The pair coordination in provisioning behaviour of a group-living bird, the vinous-throated parrotbill (Sinosuthora webbiana)

Abstract

조류를 포함한 동물들에서 번식 쌍 사이에 협력적 관계는 흔히 발생한다. 특히 사회성이 강한 조류에서 번식 쌍과 그룹의 다른 구성원간의 상호작용이 부모의 협력적 관계에 영향을 미치는지에 관한 연구가 거의 시행되지 않았다. 본 논문은 참새목 조류인 붉은머리오목눈이의 번식기 동안 부모의 협력적 관계가 어떤 요인에 의해 발생하는지 조사했으며, 이에 대한 메커니즘에 관한 연구에 초점을 맞추었다. 본 종의 연구는 집단생활을 하는 동물의 연구 모델로 이용할 수 있을 것으로 기대된다. 이전 연구에서 붉은머리오목눈이는 구성원 사이에서 복잡한 사회적 관계를 지속적으로 유지하는 것으로 밝혀졌다. 부모의 새끼 양육 동안 지속적인 협력적 관계에 의해서 유지될 수 있는 번식 쌍의 동시 둥지 방문에 관한 주제를 각 장에서 토론하였다. 부모들은 새끼 양육에 필요한 먹이를 구하기 위해 암수가 함께 취식 활동을 하며 둥지에 동시에 함께 방문한다. 암수의 둥지 동시방문 행동의 원인에 대해 제 2장에서 여러 가능한 가설과 예견을 토대로 검토했다. 붉은머리오목눈이 부모 암수는 동시에 둥지를 방문하는 비율이 매우 높았으며, 이런 행동은 계절에 따라 변하는 둥지의 밀도에 따라 유동적인 것으로 나타났다. 동시 방문의 빈도는 번식(둥지) 밀도가 증가함에 따라 감소하였으며, 반대로 번식 밀도가 낮은 지역에서 동시방문 빈도는 증가하였다. 부모의 조화로운 협력 과정이 필요한 암수의 둥지 동시 방문은 동지 인근에 위치한 다른 사회적 멤버들간의 사회적 상호작용의 증가로 인해 감소할 수 있다는 가설을 제시하였다. 또한 새끼에게 먹이 급여 효율성은 단독 혹은 낮은 밀도에서 증가 했으나 높은 밀도에서는 감소하였다. 부모의 번식쌍 사이의 협력적 관계가 부모의 연령이나 둥지 주변의 사회구성원의 관계에 어떻게 달라지는지에 대해 제 3장에서 토론했다. 부모들은 단독생활을 할 때 동시 방문의 빈도가 나이든 부모번식쌍에서 가장 높았으며, 1년생 부모에서는 가장 낮게 나타났다. 그러나 밀도가 높아졌을 때 부모의 나이에 상관없이 전반적으로 낮게 나타났다. 또한 동시에 함께 번식한 이웃들이 함께 번식할 때 동시 둥지 방문 비율이 떨어지지 않았지만 비 동시에 번식한 이웃이 많았을 때는 크게 감소했다. 부모는 새롭게 유입된 번식 쌍이 많아질수록 조화로운 암수 간의 협력적 행동이 방해 받을 가능성을 높아진다는 결과를 제시하였다. 제 4장에서는 두 부모의 지속적인 동시 둥지 방문을 위한 메커니즘에 대해 토론했다. 부모가 먹이 제공의 피크 기간 동안 둥지에서 오랜 시간 머무르는 것은 일시적으로 부모가 분리되었을 때 둥지에서 파트너를 기다리는 행동일 가능성이 있다는 가설을 제시하였다. 또한 동시 도착 동안 먼저 급여하는 개체와 나중에 급여하는 개체간의 먹이 양과 먹이효율성을 비교한 결과 먼저 먹인 개체는 암수에 상관없이 더 큰 먹이를 가져왔으며, 먹이 효율성도 높았다. 이것은 번식 쌍이나 개체의 특성에 보다 도착 순서에 의해 부모의 급이 먹이양에 차이가 나며, 더 성공적인 개체가 리더로서 일찍 도착하며 다른 파트너가 뒤따를 가능성이 높다는 것을 의미한다. 붉은머리오목눈이 부모는 육추기 동안 높은 수준의 협력적 관계를 유지했으며, 부모의 나이와 같은 개체의 특성과 번식 밀도와 같은 사회적 환경에 의해 영향을 받을 수 있다는 것을 본 연구를 통해 밝혀졌다. 또한 부모의 조화로운 협력관계는 번식 쌍의 성공적인 양육을 위한 매우 중요한 요인이라는 것을 논문에서 제시하였다.

Behavioural coordination and synchronization in animals are common within breeding pairs as well as among group members. One of the less studied aspects in this field is the effect of interactions between breeding pairs and group members on the degree of coordination and synchronization within a breeding pair. Birds have been convenient subjects for the study of these phenomena. In this thesis, I investigate multiple aspects of synchronization and behavioural coordination of brood provisioning in a small passerine bird, the vinous-throated parrotbill Sinosuthora webbiana. This species can be used as a research model of a social, group-living animal in the natural habitat. Previous studies have suggested that vinous-throated parrotbills form social groups with complicated and long-lasting relationships among members. However, relatively few studies have been conducted on the links between social aspects of their biology and synchronization or coordination within a breeding pair in the breeding season. Therefore, in the three chapters (2, 3, 4) I focus on several aspects of behavioural synchrony and pair coordination during brood provisioning by the vinous-throated parrotbill. Chapter 2 explored several mutually nonexclusive hypotheses that may explain synchronous nest vist. Parents may coordinate the timing of nest visits, thus decreasing the overall frequency of activity at the nest, in order to lower the risk of nest detection by predators. Parents may also simply move together for their own safety, or because foraging together increases foraging efficiency. In species that maintain social groups during the breeding season, the interactions with group members may affect the synchronization of parental visits to the nest. If other group members provide safety from predators, synchronous nest visit may not be needed for nest or parents survival. If other group members help in finding food, then their presence increases foraging efficiency of a pair, and may therefore indirectly affect the degree of synchronous nest visits, especially if synchrony is caused by increase in foraging efficiency. Finally, presence of group members may cause many social interactions, which may disrupt normal nest provisioning pattern and decrease the synchrony of nest visits. Using observational evidence, I evaluated those hypotheses. I found that parents frequently synchronize provisioning visits (on average 66.7% of visits in each pair). Higher synchrony was not associated with higher nest survival, and higher local nest predation rate did not affect the level of synchrony of a pair. These results are inconsistent with the hypothesis that the function of synchrony is to avoid nest predation. Although at the population level, the average foraging efficiency of synchronous nest visits was not higher than that of asynchronous nest visits, the pairs increased the degree of synchrony in situations where the foraging efficiency associated with synchronous nest visits was higher than with asynchronous nest visits, but only at low local nest densities. This is consistent with the idea that at lower nest densities, when social interactions (e.g. mate-guarding) presumably do not strongly affect within-pair dynamics, parental synchrony helps in foraging. The level of synchrony was lower at nests with higher local nest density, and vice versa, and the pairs with multiple breeding attempts decreased their level of synchrony in response to increased nesting density over time. This is consistent with the idea that pairs may synchronize their visits to increase their foraging efficiency and/or their own safety, and that the presence of other group members either disrupts the synchrony through social interactions or because they provide alternative safety, so breeding pairs no longer need to synchronize their behaviour. However, longer inter-visit intervals in higher densities suggest that social disruption (e.g. mating guarding or competition over nest site) is a more likely explanation than the decreased perceived predation risk to adults. In conclusion, chapter 2 shows that parental coordination in group-living species is an outcome of within-pair mechanisms modified by social interactions with the group members. The degree of coordination and synchronization of parents may decrease as nest density and thus interactions with neighbour increase. However, these effects may vary depending on the age and age-related experiences of a focal pair, and the breeding stages of other group members and neighbouring pairs (i.e. whether they are in the similar breeding stage with the focal pair or not). Hence, not only the local nest density, but also the breeding timing of the neighbouring pairs may affect the level of synchronous nest visit of a focal pair. Therefore, in chapter 3, I further investigated how provisioning rate, proportion of synchronous nest visit vary according to parental age, local nest density, and the proportion of neighbouring pairs that breed simultaneously or asynchronously with the focal pair. I found that older parents showed a higher level of synchronous nest visit than young parents among solitary breeders. However, there was no difference in the level of pair coordination according to parental age classes at high densities. Also, I found that the density of neighbours that breed simultaneously was not related to the level of pair coordination. However, when the number of neighbours that reproduce asynchronously with a focal pair (i.e. whether they do not breed or they are at different breeding stages) increased, the level of pair coordination decreased rapidly. These findings further confirm that a decrease in pair coordination level may be linked to the social interactions (disruptions of synchronous nest visit) with the social group members (local neighbours) that are not engaged in intense parental provisioning of their own broods. The within-pair behavioural mechanisms by which synchrony is achieved and maintained are not fully understood. In chapter 4, I analysed several specific variables that may help to propose observation-based hypotheses regarding the behavioural mechanisms leading to synchrony in parrotbills. Specifically, I investigated the arrival patterns of breeding pairs, the volume of food per visit, the preceding inter-visit interval as a proxy of foraging trip duration, and overall foraging efficiency. I found that one of a breeding pair often spend a long time at the nest after visiting alone, and leave the nest together with its partner who arrive the nest later to feed nestlings. Our finding suggested that waiting for a partner at the nest is likely a mechanism for maintaining continued synchrony. Additionally, during synchronous nest visits, the parent who arrived at the nest first had a larger food load than the follower. Based on these observations, I hypothesize that the first-comer might be the leading individual initiating movement towards the nest and the partner will immediately follow him (or her), which leads to coordinated, synchronous nest visits. Taken together, these results suggest that the breeding pairs of the vinous-throated parrotbills who live in groups developed behavioural mechanism that facilitate the rearing of offspring, with which they showed a very high level of coordination and synchronous nest visits during chick provisioning. However, the degree of parental coordination may vary depending on individual features (e.g. age, experience) and social environment (e.g. proportion of simultaneous breeding pairs).