SPECIES of the stoplight loosejaw genus

Transcription

1 Copeia, 2007(4), pp Revision of the Stoplight Loosejaw Genus Malacosteus (Teleostei: Stomiidae: Malacosteinae), with Description of a New Species from the Temperate Southern Hemisphere and Indian Ocean CHRISTOPHER P. KENALEY Species of the deep-sea stomiid fish genus Malacosteus are readily diagnosed within the Malacosteinae by the presence of a single round nostril on each side of the snout, palatine bones without teeth, and a single large tear-shaped accessory light organ positioned below the anterior margin of the eye. In contrast to the many recent investigations into the biochemical basis of the red-shifted bioluminescence produced by the accessory light organ, Malacosteus has received little taxonomic scrutiny in the last 75 years. Four nominal species of Malacosteus have been described: M. niger, M. indicus, M. choristodactylus, and M. danae. Two species are considered valid: M. niger and a new species known from 182 specimens captured in temperate and sub-antarctic waters of the southern hemisphere, the tropical Indian Ocean, and waters of the Indo- Australian Archipelago. Diagnosed primarily on the basis of postorbital photophore size and serial photophore counts, the new species differs further from its only known congener in having relatively small jaws and fleshy orbit. SPECIES of the stoplight loosejaw genus Malacosteus occur in midwaters worldwide between Arctic and sub-antarctic latitudes. This genus is diagnosed within the Stomiidae by having enormous jaws, a single circular nostril on each side of the snout, a large tear-shaped accessory orbital photophore, serial photophores reduced in size and number, and intramandibular membrane, hyoid barbel, and palatine teeth absent. Malacosteus is the type genus of the family Malacosteidae (sensu Morrow, 1964; Harold, 2003) or is placed in the expanded Stomiidae (sensu Fink, 1985), and subsequently the type of the subfamily Malacosteinae as well (Eschmeyer, 1998; Nelson, 2006). Fink (1985) assigned Malacosteus to an unresolved polytomy containing the other three loosejaw genera Photostomias, Pachystomias, and Aristostomias. As such, these four genera constitute the most derived clade within the Stomiidae and thus the Stomiiformes (Fink, 1985), a position that corresponds with unique visual capabilities and modes of feeding. The accessory orbital photophore of three of the four malacostein genera, Malacosteus, Pachystomias, and Aristostomias, emits a red-shifted light that is visually undetectable by all other fishes in the mesopelagic realm (O Day and Fernandez, 1974; Partridge and Douglas, 1995; Herring and Cope, 2005). Unlike Aristostomias and Pachystomias, which possess a full complement of redsensitive retinal pigments matching the frequency emitted by the accessory orbital photophore, Malacosteus achieves long-wave sensitivity with a bacteriochlorophyll-based photosensitizer (Campbell and Herring, 1987; Douglas et al., 1998, 1999), making this genus unique among animals as the only taxon that in effect uses chlorophyll to perceive red-light. In contrast to the many recent investigations into the biochemical basis of its visual ecology, Malacosteus has received little taxonomic scrutiny in the last 75 years. Malacosteus was established in 1848 by Ayres for the single species M. niger based on a single specimen captured in the western North Atlantic off Nova Scotia. A more thorough description by Ayres appeared a year later (Ayres, 1849). From that time, published records of species of Malacosteus are unknown in the literature until Günther s (1878) description of M. indicus based on a single specimen collected south of the Philippines during the HMS CHAL- LENGER Expedition. A decade later, Vaillant (1888) described a third species of Malacosteus, M. choristodactylus, based on three specimens captured by the TALISMAN in the eastern North Atlantic off Morocco. After reviewing specimens collected by the INVESTIGATOR in the Andaman Sea, Alcock (1899) questioned the validity of M. indicus and M. choristodactylus. Zugmayer (1911) made the most detailed comparison of these three nominal species to date and concluded that M. indicus and M. choristodactylus were synonyms of M. niger. Parr (1927), Regan and Trewavas (1930), and Morrow (1964) arrived at the same conclusion. Regan and Trewavas (1930) described the most recent nominal species, M. danae, based on two specimens captured by the R/V DANA in the Gulf of Panama. Morrow (1964) recognized M. danae as valid but suggested that subsequent examination of additional material would indicate conspecificity with M. niger. # 2007 by the American Society of Ichthyologists and Herpetologists

2 KENALEY REVISION OF MALACOSTEUS 887 Goodyear (1990) placed all nominal species in the synonymy of M. niger; however, Harold (1999) chose to recognize M. indicus. Additionally, M. danae has been recognized in several recent biogeographic inventories (Aizawa, 1990; McAllister, 1990). Hence, three species of Malacosteus are currently recognized. Based on an examination of more than 450 specimens, the largest body of material examined to date for any stomiid taxon, the present study resolves this taxonomic uncertainty. In addition, a new species is described from temperate and sub-antarctic waters of the southern hemisphere, the tropical Indian Ocean, and waters of the Indo-Australian Archipelago; it is readily diagnosed on the basis of the relative size of the post-orbital photophore, photophore counts, and relative size of the eye and upper and lower jaws. MATERIALS AND METHODS All specimen lengths are given as standard length (SL) and all morphometric characters are expressed as percent SL unless specified otherwise. Counts and measurements were made according to Hubbs and Lagler (1958), with exceptions outlined by Kenaley and Hartel (2005) and those described herein. Lateral and ventral photophore terminology was altered from Gibbs et al. (1983:fig. 1) to include both total number of photophores in a group (annotated with a p, e.g., OVp) and number of clusters among which the photophores of that group are distributed (annotated with a c, e.g., OVc). Cephalic photophore terminology follows Fink (1985:fig. 70) and Kenaley and Hartel (2005:fig. 1; Fig. 1). Postorbital photophore (PO) length was measured as the longest dimension of the bulbous organ including that portion of the organ covered by black tissue; accessory orbital photophore (AO) length was measured as the longest dimension of the opening in the skin through which the AO is visible (Fig. 1). The AO is that photophore mistakenly referred to as the suborbital or subocular organ in many studies of the bioluminescent properties of the AO (Widder et al., 1984; Partridge and Douglas, 1995; Herring and Cope, 2005). The suborbital photophore (SO) of species of Malacosteus, a minute luminescent organ embedded in the posteroventral margin of the fleshy orbit (Fig. 1), is purportedly homologous to the suborbital photophore of similar size and position present in all other stomiid taxa (Fink, 1985). Descriptions of and terminology associated with osteological characters are drawn largely from Fink (1985). Upper jaw length (UJL) was Fig. 1. Schematic diagram of head of species of Malacosteus in left lateral view showing position of the cephalic photophores with their axes and points of measurement and that of the eye. Abbreviations: EW, eye width; AO, accessory orbital photophore; PO, postorbital photophore; SO suborbital photophore. measured from the anteriormost point of the premaxilla to the posterior point of the maxilla; lower jaw length (LJL) was measured from anteriormost point of the symphysis of the dentary to the posterior process of the anguloarticular. Head length was measured from the anteriormost tip of the premaxilla to the anterodorsal junction of the opercular flap and the head. Eye width (EW) was measured as the outside diameter of the ring of small photophores surrounding the pupil of eye (Fig. 1). Head width (HW) was measured as the greatest lateral distance between the sphenotic processes. Dorsal- and anal-fin ray counts include all the external elements. Bracketed counts, such as those given in the key, descriptions, and diagnoses, refer to extreme values recorded with a frequency less than 5%. Vertebral counts were obtained from digital radiographs; the unossified elements between the skull and the first vertebral centrum were not included; the preural and ural centra were counted as one vertebra. Sex was determined by gross microscopical examination of the gonads. Specimens smaller than 50 mm SL could not be sexed reliably. Many of the measurements are affected by the condition of the specimen and the degree to which the specimen was manipulated while measuring. To minimize imprecision, diagnostic morphometric characters are reported as per-

3 888 COPEIA, 2007, NO. 4 TABLE 1. MORPHOMETRIC MEASUREMENTS AND MERISTICS OF Malacosteus australis, NEW SPECIES, THE HOLOTYPE OF M. australis (AMS I ), AND M. niger. Malacosteus australis, new species Malacosteus niger Range (mean 6 SD) n holotype Range (mean 6 SD) n Standard length ( ) ( ) 255 Upper jaw length (UJL) %SL ( ) ( ) 221 Lower jaw length %SL ( ) ( ) 74 Longest dentary tooth %SL ( ) ( ) 71 Eye width %SL ( ) ( ) 233 Accessory orbital photophore ( ) ( ) 236 (AO) %SL AO %UJL ( ) ( ) 217 = Postorbital photophore (PO) ( ) ( ) 90 %SL = PO %UJL ( ) ( ) 83 R PO %SL ( ) ( ) 142 R PO %UJL ( ) ( ) 130 Predorsal length %SL ( ) ( ) 60 Preanal length %SL ( ) ( ) 60 Dorsal-fin base %SL ( ) ( ) 67 Anal-fin base %SL ( ) ( ) 66 Head length %SL ( ) ( ) 108 Body depth at cleithrum %SL ( ) ( ) 56 Body depth at anal-fin origin %SL ( ) ( ) 59 Caudal peduncle depth %SL ( ) ( ) 59 Pectoral-fin length %SL ( ) 22 damaged ( ) 13 Pelvic-fin length %SL ( ) 33 damaged ( ) 23 Prepelvic length %SL ( ) ( ) 59 Pectoral-fin rays 3 5 ( ) ( ) 184 Pelvic-fin rays 6 ( ) ( ) 181 Dorsal-fin rays ( ) ( ) 165 Anal-fin rays ( ) ( ) 167 Dorsal premaxillary teeth 4 22 ( ) ( ) 70 Ventral premaxillary teeth 6 31 ( ) ( ) 71 Dentary teeth ( ) ( ) 71 Branchiostegal rays 7 9 ( ) ( ) 57 Total vertebrae ( ) ( ) 20 cent of UJL, a more fully ossified, less easily damaged structure. Morphometric characters in the species descriptions are followed in parentheses by the range and mean; meristic characters are followed by the mean. Post hoc ANCOVA analyses were used to compare each morphometric character, with UJL and standard length as covariates. Where regression analysis was not appropriate, characteristics were analyzed using a Mann Whitney U-test (MWU). Values for n in all analyses follow those given in Table 1. Specimens were captured using several pelagic and benthic net systems; trawl type and more precise capture information than that given in Material Examined is available on-line via institutional websites. Institutional codes follow Leviton et al. (1985). Malacosteus Ayres, 1848 Malacosteus Ayres, 1848:69 (type species Malacosteus niger Ayres, 1848, by monotypy). Diagnosis. Species of Malacosteus differ from species of all other genera of the family Stomiidae (sensu Fink, 1985) in having one round nostril on each side of head anterior to eye; palatine bones unossified and lacking teeth; margin of anterodorsal portion of neurocranium convex; a median toothplate associated with fourth basibranchial, and a single large ( % SL) tear-shaped accessory light organ (AO) along anteroventral margin of eye (Fig. 1). It differs further in having the following combination of character states: hyoid barbel and skin between mandibular rami absent, with only

4 KENALEY REVISION OF MALACOSTEUS 889 protractor hyoideus muscle linking mandibular symphysis to hyoid; jaws enormous (UJL % SL, LJL % SL), extending far posterior to fleshy orbit; all jaw teeth fixed and not depressible (Type 1 attachment; Fink, 1981); vomerine teeth absent; maxillary teeth minute, closely and regularly set; lateral ethmoid, parietal, mesopterygoid, and posttemporal absent; eyes directed slightly anteriorly; lateral and ventral photophore series clustered, reduced in size, those of IP series in two distinct rows. Description. Body elongate, depth tapering slightly from cleithrum ( % SL) to analfin origin ( % SL), and more abruptly toward caudal peduncle ( % SL). Head small ( % SL). Eye large (EW % SL). Snout blunt and short. Opercular flap long and sloping posteroventrally to posterior tip of jaw. A single round nostril on snout facing anterolaterally. Tip of basihyal with a white, fleshy, finger-like tab. Branchiostegal rays Dentary teeth on left side 18 53, variable in size and decreasing in number with SL; anteriormost tooth minute, next to mandibular symphysis, followed by a large ( % UJL), barbed, sharply curved, fang-like tooth emanating from dorsolateral margin of mandible; fang-like tooth followed by several large ( % SL), slightly curved, barbed, knife-shaped teeth; middle third of jaw populated by small barbed teeth of subequal size, some directed anterodorsally. Premaxillary teeth less numerous (12 53), small to moderate, slightly curved, often produced in two rows, a ventral row positioned along the ventral margin of the premaxilla and a dorsolateral row positioned along the anterolateral margin of the premaxilla; anteriormost tooth of the dorsolateral row barbed and usually isolated; posterior teeth of the ventral row often directed anteroventrally. Maxillary teeth minute, numerous. Palatine teeth absent. Basibranchial tooth patches placed dorsally in four groups, anteriormost three groups as bilateral patches associated with basibranchials 1, 2, and 3; posteriormost group associated with basibranchial 4, produced either as a pair of patches or as a singular, often laterally offset patch; 1 6 teeth per patch. Pharyngobranchial teeth in two groups on each side. Pectoral fin moderately elongate ( % SL); pectoral-fin rays [2]3 4[5 6]; pelvic fin moderately elongate ( % SL), placed at about mid-body, prepelvic length % SL; pelvic-fin rays 6. Dorsal and anal fins placed far back on body and nearly opposite, predorsal length % SL, preanal length % SL. Dorsal- and anal-fin bases subequal ( and % SL, respectively). Dorsal-fin rays [16 17]18 20[21], anal-fin rays [18]19 22[23 24]. Caudal fin small and emarginate, lower lobe longer than upper. Total vertebrae Three cephalic photophores near orbit: AO, PO, and SO (Fig. 1). AO large ( % UJL, % SL), subequal to orbit in specimens larger than 50 mm ( % EW), relatively larger than orbit in smaller specimens ( % EW); teardrop-shaped and positioned at anteroventral edge of fleshy orbit. PO small to moderate ( % UJL, % SL), an ovoid body posterior to fleshy orbit, ventral edge aligned with ventral margin of fleshy orbit, center aligned about one orbit-width posterior to posterior margin of eye; covered by a transparent membrane; size varying with sex and between species, larger in males, smaller in females. SO minute, round, situated on posteroventral margin in an elongate pocket with a dorsomedial opening. Small photophores and unorganized areas of accessory white luminous tissue scattered over head and body, often arranged around lateral photophores or along dark vertical lines composed of minute photophore-like structures. Ventrolateral and opercular photophores glowing blue in fresh specimens. Lateral and ventral photophore series present, arranged in discrete groups (e.g., IP, PV, VAV, etc.); each group often containing one to several clusters of photophores. Lateral series low on body extending posteriorly from a position just anterior to level of posterior angle of jaw (when closed) to just anterior to origin of anal fin; ventral series extending posteriorly from anterior tip of isthmus along ventral midline to insertion of anal fin. IPp [3]4 7[8], IPc 3 7 clusters, arranged in off set rows; PVp [3]4 7[8 9], PVc 2 6 ; VAVp [2 3]4 6[7], VAVc 2 4. OVp [3 4]5 9[10 11], OVc 3 6, arched anteroventrally; VALp 2 6, VALc 1 4; ACp [0]1 3[4], ACc 1 4, rarely absent, with several subcutaneous photophores anterior to visible group or clusters. A single small photophore placed approximately at mid-point of opercular flap on posterior margin of operculum. Skin thin, scaleless; color of fresh specimens black, fading to dark brown after lengthy preservation. Size moderate, up to 253 mm. Malacosteus niger Ayres, 1848 Northern Stoplight Loosejaw Figure 2; Tables 1, 2 Malacosteus niger Ayres, 1948:69 (original description, holotype lost, southeast of Nova Scotia, 42uN, 50uW); Regan and Trewavas, 1930:142, figs. 25, 138; Morrow, 1964:545, fig. 144; Good-

5 890 COPEIA, 2007, NO. 4 Fig. 2. Left lateral view of heads of Malacosteus niger : (A) MCZ 65810, male, mm SL; (B) MCZ , female, mm SL. year, 1973:142; Gibbs, 1984:369; Goodyear and Gibbs, 1986:236; Goodyear, 1990:339. Malacosteus indicus Günther, 1878:181 (original description, holotype BMNH , near Philippines, CHALLENGER station 214, 04u339N, 127u069E, 500 fm); Regan and Trewavas, 1930:143; Morrow, 1964:544, fig Malacosteus choristodactylus Vaillant, 1888:108, pl. 8, fig. 4 (original description, lectotype by subsequent designation of Bertin, 1940, MNHN , off Morocco, TALISMAN station 26, 1635 m; paralectotype MNHN , off Azores, TALISMAN station 129); Morrow, 1964:544. Malacosteus danae Regan and Trewavas, 1930:143, pl. 14, fig. 1 (original description, lectotype, hereby designated, ZMUC P201990, DANA station 1203, 07u309N, 79u199W; paralectotype BMNH , DANA station 1209, 07u159N, 78u549W); Morrow, 1964:545. Malacosteus sp. Alcock, 1899:149; Alcock and McArdle, 1900:pl. 33, fig. 4. Diagnosis. A species of Malacosteus with male PO % UJL, % SL, female PO % UJL, % SL; IP photophores 3 5 in 3 5 clusters. Description. UJL % SL (27.7%); LJL % SL (26.3%); longest dentary tooth % SL (3.6%); EW % SL (5.5%); AO % UJL (20.1%) and % SL (5.6%), emitting far-red light (l max. 700 nm) in freshly caught, live specimens (Widder et al., 1984; Herring and Cope, 2005); PO % UJL (4.1%) and % SL (2.2%; Fig. 3); female PO % UJL (5.1%) and % SL (1.4%; Fig. 3); PO emitting blue light (l max nm) in freshly caught, live specimens (Widder et al., 1984; Herring and Cope, 2005); predorsal length % SL (80.2%); preanal length % SL (79.6%); dorsal-fin base % SL (14.4%); anal-fin base % SL (15.5%); head length % SL (9.5%); body depth at cleithrum % SL (14.3%); body depth at anal-fin origin % SL (8.4%); caudal-peduncle depth % SL (2.4%); pectoral-fin length % SL (16.0%); pelvic-fin length % SL (20.5%); prepelvic length % SL (58.0%); pectoral-fin rays [2]3 4[5 6] (3.4); pelvic-fin rays 6; dorsal-fin rays (18.8); anal-fin rays (20.5); dorsal premaxillary teeth 4 28 (8.3), ventral premaxillary teeth (17.3); dentary teeth on left side (34.0); IPp 3 5 (4.1), IPc 3 5 (4.0); PVp [2]3 6[7 9] (5.3), PVc 3 6 (3.4); VAVp 3 6 (5.1), VAVc 2 4 (3.0); ACp [0]1 2[3] (1.3), ACc 1 3 (1.3); OVp [3]4 9 (5.9), OVc 3 5 (3.9); VALp 2 6 (3.5), VALc 1 3 (2.7); branchiostegal rays 7 10 (8.2); total vertebrae (49.1). Size to mm. Morphometric and meristic data are reported in Table 1. Comparison. The larger PO in both males and females and higher number of IP photophores distinguish M. niger from the new species. Smaller specimens, less than 50 mm, may be confused with the new species; however, in most cases M. niger can be distinguished by a lower number of IP photophores (Table 2). The following morphometric characters of M. niger were found to differ significantly from the new species: male PO larger as a percent of SL and UJL (ANCOVA: F , P, and F , P, 0.001, respectively); female PO larger as a percent of SL and UJL (ANCOVA: F , P, and F , P, 0.001, respectively); EW larger as a percent of UJL (ANCOVA: F , P, 0.001); UJL larger as a percent of SL (ANCOVA: F , P, 0.001); and LJL larger as a percent of SL (ANCOVA: F , P, 0.001; Tables 1, 2). The following meristic characters of M. niger were found to differ significantly from the new species: number of pectoral-fin rays fewer (Mann Whitney U-test: Z , P, 0.001); number of

6 KENALEY REVISION OF MALACOSTEUS 891 TABLE 2. VENTROLATERAL PHOTOPHORE COUNTS OF Malacosteus australis, NEW SPECIES, AND M. niger. Photophore terminologies follow Gibbs et al. (1983); asterisks denote counts of holotype of M. australis, AMS I sum mean 6 SD IP M. niger M. australis * PV M. niger M. australis * VAV M. niger M. australis * AC M. niger M. australis * OV M. niger M. australis * VAL M. niger M. australis * IC M. niger M. australis * OA M. niger M. australis * dorsal-fin rays greater (Mann Whitney U-test: Z , P ); number of IP photophores fewer (MWU: Z , P, 0.001); number of PV photophores fewer (MWU: Z , P, 0.001); number of VAV photophores fewer (MWU: Z , P, 0.001); number of AC photophores fewer (MWU: Z , P, 0.001); number of OV photophores fewer (MWU: Z , P, 0.001); and number of VAL photophores fewer (MWU: Z , P ; Tables 1, 2). Distribution and ecology. Malacosteus niger occurs worldwide in all oceans from Arctic latitudes at 66uN to approximately 30uS in the southern hemisphere. This species is unknown from the Mediterranean. Clarke (1974) and Sutton and Hopkins (1996a) suggested that M. niger does not undergo substantial diel vertical migration (DVM) and remains below 500 m. In a study of the DVM patterns of malacosteine taxa in the western North Atlantic based in part on material examined in this study, Kenaley and Sutton (unpubl. data) corroborated this hypothesis and proposed that M. niger makes only rare sorties into the epipelagic. Of those mesopelagic stomiid taxa for which DVM patterns have been reported (Sutton and Hopkins, 1996a, and references therein), M. niger appears to be the only member of this family that does not undertake DVMs. Sutton (2005) hypothesized that M. niger remains in the mesopelagic using long-wave, red-shifted bioluminescence (emitted from the AO) and perception to search for prey, sustaining itself on deep-dwelling calanoid copepods between rare encounters with larger prey such as myctophids or gonostomatids. A dietary origin of the photosensitizer in M. niger has been proposed by Douglas et al. (1998) and Douglas et al. (1999); hence, this species most likely gains

7 892 COPEIA, 2007, NO. 4 Fig. 3. Postorbital photophore (PO) size versus standard length of species of Malacosteus. the raw material for long-wave visual sensitivity from the consumption of copepods while at depth. Kenaley and Sutton (unpubl. data) proposed that when the nutritional state of an individual deteriorates after prolonged snacking on copepods, it may be stimulated to revert to piscivory and utilize this stealthy visual mechanism in the epipelagic zone where high densities of teleost prey aggregate on a diel cycle. Remarks. In the course of this study, all type material for the nominal species of Malacosteus was examined with the exception of the type species, M. niger, the holotype of which is undoubtedly lost. A Miss L. Felt of Boston, received the specimen from a Capt. Joseph R. Porter of St. Stephens, New Brunswick, who captured it en route from Liverpool to Boston (Ayres, 1849). The specimen was recorded in the Boston Society of Natural History (BSNH) ledger after it was received from Miss Felt. All type specimens in the BSNH collection have subsequently been absorbed by the MCZ; however, no evidence exists that the holotype was ever received there (Karsten Hartel, pers. comm., 20 May 2006). Although the holotype of M. niger is most certainly lost, M. niger is defined objectively and no ambiguity exists as to the prevailing usage of this name. Malacosteus niger is the only species of the genus known in the western North Atlantic and clearly diagnosable based on material collected near the type locality and elsewhere. Under these conditions, the designation of a neotype is unwarranted (ICZN articles 75.1 and 75.3). The detailed description of M. niger provided by Ayres (1849:54 55) outlines a species in which all other nominal species should be included: entire length eight and one-half inches or approximately 215 mm in total length and having a PO one-sixth of an inch in length or approximately 4.2 mm; thus, the PO is 2.0% total length, or greater than 2.0% SL, a value that corresponds with all other male specimens of M. niger examined (Fig. 3, Table 1). Type specimens of the other previously described nominal species, M. indicus, M. choristodactylus, and M. danae, all possess POs with sizes that fall well within the sexspecific ranges for M. niger. Characters used by Günther (1878), Vaillant (1888), and Regan and Trewavas (1930) to diagnose their respective species also fall within the range of the 288 specimens of M. niger examined in this study. Günther (1878) distinguished M. indicus in part by the presence of a pair of large fangs at the symphysis of the dentaries. These fangs, however, were present in all but the most damaged specimens examined in this study. Günther (1887) later refined his diagnosis of M. indicus, relying this time on the presence of fewer dentary teeth, the anterior portion of which differed in both number and size relative to M. niger. The holotype of M. indicus measures 105 mm, less than half the length of the holotype of M. niger. This great difference in size explains the presence of fewer dentary teeth, which are apparently not replaced as they are lost. The dentary-tooth count of the holotype of M. indicus (37 left, 46 right) falls well within the range of specimens of M. niger of similar size. Günther s (1887) description of anterior dentary teeth in M. indicus is not unique; size and position of the teeth in the holotype of M. indicus align with the variable pattern seen in material of all species of Malacosteus examined in this study: two minute symphyseal teeth followed by a large, barbed, sharply curved, fang-like tooth emanating from the dorsolateral margin of the mandible, these teeth followed by several large knife-shaped teeth. Vaillant (1888) distinguished M. choristodactylus as having a deeper body and fewer rays in all fins than M. niger. The body depth reported by Vaillant and measurements recently recorded from the lectotype and paralectotype fall well within the range of M. niger. However, Vaillant s reported fin-ray counts are mysterious; they were presumably taken from a single specimen: dorsal and anal 15, pectoral 4, and pelvic 5. The dorsal-,

8 KENALEY REVISION OF MALACOSTEUS 893 anal-, and pelvic-fin ray counts are lower than any other recorded specimen of Malacosteus (Table 1). Fin-ray counts in Vaillant s (1888:pl. 8, fig. 4) figure of M. choristodactylus, with the exception of the pelvic fin, clearly disagree with those listed in his text: dorsal 17, anal 18, pectoral 3, and pelvic 5. With the exception of the pelvic-fin rays, these counts are all within the range of M. niger. While it is possible that the specimen figured by Vaillant had an aberrant pelvic-fin ray count of 5, a count unknown in species of Malacosteus, it is more likely that the artist, Vaillant himself, or both made an error. Although not accurately represented in Vaillant s figure, the most medial rays of the pelvic fin are often spaced so closely that they can be mistaken for a single element. Further complicating the issue, Vaillant listed three specimens in his description of M. choristodactylus, all cataloged as a single lot (MNHN ): two from off Morocco, TALISMAN stations 22 and 26, and one from off the Azores, TALISMAN station 129. Bertin (1940) listed MNHN as the Holotype figuré, TALISMAN station 26 and MNHN as a Paratopotype, TALISMAN station 129. The third specimen is not addressed by Bertin, and no other Malacosteus from the TALISMAN Expedition was uncovered by the author during a review of type material at the MNHN. As calculated from the scale, the specimen figured measured approximately 160 mm TL; this approximates the length reported by Vaillant for one of his three specimens (156 mm SL, his table 1) and the length of MNHN recorded here (155 mm SL). It is possible that the aberrant fin-ray counts belong to the missing third specimen; however, all evidence suggests Vaillant erred in his enumeration of fin rays. The figured specimen (MNHN ) was apparently the basis for all meristic and morphometric data reported. Regan and Trewavas (1930) described M. danae based on two specimens captured in the Gulf of Panama. They used the relatively small size of the PO as the singular character to set this species apart from both M. niger and M. indicus, the two species considered valid by Regan and Trewavas. The difference in size of the PO is due to sexual dimorphism. Both the lectotype (ZMUC P201990) and paralectotype (BMNH ) are females; the PO size of both specimens (1.1 and 1.5% SL, respectively) fall well within the range for females of M. niger (Table 1). In their review of the Malacosteidae, Regan and Trewavas (1930) described M. niger from 16 specimens; of those five that were examined in the course of this study, all mature specimens were males possessing relatively large Fig. 4. Left lateral view of heads of Malacosteus australis, new species: (A) holotype, AMS I , male, mm SL; (B) paratype, CSIRO T879, female, mm SL. POs. Thus, it is apparent that in describing M. danae as distinct from M. niger, Regan and Trewavas overlooked sexual dimorphism. Malacosteus australis, new species Southern Stoplight Loosejaw Figures 4, 5; Tables 1, 2 Malacosteus indicus (non Günther, 1878): Brauer, 1906:65 (in part). Malacosteus niger (non Ayres, 1848): Hulley, 1972:214; Paxton et al., 1989:204. Malacosteus danae (non Regan and Trewavas, 1930): Aizawa, 1990:123. Malacosteus sp. Paulin et al., 1989:103; Gomon and Robertson, 1994:261. Holotype. AMS I , male, mm, Tasman Sea, off Brush Island, 35u369S, 150u559E, R/V KAPALA, Engle midwater trawl, station K , m, 27 Oct Paratypes. 40 specimens, mm. AMS I , 8 females, mm, 7 males,

9 894 COPEIA, 2007, NO. 4 Fig. 5. Left lateral view of Malacosteus australis, new species, holotype, AMS I , male, mm SL mm, collected with holotype; CSIRO T879, female, mm, off Tasmania, west of Hardwicke Bay, 41u399S, 144u229E, 16 July 1982; CSIRO T881, male, 93.0 mm, off Tasmania, southwest of Sandy Cape, 41u359S, 144u189E, 14 Oct. 1983; LACM , male, mm, Southern Ocean, 41u449S, 178u189W, 25 May 1966; MCZ , 2 females, mm, temperate South Atlantic Ocean, 35u599S, 17u159E, 1 May 1971; MCZ , female, mm, subtropical South Atlantic Ocean, 36u109S, 07u369W, 20 April 1971; MCZ , male, 115 mm, subtropical South Atlantic Ocean, 35u199S, 07u309E, 27 April 1971; SIO , female mm, male, 97.0 mm, subtropical South Atlantic Ocean, over south end of Walvis Rise, 32u279S, 08u499E, 6 June 1963; USNM , 11 females, , 5 males, , southern subtropical South Atlantic Ocean, off South Africa, 37u089S, 05u239E, 21 March Diagnosis. A species of Malacosteus with male PO % UJL, % SL; female PO % UJL, % SL; IP photophores 5 7[8] in 3 7 clusters. Description. UJL % SL (26.9%); LJL % SL (25.8%); longest dentary tooth % UJL (3.4%); EW % UJL (5.2%); AO % UJL (20.0%) and % SL (0.9%); male PO % UJL (4.1%) and % SL (1.3%; Fig. 3); female PO % UJL (3.5%) and % SL (1.4%; Fig. 3); predorsal length % SL (80.8%); preanal length % SL (80.5%); dorsal-fin base % SL (14.2%); anal-fin base % SL (15.2%); head length % SL (9.2%); body depth at cleithrum % SL (14.1%); body depth at anal-fin origin % SL (8.3%); caudal-peduncle depth % SL (2.2%); pectoral-fin length % SL (15.8%); pelvic-fin length % SL (19.4%); prepelvic length % SL (57.8%); pectoral-fin rays 3 4[5] (3.8); pelvic-fin rays 6; dorsal-fin rays (18.5); anal-fin rays (20.3); dorsal premaxillary teeth 4 22 (8.6), ventral premaxillary teeth 6 31 (15.7); dentary teeth on left side (32.2); IPp 4 8 (5.5), IPc 3 7[8] (5.1); PVp [3]4 8 (6.0), PVc 2 6 (3.3); VAVp 2 7 (5.7), VAVc 2 4 (3.0); ACp [0]1 3[4] (2.1), ACc 0 4 (2.0); OVp [3 4]5 9[10 11] (7.7), OVc 3 6 (4.2); VALp 2 6 (4.1), VALc 2 4 (2.9); branchiostegal rays 7 9 (8.2); total vertebrae (48.8). Size to mm. Morphometric and meristic data are reported in Table 1. Comparison. The small size of both the male and female PO distinguishes M. australis from its only known congener, M. niger (Fig. 2). Smaller specimens, less than 50 mm, may be confused with M. niger; however, in most cases M. australis can be distinguished from this species by the presence of a higher number of IP photophores (Table 2). The following characters of M. australis were found to differ significantly from M. niger (results of pair-wise statistical analyses are reported in Comparison under M. niger): male PO, female PO smaller as a percent of SL and UJL; EW smaller as a percent of UJL; UJL and LJL smaller as a percent of SL; pectoral-fin rays and number of IP, PV, VAV, AC, OV, and VAL photophores greater; dorsal-fin rays fewer (Tables 1, 2). Distribution and ecology. Malacosteus australis is distributed in subtropical and temperate marine waters of the southern hemisphere from approximately 25u to 45uS; elsewhere, this species has also been taken in the equatorial Indian Ocean and seas of the Indo-Australian Archipelago (Fig. 6). Of the 72 records of M. australis with complete capture-depth data, only four records represent specimens taken in trawls fished above 500 m. Thus, like its congener, it appears M. australis does not regularly migrate on a diel basis out of the mesopelagic. In addition, given the morphological similarity of these species, M. australis likely

10 KENALEY REVISION OF MALACOSTEUS 895 Fig. 6. Distribution of Malacosteus niger and M. australis, new species. Symbols may represent more than one record. uses the large AO in employing a far-red visual system as part of its foraging strategy. Etymology. The name australis is derived from the Latin austral, meaning southern, in allusion to the geographical range of this species. DISCUSSION Unlike many deep-sea taxa, species of the genus Malacosteus are somewhat common in museum collections worldwide. From the large body of material examined, two species of Malacosteus are clearly diagnosed. Malacosteus australis is distinguished most readily from its only known congener, M. niger, on the basis of a smaller PO in both sexes and several photophore counts (IP, PV, VAV, AC, OV, and VAL). Beyond these characters, the two species differ subtly, though significantly, in several morphometric characters including UJL, LJL, and EW. The amount of material examined in this study far surpasses that which served as the basis for descriptions of all nominal species. It is clear that the differential nature of characters used to diagnose these species can be attributed to intraspecific variation or sexual dimorphism in M. niger. Several authors, including Regan and Trewavas (1930) in their description of M. danae, overlooked sexual dimorphism, particularly in PO size. Hyoid barbel morphology provides the single most diagnostic character complex for a vast majority of stomiid species (Gibbs, 1986). In the absence of a barbel, the relative size of the PO is the most reliable diagnostic character for species of Malacosteus, as it is for species of Photostomias (Kenaley and Hartel, 2005). Many other males of stomiid species possess larger POs relative to females, including those of the malacosteine genus Photostomias and the melanostomiine genera Echiostoma and Eustomias (Krueger and Gibbs, 1996; Clarke, 2001; Kenaley and Hartel, 2005). The male PO of stomiids is most likely a signaling device, and may indeed be an indicator of fitness analogous to the secondary sexual characters of other vertebrates (Herring, 2000). Thus, the evolution of PO dimorphism may be explained in terms of a good genes model of sexual selection (Andersson and Simmons, 2006). In this case, the handicap principle (Zahavi, 1975, 1977; Grafen, 1990; Smith, 1991) may apply: males have evolved a costly trait that allows high-quality males to give larger displays, in this case greater bioluminescence, than low-quality males. Under this paradigm, male PO size is subject to opposing pressures: sexual selection forcing the organ larger and natural selection forcing the organ smaller because of its costs associated with metabolism and alerting potential predators. Under these pressures, male PO size in species of Malacosteus has independently stabilized, thus providing a relatively invariable character convenient for species diagnoses. It appears that M. niger is replaced by M. australis south of 30uS (Fig. 6). This suggests that one or several hydrogeographic features somehow act as barriers to an exchange of species either out of or into the southern transitional zone. The distribution of M. australis is largely restricted to the southern transition zone south of 30uS, with the exception of the equatorial Indian Ocean and waters surrounding the Indo- Australian Archipelago. The southern range of

11 896 COPEIA, 2007, NO. 4 M. australis appears bounded to the south by the sub-antarctic front. Why M. australis is largely bound to temperate southern transitional waters and yet occurs in the equatorial Indian Ocean, areas with dissimilar oceanographic properties, remains unclear. Sutton and Hopkins (1996b) and Sutton (2005) found that M. niger is largely planktivorous, with copepods being the most numerous prey item. The choice of relatively small plankters as prey does not appear to correspond with the morphology of species of Malacosteus, specifically the lack of an intramandibular membrane (i.e., floor of mouth absent), enormous gape and jaws, large blade-like dentary teeth, and absence of gill rakers. Mesopelagic planktivorous teleosts typically possess smaller gapes and numerous, filamentous gill rakers (Ebeling and Cailliet, 1974; Langeland and Nøst, 1995). Sutton (2005) presented a two-part hypothesis to explain this incongruence: (1) species of Malacosteus use a long-wave (red-shifted) visual system to search small volumes for prey, snacking predominantly on copepods in between rare meals of fishes; (2) because species of Malacosteus lack the inherent long-wave sensitive visual pigment present in Aristostomias and Pachystomias, they must consume copepods, more direct trophic links to bacteriochlorophyll, to sequester the raw material for long-wave sensitivity. Neither a pathway for the co-option of bacteriochlorophyll as a photosensitizer or a mechanism for reverse fluorescence by which the photosensitizer converts low-energy, long-wave photons to highenergy, short-wave blue photons has been identified. However, Douglas et al. (1999) confirmed that the same chlorophyll, composed of Chlorobium pheophorbides, is present in free-living copepods and in the gut content and retinal tissue of M. niger. In short, it is the consumption of copepods that allows species of Malacosteus to employ a unique predation strategy based on a stealthy red-shifted visual system. KEY TO THE SPECIES OF Malacosteus 1a. Male PO % UJL, % SL; female PO % UJL, % SL (Fig. 3); IP photophores 3 5 in 3 5 clusters (Table 2) Malacosteus niger Ayres, 1848 (worldwide in all oceans 66uN to30us; Fig. 6) 1b. Male PO % UJL, % SL; female PO % UJL, % SL (Fig. 3); IP photophores 5 7[8] in 3 7 clusters (Table 2) Malacosteus australis, new species (circumglobal in subtropical and temperate waters of the southern hemisphere, elsewhere in the Indian Ocean; Fig. 6) MATERIAL EXAMINED Specimens are listed north to south within ocean basins. Atlantic specimens are further arranged into Eastern and Western North Atlantic records; Pacific specimens are further arranged into North and South Pacific records. Catalog number is followed by number of specimens examined, size, and capture position. Missing data are not reported as such. Additional capture data is available via the institutions online collection databases. Malacosteus australis. South Atlantic: USNM , 3, , 36u499S, 12u179W; USNM , 1, 146.7, 37u89S, 5u239E; USNM , 20, , 38u149S, 1u159E; ZMUC P207233, 1, 113.7, 38u129S, 01u159E; ZMUC P207234, 1,133.4, 38u129S, 01u159E; ZMUCP207235, 1, 135.1, 38u129S, 01u159E; ZMUC P207236, 1, 127.6, 38u129S, 01u159E; ZMUC P207237, 1, 126.8, 38u129S, 01u159E; USNM , 2, , 39u199S, 03u159W;USNM268517,1,190.7,39u479S,43u309W; USNM , 2, , 40u019S, 07u259W; USNM , 1, 144.4, 40u189S, 35u079W. Indian: USNM , 1, 134.8, 07u149N, 59u539E; ZMUC P20487, 1, 82.2, 05u189N, 90u559E; ZMUC P20488, 1, 78.1, 05u189N, 90u559E; ZMUC P20493, 1, 118.6, 05u219N, 80u389E; USNM , 1, 99.0, 03u469N, 65u059E; USNM , 2, , 01u239N, 60u089E; ZMUC P208515, 1, 104.9, 00u079S,63u569E;LACM , 1,97.0,00u309S, 129u039E; USNM , 1, 97.2, 01u579S, 59u569E; SIO 69 21, 2, , 02u289S, 86u239E; ZMUC P208498, 1, 206.4, 04u059S, 128u169E; USNM , 2, , 05u559S, 64u489E; ZMUC P20571, 1, 117.3; USNM , 1, 114.0, 13u579S, 65u059E; SIO 61 36, 3, , 22u109S, 63u119E; ZMUC P208519, 1, u199S, 36u139E; SIO 69 27, 3, , 25u269S, 38u119E; USNM , 1, 179.2, 25u529S, 60u09E; USNM , 2, , 29u139S, 60u059E; USNM , 2, , 31u589S, 59u459E; BMNH , 1, 184.9, 32u019S, 101u599E; BMNH , 1, 128.1, 32u019S, 36u229E; USNM , 7, , 33u09S, 07u509E; CSIROH ,1, 116.4, 34u019S, 45u019E; CSIRO H , 1, 212.0, 34u019S, 45u019E; USNM , 1, 142.1, 35u139S, 23u049E; ZMUC P20553, 1, 38.8, 35u429S, 18u379E; ZMUC P208520, 1, 181.4, 35u429S, 18u379E; SIO 84 55, 1, 50.7, 35u429S, 28u359E; USNM , 1, 154.9, 40u519S, 64u499E; USNM , 1, 94.0, 41u079S, 59u529E. South Pacific: MNHN , 1, 165.8, 24u199S, 167u499E; MNHN , 1, 195.4, 24u349S, 179u129E; MNHN , 1, 253.2,

12 KENALEY REVISION OF MALACOSTEUS u039S, 168u459E; MNHN , damaged, 25u159S, 168u559E; MNHN , 1, 197.2, 25u389S, 167u389E; MNHN , 2, , 25u419S, 167u119E; AMS I , 1, 93.2, 30u009S, 167u399E; AMS I , 2, , 32u269S, 161u489E; AMS I , 1, 73.9, 33u239S, 152u379E; AMS I , 1, 202.0, 33u289S, 152u339E; AMS I , 3, , 33u289S, 152u259E; AMS I , 2, , 33u319S, 152u209E; CSIRO T884, 1, 180.0, 33u439S, 130u339E; CSIRO T887, 2, , 33u439S, 130u339E; AMS I , 1, 191.0, 33u44.59S, 152u249E; AMS I , 1, 67.5, 33u549S, 152u069E; AMS I , 1, 177.0, 33u589S, 152u209E; AMS I , 3, , 34u109S, 152u49E; AMS I , 1, 114.7, 34u349S, 168u579E; ZMUC P20589, 1, 147.9; ZMUC P20460, 1, 164.0, 35u369S, 171u529E; USNM , 1, 92.1, 35u129S, 170u259E; AMS I , 1, 129.8, 37u249S, 150u309E; NMNZ P , 1, 104.0, 37u439S, 168u549E; AMS I , 1, 164.0,38u459S, 143u009E;CSIROH ,1,151.0, 38u559S, 141u589E; CSIRO H , 1, 201.0, 38u559S, 141u589E; CSIRO H , 1, 103.2, 38u269S, 149u299E; CSIRO H , 1, 225.0, 38u349S, 149u289E; CSIRO H , 1, 154.0, 39u179S, 45u579E; LACM , 2, , 38u229S, 160u209W; CSIRO H680-2, 1, 86.0; CSIRO T880, 2, , 41u259S, 148u449E; CSIRO T888, 1, 145.7, 41u399S, 148u419E; CSIRO H1399-1, 1, 174.0, 43u349S, 145u369E; CSIRO H526-29, 1, 117.2, 43u539S, 150u099E; CSIRO H373, 1, 94.2, 43u579S, 150u299E; AMS IA.5514, 1, Malacosteus niger. Western North Atlantic: ZMUC P208768, 1, 140.8, 66u299N, 56u269W; ZMUC P , 1, 215.7, 65u559N, 56u219W; ZMUC P208687, 1, 159.8, 64u449N, 55u479W; ZMUC P208691, 1, 200.7, 64u449N, 55u479W; ZMUC P208692, 1, 196.8, 64u449N, 55u479W; ZMUC P208688, 1, 202.3, 64u409N, 55u379W; ZMUC P208747, 1, damaged, 64u259N, 56u409W; ZMUC P209062, 1, 190.2, 64u209N, 57u319W; ZMUC P208748, 1, 158.2, 64u109N, 57u219W; ZMUC P209002, 1, 167, 64u009N, 58u259W; ZMUC P209027, 1, 215, 63u209N, 55u059W; ZMUC P209060, 1, 158.4; MCZ 31612, 2, , 41u289N, 43u299W; MCZ , 1, 123.6, 40u159N, 66u79W; MCZ , 1, 107.6, approximately 40u009N, 69u009W; MCZ , 1, 148.4, 40u089N, 66u009W; MCZ , 3, , 39u559N, 67u249W; MCZ 53287, 1, 121.5, 39u389N, 70u039W; MCZ , 1, 101.8, 39u289N, 64u009W; MCZ , 1, 102.2, 39u279N, 65u359W; MCZ , 4, , 39u179N, 69u329W; MCZ , 1, 90.9, 39u059N, 68u009W; MCZ , 1, 114.8, 38u589N, 68u189W; MCZ , 1, 124.3, 38u589N, 71u159W; MCZ 53286, 1, 150.2, 38u529N, 69u199W; MCZ , 1, 122.2, 38u489N, 71u449W; MCZ , 1, 204.3, 38u399N, 71u549W; MCZ 65810, 1, 204.1, 38u399N, 72u059W; MCZ , 1, 106.5, 38u319N, 72u239W; MCZ , 1, 133, 38u229N, 70u529W; MCZ 53277, 2, , 38u049N, 67u049W; MCZ , 1, 127.6, 37u089N, 73u089W; MCZ , 1, 117, 37u029N, 73u329W; MCZ , 1, 111.9, 36u559N, 73u489W; MCZ , 1, 105.4, 36u029N, 71u239W; MCZ 53272, 1, 151.2, 35u409N, 67u099W; MCZ 53273, 1, 122.1, 35u349N, 67u469W; MCZ , 1, damaged, 34u519N, 70u219W; MCZ , 1, 94.7, 34u319N, 71u429W; MCZ , 1, 189.2, 34u299N, 71u549W; MCZ , 1, 124.2, 34u049N, 74u499W; ZMUC P20457, 1, 73; 34u009N, 70u019W; MCZ 53275, 1, 110.3, 33u379N, 65u399W; MCZ , 1, 149.6, 32u179N, 59u459W; UF41123, 1, 92.2, 29u399N, 80u059W; MCZ 41273, 1, 96.3, 27u2890N, 88u589W; MCZ 34255, 1, 164.3, 26u339N, 76u529W; MCZ 91011, 1, 68.1, 26u149N, 77u439W; MCZ 47774, 1, 137, 25u499N, 81u459W; UF , 1, 149.1, 24u259N, 76u109W, 6 March 1973; UF , 1, 111.8, 23u46945N, 76u589W; UF , 1, 148.5, 23u389N, 77u149W; UF , 2, , 23u389N, 77u709W; UF , 1, 144.1, 23u389N, 77u069W; UF , 1, 171.1, 23u349N, 76u439W, 1 Nov. 1974; UF , 1, 150.8, 23u579N, 76u009W; ZMUC P20456, 1, 76.8; 17u139N, 64u589W; MCZ 42397, 1, 85.6, 12u009N, 65u059W; USNM , 1, 132.6, 11u429N, 68u439W; UF , 1, 49.8, 09u159N, 55u269W; UF , 1, 68, 09u029N, 76u539W; NSM T- P40114, 1, 91.4, 07u539N, 54u059W; BMNH , 1, 131.5, 07u159N, 78u549W. Eastern North Atlantic: ZMUC P , 1, 159.1, 64u419N, 33u579W; ZMUC P208686, 1, 117.8, 66u149N, 30u229W; ZMUC P208298, 1, 201.5, 43u219N, 25u589W; MCZ , 1, 79.4, 43u009N, 21u429W; ZMUC P208300, 1, 179.7, 47u529N, 27u089W; ZMUC P208301, 1, 184.3, 47u529N, 27u089W; ZMUC P208287, 1, 165.3, 45u99N, 15u369W; ZMUC P208291, 2, , 44u129N, 20u049W; MNHN , 1, 121.7, 38u009N, 27u139W; BMNH , 1, 169.7, 37u339N, 25u229W; MCZ , 1, 107.9, 35u569N, 22u409W; ZMUC P20449, 1, 39.9, 35u539N, 07u269W; MCZ , 1, 87.4, 33u429N, 16u089W; MNHN , 1, 154.9, 33u109N, 09u299W; ZMUC P20454, 1, 145, 30u179N, 20u449W; MCZ , 1, 117, 18u299N, 29u139W; MCZ , 3, , 16u509N, 18u509W; BMNH , 1, 134.5, 10u489N, 20u039W; ZMUC P20455, 1, 112, 08u199N, 44u359W; ZMUC P207240, 1, 103.1, 07u329N, 20u549W; ZMUC P207242, 1, 149.1, 07u329N, 20u549W; MCZ 96776, 2, , 07u079N, 33u299W; UF , 1, 167.8, 06u319N, 22u069W; MCZ , 2, , 02u229N, 35u349W; UF , 1, 48.6, 05u099N, 04u049E; UF , 1, 131.1, 03u509N, 02u379W; SIO , 2,