FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1981 Canadian Science Publishing. This manuscript is the post-print of an article published by Canadian Science Publishing, an independent and not-for-profit organization. The final version is published in Canadian Journal of Zoology available at http://www.nrcresearchpress.com/journal/cjz and may be cited as: Jennison, B. L. (1981). Reproduction in three species of sea anemones from Key West, Florida1. Canadian Journal of Zoology, 59(9), 1708-1719. doi:10.1139/z81-235 1708 Reproduction in three species of sea anemones from Key West, Florida 1 BRIAN L. JENNISON Harbor Branch Foundation, RFD No. J Box 196, Fort Pierce , FL, U.S.A . 33450 Received February 16, 1981 JENNISON, B. L. 1981. Reproduction in three species of sea anemones from Key West, Florida. Can. 1. Zool. 59: 1708-1719. Reproduction in three species of sea anemones from Key West, Florida, was studied from October 1977 until July 1978. Condylactis gigantea is dioecious, has a I: I sex ratio, and exhibits an oviparous -+ planktonic -+ lecithotrophic reproductive pattern, based on the scheme of Chia, modified by the author. Phymanthus crucifer is also dioecious and exhibits a sex ratio not significantly different from I:I; however, this species is viviparous. Bartholomea annulata exhibits imperfect gynodioecious hermaphroditism, accompanied by asexual reproduction by pedal laceration; it is oviparous -+ planktonic -+ planktotrophic . It is argued that an oviparous habit with resultant larval dispersal is advantageous to C. gigantea, which is solitary. In contrast , viviparity in P . crucifer and pedal laceration in B. annulata represent two different methods of keeping offspring close, thereby maintaining habitat space. The evolution of three such diverse reproductive modes is discussed through an examination of the morphology, prey, and habitat type of each species . JENNISON, B. L. 1981. Reproduction in three species of sea anemones from Key West, Florida. Can. 1. Zool. 59: 1708-1719. La reproduction a ere etudiee chez trois especes d'anemones de mer de Key West, en Floride, d'octobre 1977 a juillet 1978. Condylactis gigantea est dioique, a un rapport males.femelles de I: I et son cycle reproducteur suit une sequence ovipare -+ planctonique -+ lecitotrophe, selon Ie modele de Chia rnodifie par I'auteur. Phymanthus crucifer est egalernent dioique et son rapport males.femelles ne differe pas significativement de 1:I; cette espece est par ailleurs vivipare. Bartholomea annulata se reproduit par hermaphroditisme gynodioique imparfait et par reproduction asexuee (laceration du pied); l'espece suit la sequence ovipare -+ planctonique -+ planctotrophe. La reproduction ovipare suivie de la dispersion des larves est avantageuse pour C. gigantea qui est une espece solitaire. En revanche, la viviparite de P. crucifer et la laceration du pied chez B . annulata sont deux rnecanismes destines agarder proche la progeniture, de facon aconserver intact I'habitat. L'evolution de ces trois modes de reproduction differents est examinee ala lumiere de la morphologie de l'habitat et du type de proie de chacune de ces especes . [Traduit par Ie journal] Introduction reproductive biology of these three anemones both out Although sea anemones occur in south Florida waters of basic interest in their natural history, and in the belief in variety and abundance, surprisingly little is known of that the project might yield information concerning the their reproductive biology. Some information may be ability of these animals to maintain space in their gleaned from systematic works (McMurrich 1889; respective habitats. Duerden 1898, 1902). However, Carlgren (1951) did Materials and methods not discuss the reproductive condition of his specimens Eleven to 17 (usually 12) anemones of each of three species when he reviewed the systematics of Bartholomea were collected on six occasions from October 22, 1977, until annulata and Phymanthus crucifer. Lewis (1960a) June 17, 1978. Collections were made subtidally from ledges briefly described reproduction in several anemones from and Thalassia beds just off the sea wall on the southeast corner Barbados, including a description of larval release and of the island of Key West, Florida. Generally, Bartholomea settling in P. crucifer. Although he found B. annulata annulata was found clustered on vertical ledges at depths of and Condylactis gigantea on coral reefs (1960b), he did 1-3 m, often among dense forests of the chlorophyte Hali­ not deal with their reproduction. meda sp., whereas Condylactis gigantea was collected from Bartholomea annulata and Condylactis gigantea are adjacent Thalassia flats. Phymanthus crucifer was found on important members of their subtidal communities, low rocks and in sandy areas at the edges of both Thalassia providing shelter for a variety of commensals and beds and near the ledges . Following collection, anemones were relaxed in 50:50 serving as "base stations" for fish cleaning activity (see seawater and isotonic MgCIz. Condylactis gigantea was Limbaugh et al. 1961; Mahnken 1972; Herrnkind et al. bisected longitudinally; one-half was weighed. Initially, spec­ 1976). Phymanthus crucifer, which is often found in imens of P. crucifer, B. annulata, and the other longitudinal dense beds in shallow sand surrounding rocks, can also half of C. gigantea were cleaned, fixed in Hollande's fluid, and be a dominant member of the invertebrate assemblages embedded in paraffin for histological examination . In later in which it is found. I undertook this study of the collections, after it was discovered that P. crucifer might contain brooded young, these anemones were dissected from 'Contnbution No. 223 of the Harbor Branch Foundation. the bottom prior to embedding . Sections 8-10 ILm thick were 0008-4301/81/091708-12$01 .00/0 © 1981 National Research Council of Canada/Conseil national de recherches du Canada JENNISON 1709 made on a rotary microtome. These sections were mounted, among males, females, and anemones with no gonads stained with picroindigo carmine, counterstained with basic are significant (F = 3.91 , P < 0.05). fuchsin, and examined and photographed under a compound In males, the first reproductive cells visible are the microscope. spermatogonia, which are 3.5 to 4.0 um in diameter. In order to assess whether the gonads were maturing These first appear in clusters in the gonadal endoderm. synchronously throughout their length, three cross sections were made of each specimen of B. annulata . One was taken Later they occur in vesicles surrounded by mesoglea. just below the oral disc, the second in midcolurnn , and the third The spermatogonia mature and differentiate into sperm, just above the base. Column diameters were measured from with heads approximately J .5 um in diameter. These the basal sections, using a compound microscope equipped cluster in the center of the spermatogenic vesicles (Fig. with an ocular micrometer. Only oral and basal sections were 2). Immature males were found on November 22, 1977, examined in P. crucifer because of its squat shape. Condylac­ and again on June 17, 1978; mature males were found in tis gigantea was so large that histological examination of the all collections (Table 1). entire gonad was impractical; therefore, sections were made In females, the first reproductive cells visible are from the midcolumn region only. However, fresh smears were oogonia, which arise in the endoderm of the gonadal examined during dissection in order to doublecheck the mesentery and range from 10 to 20 urn in diameter. histological results. To assess female maturation in all three species, oogon ia These cells have a relatively large nucleus and a and oocytes from each identifiable female were measured well-defined nucleolus. They migrate into the mesoglea under the microscope from prepared sections, using an ocular where they undergo vitellogenesis. According to Dunn micrometer. At least 50 gametogenic cells were measured (1975) the gametes may be considered oocytes at this from each female ; generally only those cells which had a stage (Fig. 3). Oocytes in C. gigantea are variously distinct nucleolus were measured, in order to standardize the oriented within the mesentery, and different stages of diameter measurements, as well as to avoid counting the same development may occur within a single mesentery . oocyte twice. However, if fewer than 50 cells were present in However, the germinal vesicles are always peripherally the sections, all ofthem were measured, regardless of presence located and appear to be associated during vitellogenesis or absence of a nucleolus. Male maturity was determined by with a cellular structure referred to by Nyholm (1943) the presence or absence of gonial cells and tailed sperm (see Jennison 1979). and Dunn (1975) as a trophonema. Oocytes of C. Oocytes and embryos of P. crucifer were fixed for scanning gigantea may reach a diameter of 500 urn in fixed electron microscopy in 2.5% glutaraldehyde at room temper­ material. ature for I h. The specimens were washed in Millonig's 0.4 M Phymanthus crucifer is also dioecious and exhibits a phosphate buffer, dehydrated in alcohol and amyl acetate, sex ratio not significantly different from I:I. Of 79 passed through a critical point drying apparatus, mounted and anemones examined, 36 were female, 29 were male, sputter coated . Planulae and juveniles were measured and and 14 had no gonads. No hermaphrodites were found. photographed live under a dissecting microscope. Spermatogenesis is similar to that described for C. gigantea except the gametes tend to be slightly smaller. Spermatogonia are approximately 2.5 urn in diameter, Results and mature sperm heads measure 1.0 urn across . Fur­ Gametogenesis ther, ripe testes are more densely packed with sperm Condylactis gigantea is dioecious; males and females than in C. gigantea (Fig. 4). Mature males were found in were found in a 1:I ratio. Of 71 animals examined in six all collections, although all anemones taken on May 18, collections, 33 were females and 32 were males.