Diane Colombelli-Négrel

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.

High levels of extra-pair paternity in Superb Fairy-wrens in South Australia despite low frequency of auxiliary males

Abstract The Superb Fairy-wren (Malurus cyaneus) is a model system in which to study cooperative breeding and extra-pair paternity. Previous studies in this species have shown that 61–76% of nestlings were extra-pair young and 92–95% of nests contained at least one extra-pair young. Furthermore, the probability of extra-pair paternity was higher when auxiliary males were present. We studied group size and extra-pair paternity in South Australia where, unlike other study sites, auxiliary males were relatively uncommon: 16% of nests had one auxiliary male compared to 37–80% with at least one auxiliary per nest in other studies. We predicted a lower incidence of extra-pair paternity, given the shortage of auxiliary males. Our results did not support this prediction: we found extra-pair paternity among 67% of nestlings and 83% of nests.

When subspecies matter: resident Superb Fairy-wrens (Malurus cyaneus) distinguish the sex and subspecies of intruding birds

Abstract The widely accepted functions of complex bird song—to defend a territory or attract a mate, or both—have generally been tested in northern hemisphere species in which males produce the song and females choose the singer. In our study species, the Superb Fairy-wren (Malurus cyaneus), both males and females sing a solo song throughout the year. We compare the chatter song in males and females of two genetically distinct subspecies, and test if resident birds respond to the sex and subspecies of the intruder song. Compared with island birds (M. c. ashbyi), mainland Superb Fairy-wrens (M. c. leggei) produced songs with lower frequency and fewer elements. Compared with females, males produced longer songs with more elements. Resident birds showed acoustical discrimination for the sex and subspecies of the intruder bird. The response of resident pairs was positively correlated, but each sex showed a solo response. Resident males were the first to respond to male intruders, and resident females were the first to respond to female intruders. Fairy-wrens had the strongest response towards (1) intruders of the same subspecies and (2) male intruders. The finding of signal divergence and acoustical discrimination in males and females makes this a model system to test the mechanism of reproductive isolation when both sexes sing.

A new audio-visual technique for effectively monitoring nest predation and the behaviour of nesting birds

Abstract Effective monitoring techniques are vital to understanding a range of behaviours and their consequences for evolution of life histories. Video and photographic monitoring is regularly used but rarely with audio monitoring even though it can identify birds or predators off-camera, and detect alarm calls and songs. We developed a 4-channel audio-visual recording system to continuously monitor the nests of Superb Fairy-wrens (Malurus cyaneus). This innovative system worked autonomously for 3 days and identified repeat visits by some predators, detected nest predation by Grey Currawong (Strepera versicolor) and two rodents, and provided new insights into nest defence, provisioning rates, vocalisations of parents and nestlings and interactions between them.

Host response to cuckoo song is predicted by the future risk of brood parasitism

IntroductionRisk assessment occurs over different temporal and spatial scales and is selected for when individuals show an adaptive response to a threat. Here, we test if birds respond to the threat of brood parasitism using the acoustical cues of brood parasites in the absence of visual stimuli. We broadcast the playback of song of three brood parasites (Chalcites cuckoo species) and a sympatric non-parasite (striated thornbill, Acanthiza lineata) in the territories of superb fairy-wrens (Malurus cyaneus) during the peak breeding period and opportunistic breeding period. The three cuckoo species differ in brood parasite prevalence and the probability of detection by the host, which we used to rank the risk of parasitism (high risk, moderate risk, low risk).ResultsHost birds showed the strongest response to the threat of cuckoo parasitism in accordance with the risk of parasitism. Resident wrens had many alarm calls and close and rapid approach to the playback speaker that was broadcasting song of the high risk brood parasite (Horsfield’s bronze-cuckoo, C. basalis) across the year (peak and opportunistic breeding period), some response to the moderate risk brood parasite (shining bronze-cuckoo, C. lucidus) during the peak breeding period, and the weakest response to the low risk brood parasite (little bronze-cuckoo, C. minutillus). Playback of the familiar control stimulus in wren territories evoked the least response.ConclusionHost response to the threat of cuckoo parasitism was assessed using vocal cues of the cuckoo and was predicted by the risk of future parasitism.

Risky revelations: Superb Fairy-wrens Malurus cyaneus respond more strongly to their mate’s alarm song

The study of animal communication during predator encounters has provided insights into the function of kin selection, the ontogeny of vocal development, and the mechanism of predator recognition. Less attention has been devoted to the study of geographic variation in alarm vocalisation behaviour. Here, we describe an alarm song produced by Superb Fairy-wrens (Malurus cyaneus) under immediate threat of predation. We quantify geographic and individual variation in alarm song. Next, we used playback experiments to measure the effect of familiar versus unfamiliar alarm song on the response of the pair partner to its mate’s alarm song. We found both geographic (element frequencies across sites) and sex-based (females had larger bandwidth) differences in alarm song. Playback of the alarm song evoked distinct anti-predator behavioural responses, whereby the alarm song of mates evoked stronger alarm responses (faster latency to respond, longer latency to feed, more head movements, and change in vocalisation types) than those of unfamiliar birds. We discuss the benefits of geographic and individual variation in alarm song, which may be particularly favoured in long-lived sedentary species that form pair bonds.

Video nest monitoring reveals male coloration-dependant nest predation and sex differences in prey size delivery in a bird under high sexual selection

Increased predation risk should select for reduced parental activity to decrease the probability of visually hunting predators discovering the nest. Parental activity and conspicuousness are known to increase predation risk. Here, we test for sex differences in parental visitation rate (number of visits), time seen at the nest (time at the nest × adult visibility), and food delivery (prey size) using continuous video recordings at nests. We test the role of these variables for predation outcome in the Superb Fairy-wren (Malurus cyaneus). The study species is sexually dimorphic: males have iridescent blue plumage while females have brown plumage. The results showed that nest predation was predicted by male time seen at the nest (but not visitation rate), but not female time seen at the nest (or visitation rate). Contrary to our expectation that males would have lower visitation rates than females, our analysis of video images showed that male and female visitation was comparable but that males consistently brought smaller prey items to the nest than females. These findings are discussed in the light of morphological differences between male and female beak size. We conclude that sexual selection has favoured conspicuous male signalling in this system, and that natural selection should select for reduced parental care for the conspicuous sex.

In superb fairy wrens (Malurus cyaneus), nuptial males have more blood parasites and higher haemoglobin concentration than eclipsed males

Blood parasites rupture mature red blood cells and so reduce haemoglobin concentration and hence the potential activity levels of infected males. We examined blood parasites and haemoglobin concentration in the superb fairy-wren (Malurus cyaneus) across three years and six locations in South Australia. We tested the prediction that males in nuptial plumage have more blood parasites and hence lower haemoglobin concentration than males in eclipsed plumage. Of 188 birds, 20 (10.6%) had blood parasites (Haemaproteus spp). We found that (1) there was an effect of season and sex on haemoglobin concentration; (2) there was no effect of haemoglobin concentration on prevalence of blood parasites or intensity; and (3) males in nuptial plumage had more blood parasites but higher haemoglobin concentration than eclipsed males.

Females that experience threat are better teachers.

Superb fairy-wren (Malurus cyaneus) females use an incubation call to teach their embryos a vocal password to solicit parental feeding care after hatching. We previously showed that high call rate by the female was correlated with high call similarity in fairy-wren chicks, but not in cuckoo chicks, and that parent birds more often fed chicks with high call similarity. Hosts should be selected to increase their defence behaviour when the risk of brood parasitism is highest, such as when cuckoos are present in the area. Therefore, we experimentally test whether hosts increase call rate to embryos in the presence of a singing Horsfields bronze-cuckoo (Chalcites basalis). Female fairy-wrens increased incubation call rate when we experimentally broadcast cuckoo song near the nest. Embryos had higher call similarity when females had higher incubation call rate. We interpret the findings of increased call rate as increased teaching effort in response to a signal of threat.

Extended parental care of fledglings: Parent birds adjust anti-predator response according to predator type and distance

Parent birds are expected to show anti-predator responses when predators are in the vicinity of their fledglings and to modify their response in relation to perceived risk posed by the predator. We used the superb fairy-wren ( Malurus cyaneus ) to experimentally test predictions of the risk-based alarm call hypothesis, whereby alarm vocalisation response is a proxy for predator risk (type, distance). Our results showed that birds modified their response to three factors: predator type (snake, fox, stationary and gliding sparrowhawks), predator distance (close, distant) and fledgling presence. We found evidence of post-fledging parental care in response to the fox, which was significantly higher when fledglings were present irrespective of predator distance. However, fledgling presence was not related to alarm vocalisations to the snake or the sparrowhawks (only distance predicted vocalisation response). A comparison of the different types of vocalisations (terrestrial call, aerial call, alarm song) showed that alarm vocalisations were significantly related to predator type. Fledgling presence also affected the frequency of parental terrestrial alarm calls. We conclude that anti-predator response is a dynamic process that reflects offspring presence and perceived predation risk, with implications for understanding vocal communication in birds.