Prolactin mediates behavioural rejection responses to avian brood parasitism

Adaptations resulting from co-evolutionary interactions between avian brood parasites and their hosts have been extensively studied, yet the physiological mechanisms underlying antiparasitic host defences remain little known. Prolactin, one of the main hormones involved in the regulation of avian parental behaviour, might play a key role in the orchestration of the host responses to avian brood parasitism. Given the positive association between prolactin and parental behaviour during incubation, decreasing prolactin levels are expected to facilitate egg-rejection decisions. We tested this prediction by implanting Eurasian blackbird (Turdus merula) females with an inhibitor of prolactin secretion, bromocriptine mesylate, to experimentally decrease their plasma prolactin levels. Bromocriptine-implanted individuals ejected mimetic model eggs at higher rates, and showed shorter latency to egg ejection, than placebo-treated birds. To our knowledge, this is the first experimental evidence that behavioural host defences against avian brood parasitism are mediated by prolactin.

Discrimination and ejection of eggs and nestlings by the fan-tailed gerygone from New Caledonia

Nestling ejection is a rare type of host defence against brood parasitism compared to egg ejection. Theoretically, host defences at both egg and nestling stages could be based on similar underlying discrimination mechanisms but, due to the rarity of nestling ejector hosts, few studies have actually tested this hypothesis. We investigated egg and nestling discrimination by the fan-tailed gerygone Gerygone flavolateralis, a host that seemingly accepts non-mimetic eggs of its parasite, the shining bronze-cuckoo Chalcites lucidus, but ejects mimetic parasite nestlings. We introduced artificial eggs or nestlings and foreign gerygone nestlings in gerygone nests and compared begging calls of parasite and host nestlings. We found that the gerygone ejected artificial eggs only if their size was smaller than the parasite or host eggs. Ejection of artificial nestlings did not depend on whether their colour matched that of the brood. The frequency of ejection increased during the course of the breeding season mirroring the increase in ejection frequency of parasite nestlings by the host. Cross-fostered gerygone nestlings were frequently ejected when lacking natal down and when introduced in the nest before hatching of the foster brood, but only occasionally when they did not match the colour of the foster brood. Begging calls differed significantly between parasite and host nestlings throughout the nestling period. Our results suggest that the fan-tailed gerygone accepts eggs within the size range of gerygone or cuckoo eggs and that nestling discrimination is based on auditory and visual cues other than skin colour. This highlights the importance of using a combined approach to study discrimination mechanisms of hosts.

An Experimental Test of Defenses Against Avian Brood Parasitism in a Recent Host

Theoretical studies predict that hosts of avian brood parasites should evolve defenses against parasitism in a matter of decades. However, opportunities to test these predictions are limited because brood parasites rarely switch to naïve hosts. Here, we capitalize on a recent host switch by the brood-parasitic Pacific Koel (Eudynamys orientalis) in eastern Australia, to investigate how quickly the Red Wattlebird (Anthochaera carunculata), a recent host that has been annexed by the koel within the last 90 years, can learn to recognize and mob adult cuckoos and evolve the ability to eject parasite eggs. Pacific Koel nestlings kill all host young, so there should be strong selection for hosts to evolve defenses. However, low parasitism rates and high egg recognition costs might slow the spread of egg ejection in our study populations, while adult parasite recognition should be able to spread more rapidly, as this defense has been shown to be a learned trait rather than a genetically inherited defense. We tested Red Wattlebirds at two sites where parasitism rate differed. As predicted, we found that the Red Wattlebird showed little or no ability to eject foreign model eggs at either site, whereas two historical hosts showed high levels of egg ejection at both sites. However, Red Wattlebirds responded significantly more aggressively to a koel mount than to mounts of a harmless control and nest predator at the site with the higher parasitism rate and gave significantly more alarm calls overall toward the koel mount. Our results support previous evidence that recognition and mobbing of a brood parasite are learned traits and may be especially beneficial to naïve hosts that have not had enough time or a high enough selection pressure to evolve egg rejection.

Daurian redstart Phoenicurus auroreus is a host for the common cuckoo Cuculus canorus during the second, but not the first cultch

Background: Coevolution in cavity-nesting host-cuckoo systems may differ from those in open-nesting hosts due to unique conditions in cavity nests. We investigated brood parasitism in Daurian redstarts ( Phoenicurus auroreus ), a regular cavity-nesting host of common cuckoos ( Cuculus canorus ).Results: A total of 15.6% ( n =358) of host nests were parasitized by cuckoos. Cuckoos were highly successful in parasitizing Daurian redstart nests: nearly all cuckoo eggs were laid in the nest cup, and all cuckoo chicks evicted all host offspring. However, egg ejection by Daurian redstarts was egg morph specific, i.e. hosts laying white eggs ejected most real cuckoo eggs, while hosts laying blue eggs did not eject any. In contrast, hosts ejected most mimetic cuckoo eggs. Moreover, most Daurian redstarts moved to nearby villages during the second breeding attempts, where the risk of cuckoo parasitism was reduced. Parasitism only occurred during the second breeding attempt, since cuckoos had not yet arrived at the breeding grounds when hosts started to lay their first clutches, which may indicate a novel and unique anti-parasite defense, advancing breeding time of hosts.Conclusions: Our results suggest that Daurian redstarts suffer from high risk of cuckoo parasitism showing more intense egg ejection while building nests closer to human habitation in the second clutch. This suggests that cavity-nesting hosts may show adaptations to brood parasites that differ from those of open-nesting hosts.

Differently sized cuckoos pose different threats to hosts

Hole-nesting tits Parus spp. have been classified as “unsuitable” hosts for cuckoo parasitism because cuckoos cannot enter a cavity if the entrance is too small. However, Chinese tits could reject alien eggs and egg ejection rate increased with the local diversity of parasitic cuckoo species. Antiparasitic behavior among Chinese tits may have evolved due to greater size variation among sympatric cuckoo species. This raises the question of whether differently sized parasitic cuckoos pose different threats to Chinese tits. A green-backed tit Parus monticolus population that is sympatric with Asian emerald cuckoo Chrysococcyx maculatus (eme-cuckoo, small-sized parasite) and common cuckoo Cuculus canorus (com-cuckoo, large-sized parasite), and a cinereous tit P. cinereus population that is only sympatric with com-cuckoo were chosen as study organisms. We observed behavioral response and recorded alarm calls of the 2 tit species to eme-cuckoo, com-cuckoo, chipmunk Tamias sibiricus (a nest predator) and dove Streptopelia orientalis (a harmless control), and subsequently played back alarm calls to conspecific incubating females. In dummy experiments, both tit species performed intense response behavior to chipmunk, but rarely responded strongly to the 3 avian species. In playback experiments, both tit species responded strongly to conspecific chipmunk alarm calls, but rarely responded to dove alarm calls. The intensity of response of incubating female green-backed tits to eme-cuckoo and com-cuckoo alarm calls were similar to that of chipmunk alarm calls, while the intensity to eme-cuckoo alarm calls was higher than the intensity to dove alarm calls which was similar to that of com-cuckoo alarm calls. In contrast, few female cinereous tits responded to eme-cuckoo and com-cuckoo alarm calls. These findings indicated that the threat level of eme-cuckoo was slightly greater than that of com-cuckoo for sympatric green-backed tits, but not for allopatric cinereous tits.