by migratory chum salmon to amino acids in natal stream water[J]. Zoological Science, 2009, 26(11): 778-782..》Google Scholar
|
| [37] |
Yamamoto Y, Shibata H, Ueda H. Olfactory homing of chum salmon to stable compositions of amino acids in natal stream water[J]. Zoological Science, 2013, 30(8): 607-612..》Google Scholar
|
| [38] |
Cole T B, Stacey N E. Olfactory responses to steroids in an African mouth-brooding cichlid, Haplochromis burtoni (Gunther)[J]. Journal of Fish Biology, 2006, 68(3): 661-680..》Google Scholar
|
| [39] |
Schmachtenberg O, Bacigalupo J. Olfactory transduction in ciliated receptor neurons of the Cabinza grunt, Isacia conceptionis (Teleostei: Haemulidae)[J]. European Journal of Neuroscience, 2004, 20(12): 3378-3386..》Google Scholar
|
| [40] |
Hassenklöver T, Pallesen L P, Schild D, et al. Amino acid-vs. peptide-odorants: Responses of individual olfactory receptor neurons in an aquatic species[J]. PLoS One, 2012, 7(12): e53097..》Google Scholar
|
| [41] |
Awonfor F, Yajun W, Na Y, et al. Transcriptome analysis reveals L-amino acids as olfactory stimulant in the large yellow croaker (Larimichthys crocea)[J]. Journal of Aquaculture Research & Development, 2017, 8(3): 25-29..》Google Scholar
|
| [42] |
Ueda H, Nakamura S, Nakamura T, et al. Involvement of hormones in olfactory imprinting and homing in chum salmon[J]. Scientific Reports, 2016, 6: 21102..》Google Scholar
|
| [43] |
Hinz C, Namekawa I, Behrmann-Godel J, et al. Olfactory imprinting is triggered by MHC peptide ligands[J]. Scientific Reports, 2013, 3: 2800..》Google Scholar
|
| [44] |
Gerlach G, Lysiak N. Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching[J]. Animal Behaviour, 2006, 71(6): 1371-1377..》Google Scholar
|
| [45] |
Gerlach G, Hodgins-Davis A, Avolio C, et al. Kin recognition in zebrafish: A 24-hour window for olfactory imprinting[J]. Proceedings Biological Sciences, 2008, 275(1647): 2165-2170..》Google Scholar
|
| [46] |
Brönmark C, Hansson L A. Chemical Ecology In Aquatic Systems[M]. Oxford: Oxford University Press, 2012..》Google Scholar
|
| [47] |
Ono R D. Structure of tendon organs in fishes of the genus Polymixia[J]. Zoomorphology, 1982, 99(2): 131-144..》Google Scholar
|
| [48] |
Sorensen P W, Hara T J, Stacey N E, et al. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish[J]. Biology of Reproduction, 1988, 39(5): 1039-1050..》Google Scholar
|
| [49] |
Cong X J, Zheng Q, Ren W W, et al. Zebrafish olfactory receptors ORAs differentially detect bile acids and bile salts[J]. Journal of Biological Chemistry, 2019, 294(17): 6762-6771..》Google Scholar
|
| [50] |
Won Y J, Ono F, Ikeda S R. Identification and modulation of voltage-gated Ca2+ currents in zebrafish Rohon-Beard neurons[J]. Journal of Neurophysiology, 2011, 105(1): 442-453..》Google Scholar
|
| [51] |
Sato K, Sorensen P W. The chemical sensitivity and electrical activity of individual olfactory sensory neurons to a range of sex pheromones and food odors in the goldfish[J]. Chemical Senses, 2018, 43(4): 249-260..》Google Scholar
|
| [52] |
Yoshihara Y. Molecular genetic dissection of the zebrafish olfactory system[M]//Results and Problems in Cell Differentiation. Berlin, Heidelberg: Springer Berlin Heidelberg, 2008: 1-19..》Google Scholar
|
| [53] |
Johnstone K A, Lubieniecki K P, Koop B F, et al. Identification of olfactory receptor genes in Atlantic salmon Salmo salar[J]. Journal of Fish Biology, 2012, 81(2): 559-575..》Google Scholar
|
| [54] |
Oka Y, Saraiva L R, Korsching S I. Crypt neurons express a single V1R-related ora gene[J]. Chemical Senses, 2011, 37(3): 219-227..》Google Scholar
|
| [55] |
Reed R R, Bakalyar H A, Cunningham A M, et al. The molecular basis of signal transduction in olfactory sensory neurons[J]. Society of General Physiologists Series, 1992, 47: 53-60..》Google Scholar
|
| [56] |
Thommesen G. The spatial distribution of odour induced potentials in the olfactory bulb of char and trout (Salmonidae)[J]. Acta Physiologica Scandinavica, 1978, 102(2): 205-217..》Google Scholar
|
| [57] |
Elham F, Pouya D B. Fish Behaviors in Electromagnetic Fields[J]. Molecular Biomarkers & Diagnosis,2018,9(1): 12..》Google Scholar
|
| [58] |
Gerlach G, Tietje K, Biechl D, et al. Behavioural and neuronal basis of olfactory imprinting and kin recognition in larval fish[J]. Journal of Experimental Biology, 2019, 222 (suppl 1): jeb189746..》Google Scholar
|
| [59] |
Biechl D, Tietje K, Gerlach G, et al. Crypt cells are involved in kin recognition in larval zebrafish[J]. Scientific Reports, 2016, 6: 24590..》Google Scholar
|
| [60] |
Dittman A, Quinn T. Homing in Pacific salmon: Mechanisms and ecological basis[J]. Journal of Experimental Biology, 1996, 199(Pt 1): 83-91..》Google Scholar
|
| [61] |
Ojima D, Iwata M. The relationship between thyroxine surge and onset of downstream migration in chum salmon Oncorhynchus keta fry[J]. Aquaculture, 2007, 273(2-3): 185-193..》Google Scholar
|
| [62] |
Lema S C, Nevitt G A. Evidence that thyroid hormone induces olfactory cellular proliferation in salmon during a sensitive period for imprinting[J]. The Journal of Experimental Biology, 2004, 207(Pt 19): 3317-3327..》Google Scholar
|
| [63] |
Martin S J, Grimwood P D, Morris R G. Synaptic plasticity and memory: An evaluation of the hypothesis[J]. Annual Review of Neuroscience, 2000, 23: 649-711..》Google Scholar
|
| [64] |
Hosseinzadeh M, Amiri B M, Poorbagher H, et al. The effects of diazinon on the cell types and gene expression of the olfactory epithelium and whole-body hormone concentrations in the Persian sturgeon (Acipenser persicus)[J]. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2020, 250: 110809..》Google Scholar
|
| [65] |
Sakamoto K, Dew W A, Hecnar S J, et al. Effects of lampricide on olfaction and behavior in young-of-the-year lake sturgeon (Acipenser fulvescens)[J]. Environmental Science & Technology, 2016, 50(7): 3462-3468..》Google Scholar
|
| [66] |
Dixson D L, Jennings A R, Atema J, et al. Odor tracking in sharks is reduced under future ocean acidification conditions[J]. Global Change Biology, 2015, 21(4): 1454-1462..》Google Scholar
|
| [67] |
Green L, Jutfelt F. Elevated carbon dioxide alters the plasma composition and behaviour of a shark[J]. Biology Letters, 2014, 10(9): 20140538..》Google Scholar
|
| [68] |
Porteus C S, Hubbard P C, Uren Webster T M, et al. Near-future CO2 levels impair the olfactory system of a marine fish[J]. Nature Climate Change, 2018, 8(8): 737-743..》Google Scholar
|
| [69] |
Martin S J, Grimwood P D, Morris R G. Synaptic plasticity and memory: An evaluation of the hypothesis[J]. Annual Review of Neuroscience, 2000, 23: 649-711..》Google Scholar
|
| [70] |
Wei K, Cai H Y, Chen C S, et al. Olfactory response to amino acids in Brachymystax lenok[J]. Marine Fisheries, 2018, 40(6): 728-733. [魏凯，蔡红英，陈春山，等. 细鳞鲑对水溶性氨基酸的嗅觉行为反应[J]. 海洋渔业，2018, 40(6): 728-733.].》Google Scholar
|
| [71] |
Wang X M, Zhu G L, Tang W Q. Cloning, sequence analysis and tissues expression of Coilia nasus olfactory receptor gene mor-51i2[J]. Acta Hydrobiologica Sinica, 2017, 41(1): 33-42. [王晓梅，朱国利，唐文乔. 刀鲚嗅觉受体基因MOR-51I2克隆、序列分析及组织表达[J]. 水生生物学报，2017, 41(1): 33-42.].》Google Scholar
|
| [72] |
Rand P S, Berejikian B A, Bidlack A, et al. Ecological interactions between wild and hatchery salmonids and key recommendations for research and management actions in selected regions of the North Pacific[J]. Environmental Biology of Fishes, 2012, 94(1): 343-358..》Google Scholar
|
| [73] |
Dittman A H, Pearsons T N, May D, et al. Imprinting of hatchery-reared salmon to targeted spawning locations: A new embryonic imprinting paradigm for hatchery programs[J]. Fisheries, 2015, 40(3): 114-123..》Google Scholar
|