Bo Terning Hansen

Mate choice and imprinting in birds studied by cross-fostering in the wild

Sexual–selection theories generally assume that mating preferences are heritable traits. However, there is substantial evidence that the rearing environment may be important for the development of mating preferences, indicating that they may be learnt, or modified by experience. The relative importance of such sexual imprinting across species remains largely unexplored. Here, we report results of a large–scale cross–fostering experiment in the wild in which nestling birds were raised by parents of a different species. We show that resulting sexual imprinting may have a negative effect on pairing success in one species (the great tit, Parus major), but not in two other species (the blue tit, P. caeruleus and the pied flycatcher, Ficedula hypoleuca). A remarkable variation thus seems to exist, even between species that are congeneric and have similar breeding ecologies. The cross–fostering resulted in heterospecific pairings between the two tit species (female blue tit breeding with male great tit), which has never, to our knowledge, been previously documented. However, the chicks fledging from these nests were all blue tit.

Sexual Imprinting and the Origin of Obligate Brood Parasitism in Birds

We discuss two pathways along which obligate brood parasitism (OBP) may evolve and examine some of the critical steps that must be passed by letting great tits Parus major be reared by blue tits Parus caeruleus in a field experiment. The cross‐fostered chicks survived well in blue tit nests, but their local recruitment and reproductive success was much lower than that of controls. The effect was strongest when great tits grew up with siblings of the host species rather than with conspecific siblings in blue tit nests. The low success seemed to be caused by misimprinting because the cross‐fostered birds behaved like blue tits in several aspects (species association, alarm calls, and aggressive response by resident females to caged intruders). Some birds of both sexes were apparently so strongly imprinted that they did not attract or accept a social mate of their own species. We conclude that imprinting may be necessary for OBP to evolve in birds because the parasite must be attracted to the nests of the host species to add eggs and thereby continue the parasitic life cycle. However, strong imprinting may also prevent OBP from occurring if parasitic offspring seek a mate from the host species.

Imprinted species recognition lasts for life in free-living great tits and blue tits

Species recognition may be learned through imprinting early in life. Imprinting has normally been studied under highly unnatural conditions in the laboratory. We tested whether species recognition mediated through imprinting is individually modifiable in a field setting where great tits, Parus major, have been artificially cross-fostered to blue tits, Cyanistes caeruleus, and vice versa. We have shown previously that cross-fostered birds have deviant species recognition, in terms of both mate choice and aggressive responses towards rivals. Natural interactions among conspecifics and heterospecifics are common in these populations, potentially giving cross-fostered birds scope for relearning their species identity. We tested whether species recognition may change with experience during adulthood by comparing the aggressive response of cross-fostered birds and controls of different ages towards caged intruders. When breeding, cross-fostered birds responded aggressively towards same-sex individuals of their heterospecific foster species, while unmanipulated controls responded mainly towards conspecifics. We found that the aggressive response decreased with age at similar rates in both treatments and in both species. Moreover, there was no effect of age on the relative response towards conspecifics and heterospecifics in either treatment. Hence, we found no evidence that the species recognition behaviour towards same-sex individuals is shifted towards conspecifics with age in interspecifically cross-fostered birds. We conclude that species recognition is irreversible once it has been established in free-living great tits and blue tits. This is the first study to investigate the stability of species recognition in the field.

Predators use environmental cues to discriminate between prey

The cognitive processes of predators play a central role in the evolution of prey characters. Numerous studies have shown that vertebrate predators may learn to associate the characteristics of prey (e.g. color) with the cost or benefit of ingesting them, thus forming preferences and aversions for different kinds of prey. Although the distribution and quality of prey types can differ between environmental contexts, which may make it profitable to attack a prey type in some contexts but not in others, the influence of environmental cues in decisions to attack has rarely been addressed. Recent theory suggests that modification of prey preferences by environmental cues such as microhabitat or temperature may influence the evolution of prey characteristics. Here, we show that the environmental foraging context may determine prey choice in great tits (Parus major) through learned association between the prey phenotype (appearance and palatability) and a contextual background cue. The same individuals were able to learn and maintain two different sets of food preferences and aversions for use in two different environmental contexts (aviaries with red or blue wooden boards), indicating a role for contextual learning in vertebrate foraging behavior.

Interspecific cross-fostering affects mate guarding behaviour in great tits (Parus major)

Mate guarding is thought to decrease the likelihood of cuckoldry and, hence, increase the fitness of guarding males. Mate guarding is costly for males and must be traded off with other fitness-enhancing behaviours. Over several years, we have cross-fostered great tits ( Parus major ) to blue tits ( Cyanistes caeruleus ) and this experimental treatment has influenced the mate and rival recognition of cross-fostered birds. Here we show that cross-fostered great tit males mate guard their females less than do control great tits, regardless of whether the cross-fostered males were mated to great tit females or cross-fostered blue tit females. Cross-fostered great tit males sang more and interacted more frequently with blue tit males than did controls. Females paired to males of the two groups did not differ in the extent to which they initiated movements away from their mates. We conclude that the altered species-assortative behaviour resulting from interspecific cross-fostering influences mate guarding in great tit males, probably by cross-fostered males increasing investment in territorial behaviour at the expense of mate guarding, and/or by cross-fostered males mate guarding less due to a reduced affinity for their female. Such trade-offs may have a general significance for mate guarding species.

No cultural transmission of species recognition between parents and offspring in free-living great tits and blue tits

Imprinting plays a key role in the development of species recognition, with young imprinting upon the morphological characters of their parents. However, the potential role that cultural transmission might play in species recognition remains largely uninvestigated. Great tits (Parus major) and blue tits (Cyanistes caeruleus) do not normally perceive each other as sexual competitors or potential partners. However, after reciprocal interspecific cross-fostering, both species may perceive individuals of the foster species as potential rivals or mates. Although the experience of being raised by heterospecifics clearly has affected the species recognition of cross-fostered birds, some of them breed naturally with conspecifics. The offspring of such cross-fostered birds (OCF) are hence raised by parents that look like ordinary conspecifics but display deviant species recognition as compared to controls in terms of aggressive response towards rivals. Comparing the aggressive behavior of OCF, cross-fostered birds and controls towards territorial intruders may thus help tease apart the influence of morphological vs behavioral cues of parents in the development of offspring species recognition. To this end, we compared birds from all three treatments with respect to their aggressive response to territorial intruders of both species during the breeding season. OCF and controls did not differ in their pattern of response towards heterospecific and conspecific stimuli. Compared to cross-fostered birds, OCF and controls showed less aggression towards heterospecific intruders, while the response towards conspecific intruders did not differ between treatments. These results demonstrate that both tit species imprint on the morphological characters of their parents, but that parental behavior is not important for the development of species recognition in terms of aggressive response towards territorial intruders.

Interspecific cross-fostering of great tits (Parus major) by blue tits (Cyanistes caeruleus) affects inter- and intraspecific communication

Summary Bird song is used to attract mates and deter rivals, and also functions as a species recognition cue. It is a flexible trait affected by learning, hence the choice of song tutors may affect an individuals’ singing. By interspecifically cross-fostering great tits (Parus major) to blue tits (Cyanistes caeruleus) in the wild, we have manipulated the species recognition of great tits, which in turn has influenced their song. In the present study, we presented breeding great tit and blue tit control males with playback of the aberrant song of cross-fostered great tit males and playback of the normal song of control great tit males. Blue tit males responded more to cross-fostered than control great tit song while great tit males showed the inverse response pattern. This shows that interspecific cross-fostering may affect both inter- and intraspecific communication. However, the response of males of both species towards the song of crossfostered great tit males was not of the same magnitude as the response towards ordinary blue tit song; thus, the real species identity is to some extent maintained in the aberrant song of cross-fostered males.