The Anatomy of the bill Tip of Kiwi and Associated Somatosensory Regions of the Brain: Comparisons with Shorebirds

Three families of probe-foraging birds, Scolopacidae (sandpipers and snipes), Apterygidae (kiwi), and Threskiornithidae (ibises, including spoonbills) have independently evolved long, narrow bills containing clusters of vibration-sensitive mechanoreceptors (Herbst corpuscles) within pits in the bill-tip. These ‘bill-tip organs’ allow birds to detect buried or submerged prey via substrate-borne vibrations and/or interstitial pressure gradients. Shorebirds, kiwi and ibises are only distantly related, with the phylogenetic divide between kiwi and the other two taxa being particularly deep. We compared the bill-tip structure and associated somatosensory regions in the brains of kiwi and shorebirds to understand the degree of convergence of these systems between the two taxa. For comparison, we also included data from other taxa including waterfowl (Anatidae) and parrots (Psittaculidae and Cacatuidae), non-apterygid ratites, and other probe-foraging and non probe-foraging birds including non-scolopacid shorebirds (Charadriidae, Haematopodidae, Recurvirostridae and Sternidae). We show that the bill-tip organ structure was broadly similar between the Apterygidae and Scolopacidae, however some inter-specific variation was found in the number, shape and orientation of sensory pits between the two groups. Kiwi, scolopacid shorebirds, waterfowl and parrots all shared hypertrophy or near-hypertrophy of the principal sensory trigeminal nucleus. Hypertrophy of the nucleus basorostralis, however, occurred only in waterfowl, kiwi, three of the scolopacid species examined and a species of oystercatcher (Charadriiformes: Haematopodidae). Hypertrophy of the principal sensory trigeminal nucleus in kiwi, Scolopacidae, and other tactile specialists appears to have co-evolved alongside bill-tip specializations, whereas hypertrophy of nucleus basorostralis may be influenced to a greater extent by other sensory inputs. We suggest that similarities between kiwi and scolopacid bill-tip organs and associated somatosensory brain regions are likely a result of similar ecological selective pressures, with inter-specific variations reflecting finer-scale niche differentiation.

三类以探查取食为策略的鸟类类群——鹬科（Scolopacidae，鹬与沙锥）、无翼鸟科（Apterygidae，几维鸟）以及鹮科（Threskiornithidae，朱鹮类，包含琵鹭）——独立演化出了修长狭窄的喙，其喙尖的凹陷结构内分布着成簇的振动敏感机械感受器——赫氏小体（Herbst corpuscles）。这类被称为“喙尖器官”的结构，可使鸟类通过基质传导的振动以及/或者间隙压力梯度，探测埋藏于地下或隐匿于水下的猎物。鸻鹬类、几维鸟与鹮科类群的亲缘关系极为疏远，其中几维鸟与另外两个类群之间的系统发育分化尤为深邃。为明晰这两类群间此类感官系统的趋同演化程度，我们对比了几维鸟与鸻鹬类的喙尖结构，以及二者脑中对应的体感区域。为保障对照实验的严谨性，本研究同时纳入了其他类群的数据，包括雁形目鸭科（Anatidae）、鹦鹉科（Psittaculidae与凤头鹦鹉科Cacatuidae）、非无翼鸟科的平胸鸟类，以及其他探查取食与非探查取食的鸟类——例如非鹬科的鸻形目鸟类（鸻科、蛎鹬科、反嘴鹬科与燕鸥科）。研究结果表明，无翼鸟科与鹬科的喙尖器官结构大体相似，但两组间在感受器凹陷的数量、形态与朝向方面存在一定的种间差异。几维鸟、鹬科鸻鹬类、鸭科鸟类与鹦鹉类均呈现出主要三叉神经感觉核的肥大或近乎肥大的状态。而喙基核（nucleus basorostralis）的肥大仅见于鸭科、几维鸟、本次研究涉及的三种鹬科物种，以及一种蛎鹬（鸻形目：蛎鹬科）。几维鸟、鹬科以及其他触觉特化类群的主要三叉神经感觉核肥大现象，似乎与喙尖的特化特征协同演化；而喙基核的肥大则可能更多受到其他感官输入的影响。我们推测，几维鸟与鹬科鸟类的喙尖器官及其对应的体感脑区之间的相似性，大概率源于相似的生态选择压力，而种间差异则反映了更精细尺度上的生态位分化。