Marine Biology 3, 8t--86 (1969)

Investigations on some tropical euphausiid species of the Indian Ocean L. A. PO)rOMAR~VA Institute of Oceanology, Academy of Sciences of the USSR; Sadovaya, Moscow, USSI~ A]~tract In spite of the great eoologic~l importanee of euphausiids in large axea~ of the sea, very little is known about their early developmental stages. During the 40th and 41st cruises of RV "Vityaz" (USSR) in the western part of the Indian Ocean, new information was obtained on the development of 2 species common in that area: Euphausia diomedeae and Styl~heiron carinatura. In E. diomedeae, the time between fertilization and hatohlng of the nauplius amounts to about 16 h; the metanauplius stage lasts 2 days, the calyptopis stage I also 2 days, and the calyptopis stage IX/up to 4 days, at water temperatures ranging from 22~ to 26 ~ The developmental stages of both species are described and illustrated. In~'oduetion

There have been few investigations of euphansiid eggs and early larval stages in comparison with later stages. This fact m a y be explained b y difficulties in ideniifieation of the former. All authors studying the early larval stages of enphausiids report the impossibility of their identification on the basis of material collected in the sea. Such identification is only valid when spawning females are caught and the development of eggs and larvae observed in aquariums. The development of main subarctic and antarctic species of euphausiids is well known from the works of a number of researchers. There are some data on the development of some species distributed in the tropical zone ( I m w ~ , 1955 ; GuP~EY, 1947), but most researchers have used material collected in the subantarctie zone ( S m ~ D , t953), the intermediate zone (BODE)r, 1950), or the Mediterranean Sea (L~mov~, t926; CaSa_WovA-Sou~IER, 1968). However, breeding biology, dimensions and, possibly, to some extent the morphology, of early larval stages of the same species, observed in the tropical zone and in colder regions, are rather different. There are, however, no new data concerning the development of euphansfid species inhabiting the tropical p a r t of the oceans. This is evidently caused, in the first place, b y difficulties in collecting material: even the most widespread species are seldom found in the tropical zone in great numbers. Furthermore, the eggs and early larval stages are extremely sensitive to temperature and salinity changes, and it is therefore necessary to examine t h e m immediately after catching. This is, however, possible only on big expedition vessels. Also, the tropical region eont~in~ few biological stations, most of which are situated on the mainland. The oceanic species axe consequently almost inaccessible. I n this paper the author proposes to fill in the gap to some extent, describing for the first time, chiefly the so far unreported development of early larval Biology,VoL3

stages of 2 of the most widespread species of enphansiids from the Indian Ocean. Methods

During the 40th and 41st cruises (January to June, 1967) of the research vessel "Vityaz" of the Institute of 0oeanology of the Academy of Sciences of the USSR, conducted in the western part of the Indian Ocean, hydrodynamical investigations were carried out on polygons, and material was collected on the development of 2 species of euphansfids : Euphausia diomedene and Stylocheiron carinatum. Although these species are the dominant ones of ~he tropical zone of the Indo-West Pacific and represent the most abundant forms in the Indian Ocean (Po)roMAR~VX, 1969), their development in these regions was hitherto nnl~own: the development of Euphausia d ~ had never been observed, while in Stylocheiron carinatum, nauplii, ealyptopis and furcilla I stages had been described on the basis of material from the Atlantic (L~Botm, 1926; LEwis, t955). Development of eggs and early larval stages was observed in the laboratory on board the 'Wityaz", during the 2 cruises mentioned above. Material and method Material was chiefly collected in a quadrangle sea area bounded by 11~ to 12 ~ and 64 ~ to 65 ~ Supplem e n t a r y data were obtained in the region south of latitude 5 ~ at the same longitude. Collections were made b y the J u d e y net oceanic model ( ;~ 80/113, mesh No. 38). Plankton was collected at 0 to 30 m depth, as the 30 m level was found to be the m a x i m u m or near m a x i m u m depth for collection of not only live, but also viable, material. Larvae, and often adult, crnstar~cans obtained from great depths usually die within minutes. I t is possible t h a t death is not only caused b y the rapid change of hydrostatic pressure during hoistlug, but also b y the period (although of short duration) of high oxygen deficiency during hoisting of the net and examination of a sample. I n the samples kept for i to 2 h, most p l a n k ~ r s die. Samples were poured into a crystallization vessel and, immediately after collection, eggs and larvae stages were transferred to vessels of 10 cm diameter and to petri dishes. During the first 12 h after collection the eggs were constantly observed with a binocular (lens M~BI-I). As the water temperature in the petri dishes rapidly increased until reaching air temperature

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L. iL Po~oMAm~vx: Eaplmusiid speciesof the Indian Ocean

(26~ to 28 ~ causing the eggs to die soon, the water in the dishes was continually cooled by a fan. The larvae were put into crystallization vessels andthe latter placed on porolon plates floating in water poured into a big crystallization vessel. In this way, the rather high vibration level caused by the ship's propeller was significantly reduced. Ice was added to the water when necessary. The optimal temperature for incubation was found to be 20 ~ to 24 ~ Observations on larvae at early stages were also carried out each half hour with the aid of a binocular lense. In 80 plankton samples, eggs and early larval stages were sorted out and measured.

Develolmmnt of Euphauda diomedeae Representatives of the genera Thysanopoda, Euphau~ffa, Pssudeuphau~ia, Nematoscelis, Nematobrach. /on and Stylocheiron are found in the tropical zone of the Indian Ocean. Crustaceans belongfi'ng to the 4 latter genera carry their eggs in bags. Only Euphau,Wa and Thysanopoda oviposit floating eggs. In our collections, the eggs of Euphauoia d~rmd.ene were easily defined, since females of this species twice oviposited in our aquarium. Bigger eggs (see below) were also found; they probably belong to the larger representatives of the genus Thysanopo&t, of which only T. tr/cusp/data is a very abundant species; it inhabits mainly the upper water layers (0 to 200 m). Until proof to the contrary, we shall therefore consider the large eggs and larvae as belonging to T. tr/cusp/data. The eggs were found in plankton samples throughout the period of the investigation, from the end of January until June, With maximum numbers in February and M~reh. Permanent occurrence of eggs and larvae in almost haft of the plankton samples taken from one point is evidence of a protracted spawning period of the species; the females of several populations appear to participate in reproduction successively, and to oviposit separately throughout the spawning period. This assumption is confirmed by the fact that, in both eases observed, the females caught oviposited in the aquarium no more than t0 to 20 eggs at a time. The protracted spawning period, however it may be achieved, is an advantageous adaptation for preservation of the species and, possibly, for increase in individual numbers. The pecnli~rities of euphansiid reproductive biology evidently guarantee preservation, despite their short life cycle, through rapid restoration of numerical strength. Significant numbers of larvae of a given stage present in the sea at one time, would result in considerable and rapid deterioration of feeding conditions. This would be of particular importance in the tropical zone which is rather poor in phytoplankten and coccohths used, especially by juveniles, as food source. Thus, the area of reproduction, and ultimately of feeding, is used with the utmost expediency.

Mar. B/o/.

The period of spawning, well-defined in subarctic and antarctic waters, is impossible to distinguish in tropical waters. Evidently the ornstaceans spawn several times during the year and protraction of the reproductive period of individual populations entirely masks the time limits of these periods, resulting in the wrong conclusion, that the spawning period is continuous. I t is, therefore, impossible to ascertain the frequency and dates of the spawning period according to the appearance of eggs in the plankton; 24-h collections are necessary. most eggs observed were collected on i9 November, 1967 at station No. 5733 (latitude ll~ longitude 64~ and in May/Jtme at latitude 5 ~ and longitude 64~ Approximately 373 eggs of Euphausla d ~ i ~ e were examined. The mea~alrements showed some distinctions in egg dimensions from 0.30 mm up to 0.42 EtzIn, w i t h

a

perivitelline

spar_A) of O . 0 4 m m .

Occasionally eggs were found with diameters of 0.35 mm to 0.38 mm and with very narrow perivitelline spaces (below 0.02 ram). Unable to identify these eggs with confidence, we tentatively assign them as belonging to Euphau~ia sp. During the last period of our work (May to early June) in the section at 5 ~ (longitude from 52~ to 68~ a number of very large eggs and nauplii of euphansiids (egg diameter 0.7i to 0.87 ram) w e r e found in the plankton. These dimensions were more than double those of eggs and nauplii of Euphausia d ~ , and this led us to consider the former to belong to Thysanopoda tricuspida2a. The eggs are transparent and slightly irradiate in oblique light; cleavage is the same as in all euphansiids - - complete, almost even, determinated and forming a celoblastum. At stage 32 of the blas~mem, 2 entoblasts appear. Two definite cells of 8, disposed around the entoblaat, form a mesoderm. Euphausiids, as most crnst~ceans possessing the same cleavage (Txv~E, 1909), have no invagination. On the whole, the morphology of cleavaged eggs of E. dio~md~ does not differ from that of other species. Observations on the cleavage of eggs and their further development were carried out with the help of a binocular lens. These observations have shown that the eggs, beginning With cleavage into 2 blastomeres, pass through all stages to the mnlticellular blastula within i h 30mln. Subsequent cleavage furrows appear, on an average, in 10 rain. An egg remains t h 20 rain in the blastula stage. The development of the egg from the gastrula stage to formation of the imuplii takes 3 h 40 mln ; development is then delayed, and a nauplius finally appears in 9 h 30 rain. The complete development lasts i6 h. The nauplins of Euphausia d ~ has an eggli~e, pink body with 2 spines at the terminal, 3 pairs of extremities, singie-hranched antennules, double-branched antennae, and mandibles. The antennules bear i long and 3 shorter bristles, antenna~ 3

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L.A. PONOMARgVA:Euphausiid species of t3ae Indlp,n Ooea~

83

Fig. 1. Developmental stag~ of Eui~haus/a d/omedeae. (a) Nauplius I; (b) n~uplius 1:[; (c) metanauplius; (d) calyptopis I; (o) calyptopis II, ventral view; (f) calyptopis ]3, lateral view; (g) furoilia II bristles on one branch and 2 on the other. During the t r a n s f o m a t i o n of nauplius I into nauplius I I the thorax legs (thora~Dpodae) are formed (Fig. ia, b). The mandibles become perceptibly reduced and no longer assist in swimming. The larvae remain in the stages of naupHns I and nauplius IX for 1 t to 14 h. The metanauplins has a carapace with denticles at the anterior margin and a sharp eminence on the terminal part (Fig. t c). The carapace does not cover the terminal part of the larval body upon which 6 terminal spines emerge (the lateral ones become perceptible at the next stage). Clearly visible are the anlagen of the thoracic legs (in the form of buds) and the mouth parts. The number of spines on the antennula remains the same. The metanauplius stage I s i s 2 days. I t should be noted that, under laboratory conditions, the larvae usually died at this stage, and the transformation of metanauplius into calyptopis had to be ob11"

served in larvae caught in the sea. At the metananplius stage the formation of the most complicat~t internal organs of the larvae takes place; at the same time, the larvae become most sensitive to changes in external conditions. I~BOUR (i926), using incubated early larval stages of the Atlantic species, was also unsuc~ in tracing the complete developmental cycle under laboratory conditions. A complicated organogenesis is also indicated by the following fact: the duration of each early stage is no longer than 14 h ; however, at the metan~uplius stage, it extends to 2 days, and at the calyptopis I stage to 4 days, i.e. almost as long as that of larvae of subtropical waters. Further observations were carried out with newly collected nauplii and metanauplii which were raised to metan~uplii and calyptopis I, I I and H I , respectively, i.e. by a
84

L.A. Po~o~(Aagv~: Euphansiid speoios of the Indian Ocean

We succeeded only once in tracing the development to the last stage. Three metanauplii from a plankton sample were not kept in the laboratory, but in a refl~gerator at a temperature of 10 ~ they developed into calyptopis I in 2 days and, within the 4 following days, into ealyptopis II. For comparison, we give the rate of development of the Pacific subarctic species: 5 to 7 days from fertilization to hatching, 2 days from nauplins int~) metanauplius (Po~TO~AREYA, 1963). However, the subsequent development from the metanauplins into the ealyptopis I and H is, in the tropical zone, 6 days, i.e. little different from the development of the analogous stages of subarctic species. One may assume that the low temperature of 10 ~ at which calyptopis lived in our experiment, acted as a delaying factor. During our observations, a similar temperature was recorded in the sea only at a depth of 400 m. According to our collections, the development of Euphausia dionmizae larvae occurs at lesser water deptlm with high temperatures, in particular at 30 m (at which depth the material was usually collected) and water temperatures not lower than 20 ~

Mar. Biol.

observed in petri dishes with the aid of a binocular lens. On the i4th February, t967, at i i p. m., for instance, we observed the hatching of nauplfi of a female caught at latitude il~ longitude 64~ (Fig. 2). No data have previously been published on such observations. The perfectly formed nauplii extended and contracted the anterior pair of appendages, pinning the egg membrane by short dense spines and then, parting their appendages (swimming movements), ruphlred the nearest part of the egg membrane and subsequently emerged into the surrounding water. After the hatching the female remained motionless and the nauplii swam near the rupVu_red bag. Within 24 h they dispersed throughout the aquarium. We did not encounter the nauplii of S. carinatum in plankton samples. Immediately after hatching they probably stay near the female also in the sea, i.e. at a depth of more than 30 m. The number of eggs of Stylocheiron species (as well as of other species which incubate their eggs in bags) ranges from 30 to 40, while species whose eggs develop in the sea produce hundreds or more than l(D0 (subarctic species) eggs per female. Evidently a great number of eggs are necessary for species which periodically gather in schools and are vigorously grazed upon; species with small egg numbers (tropical species) have a dispersed distribution and are not threatened by vigorous grazin g. Very small numbers (30 to 40 specimens) may, however, endanger the local existence of such species, necessitating egg-bag Fig. 2. Hatching of the nauplii in the brood pouch of Stylocheiron carinatura securitsr at an early developmental stage. I t should also be taken into The ealyptopis I has a considerably bigger carapace account that there is considerably less food available than the preceding stage, elongated in its terminM for larvae in tropical waters than in high latitudes. part (Fig. 1 d), and an elongated abdomen with i or 2 The nauplii of Stylocheiron carinatum clearly differ ehromatophores on its terminal region. The chromate- from those of Euphausia, the former possessing not phores are of different size, and are sometimes conju- egg-like, but heart-shaped configuration, with sculpgated. The telson bears i2 terminal spines on both tural back and 3 clearly-perceptible, translucent spots. sides. Thoracic legs begin to develop. The metanaupllns transforms after 24 h into the The ealyptopis H has a 5-segmented abdomen; its ealyptopis stage I (Fig. 3 c). In its general development telson carries t3 terminal spines; the anterior margin this stage is similar to that of other larvae of the family of the carapace still bears denticles, but the latter have Euphansiacea; S. car/nature differs in some morphologbecome larger and more sparse (Fig. te). The anten- ical features. nula has a 3-segmented basopedite; the number of The nauplii observed differed completely from bristles remain unchanged; the compound eyes are those described for the same species by L~BOV~ (1949), clearly perceptible; the first pairs of thoracic legs who obtained her material from the region of the become visible under the carapace. Insufficient information was available with regard Bermuda Islands (Fig. 3 a, b). The carapace of the calyptopis stages does not bear to furcilias.A drawing of the f u r c ~ II is presented in denticles and has a quite flat configuration (with no Fig. ig. elongated t e ~ l part) but a small eminence in the Development of Stylocheiron carinatum centre which, in following stages, shifts to its anterior Representatives of the genus Styloc~iron carry margin. The abdominal segments of the calyptopis II special bags or capsules in which the eggs develop to and IX[ stages terminate on each side in spines the nauplius stage. Females of S. carinatum were (Fig. 3d, e); the antennula bears 5 bristles on each placed in an aquarium and the hatching of nauplii branch and t spine at the end of the second segment;

Vol. 3, No. 2, 1969

L.A. PO~O~(A~VA: Euphausiid species of the Indian Ocean

85

Fig, 3. Developmental stages of Stylocheiron carinatum. (a)Nauphus I; (b) nauphus I I - acoording to L ~ o t m (i949); (c) calyptopis I; (d) ealyptopis II from side; (e) c~lyptopis II from 8,bove; (f) furci/ia IT

the telson (as well as the calyptopis I stage) has 6 t~rmlnal spines. At the c~lyptopis I ~ stage, the eyes are almost free fxom carapa~, the telson bears 7 termiual spines and its ex~rnM pair of lateral spines is highly reduced.

As already pointed out, we had Mmost no furcilia material. Furcili~ II, with a pair of pleopods as yet not overgrown with spines, is shown in Fig. 3f; its eyes are well developed and distinctly dividod into 2 parts wi~h ommatids of different lengths.

86

L h. P o ~ o ~ g v x :

Euphatmiid species of the Indian Ocean

Summary t. Very ht~le is k n o w n a b o u t the development of early larval stages of e u p h a ~ i i d s from tropical waters. New information on euphausiid species collected in the sea and observed in aquaria on board the R V '~Vityaz", is presented. 2. The development of Euphausia dlomed,e ~ and Stylocheiron car/nakum - - 2 of the m o s t widespread species of the I n d i a n Ocean - - is illustrated and described. 3. In Euphausia d ~ development from the egg to the nauplius stage takes approwimately 16 h. The nauplius passes t h r o u g h stages I and II in Ii to 14 h. Further development is protracted, the larvae remaining 2 days in the meC~nauplius stage. The calyptopis stage I lasts 2 days, the calyptopis stage I / up to 4 days. IAteratm~ cited BODm% B. P.: The post-naupliar stages of crustaeean Buphau~a pac/fica. Trans. Am. microso. See. 69, 5t5--527 (1950). C~ovx-So~, B.: Une s4rie larvaire d~na le genre N~C~-~/u~ ( E u p M u ~ i ~ ) . ~ h . ~Biol. mar. 9, 1---1t (1~S).

Mar. Biog.

G u ~ r r , R. : Some notes on the development of the Euphausiacea. Prec. zool. See. Lend. 117, 49--64 (1947). L~OVB, M~: On some larval euphansiids from the Mediterranean in the neighbourhood of Alexandria, Egypt. Proe. zooL SOc. Lend. ~ , 765--776 (i926). - - Some euplmusiicls from Bermuda. th'oc, zook Soo. Lond. 119, 111--1t_5 (1949). ~ , J. : Some larval euphausiids of the genus S~y/o~ron from the Florida Current. Bun. mar. SOL Gull Caribb. ~, t 90--202 (1955). Po~o~A~gvz, L. A.: The eupl~usfids of the Nort3a Pacific, theirclistn~but~onand eommon species.[Russ.].Monograph. pp 105--108. Academy of Sciences USSR 1963. - - The euphausfids of the Indian Ocean and the Red Sea. [Russ.]. Monograph. Academy of S0iencos USSR 1969

(in pr~).

S~AgD, K. : Taxonomy, digtribu~on and development of the Euphausiacea (CrusCacoa). Rep. B ~ N . Z . antarct. Re~. Expo~ 8, 3~-3S (1953). TXUBE, E. : Beitrgge zur EnLwdcklungsgoschichte der Euphausiiden. I. Die Forschung dos FAs bis zur G~rula~ion. Z. wise. Zool. 9~, 427 464 (1909). Author's address: Dr. L. A. PO~IOMARZVA In~Rut~ of Oceanology Aos.demy of Soiances of the USSR Sadovaja 1 Moeoow,J-387,~USSR

Date of nnal rn~nUs(Lriptaocoptadloo: Maroh 27, i909. Oommuni~tod by M~ E. VlsoGPaLuov, Moscow