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Referential alarm calls that denote specific types of dangers are common across diverse vertebrate lineages. Different alarm calls can indicate a variety of threats, which often require specific actions to evade. Thus, to benefit from the call, listeners of referential alarm calls must be able to decode the signaled threat and respond to it in an appropriate manner. Yellow warblers ( Setophaga petechia ) produce referential “seet” calls that signal to conspecifics the presence of nearby obligate brood parasitic brown-headed cowbirds ( Molothrus ater ), which lay their eggs in the nests of other species, including yellow warblers. Our previous playback experiments have found that red-winged blackbirds ( Agelaius phoeniceus ), a species also parasitized by brown-headed cowbirds, eavesdrop upon and respond strongly to yellow warbler seet calls during the incubation stage of breeding with aggression similar to responses to both cowbird chatters and predator calls. To assess whether red-winged blackbird responses to seet calls vary with their own risk of brood parasitism, we presented the same playbacks during the nestling stage of breeding (when the risk of brood parasitism is lower than during incubation). As predicted, we found that blackbirds mediated their aggression toward both cowbird chatter calls and the warblers’ anti-parasitic referential alarm calls in parallel with the low current risk of brood parasitism during the nestling stage. These results further support that red-winged blackbirds flexibly respond to yellow warbler antiparasitic referential calls as a frontline defense against brood parasitism at their own nests.
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Functional neurogenomic responses to acoustic threats, including a heterospecific referential alarm call and its referent, in the auditory forebrain of red-winged blackbirds
Abstract In animal communication, functionally referential alarm calls elicit the same behavioral responses as their referents, despite their typically distinct bioacoustic traits. Yet the auditory forebrain in at least one songbird species, the black-capped chickadeePoecile atricapillus, responds similarly to threat calls and their referent predatory owl calls, as assessed by immediate early gene responses in the secondary auditory forebrain nuclei. Whether and where in the brain such perceptual and cognitive equivalence is processed remains to be understood in most other avian systems. Here, we studied the functional neurogenomic (non-) equivalence of acoustic threat stimuli perception by the red-winged blackbirdAgelaius phoeniceusin response to the actual calls of the obligate brood parasitic brown-headed cowbirdMolothrus aterand the referential anti-parasitic alarm calls of the yellow warblerSetophaga petechia,upon which the blackbird is known to eavesdrop. Using RNA-sequencing from neural tissue in the auditory lobule (primary and secondary auditory nuclei combined), in contrast to previous findings, we found significant differences in the gene expression profiles of both an immediate early gene, ZENK (egr-1), and other song-system relevant gene-products in blackbirds responding to cowbird vs. warbler calls. In turn, direct cues of threats (including conspecific intruder calls and nest-predator calls) elicited higher ZENK and other differential gene expression patterns compared to harmless heterospecific calls. These patterns are consistent with a perceptual non-equivalence in the auditory forebrain of adult male red-winged blackbirds in response to referential calls and the calls of their referents.
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- PAR ID:
- 10493604
- Publisher / Repository:
- Nature Springer
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Many avian species are negatively impacted by obligate avian brood parasites, which lay their eggs in the nests of host species. The yellow warbler (Setophaga petechia), which is host to the brood-parasitic brown-headed cowbird (Molothrus ater), represents one of the best-replicated study systems assessing antiparasitic host defenses. Over 15 prior studies on yellow warblers have used model-presentation experiments, whereby breeding hosts are exposed to models of brown-headed cowbirds or other nest threats, to test for anti-parasitic defenses unique to this species. Here we present results from our own quasi-replication study of the yellow warbler/brown-headed cowbird system, which used a novel design compared to previous experiments by pivoting to conduct acoustic playback treatments only, rather than presenting visual models with or without calls. We exposed active yellow warbler nests to playbacks of brown-headed cowbird chatters (brood parasite), blue jay (Cyanocitta cristata; nest predator) calls, conspecific “seet” calls (a referential alarm call for brood parasitism risk), conspecific “chip” calls (a generic alarm call), or control wood thrush (Hylocichla mustelina; harmless heterospecific) songs during the incubation stage. Similar to previous studies, we found that female yellow warblers seet called more frequently in response to playbacks of both brood parasitic chatter calls and conspecific seet calls whereas they produced more chip calls in response to the playback of nest predator calls. In contrast, female yellow warblers approached all playbacks to similar distances, which was different from the proximity patterns seen in previous studies. Our study demonstrates the importance of both replicating, and also pivoting, experimental studies on nest defense behaviors, as differences in experimental design can elicit novel behavioral response patterns in the same species.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1038/s41598-024-51797-y
