Female Black-capped Chickadees Research Articles

Experimental test of selection against hybridization as a driver of avian signal divergence.

Signal divergence may be pivotal in the generation and maintenance of new biodiversity by allowing closely related species to avoid some costs of co-occurrence. In birds, closely related, sympatric species are more divergent in their colour patterns than those that live apart, but the selective pressures driving this pattern remain unclear. Traditionally, signal divergence among sympatric species is thought to result from selection against hybridization, but broad evidence is lacking. Here, we conducted field experiments on naïve birds using spectrometer-matched, painted 3D-printed models to test whether selection against hybridization drives colour pattern divergence in the genus Poecile. To address selection for male colour pattern divergence without the influence of learning or the evolution of female discrimination in sympatry, we simulated secondary contact between Poecile species, and conducted mate choice experiments on naïve, allopatric females. We found that female black-capped chickadees (Poecile atricapillus) are equally likely to perform copulation solicitation displays to sympatric and allopatric heterospecific congeners when they are paired with conspecifics, but exhibit a strong preference for less divergent males when presented with paired heterospecific congeners. These results suggest that increased colour pattern divergence among sympatric species can reduce the likelihood of mixed mating in some contexts, and therefore should be favoured by selection against hybridization.

Individual acoustic differences in female black-capped chickadee (poecile atricapillus) fee-bee songs.

In songbirds, song has traditionally been considered a vocalization mainly produced by males. However, recent research suggests that both sexes produce song. While the function and structure of male black-capped chickadee (Poecile atricapillus) fee-bee song have been well-studied, research on female song is comparatively limited. Past discrimination and playback studies have shown that male black-capped chickadees can discriminate between individual males via their fee-bee songs. Recently, we have shown that male and female black-capped chickadees can identify individual females via their fee-bee song even when presented with only the bee position of the song. Our results using discriminant function analyses (DFA) support that female songs are individually distinctive. We found that songs could be correctly classified to the individual (81%) and season (97%) based on several acoustic features including but not limited to bee-note duration and fee-note peak frequency. In addition, an artificial neural network was trained to identify individuals based on the selected DFA acoustic features and was able to achieve 90% accuracy by individual and 93% by season. While this study provides a quantitative description of the acoustic structure of female song, the perception and function of female song in this species requires further investigation.

Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)

The black-capped chickadee is a songbird that has been used extensively as a model of animal communication in field and laboratory settings. Although many studies have focused on the complex call and song systems of the black-capped chickadee, relatively fewer studies have focused on chickadee audition. However, we do know from behavioral and molecular work that chickadees (and auditory processing areas in their brains) discriminate between artificially generated tones, between conspecific and heterospecific vocalizations, and among different types of conspecific vocalizations. In this paper we investigate peripheral auditory processing of frequency in the black-capped chickadee and the potential influence of sex on frequency sensitivity using a technique called auditory evoked potentials. We found that male and female black-capped chickadees did not differ in any measure of frequency sensitivity. Both sexes had the greatest sensitivity to frequencies between 2 and 4kHz. This range of frequencies is well represented in black-capped chickadee song, partially supporting the idea that sender and receiver coevolve. Finally, we suggest that the call and song system of North American parids make them an ideal taxonomic group for comparative work exploring the relationship between call systems and the evolution of auditory processing.

Differential effects of vocalization type, singer and listener on ZENK immediate early gene response in black-capped chickadees ( Poecile atricapillus)

Here we examined immediate early gene (ZENK) induction to vocalizations in the ascending auditory pathway of black-capped chickadees ( Poecile atricapillus) to assess the impact that the sex of the producer and perceiver has on ZENK induction. We manipulated the playback by both the vocal type (song/call) and sex of producer (male/female), and then presented these stimuli classes to either male or female black-capped chickadees. Neural response to the stimulus was quantified by the amount of protein of the IEG ZENK (also known as zif-268, egr-1, ngf-Ia and krox-24) in the caudal medial nidopallium (NCM) and caudomedial mesopallium (CMM). Overall, there was more ZENK induction in CMM and the dorsal parts of the caudal medial nidopallium (NCMd) than in the ventral parts of the caudal medial nidopallium (NCMv) and males had more ZENK induction than females. CMM had the most complex responding of ZENK induction to stimuli such that vocalization type, sex of producer, and sex of perceiver all affected ZENK induction. The silence controls had the least ZENK induction compared to any other group.

Natal nutrition and the habitat distributions of male and female black-capped chickadees

In nonmigratory passerines, dispersing juveniles may compete to settle in suitable habitat patches, leading to phenotypic assortment across habitat types. We compared the past natal nutrition of 1st year black-capped chickadees (Poecile atricapillus (L., 1766)) that settled in two adjacent patches known to differ in suitability as breeding habitat: a mature mixed forest (good habitat) versus a young regenerating forest dominated by conifers (poor habitat). The past natal nutrition of recruits was estimated by measuring growth bars on their tail feathers grown as nestlings; growth bars were positively associated with body condition of birds at the time of capture, suggesting this measure may accurately reflect individual condition. Males that settled in either habitat had similar growth bar size; however, females that settled in the mature habitat had slightly larger growth bars than those in poor habitat. Individuals occupying the disturbed site were of similar size and in similar body condition compared with those that settled in the mature forest. These findings suggest that females may be more discriminating of habitat quality than males during natal dispersal, matching what is known about chickadee dispersal behaviour. We suggest that males are distributed with a non-ideal despotic distribution, whereas females are distributed with an ideal despotic distribution.

A test of absolute photorefractoriness and photo-induced neural plasticity of song-control regions in black-capped chickadees (Poecile atricapillus)

We tested whether male and female black-capped chickadees, Poecile atricapillus (L., 1766), were absolutely photorefractory according to Hamner's (1968) criteria of (i) spontaneous regression of gonads during prolonged long-day exposure and (ii) no subsequent recrudescence of gonads in response to constant light. We initially exposed black-capped chickadees to constant long-day photoperiods. Gonads regressed spontaneously, demonstrating that the birds met Hamner's first criterion for absolute photorefractoriness. Once their gonads fully regressed and the birds were in advanced prebasic moult, we exposed them to one of three photoperiods for an additional 2 weeks: constant light (24 h L), short days (8 h L), and controls (15 h L). Constant light challenge had no effect on gonadal condition or rate of moult, confirming that the birds met Hamner's second criterion for absolute refractoriness. We also compared volumes of song-control nuclei in the three groups and found that males overall had larger HVC, robust nucleus of arcopallium, and area X than females, but that longer days (24 h L) did not increase volumes and that shorter days (8 h L) did not decrease volumes compared with controls (15 h L). These data support the inference that black-capped chickadees do indeed become absolutely photorefractory, and that photorefractoriness precludes photo-induced plasticity of the song-control system.

The reproductive choices of eavesdropping female black-capped chickadees, Poecile atricapillus.

In animals where males engage in signalling interactions, females might evaluate male-male contests to inform their reproductive choices. We used interactive playback to engage territorial male black-capped chickadees (Poecile atricapillus) of known dominance status in countersinging contests with an aggressive or submissive opponent. Previous analysis of these data showed that high-ranking males who received aggressive playback were more likely to be cuckolded. Here we describe the particular reproductive decisions of females whose partners received aggressive versus submissive playback. The proportion of extra-pair young per brood was higher for females paired to high-ranking males that received aggressive playback compared to submissive playback, and similar to levels in broods of females paired to low-ranking males. We found no strong predictors of whether high-ranking subjects lost paternity following aggressive playback. Females usually preferred extra-pair sires with high dominance status. When females had extra-pair fertilizations with low-ranking males, females chose males who had received submissive playback. We conclude that females mated to aggressive-playback, high-ranking males pursued mixed mating strategies similar to those of females mated to low-ranking males. Our results support the idea that male performance in song contests may influence multiple aspects of female reproductive choices.

Effects of songs and calls on ZENK expression in the auditory telencephalon of field- and isolate-reared black capped chickadees

We examined the effects of hearing two different conspecific vocalizations on expression of the immediate-early gene ZENK in the caudomedial neostriatum (NCM) and the caudomedial portion of the ventral hyperstriatum (cmHV) in male and female black-capped chickadees ( Poecile atricapilla). Both the fee-bee song and the chick-a-dee call induced Zenk protein expression in NCM and in cmHV, however, patterns of expression to songs and calls varied across brain region. In the dorsal region of NCM, fee-bee songs induced more Zenk expression than chick-a-dee calls. In ventral NCM and cmHV, Zenk expression did not differ between songs and calls. We found that sex of the listener also affected Zenk expression: there was more robust ZENK response in males than in females. Finally, we compared field- and isolate-reared chickadees and found similar Zenk expression to fee-bee song in each group. These findings indicated that the type of conspecific vocalization, as well as the sex of the listener, appear to modulate IEG expression in the songbird ascending auditory pathway.

Photostimulation induces rapid growth of song-control brain regions in male and female chickadees ( Poecileatricapilla)

To examine the effect of photoperiodic condition on song-control nuclei we examined three groups of male and female black-capped chickadees ( Poecile atricapilla). Photorefractory birds were held on long days for several months and had fully regressed gonads. Photosensitive birds were held on short days for several months and had small gonads. Photostimulated birds were transferred to long days for 16 days following several months of short days. Following these photoperiod treatments we determined the volume of the song-control nuclei HVc, Area X, and (RA). There were significant sex differences in HVc and Area X, but not in RA. There were also significant photoperiod effects in HVc and Area X. Thus, sex and photoperiod differences in the song system exist in a species in which both sexes produce learned calls year-round.

Determinants of social rank in female black-capped chickadees (Poecile atricapilla)

Black-capped chickadees (Poecile atricapilla) mate assortatively by social rank. Previous field studies suggest that intrinsic characteristics of females may influence success at pairing with dominant males. Here we examined factors leading to dominance using dyads of captive unfamiliar females. The owner–intruder hypothesis predicts that prior residency determines dominant–subordinate relationships. The resource-value hypothesis suggests that social status is initially determined by need and the relationship persists through familiarity of the interactants. The resource holding potential hypothesis suggests that individuals win in dyadic contests because of intrinsic characteristics such as size or age. We tested the owner–intruder and resource-value hypotheses by allowing females prior residency in aviaries where dominance interactions subsequently occurred and by food depriving the intruders. Post-hoc comparisons of dominant–subordinate attributes tested the resource holding potential hypothesis. We found that owners were more likely to win interactions. Hungry individuals showed no competitive advantage. Dominants and subordinates did not differ in morphology or age. Our results agree with data from willow tits (Parus montanus) which show that captive females establish dominance independent of males and that prior residence plays a key role. These findings, together with field studies, suggest that assortative mating in chickadees results, at least in part, from intrasexual interactions among females.

Divorce and extrapair mating in female black-capped chickadees ( Parus atricapillus ): separate strategies with a common target

Patterns of divorce and extrapair mating can provide insights into the targets of female choice in free- living birds. In resident, site-faithful species with contin- uous partnerships, the better options and the incompati- bility hypotheses provide the most likely explanations for divorce. Extrapair mating can be explained by a num- ber of hypotheses often making similar predictions. For example, the good genes and future partnerships hypo- theses predict similar patterns if males with good genes also make the best future partners. By considering both divorce and extrapair mating, it may be possible to dis- tinguish between these comparable hypotheses. We ex- amined natural patterns of divorce and extrapair mating in a long-term study of black-capped chickadees ( Parus atricapillus). Out of 144 partnerships over 8 years, we observed 11 divorces and 38 faithful pairs between sea- sons. Females usually divorced between their first and second breeding seasons for males of higher social rank than their previous partners, had similar reproductive success prior to divorce as females who retained their previous partners, and did not divorce on the basis of previous reproductive success. These results confirm earlier experimental evidence that females divorce for better options. Females who divorced were significantly more likely to have had mixed-paternity broods prior to divorce than females who stayed with their previous partners. There was no evidence that females divorced in favour of previous extrapair partners. These results sup-

Nest-Site Selection by Female Black-Capped Chickadees: Settlement Based on Conspecific Attraction?

Female Black-capped Chickadees (Poecile atricapillus) solicit extrapair copu- lations (EPCs) from neighboring high-ranked males, and these EPCs result in extrapair young. Females might choose to locate their nests near the territory boundaries of attractive males to facilitate access to EPCs. Other hypotheses might also explain choice of nest site, namely: (1) habitat characteristics, (2) prey abundance, and (3) previous experience. We test- ed these four hypotheses in 1996 and 1997. Out of 27 habitat characteristics measured, we found only one that was significantly different between nests and control sites in both years. The abundance of large trees was lower at nest sites than at control sites in each year and when years were pooled. Relative prey abundance did not differ between nests and control sites for either year of the study. We found no difference in interyear nest placement based on female experience; experienced females nested farther than 60 m from their previous nest sites in both years of the study. In 1996, females whose neighboring males were higher ranked than their social partner located their nests significantly closer to territory bound- aries than did females whose nearest neighbors were lower ranked than their social partner. In 1997, all pairs nested near territory boundaries. We conclude that choice of nest location in Black-capped Chickadees is influenced by conspecific attraction based on mating tactics.

Enhanced Reproductive Success of Female Black-Capped Chickadees Mated to High-Ranking Males

Overwinter survival of female Black-capped Chickadees (Poecile atricapillus) depends in part on the rank of their mates. We investigated whether females also gain re- productive benefits by pairing with high-ranking males. We assessed breeding success in 1993 to 1995 and 1997 by comparing clutch size, proportion of eggs hatched, hatching date, and predation rates on nests of females mated to either high-ranking or low-ranking males. We also compared feeding rates of males to incubating females and to offspring during the early nestling period in 1994 and 1995. High-ranking and low-ranking males did not differ in feeding rates during early incubation or early nestling stages. Females mated to high- ranking males incubated for longer periods than females mated to low-ranking males. Youn- ger males and females mated to low-ranking males fed nestlings at a higher rate than did older males and females mated to high-ranking males, respectively. Females mated to high- ranking males had larger clutches, hatched a significantly greater proportion of their eggs, and suffered lower nest predation than females mated to low-ranking males. In 1995 and 1997, where the ranks and ages of both members of 23 pairs were known, female rank was strongly correlated with mate rank and age but was only weakly associated with female age. Female rank accounted for significant variation only in clutch size, and male rank accounted for a greater proportion of variation in clutch size and fledging success than did the female's

Do female black-capped chickadees prefer high-ranking males as extra-pair partners?

Previous studies have shown that some female black-capped chickadees (Poecile atricapillus) solicit copulations from males that rank higher in winter flocks than their social mates, and extra-pair paternity in nests occurs commonly enough to be considered a potential female mating tactic. This study uses blood samples collected in 1992–1995 from 58 families of black-capped chickadees to test whether females with extra-pair offspring have chosen extra-pair sires higher in social rank than their mates. Paternity was assessed with multilocus DNA fingerprinting in 1992–1994 nests and with microsatellite and single-locus minisatellite DNA typing in 1995 nests. Seventeen of 58 nests (29.3%) contained young genetically mismatched with their social father. In 11 of 15 cases where the identity of the extra-pair male was known, the extra-pair male was dominant to the social father. Using data from 29 nests located in 1994 and 1995 for which we had the most data on relative ranks of males, high-ranking males had greater realized reproductive success than low-ranking males as a result of extra-pair fertilizations. There was no significant difference between the number of nests containing extra-pair young of females mated to low-ranked versus high-ranked males. Two nests in 1995 contained young either genetically mismatched with both social parents (intraspecific brood parasitism) or, in one nest, genetically mismatched with the social mother but not the social father (quasi-parasitism). The implications of female strategies acquiring genetic benefits through extra-pair copulations are discussed.

Female initiated divorce in a monogamous songbird: abandoning mates for males of higher quality

Divorcing a current partner to re-pair with a mate of higher quality may be a strategy to increase reproductive success used by socially monogamous birds. By increasing the availability of males through selective mate removal during the nest building period, we found that female black-capped chickadees, Parus atricapillus, will desert their mates to pair with males of higher social rank, a trait closely associated with resource holding potential in this species. Females from neighbouring territories were more likely to desert their mates for high ranked rather than the low ranked widower males; six of seven high ranking and one of six low ranking males were chosen by the divorcing females. Six of the seven widower males chosen by divorcing females were dominant to the males that the females deserted. Once released, the originally removed females were able to re-establish pairbonds with their mates. Higher social ranks of removed females may have enabled them to exclude lower ranked replacement females, and may reflect a natural constraint on female choice.

Extra-Pair Paternity in the Black-Capped Chickadee

Studies of the mating strategies of birds are increasingly shifting their focus to the role that females take in controlling copulation (Hunter et al. 1993, Petrie 1992, Birkhead and Moller 1993). In some avian species, females appear able to control whether copulations occur by accepting or rejecting copulation attempts (BjSrklund et al. 1992, Lifjeld and Robertson 1992, Westneat 1992). Similarly, females of some species actively solicit copulations by seeking the extra-pair male in his own territory (Smith 1988, Kempenaers et al. 1992, Venier et al. 1993). In species where females do control the outcome of copulation attempts, there is a need to, first, determine the extent that extra-pair copulations (EPCs) lead to fertilizations and, second, establish potential benefits that a female may obtain by engaging in EPCs. Smith (1988) reported that female Black-capped Chickadees, Parus atricapillus, seek EPCs from males on territories adjacent to the territory defended by the female's mate. Interestingly, Smith observed that females preferentially sought males for EPCs that held higher dominance rank than the female's mate in the preceding winter's flock. Thus, female Black-capped Chickadees may be engaging in a mixed reproductive strategy of social monogamy while increasing reproductive success by extra-pair copulations with males of higher genetic quality than their own mate (Trivers 1972, Smith 1988, Hamilton 1990). Females may also benefit from engaging in EPCs with dominant males if, by doing so, this facilitates rapid pair bonding with the dominant male in the event that his mate dies. There is a need for data on whether EPCs are resulting in extra-pair paternity of the nestlings in order to imply a fitness benefit to the female's behavior. In this study we document rates of extra-pair paternity in an Ontario population of Black-capped Chickadees, using DNA fingerprinting, and provide support for Smith's hypothesis by showing that extra-pair males were of higher dominance rank than the female's mate. We also suggest a paternity-related explanation for occasional observations ofpolyandry in chickadees (Waterman et al. 1989, Howitz 1991).

A survey of the prevalence of selected bacteria in wild birds.

We determined the prevalence of six genera of bacteria from a sample of 387 cloacal swabs from 364 passerines and woodpeckers. The prevalence of bacteria were as follows: Escherichia coli (1%), Pseudomonas spp. (22%), Salmonella spp. (0%), Staphylococcus spp. (15%), Streptococcus spp. (18%), and Yersinia spp. (1%). The prevalence of Streptococcus spp. was higher in omnivorous species than in granivorous species (20% versus 8%). Individuals captured at feeders had a lower prevalence of both Streptococcus spp. (15% versus 33%) and Escherichia coli (0.5% versus 4%) than birds that did not have access to feeders. These differences are probably not due to the feeder per se, but instead to other site related differences. The prevalence of bacteria did not differ between male and female black-capped chickadees, Parus atricapillus. For 279 color marked black-capped chickadees, we calculated the cumulative mortality rate during 12 wk following swabbing. Although the cumulative mortality rates of infected birds were consistently higher than the rates of non-infected birds, none of these differences were significant. Infections may cause slight reductions in survival rates, but we were not able to confirm this with our data.

Female demands: some fitness implications in chickadee flocks

Female black-capped chickadees (Parus atricapillus), besides searching for their own food, "demand" food from their mates in the spring for extra energy needed to produce and incubate eggs. This behaviour signals their readiness to copulate and it is followed by increased levels of male – male aggression, probably to prevent cuckoldry. Increased aggression owing to limited nest site availability may also be locally important. Subordinate pairs disperse and many presumably die. The extra food allows females with nest sites to breed earlier than if they fed themselves exclusively, and producing early broods appears to be a better fitness strategy than having larger clutches or additional broods. Juveniles from early broods survive better and attain higher social ranks in flock hierarchies, and dominant pairs have the highest overwinter survival rates as well as a better chance than subordinate pairs of obtaining a territory in the spring.