摘要：For centuries, humans have been fascinated by how migratory animals find their way over thousands of kilometres. Here, I review the mechanisms used in animal orientation and navigation with a particular focus on long-distance migrants and magnetoreception. I contend that any long-distance navigational task consists of three phases and that no single cue or mechanism will enable animals to navigate with pinpoint accuracy over thousands of kilometres. Multiscale and multisensory cue integration in the brain is needed. I conclude by raising twenty important mechanistic questions related to long-distance animal navigation that should be solved over the next twenty years.
如何下的结论？可信性如何？如何实验证明？你又不是鸟 怎知鸟的机理 身体构造
几个世纪以来，人类一直着迷于迁徙动物是如何在数千公里之外找到它们的路的。在这里，我回顾了动物定向和导航中使用的机制，特别关注远距离迁徙和磁接收（particularly focus on）。我认为，任何远程导航任务都由三个阶段组成，没有任何单一的提示或机制能够使动物在数千公里的范围内精确导航。大脑需要多尺度和多感官的线索整合。最后，我提出了20个与远程动物导航相关的重要机械问题，这些问题将在未来20年内得到解决。
each year, billions of small songbirds (Fig. 1a), with ‘birdbrains’ weighing only a few grams, leave their Arctic and temperate breeding areas to overwinter in the tropics and subtropics. Most migrate at night, and young birds do so without regular contact with experienced individuals. Thus, their navigational capabilities must be innate or learned before their first departure1–5. After having completed one round trip, many adult birds are able to navigate with an ultimate precision of centimetres over distances of 5,000 km or more6. Other impressive navigational tasks mastered by birds include bar-tailed godwits (Limosa lapponica, Fig. 1b) migrating from Alaska to New Zealand in a single non-stop flight lasting 7–9 days and nights 7, arctic terns (Sterna paradisaea) breeding around the North Pole and wintering around the South Pole8, and sea-birds (Fig. 1c) flying more than 100,000 km per year to return to tiny islands in the middle of vast oceans to breed9,10
每年，数十亿只“鸟脑”只有几克重的小型鸣禽（图1a）离开北极和温带繁殖区，在热带和亚热带越冬。大多数在夜间迁徙，幼鸟在没有与有经验的个体定期接触的情况下也会这样做。因此，他们的导航能力必须是天生的或在第一次出发前就学会的。成一次往返飞行后，许多成年鸟类能够在5000公里或更长的距离内以厘米的终极精度进行导航。其他令人印象深刻的由鸟类掌握的导航任务，包括斑尾塍鹬（Limosa Lapponica，图1b）从阿拉斯加迁移到新西兰的单程不间断飞行，持续7-9天昼夜不停，北极燕鸥（Sterna Paradisea）在北极繁殖，在南极过冬，和海鸟（图1c）飞行超过每年10万公里，返回大洋中部的小岛繁殖。
Even insects with much simpler brains than birds are capable of performing impressive navigational tasks11–18. In autumn, Monarch but-terflies (Danaus plexippus, Fig. 1d) migrate from the USA and Canada to very specific overwintering trees in Mexico, up to 3,000 km away11. A year later, the third-to-fifth-generation descendants of the previous year’s autumn migrants return to the exact same trees in Mexico11. A similarly impressive return migration—but involving only a single gen-eration—occurs in Southeast Australia, where millions of Bogong moths (Agrotis infusa, Fig. 1e) fill the night skies on their way to and from their yearly aestivation caves in the Snowy Mountains18. Recently, Chapman et al.17,19,20 demonstrated that directed long-distance return migrations are also widespread among high-flying insects. These movements of trillions of individual insects are critical for understanding both natural and man-made ecosystems21.
即使是大脑比鸟类简单得多的昆虫也能执行令人印象深刻的导航任务。秋季，帝王蝶（Danaus Plexippus，图1d）从美国和加拿大迁徙到墨西哥非常特殊的越冬树，最长可达3000公里长。一年后，上一年秋季移民的第三到第五代后代回到了墨西哥人的同一棵树上。同样令人印象深刻的回程迁徙在澳大利亚东南部也只发生了一代，那里有数以百万计的博贡蛾（Agrotis infuta，图1e）在它们往返雪山上的一年一度的捕食洞穴的途中填满了夜空。最近，Chapman等人17、19、20证明，定向长距离回返迁徙在高飞行昆虫中也很普遍。这些几万亿个体昆虫的运动对于理解自然生态系统和人造生态系统至关重要。
In the ocean, Salmonid fish (Fig. 1f ) and sea turtles (Fig. 1g), for instance, return to their natal streams or beaches over thousands of kilometers 22–25 and many dispersing coral reef fish larvae relocate their natal reefs after being at the mercy of sea currents for weeks 26–28
例如，在海洋中，鲑鱼（图1f）和海龟（图1g）在数千公里外返回其出生的溪流或海滩，许多分散的珊瑚礁鱼幼虫在受海流影响数周后重新定位到其出生的珊瑚礁。
To complete their long voyages, migratory animals have developed elaborate abilities to detect a variety of sensory cues, to integrate these signals within their nervous systems, and to use them as part of highly efficient navigational strategies 1,3,4,10,17,29–32. Navigation skills are also vitally important to non-migratory animals of almost any class 1,13,14,33,34.However, this review focuses primarily on long-distance navigation and homing. After discussion of the basic principles underlying these processes, I discuss how animals use, detect and process the main types of navigation-relevant cue. I consider magnetic cues in more detail than other cues because the sensory mechanisms that underlie sight, olfaction and hearing are generally understood. By contrast, even though a lot of progress has been made recently, the mechanisms by which animals sense the geomagnetic field remains one of the most fundamentally important questions in sensory biology. I also highlight twenty of the most important outstanding mechanistic questions that remain to be answered (Box 1; denoted as ‘question 1’ and so on throughout the Review).
为了完成它们的长途航行，迁徙动物已经发展出精密的能力来探测各种感官信号，将这些信号整合到它们的神经系统中，并将它们作为高效导航策略的一部分。对于几乎所有类的非迁徙动物来说，导航技能也至关重要。然而，本综述主要关注远程导航和归航。在讨论了这些过程的基本原理之后，我讨论了动物如何使用、检测和处理与导航相关提示的主要类型。我考虑磁线索比其他线索更详细，因为视觉、嗅觉和听觉的感觉机制是普遍理解的。相比之下，尽管最近取得了许多进展，动物感知地磁场的机制仍然是感官生物学中最基本的重要问题之一。我还强调了20个最重要的有待回答的突出机械问题（框1；在整个Review中表示为“问题1”，依此类推）。
Studying navigation导航研究
Navigation and orientation导航与方向
The terms ‘navigation’ and ‘orientation’ are used inconsistently in different fields. Here, ‘orientation’ means that only the direction of movement is being determined. To perform ‘true navigation’, animals need first to determine their location (map position) and then the compass direction to their goal 3,31,35. True navigators can correct for displacements during any phase of their journey3,31,35–37. ‘Navigation’ is used for anything within the continuum between true navigation and pure compass orientation.
在不同领域，术语“导航”和“方向”的用法并不一致。这里，“方向”只是指代移动的方向。为了执行“真正的导航”，动物首先需要确定它们自己的位置（地图坐标），然后指南针再指向它们的目的地。真正的导航员可以在旅程的任何阶段纠正移动方向。“导航”用于真正导航和纯罗盘方向之间的连续范围内的任何事物。
Maps and compasses地图与指南针
Map and compass information are often determined independently1,3,4,31. To get a sense of direction, only a reference compass direction, such as magnetic and/or geographical North, needs to be determined, which an animal can then use to orient in any desired direction. Location can be determined in various ways. In some animals, location is defined relative to home1,13,14,34, whereas many experienced migrants have developed large-scale, probably multisensory and multicoordinate maps, which can be extrapolated to correct for displacements, even at unfamiliar locations1,3,4,10,30,31,36–38
地图和罗盘信息通常独立确定。为了获得方向感，只需要确定一个参考罗盘方向，例如磁性和/或地理北向，然后动物就可以用它来确定任何所需方向的方向。位置可以通过多种方式确定。在一些动物中，位置是相对于家来定义的，而许多有经验的移徙者已经开发出大规模的、可能是多传感器的和多坐标的地图，这些地图可以外推以校正位移，即使是在不熟悉的位置。
For instance, the angle of the celestial rotation centre above the horizon, geomagnetic field intensity, and geomagnetic inclination angle all gradually increase from south to north in most parts of the world1,3,30,38. Thus, higher or lower values indicate displacement to the north or south, respectively. How long-distance migrants determine longitude (east–west position) is much less clear (question 19). Magnetic declination is an excellent east–west cue in some parts of the world, and experienced Eurasian reed warblers seem to use magnetic declination as part of their map38. Because magnetic declination is the angular deviation between magnetic and geographical North, map and compass cues might not always be as separable as previously thought. Experimental compass manipulations could also influence the map.
例如，在世界大部分地区，地磁强度和地磁倾角都是由南向北逐渐增大的。因此，较高或较低的值分别表示向北或向南的位移。长途移民决定经度（东西位置）的原因还不太清楚（问题19）。磁偏角是世界上一些地方的一个极好的东西向线索，经验丰富的欧亚芦苇莺似乎把磁偏角作为他们地图的一部分。因为磁偏角是磁北和地理北之间的角度偏差，地图和罗盘的线索可能不像以前想象的那样总是可以分开的。实验罗盘操作也会影响地图。
Experienced versus naive animals有经验VS无经验的动物
When studying long-distance navigation, it is important to consider whether animals are travelling for the first time. Animals such as migratory insects and coral reef fish larvae are always inexperienced migrants, as they complete only a single return journey or less 11,18–20,39. By contrast, most migratory birds and sea turtles make several similar journeys 1,3,4,30,31
在研究远程导航时，考虑动物是否是第一次旅行是重要的。诸如迁徙昆虫和珊瑚礁鱼幼虫等动物总是缺乏经验的迁徙者，因为它们只完成一次回程，或者不到一次回程。相比之下，大多数候鸟和海龟都会进行几次类似的旅行。
First-time migrants must use relatively simple orientation systems based on information inherited or learned before departure. Young night-migratory songbirds inherit their migratory direction and distance2, but the genes underpinning this have not been identified40 (question 16). Inexperienced migrants cannot have a detailed map of their migration route, but could have inherited simple cue values for the goal and/or a few ‘signposts’ and associated these with adaptive behaviours, such as the responses of hatchling sea turtles to magnetic parameters 22,30,41. Inexperienced bird migrants usually follow experienced companions or rely on a simple clock-and-compass strategy (vector navigation) using only an innate circannual clock and compass orientation programmes, but no map. They are therefore, except for a few emergency plans, unable to correct for geographical displacement 3,4,31,36,38,42–45. It remains unclear exactly which combination of sensory parameters triggers the start and stop of the first natural migration (question 17).
第一次移民必须使用相对简单的定位系统，基于离开前继承或学习的信息。年轻的夜间候鸟继承了它们的迁徙方向和距离，但支撑这一点的基因尚未被确认（问题16）。缺乏经验的移民无法获得其迁徙路线的详细地图，但可以继承目标和/或几个“路标”的简单提示值，并将其与适应性行为相关联，例如孵化的海龟对磁参数的响应。缺乏经验的鸟类迁徙者通常跟随有经验的同伴，或依靠简单的时钟和罗盘策略（矢量导航），只使用固有的全年时钟和罗盘定向程序，但没有地图。因此，除了一些应急计划外，他们无法纠正地理位移。目前尚不清楚哪些感官参数组合触发了第一次自然迁移的开始和停止（问题17）。
By contrast, many experienced migrants travelling for the second or later time have experienced cue gradients and generated a map that they can use to correct even for displacements to unknown locations. They can thus perform true navigation1,3,4,31,36–38,43,45–48
相比之下，许多有经验的移民在第二次或以后的旅行中经历了线索梯度，并生成了一张地图，他们甚至可以用来校正到未知位置的位移。因此，它们可以执行真正的导航。
The three phases of a navigational task导航任务的三个阶段
Navigational cues that can be used over thousands of kilometres differ from those that are useful over a few kilometres, metres, or centimetres over time-scales of a few seconds, minutes or hours (Table 1). Furthermore, animals mostly use quite simple navigational strategies that are good enough to solve the tasks needed for survival, but not ‘perfect’ mathematical solutions. Consequently, a succession of at least three different phases or stages is needed to account for the pinpoint accuracy of experienced long-distance migrants 32(Fig. 2). The three phases are: (1) a long-distance phase; (2) a narrowing-in or homing phase; and (3) a pinpointing-the-goal phase. To achieve a holistic understanding of animal navigation, all phases need to be understood, and a comparative approach is needed to evaluate whether species, groups or classes of animals use similar or different solutions.
可用于数千公里以上的导航提示不同于在几公里、几米或几厘米的时间尺度（几秒、几分钟或几小时）上有用的导航提示（表1）。此外，动物大多使用非常简单的导航策略，这些策略足以解决生存所需的任务，但不是“完美”的数学解。因此，至少需要连续三个不同的阶段或阶段来解释有经验的长途移民32的精确性（图2）。这三个阶段是：（1）远距离阶段；（2）变窄或归位阶段；（3）精确定位目标阶段。为了全面了解动物导航，需要了解所有阶段，并需要一种比较方法来评估动物物种、群体或类别是否使用相似或不同的解决方案。
The long-distance phase refers to navigation far away from the animal’s home ranges and it usually relies on global or regionally stable cues such as celestial and/or geomagnetic information. Simple, compass-based, vector orientation relying on an inherited initial direction2,3,11,27,31 seems to be the only mechanism available to many inexperienced animals that travel without experienced companions 2,3,27,31,36,39,42–44. By contrast, experienced animals can often modify their compass headings on the basis of learned map information3,4,31,36–38,43,47–49. During the narrowing-in or homing phase, in or near a familiar home range, learned local gradient maps that rely on a variety of senses and environmental cues are usually important 1,10,32,34,39,49. The pinpointing-the-goal phase is mostly based on remembering very specific visual landmarks and/or the odours of a specific location25,50,51
远距离阶段指的是远离动物的家养范围的航行，它通常依赖于全球或区域稳定的线索，如天体和/或地磁信息。简单、基于罗盘的矢量定向依赖于遗传的初始方向似乎是许多缺乏经验的动物的唯一机制，它们没有经验的同伴。相比之下，经验丰富的动物通常可以根据所学的地图信息修改指南针方向。在变窄或归位阶段，在熟悉的家庭范围内或附近，学习依赖各种感官和环境线索的局部梯度图通常很重要。确定目标阶段主要基于记住非常具体的视觉标志和/或特定位置的气味。
The three navigational phases seem quite universal. Night-migratory songbirds use mainly celestial and magnetic cues during the long- distance phase1,3,4,31,37,38, a variety of learned, multisensory, local gradient maps during their homing phase1,32,49, and visual landmarks to find their nest or sleeping perch during the pinpointing-the-goal phase32
这三个航行阶段似乎相当普遍。夜间候鸟主要在远距离阶段中使用天体和磁场信号，在归航阶段中使用各种学习的、多传感器的局部梯度图，以及在精确定位目标阶段中找到它们的巢或栖息处的视觉标志。
Monarch butterflies use a time-compensated sun compass during the long-distance phase12,52,53. Monarchs do not like to cross large bodies of water (the Gulf of Mexico constrains movement towards the southeast) or to fly over high mountains (the Rocky Mountains limits them to the west). The resulting geographic funnelling effect brings the monarchs to within a couple of hundred kilometres of their wintering range39. How the later parts of the narrowing-in and pinpointing-the-goal phases work in these one-time migrants is currently unknown (question 20). The latter could be based on a combination of attraction to smells left by previous generations of conspecifics beaconing from the wintering trees and searching for the right micro-climate and tree species.
Salmon might use an innate signpost ‘map’ coupled with adaptive compass responses similar to those of sea turtles 22 to stay within a suitable oceanic range and to return as adults to the approximate location of the river mouth23. At this point, their navigational strategy changes to one based mainly on chemical or olfactory cues, which they use to home in on the exact spawning ground where they were born25,54,55. Coral reef fish larvae first seem to use an innate celestial and magnetic compass direction to relocate the vicinity of the reef 27,28, then olfactory 26 and/or auditory cues 56 to narrow in on the reef, and finally vision to locate a suitable microhabitat within the reef.
In summary, several cues are often used together during a phase, and the cues, brain-processing strategies, and behaviours involved vary substantially between phases in most cases. What determines when an animal switches from one navigational phase to the next, and how processing strategies in the nervous system transition between phases, remain exciting open questions (questions 10, 11, 18).
Owing to the three navigational phases, it is extraordinarily unlikely that a single sense or cue is used exclusively throughout a journey. One consequence of this is that animals tested at the wrong location relative to where the relevant phase takes place in nature may not reveal their true abilities during that phase. Testing of animals during different phases or at wrong locations might explain some of the apparent contradictions in the long-distance navigation literature
Magnetic cues and how they are sensed
The Earth’s magnetic field, also called the geomagnetic field, is shaped as if a big bar magnet were placed at the centre of the Earth4,57. The geomagnetic field provides omnipresent information, which can help animals to navigate. Magnetic direction (polarity) and/or inclination angle (the angle between the field lines and the Earth’s surface) can be used to determine a favourable direction of movement 1,4,57,58. Total magnetic intensity, inclination angle, and magnetic declination can help animals to determine position1,4,22,30,38,41,48,57
.