A Microtomographic Osteology of the Supraoccipital Hook of Nurseryfish, Kurtus gulliveri (Perciformes: Kurtidae)
The Nurseryfish, Kurtus gulliveri, is known for “forehead brooding” parental care behavior in which the adult male carries the egg mass on a hook that overhangs the “forehead” region. This hook is derived from the supraoccipital bone, and it has been suggested to be formed through absorption rather than growth of the supraoccipital crest (SOC). Here we employed X-ray microtomography to investigate the neurocranium with focus on occurrence of the supraoccipital hook in a series of specimens from postflexion larva to adult male and female (10–200 mm SL). A slit-like cavity filled with soft tissue but not spongy bony tissue was revealed in the SOC in all examined specimens except the two smallest larvae (<15 mm SL), thus the cavity appears in the late postflexion-stage. The SOC can be divided into three parts from anterior to posterior in juveniles and adult females by reference to the cavity. 1. The crest rostrum is the most anterior end of the supraoccipital, and it increases in height with a sloped dorsal edge at about a 30° angle. 2. The intermediate segment in the middle of the crest contains a slit-like cavity filled with soft tissue, and its dorsal edge is horizontal and serrated. 3. The posterior process occupies the entire rear portion and is vertically expanded with two transverse ridges. The supraoccipital hook in adult males is derived from this basic configuration by the modifications: the crest rostrum is resorbed ontogenetically, and the dorsal anterior part of the intermediate segment protrudes forward to form the hook; the cavity within the intermediate segment extends into the hook termination. The function of cavity is not yet known; however, our results combined with the previous histological study imply that it may accommodate vessels nourishing the SOC in K. gulliveri. Apogonid fishes, putative relatives of the family Kurtidae, were included in this study for comparison. The SOC is a simple laminar structure without any cavity in Jaydia lineata and J. truncata. Based on the above findings, we suggest that: 1. the supraoccipital hook in adult males is formed by resorption of the crest rostrum combined with growth of the anterodorsal part of the intermediate segment of the SOC; 2. the SOC with a cavity is a unique osteological feature and may represent an anatomical pre-adaption allowing the development of the supraoccipital hook which made possible the evolution of the unique method of paternal forehead brooding in K. gulliveri.
Kurtus gulliveri examined for this study.
3D rendering of the neurocranium of adult male Kurtus gulliveri (NTM S. 15095-002,199 mm SL) in dorsal (A), anterior (B), posterior (C), ventral (D), and lateral (E) views. Abbreviations: BO = basioccipital, BSP = basisphenoid, EPO = epiotic, EXO = exoccipital, F = frontal, f ix = foramen for glossopharyngeal nerve, f le = foramen piercing lateral ethmoid, f lef = foramen between lateral ethmoid and frontal, f mag = foramen magnum, f x = foramen for vagus nerve, io sp = interorbital septum, LE = lateral ethmoid, ME = mesethmoid, os = otic capsule, oto = otolith, P = parietal, PSP = parasphenoid, pt f = posttemporal fossa, PTE = pterotic, SOC = supraoccipital, soc sh = supraoccipital crest shelf, SPH = sphenotic, spo r = supraorbital ridge, V = vomer. Arrowhead indicates the suture-like impression on the supraoccipital. Scale bar: 4.5 mm.
3D renderings of the neurocranium from different sizes of K. gulliveri (A–D) and the apogonid, Jaydia lineata (E). The panel number is organized as letter + numeral. (A) Late postflexion larva (exs. NTM S. 14735-001, 27 mm SL). (B) Juvenile (exs. NTM S. 11569-001, 40 mm SL). (C) Putative subadult male (unnumbered, 99 mm SL). (D) Female (NTM S. 15543-001, 151 mm SL). (E) Jaydia lineata (unnumbered, 63 mm SL). Numeral 1 indicates dorsal view; 2, ventral view; 3, lateral view; 4, frontal view; 5, rear view. Note the SOC of putative subadult male (C3), which indicates an intermediate status. Scale bar: 0.7 mm in A, 1.0 mm in B, 2.5 mm in C, 3.5 mm in D, 2.0 mm in E. Small arrowheads indicate the villiform teeth on along left anterolateral edge of the vomer. Bigger arrowheads indicate the bony interorbital septum. Arrows indicate radiotransparent areas in ethmoid region and posterior wall of the neurocranium at left side (except that in panel A1 at the right). Long arrows indicate the radiotransparent region at the left otic capsule where the otoliths are exposed.
The cavity filled with soft tissue in the bony hook termination extends from the intermediate segment of SOC in male adult K. gulliveri (NTM S. 15095-002, 199 mm SL). (A) Cutaway of 3D rendering of SOC and associated elements. (B) Virtual sagittal section along the median line. (C–F) Virtual coronal slices. (C) Representative slice across the anterior end of supraoccipital hook. (D) Representative slice across the bony hook termination, showing the cavity within the hook. (E) Representative slice across the intermediate segment, showing slit-like cavity. (F) Representative slice across the posterior segment, showing the crest being bony plate. The cavity within SOC is depicted in green and indicated by arrows. Asterisk indicates the suture-like impression on the supraoccipital. Scale bar: 4.0 mm.
The representative virtual coronal slices of SOC from different sizes of K. gulliveri (A–D) and the apogonid, Jaydia lineata (E). These are the same fishes depicted in Figure 3. The panel number is organized as letter + numeral. (A) Late postflexion larva (exs. NTM S. 14735-001, 27 mm SL). (B) Juvenile (exs. NTM S. 11569-001, 40 mm SL). (C) Putative subadult male (unnumbered, 99 mm SL). (D) Female (NTM S. 15543-001, 151 mm SL). (E) Jaydia lineata (unnumbered, 63 mm SL). Numeral 1 indicates slice from anterior segment of SOC (crest rostrum); 2, 3, slices from intermediate segment containing slit-like cavity; 4, slice from posterior process. Bigger arrowheads indicate cavities within the SOC, and smaller arrowheads indicate the bony lamella attached to the bottom of SOC. Scale bar: 1.0 mm in A, B, 2.0 mm in C, 3.0 mm in D, E.
The supraoccipital crest of an adult (A) female (NTM S. 15543-001, 151 mm SL) and (B) male (NTM S. 15095-002, 199 mm SL). The supraoccipital hook in the male is derived from basic SOC configuration in juveniles and adult females. (A) Three segments of SOC (crest rostrum, intermediate segment, vertically expanded posterior process) in adult female delineated by dotted lines. (B) SOC in adult male. The SOCs are semi-transparent, and cavities within SOCs are depicted in green. Scale bar: 4.0 mm.
The SOC (A) and the neurocranium (B, C) of a putative subadult male (unnumbered, 99 mm SL). The SOC is presented in a cutaway with the cavity depicted in green, and the concave dorsal edge of the crest rostrum is indicated by the white arrow. The neurocranium is presented in oblique-ventral views to show the fusion of paired pterosphenoid, indicated by black arrows. Scale bar: 1.5 mm in A, 2.5 mm in B, C.
Contributor Notes
Associate Editor: T. Grande.