Vocal traits of shorebird chicks are related to body mass and sex

Acoustic communication is critical during early life phases in precocial birds. For example, adult alarm calls can elicit antipredator behaviour in young, and chick vocalisations can communicate information to parents about chick identity, condition, location, sex, or age. We investigated whether chick calls of two species of Australian Charadriidae vary with sex or body mass. We handled Red-capped Plover Charadrius ruficapillus and Southern Masked Lapwing Vanellus miles novaehollandiae chicks for purposes of measurement, blood sampling, and banding. We opportunistically recorded their distress calls while in the hand, and analysed the calls to determine whether call structure is related to sex or body mass (a proxy for age). We measured five traits per call, plus time intervals between successive calls, for 26 plover chicks (2600 calls) and 95 lapwing chicks (6835 calls). In plovers, inter-call intervals were shorter in males and both inter-call interval and the dominant frequency range of calls decreased with increasing body mass. In lapwings, frequency modulation (computed as the range in the rate of change of the dominant frequency) was lower in male calls. The dominant frequency range of lapwing calls decreased with mass in both sexes, but the decline was greater in males, resulting in a lower dominant frequency range in males. Frequency modulation and entropy of lapwing calls also decreased with increasing body mass. Minimum dominant frequency did not change with body mass or sex in either species. Our study provides the first evidence for charadriid chicks of (a) a sexual difference in call structure and rate and (b) gradual growth-related changes in call structure and rate, across chicks. Studies on calls from a greater range of chick ages and from more species within this large and diverse family would be valuable. We provide a foundation for further studies of shorebird vocalisations during growth, which may elucidate the development and functional significance of such vocalisations.

Temperature-induced changes in egg white antimicrobial concentrations during pre-incubation do not influence bacterial trans-shell penetration but do affect hatchling phenotype in Mallards

Microbiome formation and assemblage are essential processes influencing proper embryonal and early-life development in neonates. In birds, transmission of microbes from the outer environment into the egg’s interior has been found to shape embryo viability and hatchling phenotype. However, microbial transmission may be affected by egg-white antimicrobial proteins (AMPs), whose concentration and antimicrobial action are temperature-modulated. As both partial incubation and clutch covering with nest-lining feathers during the pre-incubation period can significantly alter temperature conditions acting on eggs, we experimentally investigated the effects of these behavioural mechanisms on concentrations of both the primary and most abundant egg-white AMPs (lysozyme and avidin) using mallard (Anas platyrhychos) eggs. In addition, we assessed whether concentrations of egg-white AMPs altered the probability and intensity of bacterial trans-shell penetration, thereby affecting hatchling morphological traits in vivo. We observed higher concentrations of lysozyme in partially incubated eggs. Clutch covering with nest-lining feathers had no effect on egg-white AMP concentration and we observed no association between concentration of egg-white lysozyme and avidin with either the probability or intensity of bacterial trans-shell penetration. The higher egg-white lysozyme concentration was associated with decreased scaled body mass index of hatchlings. These outcomes demonstrate that incubation prior to clutch completion in precocial birds can alter concentrations of particular egg-white AMPs, though with no effect on bacterial transmission into the egg in vivo. Furthermore, a higher egg white lysozyme concentration compromised hatchling body condition, suggesting a potential growth-regulating role of lysozyme during embryogenesis in precocial birds.

Common Patterns of Skull Bone Fusion and Their Potential to Discriminate Different Ontogenetic Stages in Extant Birds

The degree of sutural closure between bones generally allows for the classification of skeleton maturity in tetrapods. In mammals, the sutural closure of skull bones was previously used as proxy to evaluate the ontogenetic stage of single individuals. However, due to temporal variation, this process can be only applied among mammalian subclades, but not for all mammals in general. In contrast, the process of sutural closures in bird skulls could be a more reliable ontogenetic proxy for this clade as adult birds commonly show a generally high degree of bone fusion. To test this, we studied the process of sutural closure in ontogenetic series of 18 extant bird species regarding the presence of an ontogenetic signal and compared the results with changes in skull size and proportions. Univariate analyses indicate that bone fusion happens faster in altricial than in precocial birds. However, the use of PCoA and multivariate regressions reveal that the skull bone fusion follows a common pattern among birds and thus can be used as proxy to identify different ontogenetic stages. In general, the process of sutural closure spreads from posterior to anterior and from ventral to dorsal. In contrast, skull measurements reflect rather interspecific allometry than ontogeny. The used of bone fusion as proxy will help to better identify and compare different stages of maturation in birds, including historical material from osteological collections.

Partial incubation-induced changes in concentrations of egg white antimicrobials do not influence trans-shell infection but affect hatchling phenotype

Host-microbiome interactions during embryonal and early phase of life is critical point in microbiome formation and assemblage in neonates. In birds, transmission of microbes from the outer environment into the egg interior was found to shape embryo viability and hatchlings phenotype. Microbes’ transmission may be modulated by egg white antimicrobial proteins (AMPs) whose concentration and antimicrobial action are temperature-modulated. As partial incubation and clutch covering with nest-lining feathers during pre-incubation period may both significantly alter temperature conditions acting on eggs, we experimentally investigated effects of these behavioural mechanisms on the concentrations of primary egg white AMPs - lysozyme and avidin using Mallard (Anas platyrhychos) eggs. Moreover, we studied in vivo if concentrations of egg white AMPs reduced probability and intensity of bacterial trans-shell infection and hatchlings phenotype. We found significantly higher egg white lysozyme concentration, while avidin concentration tended to be higher in partially incubated eggs. Clutch covering with nest-lining feathers had no effect on egg white AMPs concentrations. Neither probability nor intensity of bacterial trans-shell infection was associated with concentrations of egg white AMPs. Finally, increased egg white lysozyme was associated with decreased scaled body mass index of hatchlings. These outcomes demonstrate that incubation prior to clutch completion in precocial birds may modulate concentrations of particular egg white AMPs, yet without any effect on transmission of bacteria into the egg in vivo. Furthermore, increased egg white lysozyme may compromise body condition of hatchlings supporting growth-regulating role of lysozyme during embryogenesis in precocial birds.

Do small precocial birds enter torpor to conserve energy during development?

ABSTRACTPrecocial birds hatch feathered and mobile, but when they become fully endothermic soon after hatching, their heat loss is high and they may become energy depleted. These chicks could benefit from using energy-conserving torpor, which is characterised by controlled reductions of metabolism and body temperature (Tb). We investigated at what age the precocial king quail Coturnix chinensis can defend a high Tb under a mild thermal challenge and whether they can express torpor soon after achieving endothermy to overcome energetic and thermal challenges. Measurements of surface temperature (Ts) using an infrared thermometer showed that king quail chicks are partially endothermic at 2–10 days, but can defend high Tb at a body mass of ∼13 g. Two chicks expressed shallow nocturnal torpor at 14 and 17 days for 4–5 h with a reduction of metabolism by >40% and another approached the torpor threshold. Although chicks were able to rewarm endogenously from the first torpor bout, metabolism and Ts decreased again by the end of the night, but they rewarmed passively when removed from the chamber. The total metabolic rate increased with body mass. All chicks measured showed a greater reduction of nocturnal metabolism than previously reported in quails. Our data show that shallow torpor can be expressed during the early postnatal phase of quails, when thermoregulatory efficiency is still developing, but heat loss is high. We suggest that torpor may be a common strategy for overcoming challenging conditions during development in small precocial and not only altricial birds.

Imprinting as Social Learning

Imprinting is a form of rapid, supposedly irreversible learning that results from exposure to an object during a specific period (a critical or sensitive period) during early life and produces a preference for the imprinted object. The word “imprinting” is an English translation of the German Prägung (“stamping in”), coined by Konrad Lorenz in 1935 to refer to the process that he studied in geese. Two types of imprinting have traditionally been distinguished: filial imprinting, involving the formation of an immediate social attachment to the mother or a mother-substitute, and sexual imprinting, involving the formation of a sexual preference that is manifested later in life. Both types of imprinting were subject to extensive experimental study beginning around 1950. Originally described in precocial birds (ducks, geese, and domestic chickens), imprinting has also been used to explain the formation of early social attachments in other species, including human infants. Imprinting has served as a useful model for studying the neural processes involved in learning and behavioral development and has provided a framework for thinking about other developmental processes.

Vocal recognition of a nest-predator in black grouse

Corvids count among the important predators of bird nests. They are vocal animals and one can expect that birds threatened by their predation, such as black grouse, are sensitive to and recognize their calls. Within the framework of field studies, we noticed that adult black grouse were alerted by raven calls during periods outside the breeding season. Since black grouse are large, extremely precocial birds, this reaction can hardly be explained by sensitization specifically to the threat of nest predation by ravens. This surprising observation prompted us to study the phenomenon more systematically. According to our knowledge, the response of birds to corvid vocalization has been studied in altricial birds only. We tested whether the black grouse distinguishes and responds specifically to playback calls of the common raven. Black grouse recognized raven calls and were alerted, displaying typical neck stretching, followed by head scanning, and eventual escape. Surprisingly, males tended to react faster and exhibited a longer duration of vigilance behavior compared to females. Although raven calls are recognized by adult black grouse out of the nesting period, they are not directly endangered by the raven. We speculate that the responsiveness of adult grouse to raven calls might be explained as a learned response in juveniles from nesting hens that is then preserved in adults, or by a known association between the raven and the red fox. In that case, calls of the raven would be rather interpreted as a warning signal of probable proximity of the red fox.

An imprinting object rapidly acquires high attractiveness when associated with food delivery

Young precocial birds develop a preference for an imprinting object by mere visual exposure to it in the absence of conventional physiological reinforcement. The lack of the necessity of conventional reinforcement for imprinting, however, does not mean that such reinforcement is unimportant. The evidence presented here shows that an imprinting object rapidly acquires high attractiveness to young chicks when it is associated with food provisioning. Domestic chicks, Gallus gallus domesticus, were first exposed to two different imprinting objects in the absence of any reinforcement. Subsequently, two groups of chicks received a single feeding session wherein they were provided with prey from one of the imprinting objects. A third group served as a control in which the chicks were exposed to one of the imprinting objects and prey delivery in an unpaired way. Finally, all chicks received two choice tests to assess their preferences for the two imprinting objects. The chicks that received food from an imprinting object strongly preferred that object to the alternative familiar-only object, and preferred the familiar-only object to a novel object. The control group did not show any preference between the two imprinting objects, but preferred the unpaired imprinting object to a novel object. These results suggest that primary-need reinforcers such as food contribute to increasing the attractiveness of an imprinting object by promoting rapid associative learning.