The ecology of zebra finch song and its implications for vocal communication in multi-level societies.

Acoustic signalling is crucial in affecting movements and in social interactions. In species with dynamic social structures, such as multi-level societies, acoustic signals can provide a key mechanism allowing individuals to identify and find or avoid each other and to exchange information. Yet, if the spacing between individuals regularly exceeds the maximum signalling range, the relation between movements and signals becomes more complex. As the best-studied songbird in captivity, the zebra finch (Taeniopygia castanotis) is a species with individually distinct songs that are audible over just a few metres and a widely ranging dynamic multi-level social organization in the wild, raising questions on the actual role of its song in social cohesion and coordination. Here, we provide an overview of birdsong in social organizations (networks) and use the ecology of the zebra finch and male song to discuss how singing can facilitate social cohesion and coordination in species where the signal range is very short. We raise the question of the extent to which zebra finches are a representative species to understand the function of song in communication, and we broaden current views on the function of birdsong and its individual signature. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

High nest failure in a zebra finch population and persistent nest predation by a monitor lizard.

Predation is well known to have substantial effects on behaviour and fitness in many animals. In songbirds, nest predation is rarely observed directly, so that research focusses primarily on the consequences of predation and less on the behaviour of the predator. Here, we report predation data in a zebra finch (Taeniopygia catanosis) nest box population, highlighting a 22-min-long sequence, captured on video, of a sand goanna (Varanus gouldii) predating a zebra finch nest in the wild. This monitor lizard appeared to be extremely persistent with climbing and jumping up to the next box nine times, including three successive unsuccessful attempts that lead to a change in approach strategy. It removed all six nestlings from the nest box during those repeated approaches and consumed them. In combination with overall high predation rates in the study population we document here, the findings highlight the role that a single predator species can have on nest success and, thus potentially also breeding decisions and social organisation of the prey population. Specifically so in a species like the zebra finch which synchronises reproductive attempts through the use of social information acquired through nest inspections and which uses social hotspots where they could gather information on changes in local social composition due to the individualised signals they use.

Edge computing in wildlife behavior and ecology.

Modern sensor technologies increasingly enrich studies in wildlife behavior and ecology. However, constraints on weight, connectivity, energy and memory availability limit their implementation. With the advent of edge computing, there is increasing potential to mitigate these constraints, and drive major advancements in wildlife studies.

The social role of song in wild zebra finches.

Male songbirds sing to establish territories and to attract mates.1,2 However, increasing reports of singing in non-reproductive contexts3 and by females4,5 show that song use is more diverse than previously considered. Therefore, alternative functions of song, such as social cohesion3 and synchronization of breeding, by and large, were overlooked even in such well-studied species such as the zebra finch (Taeniopygia guttata). In these social songbirds, only the males sing, and pairs breed synchronously in loose colonies,6,7 following aseasonal rain events in their arid habitat.8,9 As males are not territorial, and pairs form long-term monogamous bonds early in life, conventional theory predicts that zebra finches should not sing much at all; however, they do and their song is the focus of hundreds of lab-based studies.10,11,12,13,14,15,16,17,18,19,20,21,22 We hypothesize that zebra finch song functions to maintain social cohesion and to synchronize breeding. Here, we test this idea using data from 5 years of field studies, including observational transects, focal and year-round audio recordings, and a large-scale playback experiment. We show that zebra finches frequently sing while in groups, that breeding status influences song output at the nest and at aggregations, that they sing year round, and that they predominantly sing when with their partner, suggesting that the song remains important after pair formation. Our playback reveals that song actively features in social aggregations as it attracts conspecifics. Together, these results demonstrate that birdsong has important functions beyond territoriality and mate choice, illustrating its importance in coordination and cohesion of social units within larger societies.

Zebra finch song is a very short-range signal in the wild: evidence from an integrated approach.

Birdsong is typically seen as a long-range signal functioning in mate attraction and territory defense. Among birds, the zebra finch is the prime model organism in bioacoustics, yet almost exclusively studied in the lab. In the wild, however, zebra finch song differs strikingly from songbirds commonly studied in the wild as zebra finch males sing most after mating and in the absence of territoriality. Using data from the wild, we here provide an ecological context for a wealth of laboratory studies. By integrating calibrated sound recordings, sound transmission experiments and social ecology of zebra finches in the wild with insights from hearing physiology we show that wild zebra finch song is a very short-range signal with an audible range of about nine meters and that even the louder distance calls do not carry much farther (up to about fourteen meters). These integrated findings provide an ecological context for the interpretation of laboratory studies of this species and indicate that the vocal communication distance of the main laboratory species for avian acoustics contrasts strikingly with songbirds that use their song as a long-range advertisement signal.

Great tits do not compensate over time for a radio-tag-induced reduction in escape-flight performance.

The use of biologging and tracking devices is widespread in avian behavioral and ecological studies. Carrying these devices rarely has major behavioral or fitness effects in the wild, yet it may still impact animals in more subtle ways, such as during high power demanding escape maneuvers. Here, we tested whether or not great tits (Parus major) carrying a backpack radio-tag changed their body mass or flight behavior over time to compensate for the detrimental effect of carrying a tag. We tested 18 great tits, randomly assigned to a control (untagged) or one of two different types of a radio-tag as used in previous studies in the wild (0.9 g or 1.2 g; ~5% or ~6-7% of body mass, respectively), and determined their upward escape-flight performance 1, 7, 14, and 28 days after tagging. In between experiments, birds were housed in large free-flight aviaries. For each escape-flight, we used high-speed 3D videography to determine flight paths, escape-flight speed, wingbeat frequency, and actuator disk loading (ratio between the bird weight and aerodynamic thrust production capacity). Tagged birds flew upward with lower escape-flight speeds, caused by an increased actuator disk loading. During the 28-day period, all groups slightly increased their body mass and their in-flight wingbeat frequency. In addition, during this period, all groups of birds increased their escape-flight speed, but tagged birds did so at a lower rate than untagged birds. This suggests that birds may increase their escape-flight performance through skill learning; however, tagged birds still remained slower than controls. Our findings suggest that tagging a songbird can have a prolonged effect on the performance of rapid flight maneuvers. Given the absence of tag effects on reproduction and survival in most songbird radio-tagging studies, tagged birds in the wild might adjust their risk-taking behavior to avoid performing rapid flight maneuvers.

Extraterritorial forays by great tits are associated with dawn song in unexpected ways.

Conspicuous male signals often play an important role in both attracting mates and deterring rivals. In territorial species with extrapair mating, female and male forays to other territories may be an important component underlying female choice and male mating success and might be influenced by male advertisement signals. Yet, whether off-territory foraying is associated with male signals is still not well understood. Here, we tested how female and male forays are associated with short-range visual and long-range acoustic signals (dawn song). We used an automated radio tracking system to follow the movements of wild great tits (Parus major) to other territories in relation to male dawn song, plumage ornaments, and extrapair paternity. We show that both sexes frequently forayed into others' territories throughout the breeding period. Movements of both males and females were associated with male song but not with plumage ornaments. Contrary to our expectations, females stayed away from territories where males sang elaborately, whereas males were attracted to those territories. Moreover, neither female nor male forays were associated with the occurrence of extrapair offspring. Our results, thus, suggest that, although forays into other territories are associated with male dawn song, females may not be attracted and males not repelled by dawn song. This sheds a different light on the sex-specific effects of male advertisement signals, expanding the view on the selection pressures shaping such communication systems.

Bumblebees land remarkably well in red-blue greenhouse LED light conditions.

Red-blue emitting LEDs have recently been introduced in greenhouses to optimise plant growth. However, this spectrum may negatively affect the performance of bumblebees used for pollination, because the visual system of bumblebees is more sensitive to green light than to red-blue light. We used high-speed stereoscopic videography to three-dimensionally track and compare landing manoeuvres of Bombus terrestris bumblebees in red-blue light and in regular, broad-spectrum white light. In both conditions, the landing approaches were interspersed by one or several hover phases, followed by leg extension and touchdown. The time between leg extension and touchdown was 25% (0.05 s) longer in red-blue light than in white light, caused by a more tortuous flight path in red-blue light. However, the total landing duration, specified as the time between the first hover phase and touchdown, did not differ between the light conditions. This suggests that the negative effects of red-blue light on the landing manoeuvre are confined to the final phase of the landing.This article has an associated First Person interview with the first author of the paper.

Early-life microbiota transplantation affects behavioural responses, serotonin and immune characteristics in chicken lines divergently selected on feather pecking.

Gut microbiota influences host behaviour and physiology, such as anxiety, stress, serotonergic and immune systems. These behavioural and physiological characteristics are related to feather pecking (FP), a damaging behaviour in chickens that reduces animal welfare and productivity. Moreover, high FP (HFP) and low FP (LFP) lines differed in microbiota composition. However, it is unknown whether microbiota can influence the development of FP. For the first time, we identified the effects of microbiota transplantation on FP, and behavioural and physiological characteristics related to FP. HFP and LFP chicks received sterile saline (control), HFP or LFP microbiota transplantation during the first two weeks post-hatch. Microbiota transplantation influenced behavioural responses of the HFP line during treatment and of the LFP line after treatment. In both lines, homologous microbiota transplantation (i.e., receiving microbiota from their line) resulted in more active behavioural responses. Furthermore, microbiota transplantation influenced immune characteristics (natural antibodies) in both lines and peripheral serotonin in the LFP line. However, limited effects on microbiota composition, stress response (corticosterone) and FP were noted. Thus, early-life microbiota transplantation had immediate and long-term effects on behavioural responses and long-term effects on immune characteristics and peripheral serotonin; however, the effects were dependent on host genotype. Since early-life microbiota transplantation influenced behavioural and physiological characteristics that are related to FP, it could thus influence the development of FP later in life.

Repeatability of signalling traits in the avian dawn chorus.

BACKGROUND: Birdsong, a key model in animal communication studies, has been the focus of intensive research. Song traits are commonly considered to reflect differences in individual or territory quality. Yet, few studies have quantified the variability of song traits between versus within individuals (i.e. repeatability), and thus whether certain song traits indeed provide reliable individual-specific information. Here, we studied the dawn chorus of male great tits (Parus major) to determine if key song traits are repeatable over multiple days and during different breeding stages. Additionally, we examined whether repeatability was associated with exploration behaviour, a relevant personality trait. Finally, we tested if variation in song traits could be explained by breeding stage, lowest night temperature, and exploration behaviour. RESULTS: We show that the start time of an individual's dawn song was indeed repeatable within and across breeding stages, and was more repeatable before, than during, their mate's egg laying stage. Males started singing later when the preceding night was colder. Daily repertoire size was repeatable, though to a lesser extent than song start time, and no differences were observed between breeding stages. We did not find evidence for an association between exploration behaviour and variation in dawn song traits. Repertoire composition, and specifically the start song type, varied across days, but tended to differ less than expected by chance. CONCLUSIONS: Our findings that individuals consistently differ in key song traits provides a better understanding of the information receivers can obtain when sampling songs of different males. Surprisingly, start time, despite being influenced by a highly variable environmental factor, appeared to be a more reliable signal of individual differences than repertoire size. Against expectation, singers were more repeatable before than during their mate's egg laying stage, possibly because before egg laying, females are less constrained to move around unguarded and thus may then already sample (and compare) different singers. Combining repeated dawn song recordings with spatial tracking could reveal if the sampling strategies of receivers are indeed important drivers of repeatability of song traits. Such a complementary approach will further advance our insights into the dynamics and evolution of animal signalling systems.

Differences in gut microbiota composition of laying hen lines divergently selected on feather pecking.

Feather pecking (FP), a damaging behavior where laying hens peck and pull at feathers of conspecifics, is multifactorial and has been linked to numerous behavioral and physiological characteristics. The gut microbiota has been shown to influence host behavior and physiology in many species, and could therefore affect the development of damaging behaviors, such as FP. Yet, it is unknown whether FP genotypes (high FP [HFP] and low FP [LFP] lines) or FP phenotypes (i.e., individuals differing in FP, feather peckers and neutrals) differ in their gut microbiota composition. Therefore, we identified mucosa-associated microbiota composition of the ileum and cecum at 10 and 30 wk of age. At 30 wk of age, we further identified luminal microbiota composition from combined content of the ileum, ceca, and colon. FP phenotypes could not be distinguished from each other in mucosa-associated or luminal microbiota composition. However, HFP neutrals were characterized by a higher relative abundance of genera of Clostridiales, but lower relative abundance of Lactobacillus for the luminal microbiota composition compared to LFP phenotypes. Furthermore, HFP neutrals had a higher diversity and evenness for the luminal microbiota compared to LFP phenotypes. FP genotypes could not be distinguished from each other in mucosa-associated microbiota composition. Yet, FP genotypes could be distinguished from each other in luminal microbiota composition. HFP birds were characterized by a higher relative abundance of genera of Clostridiales, but lower relative abundance of Staphylococcus and Lactobacillus compared to LFP birds. Furthermore, HFP birds had a higher diversity and evenness for both cecal mucosa-associated and luminal microbiota compared to LFP birds at adult age. In conclusion, we here show that divergent selection on FP can (in)directly affect luminal microbiota composition. Whether differences in microbiota composition are causal to FP or a consequence of FP remains to be elucidated.

Dog ownership satisfaction determinants in the owner-dog relationship and the dog's behaviour.

Dog ownership satisfaction relates to the quality of life of both owner and dog, and when seriously compromised may even lead to dog abandonment. Knowledge on determinants of dog ownership satisfaction is limited, obstructing solutions for promoting satisfaction, and here we quantified causes making dog owners less than very satisfied with their dog. We focused on the owner perceived relationship with the dog, unwanted dog behaviour, and dog obedience class attendance. The study population included only few seriously dissatisfied dog owners, preventing discrimination of multiple levels below 'very satisfied'. Consequently, existing relationships in the entire population may have been missed or underestimated and the findings apply specifically to dog owners that are relatively contented with dog ownership. Nine hundred seventy-seven Dutch dog owners completed an online questionnaire and we found the probability of being very satisfied to associate with all three subscales of the Monash Dog Owner Relationship Scale. Most strongly with perceived costs of ownership and less so with shared activities between owner and dog, and perceived emotional closeness to the dog. Aggression and/or disobedience related directly to high perceived ownership costs and to an increased probability of being less than very satisfied. Interaction effects indicated that dog disobedience was less influential on ownership satisfaction at high levels of aggression. Surprisingly, dog ownership satisfaction was unrelated to dog obedience class attendance, raising questions about the effectiveness of these classes in establishing satisfying dog-owner relationships. Training aids used during classes could play a role here, as choke chain use associated with high perceived costs and increased probabilities of being less then very satisfied with dog ownership. Ownership satisfaction in relatively contented dog owners, seems more influenced by unwanted dog behaviour and perceived costs of ownership, than by perceived emotional closeness to the dog, shared activities and dog obedience class attendance.

The existence of parenting styles in the owner-dog relationship.

Parents interact with children following specific styles, known to influence child development. These styles represent variations in the dimensions of demandingness and responsiveness, resulting in authoritarian, authoritative, permissive or uninvolved parenting. Given the similarities in the parent to child and owner to dog relationships, we determined the extent to which parenting styles exist in the owner to dog relationship using the existing Parenting Styles and Dimensions Questionnaire for the parent-child relationship and an adapted version for dog owners. Items on the parenting of children/dogs were rated for applicability on a five-point Likert scale by 518 Dutch dog owning parents. Principal Component Analyses grouped parenting propensities into styles, with some marked differences between the findings for children and dogs. Dog-directed items grouped into an authoritarian-correction orientated style, incorporating variation in demandingness and focussing on correcting a dog for behaviour verbally/physically, and in two styles based on authoritative items. An authoritative-intrinsic value orientated style reflected variation in mainly responsiveness and oriented on the assumed needs and emotions of the animal. A second authoritative-item based style, captured variations in demandingness and responsiveness. We labelled this style authoritative-training orientated, as it orientated on manners in teaching a dog how to behave in social situations. Thus, we defined dog-directed parenting styles and constructed a Dog-Directed Parenting Styles and Dimensions Questionnaire along the lines of the existing theoretical framework on parenting styles. We did not find a dog-directed parenting style of being permissive or uninvolved, which we attribute to a study population of devoted dog owners and our findings should be interpreted with this specific study population in mind. We found evidence of dog-directed parenting styles and provide a fundament for determining their possible impact on the different aspects of a dog's life.

Implications of nutritional stress as nestling or fledgling on subsequent attractiveness and fecundity in zebra finches (Taeniopygia guttata).

The conditions an organism experiences during early development can have profound and long lasting effects on its subsequent behavior, attractiveness, and life history decisions. Most previous studies have exposed individuals to different conditions throughout development until nutritional independence. Yet under natural conditions, individuals may experience limitations for much shorter periods due to transient environmental fluctuations. Here, we used zebra finches (Taeniopygia guttata) in captivity to determine if conditions experienced during distinctly different early developmental phases contribute differently to male and female attractiveness and subsequent reproduction. We conducted a breeding experiment in which offspring were exposed to food regimes with (a) low quality food provided only during the nestling period, (b) low quality food provided only during the fledgling period, or (c) high quality food throughout early development. We show that despite short-term effects on biometry and physiology, there were no effects on either male or female attractiveness, as tested in two-way mate choice free-flight aviary experiments. In a subsequent breeding experiment, the offspring from the initial experiment were allowed to breed themselves. The next generation offspring from mothers raised under lower quality nutrition as either nestling or fledging were lighter at hatching compared to offspring from mothers raised under higher quality nutrition whereas paternal early nutrition had no such effects. The lack of early developmental limitations on attractiveness suggests that attractiveness traits were not affected or that birds compensated for any such effects. Furthermore, maternal trans-generational effects of dietary restrictions emphasize the importance of role of limited periods of early developmental stress in the expression of environmentally determined fitness components.

Sex-specific responses to territorial intrusions in a communication network: Evidence from radio-tagged great tits.

Signals play a key role in the ecology and evolution of animal populations, influencing processes such as sexual selection and conflict resolution. In many species, sexually selected signals have a dual function: attracting mates and repelling rivals. Yet, to what extent males and females under natural conditions differentially respond to such signals remains poorly understood, due to a lack of field studies that simultaneously track both sexes. Using a novel spatial tracking system, we tested whether or not the spatial behavior of male and female great tits (Parus major) changes in relation to the vocal response of a territorial male neighbor to an intruder. We tracked the spatial behavior of male and female great tits (N = 44), 1 hr before and 1 hr after simulating territory intrusions, employing automatized Encounternet radio-tracking technology. We recorded the spatial and vocal response of the challenged males and quantified attraction and repulsion of neighboring males and females to the intrusion site. We additionally quantified the direct proximity network of the challenged male. The strength of a male's vocal response to an intruder induced sex-dependent movements in the neighborhood, via female attraction and male repulsion. Stronger vocal responders were older and in better body condition. The proximity networks of the male vocal responders, including the number of sex-dependent connections and average time spent with connections, however, did not change directly following the intrusion. The effects on neighbor movements suggest that the strength of a male's vocal response can provide relevant social information to both the males and the females in the neighborhood, resulting in both sexes adjusting their spatial behavior in contrasting ways, while the social proximity network remained stable. This study underlines the importance of "silent" eavesdroppers within communication networks for studying the dual functioning and evolution of sexually selected signals.

Regional level risk factors associated with the occurrence of African swine fever in West and East Africa.

BACKGROUND: African swine fever (ASF) causes severe socio-economic impacts due to high mortality and trade restrictions. Many risk factors of ASF have been identified at farm level. However, understanding the risk factors, especially wild suid hosts, determining ASF transmission at regional level remains limited. METHODS: Based on ASF outbreak data in domestic pigs during 2006-2014, we here tested, separately for West and East Africa, which risk factors were linked to ASF presence at a regional level, using generalized linear mixed models. RESULTS: Our results show that ASF infections in the preceding year was an important predictor for ASF presence in both West and East Africa. Both pig density and human density were positively associated with ASF presence in West Africa. In East Africa, ASF outbreaks in domestic pigs were also correlated with higher percentages of areas occupied by giant forest hogs and by high-tick-risk areas. CONCLUSIONS: Our results suggest that regional ASF risk in East Africa and in West Africa were associated with different sets of risk factors. Regional ASF risk in West Africa mainly followed the domestic cycle, whereas the sylvatic cycle may influence regional ASF risk in East Africa. With these findings, we contribute to the better understanding of the risk factors of ASF occurrence at regional scales that may aid the implementation of effective control measures.

Personality-dependent differences in problem-solving performance in a social context reflect foraging strategies.

Individuals develop innovative behaviours to solve foraging challenges in the face of changing environmental conditions. Little is known about how individuals differ in their tendency to solve problems and in their subsequent use of this solving behaviour in social contexts. Here we investigated whether individual variation in problem-solving performance could be explained by differences in the likelihood of solving the task, or if they reflect differences in foraging strategy. We tested this by studying the use of a novel foraging skill in groups of great tits (Parus major), consisting of three naive individuals with different personality, and one knowledgeable tutor. We presented them with multiple, identical foraging devices over eight trials. Though birds of different personality type did not differ in solving latency; fast and slow explorers showed a steeper increase over time in their solving rate, compared to intermediate explorers. Despite equal solving potential, personality influenced the subsequent use of the skill, as well as the pay-off received from solving. Thus, variation in the tendency to solve the task reflected differences in foraging strategy among individuals linked to their personality. These results emphasize the importance of considering the social context to fully understand the implications of learning novel skills.

Individual differences in personality in laying hens are related to learning a colour cue association.

Personality can influence how animals perceive and learn cues. The behaviour and physiological responses animals show during stressful events is indicative of their personality. Acute induced stress prior to a cognitive test are known to affect the judgement of a stimulus, but personality of an individual could also affect learning of a specific cognitive paradigm. Here, we assessed if adult laying hens' behaviour and physiological responses, as indicators of their personality, were related to their cognitive performance. We assessed their behavioural responses to a tonic immobility test, an open field test, and a manual restraint test, and measured plasma corticosterone levels after manual restraint. After that, hens (n=20) were trained in a pre-set training schedule to associate a colour-cue with a reward. In a two-choice go-go test, hens needed to choose between a baited or non-baited food container displayed randomly on the left or right side of an arena. Success in learning was related to personality, with better performance of hens which showed a reactive personality type by a long latency to walk, struggle or vocalize during the tests. Only eight out of 20 hens reached the training criteria. The non-learners showed a strong side preference during all training days. Side preferences were strong in hens with high levels of plasma corticosterone and with a long duration of tonic immobility, indicating that fearful, stress-sensitive hens are more prone to develop side biases. Our results show that learning can be hindered by side biases, and fearful animals with a more proactive personality type are more sensitive to develop such biases.

Female signalling to male song in the domestic canary, Serinus canaria.

Most studies on sexual selection focus on male characteristics such as male song in songbirds. Yet female vocalizations in songbirds are growing in interest among behavioural and evolutionary biologists because these vocalizations can reveal the female's preferences for male traits and may affect male display. This study was designed to test whether male song performance influences the different female signals in the domestic canary (Serinus canaria). Female canaries were exposed to three types of song performance, differing in the repetition rate of sexy syllables. This experiment demonstrates that female birds are engaged in multimodal communication during sexual interaction. The results support the copulation solicitation hypothesis for female-specific trills: these trills were positively correlated and had a similar pattern to the copulation solicitation displays; responses were higher to the songs with higher performance and responses decreased with the repetition of the stimulation. Also, we observed a sensitization effect with the repetition of the song of the highest performance for the simple calls. Simple trills and other calls were more frequent during the broadcast of canary songs compared with the heterospecific control songs. The differential use of female signals in response to different song performance reveals a highly differentiated female signalling system which is discussed in light of the role of female traits to understand sexual selection in a broader perspective.