DESCRIPTION

1 This work was supported by National ScienceFoundation Grant GB 20993. Manuscript received10 May 1972.

2 Department of Oceanography, University of Ha­waii, Honolulu, Hawaii 96822.

VERY LITTLE IS KNOWN about the reproductivehabits of oceanic cephalopods, particularly thoseinhabiting the deep sea. Recently a specimen ofthe poorly known octopus Bolitaena microcotylaHoyle, 1886, was captured off Oahu, Hawaii.The specimen was taken at depths between 830and 975 m in an opening-closing mid-watertrawl (modified Tucker Trawl). Off Hawaiithese depths lie within the bathypelagic zone.Examination of the specimen revealed that itwas a brooding female.

Brooding in a Bathypelagic Octopusl

RICHARD EDWARD YOUNG2

ABSTRACT: A mature female and 12 larvae of the octopus Bolitaena microcotylawere captured at bathypelagic depths off Hawaii. The female appears to have beenbrooding the larvae in a large chamber formed by the oral arms and web. Thisfinding supports the likelihood that the brooding habit is universal in pelagic incir­rate octopods.

usual position. They arch forward and convergenear their tips. All of the arms except the twoventral ones are connected by a deep web whichis characteristic of this species. The web islongest between the dorsal arms where it reachesabout 60 percent of the arm length, becomesprogressively shorter between arms I and II,arms II and III, and arms III and IV althoughstill extending to about 40 percent of the armlength in the latter. The web is almost com­pletely lacking between the ventral arms. Thearms and web, therefore, form a capacious pouchwhich, very likely, held the larvae (Fig. 1A).Unfortunately all of the young had been dis-

In formalin, the small female specimen has a lodged by the time the specimen was examinedlateral mantle length of 30 to 35 mm and a total and no remnants of egg capsules, stalks, or anyof about 75 mm. Although fragile-it has the special modifications for egg attachment wereconsistency of a jellyfish-it was only slightly found.damaged in the trawl. A number of larval octo- The buccal mass, which lies at the posteriorpods were fortuitously attached to the head and end of this pouch is entirely sealed except for abody of the adult by radiolarian skeletons. minute central pore. This closure is not formedNearly all of the fragile deep-living octopods by the fusion of the lips that surround the buccalthat have come to my attention have had radio- mass; rather, it is the integument of the orallarians stuck to their bodies as a result of con- surface of the buccal crown that extends over thetact within the trawl. The larval octopods are lips and buccal mass. Careful examination ini­equally susceptible to empalement by radiolar- tially failed to reveal the presence of any open­ians, and it was by this means that they were ing. Only when the overlying integument wasattached to the surface of the adult specimen. being dissected, did pressure by the scissors

___-'-A~.----.tolaLoLlLlar.Yae--.ReRLecjL"-eftd~~.duding,--=-f~or::.'c:.:-e---a...s-.-m-:oa=-I---1 a_:om.:.-o:.:_u...n:.:-t of w...h...i...te~fl",oc,":,cu=le..,.nc"t m=at"e",n...·a",I 1

a few that were found in the bottom of the through the integument, indicating the presencespecimen jar; all were at the same stage of de- of a minute pore. Although it was still impos­velopment. sible to see the pore, a short canal was detected

The arms of the female are in a rather un- leading from a cavity around the lips and beaksto the area where the pore was presumed to be.The presence of this canal suggests that a poreand not a rupture allowed the material to es­cape. The flocculent material consisted of acellular debris heavily infested with several

400

Brooding in a Bathypelagic Octopus-YOUNG 401

A

c

St.Cae.

Hep. Int.

B

Br. H.--+--~~""

FIG. 1. A, lateral view of Bolitaena microcotyla. Dashed line indicates extent of brood chamber; B, larvaof B. microcotyla; C, mature egg from ovary.

SYMBOLS: Br. H., branchial heart; Cae., caecum; Cr., crop; Es., esophagus; Fu. 0., funnel organ; G., gill;Hep., hepatopancreas; Int., intestine; Int. Y. S., internal yolk sac; M., mantle; Op. L., optic lobe; P. Sal. Gl.,posterior salivary gland; St., stomach; Stat., statocyst; Ste. G., stellate ganglion; Subes. M., subesophageal massof brain; Sue., suckers.

types of ciliate protozoans. This same materialcould be squeezed from the buccal mass, andsimilar debris including the ciliates was found

--in-the-stoma'chohneOLtopus.The ovary is depleted except for a single large

egg and a residue of deteriorating ovarian tis­sue. The egg is ovate, 2 by 1.5 mm, and pos­sesses a short stalk (Fig. Ie). The digestivetract apparently is in a state of degeneration. Thecrop is collapsed and the stomach is contractedand infested with ciliates. The hepatopancreas isvery small and the posterior salivary glands aresmall and flaccid.

The larvae measured 2 mm in lateral mantlelength (Fig. 1 B). The eight stubby arms eachcarry four large suckers. The distal two suckersfrequently he on opposite sides of the arm, ap­parently due to crowding. The eyes are large,elliptical in outline, and directed forward. Athin layer of iridophores lies on the surface ofeach eye. The mantle is thick and gelatinous.Large reddish brown chromatophores are scat­tered over the surfaces of the mantle, head,arms, and dorsal surface of the visceral mass.The larva has the same general appearance asthe adult, except that it has relatively shorter

402 PACIFIC SCIENCE, Volume 26, October 1972

DISCUSSION

The order Octopoda consists of two sub­orders: the Cirrata, the finned octopods, whosemembers are benthic, benthopelagic, or pelagic(Roper and Brundage, in press); and the In­cirrata, octopods without fins. Incirrate octopods

arms and larger eyes that face anteriorly. Thelargest portion of the viscera consists of theinternal yolk sac which suggests that the youngoctopods had only recently hatched from theegg capsules. In several larvae an elongate pel­let was found in the digestive tract at the junc­ture between the esophagus and crop. The pel­let is composed of a mass of droplets of varyingsizes, presumably yolk.

generally are regarded as benthic animals butsix of the nine families are wholly pelagic. (Thevast majority of species, however, occurs in thebenthic family Octopodidae.) The pelagic in­cirrate octopods are probably derived frombenthic ancestors since their general morphologyretains many of the benthic adaptations foundin their bottom-living relatives. The pelagicrealm has been invaded by octopods on morethan one occasion during their history. A greatnumber of species of octopods lay small eggs

CONCLUSIONSwhich produce small larvae that spend con-

The evidence, summarized below, clearly in- siderable periods in the plankton. These larvaedicates that this specimen of Bolitaena micro- generally are similar to juveniles or subadultscotyla was brooding larvae at the time of cap- except for their relative body proportions, andture. they may reach considerable size while in the1. Twelve recently hatched larvae are associated plankton. A mantle length of 25 mm and an

with a female octopus. arm spread of over 100 mm was recorded for a2. The arms and web form a large chamber pelagic larva taken off California (Young, in

suitable as a brood pouch. press). This larva is larger than the adults of3. The mouth is almost completely sealed and, some benthic octopods (Robson, 1929:1) .

apparently, incapable of ingesting food Seemingly the transition to a wholly pelagicparticles. existence by an octopus with an extended larval

4. The digestive tract appears degenerate and stage would not be great, although a numbernonfunctional. of modifications would be required. One of

5. The deteriorated and depleted condition of these concerns the reproductive habits.the ovary indicates that the octopus had As far as is known, all shallow water benthicspawned. octopods attach their eggs to some solid sub­

strate, usually rocks, coral, or shells. After de-Shallow water octopods feed rarely or not at positing the eggs, the female broods them until

all while brooding their embryos (Nixon, hatching. The brooding process apparently as­1969). Therefore the apparent cessation of sures (among other things) that the eggs arefeeding in this animal is not unexpected. Feed- properly ventilated. Pelagic incirrate octopods,ing, seemingly, would be incompatible with as far as is known, have not adopted what mightoral brooding. Since the web between the ventral seem to be the simplest solution to this problem,arms is almost totally lacking, the funnel, pre- i.e., abandonment of the brooding habit and thesumably, could extend into this gape or, at least, production of free-floating eggs or egg masses.reach between the ventral arms when the oral Rather, they have retained the brooding habit,crown is flexed ventrally. In either case insertion which has necessitated considerable adaptation.of the funnel into the brood chamber would There are three families of octopods which

____provide a means of depositing~Dgs,,----,ac:::n,,-,d,,----,o:c:f,-_a_r,e.-e~p~ipLe:-.l~ag,;-ic:Argonautidae, Tremoctopodidae,directing water currents over the embryos. and Ocythoiaae. (A fourtnfamJ1y,theA:n'-:cop=o=---~

sidae, has been reported many times in the near­surface plankton, but species in this family arealso found associated with the bottom [Thore,1949]. Their habits are not clearly under­stood.) Female members of the monotypicgenus Argonattta form delicate shells throughsecretions of the dorsal arms. Egg strings areattached to the inner ~nds of the shell, where

Brooding in a Bathypelagic Octopus-YOUNG 403

LITERATURE CITED

ACKNOWLEDGMENTS

I would like to thank the following peoplefor reading and commenting on the manuscript:C. F. E. Roper, Smithsonian Institution; S. v.Boletzky, Laboratoire Arago; J. M. Arnold, Pa­cific Biomedical Research Center; and J. Wal­ters, University of Hawaii.

brooded. All species of epipelagic octopods areknown to have some means of brooding theiryoung. It seems likely that the remaining pelagicincirrate octopods also possess this habit, eventhough some evidence to the contrary exists.Thore (1949) examined the Dana collectionsfor eggs of bathypelagic octopods. He foundeggs in four deep trawls which he attributed toEledonnella pygmaea and Japetella diaphana(both family Bolitaenidae). He suggested thatmating and oviposition in these species takeplace at great depths and that the ova float ingreat clusters at these depths until hatched.Clearly more information is needed before wecan be certain that brooding is universal in pe­lagic incirrate octopods.

they are brooded by the female. The shell mayalso function as a buoyancy device by trappingair at its apical end (J. Z. Young, 1960) andundoubtedly functions as a protective structure.In octopods of the monotypic genus Tremoeto­pus, the eggs are attached to short, rodlike struc­tures formed by interwoven and cemented eggstalks. The rods are held by the suckers of thedorsal arms and the eggs are brooded in thislocation (Naef, 1923). In female members ofthe monotypic genus oeythoe, the oviducts areextremely long and convoluted and can holdgreat quantities of eggs. Embryonic develop­ment proceeds as the eggs slowly move downthe oviducts (Naef, 1923). This animal is,apparently, ovoviviparous.

There are three families of bathypelagic ormesopelagic incirrate octopods: Bolitaenidae,Amphitretidae, and Vitreledonellidae. Informa­tion on spawning habits was previously knownfor only a single species in these three families.Joubin (1929) found hundreds of larvae withinthe mantle cavity of a specimen of Vitrele­donella riehardi. (Thore, [1949] consideredadults of this species to be bathypelagic.) Somespecimens were also found near the bases ofthe arms around the mouth. Peculiarly, threeembryos were found embedded in the skin onthe dorsal surface between the first and secondarms on the left side. Joubin had no explanation HOYLE, W. E. 1886. Report on the scientificfor this occurrence. The relative size of the results of the voyage of the H.M.S. Chal-mantle of this species is rather small. Joubin's lenger during the years 1873-1876. Vol. 16,specimen had a total length of 330 mm and the pt. 44, Cephalopoda, p. 1-246. Reprinteddorsal arms had a length of 240 mm. The man- 1966. Johnson Reprint Corp., New York.tIe length, therefore, must be about 80 mm (see JOUBlN, 1. 1929. Notes preliminaires sur lesThore, 1949: 58). In spite of the small cavity, cephalopodes des croisieres du "Dana"there can be little doubt that the larvae origi- (1921-1922). Octopodes ze partie. Ann.nated within this cavity. This octopus apparently Inst. oceanogr., Paris 7: 1-24.brooded its embryos somewhere within the man- NAEF, A. 1923. Die Cephalopoden. Fauna u.tIe cavity or viscera and, therefore, has quite a Flora Neapel, monogr. 35, pt. 1 (2) :149-different method from that described here for 863.--B()Ht-aentt;-lt--is-interesting-that;-in-buth-of-th:~es~e'--N-l~X~O!-N:-,-M-.-1-9-69-.-T-he-h-·f-es-p-a-n-o-f-O-et-o-p-u-s-v-u-l_------I

species, larvae, not embryos, were found with garis Lamarck. Proc. Malac. Soc. Lond. 38:the female, indicating that the brooding period 529-540.extends past hatching although it is possible thatthe trauma of capture initiated hatching. ROBSON, G. C. 1929. A monograph of the re-

Bolitaena mieroeotyla is only the second spe- cent Cephalopoda. Part 1. Octopodinae.cies of bathypelagic incirrate octopod in which British Museum. 236 p.the reproductive habits are clearly known. In ROPER, C. F. E., and W. 1. BRUNDAGE, JR. Inboth of these bathypelagic species the young are press. Cirrate octopods with associated deep-

404

sea organisms: new biological data based ondeep benthic photographs (Cephalopoda) .Smithson. Contr. Zool.

THORE, S. 1949. Investigations on the "Dana"Octopoda. Dana Rep. 33:1-85.

YOUNG, J. Z. 1960. Observations on Argonauta

PACIFIC SCIENCE, Volume 26, October 1972

and especially its method of feeding. Proc.Zool. Soc. Lond. 133 (3) :471-479.

YOUNG, R. E. In press. Systematics and arealdistribution of pelagic cephalopods from theseas off southern California. Smithson. Contr.Zool.