Asexual Reproduction In Linuche Unguiculata (Swartz, 1788) (Scyphozoa : Coronatae) By Planuloid Formation Through Strobilation And Segmentation

14 Pages·1998·5.3 MB·

by  Fl Da Silveira

PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
lll(4):781-794. 1998.
Asexual reproduction in Linuche unguiculata (Swartz, 1788)
(Scyphozoa: Coronatae) by planuloid formation through
strobilation and segmentation
Fabio Lang da Silveira and Andre Carrara Morandini
Departamento de Zoologia, Instituto de Biociencias, Universidade de Sao Paulo,
Caixa Postal 11461, 05422-970 Sao Paulo, SP Brazil
—
Abstract. Scyphistomae ofLinuche unguiculata from Sao Paulo State, Bra-
zil, were reared for one year to study the life cycle of this warm-water species
(in subtropical western South Atlantic waters). We found L. unguiculata re-
produces more by the development of planuloids than by medusae. The scy-
phistoma is rejuvenated by an operculated regression-regeneration cycle. We
hypothesize that reproduction of the species by production, either via segmen-
tation or strobilation, and liberation of planuloids explains the absence of re-
ports of ephyrae and medusae in the area.
Jarms (1997) reviewed the history of unguiculata typically passes intervals of
knowledge about scyphistomae of Corona- many years between periods of production
tae. The only records of coronate Scypho- of large numbers of medusae (Russell &
zoa from the Brazilian coast are of the me- Tomchik 1993, Black et al. 1994); therefore
dusa stage of Nausithoe punctata Kolliker, it would not be strange that between these
1853, from the north of Bahia State (Goy periods the probability of finding medusae
1979) and material recorded during study were very small; the species was not L. un-
ofthe life cycle ofNausithoe aurea Silveira guiculata, although the characters of the
& Morandini, 1997, from the north of Sao periderm tubes of our material were similar
Paulo State. Silveira & Morandini (1996) to that reported in the species.
redescribed the scyphistoma of a coronate, Our field observations were thatno ephy-
Stephanascyphistoma corniformis (Komai, rae/medusae occurred in plankton or supra-
1936), from the south-east Brazilian coast. benthic samples during 1 yr and our labo-
The present study on the life cycle of L. ratory observations were that few polyps
strobilated producing a small number of
unguiculata was undertaken over a 14
ephyrae, but many planuloids were pro-
month interval. Observations werebasedon
duced together with segmentation of other
cultures of the scyphistomae from south-
scyphistomae. Thus, few ephyrae were pro-
east Brazil.
duced, which supports the second explana-
We found colonial coronate scyphisto-
tion.
mae (presumed to be L. unguiculata) fre-
quently in Sao Sebastiao Channel, and we
Material and Methods
asked: why are there no records ofmedusae
or of any dermatitis caused by their planu- Colonial scyphistomae (Fig. 1) were
lae? We presumed three possible explana- sampled from calcareous debris, mainly
tions to account forthis: the ephyrae belong fragments of the stony coral Mussismilia
to suprabenthic communities and are trans- hispida (Verrill, 1902) (Scleractinia, Mus-
ported to distant places, so that medusae of sidae) at 2-6 m depth by SCUBA diving,
this species are not found near the coast; L. in Sao Sebastiao Channel (23°50'S,
.
782 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
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Fig. I. Colony ofLinuche unguiculata, as seen soon after sampling. The living tissues are much contracted
within the base ofthe tubes. Note that the scyphorhiza (arrows) is delicate and encrusting. Scale: 0.6 mm.
VOLUME 111, NUMBER 4 783
Wim
^''^'
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Fig. 2. Colony of Linuche unguiculata. The oral discs of the scyphistomae are partly or fully extended.
Scale: 1.25 mm.
45°25'W), of the rocky shore at Urubu each with 2 to 8 living polyps (Fig. 2). The
Point and on Praia Grande reef, Ilhabela colonies were transferred into and main-
County, SP SampUng was done on one or tained in small Petri dishes containing
two days of every month, except August, about 70 ml of filtered sea-water. At least
from June 1996 until May 1997. We twice a month, the colonies were cleaned
searched for the colonies on lumps of the by gentle rubbing with a delicate brush or
calcareous substratum collected, with the by removing the many filamentous algae
aid of a stereomicroscope. Each monthly with fine forceps.
sample included a minimum of 15 colonies. In each search for medusae or ephyrae.
784 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
three plankton and suprabenthic faunal Free-swimming ephyrae, from strobilat-
samples were taken on three consecutive ing scyphistomae, were transferred into sin-
days following the sampling of calcareous gle airtight pots (universal samplers for
debris. Twenty-minute tows were made in medical analysis ZESTER® 140 ml). They
the vicinity of the sampling sites ofthe de- were fed from a deep-frozen stock of ho-
bris with a plankton net and a dredge (the mogenized clam gonads. The ephyrae and
last equipment according to Wakabara et al. medusa were fed every day. They were in-
1993) at a depth of 5 to 10 m, both with dividually immersed in the homogenized
mm
0.5 stretch mesh, using a small out- food, observed under a stereomicroscope
board motor boat. Two divers followed the until their stomachs were full, and removed
equipment to maintain the plankton net at to a new pot with clean filtered sea water.
m
3 below the surface and to prevent the Free-swimming planuloids (samples of
dredge from being clogged with bottom March, April and May 1997), produced by
sediments. strobilating or from segmenting scyphisto-
The scyphistomae reared in the Centro de mae, were transferred into single dishes, at
Biologia Marinha da Universidade de Sao 24 h intervals, for further observations.
Paulo (CEBIMar USP), at Sao Sebastiao, We studied the cnidome of live speci-
SP, were treated as follows. From 6 June to mens and of specimens preserved in sea-
25 July 1996 all colonies were kept at room water-formaldehyde solution. In preserved
temperature (18°C-28°C) and from 1 April tissues, only undischarged nematocysts
to 7 June 1997 halfwere kept at room tem- were measured.
perature (21°C-30°C, although during 24 h Voucher specimens are: National Muse-
the temperature range never exceeded 4°C) um of Natural History, Smithsonian Insti-
and one-half were treated with temperature tution (USNM 99376, 99377); Museu de
changes, 18-27-18°C (based on the month- Zoologia da Universidade de Sao Paulo,
ly averages ofsurface watertemperaturefor Brazil (MZUSP 12.355, 12.356); Museu
winter and summer in the area), at 7-day Nacional Universidade Federal do Rio de
intervals and 'Aa h light/dark regime inside Janeiro, Brazil (MNRJ 3126, 3127, 3128);
an incubator (FANEM® 347-CDG). The The Royal Ontario Museum, Canada, In-
scyphistomae reared in the Zoology De- vertebrate Zoology (ROMIZ B3010,
partment (IB, USP), at Sao Paulo, SP, were B3011); The Zoologisch Museum, Univer-
treated as follows. From 26 July 1996 to 11 sity ofAmsterdam, The Netherlands, (ZMA
June 1997 the June-February samples were Coel. 8507, 8508); Zoologisches Museum,
kept at controlled temperature (August-mid Universitat Hamburg, Germany, (ZMH
February a monthly increase of 1°C starting CI1639, CI1640, CI1641); and The Natu-
at 21°C; mid February-June, a monthly de- ral History Museum, United Kingdom,
—
crease of 1°C starting at 26°C following (NHM 1998.145, 1998.146).
the natural surface water temperature
monthly averages) and %s h light/dark re- Results
gime inside an incubator. The seawaterwas
changed and the animals were fed every We found no ephyrae or medusae ofLin-
other day with a deep-frozen stock of ho- uche unguiculata in plankton and supra-
mogenate of the clam Perna pema (Lin- benthic samples. During June 1996-June
naeus, 1767) (Bivalvia, Mytilidae). Some of 1997, over 240 scyphistomae were reared
the specimens collected in April 1997 were in the Zoology Department, at Sao Paulo
used to measure the periderm tube (total City, but none of them strobilated. Never-
length, diameter at aperture and base), and theless, on many occasions we observed
the internal cusp was examined in 42 pol- that some scyphistomae produced a peri-
yps. derm operculum closing the tube. The oral
VOLUME 111, NUMBER 4 785
disc and the gastric septa of those scyphis- tate clockwise upon its oral-aboral axis
tomae regressed, but the column remained while swimming. The short, translucentten-
and they were able to contract and extend tacles were situated within the clefts be-
within the tube. We followed some closed tween the lappets. The eight conspicuous
tubes over a varied period of 1-3 d, at the rhopalia were directed outward while the
end ofwhich the operculum opened and the medusa was at rest or downward during
polyp regenerated septa and the oral disc. contraction of the bell. The ephyrae of the
During the period late March-June 1997, remaining material were preserved before
among 559 scyphistomae (some 130 colo- reaching the medusa stage (Table 1).
nies) reared at room temperature in CEBI- At the start of segmentation, the polyp
Mar, only 6 strobilated (two in the same resorbed the oral disc and produced a peri-
colony) and 3 segmented irregularly. derm operculum, it acquired a transverse
At the start of strobilation, the polyp re- segmenting region overmost ofthe column,
sorbed the oral disc, the strobilating region and the segments tended to become spher-
occurred over most of the column, disc ical in shape. In one colony we observed
number varied from 8 to 17, and no oper- that in one operculate scyphistoma many
culum, of either periderm or tissue was planuloids appeared by irregular segmen-
present. Initially, the discs were set well tation. These fused together to restore the
apart and the remaining column tissues be- column of the polyp, but without differen-
tween them were bulged. From a few hours tiation of septa and oral disc (see sequence
to 3 d, the discs changed into irregular tis- in Figs. 6, 7). Thus, the process lasted until
sue fragments and most of the remaining the end of April. In some colonies, we not-
and interconnecting column tissues con- ed that after a few weeks, near the oper-
stricted. Only the distal disc enlarged and culum margin, a fissure developed through
metamorphosed into an ephyra (Fig. 3), which a few planuloids could emerge (Fig.
while the other discs directly transformed 8). The crack was apparently caused by the
into planuloids. Among the six strobilae, egress of the planuloids.
five released one ephyra each and in anoth- The measurements, length of the tubes
er the ephyra transformed into a planuloid and diameter at the base and at the aperture,
within the tube. Release ofthe ephyra (Fig. are: 1.8-12.7 mm, 0.12-0.49 and 0.25-0.68
4) varied from 1 to 3 d after onset of stro- mm. Most tubes had one cusp; none, two
bilation (Table 1). The earliest stage at or three were less frequent. The cusps were
which the ephyra acquired noticeably me- cup-shaped, with longitudinal ridges, main-
mm
dusa-like characters was at about 5 in ly at the broad round margin (Fig. 9). The
diameter (specimen 8, Table 1). The gonad axis of the cusp base outline was long, nar-
primordia were fourpairs ofradiatingtissue row, and parallel with the long axis of the
cords on each side ofthe perradii. At about tube, whereas the proximal end was bulging
47 d, each gonad pair had fused giving rise and circular (Fig. 9).
to four cleft crescents (Fig. 5). This medusa Liberated planuloids were elliptical,
had an anomalous number oflappets due to swam actively by cilia, and had transparent
an injury at early ephyra stage (fourteen epidermis and a gastrodermis with many
lappets, two perradial pairs being fused. zooxanthellae. Two planuloids (from spec-
Fig. 5). Most of the zooxanthellae were ir- imen 8, Table 1) settled on the bottom of a
regularly distributed within the gastroder- small Petri dish on 27 May and 01 June
mis, in side view mostly below the coronal respectively and were reared for 58 and 54
groove (Fig. 5) and in the comers of the d. Each zooxanthellate polyp had five ten-
lips of the manubrium. The lappets were tacles within 3 d. Each produced a delicate
round, and slightly overlapping in an or- cylindrical tube, without branching and
derly fashion, which made the medusa ro- without cusps.
786 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
A
If B
3 / GRCM GRCM /
Fig. 3. Strobila of Linuche unguiculata (April 1997). A, early strobilation phase, at 24 h, in which the
connections between the discs narrow and the distal disc is bigger; B, late strobilation phase, at 72 h, in which
the distal disc has differentiated into an ephyra and the remaining ones into planuloids. Scale: 0.6 mm.
VOLUME 111, NUMBER4 787
GWOfA
Fig. 4. Ephyra (oral view) ofLinuche unguiculata, two days afterrelease from the strobila. Note the many
zooxanthellae. (From photomicrograph). Abbreviations: eg = coronal groove, gf = gastric filament, r = rho-
palium, z = zooxanthellae. Scale: 0.6 mm.
Scyphistomae, planuloids and ephyrae tion ofthe species was based on the medusa
(Table 2) all had holotrichous isorhizas and stage (Swartz 1788) and it is wise to study
heterotrichous microbasic euryteles nema- both stages in the life-cycle to make a pre-
tocysts. cise identification (Jarms 1990, 1991). Wer-
ner (1979) was first to link the polyp stage
Discussion of Stephanoscyphus komaii with the me-
Our original assumption was that the co- dusa L. unguiculata.
lonial coronates in Sao Sebastiao Channel The lack ofeither ephyrae or medusae in
were Linuche unguiculata, considering the plankton and suprabenthic faunal samples
morphology and number of the internal had been difficult to explain. Their absence
cusps within the tube. The cup-shaped cusp was evidently due to the asex—ual reproduc-
is diagnostic of polyps of L. unguiculata tive modes employed locally direct trans-
(Leloup 1937, Ortiz-Corp's et al. 1987, formation of strobilating discs and segmen-
Jarms 1991). Moreover, the size and pro- tation originating planuloids, newly report-
portions of the periderm tubes were within ed reproductive strategies for L. unguicu-
the ranges ofL. unguiculata studied by Le- lata and novelties for coronates. Aral
loup (1937), Allwein (1968) and Ortiz- (1997:166) defined strobilation as the
Corp's et al. (1987). The original descrip- process by which scyphistoma produces
788 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
— —
Table L Observations on 8 colonial scyphistomae ofLinuche unguiculata. Abbreviations: St-e length of
—
per—iod ofstrobilation (ds) originating ephyrae,—St-p lengthofperiod ofstrobila—tion (ds) originatingplanuloids,
Se length of period of segmentation (ds), E ephyra development (ds), E/M observations (ds) of ephyrae
and medusa.
Scyphistoma 3 4
(samplemonth) (Jun96) (Mar97) (Mar97) (Mar97) (Mar97) (Mar97) (Mar97) (Apr97)
St-e 3 2 and 1
St-p —7 8 a—nd 1
Se 10
E 30
E/M 36 2" and 38 27 54
The ephyra was preserved to study the cnidome.
ephyrae: "This requires disc formation Therefore, the word segmentation in this
('segmentation') leading to fission, and also work applies to the transverse fission ofthe
metamorphosis in which structures of the scyphistoma, within an operculate tube,
polyp are lost and replaced in each disc comparable with the strobilation in which
with those of the developing ephyrae." all discs metamorphose into ephyrae. Wer-
/':"
:'
4:':':j/:-::.: '^f^^/:^^-"-".-.'•
GRCLNA
Fig. 5. Young medusa ofLinuche unguiculata. The animal is shown in side view, to show the darkpattern
due to the zooxanthellae in the gastrodermis and the arrangement ofthe paired gonads in cleft crescents. Note
that the nearest lappet is enlarged as result of injury and later fusion of two original lappets. (From life and
close-up VHS). Scale: 1 mm.
VOLUME 111, NUMBER 4 789
i .^
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I
B D
gskUA GRc^^^
tj-KOn
Fig. 6. Colony ofLinuche unguiculata undergoing segmentation. A, planuloidformation (3.rV.97); B, plan-
uloids almost distinct and the distal ones fused together (4.IV.97); C, regeneration ofthe column ofthe polyp
starts by fusion of planuloids (dark areas) and the stretching of basal tissues (9.IV.97); D, contraction of the
basal tissues, upon stimulation with a forceps, showing that the distal planuloids are entirely fused together
(9.IV.97). Scale: 1.25 mm.
ner (1973) reviewed the known variation of in place of consecutive strobilation within
the operculum in the scyphistomae of Co- one year the way solitary coronates are
ronatae. The only paper with a thorough ac- likely to do.
count of the strobilation of L. unguiculata Jarms (1997) reported shortened life cy-
is that of Ortiz-Corp's et al. (1987). They cles of five species of Coronatae, the trans-
observed the process in Puerto Rico, at formation of free ephyrae into planuloids
temperatures of 25-28°C (December-May) and these into new polyps, due to unfavor-
and 28-30°C (June-November), for 7 yr. able conditions of salinity, temperature or
They noted strobilation once a year, some- food supply. Planuloid formation by trans-
times within an operculate tube, with the formation offree ephyrae within the tube is
production offree-swimming ephyrae. Wer- known in the solitary Nausithoe planulo-
ner (1979) also accounted for the annual phora (Werner 1971, Werner & Hentschel
strobilation of L. unguiculata under labo- 1983, Jarms 1997) and N. aurea (Silveira
ratory conditions. Werner (1979:94) hy- & Morandini 1997), and by parthenogene-
pothesized that for the colonial coronates sis in Thecoscyphus zibrowii (Werner
"... their strobilation activities are geneti- 1984). A unique feature we have observed
cally fixed to one distinct short season." He is the differi—ng destiny of discs from the
argued that the surplus of energy stored by same strobila one ephyra and many plan-
—
the polyps is available for colony growth, uloids with differing regulative mecha-
790 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
t I
\ G«^GH\ GROA GP.CM
Fig. 7. Colony of Linuche unguiculata undergoing segmentation. A, the column of the polyp is almost
entirely regenerated (13.IV.97); B, contraction ofthe tissues, upon stimulation with aforceps, to show thatthere
is integration between the regenerated pieces, but that the column as a whole does not contract (13.IV.97); C,
column totally regenerated, but the dark areas indicate the remains offusing planuloids (14.IV.97). Scale: 1.25
mm.
nisms for each developing structure. Fol- to a subtropical area in which there is a
lowing the reasoning of Jarms (1997:275) marked influence of both warm and cold
on planuloid formation byA^. planulophora, water masses (see Campaner 1985). The ab-
we believe the planuloids ofL. unguiculata sence of ephyra and medusa from plankton
must be an alternative dispersive stage, and suprabenthic samples is thereby ex-
since we have observed settlement and de- plained.
velopment of two new colonies. We hy- The ephyrae (Fig. 4) and the young me-
pothesize that segmentation is an advanced dusa (Fig. 5) closely resemble the descrip-
trait derived from the peculiar strobilation, tions of the adult medusa ofL. unguiculata
with the addition ofthe operculum, perhaps (Mayer 1910, Ortiz-Corp's et al. 1987). The
the most derived response to the regulation medusa illustrated in the present paper re-
of asexual reproduction in the species. L. sembles the developmental stage that May-
unguiculata is a warm-water species (May- er (1910:559) described "that the gonads
mm
er 1910, Kramp 1961, Ortiz-Corp's et al. appear when the medusa is about 5
1987), and we have observed a new repro- wide." The arrangement of the gonads and
ductive mechanism of the species to adapt the shape and coloration ofthe umbrella are