Niphon Spinosus: a Primitive Epinepheline Serranid, with Comments on the Monophyly and Intrarelationships of the Serranidae Author(S): G

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Niphon spinosus: A Primitive Epinepheline Serranid, with Comments on the Monophyly and Intrarelationships of the Serranidae Author(s): G. David Johnson Source: Copeia, Vol. 1983, No. 3 (Aug. 16, 1983), pp. 777-787 Published by: American Society of Ichthyologists and Herpetologists Stable URL: http://www.jstor.org/stable/1444346 Accessed: 02/06/2010 14:09

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http://www.jstor.org Copeia, 1983(3), pp. 777-787

Niphon spinosus: A Primitive Epinepheline Serranid, with Comments on the Monophyly and Intrarelationships of the Serranidae

G. DAVID JOHNSON

Three reductive specializations (absenceof the posterior uroneural, procurrent spur and third preural radial cartilages) define the percoid family Serranidae with respect to the ostensibly polyphyletic Percichthyidae (sensu Gosline, 1966). A single innovative specialization, the presence of three spines on the opercle, indicates that the Serranidae are monophyletic. All members of the serranid subfamily Epinephelinae, comprising five tribes, share a unique modification of the first dorsal pterygiophore, seemingly a specialization for support of the elongate dorsal spine of the larvae. The enigmatic Niphon spinosus, placed in the Percichthyidae by Gosline (1966), and in the Centropomidae by Rivas and Cook (1968), shares the epinepheline specialization, as well as the four specializations that characterize the Serranidae. It is hypothesized that the monotypic Niphon is the sister group of all other epinephelines. Identification of the larva of Niphon could provide corroborative evidence for this hypothesis.

TIPHON spinosus Cuvier is a percoid fish in- acters that he regarded as diagnostic for the IV habiting shallow marine waters along the Centropomidae (expanded second neural spine coasts of Japan, Korea, China and the Philip- and lateral line extending to the posterior mar- pines. Its chief distinctive external features are gin of the caudal fin) and concluded that the a large spine at the angle of the preopercle and closest relatives of Niphon would probably prove robust serrations along the ventral margin of to be among the heterogeneous assemblage of the lacrimal (Figs. 1, 2). The evolutionary affin- genera placed by Gosline (1966) in the Percich- ities of the monotypic Niphon within the Per- thyidae. The purposes of this paper are to dis- coidei have been the subject of some debate. cuss the monophyletic integrity of the Serran- Although Jordan (1923) placed Niphon in a idae, to consider certain aspects of serranid in- monotypic family, most authors prior to Gosline trarelationships, and to present evidence that (1966), treated it as a serranid (Berg, 1940; Ka- Niphon spinosus is a primitive member of the tayama, 1959; McCully, 1961; Norman, 1966; serranid subfamily Epinephelinae. Greenwood et al., 1966). In 1966, Gosline removed a number of genera, including Niphon, MATERIALS AND METHODS from the Serranidae, and placed them in the Percichthyidae. Osteological features were studied primarily Rivas and Cook (1968) used a phenetic anal- in specimens cleared and stained for bone and ysis of 22 characters to argue that Niphon is cartilage, but a few specimens were stained only more similar to the Centropomidae than to the for bone. Where specimens were not available Percichthyidae or Serranidae and, therefore, for clearing and staining, certain osteological placed Niphon in the Centropomidae. In their characters were determined from radiographs. comparative analysis, Rivas and Cook consid- Various aspects of soft anatomy were examined ered only one species of centropomid, one per- in whole specimens. cichthyid and no serranids. Greenwood (1977) Cleared and stained specimens of represen- pointed out that because Niphon shares 20 of tative genera from a wide variety of perciform these 22 characters with some serranids, per- families were examined for comparative pur- cichthyids, or both, the similarity indices have poses, including all nominal genera of the Per- little meaning. In addition, Rivas and Cook failed cichthyidae and the serranid subfamilies Ser- to consider that centropomids are variable in raninae and Epinephelinae. Only the most some of the characters that Niphon allegedly pertinent material, that representing the Epi- shares with them. Finally, Greenwood observed nephelinae and the genera herein removed from that Niphon does not exhibit either of the char- the Serranidae, is listed.

? 1983 by the American Society of Ichthyologists and Herpetologists 778 COPEIA, 1983, NO. 3

Fig. 1. Niphonspinosus Cuvier, 480 mm SL, Pusan, Korea (after Lindberg and Krasyukova,1971).

Abbreviations.-GMBL, Grice Marine Biologi- gladifer Robins, USNM 201422, R; Liopropoma cal Laboratory, College of Charleston, Charles- susumi (Jordan and Seale), USNM 218726, C; ton, S.C.; ORI, Ocean Research Institute, Uni- Pikea longilepis (Garman), USNM 153602, R; versity of Tokyo; RUSI,J. L. B. Smith Institute Rainfordia opercularis McCulloch, USNM of Ichthyology, Rhodes University, South Af- 203247, C. Grammistini: Aporops bilinearis rica; USNM, National Museum of Natural His- Schultz, USNM 218920, C; Grammistessexlinea- tory, Smithsonian Institution, Washington, D.C.; tus (Thunberg), USNM 218886, C; Grammistops ZUMT, University Museum, University of To- ocellatus Schultz, USNM 218873, C; Pogonoperca kyo; C, cleared and stained; R, radiographed. punctata (Valenciennes), USNM 205491, R; Pseudogramma polycantha Bleeker, USNM Epinephelinae.-Niphonini: Niphon spinosus Cu- 205491, C; Suttonia lineata Gosline, USNM vier, ZUMT 49162, C; ORI uncat., C; USNM 209705, C. 57737, R. Epinephelini: Anyperodon leucogram- micus(Valenciennes), USNM 218817, C; USNM Incertae sedis.-Dinoperca petersii (Day), RUSI 22729, R; Cromileptes altivelis (Valenciennes), 76-4, C; Hemilutjanus mnacrophthalmus(Tschudi), USNM 183245, R; Epinephelus flavolimbatus USNM 77623, C; Polyprion americanus (Schnei- Poey, GMBL 78-132, C; E. cruentatus (La- der), USNM 39897, R; Stereolepisgigas Ayres, cepede), USNM 218869, C; E. inermis (Valen- SIO 68-382, C. ciennes), USNM 8086, R; E. itajara (Lichten- stein), USNM 133692, R; E. morio DISCUSSION (Valenciennes), GMBL 73-133, R; E. multigut- tatus (Evermann and Radcliffe), USNM 128755, Monophylyofthe Serranidae.-The Serranidae has R; E. niveatus (Valenciennes), GMBL 76-254, C; historically served as a classificatory "wastebas- Gonioplectrushispanus (Cuvier), USNM 24952, ket" within the percoids, providing a conve- R; Gracila albomarginataRandall, USNM 89985, nient pigeonhole for those generalized perch- R; MycteropercaphenaxJordan and Swain, GMBL like fishes whose relationships could not ob- 78-132, C; Paranthias furcifer (Valenciennes), viously be shown to lie with some other percoid USNM 170020, C; Plectropomus maculatus family. Prior to 1966, the monophyly of the (Bloch), USNM 218818, C; Trisotropis dermop- Serranidae was rarely questioned in the litera- terus(Temminck and Schlegel), USNM 177777, ture. Instead, efforts were directed toward sub- R; Variola louti (Forskal), USNM 218820, C. Di- dividing the existing Serranidae into numerous ploprionini: Aulacocephalus temmincki Bleeker, subfamilies, usually with little suggestion as to USNM 64640, R; USNM 22524, R; Belonoperca how these might be interrelated (Jordan and chabanaudi Fowler and Bean, USNM 217837, Eigenmann, 1890; Jordan, 1923; Katayama, C; Diploprion bifasciatum Kuhl and van Hasselt, 1959; McCully, 1961). USNM 218889, C. Liopropomini: Jeboehlkia A major advance in this regard resulted from JOHNSON-NIPHON PHYLOGENETIC RELATIONSHIPS 779

Gosline's (1966) attempt to redefine the limits able (e.g., swimbladder projections), too sub- of the Serranidae. On the basis of several shared jective (e.g., relative length of postpelvic pro- morphological features (most of which are ap- cess; relative .development of Baudelot's parently primitive for the Perciformes) Gosline ligament), or both, to serve as valid phyloge- removed a number of genera and restricted the netic indicators in these groups. Serranidae to three subfamilies, the Serraninae, A few characters warrant discussion. Gosline Anthiinae and Epinephelinae, and suggested pointed out that most serranids have 24 ver- that the Grammistidae forms a specialized ser- tebrae, whereas percichthyids have 25 or more. ranid offshoot. Most of the newly excluded gen- However, anthiines have 26, the serranine era were placed in the Percichthyidae, origi- Acanthistius Gill has 26 and occasional speci- nally erected by Jordan and Eigenmann (1890) mens of other serranids may have 25 or more. for the South American genera PercichthysGi- The phylogenetic significance of vertebral rard and Percilia Girard. The value of Gosline's number within the percoids is difficult to eval- work lies not in his emendation of the Percich- uate. In some groups (e.g., lutjanids, sparids) it thyidae (which is almost certainly a polyphyletic is remarkably constant, whereas in others, there assemblage defined solely on the basis of ple- is considerable intragroup variation, and there siomorphic characters) but in his restriction and is no clear indication as to what might be the redefinition of the Serranidae based on several primitive percoid number. Cases of departure character states that appear to be derived, at from the typical number by only one member least in relation to those of the excluded genera. of a family are also known. Although his survey of these character states Gosline noted that all his excluded genera was cursory and involved a relatively small por- have several trisegmental pterygiophores (those tion of the total number of nominal serranid with separate medial radials) at the posterior genera (for some characters he relied on Ka- portion of the median fins, whereas serranids tayama, 1959, a considerably broader survey), have none, the medial radial apparently having Gosline nevertheless provided us with a testable fused to the proximal radial in all pterygio- hypothesis, i.e., that his Serranidae, "thus shorn phores. His survey of this character in the ser- of its accretions," represents a monophyletic ranids was inadequate, for a number of epi- family. nepheline genera have trisegmental This hypothesis has not been seriously ex- pterygiophores, and grammistines (which he amined to date. Gosline's classification is in gen- considered serranid offshoots) have more than eral use, but there seems to exist considerable most percichthyids. Nor does the configuration doubt concerning the monophyly of the Ser- of the predorsal bones (one to three predorsals, ranidae. For example, Smith (1971), in his def- the last interdigitating between the first and inition of the Serranidae, apparently chose not second neural spines) serve to define the family, to use Gosline's work or his diagnostic charac- because, as Gosline pointed out, the Serraninae ters, even though he cited Gosline's paper. More is an exception, exhibiting the apparently prim- recently Greenwood (1977) referred to "the itive predorsal pattern (three predorsals, the last heterogeneous and aphyletic assemblage of ser- between the second and third neural spines) ranid-percichthyid species." Because of this found in most percichthyids. general state of doubt or confusion, I felt it One of Gosline's reductive characters does would be useful to briefly review the available seem to be consistent with his classification, al- evidence for the definition of the Serranidae as though its significance is lessened by the fact a monophyletic family. In the following discus- that it has probably arisen independently a sion, the terms Serranidae and Percichthyidae number of times in percoid evolution. This is are sensu Gosline (1966). the loss of the small posterior uroneural pair or An ongoing study of lower percoid phylogeny its fusion to the larger anterior pair (Gosline, has led me to reconsider most of the characters 1966: Fig. 10). All of Gosline's serranids have used by Gosline and their bearing on the ser- only one pair of uroneurals whereas most of the ranid-percichthyid problem. Essentially, this excluded genera have two. means that I have examined those characters Johnson (1975) supported Gosline's classifi- in a broader range of genera than did Gosline, cation in reporting that the Serranidae lack a in the Serranidae, the Percichthyidae and sev- procurrent spur and that all but two genera eral other percoid families. I conclude that all (Maccullochella Whitley and Niphon) of the per- but a few of his characters are either too vari- cichthyids examined have a well-developed pro- 780 COPEIA, 1983, NO. 3 current spur. This spur projects ventrally from the base of the posteriormost ventral procurrent caudal ray and is usually accompanied by a basal foreshortening of the preceding procurrent ray. Presence of this condition was in- A terpreted as primitive for the Perciformes, sug- gesting that absence of the spur in the serranids represents a derived condition with respect to the percichthyids. The serranids are not unique, however, in lacking the procurrent spur. Its absence in a number of other percoid families may be the result of independent losses (Johnson, 1975). Another apparently derived character state in serranids is absence of the third preural radial cartilages. In the Percichthyidae and many oth- B x er lower percoid families (including the Cen- C tropomidae, Ambassidae, Apogonidae, Cen- trarchidae, Kyphosidae and Girellidae), a radial Fig. 2. Niphonspinosus (ZUMT 49162), right side. cartilage of variable size lies along the anterior A) Infraorbitalseries. B) Opercle. C) Preopercle. margin of the distal ends of neural and haemal spines of the third preural centrum, just proximal to the bases of the procurrent caudal rays. This cartilage is also found in the Beryciformes, Archoplites Gill and Howella Ogilby where the and its occurrence within the Perciformes seems primary spine has apparently splayed out to to represent the primitive condition. Absence create many smaller spines, a condition in no of this cartilage, here interpreted as the derived way comparable to that of the serranids). The state, characterizes a number of percoid fami- presence of three opercular spines is an uncom- lies, including the Serranidae. Again, it seems mon perciform feature and I know of only one likely that loss of this cartilage has occurred other percoid that exhibits it. The monotypic independently several times. genus SphyraenopsPoey (=ScombrosphyraenaFra- Thus, there are at least three derived reduc- ser and Fourmanoir) has an additional oper- tive character states that are consistent within cular spine below the main spine. This third the Serranidae (absence of a posterior uro- spine is apparently independently derived, as neural, absence of the procurrent spur and ab- Sphyraenops does not exhibit any of the other sence of a third preural radial cartilage). Be- three serranid specializations mentioned above cause none of these apomorphous reductions is but instead shares at least one derived feature unique to serranids, even their co-occurrence with the Epigonidae, rod-like elongation of the here does not represent unequivocal evidence typically biconcave cartilaginous meniscus that for serranid monophyly. There may well be non- lies between the vomer and the maxillary head. serranid perciforms that also have these three Other epigonids have only two opercular spines. structures absent. Nevertheless, their absence One other perciform family, the Trachini- in serranids at least suggests the possibility of dae, has three opercular spines arranged in a descent from an immediate common ancestor fashion similar to that of the Serranidae. This that had lost them and defines the family with is probably an independently derived condition respect to the Percichthyidae. but could indicate a sister group relationship A single, apparently uniquely derived, inno- with the serranids. Future investigations of vative specialization has been identified for the trachinoid fishes should address this question. Serranidae. As noted by Gosline (1966) all ser- Currently, the Trachinidae are placed in the ranids share the presence of an opercular spine suborder Trachinoidei, the other members of below the primary spine, making a total of three which do not possess three opercular spines. spines on the opercle (Fig. 2B). In almost all Gosline (1968) noted several features that other percoids there are only two opercular trachinids share with other members of his su- spines, the primary one and a smaller one above perfamily Trachinoidae (Uranoscopidae, Lep- this (excluding, as did Gosline, such genera as toscopidae and Dactyloscopidae). These fea- JOHNSON-NIPHON PHYLOGENETIC RELATIONSHIPS 781 tures include a specialized ridge on the pelvic sal pterygiophore (Fig. 4), both common per- girdle, a hook-like process on the posterior rim coid features. Supernumerary spines are those of the hyomandibular, firmly connected and ex- which have a secondary or non-serial associa- panded circumorbital bones, and an enlarged tion with the pterygiophore on which they are scapular foramen. Trachinoids also have long borne. Using the formula of Ahlstrom, Butler soft dorsal and anal fins, pelvic fins placed well and Sumida (1976) the pattern is 0/0/0+2/ in advance of pectorals, reduced caudal fin ray 1+ 1/. Within the Anthiinae, Kendall found two counts and dorsally placed eyes. It thus seems patterns-0/0+0/2/1+ 1/ and 0/0/2/1+1/, likely that the three opercular spines of tra- the third predorsal presumably having been lost chinids arose independently of those of serran- in the latter configuration. Kendall considered ids, perhaps in association with the opercular the serranines and anthiines to form one lineage poison gland. within the Serranidae and the epinephelines and The Serranidae may currently be defined, grammistines to form another. then, on the basis of four shared specializations, Although the epinepheline lineage can be 3 reductive and I innovative, the latter offering clearly delineated, as discussed below, limits and the strongest evidence in support of the hy- relationships of the serranine-anthiine line await pothesized monophyly. Gosline noted that the further clarification. The Serraninae cannot be family thus delimited "is restricted to the defined on the basis of the predorsal pattern subfamilies Serraninae, Epinephelinae, and An- alone since this pattern is shared by many lower thiinae (except Callanthias), of Jordan and Ei- percoids. The two patterns seen within the An- genmann (1890)." This statement is somewhat thiinae are probably derived with respect to that misleading because Jordan and Eigenmann in- of the serranines; however, McCully (1961) cluded in their Epinephelinae Polyprion Oken showed that although most genera now placed and StereolepisAyres, two genera which Gosline within the Anthiinae share a unique scale mor- correctly excluded from the Serranidae. Hemi- phology, some have scales that are quite similar lutjanus Bleeker, also considered an epinephe- to those of the Serraninae. Additional morpho- line by Jordan and Eigenmann, and Dinoperca logical investigations will be required to resolve Boulenger (=Centrarchops Fowler), treated as a the limits of these two subfamilies. serranid by most authors, should also be ex- More pertinent to the problem at hand (the cluded. The affinities of these four genera are placement of Niphon) is the other line of diver- unclear, but none possess any of the four spe- gence, the epinepheline-grammistine lineage, cializations diagnostic of the Serranidae. which Kendall defined by loss of the posterior The classification of Jordan and Eigenmann predorsal and of the first dorsal spine. All mem- (1890) is clearly outdated and includes only Eu- bers of this group have no more than two pre- ropean and American genera; a complete al- dorsals and bear no more than one supernu- location of genera to the Serranidae and an merary spine on the first dorsal pterygiophore understanding of their interrelationships can (Figs. 3, 5). Thus, the epinephelines (of Jordan come only with a worldwide revision of the fam- and Eigenmann), the grammistids, the liopro- ily, an undertaking not likely to be realized in pomines (including Rainfordia) and the pseu- the near future. Despite this, elaboration of cer- dogrammids were regarded as constituting a tain aspects of serranid intrarelationships is war- monophyletic group. Actually, neither loss of ranted and will help to clarify my placement of the third predorsal (also absent in anthiines) nor Niphon. loss of the first dorsal spine is unique among percoids, and the shared absence of both struc- Serranid intrarelationships.--The most recent tures does not categorically demonstrate mon- analysis of serranid intrarelationships is that of ophyly. Although I concur with Kendall's treat- Kendall (1976), based on a single character ment of this lineage as monophyletic, I base this complex, the predorsals and associated bones conclusion on an additional synapomorphy, a (Fig. 3). Kendall agreed that Jordan and Eigen- unique modification of the first dorsal pteryg- mann's three subfamilies are valid; he combined iophore. the liopropomines and the grammistids and In his characterization of the epinepheline- pseudogrammids of Gosline (1960) as a fourth grammistine lineage, Kendall noted that the serranid subfamily, the Grammistinae. grammistines have the additional specialization Serranines have three predorsal bones and of a uniquely shaped first dorsal pterygiophore bear two supernumerary spines on the first dor- (Fig. 3). He suggested that the thin, elongate 782 COPEIA, 1983, NO. 3

Pseudogramnma Rainfordia

tossofRt precorsals

predorsal

Anthias loss of anterior loss of posterior dorsal spine predorsal

Grammistinae Grammistes

changein characterof first pterygiophore D Epinephelus Plectranth Epinephelinae

loss of posterior predorsal change in position of Aulacocephalus posterior predorsal loss of anterior dorsal spine Hp ectS Serraninae HypoPogonopletruserc

Pogonoperca Fig. 3. Scheme of evolutionary relationships in some serranid fishes based on predorsal and associated bones (Kendall, 1976: Fig. 1). Predorsalbones solid; first pterygiophore stippled;second pterygiophore and its serially associatedspine solid. Presence or absence of skin toxin grammistinindicated by + or - in those taxa examined for it.

grammistine pterygiophore was probably relat- tal element (Fig. 7B, C). This element has either ed to the support of the flexibly elongated sec- been lost or fused to the posterior portion of ond or second and third dorsal spines which are the proximal-medial element. The typical per- characteristic of the larvae. Larvae of the less coid condition is shown in Fig. 8A. The config- specialized epinephelines, the groupers, also uration of the posterior portion of this modified have a greatly elongated second dorsal spine pterygiophore resembles that of a distal ele- (Fig. 6), although the general appearance of the ment in having a small hook-like process that first pterygiophore in these fishes is not partic- projects through the foramen in the base of the ularly unusual. serially corresponding spine, a condition that On further examination, I have found that supports the hypothesis of fusion of the distal the first dorsal pterygiophore of all members of element rather than its loss. There is, however, Kendall's epinepheline-grammistine line is no evidence of ontogenetic fusion (Fig. 6), and uniquely modified in having no autogenous dis- in Kendall's more primitive epinephelines, the JOHNSON-NIPHON PHYLOGENETIC RELATIONSHIPS 783

dorsal spines

Sdistal radials dorsal spines distal radials predorsals

predorsals proximal- proximal- medial . V mediai radials rodials ' . neurocranium

neural spines neural spines Fig. 4. Centropristisstriata (GMBL 72-417), right Fig. 6. Predorsal bones (cartilaginous)and ante- side. Predorsal bones and anterior dorsal pterygio- rior dorsalpterygiophores (first two ossified)of larval phores. Epinephelussp. (8 mm SL), right side. Second dorsal spine extends to three times length shown. close approximation of the first and second pterygiophores relative to those remaining would valid, his analysis of relationships within the lin- seem to indicate loss of the distal element, or eage is less convincing, particularly his place- at least extreme reduction prior to fusion. In ment of the genus Pogonoperca (Fig. 3). This any case, whether lost or fused, the absence of analysis involved only characters directly asso- an autogenous distal element and associated ciated with the predorsal-dorsal pterygiophore modification of the first dorsal pterygiophore is complex.These characters are, in every case, a specialization unique to the epinepheline- reductive ones associated with a complex which grammistine lineage, one undoubtedly related had already undergone considerable reduction to support of the extremely elongate spine in at the base of the lineage. Given the possible the larvae. It probably serves no special function instability of such a complex it would seem that in the juvenile or adult. continued reductions and losses of component Whereas Kendall's delineation of a mono- elements might be likely to occur independently phyletic epinepheline-grammistine line appears within the group and thus should not necessar- ily be used as the sole transformation series on which to base a phylogeny. Consideration of additional morphological features indicates that dorsal spines the component genera of Kendall's epinepheline-grammistine lineage (hereafter treated as distal radials subfamily Epinephelinae) can be assigned to one of several ostensibly monophyletic tribes (Table

predorsats

proximal-,

radialse s

A B C neural spines Fig. 5. Mycteropercaphenax (GMBL 78-132), right Fig. 7. First dorsal pterygiophore, spines re- side. Predorsal bones and anterior dorsal pterygio- moved. A) Centropristis striata (note free distal). B) phores. Niphon spinosus. C) Mycteropercaphenax. 784 COPEIA, 1983, NO. 3

TABLE1. ALLOCATIONOF GENERATO TRIBESOF SUBFAMILYEPINEPHELINAE.

Niphonini -Niphon Cuvier and Valenciennes Epinephelini -Anyperodon Gunther; CromileptesSwainson; Epinephelus* Bloch; GonioplectrusGill; Gracila Randall;Mycteroperca Gill; ParanthiasGuichenot; Plectropomus Oken; "Trisotropis"dermopte- rus** (Temminck and Schlegel); VariolaSwainson. Diploprionini -AulacocephalusTemminck and Schlegel;Diploprion Kuhl and van Hasselt;Belonoperca Fowler and Bean. Liopropomini -Jeboehlkia Robins;Liopropoma Gill; PikeaSteindachner; Rainfordia McCulloch. Grammistini -Aporops Schultz;Grammistes Bloch and Schneider;Grammistops Schultz; Pogonoperca Gunther; PseudogrammaBleeker; RypticusCuvier; Suttonia Smith. * Including subgenera Epinephelus, Promicrops,Cephalopholis, Dermatolepis and Alphestes after Smith (1971). ** This Japanese species is currently the only one referred to TrisotropisGill, which is a junior synonym of Mycteroprca (type species guttatus = Schneider venenosa Linnaeus). Examination of specimens of this species indicates that it is a distinct genus, and should therefore be renamed.

1) and suggests an alternate hypothesis regard- position of the third predorsal. The presence ing the placement of Pogonoperca. of this "third predorsal" led Kendall to treat In Kendall's scheme (Fig. 3), the epinepheline Pogonoperca as the most primitive member of lineage is composed of two subfamilial group- this lineage (and thus well separated from his ings, Epinephelinae* [Hereafter all subfamilial Grammistinae*). Because Pogonopercapossesses categories followed by an asterisk are sensu grammistin, this scheme would require that the Kendall. Subfamilial and tribal categories not toxin was present primitively, and was second- so marked refer to the proposed classification arily lost in the Epinephelinae* while being re- (Table 1).] and Grammistinae* (the latter in- tained in Aulacocephalus, Diploprion and the cluding liopropomines and pseudogrammids). Grammistinae*. This conclusion is untenable Three of the genera he examined, Pogonoperca, when additional characters are considered, for Diploprion and Aulacocephalus(representative of it is clear that Pogonoperca is a member of the itself and Diploprion in Kendall's diagram) were more specialized Grammistini. It shares with all not included in either subfamily, but were placed other members of that tribe a nasal rosette with as early offshoots on the line leading to these a single row of longitudinally oriented lamellae, two groups. Kendall cited as a hallmark of the specialized preopercular spine configuration, grammistine* line the thin and elongate char- loss of articulation between the third and fourth acter of the first dorsal pterygiophore (in other dorsal pterygiophores, reduced number of pro- serranids it is relatively stout). The absence of current rays and increased number of triseg- this uniquely modified pterygiophore, the ab- mental pterygiophores in the median fins. In sence of a highly modified nasal rosette, and the addition, it shares with the grammistine genera higher dorsal spine number led Kendall to ex- Rypticus, Grammistesand Grammistops,modified clude Aulacocephalus and Diploprion from the cycloid scales (McCully, 1961) and the presence Grammistinae* despite their possession of the of the toxin grammistin not only in the epider- skin toxin grammistin. These two genera, to- mis (as in the Diploprionini) but also in flask- gether with Belonoperca(not considered by Ken- shaped dermal glands (Randall et al., 1971). dall) are here considered to comprise the mono- Biochemically, the grammistin of Pogonopercais phyletic Diplopronini, based on their common more like that of Grammistesthan that of Au- possession of rugose areas on the neurocranium lacocephalusor Diploprion (Oshima et al., 1974). and infraorbitals and a unique scale type (de- Finally, Pogonoperca exhibits the grammistine scribed by McCully, 1961, for Aulacocephalus hallmark, a thin elongate first dorsal pterygio- and Diploprion). phore. The evidence clearly indicates that Po- A major discrepancy in Kendall's scheme is gonoperca cannot be placed at the base of Ken- his placement of Pogonoperca. As noted earlier, dall's epinepheline-grammistine* line, but the epinepheline-grammistine* lineage is char- belongs in the well-defined tribe Grammistini. acterized by the absence of the third predorsal. The third predorsal is most parsimoniously in- The exception is the genus Pogonoperca,in which terpreted as secondarily acquired. there is a small nubbin of bone in the usual Kendall considered Liopropoma(includingJe- JOHNSON-NIPHON PHYLOGENETIC RELATIONSHIPS 785 boehlkia and Flagelloserranus), Pikea (not shown hypurals 35-5 in his and to be re- diagram) Rainfordia closely epurals lated and placed them as what might be considered the sister group of his remaining gram- uroneural mistines*. This seems reasonable because these neural genera (tribe Liopropomini) share a distinctive spines scale type (McCully, 1961), a hook-like exten- rostyle sion of the posteroventral corner of the max- preural centrum 2 illary and a subocular shelf extending from more than one infraorbital. The Liopropomini share with the Grammistini an elongate nasal rosette, thin curved first dorsal pterygiophore and reduced number (1-3) of pyloric caeca. Although synapomorphies of adult Epine- phelini have not been identified, monophyly of this tribe is evidenced in the unique larval type shared by the component genera. All larval Epi- nephelini are characterized by robust serrations haemrnalspines on the elongate second dorsal, pelvic and preopercular spines and a distinctive pigment spot parahypural on the caudal peduncle (Kendall, 1979;Johnson radial cartilages and Keener, in press). A complete phylogenetic analysis of the hypurals 1-2 subfamily Epinephelinae is beyond the scope of Fig. 8. Caudalskeleton of Niphonspinosus (ZUMT this For reasons discussed above, I believe study. 49162), right side. the classification proposed here represents an improvement over the existing scheme based on available evidence. In addition, it provides a clear and readily testable hypothesis. Justifi- cation for the single remaining tribe, Niphon- believed that Niphon would probably eventually ini, is discussed below. be shown to be closely related to some, if not all, of Gosline's percichthyids. Greenwood was The relationships of Niphon.-It is apparently a apparently also misled by his interpretation of misunderstanding of the limits of the Serrani- the caudal skeleton. He reported that Niphon dae and its monophyly that has resulted in the has two uroneurals and thus concluded that its confusion associated with the relationships of "caudal skeleton is virtually identical with that N. spinosus. in the percichthyids" he had examined (all ser- The phenetic approaches of both Gosline ranids have only one uroneural). However, as (1966) and Rivas and Cook (1968) led them to Greenwood himself noted, these "two uro- dismiss the significance of the unique special- neurals" are fused basally, and thus, I believe, ization shared by Niphon and the serranids (three should be interpreted as one. There is no reason opercular spines). Gosline argued that Niphon to believe that the distal processes on the uro- could not be a serranid because, unlike all other neural actually represent remnants of two uro- serranids, it has a serrated lacrimal. This au- neurals. One specimen I examined (Fig. 8) tapomorphic feature, however, does not pre- showed two of these processes on one side and clude serranid affinities. Rivas and Cook, on the three on the other. They are most likely sec- other hand, were more concerned with the ondary in origin. overall similarity of Niphon to centropomids Niphon possesses all four derived characters based on a subjectively chosen suite of charac- that are diagnostic of the Serranidae. Besides ters, most of which are primitive ones and none the three opercular spines (Fig. 2) and single of which is unique to the centropomids. uroneural, the procurrent spur is absent, and Greenwood's (1977) failure to recognize the there are no radial cartilages anterior to the serranid affinities of Niphon clearly resulted not third preural neural and haemal spines (Fig. 8). from his methodology, but from his reluctance On this basis alone, there is good reason for the to accept the monophyly of the Serranidae. He placement of Niphon within the Serranidae. In 786 COPEIA, 1983, NO. 3

distal radials other serranid. Niphon also differs from other dorsal spines serranids in having an unusual dorsal fin count (XIII, 11), a higher vertebral number (30 vs 24-26), a serrated lacrimal and an enlarged pre- predorsals opercular spine (characteristic of many percoid larvae, including those of the Epinephelini, but uncommon in adults). These character states could be primitive ones, but this does not seem likely because the affinities of Niphon lie with the and the more proximaneural spines specialized Epinephelinae, primitive Serraninae do not possess them. As autapomorphies, these characters support the monophyly of the monotypic tribe Niphonini. Absences of the third supernumerary spine and neural spines the third predorsal bone in the remaining epi- tribes unites them as a Fig. 9. Niphonspinosus (ZUMT 4916), right side. nepheline monophyletic in these two fea- Predorsalbones and anterior dorsal pterygiophores. group. Niphon, being primitive tures, is hypothesized to be the sister group of all other epinephelines. Corroborative evidence for this hypothesis could be provided through identification of the larva of N. spinosus, to date addition, Niphon shares the uniquely modified unknown. This evidence relates to the pres- first dorsal pterygiophore of the serranid ence, in Niphon, of two supernumerary spines subfamily Epinephelinae. As illustrated in Fig. on the first dorsal pterygiophore. If the rela- 7B, this pterygiophore has no autogenous distal tionships of Niphon (and the function of the element and its posterior portion bears a small modified first dorsal pterygiophore) are as pos- process that projects through the foramen in tulated, its larva should have an elongate dorsal the base of the serially corresponding spine. It spine as do other epinepheline larvae. However, will be noted that in Niphon (Fig. 9), the spine other epinephelines always have the first or sec- that has serial correspondence with the first ond spine elongate, whereas in Niphon these dorsal pterygiophore is the third rather than first two spines are supernumerary and should the second. This is because the first pterygio- not be produced. The larva of N. spinosus, then, phore bears two (rather than one) supernu- should have an elongate third dorsal spine. merary spines. In the Epinephelini there is only one supernumerary spine and in some genera ACKNOWLEDGMENTS of the more specialized epinepheline tribes (e.g., the Grammistini) there are none. In these cases Thanks are due the following individuals and the serially corresponding spine of the first dor- their institutions for the loan of specimens: To- sal pterygiophore (the one which is strongly kiharu Abe (ZUMT); William D. Anderson produced in the larvae) is the second or first (GMBL); Phillip C. Heemstra (RUSI); Muneo respectively. Because two supernumerary spines Okiyama (ORI); Victor G. Springer (USNM). is the most common percoid condition, and is For reading and criticizing the manuscript, I found in other serranid subfamilies, Niphon ap- thank William D. Anderson, P. Humphrey pears to be primitive in this feature with respect Greenwood, Arthur W. Kendall, Richard H. to the other epinephelines. An additional (al- Rosenblatt, Sally Richardson and Victor G. though not unique) specialization that Niphon Springer. Karen Swanson prepared the final il- shares with the epinephelines is the presence of lustrations. only two predorsal bones. Here again, the ro- The major portion of this study was com- bust nature of these two bones is a primitive pleted during a Postdoctoral Fellowship at the condition. The other epinephelines have con- Smithsonian Institution, Washington, DC. Spe- siderably reduced predorsals (Figs. 3, 5). cial thanks go to Victor G. Springer for his en- Niphon differs from other serranids in several couragement, hospitality and many valuable respects (presumably autapomorphies of the ge- discussions during my stay there. South Caro- nus). The predorsal pattern (0+0/2/1/1/) is lina Wildlife and Marine Resource Department unusual for percoids and is unlike that of any Contribution 151. JOHNSON-NIPHON PHYLOGENETIC RELATIONSHIPS 787

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