Cranial evolution in the extinct Rodrigues Island owl Otus murivorus (Strigidae), associated with unexpected ecological adaptations

Island birds that were victim of anthropic extinctions were often more specialist species, having evolved their most distinctive features in isolation. Here we studied a fossil cranium of the ‘giant’ extinct scops owl Otus murivorus from Rodrigues Island (Mascarene Islands, southwestern Indian Ocean), to determine any potential unique characters. The fossil and extant strigids were imaged through x-ray microtomography, providing 3D views of external and internal (endocast, inner ear) cranial structures. Geometric morphometrics and analyses of traditional measurements yielded new information about the Rodrigues owl’s evolution and ecology. Otus murivorus exhibits a 2-tier “lag behind” phenomenon for cranium and brain evolution, both being proportionately small relative to increased body size. It also had a much more developed olfactory bulb than congeners, indicating an unexpectedly developed olfactory sense, suggesting a partial food scavenging habit. In addition, O. murivorus had the eyes placed more laterally than O. sunia, the species from which it was derived, probably a side effect of a small brain; rather terrestrial habits; probably relatively fearless behavior; and a less vertical posture (head less upright) than other owls (this in part an allometric effect of size increase). These evolutionary features, added to gigantism and wing reduction, make the extinct Rodrigues owl’s evolution remarkable, and with multiple causes.

Methods
This dataset comprises fossil cranium FLMR617 of the extinct owl Otus murivorus from Rodrigues Island, and ten crania of extant species of owls (Strigidae), as follows:

Otus scops male (UCBL-FSL-SKT 246.2), O. sunia (MNHN-LAC 2000.329), O. senegalensis (MNHN-LAC 1997.476), Megascops asio naevius (UCBL-FSL-SKL 1856-540), Bubo scandiacus male (UCBL-FSL-SKL 2626), B. bubo male (UCBL-FSL-SKL, no number, from Ariège), B. cinerascens (UCBL-FSL-SKL 453, FSL), B. zeylonensis male (MNHN-LAC 1986-05), Athene noctua glaux (UCBL-FSL-SKL 568-379), A. cunicularia (UCBL-FSL-SKL 656-436).

Institutions abbreviations: FLMR, François Leguat Museum, Rodrigues, Republic of Mauritius; MNHN-LAC, Laboratoire d’Anatomie Comparée, collection of bird skeletons, Muséum National d’Histoire Naturelle, Paris, France; UCBL-FSL-SKL, collection de la Faculté des Sciences de Lyon de l’Université Claude Bernard Lyon 1 (Villeurbanne, France), category extant bird skulls; UCBL-FSL-SKT, collection de la Faculté des Sciences de Lyon de l’Université Claude Bernard Lyon 1 (Villeurbanne, France), category extant bird skeletons.

All 11 specimens were imaged through x-ray microtomography at ENS de Lyon (GE Phoenix Nanotom 180 device (platform US8/UMS3444 SFR BioSciences), in order to obtain 3D reconstructions of cranium, endocast and inner ear, as well as virtual sections of cranium. Details anout the parameters of all 11 scans are given with the data itself for every taxon (see Usage Notes).

曾受人为灭绝影响的岛屿鸟类往往为特化物种，其独特特征均于孤立生境中演化形成。本研究针对采自印度洋西南部马斯卡林群岛罗德里格斯岛的已灭绝“巨型”鸣角鸮（Otus murivorus）颅骨化石开展分析，以探寻其潜在独有特征。本研究通过X射线显微断层成像（X-ray microtomography）对该化石与现生鸱鸮科（Strigidae）鸟类进行扫描，获取其颅骨外部与内部（颅内模（endocast）、内耳）结构的三维影像。结合几何形态测量学（geometric morphometrics）与传统测量分析，本研究获取了该罗德里格斯鸮演化与生态的全新认知。

Otus murivorus在颅骨与大脑演化方面呈现双层“滞后”现象：相较于体型增长的比例，其颅骨与大脑的尺寸均相对偏小。相较于同属类群，该鸮的嗅球（olfactory bulb）发育程度显著更发达，表明其嗅觉能力远超此前预期，提示其存在部分食腐性觅食行为。此外，Otus murivorus的双眼相较于其祖先类群太阳鸣角鸮（O. sunia）更偏侧向分布，这或为大脑尺寸偏小的附带效应；其栖息习性偏向陆栖，行为相对无惧干扰，且相较于其他鸮类，其身体直立程度更低（这在一定程度上属于体型增大带来的异速生长（allometric）效应）。上述演化特征，加之体型巨型化与翼部退化，使得该已灭绝罗德里格斯鸮的演化历程极具特殊性，且其演化驱动因素具有多元性。

研究方法
本数据集包含采自罗德里格斯岛的已灭绝鸣角鸮（Otus murivorus）颅骨化石FLMR617，以及10件现生鸱鸮科（Strigidae）物种的颅骨标本，具体如下：
1. 红角鸮（Otus scops）雄性标本（编号UCBL-FSL-SKT 246.2）
2. 太阳鸣角鸮（O. sunia）（编号MNHN-LAC 2000.329）
3. 塞内加尔鸣角鸮（O. senegalensis）（编号MNHN-LAC 1997.476）
4. 美洲鸣角鸮内维斯亚种（Megascops asio naevius）（编号UCBL-FSL-SKL 1856-540）
5. 雪鸮（Bubo scandiacus）雄性标本（编号UCBL-FSL-SKL 2626）
6. 雕鸮（B. bubo）雄性标本（编号UCBL-FSL-SKL，无编号，采自阿列日省）
7. 灰雕鸮（B. cinerascens）（编号UCBL-FSL-SKL 453, FSL）
8. 斯里兰卡雕鸮（B. zeylonensis）雄性标本（编号MNHN-LAC 1986-05）
9. 小鸮（Athene noctua glaux）（编号UCBL-FSL-SKL 568-379）
10. 穴小鸮（A. cunicularia）（编号UCBL-FSL-SKL 656-436）

机构缩写说明：
FLMR：罗德里格斯岛弗朗索瓦·勒加博物馆（毛里求斯共和国）；
MNHN-LAC：法国巴黎国家自然历史博物馆比较解剖实验室鸟类骨骼馆藏；
UCBL-FSL-SKL：法国里昂第一大学克洛德·贝尔纳里昂大学理学院馆藏（法国维勒班），现生鸟类头骨标本类；
UCBL-FSL-SKT：法国里昂第一大学克洛德·贝尔纳里昂大学理学院馆藏（法国维勒班），现生鸟类骨骼标本类。

全部11件标本均于里昂高等师范学院采用GE Phoenix Nanotom 180型设备（平台US8/UMS3444 SFR生物科学中心）开展X射线显微断层成像（X-ray microtomography）扫描，以获取颅骨、颅内模（endocast）与内耳的三维重建模型及颅骨虚拟切片。所有11件扫描的参数细节已随各分类单元的数据集同步提供（详见使用说明）。