Phylogeny of the flyingfish family Exocoetidae (Teleostei, Beloniformes) J u a n i t o C. D a s i l a o , Jr. ~ & K u n i o S a s a k i : ; Uni&'d Graduate School '7I. Igric'uhur<'l Science.s'. Ehime Univc'z:s'itv. 3--5-7 ~,rumi. .~,{atsmama. Ehhne 790-0905..&pan Pre.~'enl addre.sx: Uso tturine BioicNical hTxtitute, Kochi I_,.nivervitv. Tosa. lnoshiri. K, chi 7,S1- I 164..]apan (e-mail: da>ilao~g:cc.,tochi-,.ac.ip) : l)ep{wtment ,?lHir Fcw,dLv r l~Tchi ('nil'cn~'im,. 2-5- I tk~,tv)no-cho. IQ)chi L~O-,h'520.Jopan

(Rcceixed 2" l)t'cemher 1997: in revised torm 21 .ttmi1199,~: acceptcd 23 April 19970

Ichthyological Research '

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Dasilao, Jr.. J. {2'. :rod K. Sasaki. 1998. Ph,,Iogeny of the flyingfish liimilv Exocoetidac (Fcleostei, Beloniformes). lchthyol. Res., 45 141:34 7 353. A.listract

The phylogeny of the flyingfish family Exocoetidae is studied cladistically.

using 41 morphological ch:lracters encompassing early life history, and external and internal features. The monophyl> of tile Iamily is supported b> 10 s.,,napomorphics. Within the family. ().tTpr is the sister group to all other genera, the monophyly o( the lauer being defined by 10 :,>napoinorphies. t:bdialor is the sister group of genera characteriTed b,, the presence of" chin barhcls in juveniles. Parex<~c<)cnt~ is the sister group of Kvoc'oetu.~. ()pxelur,l~. Prognict~ttns and ttir,r the latter being defined by four synapoinorphics. In the latter group. /:vocoetu.v is the sister group of the other three genera. lhe ph.,,Iogen.v of the Exococtidac is characterized b.,, the stepw ise upgrading of gliding capability, ~.ith sequential modifications of the caudal, pectc)r,ll and pclx ic lins. lhe sub(amily Oxyporhamphinae is resurrected. Key word~. 9 [-xocoetidac: phylogeny: morpholog.v.

he cladistic analysis and subsequent redefinition of the flvinefish family Kxocoetidae by C'ollette et al. 11984) considered intergeneric relationships based mainly on early life history' and external characteristics. Follm~ing examination of the caudal complex. Dasilao et al. (199 "} argued that the "hemiramphid'" O.'g7>orhamphtt,v (Collette et al.. 1984) was an exocoetid, having a sister relationship ~ith the other genera in the family. A subsequent anatomical study of the Exocoetidae revealed further useful osteological and myological characters enabling a reevaluation of previous views on exocoetid phylogeny. Except tbr the inclusion of O.w'porhamphus in the Exocoetidae. the combined character set of Collette et al. (1984) and this paper generally strengthens the phylogenetic hypothesis of the former. The purpose of this paper is to describe and discuss exocoetid characters additional to those in Collette et al. (1984). Materials examined were as listed in Dasilao et al. (1997), plus two examples of bbdiator ac'ultt,5 (['xocoetidael; C/kS (California Acadernv of Sciences} 39810. 131 mm SI.. CAS 3981 I, 120ram SL. To substantiate the treatment of O.D'porllamphus as an exocoetid. Hemiramphidae tsensu Dasilao et al., 1997)

T

was also included in the ingroup. Following the cladogram in Co[lettc et al. (1984L the outgroup was the Scomberesocoidea (Scomberesocidae plus Belonidae), being the sister group of the Exocoetoidea (I-lemmunphidae plus Exocoetidae). The data matrix (Table 1) was run on PAUP version 3.Or (Sx~oflbrd. t991 ).

Results Figure I shov, s the single shortest tree obtained from Table I v,.'ith length 41 steps (C.I.=0.88, R.l.=0.91 ). when five unique autapomorphic characters (Characters 37-41. see below) were omitted. Evolutionary interpretations of two characters (Characters 35 and 36) differed owing to the optimization options used (DELTRAN and ACCTRAN). Characters common to Nodes A - G in the w,o options are shown in Figure 1 and listed first. Collette et al. (1984) defined Node A (as the Exococtoidea) by: (I) third pair of tipper pharyngeal bones united into a plate: (2) t\~urth tipper pharyngeal bone lost: (3} postorbital section of cephalic lateralis

348

J.C.

Dasilao, Jr. & K. Sasaki

Fig. 1. Cladogram of the families Hemiramphidae and Exocoetidae INode B). Numbers following each node are characters supporting that node (see text for character descriptions/. The character marked by R is a reversal to the primitive condition. Only characters common to Nodes A43 in ACCTRAN and DE[.,TRAN options are shown. Autapomorphies of terminal taxa are also omitted. Drawings of fishes from Bruun (1935).

system lost; (4) secondary bony canals of cephalic lateralis system lost. Node B is the Exocoetidae of Dasilao et al. (19~7), defined by 10 synapomorphies: (5) neural spines o1' preural vertebrae broader than haemal spines: (6) spur present on posterior margin of neural spree of preural vertebra 2; (7) upper hypural plate steeply angled; (8~ lower hypural plate strongly extended poste-

riorly: (9) lower hypural plate deeply surrounded by caudal fin rays; (10) flexor ventralis well developed; (1 I) llexor ventralis externus well developed: (I 2) adductor dorsalis well developed: (13)lower jan. of adults not elongated; (14) premaxilla with a straight anterior margin. Although Collette et al. (1984) defined Node C (as the Exocoetidae) by six synapomorphies, two of these

Phylogeny

of E x o c o e t i d a e

349

Fig. 2. Dorsal (l@) and posterior views (right) o( crania of two exocoetids \ ) O.DT)orhamphu.s microt)tc'ru.s" micropteru.s': B) Pare.'eocoetux mento menlo BOC--basioccipital: B O ( ' P - b a s i o c c i p i t a l process; E--ethmoid: ECA.--ethmoid cartilage: EO--epiotic: EOC--exoccipital: EOCC-.exoccipital condyle: EOCP--.exoccipita[ process: F--fronlal: F.'vl--l'oramen magnum: LE-.lateral ethmoid: N--.nasal: PTO--. pterotic: SOC--supraoccipital; SP- .sphenotic. [Bar= 10 ram.

(13, 14) o c c u r r e d at N o d e B. T h e r e m a i n i n g characters included: (151 s w i m b l a d d e r e x t e n d i n g into haemal canal: (16) pectoral fins long: (17) pectoral fins form last; (18) preanaI fin told reduced. N o d e C is further s u p p o r t e d by additional six s y n a p o m o r phies. 19. Basioccipital process a b s e n t . - In the outgroup, h e m i r a m p h i d s and Oxyporhamphus, a p r o m i n e n t posterior process, which serves as the attach-

Table 1. Characters Scomberesocoidea Hemiramphidae

Ox)Torhamphus Fudiazor Parexocoetus Exocoetus Prognichthy.s Himmdichtt(vs Q~Tselurus

m e n t site o f Baudelot's l i g a m e n t , is present on the basioccipital ( 0 = p r i m i t i v e ) (Fig. 2A), but is a b s e n t in other exocoetids ( l = d e r i v e d ) (Fig. 2B).

20. Adductor super/icialis well developed.---In tile o u t g r o u p , h e m i r a m p h i d s a n d Oxyporhamphus, the a d d u c t o r supcrficialis is poorly d e v e l o p e d (0) (Fig. 3B). In other exocoetids, however, the m u s c l e is well developed, f'unctioning to " c l o s e " the large pectoral fins ( l ) (Fig. 3D, E G). A large s e m i c i r c u l a r projec-

Data matrix used in phylogenetic analysis ofexocoetids

1-5

6-10

I 1-15

16-20

21-25

26--30

31-35

36-40

00000 1 l 1t 0 I 11 I I 111 I 1 l I t 11 I I 11 I 1l 1I 1 l l 111 !l i t l

00000 00000 l l 1l l 11111 1111 I I 1 III 111 l I I 1 l 11 I I l 1l

00000 00000 I 1110 I I 1I t 111 l 1 11 l I 1 11 I I 1 l 1I I I l 1I 1l

00000 O00OO 00000 1I l i 1 111 I 1 11 I 11 11111 111 I I 1I I 1l

00000 00000 00000 I 1 ] 10 11 I 11 I I I 1I 11110 I 11 I0 1I 1I 1

00000 00000 00000 00000 00000 11111 I 1 110 I 1I I I ! 11 I I

00000 00010 O00lO 00000 00001 0000l I 1100 I 1100 I i 100

00000 00000 00000 00000 00111 11000 000t)0 10000 00000

0 0 0 0 1 0 0 0 0

350

J.C. Dasilao, Jr. & K. Sasaki

Fig. 3. Pectoral girdles and associated muscles of three exocoetids. AL B}. E/Oxk_,porha,,phus microprerus microprerus: CL D). G~ Hirundichthvs a~nis: F} Parexocoems memo memo. A~, C), E)-G) lateral view: B j, D) medial wew. A B P a b d u c t o r prof'undus: ABS--abductor supevficialis: ADP--adductor profundus: ADS-adductor superficialis: ARRD---arrector dorsalis: ARRV--arrector ventralis: CL---cteithrum: CL-EOCC--cteithrum- exoccipital condyle: COR coracoid: K k e e l : PRP--protractor pectoralis: PT posttemporal: R radials: SC--scapula: SCL supracleithrum: SrH--sternohyoideus: VF--ventral fenestra. Bar= 10 mm

tion on the dorsal portion of the cleithrum serves as the muscle attachment site. 21. Adductor pr@mdus well developed. The adductor profundus, which functions together with the adductor superficialis, is weakly developed and restricted to the dorsal half of the pectoral girdle in the outgroup, hemiramphids and Ox?porhamphus (0) (Fig. 3B). whereas in other exocoetids it is well developed and occupies the dorsal two thirds (1) (Fig. 3D). 22. lnterradialis gap absent. Although a narrow rounded gap occurs between the radials in O.ryporhamphus as in the outgroup and hemiramphids (0) (Fig. 3E). such is lost in other exocoetids (1) (Fig. 3E G~ owing to the formation o f a single stiffplate by the radials, thereby supporting the large pectoral fins. 23~ Restricted insertion of promactor pectoralis. - The insertion o f the protractor pectoralis extends close to the middle portion of the cleithrum in the outgroup, hemiramphids and O~,porhamphus {0) (Fig. 3A), but is restricted to the dorsal portion in other exocoetids ( 1 ) (Fig. 3C).

24. H.vpurals 3 + 4 and 5jitsed. In the outgroup, hemiramphids and Oxyporharnphus, hypural 5 is separated from hypurals 3 + 4 (0) (Dasilao et al.. 1997: fig. 2C). In other exocoerids, hypurals 3 + 4 and 5 are fused together forming a single plate (1) (fig. 2D). thereby increasing the support of the upper caudal fin lobe. Collette et al. (1984) defined Node D by the presence o f barbels on the lower j a w in juveniles (25). Although Prognichthys and Hirundichthvs do not develop such barbels (Kovalevskaya, 1982: Chen, 1988). their seconda W toss at Node G is the most parsimonious interpretanon. Collette et al. (1984) defined Node E by three characters: (26) pectoral lateral line branch lost: (27) beak lost in juveniles: (28) pectoral fin greatly enlarged. The following two characters further strengthen Node E. 29. Opetcle pointed dorsally. In the outgroup, hemiramphids and some exocoetids, the dorsal margin o f the opercle is gently rounded (0) (Fig. 4A),

P h y l o g e n y of Exocoetidae

351

Fig. 4. Lateral view ofcranial-opercular muscles (lr suspensoria and opercular apparatus fig/? and right) of two exococtids. ,,\) O.r micropteruv microt)teru.~; 13) flir~tndichthvs q//mis. ,,I 1 +2--sections of adductor mandibulac: :I,.tP--adductor arcus palatini: DO--.-dilatator operculi: ENr--r I-F4.V .epaxial muscle- H}O---hyomandibular: IOP--interopercle: L:lP--levator arcu,,, palatini; LO.----levator opercull; L/'--.ligamentum primordium: .~lET" -metapterygoid: OP--opercle: P.41.--palatine: POP--preoperclc: Q(,A ~:tuadrate, SOP..-subopercle: 5FM-. symplectic. Bar= I 0 ram.

whereas in Exocoems, Prognichthys, Hirundichthvs and Qvp.selurus, it is acutely pointed (I) (Fig. 4B). 30. Ppw~percle extending to ~h~twal mar~in :("hvomandihulap: --- This condition was found in s tus, Hirundichthvs and Cvpselurus (I) (Fig. 4B), but was absent in the outgroup, hemiramphids and some exocoetids (0) IFig. 4Ai. Absence of the derived condition in Prognichthys was considered a reversal. Collette et al. (19841 defined Node F (as the subfamily Cypselurinae) by two characters: 131l pelvic fin long; (32) swimbladder extending well into haemal canal. An additional character is presented below. 33. Attachment o/supracleithrum close to mMdle portion O ( p o s t t e m p o r a l . - In the outgroup, henriramphids and some cxocoetids, the supracleithrum is attached to the ventral portion of the posttemporal (O) (Fig. 3A~, compared with its attachment close to the middle portion of the latter in Prognichth.t's, Hirundichthvs and Qvpselurus 11) (Fig. 3C). Collette ct al. /1984) did not infer relationships

within tile Cypselurinae (Node G). A sister relationship between Prognichthy,~ and ttirundichthvs is hypothesized here owing to their shared reversal of Character 25 (denved-+primitive) at Node E The following two characters were open to interpretation according to the optimization options applied. 34. Third pair o f upper phatTngeal hones ./used. --. In the outgroup and most exocoetids, the right and left bones are united but not fused (0) (Dasilao et al.. 1997: fig. 4C), whereas they are fused in the Hemiramphidae (fig. 4A) and Oxvporhamphux {fig. 4B) (I). A.hhough Collette et al. (1984) placed the latter in the Hemiramphidae because of the shared fused condition, this move was rejected by Dasilao et al. (1997) and this study. DELTRAN interpreted the fusion as parallel development, whereas ACCTRAN favored the fusion as occurring at Node A, being secondarily separated at Node C. As discussed by Dasilao et al. (1997), we consider parallel attainment as the rnore likely, since the fusion pattern differs signif

352

J.C. Dasilao, Jr. & K. Sasaki

Fig. 5. Lateralxiew of upper jaw bones of two exocoetids showing with ethmo-pre;omerine region of cranium (right). ,,\) (_)7)selurus agoo a goo: B). C) Pare.rocoems mento mento. .4P-ascending process: EC4-ethmoid cartilage: .14.-.maxilla: MCC--.-maxit!o-cranial condyle: MC'C..t---maxillo-cranial cartilage: MH.-maxitla~ head: N---nasal: R-1L-.--palatine: PM--premaxilla: PMP--.postmaxillary process: P/,~prevomer: QUA.--quadrate. Bar=Store.

icantly between ttemiramphidae and Oxvporhamphtts. In any case. inclusion of Oxvporhamphus in the Hemiramphidae results in paraphyly of the Exocoetidae. 35. Maxillo-cranial cartit~Ne present. - - In Parexocoetus and Exocoems, the maxillary cranial condyle is connected with the ethmoid cartilage of the cranium by' a short tubular cartilage (11 (Fig. 5B, C). Such a cartilage is absent in the outgroup, hemiramphids and other exocoetids, the condyle articulating directly with the cranium (0) (Fig. 5A). tn the former genera, the cartilage is directed upward when the jaws are closed, but swings forw'ard when the latter are protruded, owing to the forward displacement of the maxillary head. The degree of protrusion is slight in Exocoetus. In the DELTRAN tree, the cartilage was deduced as having been independently obtained in the two genera. Howe'~er, in the ACCTRAN tree, it appeared as a synapomorphy at Node D. being secondarily lost at Node E The following character was considered to represent parallel development. 36. Levator operculi extended lawralh'. --- In most

exocoetids, the levator operculi is inserted onto the medial surface of the preopercle (0) (Fig. 4A.), as in the outgroup and hemiramphids. However, in Exocoetus and Hirundichthvs the muscle extends to the lateral surface (1) (Fig. 4B). The following five characters are unique autapomorphies. 37. Egg filaments l o s s . - - C o l l e t t e et al. (1984) characterized E.roc,mtus by the loss of egg filaments, such being supported by the outgroup comparison. ?8. Premaxilta with a long ascending p r o c e s s . - -

In the outgroup, hemiramphids and most exocoetids, the ascending process of the premaxilla is barely apparent (0) (Fig. 5A). whereas in Parexocoems the process is prominent (l/ (Fig. 5B). serving as a bar sliding against the concave dorsal surface of the ethmoid cartilage (Fig. 2B) during protrusion. 39. Premaxilla with a postmaxillar): process. - - In

the outgroup, hemiramphids and most exocoetids, a postmaxillary process is absent on the premaxilla (0) (Fig. 5A), whereas it is present in Parexocoetus (1) (Fig. 5B), serving as a sliding guide during protrusion.

353

P h y l o g e n y of Exocoetidae

40. Maxilla sickle-shaped posteriorly - - In the outgroup, hemiramphids and most exocoetids, the maxilla is broad posteriorly' t0t (Fig. 5A), whereas it is sickle-shaped in Pare.vocoetus (I) (Fig. 5B). 4l. Exoccipital articulating directh' with cleit h r u m . - In the outgroup, herniramphids and most exocoetids, the exoccipital does not possess a process for direct articulation with the cleithrum (0) (Fig. 2A). However, in Parexocoetus, such a process is present ( 1) (Fig. 2By, articulating directl;' v,,ith a condyle on the dorsal surface of the cteithrum (Fig. 3F).

Discussion The phylogeny of the Exocoetidae is characterized by the stepwise upgrading of gliding capability (Fig. 1). Structural rigidity ,,,,as initially established at the caudal complex, thereby, increasing the propelling force of the caudal fin at the momcnt of take-off (Node By. The next step ",~.as the improvcrnent in stability after take-ofl~ accomplished bv the developn|ent of large pectoral fins with well-developed related muscles (Node C). Follov.ing the acquisition of greatly.' enlarged pectoral fins (Node El. the pelvic tins subsequently became enlarged, thus improving pitching (tbre and aft) stability (see Davenport, 1992. for functions) (Node F). Initial upgrading of the caudal complex is t\mctionally rational, because without take-off, long pectoral (and pelvic) fins would be of no value lbr gliding. We did not assume the cladogram to sirnply reflect gliding function, with the abo,,e discussion being tautological since the characters applied are related to function. In fact. /he gliding-related characters described are good indicators of exocoetid interrelationships because of their high congruency with other characters. At Node B. eight caudal complex characters are congruent with two oral jaw characters. At Node C, five pectoral fin characters are consistent with early life history and cranial characters. Similarly, at Nodes E and E pectoral and pelvic fin characters are accompanied by non-gliding-related characters, such as the shape of the opercle, respectively. Hence, v,'e consider each respective improvement in gliding capability as a unique event in exocoetid evolution. Parerocoems is unique m having strongly' protrusive jaws. the premaxilla, with its distinct ascending and postmaxillary processes, structurally endorsing such an action. Pare.w)coetu.~ is also unique m having a process on the exoccipital for direct articulation with a condyle on the clcithrum. It is likely that the

increased maneuverability of the head, owing to the jointly-connected cranium and shoulder girdle, enhances the efficacy of jaw protrusion, cranial elevation resulting in enhanced jaw protrusion in se',eral teleosts (Motta, 1984: Type C). Moreover, although not unique to Parexocoetus. the connection betv,.een the maxilla and cranium via a tubular cartilage also aids protrusion because such a structure allows the to,yard displacement of the maxillary head that in turn pushes the premaxilla forward. Collette et al. (1984) recognized four subfamilies within the Exococtidae--Fodiatorinae (genus meluded: Fodiazor), Parexocoetinae (Parexocoems). Exocoetinae (s and Cyl'~selurinae (P;'(Nnichthvs. Hirundichthvs and Qvpselurus). Because all of the subfamilies are monophyletic, we follow this classification, in addition to resur|ectir|g the Oxyporhamphinae (Fowler. 1934).

..lc'km?n'le'dgmenr~.

Tornio iwantnto pro,,ided us with important study |naterial. (aro[e C. Baldwin and Graham S. Hardy provided helpt\H comments on preparation of the manuscript.

Literature Cited Bruun, A. F. 1935. Fl,,hlg-fishes (Exocoetidae)of tile Atlantic. Dana Rep., 0: I 106. ('hell. C.-tl. 1988. Exocoetidae. Pages 275. 301 in M. Okiyama, ed. An atlas of the early stage lishes in .lapan. Tokai Univ. Press. Tokyo. (In Japanese. ) Collette. B. B., G. E. McGowen, N. V. Parm and S. Mito. 1984. Beloniformes: development and relationships. Pages 334--354 in II. G. Moser, W J. Richards. D. M. Cohen. M P. Fahav, A. "~b: Kendall. Jr. and S L. Richardson. eds. Ontogeny and systematics of" fishes. Am. Soc. Ichthyol. Herpetol. Spec. Publ. 1. Dasilao, Jr., J. C., K. Sasaki and O. Okamura. 1007. The hemiramphid, Ox3y)orhaml#m.s. is a flyingfish (Exocoetidae).lchth2oI. Res.,44: 10l 107. [)a~enpon. J. 1992. Wing-loading. stability, and morphometric rela|.ionships ill flying fish (Exocoetidae) from the north-easlern Atlantic. J. Mar. Biol. Assoc. UK, 72: 25--39. Fowler, It. ~ 1934. Descriptions of`a new fish obtained 1907 to 19 If), chiefly in the Ptdlippine Islands and adjacent seas. Proc. Acad. Nat. Sci. Phila., 85:233 363. Kovale;skaya, N. x,: 19.32. Superfluous reproduction and development of flying fishes of the family Exocoetidae. ,I. lchthyol.. 22: 48-54. (English translation from Vopr. Ikhtiol.) Motta. R J. 1984. Mechanics and functions ofjaw protrusion m teleost fishes: a review. Copeia. 1084: i. 18. Sxvolli>rd. D. I... 199l. EXUP: Phylogenetic anab, sis using parsimony, version 3.0r. Illinois Natural llistory Survey. Champaign, Illinois,.