Award Abstract # 1953226
Collaborative Research: Referential alarm calling as a window into the mechanisms and evolution of a complex cognitive phenotype

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: UNIVERSITY OF ILLINOIS
Initial Amendment Date: April 27, 2020
Latest Amendment Date: April 24, 2023
Award Number: 1953226
Award Instrument: Continuing Grant
Program Manager: Susan Renn
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: June 15, 2020
End Date: February 29, 2024 (Estimated)
Total Intended Award Amount: $632,542.00
Total Awarded Amount to Date: $632,542.00
Funds Obligated to Date: FY 2020 = $187,656.00
FY 2021 = $198,725.00

FY 2022 = $121,802.00

FY 2023 = $90,047.00
History of Investigator:
  • Mark Hauber (Principal Investigator)
    mhauber@gc.cuny.edu
Recipient Sponsored Research Office: University of Illinois at Urbana-Champaign
506 S WRIGHT ST
URBANA
IL  US  61801-3620
(217)333-2187
Sponsor Congressional District: 13
Primary Place of Performance: University of Illinois at Urbana-Champaign
Henry Admin Blg, 506 S. Wright S
Urbana
IL  US  61801-3620
Primary Place of Performance
Congressional District:
13
Unique Entity Identifier (UEI): Y8CWNJRCNN91
Parent UEI: V2PHZ2CSCH63
NSF Program(s): Animal Behavior
Primary Program Source: 01002021DB NSF RESEARCH & RELATED ACTIVIT
01002122DB NSF RESEARCH & RELATED ACTIVIT

01002223DB NSF RESEARCH & RELATED ACTIVIT

01002324DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 9178, 9179
Program Element Code(s): 765900
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

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.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Antonson, Nicholas_D and Rubenstein, Dustin_R and Hauber, Mark_E and Botero, Carlos_A "Ecological uncertainty favours the diversification of host use in avian brood parasites" Nature Communications , v.11 , 2020 https://doi.org/10.1038/s41467-020-18038-y Citation Details
Enos, Janice K. and Bruno, Julia Hyland and Hauber, Mark E. "Aggressive responses of Eastern Phoebes (Sayornis phoebe) and American Robins (Turdus migratorius) toward brood parasites and nest predators: A model presentation experiment" The Wilson Journal of Ornithology , v.132 , 2020 https://doi.org/10.1676/1559-4491-132.2.428 Citation Details
Lawson, Shelby L and Enos, Janice K and Antonson, Nicholas D and Gill, Sharon A and Hauber, Mark E. "Do hosts of avian brood parasites discriminate parasitic vs. predatory threats? A meta-analysis" Advances in the study of behavior , v.53 , 2021 https://doi.org/10.1016/bs.asb.2021.03.002 Citation Details
Lawson, Shelby L. and Enos, Janice K. and Gill, Sharon A. and Hauber, Mark E. "Eavesdropping on Referential Yellow Warbler Alarm Calls by Red-Winged Blackbirds Is Mediated by Brood Parasitism Risk" Frontiers in Ecology and Evolution , v.9 , 2021 https://doi.org/10.3389/fevo.2021.706170 Citation Details
Lawson, Shelby L. and Enos, Janice K. and Gill, Sharon A. and Hauber, Mark E. "Redwinged blackbirds nesting nearer to yellow warbler and conspecific nests experience less brood parasitism" Ecology and Evolution , v.13 , 2023 https://doi.org/10.1002/ece3.9818 Citation Details
Lawson, Shelby L. and Enos, Janice K. and Mendes, Niko C. and Gill, Sharon A. and Hauber, Mark E. "Pairing status moderates both the production of and responses to antiparasitic referential alarm calls in male yellow warblers" Ethology , v.127 , 2021 https://doi.org/10.1111/eth.13139 Citation Details
Lawson, Shelby L. and Enos, Janice K. and Mendes, Niko C. and Gill, Sharon A. and Hauber, Mark E. "Responses of Female Yellow Warblers to Playbacks Signaling Brood Parasitism or Predation Risk: A Quasi-Replication Study" Animal Behavior and Cognition , v.8 , 2021 https://doi.org/10.26451/abc.08.02.08.2021 Citation Details
Lawson, Shelby L. and Enos, Janice K. and Wolf, Caroline S. and Stenstrom, Katharine and Winnicki, Sarah K. and Benson, Thomas J. and Hauber, Mark E. and Gill, Sharon A. "Referential alarm calling elicits future vigilance in a host of an avian brood parasite" Biology Letters , v.17 , 2021 https://doi.org/10.1098/rsbl.2021.0377 Citation Details
Lawson, SL and Leuschner, N and Gill, BJ and Enos, JK and Hauber, ME "Loss of graded enemy recognition in a Whitehead population allopatric with brood parasitic Long-tailed Cuckoos" Avocetta , v.44 , 2020 https://doi.org/10.1101/2020.02.21.958017 Citation Details

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