Editorial Type:
Article Category: Research Article
 | 
Online Publication Date: 19 Nov 2015

Development of the Rostrum and Upper Jaws in Squirrelfishes and Soldierfishes (Beryciformes: Holocentridae): A Unique Ontogenetic Trajectory

and
Page Range: 902 – 919
DOI: 10.1643/CG-15-260
Save
Download PDF

The Holocentridae are nocturnal fishes inhabiting shallow to deep water coral and rocky reefs in the tropical parts of the Indian, Pacific, and Atlantic oceans. They comprise two subfamilies, the squirrelfishes (Holocentrinae) and the soldierfishes (Myripristinae). Unlike the adults, holocentrid larvae are pelagic and are characterized by elaborate head spination, including a prominent rostrum and supraoccipital, preopercular, and opercular spines. The rostrum, formed by fused or separate nasal bones, can project far anterior to the mouth and is supported by a large, bulbous ethmoid cartilage. The spine-bearing bones, the lower jaw bones, and one pair of upper jaw bones (maxillae) are the first to ossify (at 1.2 mm NL). In several cleared-and-double-stained ontogenetic series of Holocentridae (1.2 mm NL–35.0 mm SL), we found that the other pair of upper jaw bones (premaxillae) exhibits a unique ontogenetic trajectory. The premaxillae develop late (between 5.9 mm and 6.6 mm), well after the other jaw bones and head spines are developed, and most of the remaining skeleton is ossified. Furthermore, the protuberant ethmoid cartilage precludes effective upper jaw protrusion until the larvae reach ca. 35 mm SL. In most marine fishes, all jaw bones ossify simultaneously very early in development along with the caudal fin and pectoral girdles, thus ensuring the ability to swim and feed immediately after hatching. We describe the jaw and rostrum development in holocentrids, compare it with that of tilefishes (Malacanthidae), the only other teleost in which the larvae have a rostrum comprising the nasal bones, and discuss the implications.

Copyright: © 2015 by the American Society of Ichthyologists and Herpetologists
Fig. 1. 
Fig. 1. 

Ontogenetic series of holocentrine species in lateral view, anterior facing left. (A) SEAMAP 22373, 1.2 mm NL. (B) SEAMAP 27107, 1.5 mm NL. (C) SEAMAP 27107, 1.6 mm NL. (D) SEAMAP 5521, 1.7 mm NL. (E) SEAMAP 28450, 2.0 mm NL. (F) SEAMAP 21476, 2.4 mm NL. (G) USNM 432142, 5.7 mm SL. (H) MCZ 85215, 7.9 mm SL. (I) NSMT-PL 681, 14.8 mm SL.

Fig. 2. 
Fig. 2. 

Holocentrinae versus Myripristinae. (A, B) Holocentridae from Florida Straits. Photographs by Cedric Guigand. (A) Holocentrinae sp. (ca. 8 mm SL), has been previously published in Gaines et al. (2007) and (B) Myripristinae sp. (ca. 5 mm SL), in Thorrold, Zacherl, and Levin (2007). (C) Holocentrinae sp. (USNM uncat., 3.5 mm SL). (D) Myripristinae sp. (SEAMAP 21506, 3.0 mm).

Fig. 3. 
Fig. 3. 

Development of the rostrum, supraoccipital, preopercular, and opercular spines in Holocentrinae. (A) Lateral view, anterior facing left (SEAMAP 2223, 1.8 mm NL). (B) Frontal view (SEAMAP 2223, 1.8 mm NL). (C) Suspensorium, anterior facing left (USNM 432101, 3.5 mm NL). (D) Suspensorium, anterior facing left (USNM 432143, 20.0 mm SL). (E) Dorsal view, anterior facing left (SEAMAP 2223, 1.8 mm NL). (F) Dorsal view, anterior facing left (SEAMAP 2223, 2.2 mm NL). (G) Dorsal view, anterior facing left (USNM 432101, 3.0 mm NL). (H) Dorsal view, anterior facing left (USNM uncat., 21.1 mm SL). (I) Dorsal view, anterior facing left (USNM uncat., 29.7 mm SL). (J) Dorsal view, anterior facing left, of Sargocentron vexillarium (USNM 269553, 39.0 mm SL). Abbreviations: apl, autopalatine; d, dentary; ecp, ectopterygoid; enp, endopterygoid; ethc, ethmoid cartilage; h, hyomandibula; iop, interopercle; mpt, metapterygoid; mx, maxilla; n, nasal; op, opercle; pop, preopercle; q, quadrate; soc, supraoccipital; sop, subopercle; sym, symplectic.

Fig. 4. 
Fig. 4. 

Development of the premaxilla in Holocentrinae. Lateral view, anterior facing left. (A) USNM 432101, 3.5 mm NL. (B) USNM 432101, 3.0 mm NL. (C, D) MCZ 85252, 5.9 mm SL. (E) MCZ 85215, 10.0 mm SL. (F) MCZ 85252, 7.7 mm SL. (G) USNM uncat., 21.1 mm SL. (H) USNM 432143, 20.0 mm SL. (I) Sargocentron punctatissimum (USNM 287825, 45.0 mm SL) left nasal, antorbital, and lacrimal removed. (J) Sargocentron diadema (USNM 287735, 59.0 mm SL). Abbreviations: ang-ar, anguloarticular; ap, ascending process of premaxilla; d, dentary; ethc, ethmoid cartilage; mx, maxilla; n, nasal; pmx, premaxilla; pop, preopercle; rar, retroarticular; rc, rostral cartilage; smx, supramaxilla; soc, supraoccipital.

Fig. 5. 
Fig. 5. 

Development of the rostrum in Myripristinae in dorsal view, anterior facing left. (A) SEAMAP 29494, 3.0 mm NL. (B) SEAMAP 29494, 3.8 mm NL. (C) SEAMAP 29494, 4.3 mm NL. (D) NSMT-PL 658, 4.5 mm SL. (E) Myripristina pralinia (USNM 288353, 60.0 mm SL). Abbreviations: n, nasal.

Fig. 6. 
Fig. 6. 

Development of the premaxilla in Myripristinae. Lateral view, anterior facing left. (A, B) USNM 432103, 3.5 mm NL. (C, D) USNM 432104, 6.2 mm SL. (E) NSMT-PL 693, 9.5 mm SL. (F) NSMT-PL 693, 15.5 mm SL. (G) Myripristis pralinia (USNM 288353, 46.0 mm SL). Abbreviations: ang-ar, anguloarticular; ap, ascending process of premaxilla; d, dentary; ethc, ethmoid cartilage; mx, maxilla; n, nasal; op, opercle; pmx, premaxilla; pop, preopercle; rar, retroarticular; rc, rostral cartilage; smx, supramaxilla; soc, supraoccipital.

Fig. 7. 
Fig. 7. 

Development of the upper jaw and rostrum in Caulolatilus spp., Malacanthidae. (A) Frontolateral view. (B–D) Lateral view, anterior facing left. (A, B) USNM uncat., 3.8 mm NL. (C, D) SEAMAP 33669, 2.9 mm NL. Abbreviations: ap, ascending process of premaxilla; d, dentary; mx, maxilla; n, nasal; pmx, premaxilla; pop, preopercle; pt, posttemporal.

Fig. 8. 
Fig. 8. 

Development of the upper jaw and rostrum in Hoplolatilus spp., Malacanthidae. (A–C) Dorsal view, anterior facing left; (D–G) lateral view, anterior facing left. (A, C, D) USNM 432110, 4.7 mm SL. (B) USNM 432111, 22.0 mm SL. (E) USNM 432110, 4.7 mm SL. (F) USNM 432111, 22.0 mm SL. (G) USNM 432112, 9.1 mm SL. Abbreviations: ap, ascending process of premaxilla; d, dentary; mx, maxilla; n, nasal; pmx, premaxilla; pop, preopercle; pt, posttemporal; rc, rostral cartilage.

Fig. 9. 
Fig. 9. 

Development of the upper jaw and rostrum in Malacanthus spp., Malacanthidae. (A–D) Lateral view, anterior facing left. (E, F) Dorsal view, anterior facing left. (A, B) SEAMAP 33758, 4.2 mm NL. (C–E) USNM 432105, 12.8 mm SL. (F) USNM 432107, 20.0 mm SL. Abbreviations: ap, ascending process of premaxilla; d, dentary; mx, maxilla; n, nasal; pmx, premaxilla; rc, rostral cartilage.

Fig. 10. 
Fig. 10. 

Head spination in ctenosquamate larvae and jaw protrusibility in Carangidae. (A) Nannobrachium achirus (USNM uncat., ca. 11.0 mm SL). (B, C) Branchiostegus sp. (USNM 432141, 12.0 mm SL). (D) Hoplolatilus sp. (USNM 432144, ca. 12.4 mm SL). (E) Acanthocybium sp. (USNM 432140, 13.8 mm SL). (F) Xiphias sp. (USNM uncat., 15.5 mm SL). (G) Selene sp. (USNM 432349, 3.7 mm NL). (H) Selene sp. (USNM 432349, 4.3 mm SL). (I) Caranx sp. (USNM 432348, 10.9 mm SL). (J) Nannobrachium achirus (USNM 432113, 7.5 mm SL). (K) Selene sp. (USNM 432349, 4.3 mm SL). (L) Scomberomorus maculatus, 9.0 mm (previously published in Johnson, 1986); (M) Istiophorus sp. (USNM 432352, 16.0 mm SL). (N) Istiophorus sp. (USNM 432352, 8.7 mm SL). Abbreviations: cl, cleithrum; d, dentary; mx, maxilla; pmx, premaxilla; pop, preopercle; pto, pterotic; rc, rostral cartilage. Scale bar in A–I  =  1 mm.

Contributor Notes

Associate Editor: G. Arratia.

Received: 24 Feb 2015
Accepted: 10 Mar 2015
  • Download PDF