Pacific Science (1975), Vol. 29, No.1, p. 19-25 Printed in Great Britain

Leachia pacifica (Cephalopoda, Teuthoidea): Spawning Habitat and

Function of the Brachial Photophores I

RICHARD E. YOUNG 2

ABSTRACT: Leachia pacifica reaches about 80 percent of its maximum length in near-surface waters off Hawaii, then abruptly descends to depths greater than 1,000 meters where maturation and mating occur. At these latter depths, large photophores develop on the tips of the third arms in females. The photophores provide a possible means for sexual attraction.

SMALL SQUIDS of the genus Leachia have been possible and retrieved with the ship moving thought to be epipelagic (Roper and Young, in slowly ahead. The net is pulled horizontally at press). However, off Hawaii the vertical distri­ 3 to 4 knots. Depth records for both trawls were bution of Leachia pacifica reveals an unusual obtained with a Benthos time-depth recorder. pattern, with captures as deep as 1,825 m. The Sectioned material was fixed in Bouin's sohj.~ pattern is closely associated with the stage of tion in seawater and embedded in Epon 812. maturity and the development of the brachial Sections between 1 and 10 It thick were cut on organs in females. This information bears on an A. O. rotary microtome with a steel knife two poorly understood subjects: the spawning and stained with Richardson's stain. habitats of oceanic squids and the function of their photophores. DESCRIPTION A brief description of Leachia pacifica is MATERIALS AND METHODS presented to facilitate subsequent discussion. Specimens were captured off the island of A full description is desirable but is postponed Oahu in the Hawaiian Archipelago at approxi­ until a later date. mately 158 0 18' W, 21 0 23' N, over bottom Leachia pacifica (Cranchiidae) (Figure 1c) depths of 1,500 to 4,000 m. Two types oftrawls reaches a maximum mantle length of about were used: a modified 3-meter Tucker trawl 60 mm. The thin-walled mantle is long, slender, and a 3-meter Isaacs-Kidd midwater trawl and transparent. A large pair offins, elliptical in (IKMT). The Tucker trawl opens and closes at outline, is situated at the posterior end of the the fishing depth; hence, capture of specimens mantle. The eyes of adults are small, re~ching a during setting and retrieval of the trawl (i.e., diameter of about 5.5 percent of the mantle contamination) cannot occur. The opening­ length, and lie within the head (i.e., not on closing mechanism utilizes a mechanical release stalks); however, about 2 mm separate the optic that is activated by weighted messengers sent lobes from the central mass of the brain. The down the towing cable. third arms are nearly three times the length of The IKMT is always open, and occasionally the others. In males the right fourth arm is specimens are captured during the raising and hectocotylized; it is longer than the left arm lowering of the trawl. To minimize this con­ and has an expanded tip that carries large medial tamination, the trawl was dropped as rapidly as and reduced marginal suckers. Small photo­ phores are present on the eyes. In mature or

I This study was supported by grant GA-33569 from nearfy mature fema.les,· a· large organ (the the National Science Foundation. Hawaii Institute of brachial organ) occupies the distal portion of Geophysics contribution no. 631. Manuscript received each third arm. 24 January 1974. The larval stage (= pyrgopsis stage) is ex­ 2 University of Hawaii, Department of Oceanog­ raphy, Honolulu, Hawaii 96822. tended, as is typical of the genus. 19 20 PACIFIC SCIENCE, Volume 29, January 1975

A

il\,--- Br. Organ

Lum. Ep.

FIGURE 1. A, cross section of the third arm tip and brachial organ; B, cross section of the luminous epithelium of the brachial organ; C, ventral view of Leacbia pacifica; D, frontal section through the base of the luminous epithelium. ABBREVIATIONS: Ax. N., axial nerve; Lum. Ep., luminous epithelium; Trab., trabecula; Pig. Zone, pigmented zone; Chromat., chromatophore; Br. Organ, brachial organ.

indicates the total range fished by the net while Vertical Distribution open. Within this ra.nge the net usually fishes The catch records presented in Figure 2 predominately within a narrow zone, the mid~ provide a clear picture of the vertical distribu­ point of which is indicated by either an open tion ofL. pacifica. Symbols in the figure, how­ circle (male specimen) or a large solid circle ever, require some explanation. Tucker trawl (female specimen). The IKMT also fishes captures are represented by a vertical bar that primarily within a narrow vertical range. The Leachia paciftca-YOUNG 21

0 III~O 0 • , 0 ¢e • . •

00 0 0 400 0 • • 600 • 0 'l • 0 000 11

0 0

0 E1200 • I - I- Q.. 0 ~ 1400 tl -I 1600 - 1800

2000.

2200

20 30 40 50 60 MANTLE LENGTH,m m

FIGURE 2. Vertical distribution of Leachia pacifica off Hawaii. Large solid circles = depth of capture of males; large open circles = depth ofcapture offemales; small solid circles = presumed contaminants; bars = depth range of opening-closing tows; squares = depth of capture of specimens of undetermined sex. 22 PACIFIC SCIENCE, Volume 29, January 1975 total range, of course, extends to the surface fourth specimen captured at about 1,200 m and, therefore, is not represented in Figure 2. depth shared the same features. The probable depth of capture is determined The remaining seven females were captured from the horizontal phase of the tow in the at depths greater than 1,000 to 1,200 m. Only a same manner as for captures from the Tucker single specimen has undamaged eyes, and these trawl. Every IKMT tow below 100 m passed are sessile. The eyes in the other specimens through the habitat of the younger individuals probably were sessile or nearly so. All un­ during the setting and retrieval of the net. In damaged specimens have nidamental and ovi­ such circumstances some contamination is ex­ ducal glands larger than 3 mm. pected. I have assumed that five specimens Four of the seven females have large heavily (represented by the smaller dots in the figure) pigmented brachial organs at the tips of the were captured in this fashion. Numerous third arms; the tips of these arms were missing opening-closing tows in these same inter­ on the three remaining females. mediate depths where the contaminants are Three of the seven females appear to be near recorded failed to capture small specimens. or just past the spawning stage. In one ofthem, The pattern of vertical distribution is pecu­ captured between 1,450 and 2,310 m depth, the liar. Excluding contaminants, specimens less nidamental and oviducal glands greatly ex­ than 45-mm mantle length (ML) were taken in ceeded 8 mm in length (part of the gland was the upper 100 m whereas larger specimens were missing) and are greatly swollen, slightly pig­ captured throughout the water column from mented, and gelatinous. Discharged spermato­ 30 to about 1,800 m. Day and night captures phores, imbedded in the dorsal surfaces of are intermingled at all depths; therefore, diel the head and mantle, indicated that mating had movements do not occur. Although multiple occurred. The specimen was flaccid and rather captures occur in near-surface waters, generally gelatinous, features typical of squids near or only one specimen is taken per tow at depths just past the spawning period (Young 1973). below 100 m, indicating a solitary habit for Unfortunately, the ovary was lost during cap­ deep-living individuals. ture, so the reproductive state cannot be posi­ tively determined; however, the swollen acces­ sory reprodtictive glands suggest that spawning Maturation in Females had not occurred. Two other specimens appear The change in females from larvae to adults to be in the same state. These specimens, cap­ involves several structures besides the gonads. tured at depths between 1,305 and 1,445 m and Inlarvae, the eyes are located onlong stalks that between1,700 and 2,200 m have large gelatinous extend laterally from the head (stalked eyes). In and lightly pigmented remnants ofthe oviducal adults, stalks are absent and the eyes are in­ glands and a flaccid overall consistency. Both cluded within the head (sessile eyes). In adults, have lost the ovaries, nidamental glands, and the oviducal and nidamental glands are greatly most of the oviducal glands due to damage in enlarged, and large brachial organs develop on the trawl. Although discharged spermatophores the tips of the third arms. cannot be found in these two females, there is These developmental changes are correlated no doubt they are near or just past the spawning with changes in vertical distribution. The two stage. largest females found in near-surface waters There is relatively little difference in mantle have stalked eyes, small nidamental and ovi­ length between the largest larvae and mature ducal glands (about 1 mm and 0.5 mm in diam­ adults. Since death probably follows spawning eter, respectively) and unmodified third arms. (Young 1973), this species apparently has an The three females captured between about 600 abbreviated adult life. to 900 m dep11i hive sfalIreo eyes, slIghi:fyen­ larged nidamental and oviducal glands (about 2 mm in length), and third arms with flat and Maturation of Males expanded tips. The leaflike tips bear thin In males some correlation exists between trabeculae and are colorless or nearly so. A vertical distribution and the development ofthe Leachia pacifica-YoUNG 23 secondary sexual organs. Unfortunately, mature solved in the photographs (Figure lA, B), the specimens are lacking. Initial phases of hecto­ pigmentation seems dense enough in the intact cotylus development are apparent in specimens organ to prevent passage of light. at a mantle length of 25 mm that live in near­ surface waters. WelI-developed hectocotyli are found only in specimens captured at depths DISCUSSION greaterthan 600 m. Also thepenis and spermato­ The Brachial Organ phore glands are enlarged only in specimens found below 600 m. AlI males captured have The brachial organ is almost certainly a stalked eyes and lack spermatophores. photophore. The layer of heavy pigment that envelops the oral surface ofthe organ must have a light-related function. This layer develops in Structure of the Brachial Organs depths of more than 1,000 m where biolumi­ The brachial organs are large spoon-shaped nescent light is the only detectable light. The structures formed, in part, by the distal enlarge­ trabeculate membranes provide a potential ment ofthe protective membranes and muscular means of regulating emitted light. Although supporting trabeculae of the third arms (Figure these membranes are usually found coiled over lA). The enlarged trabeculae have a rather the luminous epithelium (Figure 1A) in cap­ gelatinous core ofloose, vacuolated, connective tured specimens, the heavy aboral muscle layer tissue with scattered transverse and diagonal of the trabeculae clearly indicates that the ani­ muscle fibers passing from the oral to the aboral mals are capable of extending and exposing the sides. Each trabecula has a broad muscle band oral surface of the organ. The action is similar over its entire aboral surface with fibers running to that which occurs when the fingers of the from the base to the tip. A narrow muscle handextendand close overthepalm. This move­ strand runs up the midline of each trabecula ment of the trabeculate membranes would along its oral surface. alIow the pigment layer to act as a screen, con­ The epithelium that lines the oral surface of cealing or exposing a luminous epithelium. the organ is highly folded into a network of The organ lacks the reflecting iridocytes interconnecting ridges (Figures lB, D). The characteristic ofmany cephalopod photophores, epithelium at the base of the ridges has a rather although the composite light organs of Vam­ uniform structure of short broad celIs. In con­ pyroteuthis and the tentacular organs of Chiro­ trast, the epithelium along the ridge crests con­ teuthis are known to lack iridocytes (Pickford sists of celIs with teardrop shapes, with the 1946, Chun 1910). The tentacular organs of smalI ends attached to the basement membrane Chiroteuthis have been observed to luminesce ofthe epithelium and with much ofthe bulbular (Y. Haneda, personal communication) and to ends free from contactwith adjacent celIs. These have a luminous epithelium formed into high bulbular celIs stain more heavily than the basal interconnecting ridges (Chun 1910) similar to celIs. Although no pigmentgranuleswere found that in Leachia pacifica. The photophores of in the oral epithelium in dissection offormalin­ Chiroteuthis and Leachia pacifica both lack a diop­ preserved organs, the bulbular celIs have a tric system. slight brown tint. No evidence of a secretory function could be seen in the oral epithelium. Function of the Brachial Photophores Each organ is heavily pigmented. Most of the pigment is not contained in chromato­ The use of photophores in sexual attraction phores, although sections reveal the presence of is welI known in the terrestrial environment; at least one chromatophor~in the m~di_an line e.g., fir~flies (Buck 194~, Seliger et al. 1964). In beneath the oral epithelium(Figure lB). Spheri­ neritic waters, photophores have been experi­ cal pigmentgranules lieinthe tissue immediately mentalIy demonstrated to playa related role in beneath the oral epithelium and lateral to it courtship behavior in the fish Porichthys notatus up to the ends of the trabeculate membranes. (Crane 1965). In the midwater environment, Although the pigment granules cannot be re- evidence is circumstantial. In some groups 24 PACIFIC SCIENCE, Volume 29, January 1975

(e.g., myctophids, ceratioids, idiacanthids) the four deep tows that captured two of the squid occurrence of sexually dimorphic photophore reported in this paper. These tows spent 18 patterns suggests a role in sexual attraction hours at depths from 1,450 to 2,300 m and cap­ (Marshall 1954, Nicol 1967). The most convinc­ tured only 130 specimens (in addition to the ing case has been made for the ceratioid angler squid) ranging from large copepods to fish. fish, in which the luminous esca of the female The same amount of trawling at a depth of 600 is thought to be important in attracting males, to 700 m would yield thousands of specimens although pheromones probably playa role as and a similar high number would be found in well (Bertelsen 1951, Marshall 1967). Sexual the upper few hundred meters at night. Mating dimorphism alone is not unequivocal evidence and spawning success is particularly critical in for a sexual attraction function. Bolin (1961) these squids, as they undoubtedly reproduce presented evidence that the caudal photophores only once. By descending to great depths they in the myctophid Tarletonbeania crenularis, which are guaranteed a relatively undisturbed mating are present only in males, aid in diverting the and spawning period. The presumed technique attention of predators from females. of mate location is, of course, far better suited Circumstantial evidence also suggests that to deep water where a flashing photophore is female L. pacifica use their brachial photophores less likely to attract a predator. as sexual attractants: (1) brachial photophores Although young larvae of L. pacifica are are present only in females; (2) the adult life found in surface waters, the depth of hatching apparently is abbreviated and brachial photo­ is unknown. Therefore, the consequences of phore development occurs just prior to sexual deep-sea spawning on embryos and newly maturity and mating; and (3) brachial photo­ hatched larvae cannot be determined. phore development and mating occurs at depths greater than 1,000 to 1,200 m. At those depths, downwelling surface light is insignificant, and SUMMARY mate location, presumably, poses a serious problem for a visually dependent animal. 1. Leachia pacifica obtains most ofits growth in Mate detection through a bioluminescent near-surface waters off Oahu, Hawaii, then signal has distance limitations. The concentra­ abruptly descends to depths of 1,000 to, at tion ofL. pacifica in deep water, therefore, must least, 1,800 m. be examined. Nine successful opening-closing 2. Sexual maturity and mating occur at depths tows below 1,000 m depth filtered an estimated of more than 1,000 to 1,200 m. 1,100,000 m3 of water. If each of the five 3. At these depths, large organs, presumed to females captured was placed at the center of a be photophores, develop on the third arms separate cubic volume of water equal to one­ of the females prior to mating. fifth of the total volume filtered, the minimum 4. These photophores are presumed to func­ separation of individuals would be 61 m. Such tion in sexual attraction. a distribution is, of course, highly unlikely; 5. The value of mating and spawning in deep however, itindicates that the density ofindivid­ waters may be related to lesser predation on uals is within a reasonable order of magnitude the adults during this critical period. for sexual attraction by bioluminescence to be effective. I wish to thank Clyde Roper, United States Museum of Natural History, Yata Haneda, Yokosuka City Museum, and Thomas New­ Possible Advantages ofSpawning in Deep Water bury, John Walters, Sherwood Maynard, and Deep waters lack detectable sunlight and are Steven Amesbury, University of Hawaii, for sparsely innaPltea: These conc:Iitions presutTI:. reading and comme-ntlng on the manuscri.pt. ably reduce the chances of predation upon I also wish to thank Thomas Clarke, University gravid females. An indication of the low popu­ of Hawaii, for supplying most ofthe specimens lation densities can be seen from the series of taken in open nets. Leachia pacifica-YoUNG 25

---. 1967. The olfactory organs of bathy­ LITERATURE CITED pelagic fishes. Symp. 2001. Soc. Lond. 19: BERTELSEN, E. 1951. The ceratioid fishes: on­ 57-70. togeny, taxonomy, distribution and biology. NICOL, J. A. C. 1967. The luminescence of Dana Rep. 39: 1-276. fishes. Symp. 2001. Soc. Lond. 19: 27-55. BOLIN, R. 1961. The function of luminous PICKFORD, G. E. 1946. Vampyroteuthis infernalis organs ofdeep-sea fishes. Proc. 9th Pacif. Sci. Chun: an archair dibranchiate cephalopod. Conf. 10: 37-39. I. Natural history and distribution. Dana BUCK, J. B. 1948. The anatomy and physiology Rep. 29: 1-40. of the light organ in fireflies. Ann. N.Y. ROPER, C. F. E., and R. E. YOUNG. In press. Acad. Sci. 49: 397-482. The vertical distribution of pelagic cephalo­ CHUN, C. 1910. Die Cephalopoden. I. Oegop­ pods. Smithson. Contr. Zool. sida. Wiss. Ergebn. "Valdivia" 18 (1): 1-410. SELIGER, H. H., J. B. BUCK, W. G. FASTIE, and CRANE, J. M., Jr. 1965. Bioluminescent court­ W. D. McELROY. 1964. Flash patterns in ship display in the teleost Poricht!?Js notatus. J3maican fireflies. BioI. Bull., Woods Hole Copeia 1965: 239-241. 127: 159-172. MARSHALL, N. B. 1954. Aspects of deep sea YOUNG, R. E. 1973. Evidence for spawning by biology. Hutchinsons, London. 380 pp. Gonatus sp. (Cephalopoda: Teuthoidea) in the high Arctic Ocean. Nautilus 87: 53-58.