Marc Naguib

The evolution of animal communication

Communication is a central part of social behaviour, often directly affect-ing an individual’s fitness. As such, the study of animal communication hasbecome a central focus of animal behaviour researchers. It is a field that inte-grates a broad and diverse range of biological disciplines, from neurobiologyand biomechanics to evolution and psychology, and over the years it has at-tracted a broad range of researchers as well. The contributors to this SpecialIssue of

Nestling immunocompetence and testosterone covary with brood size in a songbird.

The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross–fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell–mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.

Maternal developmental stress reduces reproductive success of female offspring in zebra finches

Environmental factors play a key role in the expression of phenotypic traits and life-history decisions, specifically when they act during early development. In birds, brood size is a main environmental factor affecting development. Experimental manipulation of brood sizes can result in reduced offspring condition, indicating that developmental deficits in enlarged broods have consequences within the affected generation. Yet, it is unclear whether stress during early development can have fitness consequences projecting into the next generation. To study such trans-generational fitness effects, we bred female zebra finches, Taeniopygia guttata, whose mothers had been raised in different experimental brood sizes. We found that adult females were increasingly smaller with increasing experimental brood size in which their mother had been raised. Furthermore, reproductive success at hatching and fledging covaried negatively with the experimental brood size in which their mothers were raised. These results illustrate that early developmental stress can have long-lasting effects affecting reproductive success of future generations. Such trans-generational effects can be life-history responses adapted to environmental conditions experienced early in life.

Nocturnal and diurnal singing activity in the nightingale: correlations with mating status and breeding cycle

This study on the nightingale, Luscinia megarhynchos, is the first to examine both nocturnal and diurnal singing activity of mated and unmated males throughout a species’ entire breeding cycle. Nocturnal song was sung mostly by unmated males. After pair formation, males ceased nocturnal singing and resumed it if their mate deserted. These results strongly suggest that nocturnal song of unmated males functions to attract a mate. Diurnal singing activity before females settled was low and did not predict future mating status. However, unmated males showed a continuous increase in diurnal singing activity until the end of the breeding cycle, but diurnal singing activity of mated males decreased after the egg-laying period. Mated males resumed nocturnal song for, on average, 3 nights during egg laying by their mates. This second period of nocturnal song coincided with the peak of diurnal singing activity. Such a high male singing effort during egg laying might allow the female to adjust her reproductive effort to male quality, deter rival males (e.g. through honest announcement of the female’s fertility) or attract females for extrapair copulations.

Personality affects learning performance in difficult tasks in a sex-dependent way

Animals constantly need to cope with changes in their environment. Coping with changes in cues that are associated with the location and abundance of food is essential for being able to adjust behaviourally to a variable environment. The use of cues in decision making requires appropriate levels of attention and learning ability, which may be affected by the personality of an individual. The relationship between personality, attention and learning as essential mechanisms for behavioural adaptation, however, is not well understood. We studied the relationship between attention to environmental cues, behavioural flexibility in learning and exploratory behaviour, a proxy for personality, in great tits, Parus major. We used a dimensional shift learning paradigm; a learning task involving several stages differing in complexity and requiring attention to changes in relevant cues. The results show personality differences in performance in learning flexibility in only the apparently most difficult stage, yet in opposite directions for males and females. Fast-exploring males showed more flexible learning abilities than slow males, whereas in females slow explorers outperformed fast explorers. These context-dependent and sex-specific personality effects reveal behavioural and cognitive mechanisms that may underlie observed sex- and personality-dependent fitness differences in natural populations.

Chapter 1 Environmental Acoustics and the Evolution of Bird Song

Abstract Any signal must get from a sender to a receiver if information is to be transmitted. In the case of bird song, the acoustic properties of the habitat may hinder this being achieved. However, birds as senders and receivers have evolved numerous adaptations to overcome the problem of getting the message across. In this chapter, we explore habitat-dependent patterns of sound transmission, the effects of noise, signal perception, and signal interpretation such as auditory distance assessment with a specific focus on the solutions that selection has generated. We argue that along with other possible selective forces, such as sexual selection, the combination of environmental constraints on signal transmission, noise levels, and the use of signal degradation as a distance cue need mutual consideration to gain a more thorough understanding of the astounding variety of avian song and the many different ways in which birds use it.

Transgenerational effects on body size caused by early developmental stress in zebra finches.

The nutritional and social conditions that individuals experience during early development can have profound effects on their morphology, physiology, behaviour and life history. Experimental increases in brood size in birds can result in reduced offspring condition and survival, indicating that developmental deficits in enlarged broods have negative fitness consequences within the affected generation. To study long-term effects (i.e. transgenerational effects of developmental stress), we conducted a two-step breeding experiment in which we manipulated early developmental conditions in zebra finches Taeniopygia guttata. We raised zebra finches by manipulating brood sizes and controlled for maternal and genetic effects by cross-fostering. In a previous study, we showed that offspring condition and body size decreased with increasing brood size. Here we show that this effect was carried over to the next generation. Body size in nestlings and at nutritional independence was affected by the brood size in which the mothers were raised. Female offspring did significantly worse than male offspring when the mother had been raised in large broods, suggesting sex-specific influences of maternal effects. These findings directly link early developmental stress in females via maternal effects to the phenotype of the next generation.

Early Fasting Is Long Lasting: Differences in Early Nutritional Conditions Reappear under Stressful Conditions in Adult Female Zebra Finches

Conditions experienced during early life can have profound effects on individual development and condition in adulthood. Differences in nutritional provisioning in birds during the first month of life can lead to differences in growth, reproductive success and survival. Yet, under natural conditions shorter periods of nutritional stress will be more prevalent. Individuals may respond differently, depending on the period of development during which nutritional stress was experienced. Such differences may surface specifically when poor environmental conditions challenge individuals again as adults. Here, we investigated long term consequences of differences in nutritional conditions experienced during different periods of early development by female zebra finches (Taeniopygia guttata) on measures of management and acquisition of body reserves. As nestlings or fledglings, subjects were raised under different nutritional conditions, a low or high quality diet. After subjects reached sexual maturity, we measured their sensitivity to periods of food restriction, their exploration and foraging behaviour as well as adult resting metabolic rate (RMR). During a short period of food restriction, subjects from the poor nutritional conditions had a higher body mass loss than those raised under qualitatively superior nutritional conditions. Moreover, subjects that were raised under poor nutritional conditions were faster to engage in exploratory and foraging behaviour. But RMR did not differ among treatments. These results reveal that early nutritional conditions affect adult exploratory behaviour, a representative personality trait, foraging and adults physiological condition. As early nutritional conditions are reflected in adult phenotypic plasticity specifically when stressful situations reappear, the results suggest that costs for poor developmental conditions are paid when environmental conditions deteriorate.

Non-territorial nightingales prospect territories during the dawn chorus.

Male songbirds usually sing when they have occupied a territory, but the territory prospecting of non–territorial males is more elusive and has been rarely studied. Here, we simulated newly arriving, non–territorial males by translocating unmated male nightingales (Luscinia megarhynchos) to our study site. We show that territory prospecting of translocated males was largely confined to the hour before sunrise. The radio–tagged males made extensive excursions visiting several singing males at dawn, but after dawn they remained stationary outside occupied territories. As in many other songbird species, dawn was also the time when resident males sang the most. These results suggest that non–territorial male nightingales use the dawn chorus to assess singing residents or territory occupancy. For resident males, dawn singing may be important to announce territory occupancy to prospecting males and may thus play a role in territory maintenance.

Vocal interactions in nightingales, Luscinia megarhynchos: more aggressive males have higher pairing success

Song overlapping in birds is used and perceived as a signal of aggression, and evidence suggests that eavesdropping females base their extrapair mating decisions on the performance of males in vocal contests. In our study population of nightingales a large proportion of territorial males remain unpaired throughout the breeding season. A comparison between subsequently mated males and unpaired males may reveal whether females could use singing performance during vocal interactions in their choice of a social mate. We investigated how males that differed in their subsequent pairing status overlapped a noninteractive playback during the period of mate attraction, and how males used specific structural song components in response to playback. Subsequently mated males overlapped more playback songs than did males that remained unpaired throughout the breeding season. Males also adjusted the use of specific song components and decreased song rate during playback, suggesting that the flexible use of structural song components is more important in vocal contests than increasing song output. Because song overlapping is thought to be a signal of aggression, more aggressive males seem to have greater pairing success.