Gut microbiota in a host–brood parasite system: insights from common cuckoos raised by two warbler species

ABSTRACT An animal's gut microbiota (GM) is shaped by a range of environmental factors affecting the bacterial sources invading the host. At the same time, animal hosts are equipped with intrinsic mechanisms enabling regulation of GM. However, there is limited knowledge on the relative importance of these forces. To assess the significance of host-intrinsic vs environmental factors, we studied GM in nestlings of an obligate brood parasite, the common cuckoo (Cuculus canorus), raised by two foster species, great reed warblers (Acrocephalus arundinaceus) and Eurasian reed warblers (A. scirpaceus), and compared these with GM of the fosterers’ own nestlings. We show that fecal GM varied between cuckoo and warbler nestlings when accounting for the effect of foster/parent species, highlighting the importance of host-intrinsic regulatory mechanisms. In addition to feces, cuckoos also expel a deterrent secretion, which provides protection against olfactory predators. We observed an increased abundance of bacterial genera capable of producing repulsive volatile molecules in the deterrent secretion. Consequently, our results support the hypothesis that microbiota play a role in this antipredator mechanism. Interestingly, fosterer/parent identity affected only cuckoo deterrent secretion and warbler feces microbiota, but not that of cuckoo feces, suggesting a strong selection of bacterial strains in the GM by cuckoo nestlings.

Fast and furious: host aggression modulates behaviour of brood parasites

ABSTRACTAvian brood parasites pose a serious threat for hosts, substantially reducing their fitness which selects for the evolution of host defences. A classic example of a host frontline defence is mobbing which frequently includes contact attacking of brood parasites. Here, we investigated how the nest defence of a very aggressive great reed warbler (Acrocephalus arundinaceus) host influences the speed of egg-laying and egg-removing behaviour of its brood parasite – the common cuckoo (Cuculus canorus). We video-recorded 168 brood parasitic events at 102 active host nests and found that cuckoos avoided host mobbing in only 62% of cases. If hosts spotted the cuckoo at their nests, they almost always attacked it (in 91 of 104 cases), however, such attacks only rarely and temporarily prevented cuckoos from parasitizing (11 additional cases). When attacked, cuckoos parasitized host nests significantly faster and left them immediately. However, when not attacked, cuckoos frequently stayed at or near the nest suggesting that host aggression, rather than the risk of being spotted, influences the speed of brood parasitism in this species. Further, we found that cuckoos performed egg-removing behaviour in all parasitic events without regard to host aggression. As a result, cuckoos removed at least one egg during all brood parasitism events except those when an egg slipped from their beaks and fell back into the nest (in 9 of 73 cases). This indicates that egg-removing behaviour is not costly for the common cuckoo and is an essential part of its parasitism strategy, widening understanding of this currently unexplained behaviour.

Complete sporogony of the blood parasite Haemoproteus nucleocondensus in common biting midges: why is its transmission interrupted in Europe?

Haemoproteus species (Haemoproteidae) are widespread blood parasites and are transmitted by Culicoides biting midges and Hippoboscidae louse flies. Although these pathogens may cause morbidity or mortality, the vectors and patterns of transmission remain unknown for the great majority of avian haemoproteids. Haemoproteus nucleocondensus has been frequently reported in Europe in great reed warblers Acrocephalus arundinaceus after their arrival from African wintering grounds, but this infection has not been found in juveniles at the breeding sites. The factors that prevent its transmission remain unclear. This study was designed to test whether the sporogony of H. nucleocondensus (lineage hGRW8) can be completed in Culicoides impunctatus, one of the most abundant European biting midge species. Wild-caught females were infected with H. nucleocondensus from great reed warblers. Microscopic examination and PCR-based methods were used to detect sporogonic stages and to confirm species identity. This study showed that H. nucleocondensus completes sporogony in C. impunctatus, suggesting that there are no obstacles to its transmission from the point of view of vector availability and average temperature in Northern Europe. We discuss other ecological factors which should be considered to explain why the transmission of H. nucleocondensus and some other Southern origin haemosporidians are interrupted in North Europe.