Morphometric and Radiographic Characteristics of the Skull in Crested Serpent Eagle (Spilornis cheela) and Brown Wood Owl (Strix leptogrammica)

The crested serpent eagle is a medium-sized bird of prey that is found in forested habitats across the tropical Asia and; brown wood owl is a resident breeder in south Asia and is found in India, Bangladesh, Sri Lanka, Indonesia, Taiwan and South China (Choudhary et al., 2018, 2019; Keneisenuo et al., 2019a, b, c).
        
The avian skull is composed of the rostrum, the orbits and the braincase (Morugán-Lobón and Buscalioni, 2006). The geometric, morphometric analysis on avian anatomy is rare (Degrange and Picasso, 2010) and its use in morphological studies of birds is not common (Morugán-Lobón and Buscalioni, 2006). There is no previously reported information on morphometric and radiographic characteristics of skull bones in crested serpent eagle and brown wood owl. The baseline data generated on morphometric and radiographic aspects of skull bones in these species can be used by clinicians in treating surgical and other clinical disorders.

Collection of the samples
 
The specimen of skull bones were procured from four crested serpent eagle and four brown wood owl, brought from the Zoological Park, Aizawl for post mortem examination to the Department of Veterinary Pathology, College of Veterinary Sciences and Animal Husbandry, Aizawl, Mizoram.

Processing of the samples
 
After post-mortem examination, the collected specimens were macerated by boiling maceration technique for 1-2 hours (Choudhary et al., 2015; Choudhary and Singh, 2015, 2016). The macerated bone samples were kept in 3% hydrogen peroxide for one day to make the bones whitish.

These processed samples were utilized for gross anatomical studies. Various measurements (Fig 1-4) of the skull bones in both the species were measured in centimeter (mean±SD) and summarized in Table 1. Thread, scale and digital caliper were used to record morphometrical parameters and obtained parameters of skull bones were subjected to routine statistical analysis (Snedecor and Cochran, 1994). The radiographs of the skull of both the species were taken at Mizoram Health Centre, Aizawl, Mizoram.
 

 

 

 

 

 
Descriptions of various measurements and indices (Table 1 and Fig 1-4)
 
1.      Skull length (SKL): Length between the most prominent point of occipital bone and apex of the rostral part of premaxilla bone.
2.      Skull width (SKW): Width between the mandibular process of the quadrate bone of either side.
3.      Skull index (SKI): Skull width /skull length × 100.
4.      Skull base length (SBL): Length between the caudal edge of occipital condyle and apex of the rostral part of premaxilla bone.
5.      Skull height (SKH): Height between the most prominent point of frontal bone and lamina of parasphenoid bone.
6.      Cranial length (CRL): Length between the most prominent point of the occipital bone and middle point of frontonasal suture.
7.      Maximum width of neurocranium (MWN): Width between the bases of the postorbital process on the frontal bone.
8.      Cranial index (CRI): Width of neurocranium /cranial length × 100.
9.      Viscerocranial length (VCL): Length between the middle point of frontonasal suture and apex of the rostrum of premaxilla bone.
10.    Zygomatic width (ZYW): Width between projections of the lateral frontonasal suture on jugal bar (arcus jugalis).
11.    Facial index (FAI): Zygomatic width/ viscerocranial length × 100.
12.    Height of foramen magnum (FMH): Height between the middle of dorsal and ventral margins of the foramen  magnum.
13.    Width of the foramen magnum (FMW): Width between the middle of both lateral margins of the foramen magnum.
14.    Foramen magnum index (FMI): Height of foramen magnum/ width of foramen magnum × 100.
15.    Length of mandible (MAL): Maximum length of mandible.
16.    Width of mandible (MAW): Maximum width of mandible.

The skull (Fig 1-10) of crested serpent eagle and brown wood owl appeared pyramidal in shape with a wide rounded base and flat apex. The skull length, skull width, skull base length, skull height was 9.31±0.03 cm, 4.90±0.01 cm, 8.22±0.01 cm, 3.36±0.00 cm and 8.78±0.02 cm, 6.02±0.02 cm, 7.49±0.01 cm, 3.74±0.01 cm in crested serpent eagle and brown wood owl, respectively. The skull of both the species was dolichocephalic as per the cephalic index. The skull or cephalic index was 52.63±0.04 and 68.56±0.03 in crested serpent eagle and brown wood owl, respectively. It can be concluded from the present results, that more cephalic index restricts the flying ability of the birds as indicated in brown wood owl as compared to the crested serpent eagle.
 
The skull of both the species (Fig 1) composed of the neurocranium (bones of the cranium) and viscerocranium (bones of the face) which were separated by two large orbital cavities. The neurocranium was composed of the single (occipital, sphenoid, ethmoidal) and paired (temporal, parietal and frontal) bones. The viscerocranium consisted of the single (mandible, vomer and hyoid) and paired (quadrate, lacrimal, nasal, premaxilla, maxilla, zygomatic, palatine and pterygoid) bones in both the species as also reported in ostrich (Moselhy et al., 2018). The cranial length, neurocranium width, viscerocranial length, zygomatic width was 5.65±0.02 cm, 3.32±0.01 cm, 3.62±0.02 cm, 2.45±0.02 cm and 5.05±0.01 cm, 4.22±0.01 cm, 3.71±0.02 cm, 3.20±0.02 cm in crested serpent eagle and brown wood owl, respectively. The cranial index, facial index was 58.76±0.03, 67.66±0.02 and 83.56±0.03, 86.25±0.02 in crested serpent eagle and brown wood owl, respectively.
 
The occipital bone (Fig 7,8,10) in both the species was situated basally and formed by three parts; base (basioccipitale), paired lateral (exooccipitale) and squamous (supraoccipital) part as also reported in ostrich (Moselhy et al., 2018). All the parts of occipital bone were surrounded by a rounded foramen magnum in crested serpent eagle however, the foramen magnum was triangular in chickens (McLelland, 1990). The foramen magnum was vertical oval in brown wood owl as also reported in turkeys (Süzer et al., 2018).
 
The height, width of the foramen magnum was 0.75±0.02 cm, 0.76±0.01 cm and 0.57±0.02 cm, 0.68±0.02 cm in crested serpent eagle and brown wood owl, respectively. The foramen index was more (119.25±0.02) in brown wood owl as compared to (101.33±0.01) crested serpent eagle. It can be concluded that the nervous system was larger in the brown wood owl as compare to that of crested serpent eagle. The rounded single occipital condyle in both the species was situated basally, however, the occipital condyle was pear-shaped in emu (Kumar and Singh, 2014) and hemispherical in ostrich (Moselhy et al., 2018). The presence of single occipital con­dyle helps in the rotation of head on the vertebral column to a larger extent compared to that of mammals (Dyce et al., 2002). The supraoccipital part represented the thick caudal aspect of the cranial cavity which was separated from the parietal bone, dorsally by the nuchal crest and had a median external occipital protuberance as also reported in ostrich (Moselhy et al., 2018). The basal part is divided into two depressed fossae by raised area and was separated from basisphenoid by a transverse ridge. The paired lateral part was protruded, formed a broad process (paraoccipital process) that demarcated the external acoustic meatus, caudally. The hypoglossal foramen in both the species was situated medial to the paraoccipital process as reported in ostrich (Moselhy et al., 2018).  In the present study, the parietal bone in both the species was not found with distinct demarca­tion which may be due to the fusion between the frontal and parietal as the parietofrontal suture (Evans and Noden, 2006).
 
The sphenoid bone (Fig 7) was divided into rostral presphenoid and caudal basisphenoid parts as also reported in crow (John et al., 2016) and ostrich (Moselhy et al., 2018). The frontal bone (Fig 5,6,10) was the largest bone of the cranium and formed the roof of the cranium in both the species however roof of the cranial cavity was formed by the frontal, parietal and supraoccipital bones in fowl (King and McLelland, 1984; McLelland, 1990). The external surface of both sides is slopped craniocaudally and raised centrally by frontal elevation, the internal surface had a deep cerebral fossa and the orbital surface (wing) formed the caudomedial boundary of the orbit which had a large optic foramen as also mentioned in ostrich (Moselhy et al., 2018). The orbital surfaces of both sides were fused with each other, forming the interorbital septum in both the species. The supraorbital margin was formed by the lateral border while interfrontal suture was formed by the fusion of the medial borders as also reported in ostrich (Moselhy et al., 2018).
 

 

 

 

 
The frontal bone possessed frontal, lacrimal and postorbital processes as also reported in goose (Feduccia et al., 1975) and ostrich (Moselhy et al., 2018).
 
The temporal bone formed the ear capsule and squamous part as mentioned in crow (John et al., 2016) and ostrich (Moselhy et al., 2018). The ear capsule was an irregular circular pneumatic cavity which extended deeply to the floor of the cranium and internally contained round narrow internal acoustic meatus as also described in ostrich (Moselhy et al., 2018). The capsule had a crescentic groove (orobasal articular groove) for articulation with the otic process of quadrate bone. This groove was more prominent in the brown wood owl as compared to the crested serpent eagle. The squamous temporal bone had a large flat zygomatic process that projected rostroventrally below the temporal fossa and lateral to the otic process of the quadrate bone. The ventrolateral bony boundary of the cranium was formed by the temporal bone which internally had the shallow cerebellar fossa.
 
The quadrate bone in both the species has consisted of a body and three processes; mandibular, otic and orbital. The mandibular process in both the species was divided into medial and lateral condyles (Fig 8) by a deep groove (sulcus intercondylaris) as reported earlier in corvid species (Bock, 1964), crow (John et al., 2016) and ostrich (Moselhy et al., 2018); however Hassan (2012) of hooded crow reported the presence of lateral, medial and caudal condyles in the quadrate bone. The otic process of quadrate bone was embedded dorsally in between basisphenoid, ear capsule and squamous temporal bone. The orbital process was wide and projected rostomedially towards the orbit as described in crow (John et al., 2016) and ostrich (Moselhy et al., 2018). A small tubercle (Fig 6, 7) was positioned between the medial condyle and orbital process of quadrate bone as reported in crow (John et al., 2016). The quadrate bone acts as a bridge between skull and mandible and forms the basis for cranial kinesis.
 

 
The lacrimal bone (Fig 5,6) in both the species was a small bone that covered medially the frontal process of the nasal bone and fused caudally with the frontal bone as also reported in ostrich (Moselhy et al., 2018). The lacrimal process was directed ventrally and was more prominent in crested serpent eagle as compared to the brown wood owl.
 
The nasal bone (Fig 5,10) formed the nasal cavity and also fused rostrally with the frontal process of the premaxilla to form the upper beak. The nasal bone was large in the crested serpent eagle as also reported in ostrich (Moselhy et al., 2018), however, it was comparatively smaller in the brown wood owl. The nasal bone branched into three processes; frontal, premaxillary and lateral nasal.
 
The premaxilla (Fig 5,7,10) consisted of maxillary, palatine and frontal processes. The frontal process of premaxilla of both the sides fused to each other, covering the nasal bone which was directed caudally reaching the frontal bone forming nasofrontal hinge as also described in ostrich (Moselhy et al., 2018). Nasal frontal hinge, a characteristic feature of the avian skull, forms the basis of cranial kinesis. Gussekloo et al., (2001) during their study on three-dimensional kinematics of crow reported the type of cranial kinesis as prokinesis and the eleva­tion of the upper bill of the crow was 6.5°. In prokinesis, the up­per bill rotates around the nasal-frontal hinge and the bill itself remains inflexible (Zusi, 1984). Indu et al., (2013) in a study on green winged macaw, reported that the frontonasal synovial hinge joint was highly mobile and supported the well-developed pro­kinesis seen in this bird.
 
The maxilla (Fig 5,6,10) was a small, delicate bone which constitutes the caudal rim of the upper beak and a part of bony palate; its narrow rostral part (premaxillary process) joined laterally with the maxillary process of premaxilla and medially with palatine process of the premaxilla. It gradually broadened and branched caudally to fuse with pterygoid bone by the pterygoid process of maxilla medially and formed the jugal process of maxilla laterally as also reported in ostrich (Moselhy et al., 2018). The maxilla in birds is greatly reduced (Zusi, 1993), a feature that may be attributed to two different reasons. The first is that this may facilitate cranial kinesis which has been observed in most birds (Zusi, 1984; Bout and Zweers, 2001). The reduced maxilla helps in more proximal placement of the ant-orbital fenestra which provides greater vertical thrust on the rostrum. The reverse would give a more horizontal thrust and hinder a sufficient lift of the beak (Zusi, 1984). A second explanation for reduced maxilla in birds is that a proximal place­ment of the external nares is preferable to prevent the entry of mud or water into nostrils while probing for food in mud or water and thus enabling breathing while feeding. Reduction of the maxilla in both cases consequently led to a com­pensatory lengthening of the premaxilla to maintain the length of the rostrum.
 
The zygomatic or jugal bone (Fig 5-7,10) in both the species was a thin rounded rod-like prolongation of the caudolateral rim of the upper beak. The paired jugal bones diverged in a curved manner caudally toward the quadrate bone to form three fused bony parts; jugal process of maxilla bone, jugal and quadratojugal (Fig 6) as also reported in ostrich (Moselhy et al., 2018). The caudal end of jugal bone or quadratojugal formed a movable joint with quadrate bone as also reported in crow (John et al., 2016).
 
The palatine bone (Fig 6-8) in both the species was a delicate quadrilateral bony plate situated on both sides of the vomer bone and remained joined with the posterior part of premaxilla and maxilla, rostrally while it overlaps the end of rostral pterygoid process, caudally as also mentioned in ostrich (Moselhy et al., 2018). The pterygoid bones were parallel thin quadrilateral delicate bony plates placed on either side of vomer bone as also mentioned in ostrich (Moselhy et al., 2018). It articulated rostrally with the palatine, presphenoid and caudally with the quadrate bone as mentioned in crow (John et al., 2016) and ostrich (Moselhy et al., 2018).
 

 
The vomer bone (Fig 7) was a long tube-like bone located in the median plane of the floor of the skull in both the species as mentioned in crow (John et al., 2016) and ostrich (Moselhy et al., 2018); however, the vomer bone was rudimentary in fowl and pigeon (Nickel et al., 1977).
 
The mandible (Fig 9) of both the species was nearly alphabet “V” shaped with curved two rami, which formed  the mandibular symphysis cranially as mentioned in birds (Proctor and Lynch, 1993) including ostrich (Moselhy et al., 2018). The mandibles of either side were connected cranially to form the mandibular symphysis in both the species. The mandibular symphysis consisted of numerous lateral and medial rostral mandibular foramina in both the species. The lateral and medial surfaces of mandible consisted of caudal mandibular foramina as also reported in ostrich (Moselhy et al., 2018). The articular part of mandible in both the species was prismatic in shape and the dorsal articular cavity articulated with the medial and lateral condyles of the mandibular process of the quadrate bone by two medial and lateral facets to form movable quadratomandibular joint. The medial and lateral articular facets were also reported in hooded crow (Hassan, 2012) and emu (Kumar and Singh 2014). Furthermore, three facets i.e. medial, lateral and caudal facets were present in the cattle egret (Hassan, 2012). The length, width of the mandible was 6.96±0.02 cm, 3.89±0.02 cm and 5.95±0.02 cm, 4.88±0.01 cm in crested serpent eagle and brown wood owl, respectively. The hyoid consisted of bones and cartilaginous parts associated with the upper respiratory system forming the hyobranchial apparatus in both the species as also reported in ostrich (Moselhy et al., 2018).
 

 
The nasal cavity was the smallest cavity in both species and bounded dorsally by the nasal bone, premaxilla and ethmoidal bone. Dorsolaterally, the nasal cavity was limited by the lateral process of the nasal bone. The ventral boundaries from rostral to caudal were the premaxilla, maxilla, palatine bone and the rostral part of the pterygoid bone, respectively as also reported in ostrich (Moselhy et al., 2018). The cranial cavity (Fig 10) in both the species was bounded dorsally by frontal bone; rostroventrally by basioccipital and basisphenoid; caudally by parietal, supraoccipital part and rostrally by the posterior part of the interorbital septum as also mentioned in ostrich (Moselhy et al., 2018).
 
It can be concluded from the present study that the skull in both the species contained neurocranium and viscerocranium bones with the absence of interparietal bones. There were variations in the shape and components of the skull of both the species in comparison with other flying birds.

The authors are thankful to the Dean, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University (I), Aizawl, Mizoram for providing all the necessary facilities to carry out research work.