Research Article: Evolution of a Functional Head Joint in Deep-Sea Fishes (Stomiidae)

Date Published: February 1, 2017

Publisher: Public Library of Science

Author(s): Nalani K. Schnell, G. David Johnson, Wm. Leo Smith.


The head and anterior trunk region of most actinopterygian fishes is stiffened as, uniquely within vertebrates, the pectoral girdles have a direct and often strong connection through the posttemporal to the posterior region of the skull. Members of the mesopelagic fish family Stomiidae have their pectoral girdle separated from the skull. This connection is lost in several teleost groups, but the stomiids have an additional evolutionary novelty—a flexible connection between the occiput and the first vertebra, where only the notochord persists. Several studies suggested that stomiids engulf significantly large prey items and conjectured about the functional role of the anterior part of the vertebral column; however, there has been no precise anatomical description of this complex. Here we describe a unique configuration comprising the occiput and the notochordal sheath in Aristostomias, Eustomias, Malacosteus, Pachystomias, and Photostomias that represents a true functional head joint in teleosts and discuss its potential phylogenetic implications. In these genera, the chordal sheath is folded inward ventrally beneath its connection to the basioccipital and embraces the occipital condyle when in a resting position. In the resting position (wherein the head is not manipulatively elevated), this condyle is completely embraced by the ventral fold of the notochord. A manual manipulative elevation of the head in cleared and stained specimens unfolds the ventral sheath of the notochord. As a consequence, the cranium can be pulled up and back significantly farther than in all other teleost taxa that lack such a functional head joint and thereby can reach mouth gapes up to 120°.

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The family Stomiidae represents one of the dominant fish families in mesopelagic ecosystems [1], exhibiting an array of specializations to a predatory existence in this environment, e.g. huge mouth gapes with prominent teeth, distensible stomachs, elongated dark bodies with photophores, and chin barbels with bioluminescent tissue [2–8]. Malacosteus, Aristostomias, and Photostomias lack an intermandibular membrane [3], and as a consequence jaw-closing velocity is increased [3,9]. Malacosteus, Aristostomias and Pachystomias possess far-red emitting photophores and a visual system that is sensitive to such long-wave emissions [10,11]. Some stomiid taxa have from one to ten anterior vertebrae reduced or entirely absent [2,12,13], and all of them have a distinctive gap between the occiput and the first vertebra, wherein only the flexible notochord persists [13,14]. This occipito-vertebral gap does not result from loss or reduction of vertebrae, but rather from an elongation of the notochord in this area of the vertebral column [13,14]. The unparalleled occipito-vertebral gap in stomiids allows a considerable degree of cranial elevation and is notably enhanced in the genera that share the functional head joint described herein (Fig 1A). We propose that this feature is an adaptation to extend the reach of the mouth gape antero-dorsally and for engulfing particularly large prey items. The separation of the pectoral girdle from the skull, due to the loss of the posttemporal and extrascapular [15] in all genera herein discussed, reinforces the maneuverability of the head. Stomach content analyses support this hypothesis, reporting that Aristostomias, Eustomias (Fig 2), and Pachystomias are piscivorous, feeding mainly on myctophids [6,8]. Only Malacosteus and Photostomias were found to feed mainly on crustaceans (copepods and penaeidean shrimps) [6,8]. It has been suggested that there has been a secondary reversion to planktivory in Malacosteus [8] that is correlated with the unique characters of red vision and red bioluminescence [10,11,16].

Our research employed only ethanol-preserved specimens deposited in museum collections and did not involve animal experimentation or examination of fossil specimens. Examined material is listed in the following section “Material examined” and is deposited in the following institutions: National Museum of Natural History, Smithsonian Institution, USA (USNM); Scripps Institution of Oceanography, USA (SIO); Museum of Comparative Zoology, Harvard University, USA (MCZ); British Museum of Natural History, UK (BMNH); National Museum of Nature and Science, Japan (NSMT-P); Virginia Institute of Marine Science, USA (VIMS). Access to material of those collections was authorized by respective curators and specimens were examined at their original institutions or loaned to the Muséum national d’Histoire naturelle (MNHN). No permits were required for the described study, which complied with all relevant regulations. Preserved specimens were cleared and double stained (c&s) [17,18] and afterwards examined and dissected using a Zeiss Discovery V12/V20 stereomicroscope. One specimen was cleared and triple stained (c&ts) with Sudan Black B, in order to stain nerves, following the alcian blue-alizarin red staining [19]. Photographs were taken with an attached Axiocam microscope camera and processed with the Zeiss AxioVision or ZEN software to obtain composite images with an increased depth of field. The specimens for the histological serial sections (hss) were embedded in paraffin and stained with Azan [20]. All measurements referenced herein are standard length, SL, unless otherwise mentioned.

In basal stomiid genera, the notochordal sheath forms a straight connection between the occiput (the basioccipital and exoccipital) and the first vertebra, e.g., in Flagellostomias boureei (Fig 3A) and Idiacanthus antrostomus (Fig 3B). Whereas in Aristostomias, Eustomias, Malacosteus, Pachystomias, and Photostomias (Fig 3G, 3I, 3K, 3M and 3O) the notochord is folded inward ventrally beneath its connection to the basioccipital, and this extra sheath embraces the occipital condyle in a resting position (i.e., wherein the head is not manually elevated and the jaws are closed, Fig 1B, 1D and 1F). The occipital condyle is formed by only the posteriorly elongated basioccipital in Eustomias, Malacosteus, and Pachystomias, but in Aristostomias and Photostomias, it also includes the exoccipitals. A manipulative opening of the mouth, and resultant elevation of the head in cleared and stained specimens, unfolds the ventral sheath of the notochord (Figs 1C, 1E, 1G, 1H, 3H, 3J, 3L, 3N and 3P). As a consequence, the cranium can be pulled up and back farther than in taxa that lack such a functional head joint. Manipulative elevation of the neurocranium results in a 30° (Eustomias, Grammatostomias, Pachystomias) to about 80° (Aristostomias, Malacosteus, Photostomias) dorsal flexion. At the same time, the jaws are rotated anteriorly. When manipulative elevation of the head is terminated, the ventral sheath of the notochord folds back inward to its original position embracing the occipital condyle (Fig 1B, 1D and 1F), and the neurocranium moves back into a resting position, where it is ventrally declined in Aristostomias, Malacosteus, and Photostomias [3]. In Bathophilus and Grammatostomias, the ventral sheath of the notochord overlaps the basioccipital posteriorly to a much lesser extent, and the posterior margin of the basioccipital forms a ventrally directed rim to which the notochordal sheath attaches (Fig 3C–3F). Histology shows that anlagen for the head joint are present in Bathophilus and Grammatostomias, wherein the chordal sheath slightly overlaps the basioccipital ventrally and thus seemingly represents an intermediate stage (red box in Fig 3).

Cranial elevation driven by the epaxial musculature is a common feature of feeding in fishes, as it contributes to mouth opening and promotes jaw protrusion [21]. In stomiids, the presence of considerable flexibility in the anterior part of the vertebral column coincident with a functional head joint allows extension of the mouth gape antero-dorsally and enables these taxa to have gapes up to 120° [3, 9].