gametogenesis and reproductive cycles in the sea anemone anthopleura elegantissima ...
TRANSCRIPT
Gametogenesis and reproductive cycles in the sea anemone Anthopleura elegantissima (Brandt, 1835)1.2
BRIAN L. JENNISON~ Deplrrfmenf ofZoology, University of Ccrl(fortiicr, Berkeley, C A , U . S . A . 94720
Received May 15. 1978
JENNISON, B. L. 1979. Gametogenesis and reproductive cycles in the sea anemone Anthopleuru elegctntissitner (Bl'andt, 1835). Can. J . Zool. 57: 403-41 1.
Reproduction in the sea anemone Anrhopleuru elegcrntissima was investigated in central California for 3 years. Gametogenesis of anemones from four sites is described, and annual reproductive cycles are compared at a harbor and protected outel- coast site. Anthopleura elegrrnrissirncr is dioecious, although one hermaphrodite was found. Spermatogonia arise in the endoderm of the mesenteriesof males, migrate into the mesoglea, multiply, and differentiate into spermatozoa. In females, oogonia arise in the endoderm and migrate into the mesoglea where they undergo vitellogenesis. Spawning is synchronous within each population. Gamete growth is correlated with increasing temperature, and spawning occurs during periods of peak summer temperatures.
JENNISON, B. L. 1979. Gametogenesis and reproductive cycles in the sea anemone Anthopletrru eleguntissimrr (Brandt, 1835). Can. J . Zool. 57: 403-41 1.
La reproduction de I'anemone marine Anfhopleuru elegernti.s.simu a fait I'objet d'une etude de 3 ans en Californie centrale. On trouvera ici la description de la gametogenese d'antmones venant de quatre points differents ainsi qu'une comparaison entre les cyles de reproduction dans un port et plus au large, en un point protege de la c8te. Anthopleuru elegantissimcr est une espece dio'ique; on a cependant trouve un individu hermaphrodite. Chez le mile, les spermatogonies se forment dans I'endoderme du mesentere, migrent vers la mesoglee, s'y multiplient et se differencient en spermatozoi'des. Chez la femelle, les oogonies se forment dans I'endoderme et migrent vers la mesoglee ou elles subissent la vitellogenese. La reproduction est synchronisee au sein d'une population. La croissance des gametes est reliee a I'augmentation de temperature et la reproduc- tion se fait durant les ptiriodes ou les temperatures estivales sont le plus elevees.
[Traduit par le journal]
Introduction studied gametogenesis and external brooding in Early workers in cnidarian reproductive biology Epiactis prol$era, and several workers have
were primarily concerned with embryology and studied aspects of the fine structure of anemone larval development (McMurrich 1890; Appellof gametes, primarily sperm (Dewel and Clark 19727 1900; Gemmill 1920, 1921) or variations in repro- 1974; Hinsch and Clark 1973; Clark and Dewel ductive strategy as a means of classification 1974; Hinsch 1974; Lyke and Robson 1975). (Stephenson 1929). This trend has continued The Present study describes gametogenesis in (Nyholm 1949; Riernann-zurneck 19691, and Anthopleura efegantissima, which occurs from recent work has dealt with events following Alaska to Baja California (Hand 1955; Sebens 1977) spawning (Chia and spaulding 1972; spaulding "d is "...certainly the most abundant anemone on 1972, 1974; Siebert 1973, 1974; siebert and the coast...'' (Ricketts and Calvin 1968, p. 42). This Spaulding 1976). Chia (1976) discussed patterns of species forms dense clones by asexual fission and sea anemone reproduction and proposed a scheme defends these through intraspecific aggression of evolutionary relationships based on various (Francis 1973, 1976). The annual nature of sexual methods of reproduction known in these animals. reproduction (Ford 1964) is reexamined and
Nyholm (1943) briefly described confirmed for populations in sheltered and exposed in Sugurtia troglodytes, and Chia and Rostron (1970) discussed gametogenesis, development, and Materials and Methods internal brooding in ~ c t i n i a equina. Dunn (1975) specimens of Anthopleura elegantissirnu were collected at 4-
to 8-week intervals from two sites at Bodega Bay, Sonoma 'This manuscript represents part of a thesis submitted for the County, and two sites at Morro Bay, San Luis Obispo County,
Ph.D. in Zoology at the University ofCalifornia, Berkeley. from December 1973 until September 1976. One site at Bo- ZContribution No. 26 of the Harbor Branch Foundation, Inc. dega Bay was Doran Beach Rocks, an area of protected outer 'Present address: Harbor Branch Foundation, Inc., R.R. 1, coast characterized by large boulders and shifting sandy beach
Box 196, Fort Pierce, FL, U.S.A. 33450. subject to moderate wave impact. The second site was on the
0008-4301 179IO20403-09$0 1.0010 @I979 National Research Council of CanadalConseil national de recherches du Canada
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TABLE 1 . Anthopleura elegantissima. Maturation stages of males
Stage Descriotion
Stage one First appearance of spermatogonia (see text for discussion of morphology) Stage two Spermatogonial proliferation; swelling of spermatogonial vesicles t o occupy one-quarter of mesenterial width Stage three First appearance of spermatocytes; further vesicular swelling (up t o one-half of mesenterial width) Stage four First appearance of tailed sperm; vesicles occupy up to three-quarters of mesenterial width Stage five Gonads ripe; sperm vesicles occupy entire width of mesentery Spawning Sperm vesicles breaking down; many tailed sperm present Residual Only a few unspawned sperm remain
inside of the Campbell Cove Breakwater, a jetty of large stone rubble which protects the entrance to Bodega Harbor. Anemones collected here were subject to no wave action other than that caused by the wake of passing boats.
The sites at Morro Bay were in a protected area of boulders and sand, located directly behind the breakwater at the entrance to the harbor, and in the thermal outfall of a Pacific Gas and Electric Company power plant. Neither site received high wave impact, but anemones living in the outfall were subject to high flow rates from the discharge tubes and to temperatures which were often as much as 10°C above ambient temperatures found at the control site. Anemones from all four sites were used for the study of gametogenesis. Reproductive cycles for the Bodega Bay populations only are discussed here; specific effects of thermal effluents on the Morro Bay populations have been re- ported elsewhere (Jennison 1978).
Following collection, anemones were relaxed in 50:50 sea- water and isotonic MgCI,, cleaned, fixed in Bouin's fluid, and embedded in paraffin for histological examination. Sections 8-IOpm thick were made on a rotary microtome, and routinely stained with picro-indigo carmine, and counterstained with basic fuchsin, although Ehrlich's hematoxylin, Heidenhain's iron hematoxylin, and Mallory's triple connective tissue stain were also used. The sections were examined and photographed under a compound microscope.
To assess female maturation at both Bodega Bay sites, oogonia and oocytes from each identifiable female were mea- sured from prepared sections under the microscope, using a calibrated ocular micrometer, after the method of Dunn (1975). A: least 50 gametogenic cells were measured from each female, and only those cells which had a distinct nucleolus were in- cluded in the total. Males were classified into arbitrary stages based on a visual assessment of their gonadal maturity (Table 1).
Results Spermatogenesis
The earliest identifiable male gametes are the spermatogonia, which can be found in the mesen- teries of anemones with no gonads. These cells are
round, contain densely staining nuclei and little cytoplasm, and are approximately 5 pm in diame- ter. They migrate into the mesoglea either singly or in clusters of a few cells, where they form vesicles up to 50 pm across (Fig. 1). As these cells undergo mitotic divisions, the vesicles expand and are strung out linearly, giving the mesoglea of the gonadal mesentery a distinctly beaded appearance.
As the spermatogonia differentiate into sper- matocytes, a layering of the gonial cells becomes apparent, with the more mature spermatocytes lo- cated proximally to the spermatogonia. The sper- matocytes are smaller than the spermatogonia, having diameters of approximately 3 pm. Sper- matids cannot be distinguished from small sper- matocytes at this level of resolution. The vesicles which contain these proliferating gametogenic cells expand to occupy more than half the width of the gonadal mesentery (Fig. 2).
At the first appearance of mature sperm, the tes- tis is visible to the unaided eye and is characterized in histological preparations by the densely staining condensed chromatin material of the sperm heads, which are between 0.7 and 1.0 pm in diameter. As the number of mature sperm per vesicle increases, the vesicles come to occupy 75% of the gonadal mesentery in cross section. The sperm nuclei cluster together in the center of each vesicle, filling the lumen with a bouquet-like arrangement of cells (Fig. 3). When ripe, vesicles fill the entire mesen- tery, and sperm may be stored in this manner for up to 4 months.
Just before spawning, the endoderm covering the
ABBREVIATIONS USED I N FIGS. 1-8. en, endoderm; m, mesoglea; n, nucleus; nc, nucleolus; o g , oogonium; s , sperm; Sg, spermatogonia; s t , surface tears of gonadal endoderm; s y , spermatocytes; r , sperm tails; tr, trophonema; v, spermatogonial vesicle; y g , yolk granules.
FIG. I. Spermatogonial vesicles. February 4, 1974. Scale = 50 pm. Fig. 2. Vesicles containing spermatocytes. March 2, 1974. Scale = 120 pm. Fig. 3. Bouquet-like arrangement of sperm. March 30, 1974. Scale = 40 pm. Fig. 4. Mature sperm vesicles, showing spermatogonia along the periphery of the vesicles. May 10, 1974. Scale = 90 pm. Fig. 5. Oocyte with prominent yolk granules. February 4, 1974. Scale = 20pm. Fig. 6. The oocyte-trophonemajunction. February 4, 1974. Scale = 10 pm. Fig. 7. A ripe female gonad. August 11, 1974. Scale = 150 pm. Fig. 8. A female gonad following spawning. August 8, 1975. Scale = 50 pm.
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sperm vesicles is stretched thin, and spermatogonia are limited to the periphery of the vesicles (Fig. 4). The sperm heads continue to cluster tightly, and the tails lie adjacent to the thin endoderm of the mesentery. At spawning, the sperm vesicles and the thin surrounding endoderm rupture, releasing sperm into the coelenteron. Some residual sperm may be recognizable in the mesentery for up to 4 months after spawning.
Oogenesis Ovaries are located in the same position along the
mesentery as testes. Gametogenic cells with rela- tively large nuclei and little cytoplasm are first dis- tinguishable in the endoderm when 8-15 pm in diameter; these are probably primary oogonia. These cells apparently multiply in the endoderm and develop into secondary oogonia. which are 15-25 pm in diameter. occasionally reaching 45 pm. These ceFIs I ine the mesogleal-endodermal border prior to migrating inlo the rnesoglea. As no oogonia were seen undergoing division within the mesoglea. it may he inferred that they have become oocytes by this time (Dunn 1475). Once within the mesoglea, the oocytes begin to grow, and 1 he ratio of nuclear diameter to cell diameter decreases. This expansion of the cytoplasm reflects the onset of vitellogenesis. Yolk granules appear in the oocyte and become evenly distributed throughout the cell. The germinal vesicle becomes peripherally located and contains a prominent nucleolus (Fig. 5).
During vitellogenesis, a structure referred to by Nyholm (1943) and Dunn (1975) as the trophonema arises between the oocyte and the edge of the mesentery (Fig. 6). The germinal vesicle of the oocyte always lies adjacent to this structure. By the time the oocyte has completed vitellogenesis, the trophonema has disappeared. Fully grown oocytes are 140-210 pm in diameter in fixed material, while living oocytes may reach 250prn. The mesentery of the mature ovary is swollen with oocytes, and the endoderm is very thin (Fig. 7).
Polar body formation was not observed; presum- ably the final maturation divisions are delayed until after spawning. At spawning, oocytes are extruded from the mesoglea, passed through the thin en- doderm, and released into the coelenteron. Freshly spawned oocytes exhibit raised projections of ap- proximately 1.0 by 10 pm over the entire surface of the oolemma; nuclei were not observed. Once in the coelenteron, the oocytes are passed up through the actinopharynx, probably by ciliary currents, and released into the sea. After spawning, the mesentery exhibits massive tissue damage; it is riddled with large spaces and surface tears (Fig. 8).
However, production of oogonia has continued throughout the period of oocyte growth, and these oogonia may be observed lining up near and enter- ing the still-stretched mesoglea. A few residual oocytes are nften found as well.
Although A )?thople~rr.n elepn1rtissi17m is dio- ecious, one animal collected ;it Campbell Cove on June 21. 1974. was a simultaneous hermaphrodite. Two fertile mesenteries were found: one contained oocytes ranging in size from 31 to 140 pm, while the other contained mature sperm. The remaining mesenteries were sterile.
R~productive Cycles In 1974, spermatogonia and spermatocytes were
seen in animals collected at Doran Beach in the winter, and the first tailed sperm had developed by April (Fig. 9). Ripe gonads were found in half of the males collected in May, and mature sperm were present until September, when spawning occurred. Residuak sperm were seen through December. This pattern was repeated in 1975 and 1976.
At Campbell Cove (Fig. 9), a few mature male anemones were found in March, 1974. Sperm were seen throughout the summer. and one individual was spawning in August. Spawning followed be- tween September and October 1974, althol~gh IT- sidual sperm persicted as late as January 1975. Early gametogenic stages were visible in .lanuary: these developed through the spring. Sperm were present in May, and spawning had hegun by July 1975. One animal had not spawned by October, but the rest of those collected had only residual sperm. Gonadal development was similar during 1976, ex- cept spawning took place between July and Sep- tember.
Although there were few oogonia in collections made during the summer at both sites (Fig. lo), there was an increase in oogonia following spawn- ing in 1974. Oogonial numbers fluctuated through- out the spring at both sites. but dropped prior lo spawning in 1975. They then increased during the winter. i ~ n d dropped through the spring of 1976. Oogonia increased again following spawning in 1976 (hy the end of Jul y at Doran Beach and bv late September at Campbell Cove).
Small oocytes were present in the first samples from Doran Beach in January and February 1974 (Fig. 1 1): these increased in size through the spring and summer. reaching maximum diameter in early September. when spawning occurred. Although no oocytes were found in samples collected in Oc- tober, they appeared by November 1974, and de- velopment proceeded as before through the winter and spring. to a peak in July 1975. Spawning oc- C
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curred between July and October, although some residual oocytes remained until the middle of De- cember. Oocytes of the 3rd year's cycle were pres- ent in October 1975, and they increased gradually in size until July 1976, when the population spawned. Oocyte diameters were smaller prior to spawning during the 3rd year as compared with the previous two seasons. Spawning also occurred earlier in 1976 than in either of the previous years.
At Campbell Cove a similar annual pattern was observed (Fig. 12). During 1974, oocytes increased in size in the spring and summer, with females spawning during September. The oocytes of the 2nd year appeared in November, remained rela- tively constant in size during the winter, and grew larger through the late spring and summer. Again, spawning occurred between the end of July and the beginning of October. By this time, oocytes of the third season were present; they increased gradually in size until the end of July, and the anemones spawned in August and early September. Through- out the project there was little temperature differ- ence between Doran Beach and Campbell Cove. However, there were well defined seasonal changes with highest temperatures in the summer at both sites (Fig. 13).
Discussion According to Stephenson (1928), the gonads of
sea anemones are cylindrical swellings of the mesenteries between the retractor muscle and the cnidoglandular tract and occur from the base of the animal upwards to about the level of the ac- tinopharynx. Gametes arise in the gonadal en- doderm, presumably from undifferentiated inter- stitial cells (Campbell 1974). They migrate into the mesoglea, where they mature.
Spermatogenesis in Anthopleura elegantissimu is similar to that found in Actinia equina (Chia and Rostron 1970) and Epiactis prolifera (Dunn 1975). As in these species, spermatogonia arise in the endoderm, enter the mesoglea, proliferate, and differentiate into mature sperm. Some sper- matogonia persist even in late summer, when the vesicles are swollen with mature sperm. Whether these cells represent a self-sustaining progenitor component similar to that which Holland and Giese (1965) found in the purple sea urchin Stron- gylocentrotus purpurutus is unknown, because after male anemones spawn, the spent gonad is completely resorbed, and the fate of these unde- veloped spermatogonia is obscured.
It was not possible to distinguish spermatids from spermatocytes in A . elegantissimu. Clark and Dewel (1974) state that the flagellum which is des- C
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o Doran Beach Campbell Cove
BODEGA BAY A eleganlissima
R
FIG. 10. Total oogonia per collection at both Bodega Bay sites.
I DORAN BEACH ROCKS
O"dspawn~ng
d d o n d pp spownlng f ' t 99 spowned out
99 spawned res~dual
0
30.
FIG. 11. Oocyte size-frequency distributions, Doran Beach Rocks (DBR).
tined to become the tail of the sperm is already present in the spermatocyte of Bunodosoma cuvernata, thereby obscuring positive identifica- tion of these stages, and Lyke and Robson (1975) report that it is difficult to distinguish between sec- ondary spermatocytes and early spermatids, even at the ultrastructural level.
Sperm may be stored for up to 4 months prior to spawning; whether they require nourishment dur- ing this time is unknown. Although Clark and
Dewel (1974) and Lyke and Robson (1975) both reported "lipid-like" vesicles in the heads of sea anemone sperm, the authors suggested that these are reserves for swimming and consummating fer- tilization, rather than for nutrition. One hypothesis concerning the prolonged nutrition of sperm has heen put forward by Chia and Crawford ( 1973) from their study of the pennatulacean Ptiloscrrctrs g~rr- neyi. They suggest that the sperm, which are ar- ranged in vesicles similar to those in sea anemones,
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CAMPBELL COVE BREAKWATER
0-25 Y. &begun spownlng
( 0 few res~dual sperm)
> 230- some ~nspowned d d r e r n a ~ n d d a n d 99 spawned
1974 1975 1976
M I 4 6 4 1 0 1 2 8 1 4 5 1 4 2 6 4 3 5 5 7 3 3 6 6 5 5
FIG. 12. Oocyte size-frequency distributions, Campbell Cove Breakwater (CCB).
20
I Sea Temperature
I BODEGA BAY
I ] o Doran Beach Campbell Cove
15
0
z- 10- 3 C
F g 7.5 E Q)
i--
- I I I I
5 - I I I 1
1974 I 1 1975
t 1 1976
I I J F M A M J J A S O N D I J F M A M J J A S O N D I J F M A M J J A S
l t t l t l l L l l t I t I l l l l I l t l
Ti me FIG. 13. Temperature patterns at Bodega Bay.
are nourished directly by diffusion of nutrients summer, and spawning occurring in the late sum- from the coelenteron. mer or fall. Although there were subtle differences
Males of A. elegantissima exhibit an annual re- between the two sites at Bodega Bay, the data productive cycle, with early gametogenic stages suggest that anemones at both sites are part of the occurring in the spring, ripe gonads present by same local reproductive population and that they
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spawn more or less synchl-onously in response to the same intrinsic or extrinsic cue(s).
As in males, female gametogenic cells arise in the endoderm, migrate into the mesoglea, and develop to maturity. This process in Anthopleura elegun- tissima is similar in many respects to that described by Chia and Rostron (1970) for Actinia equina and by Dunn (1975) for Epiactis prolifera. However, in A. elrgantissima and E. prolifera, the polarization of oocytes, as indicated by the position of the ger- minal vesicle, is in various directions. This con- trasts with A . equina, in which the germinal vesi- cles line up along one edge of the gonad. Further, growth of femalegametes in A. elegantissima is not necessarily synchronous within a single mesentery. This is also the case in E. prolij'eru, but in A. equina oocytes apparently develop synchronously within an ovary. As in E. prolij'eru, vitellogenesis is thought to involve a trophonema in A. elegantis- simrr. This structure was not reported in A. equina.
The development of a trophonema during vitellogenesis has been reported in Sagartia (Cal- liactis) pcrrasiticu (Hertwig and Hertwig 1879), Cericrnthus lloydii (Nyholm 1943), and Epiucris prolifera (Dunn 1975). A structure resembling a trophonema is visible in a photograph ofdeveloping oocytes of Metridium senile in Loseva (1971). However, in two other cnidarian groups a trophonema was not involved in vitellogenesis. Widersten (1965) did not find trophonemata in his study of four species of scyphozoans, and Kessel (1968) demonstrated completely endogenous yolk formation in trachyline medusae. Although Nyholm (1943) and Dunn (1975) suggest that the trophonema may provide a pathway for nutrient material from the coelenteron into the developing oocyte, the development and ultrastructure of the trophonema must be examined further before its function can be determined.
The oolemma of the freshly spawned A. elegan- tissima oocyte is raised into a series of projections approximately 1.0 by 10 pm. Similar projections have been reported in Peachiu sp. (Faurot 1895), Bolocera tuediae and Actinia equina (Gemmill 1920, 192 1 ), Peachiu quinquecapitata (Spaulding 1972), Tealia crassicornis (Chia and Spaulding 1972), A. elegantissima and A. xanthogrammica (Siebert 1974), and Cribrinopsis fernaldi (Siebert and Spaulding 1976). The ultrastructure of these projections has been examined in Bunodosoma cavernata by Dewel and Clark (1974), and in Peachia quinquecapitata by Spaulding (1974), where they were shown to be large microvilli. Similar microvilli have been reported in the scyphozoan Aequorea aequorea (Szollosi 1970),
and the pennatulacean Ptilosarc~~s gurnryi (Chia and Crawford 1973). The function of these mi- crovilli is unknown.
Oogonia proliferated rapidly in the post- spi~wning period of all three reproductive seasons at both Bodega Bay sites. However. these cells were present at least at low levels in all but 5 of the 54 collections. The continuous presence of oogonia suggests either that some are prevented from further development or that some represent cells of the following year's reproductive effort. However, the mass spawning of A . elegantissima in late summer, followed by gonadal shrinking and the resorption of unspnwned oocytes. suggests that oogenesis is a 1-year process in this anemone.
Combining the oocyte size-frequency data with the sperm development data, and comparing the outer coast and the harbor sites at Bodega Bay. it appears that differences in the timing of repro- ductive events between the two sites were minor. The spring proliferation of gametogenic cells and maturation of gonads of both sexes correlates well with the seasonal increase of temperature each year, and. although the data are not conclusive. spawning occurred during the period of highest summer tempera1 ures each year. These results are in agreement with those of Ford (1964) for anemones in Marin County, C A . The maximum temperature viiried annually. but mass population spawning took place each summer within a month of the peak temperatures. Whether these high summer temperatures cue spawning, or are merely coincidental. cannot be determined totally from field data. It would appear, however, that anem- ones from the outer coast and harbor populations are potentially all members of one local breeding population, based on the similarities in timing of reproductive events between the populations.
Acknowledgments I wish to thank the members of my thesis com-
mittee, Drs. Cadet Hand, John S. Pearse, and Mar- valee H. Wake for reading an early draft of this manuscript. Thanks to Drs. Kevin J. Eckelbarger and Mary E. Rice for commenting on the final draft, and to Drs. Daphne F. Dunn and Edward B. Lyke for discussion of the data. Dr. Edward E. Ruppert, Dr. A. E. Siebert, Jr., Margaret L. C. Siebert, and PhyIlis Thompson helped with figure preparrttion. Final manuscript preparation and support were provided by the Harbor Branch Foundation, Inc. This work was supported by a traineeship as- sociated with project No. RIE-10, grant No. 046- 158-44321, awarded to Professors Cadet Hand nnd Ralph I . Smith by the University of California Sea C
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Grant College Program, National Oceanic and At- mospheric Administration, United States Depart- ment of Commerce.
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