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

在鸟类幼鸟寄生的情况下，鸟类把蛋产在其他鸟类的巢里，让寄主照顾寄生的幼鸟。一些寄主通过积极保护自己的巢穴不受成年寄生虫的侵害来对抗这种寄生。黄莺（Setophaga petechia）发出独特的“seet”叫声来警告褐头牛鹂（Molothrus ater）的存在。作为对鸣叫的回应，雌性莺会回到巢中紧紧地坐着，以防止牛鹂寄生。这意味着，就像人类语言中的单词一样，see call象征着莺寄生在牛郎鸟身上。该项目的目的是通过研究莺的行为反应（在野外）和神经生理模式（使用功能磁共振成像）来了解宿主如何感知和处理这些象征性信号的声学和功能意义，这些声音来自牛郎鸟自己的叫声、啼叫和其他莺栖息地的典型声音。该基金将培养一名博士后、三名博士生、一名硕士生和至少八名本科研究人员，其中包括来自STEM领域代表性不足群体的学生。研究人员将根据他们的研究撰写和分享案例研究，作为有机体生物学本科课程的开放在线教育资源。其他更广泛的影响将包括为公众举办的鸟类绑带讲习班，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虚拟现实短片《牛角鸟的一天》，从寄生虫自己的角度，展示寄生鸟的日常活动以及它们与宿主的互动。目前和过去对动物报警呼叫的研究往往集中在对参考通信信号意义的详细发现和表征上。然而，动物识别参考呼叫的感觉-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探索。通过整合现场和实验室实验以及水平分析，本研究旨在验证参考信号需要高水平认知能力的总体假设。以黄莺对褐头牛头鸟的抗巢寄生报警叫声为研究系统，评估了四种具体的预测，即参照鸣叫(i)涉及报警叫声及其参照物的感知等效性，（ii）是社会获得的，但可能被个人与牛头鸟的经验所修改，（iii）涉及心理意象，情景记忆和心理时间旅行，修改未来行为以降低健康风险。（iv）是对专性幼虫寄生的功能特异性反应。该项目将黄莺对鸣叫反应的行为和种群水平预测与探索野生鸟类的发育轨迹和参考通信的神经基础相结合，通过体内成像（fMRI）反复收集整个发展过程中的数据。这一综合研究将为认知生态学和指称通信机制提供新的视角，包括对象征呼叫感知的神经基础的潜在变革性理解，新环境下心理时间旅行的存在，以及指称信号的功能基础。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值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.