ROLE OF LARVAL STAGES IN SYSTEMATIC INVESTIGATIONS OF MARINE TELEOSTS: THE MYCTOPHIDAE, A CASE STUDYl
H. GEOFFREY MOSER AND ELBERT H. AHLSTROM2
ABSTRACT
The lanternfish family Myctophidae is the most speciose and widespread family ofmid-water fishes in the world ocean. As presently recognized it contains about 30 genera and 300 nominal species. Their larvae are highly prominent in the plankton and make up about 50% ofall larvae taken in open-ocean plankton tows. Our studies of myctophid larvae, on a worldwide basis, have demonstrated that characters of the larval stages oflanternfishes are ofgreat utility in systematic analysis. The genera and species can be recognized on the basis ofeye and body shape, the shape and length ofthe gut, and pigmentpattern and by the sequence of photophore development. In this paper the larvae of 55 species representing 24 genera are illustrated and used to demonstrate the usefulness oflarvae in understanding the relation ships of species within genera. Charactersofthe larvae provide insight into generic affinities oflanternfish, allowing us to construct an evolutionary scheme of tribes and subfamilies that differs in some aspects from those proposed on the basis of adult characters. The concept of using larval characters in combination with adult characters to delineate phylogenetic lines in myctophids is discussed, as is our view of evolutionary strategy in the family.
A major facet ofcomprehensive systematic inves played a large role in the taxonomy of anguil tigations is the search for functionally unrelated liform fishes (Castle, 1969) partly because of the characters. Whether the independence of these conspicuousness ofeel leptocephali and partly be characters is actual or merely apparent, they con cause ofthe unavailability ofadults ofmany ofthe stitute useful elements in the analysis ofsystema families. Bertelsen's (1951) treatment of the tic relationships. Ample evidence of this is the ceratioid fishes is a superb example ofthe value of higher classification ofteleosts (Greenwood et al., utilizing larval stages in a systematic revision ofa 1966) generated by the synthesis of a diverse large group of teleosts. Apart from these two array of classical taxonomic characters. The re groups, it is the larvae of myctophiform fishes cent surge ofserological and biochemical studies which have received the most attention from tax on fish has placed a fresh group ofcharacters in the onomists. Ege (1953, 1957) relied heavily on lar hands of systematic ichthyologists (De Ligny, val stages in his extensive works on the 1969). Likewise, recent advances in fish cytogene Paralepididae. Johnson (1971) employed larval tics (e.g., Ohno, 1970; Benirschke and Hsu, 1971; characters in defining species and genera of Ebeling, Atkin, and Setzer, 1971) are providing Scopelarchidae. Bertelsen, Marshall, and Krefn another group oftaxonomic characters. It is likely (pers. commun.) have used larval stages exten that behavioral science will be still another source sively in their revision of the Scopelosauridae. of taxonomic characters, as exemplified by the Our studies on the family Myctophidae itself growing body of information on the acoustic be (Moser and Ahlstrom, 1970, 1972) indicated that havior of fishes (Fish and Mowbray, 1970). larval characters can aid significantly in differen One group ofwell known taxonomic characters, tiating taxa and defining evolutionary lineages those ofthe embryonic and larval stages, has re within this family. ceived scant attention from all but a few systema The lanternfish family Myctophidae is the most tic ichthyologists. Characters of the larvae have speciose and widespread family of mid-water fishes in the world ocean. As presently recognized it contains about 30 genera and 300 nominal 'This paper was presented atthe International Symposium on the Early Life History ofFish (sponsored by IABO, FAO, ICES, species. Their larvae are highly prominent in the ICNAF, and SCOR) held at Oban, Scotland, 17-23 May 1973. plankton and make up about 50% of all larvae 'Southwest Fisheries Center, National Marine Fisheries Ser vice, NOAA, La Jolla, CA 92037. taken in open-ocean plankton tows.
Manuscript accepted Agust 197J. FISHERY BULl.ETIN: VOL. 72, NO.2, 1974. 391 FISHERY BULLETIN: VOL. 72. NO.2 Our studies of the larvae of this family have longations of choroid tissue and some have the included material from all oceans. We have been eyes on stalks. Paxton recognized 11 genera in able to identify larvae from all recognized genera the subfamily Myctophinae and distributed them except Hintonia and Dorsadena. Larval evidence into two tribes, the Myctophini and the Gonich supports giving generic status to Metelectrona and thyini. Larvae of the species in each of these Parvilux. Including these, we have developmental genera generally conform to a particular morph series for 29 myctophid genera and for many gen based on form, pigment, and developmental era we have series for all known species. This has pattern and, although these morphs are remark afforded a more comprehensive view of the range ably diverse, we can find no character or set of and variability of larval characters, and we are characters that would divide the genera into increasingly impressed with the functional inde tribes. Within each genus of the subfamily, how pendence ofthe larval and adult characters. It is ever, the larval characters are indispensible in apparent that the world of the larvae and the delineating groups ofrelated species or subgenera. world of the adults are two quite separate This is best illustrated by examining the impor evolutionary theaters. Our studies of larval tant genera of the Myctophinae. lanternfishes have disclosed a full range ofcharac Protomyctophum larvae have a slender shape ters, from generalized to specialized and from con (Figure 1). For all species exceptP. anderssoni, the servative to labile, equal in scope to those of the gut is short during most of the larval period and adults. These characters fall into several characteristically there is a marked interspace categories. An important group is the shape of between the anus and the origin of the anal fin various structures such as the eye, head, trunk, (Figure lA-D). The gut elongates dramatlically in guts, and fins, especially the pectoral fins. Another late larvae, to fill the interspace. Gut development group is the sequence of appearance and the posi is completely dissimilar in P. anderssoni, where tion of fins, photophores, and bony elements. the gut is long at all larval sizes, in fact longer Another is the size of the larvae when fins and than in most other lanternfish larvae (Figure IE). other features appear and the size of the larvae Series of ventral tail melanophores are formed in when they transform intojuveniles. Pigmentation some species of both recognized subgenera provides an important group of characters based (Heirops and Protomyctophum sensu stricto), for on the position, number, and shape of melano example in P. Protomyctophum normani (Figure phores. Finally, there are the highly special 1A) and P. Heirops thompsoni (Moser and Ahl ized larval characters such as voluminous fin strom, 1970). Larvae ofthe subgenera can be sepa folds, elongated and modified fin rays, chin bar rated, however, on the basis ofeye shape, the eyes bels, preopercular spines, etc. It is our purpose ofHeirops (Figure 1C, D) being characteristically here to point out some of these characters and narrower than those of Protomyctophum sensu demonstrate how they can be of advantage in stricto (Figure lA, B). Choroid tissue is absent defining taxa and establishing phylogenetic from the ventral surface ofthe eye in all species of lineages. the genus exceptP. anderssoni, which has a well developed "teardrop" (Figure IE). Larvae of P. THE SUBFAMILY MYCTOPHINAE anderssoni are so markedly different from those of all other species of Protomyctophum, which The most trenchant character of larval myc otherwise form a rather cohesive group, that this tophids is eye shape. Our studies show that species should be placed in a separate subgenus or lanternfish larvae fall naturally into two groups perhaps even in a distinct genus. This suggestion on the basis ofeye shape-those with narrow ellip is supported by the unique placement of certain tical eyes and those with round or nearly round photophores and by the structure of the sup eyes (Moser and Ahlstrom, 1970). The species racaudalluminous tissue in adults ofthis species. composition of these two groups agrees closely Larvae of the genus Electrona are a less with that ofthe two subfamilies, Myctophinae and homogeneous group but are united by a common Lampanyctinae, established by Paxton (1972) on ality ofbody shape and especially gut shape (Fig the basis of osteological and photophore charac ure 2). A marked interspace is present between ters of adults. Larvae of the Myctophinae have the end of the gut and the origin of the anal fin. elliptical eyes; some species have ventral pro- This space is closed only at the termination ofthe
392 MOSER anJ AHLSTROM: ROLE 01' LARVAE IN SYSTEMATICS
A ------~
8
....----
E
FIGURE I.-Larvae of Protomyctophum. A. P. Protomyctophum normani, 15.2 mm; B. P. Protomyctophum teni soni, 14.5 mm; C.P. Hierops subparallelum. 15.2 mm; D.P. Hierops chilensis, 11.0 mm; E.P. anderssoni, 15.7 mm.
393 FISHERY BULLETIN: VOL. 72. NO.
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B
c
o
FIGURE 2.-Larvae of Electrona and Metelectrona. A. E. antarctica, 12.7 mm; B. E. carlsbergi, 11.1 mm; C. E. subaspera, 10.5 mm; D. M. ahlstromi, 10.3 mm.
394 MOSER and AHLSTROM: ROLE OF LARVAE IN SYSTEMATICS larval period. None of the species forms photo are synonyms, however, the uniqueness of the phores during the larval period other than the Br2 larva strongly suggests the resurrection of pair. Metelectrona as a valid genus. The characters that most clearly separate the The genus Benthosema IS the least cohesive of three developmental lines in Electrona are eye any genus inthe subfamily Myctophinae, from the shape and the amount ofchoroid tissue developed viewpoint of larval structure (Figure 3). We can under the eye. Electrona antarctica has an elon find only four types of larvae in the world ocean, gate choroid mass uniquely divided into two nar although Nafpaktitis (1973) recognizes five row eyes (Figure 2A). Also, E. antarctica larvae species on adult characters. We cannot distin attain a large size (20 mm), are the deepest-bodied guish larvae of B. pterota and B. panamense ofall Electrona larvae, and have the heaviest pig although Nafpaktitis has listed a number of con mentation. The two species in the second de vincing characters that distinguish the adults of velopmentalline transform at a small size (ca. 10 the two species. We find two highly divergent mm in E. rissoi and 12-13 mm in E. carlsbergi), species pairs. One is composed of B. glaciale and have a small choroid mass under a moderately B. suborbitale with a narrow eye subtended by a narrow eye, and develop scant pigment (Figure lunate choroid mass and with a pronounced inter 2B). In the third line, consisting ofE. subaspera space between the anus and the anal fin origin, and E. paucirastra, the eye is the least narrow, reminiscent of Protomyctophum and Electrona has no choroid tissue, and the larvae attain a large (Figure 3A-C). In the other pair, consisting of B. size (20 mm) (Figure 2C). panamense-pterota and B. fibulatum, the eye is The larva of the species described as Metelec wider, is subtended by a mere sliver of choroid trona ahlstromi (Wisner, 1963) is illustrated in tissue and the gut, of moderate length, lacks a Figure 2D. It is more laterally compressed than postanal interspace (Figure 3D, E). any species of Electrona and has no interspace The one feature held in common by the four between the anus and origin of the anal fin. In species is the development ofsome photophores in some features it resembles the larvae of addition to the Br2 during the larval period. The Hygophum; it has a late-forming dorsal fin and the only other myctophine genera that develop photo gut is shaped very similarly to that inH. taaningi phores in addition to the ubiquitous Br2 during the and H. macrochir. Its pigment is unique and the larval period are Diogenichthys, Myctophum, eye is distinct, with the ventral edge ofthe scleral and Metelectrona. This feature is much more pre envelope characteristically squared off. Also, in valent among genera ofthe Lampanyctinae and is late-stage larvae, in addition to the Br2, a second helpful in defining groups ofrelated genera there pair of photophores (pas) develops, a feature (Moser and Ahlstrom, 1972). found in neitherHygophum norElectrona. Paxton In B. panamense-pterota and B. fibulatum the (972) synonymized Metelectrona with Electrona Dn pair is formed soon after the Br2 at about and suggested that M. ahlstromi and E. ventralis 5.0-6.0 mm. The pas pair is the third to appear in
TABLE I.-Sequence of photophore formation in larvae of three species ofBenthosema.
Size No. of Smallest larva photophore juvenile Species (mm) Photophores pairs (mm)
B. flbulatum ca. 4.0 B" 1 132 5.4 B" On 2 6.0 Br, On pas 3 6.4 B" On pas PO, 4 7.3 B" On pas PO, AOa, 5 7.7-8.7 Br, On pas PO, AOa, PO, 6 ca. 10.0 Br, On pas PO, AOa, PO, Op, VLO 8 B. plerala (panamense) 4.0 Br, 1 118 5.0 Br, On 2 6.0 B" On pas 3 ca. 7.0 B" On pas PVO, 4 7.1 Br, On pas PVO, Op, 5 7.5 B" On pas PVO, Op, va, PVO, 7 8.0 Br, On pas PVO, Op, va, PVO, PO, AOa, 9 B. suborbilale 4.1 B" 1 107 8.3-9.2 Br2 PO, P02 3 9.4 Br, PO, PO, Br, BrJ Op, 6 11.5 B" PO, PO, Br, BrJ Op, POJ PO. pas AOa, AOa, 11
395 FISHERY BULLETIN: VOL. 72. NO.
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B
c
...,
FIGURE 3.-Larvae of Benthosema. A. B. glaciale. 7.2 mm; B. B. glaciale, 10.5 mm; C. B. suborbitale. 9.2 mm; D. B. pterota, 8.5 mm; E. B. fibulaturn. 8.7 mm.
396 MOSER and AHLSTROM: ROLE OF LARVAE IN SYSTFMATICS larvae about 6.0 mm long. Thereafter the pattern dorsally into a prominent enlarged posterior sec diverges as shown in Table 1, but both species tion. In H. macrochir this enlarged section is gradually add about a dozen pairs during the lar covered with large melanophores. Larvae of this val period. Specimens of B. pterota from the Per group occur only in the Atlantic. sian Gulf off India, formed photophores at some The genus Hygophum affords an excellent ex what larger sizes than larvae of B. panamense, ample of the taxonomic utility of larval stages. but in the same sequence. Transformation occurs The juveniles and adults of some species are at a small size, 10-12 mm in B.panamense-pterota notoriously difficult to identify. In contrast, the and 11-13 mm in B. fibulatum. larvae of these species are highly distinct and can Photophores appear relatively late in larvae of be readily identified. We have 11 such distinct B. suborbitale and B. glaciale, however, the Brl' larval types, whereas only 9 species are currently BI'l, O\l2, and PO series appear in late larvae of known for the adults. Search for adults of the two bot~ species (Table 1). Transformation occurs at remaining larval types has led to the discovery of about 9-11 mm in both species. The larvae ofB. two undescribed species. In addition, characters of panamense-pterota and B. fibulatum are close to the adults of this genus reveal little about the the larvae ofDiogenichthys in several characters relationships of the member species (Becker, including body shape, gut shape, and early ap 1965). A study ofthe larvae, however, shows that pearance of photophores. there are three highly distinct subgeneric groups, As in Benthosema, the larval characters of each containing from two to six closely related Hygophum suggest some divergence within the species. Such an independent view ofthe complete genus, although all species have a highly charac species complement of a genus is an invaluable teristic series of isthmal melanophores, form the tool in the formal revision of that genus. dorsal fin late in the larval period, and develop no Larvae of the species of Symbolophorus are photophores other than the Br2' as larvae (Figure perhaps the most cohesive of all myctophine gen 4). The genus contains three divergent types of era (Figure 5A). In all species known to us the larvae. The most unusual of these are the ex pectoral fin is large and is supported by an elon tremely elongate larvae ofH. reinhardti and H. gate aliform base. Also, the pelvic fins are large atratum, which have very narrow eyes that are and develop earlier than in any other lanternfish underlain by prominent choroid tissue and are genus. The narrow eyes have choroid tissue and borne on short stalks (Figure 4A). The amount of are borne on short stalks. The amount ofpigmen pigmentation along the gut and tail and on the tation decreases towards the end of the larval myosepta and fin fold increases throughout the period. Most species attain a large size-up to 24 larval period. mm. The species differ principally in the size at A second larval type is represented by the which various larval structures appear. largest number of species, H. proximum, H. The closely related genus, Myctophum, has a hygomi, and H. brunni, all illustrated (Figure diversity of larval form unmatched in the family 4B-D), as well as H. benoiti, H. hanseni, and an (Figures 5, 6, 7). Before taking up the bulk of the undescribed form in our collection. These larvae species in this genus we must first examine the are only moderately slender and have unstalked most aberrant ofall lanternfish larvae, that of M. eyes of moderate width, subtended by prominent aurolaternatum (Figure 5BJ. In this remarkable choroid tissue. Melanophores are located chiefly larva the eyes are borne on long stalks and the free on the head and gut, however some species have trailing section of the gut is almost as long as the pigment on the myosepta and fin fold. The trend in fish itself. The dorsal fin forms at the margin ofthe this group ofspecies is for the early larval stages fin fold. These characters are so bizarre that it to have the heaviest pigment and for melano would seem preposterous to identify it as a phores to be lost as development proceeds. lanternfish larva, much less that ofM. aurolater A third type of larva is exhibited by H. mac natum. Nonetheless, A. Vedel Taning first sug rochir, H. taaningi, and an undescribed form in gested the true identity ofthis larva (E. Bertelsen, our collection (Figure 4E, F). These are relatively pers. commun.) which we can now confirm since deep-bodied, have large, relatively wide eyes with recently receiving the critical transforming little or no choroid tissue, and lack tail pigment. specimens through the courtesy of Warren Also, the gut has a highly distinctive form; the Freihofer (California Academy of Science). The anterior halfhas a very small diameter and opens uniqueness of this larva would certainly suggest
397 FISHERY BULLETIN: VOL. 72. NO.
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,':' i;"'.-,:'®:".'lIIl.'·.:'i~,..'. ~
FIGURE 4 .-Larvae ofHygop hum. A. H. reinhardti, 12.8 mm' . mm; D. H. brunni, 9.7 mm; E. H. macrochir, 73B. H: proxlmum: 8.9 mm; C. H. hygomi, 8.1 . mm, F. H. taamngi, 6.8 mm.
398 MOSER and AHLSTROM: ROLE OF LARVAE IN SYSTEMATICS
FIGURE 5.-Larvae of Symbolophorus and Myctophum. A. S. californiense, 9.6 mm; B. M. aurolater natum. 26.0 mm; C. M. punctaturn, 13.6 mm; D. M. nitidulum. 8.2 mm; E. M. phengodes. 9.8 mm.
399 FISHFRY BULLFTlN: VOL. n. NO.2 the creation of a distinct genus for M. aurolater Myctophum sp. (possibly brachygnathum) and is natum and it is highly probable that corroborative developed on the jaws, branchistegal membrane characters will appear after careful reexamina and lower part of the pectoral fin base in Myc tion of the adults. tophum sp. (possibly fissunovi) as seen in Figure With the removal ofM. aurolaternatum. the re 6B-D. The latter three species form the PLO maining larvae ofMyctophum form a diverse, yet photophores on the pectoral fin base soon after the recognizable, group. All have large broad pectoral appearance of the Dn organs (Table 2). fins supported on a highly characteristic fan Nafpaktitis (1973) has listed a number of shaped base. The species may be divided into two characters for distinguishing adult M. ob groups, those which form only the Brz photophores tusirostre from M. brachygnathum. He showed and those which develop additional photophores that M. pristilepis is a synonym of M. brachyg during the larval period. In the first group the nathum. The status of M. imperceptum Bekker elongate larva of M. punctatum (Figure 5C) has and Borodulina has yet to be determined. stalked eyes and a slightly aliform pectoral fin A second larval type is represented by M. base, reminiscent of Symbolophorus larvae, and selenops (Figure 7A) and a closely related species may be the closest relative of that genus among restricted to the Indian Ocean and Persian Gulf the species of Myctophum. A closely related for which we can find no adult (Figure 7B). In species, M. nitidulum. is also stalk-eyed, but is these rotund species, the head is relatively longer deeper-bodied, more heavily pigmented, and has a and narrower than in the previous group and the more fan-shaped pectoralfin base