- NSF-PAR ID:
- Date Published:
- Journal Name:
- Frontiers in Ecology and Evolution
- 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
Defending offspring incurs temporal and energetic costs and can be dangerous for the parents. Accordingly, the intensity of this costly behavior should reflect the perceived risk to the reproductive output. When facing costly brood parasitism by brown‐headed cowbirds (
Molothrus ater), where cowbirds lay eggs in heterospecific nests and cause the hosts to care for their young, yellow warblers ( Setophaga petechia) use referential “seet” calls to warn their mates of the parasitic danger. Yellow warblers of both sexes produce this call only in response to cowbirds or seet‐calling conspecifics. Seet calls are mainly produced during the laying and incubation stages of breeding, when risk of brood parasitism is highest, rather than during the nestling stage. On the other hand, general alarm calls (chips) are produced throughout the nesting cycle and are also used in conspecific interactions unrelated to nesting. We hypothesized that context shapes responses prior to breeding as well, such that yellow warblers without a mate and active nest would be less likely to respond to playbacks that simulate brood parasitism risk. To test this hypothesis, we presented playbacks of two nest threats, cowbirds (brood parasite) and blue jays ( Cyanocitta cristata; nest predator), on territories of unmated male warblers (unpaired) and male warblers with a known mate (paired). We found that unpaired males were unresponsive toward playbacks indicating nest threats, whereas paired males were significantly more aggressive and vocal toward these playbacks compared to control playbacks. However, both paired and unpaired males were vocally responsive toward chip calls, which are informative for males regardless of pairing status. Male yellow warblers appear to adjust their responses during the earliest stages of breeding depending on the contextual relevance of specific threat stimuli, and together with prior studies, our work further supports that referential seet calls are associated with stage‐specific risk of brood parasitism.
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 chickadee
Poecile 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 blackbird Agelaius phoeniceusin response to the actual calls of the obligate brood parasitic brown-headed cowbird Molothrus aterand the referential anti-parasitic alarm calls of the yellow warbler Setophaga 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.
Yellow warblers ( Setophaga petechia ) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds ( Molothrus ater ). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.more » « less
Nest‐sharer avian brood parasites do not evict or otherwise kill host chicks, but instead inflict a range of negative effects on their nestmates that are mediated by interactions between the parasite and host life history traits. Although many of the negative fitness effects of avian brood parasitism are well documented across diverse host species, there remains a paucity of studies that have examined the impacts of parasitism across the entirety of host ontogeny (i.e., from when an egg is laid until independence). More specifically, few studies have examined the impact of brood parasitism on the pre‐ and post‐fledging development, physiology, behavior, and survival of host offspring. To help fill this knowledge gap, we assessed the effects of brood parasitism by Brown‐headed Cowbirds (
Molothrus ater) across the ontogeny (incubation, nestling, and post‐fledging period) of nine sympatrically breeding host species in central Illinois, USA; due to sample sizes, impacts on the post‐fledging period were only examined in two of the nine species. Specifically, we examined the impact of brood parasitism on ontogenetic markers including the embryonic heart rate, hatching rate, nestling period length, nest survival, and offspring growth and development. Additionally, in species in which we found negative impacts of cowbird parasitism on host nestmate ontogeny, we examined whether the difference in adult size between parasites and their hosts and their hatching asynchrony positively predicted variation in host costs across these focal taxa. We found that costs of cowbird parasitism were most severe during early nesting stages (reduction in the host clutch or brood size) and were predicted negatively by host size and positively by incubation length. In contrast, we only found limited costs of cowbird parasitism on other stages of host ontogeny; critically, post‐fledging survival did not differ between host offspring that fledged alongside cowbirds and those that did not. Our findings (i) highlight the direct costs of cowbird parasitism on host fitness, (ii) provide evidence for when (the stage) those costs are manifested, and (iii) may help to explain why many anti‐cowbird defenses of hosts have evolved for protection from parasitism during the laying and incubation stages.