Dustin G. Reichard

Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis).

In male dark-eyed juncos (Junco hyemalis), experimentally elevated testosterone (T) decreases male parental care and offspring survival, but results in higher overall fitness through greater mating success. To help address the ensuing question of what prevents selection from favoring higher levels of T in male juncos, we manipulated T in female juncos. A previous study demonstrated no effect of experimentally elevated T on female incubation behavior, suggesting that female parental behavior might be insensitive to T. In this study we asked whether experimentally elevated T mediates other female parental behaviors and whether variation in T-mediated parental behavior might influence reproductive success. We videotaped free-living control- and T-females during nesting to quantify brooding behavior when young were 3 days old and provisioning behavior when young were 6 days old. Nest defense was measured by quantifying responses to a mounted predator placed near the nest. Reproductive success was assessed via fecundity, nestling quality, and nest survival. T-females spent less time than control females brooding but did not differ in provisioning rate. T-females performed fewer dives at the predator mount and, unlike controls, failed to increase defense as nesting progressed. T-females also had lower daily nest survival and lower nest success (odds of producing at least one fledgling). We conclude that some aspects of female parental behavior are sensitive to experimentally elevated T while others are not and consider the implications for the evolution of T-mediated characters in both sexes.

Deciphering Information Encoded in Birdsong: Male Songbirds with Fertile Mates Respond Most Strongly to Complex, Low-Amplitude Songs Used in Courtship

Research on the function of acoustic signals has focused on high-amplitude long-range songs (LRS) and largely ignored low-amplitude songs produced by many species during close-proximity, conspecific interactions. Low-amplitude songs can be structurally identical to LRS (soft LRS), or they can be widely divergent, sharing few spectral and temporal attributes with LRS (short-range song [SRS]). SRS is often more complex than LRS and is frequently sung by males during courtship. To assess function, we performed two playback experiments on males of a socially monogamous songbird. We compared responses of males whose mates were fertile or nonfertile with differences in song structure (SRS vs. LRS and soft LRS), amplitude (SRS and soft LRS vs. LRS), and tempo (slow SRS vs. fast SRS). Males responded more strongly to SRS than to LRS or soft LRS, indicating that song structure had a greater effect on response than song amplitude. SRS tempo did not detectably affect male response. Importantly, males responded more strongly to SRS when their mates were fertile, presumably because hearing SRS can indicate that a male’s mate is being courted by an intruding male and a strong response can deter extrapair competitors. We conclude that low-amplitude songs can function in both inter- and intrasexual communication and should receive greater attention in future studies of mate choice and male-male competition.

Robust behavioral effects of song playback in the absence of testosterone or corticosterone release.

Some species of songbirds elevate testosterone in response to territorial intrusions while others do not. The search for a general explanation for this interspecific variation in hormonal response to social challenges has been impeded by methodological differences among studies. We asked whether song playback alone is sufficient to bring about elevation in testosterone or corticosterone in the dark-eyed junco (Junco hyemalis), a species that has previously demonstrated significant testosterone elevation in response to a simulated territorial intrusion when song was accompanied by a live decoy. We studied two populations of juncos that differ in length of breeding season (6-8 vs. 14-16 weeks), and conducted playbacks of high amplitude, long-range song. In one population, we also played low amplitude, short-range song, a highly potent elicitor of aggression in juncos and many songbirds. We observed strong aggressive responses to both types of song, but no detectable elevation of plasma testosterone or corticosterone in either population. We also measured rise in corticosterone in response to handling post-playback, and found full capacity to elevate corticosterone but no effect of song class (long-range or short-range) on elevation. Collectively, our data suggest that males can mount an aggressive response to playback without a change in testosterone or corticosterone, despite the ability to alter these hormones during other types of social interactions. We discuss the observed decoupling of circulating hormones and aggression in relation to mechanisms of behavior and the cues that may activate the HPA and HPG axes.

Low-amplitude songs produced by male dark-eyed juncos (Junco hyemalis) differ when sung during intra- and inter-sexual interactions

The function and relative importance of low-amplitude (quiet) acoustic signals remains a poorly understood aspect of animal communication. Research in songbirds has predominantly focused on the role of low-amplitude songs as reliable predictors of attack and signals of aggressive intent. However, many species of songbirds produce low-amplitude song in the presence of both male and female conspecifics, suggesting a broader range of functions beyond aggressive behavior. Male dark-eyed juncos (Junco hyemalis) produce two distinct types of low-amplitude song: (1) soft long-range song (LRS), which is a lower amplitude version of junco LRS, and (2) short-range song (SRS), which is substantially more complex and structurally distinct from LRS. SRS is also sung at two distinct tempos (slow and fast) and has been observed in both male- and female-directed contexts. In this study, we presented free-living male juncos with a caged male or female conspecific accompanied by playback of LRS, a female precopulatory trill, or slow SRS and quantified the songs elicited by each social condition. Males produced slow SRS only in response to a female conspecific paired with a precopulatory trill or slow SRS, never to a male, even when males were paired with slow SRS. Together these observations indicate that slow SRS is a female-directed song. In contrast, males produced both LRS and soft LRS in the presence of conspecifics of both sexes, which suggests that LRS may serve a similar function with respect to male and female receivers regardless of amplitude. These results highlight the importance of investigating the production of low-amplitude songs in both intra- and inter-sexual contexts and provide further evidence that in juncos, slow SRS functions in courtship.

Highly context-specific activation of the HPG axis in the dark-eyed junco and implications for the challenge hypothesis.

One of the best studied hormone-behavior interactions is the transient rise in testosterone (T) associated with male-male aggression. However, recent research on songbirds has demonstrated numerous exceptions to this pattern.One species previously thought to elevate T in response to a simulated territorial intrusion is the dark-eyed junco (Junco hyemalis). Here, we show that under most circumstances male juncos do not elevate circulating T or CORT levels in response to social stimuli, despite being physiologically capable of elevating T as indicated by their response to GnRH. The lack of hormonal response was found regardless of the sex of the social stimulus (singing male vs. soliciting female), its sensory modality (song only, song + live lure, song + taxidermic mount), or the timecourse of sampling. Notably, males did elevate T levels when exposed to a simulated territorial intrusion in the days following simulated predation of their chicks. Whether the high T seen in these narrow circumstances represents stage-dependent social modulation of T or re-activation of male reproductive physiology in preparation for re-nesting (i.e. socially independent T modulation) remains to be determined. It is clear, however, that activation of the HPG axis is highly context-specific for male juncos. These results highlight important and unresolved issues regarding the socially mediated component of the challenge hypothesis and how it relates to the evolution of hormone-mediated traits.

Male Dark-eyed Juncos (Junco hyemalis) Respond Differentially to Playback of Local and Foreign Song

ABSTRACT The songs of oscine birds, given their cultural inheritance, can readily diverge, which can foster assortative mating and ultimately reproductive isolation. The species complex of Dark-eyed Juncos (Junco hyemalis) consists of at least six distinct subspecies and represents an ideal system for studying divergence in mating signals owing to its recent, rapid radiation throughout North America since the last glaciation (<15,000 yrs). Each subspecies of Dark-eyed Junco is characterized by distinct plumage and morphological characteristics, but divergence among the subspecies in song and the role of song as a potential isolating mechanism remains to be rigorously tested. In this study, I compared territorial responses of male juncos in Virginia to playback of locally recorded songs and songs recorded from a different population and subspecies in California. Males responded aggressively to playbacks from both populations, but they approached more rapidly and closely, and performed more flyovers when responding to local song types. While these results suggest that male juncos can discriminate between songs of different populations, future work should investigate female preferences for local and foreign songs and also address more populations, particularly those located in active hybrid zones.

Estimation of Female Home-range Size During the Nestling Period of Dark-eyed Juncos

Abstract Studies of spatial activity of songbirds during the nesting cycle have largely focused on male activity and neglected female space use, particularly outside the fertile period. We estimated the home-range size of seven female Dark-eyed Juncos (Junco hyemalis) 3 days after their nestlings had hatched. We used radiotelemetry to track female movements for 2 hrs on the afternoon of day 3 of nestling life, and 2 hrs on both the morning and afternoon of days 4 and 5. Female location and behavior were recorded every 10 min for the duration of tracking. Females exhibited a mean home-range size of 0.833 ha (range  =  0.156–2.450 ha). Our estimate of home-range size during the nestling period was significantly smaller than a previous estimate of female home-range size during the fertile period in the same junco population. Home-range size varied greatly between individuals, and the observed differences may be attributable to variation in resource availability.

Species recognition in a vocal mimic: repetition pattern not the only cue used by Northern Mockingbirds in discriminating songs of conspecifics and Brown Thrashers

Abstract Vocal mimics that produce large repertoires of song types, such as in the Mimidae, have unique challenges discriminating songs of conspecifics from those of other mimids in areas where these species co-occur. We investigated cues used by Northern Mockingbirds (Mimus polyglottos) in discriminating their songs from songs of a sympatric mimid, the Brown Thrasher (Toxostoma rufum). We presented territorial mockingbirds with four playback treatments in which either mockingbird song types or thrasher song types had either a standardized mockingbird repetition pattern (5 repetitions) or a standardized thrasher pattern (2 repetitions). Four measures (time within 2 m of speaker, latency to approach, closest approach, and number of flights) were used to estimate a subjects response to each playback. Subjects responded significantly more strongly to mockingbird song types in a mockingbird repetition pattern than to thrasher song types in either repetition pattern. Responses to mockingbird song types in a thrasher repetition pattern elicited intermediate responses. Thus, mockingbirds can distinguish conspecific songs from Brown Thrasher songs based on song types alone regardless of their repetition pattern, although repetition pattern still appears to have a role in conspecific recognition. Brown Thrasher song includes a significantly broader frequency range than mockingbird song, which may allow direct discrimination. Our results suggest cues used by mimids in species discrimination are not necessarily the same as those used by human observers.

Condition- and context-dependent factors are related to courtship behavior of paired and unpaired males in a socially monogamous songbird

ABSTRACT Males of many animal species display to attract and stimulate potential mates. In socially monogamous species, males will court females both to establish a pair bond and to solicit extrapair copulations. We investigated whether paired and unpaired male Dark-eyed Juncos (Junco hyemalis) differ in their courtship of a novel female and whether their courtship behavior is related to their morphology or circulating hormones. We conducted simulated courtship interactions (SCI) by presenting free-living paired and unpaired males with a live, caged conspecific female accompanied by playback of a precopulatory trill, a signal of female receptivity, and tested predictions of multiple hypotheses. We quantified courtship behaviors for 20 min and then captured the males, measured them, and collected blood samples to quantify circulating post-SCI testosterone and corticosterone levels as well as restraint-induced corticosterone. Paired males approached the female more rapidly and spent more time in close proximity to the female than unpaired males. Paired males were also more active and spent more time with body feathers fully erect, but sang fewer songs, compared to unpaired males. Unpaired males were smaller in mass than paired males and had higher post-SCI corticosterone and restraint-induced corticosterone than paired males, but the groups did not differ in post-SCI testosterone. We discuss whether these findings should be interpreted as differences in how males court when seeking a social mate vs. an extrapair mate or as inherent differences between successful and unsuccessful males.

Avian olfactory displays: a hypothesis for the function of bill-wiping in a social context

Bill-wiping, or the scraping by a bird of its bill along a substrate, has been observed in social contexts and cited as an irrelevant displacement activity. However, several behaviors once categorized as displacement behaviors have since been shown to serve adaptive functions. Here, we hypothesize that bill-wiping may function in social interactions by releasing odors from the waxy residue of preen oil on the bill. We assessed behavioral context associated with bill-wiping by comparing the frequency of bill-wiping by free-living male songbirds when presented with a caged male or female conspecific paired with playback; males bill-wiped significantly more often in response in a courtship context and in a mate-guarding context than in a territorial context. Bill-wiping frequency correlated with courtship behaviors, such as tail spreading and singing short-range songs, but not with aggressive behaviors. We also noted attributes of individuals that engaged in bill-wiping during courtship and found that younger, smaller males performed this behavior more frequently than older, larger males. Finally, we conducted a captive Y-maze experiment to test whether dried preen oil residue would be more detectable if it were manipulated (scratched to potentially release odor) or unmanipulated. Preliminary evidence suggests that males could be more responsive to manipulated preen oil, though stronger tests are needed. Taken together, our results suggest a functional hypothesis: bill-wiping during courtship may be an olfactory display that releases odor that may be detected by potential mates and rivals. We conclude by suggesting ways in which future work can test the olfactory display hypothesis.