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

在鸟类幼鸟寄生中，鸟类将蛋下到其他鸟的巢中，留下寄养的宿主来照顾寄生的幼鸟。一些寄主通过积极保护它们的巢不受成年寄生虫的攻击来对抗这种寄生。黄莺发出独特的“seet”叫声，警告棕头牛鸟(Molothrus Ater)的存在。雌性林莺响应海燕的叫声，返回鸟巢，紧紧地坐在巢中，以防止牛鸟寄生。这意味着，就像人类语言中的单词一样，seet的叫声象征着林莺对牛鸟的寄生。该项目的目的是通过研究林莺对牛鸟自己的叫声、seet叫声和其他林莺栖息地典型声音的行为反应(在野外)和神经生理模式(使用fMRI)，了解宿主如何感知和处理这些符号信号的声学和功能意义。这笔拨款将培训一名博士后研究员、三名博士生、一名硕士生和至少八名本科生，其中包括来自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，作为生物生物学本科课程的在线开放教育资源。其他更广泛的影响将包括为公众举办鸟类环志研讨会，特别是在伊利诺伊州中部和密歇根州活跃的迁徙季节。最后，将制作一部名为《牛鸟的一天》的3D虚拟现实短片，从寄生虫的角度展示寄生鸟特有的日常活动以及它们与宿主的互动。目前和过去对动物警报叫声的研究往往集中在详细发现和表征所指通信信号的含义上。然而，动物识别参照呼叫的感觉-感知能力以及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。本研究通过结合现场实验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这一最重要的假设。以黄莺对褐头牛鸟的反寄生警报叫声为研究系统，将评估四个具体预测：(I)涉及警报叫声及其所指对象的知觉对等；(Ii)社交习得但可能被与牛鸟的个人经验所改变；(Iii)涉及心理意象、情景式记忆和心理时间旅行，改变未来行为以降低健康风险；以及(Iv)是对强制幼鸟寄生的功能特异性反应。该项目将对黄莺对SEET叫声的反应的行为和种群水平的预测与通过活体成像(FMRI)探测野生鸟类的发育轨迹和参考沟通的神经基础相结合，以重复收集整个发育过程的数据。这项综合性研究将为指称交流的认知生态和机制提供新的视角，包括对符号呼唤感知的神经基础的潜在变革性理解，新语境中心理时间旅行的存在，以及指称信号的功能基础。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

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.