Collaborative Research: Referential alarm calling as a window into the mechanisms and evolution of a complex cognitive phenotype

合作研究：参考警报呼叫作为了解复杂认知表型的机制和演化的窗口

• 批准号: 1953226
• 负责人: Mark Hauber
• 金额: $ 63.25万
• 依托单位: University of Illinois at Urbana-Champaign
• 依托单位国家: 美国
• 项目类别: Continuing Grant
• 财政年份: 2020
• 资助国家: 美国
• 起止时间: 2020-06-15 至 2024-02-29
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1953226&HistoricalAwards=false
• 关键词: Collaborative; Research; Referential; alarm; calling

In avian brood parasitism, birds lay their eggs into others’ nests, leaving the foster hosts to look after the parasitic young. Some hosts combat such parasitism by actively defending their nests from adult parasites. Yellow Warblers (Setophaga petechia) produce unique "seet" calls to warn about the presence of Brown-headed Cowbirds (Molothrus ater). In response to seet calls, female warblers return to sit tightly on the nest to prevent cowbird parasitism. This means that, much like words in human languages, seet calls symbolize cowbird parasitism for the warblers. The project’s aim is to understand how hosts perceive and process the acoustic and functional meaning of these symbolic signals by studying the behavioral responses (in the field) and neurophysiological patterns (using fMRI) of warblers to the cowbird’s own calls, seet calls, and other sounds typical of the warbler’s habitat. The grant will train a postdoctoral fellow, three PhD students, one Master's student, and at least eight undergraduate researchers, including students from groups underrepresented in STEM fields. The researchers will write and share case studies based on their research as open online educational resources for undergraduate courses in organismal biology. Additional broader impacts will include bird banding workshops for the general public, especially during the vibrant migratory seasons in central Illinois and Michigan. Finally, a short 3D virtual reality film-feature will be produced entitled "A Day in the Life of the Cowbird", featuring characteristic daily activities of parasitic birds and their interactions with hosts, as seen from the parasite's own eyes' perspective.Current and past research on alarm calling in animals has often focused on the detailed discovery and characterization of the meaning of referential communication signals. However, the sensory-perceptual abilities of animals to recognize referential calls and the potentially high-level neural processing that ultimately leads to a specific behavioral response have not yet been fully explored. Through integrating field and laboratory experiments and levels of analyses, this research aims to test the overarching hypothesis that referential signaling requires high-level cognitive abilities. Using Yellow Warblers’ anti-brood parasitic alarm calls to Brown-headed Cowbirds as a study system, four specific predictions will be assessed regarding that referential calling (i) involves perceptual equivalency of alarm calls and their referents, (ii) is socially acquired but may be modified by personal experience with cowbirds, (iii) involves mental imagery, episodic-like memory, and mental time travel, modifying future behavior so as to decrease risks to fitness, and (iv) is a functionally specific response to obligate brood parasitism. The project couples behavioral and population-level predictions of Yellow Warblers' responses to seet calls with probing of developmental trajectories and neural substrates of referential communication in wild birds via in vivo imaging (fMRI) to repeatedly collect data across development. This integrative research will provide new perspectives on the cognitive ecology and mechanisms of referential communication, including potentially transformative understanding of the neural substrates underlying the perception of symbolic calls, the existence of mental time travel in novel contexts, and the functional substrates of referential signaling.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

在鸟类的育雏寄生中，鸟类将卵产在其他鸟类的巢中，让寄养宿主照顾寄生的幼鸟。一些宿主通过积极地保护它们的巢穴免受成年寄生虫的侵害来对抗这种寄生。黄莺（Setophaga petechia）产生独特的“seet”呼叫，以警告褐头牛鹂（Molothrus ater）的存在。为了回应筑巢的叫声，雌性莺会返回并紧紧地坐在巢穴上，以防止燕八哥寄生。这就意味着，就像人类语言中的单词一样，塞埃特的叫声象征着燕八哥对莺的寄生。该项目的目的是了解主机如何感知和处理这些符号信号的声学和功能意义的行为反应（在现场）和神经生理模式（使用功能磁共振成像）的莺燕八哥自己的电话，seet呼叫，和其他声音的莺的栖息地的典型。该补助金将培养一名博士后研究员，三名博士生，一名硕士生和至少八名本科生研究人员，包括来自STEM领域代表性不足的群体的学生。研究人员将根据他们的研究撰写和分享案例研究，作为有机生物学本科课程的开放式在线教育资源。其他更广泛的影响将包括为公众举办鸟类环志讲习班，特别是在伊利诺斯州中部和密歇根州充满活力的迁徙季节。最后，将制作一部3D虚拟现实电影短片，名为《牧牛鸟生活中的一天》，从寄生虫自己的视角展示寄生鸟的日常活动及其与宿主的互动。当前和过去关于动物警报呼叫的研究通常集中在详细发现和描述参考通信信号的含义。然而，动物识别参照呼叫的感官知觉能力和最终导致特定行为反应的潜在高级神经处理尚未得到充分研究。本研究通过整合实地和实验室实验以及不同层次的分析，旨在验证指称信号需要高水平认知能力的总体假设。使用黄莺对褐头牛鹂的反育雏寄生警报呼叫作为研究系统，将评估四个具体的预测，即参考呼叫（i）涉及警报呼叫及其所指对象的感知等效性，（ii）是社会获得的，但可能会被燕八哥的个人经验所修改，（iii）涉及心理意象，情节记忆和心理时间旅行，修改未来的行为，以减少风险健身，和（iv）是一个功能特异性反应专性育雏寄生。该项目通过体内成像（fMRI）将黄莺对seet呼叫的反应的行为和种群水平预测与野生鸟类中参考通信的发育轨迹和神经基质的探测结合起来，以重复收集整个发育过程的数据。这种综合性研究将为认知生态学和指称交流机制提供新的视角，包括对象征性呼叫感知背后的神经基质的潜在变革性理解，新语境中心理时间旅行的存在，该奖项反映了NSF的法定使命，并被认为值得通过使用基金会的学术价值和更广泛的影响审查标准。

项目成果

Loss of graded enemy recognition in a Whitehead population allopatric with brood parasitic Long-tailed Cuckoos

• DOI: 10.1101/2020.02.21.958017
• 发表时间: 2020-02
• 期刊: bioRxiv
• 作者: S. Lawson;Nora Leuschner;B. Gill;J. K. Enos;M. Hauber

Responses of Female Yellow Warblers to Playbacks Signaling Brood Parasitism or Predation Risk: A Quasi-Replication Study

雌性黄莺对预示巢寄生或捕食风险的回放的反应：一项准复制研究

• DOI: 10.26451/abc.08.02.08.2021
• 发表时间: 2021
• 期刊: Animal Behavior and Cognition
• 作者: Lawson, Shelby L.;Enos, Janice K.;Mendes, Niko C.;Gill, Sharon A.;Hauber, Mark E.
• 通讯作者: Hauber, Mark E.

Ecological uncertainty favours the diversification of host use in avian brood parasites

• DOI: 10.1038/s41467-020-18038-y
• 发表时间: 2020-08-21
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Antonson, Nicholas D.;Rubenstein, Dustin R.;Botero, Carlos A.
• 通讯作者: Botero, Carlos A.

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

参考警报呼叫引起了鸟类寄生寄生虫宿主的未来警惕

• DOI: 10.1098/rsbl.2021.0377
• 发表时间: 2021
• 期刊: Biology Letters
• 影响因子: 3.3
• 作者: Lawson, Shelby L.;Enos, Janice K.;Wolf, Caroline S.;Stenstrom, Katharine;Winnicki, Sarah K.;Benson, Thomas J.;Hauber, Mark E.;Gill, Sharon A.
• 通讯作者: Gill, Sharon A.

Aggressive responses of Eastern Phoebes (Sayornis phoebe) and American Robins (Turdus migratorius) toward brood parasites and nest predators: A model presentation experiment

东部菲比 (Sayornis phoebe) 和美洲知更鸟 (Turdus migratorius) 对巢内寄生虫和巢穴捕食者的攻击性反应：模型演示实验

• DOI: 10.1676/1559-4491-132.2.428
• 发表时间: 2020
• 期刊: The Wilson Journal of Ornithology
• 作者: Enos, Janice K.;Bruno, Julia Hyland;Hauber, Mark E.
• 通讯作者: Hauber, Mark E.