Male courtship vocalizations represent a potent signal designed to attract females; however, not all females find male signals equally attractive. We explored the possibility that the affective state induced by hearing courtship vocalizations depends on the motivational state of a receiver. We used a conditioned place preference test of reward to determine the extent to which the rewarding properties of hearing male courtship song differed in female European starlings categorized as nest box owners (a sign of breeding readiness) or non-owners. Nest box owners developed a preference for a chamber in which they previously heard male courtship song. Non-owners displayed no preference for a chamber in which they previously heard song. Positive correlations were identified between the preference a female developed for the song-paired chamber and female nesting and dominance behaviors observed prior to conditioning (indices of the motivation to breed). Immunolabeling for met-enkephalin (an opioid neuropeptide involved in reward) in the medial preoptic nucleus, ventromedial nucleus of the hypothalamus, nucleus accumbens, and periaqueductal gray was higher in females with compared to those without nest boxes. Both nest box entries and song-induced place preference also correlated positively with met-enkephalin labeling in the ventromedial nucleus of the hypothalamus. These findings indicate that the reward value of vocal signals is linked to individual differences in motivational state; and that differences in enkephalin activity may play a role in modifying an individual’s motivational state and/or the reward value of song.
How do territorial neighbors resolve the location of their boundaries? We addressed this question by testing the predictions of 2 nonexclusive game theoretical models for competitive signaling: the sequential assessment game and the territorial bargaining game. Our study species, the banded wren, is a neotropical nonmigratory songbird living in densely packed territorial neighborhoods. The males possess repertoires of approximately 25 song types that are largely shared between neighbors and sequentially delivered with variable switching rates. Over 3 days, boundary disputes among pairs of neighboring males were synchronously recorded, their perch positions were marked, and their behavioral interactions were noted. For each countersinging interaction between 2 focal males, we quantified approach and retreat order, a variety of song and call patterns, closest approach distance, distance from the territorial center, and female presence. Aggressors produced more rattle-buzz songs during the approaching phase of interactions, whereas defenders overlapped their opponent's songs. During the close phase of the interaction, both males matched frequently, but the key determinant of which one retreated first was song-type diversity-first retreaters sang with a higher diversity. Retreaters also produced more unshared song types during the interaction, and in the retreating phase of the interaction, they overlapped more. A negative correlation between song-type diversity asymmetry and contest duration suggested sequential assessment of motivational asymmetry. The use of this graded signal, which varied with distance from the center and indicated a male's motivation to defend a particular position, supported the bargaining model. The bargaining game could be viewed as a series of sequential assessment contests.
In seasonally breeding male songbirds, both the function of song and the stimuli that elicit singing behavior change seasonally. The catecholamine norepinephrine (NE) modulates attention and arousal across behavioral states, yet the role of NE in seasonally-appropriate vocal communication has not been well-studied. The present study explored the possibility that seasonal changes in alpha 2-noradrenergic receptors (α2-R) within song control regions and brain regions implicated in sexual arousal and social behavior contribute to seasonal changes in song behavior in male European starlings (Sturnus vulgaris). We quantified singing behavior in aviary housed males under spring breeding season conditions and fall conditions. α2-R were identified with the selective ligand [3H]RX821002 using autoradiographic methods. The densities of α2-R in song control regions (HVC and the robust nucleus of the arcopallium [RA]) and the lateral septum (LS) were lower in Spring Condition males. α2-R densities in the caudal portion of the medial preoptic nucleus (POM) related negatively to singing behavior. Testosterone concentrations were highest in Spring Condition males and correlated with α2-R in LS and POM. Results link persistent seasonal alterations in the structure or function of male song to seasonal changes in NE α2-Rs in HVC, RA, and LS. Individual differences in α2-R in the POM may in part explain individual differences in song production irrespective of the context in which a male is singing, perhaps through NE modification of male sexual arousal.
Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.
Variation in signals often encodes additional information beyond that provided by the main signal. Many species communicate degree of threat using such signal variation. However, multiple signal parameters often covary with threat level, and it is unclear whether receivers are using variation along one or more parameters when assessing threat level. White‐throated magpie‐jays (Calocitta formosa) vary several call parameters when mobbing, and here I report on an experiment testing whether such variation contains information used by conspecific receivers, and which parameters are salient to receivers. I collected data on natural mobbing sequences in two threat contexts and found that mobbing calls were highly variable in both length and inter‐call interval, but on average, both parameters were shorter in high threat contexts, while call frequency did not differ. To determine how jays respond to such between‐context variation, I conducted a playback experiment in which call length and inter‐call interval were independently varied in a factorial design. This is one of the first studies to my knowledge to deconstruct and independently test covarying signal parameters in an anti‐predator signaling system. Magpie‐jays responded more often to treatments with either short call lengths or short inter‐call intervals, in concordance with the natural calling data. However, the two parameters did not appear to act independently; responses were not additive, and short calls at short inter‐call intervals elicited no stronger of a response than short calls at long intervals or long calls at short intervals. Receivers can use either parameter when assessing threat level. These data demonstrate that mobbing can signal threat level, that call length and call rate are redundant, and that receivers need not use both to determine whether to approach.
Food begging is common in nutritionally dependent young of many animals, but structurally homologous calls recur in adult signal repertoires of many species. We propose eight functional hypotheses for begging in adults; these stem from observations in birds but apply broadly to other taxa in which begging occurs. Adult cooperatively-breeding white-throated magpie-jays (Calocitta formosa) use loud begging vocalizations, particularly near the nest site during reproduction. We analysed the social context and behavioural phenology of loud calling and allofeeding in this species and compared these with predictions from each functional hypothesis. We found that reproductive females are the primary producers of beg calls, and their begging peaks during the fertile period when reproductive conflict among males and females was highest. Loud begging rates correlated positively with provisioning rates, but females called more in the pre-incubation fertile period than after they initiated incubation. Based on the context, phenology and active space of the signal, we conclude that female loud begging vocalizations function to signal nutritional need to group members, but also have been evolutionarily co-opted to advertise fertility to potential extra-pair partners. The location of calling is likely a consequence of nest guarding by breeding females to prevent intraspecific brood parasitism.
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