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Chinese Science Bulletin, Volume 62 , Issue 12 : 1204-1213(2017) https://doi.org/10.1360/N972016-00936

How do migrating birds find their way?

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  • ReceivedAug 26, 2016
  • AcceptedDec 29, 2016
  • PublishedMar 28, 2017

Abstract

Bird is one of the most abundant and widespread groups in the world. With many specialized structures, such as plumage, air sacs, and hollow bones, most bird species have got flight ability to adapt various niches. Therefore, bird can migrate between wintering and breeding ground, which is usually a long distance, and it’s called migration. Bird navigation is important in migration and is a complex process, which attracts many scientists to dig in how bird finds its way. Since 1873, Charles Darwin has ever mentioned that bird might take the method of dead reckoning on a long-distance migration like human, but at that time no one made further progress. Until 1950s, Kramer firstly found that Common Starling (Sturnus vulgaris) can respond to solar azimuth via mirror test. From then on, many experiments revealed that at least four navigation mechanisms are used in bird migration via more than nine external factors. They are: (i) celestial navigation, celestial clues (e.g. solar azimuth, star position, and polarized light) are used during migration period. (ii) Olfactory navigation, odor distributing in the air forms odorous gradient map or mosaic map which can be detected, or can activate directly certain mechanism to navigate. (iii) Auditory navigation, infrasound (0.05 Hz) produced by mountains and rivers generate sonic gradient map. And (iv) magnetic navigation, geomagnetic field can be detected via magnetic materials or chemical magnetoreception to find correct directions. Although many scientists approve that magnetic navigation may be the main mechanism to orientate and navigate, bird has never taken just one mechanism to migrate. Indeed, many species also use the other three mechanisms to calibrate direction, for example, Savannah Sparrow (Passerculus sandwichensis) can use polarized light to calibrate the magnetic compass at both sunrise and sunset. Different external clues correspond to different sense organs, so various brain areas should deal with information from different navigation mechanisms. The hippocampus participates in spatial perception and manages anything about celestial navigation via the tectofugal visual pathway and the thalamofugal visual pathway. The piriform cortex (CPi) is the main area to receive stimulation from olfactory bulb and determines how to migrate after receiving olfactory clues. Nervous systems of magnetic navigation include two parts which are trigeminus system and Cluster N. Despite the controversy whether there are some magnetic materials on bird, many experimental evidences have proved that magnetic materials detecting geomagnetic field involve to Trigeminus system. Cluster N, however, is an active area when bird migrates at night and it has an important role in transferring information from chemical magnetoreception to the hippocampus. As illustrated above, navigation mechanisms can get full information from many clues, and then, different brain areas trade off those and co-operate each other to make an elaborate map. Bird navigation involves the receptors to environment and the response of nervous system, so many issues are still maintained. The exact mechanism will be revealed with the new techniques and model animal applied.


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  • Figure 1

    Three hypotheses about olfactory navigation[4,20,21,23]. (a) Mosaic map hypothesis, formed by various odors; (b) olfactory activation hypothesis, mean vectors of experimental groups, N, presenting navigation hypothesis, and A, showing activation hypothesis. The left is process of integrating information, green circles, showing synthetic and artificial odors on flight way, red circles, presenting artificial odors. The right is map information, blue and green circles presenting that birds can smell natural air and artificial odors, respectively, and the red is control treatment. Arrows stand for distributing directions; (c, d) gradient map hypothesis, dots presenting odorous gradient, and arrows showing directions. (c) Learning phase, birds learning to distinguish the relation between odors and wind direction. (d) Operational phase, pigeon detecting local odors

  • Figure 2

    (Color online) Chemosensor mechanism[25,33]. The cryptochromes (CRYs) absorb photons, forming FAD-Try radical pairs in the retina, whose direction relating to geomagnetic field vector decides the reaction yields. An ordered structure was produced, if the CRYs connected with the outer membrane disks of the photoreceptors, and various reaction yields respond to different parts of the retina could provide a visual compass

  • Figure 3

    Schematic mechanism of chemical amplification[35]. (a) Free radicals reaction among FADs; (b) free radicals reaction within CRYs. Free radical and ground state substrates kept high concentration under sustained low intensity light stimulating. Other species just kept a few microseconds and obviously represented low level of photochemical reaction. When stimulated by high-intensity magnetic field, free radicals became inefficiency to produce ground state substrates and kept higher concentration, then resulting to reduce 1F*. Detected magnetic field was determined to be amplified by kD and kF

  • Figure 4

    (Color online) Neural circuits of navigation[38]. (a) Celestial compass-processing pathways and brain areas, the tectofugal visual pathway (eye>optic tectum>Rt>entopallium) and the thalamofugal visual pathway (eye>GLd>visualWulst); (b) olfactory compass-processing pathways and brain areas; (c) magnetic particle-processing pathways and brain areas; (d) light-dependent magnetic compass-processing pathways and brain areas. Abbreviations: CDL, area corticoidea dorsolateralis; CPi, piriform cortex; Ei, entopallium internum; CPP, prepiriform cortex; OB, olfactory bulb; Ep, entopallial belt; GLd, dorsal lateral geniculate nucleus; HA, hyperpallium apicale; HD, hyperpallium d ensocellulare; HI, hyperpallium intercalatum; IHA, interstitial nucleus of HA; MVL, mesopallium ventrolaterale; NB, nucleus basalis; NFL, nidopallium frontolaterale; NFT, trigeminal part of the nidopallium frontale; NIL, nidopallium intermedium laterale; PrVd, PrVv, principal sensory nucleus of the trigeminal nerve; SpV, spinal sensory nucleus of the trigeminal nerve

  • Figure 5

    (Color online) Birds integrate different navigational systems through inherent and acquired abilities[51]

  • Figure 6

    (Color online) Different neural regions and circuits control navigation together[25,38]. (a) Hippocampus region and pathway to store, integrate, and retrieve information about maps and compasses; (b) navigation-relevant brain regions deliver information to NCL; (c) the motor output pathways in bird brain; (d) all brain regions and pathways about navigation

  • 雷富民

    中国科学院动物研究所研究员, 中国科学院大学岗位教授, 博士生导师, 国家杰出青年科学基金获得者、万人计划领军人才; 国际鸟类学会副主席; Journal of Biogeography, Journal of Ornithology等4个国际学术期刊副主编. 目前主要从事鸟类系统演化、谱系地理、特殊环境适应的比较基因组, 以及禽流感溯源与病源生态等方面研究. 已发表论文、论著260余篇、部, 其中Science, Lancet, Nature Communications, Molecular Ecology, Global Ecology and Biogeography等国际SCI源刊论文128篇.

  • Table 1   Nine kinds of navigational hypotheses

    Ⅰ假说

    Ⅱ假说

    年份

    提出者

    天文导航

    (视觉)

    太阳导航

    1950

    Kramer[5]

    星辰导航

    1957

    Wagner和Sauer[8]

    偏振光导航

    1982

    Able[2]

    嗅觉导航

    镶嵌图假说

    1971

    Papi等人[6]

    梯度图假说

    1974

    Wallraff[9]

    嗅觉激活假说

    2009

    Jorge等人[4]

    听觉导航

    次声波导航

    1977

    Yodlowski等人[10]

    地磁导航

    (第六感)

    磁铁石假说

    1978

    Gould等人[3]

    化学磁感受

    1978

    Schulten等人[7]

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