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New Observations on the Asexual Reproduction of Aurelia Aurita (Cnidaria, Scyphozoa) with Comments on Its Life Cycle and Adaptive Significance

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New Observations on the Asexual Reproduction of Aurelia Aurita (Cnidaria, Scyphozoa) with Comments on Its Life Cycle and Adaptive Significance Invertebrate Zoology, 2007, 4(2): 111127 © INVERTEBRATE ZOOLOGY, 2007 New observations on the asexual reproduction of Aurelia aurita (Cnidaria, Scyphozoa) with comments on its life cycle and adaptive significance Alejandro A. Vagelli New Jersey Academy for Aquatic Sciences. 1 Riverside Drive, Camden. N. J. 08103. U.S.A. e-mail: [email protected] ABSTRACT: Two previously unreported asexual reproductive mechanisms have been observed in Aurelia aurita (Linnaeus, 1758). In one, scyphistomae produce internally several planula-like propagules that are released through the oral cavity and pass through a planktonic stage before settlement and metamorphosis. The second consists in the generation of free-swimming planuloids which are extruded through the external body wall of the scyphistomae. In contrast to the various budding process described in scyphozoans, both new mechanisms produce ramets that do not develop adult scyphistoma morphology prior to their release, and they only do so after passing through a free-swimming period that lasts up to several weeks. KEY WORDS: planuloids, dispersal, metagenesis, gemmation. Íîâûå ñâåäåíèÿ î áåñïîëîì ðàçìíîæåíèè Aurelia aurita (Cnidaria, Scyphozoa), çàìå÷àíèÿ î æèçíåííîì öèêëå è åãî àäàïòèâíîì çíà÷åíèè À.À. Âàãåëëè New Jersey Academy for Aquatic Sciences. 1 Riverside Drive, Camden. N. J. 08103. U.S.A. e-mail: [email protected] ÐÅÇÞÌÅ: Äâà ðàíåå íåèçâåñòíûõ ñïîñîáà áåñïîëîãî ðàçìíîæåíèÿ îáíàðóæåíû ó Aurelia aurita (Linnaeus, 1758).  îäíîì ñëó÷àå âíóòðè ñöèôèñòîìû îáðàçóþòñÿ ïëàíóëîïîäîáíûå ïðîïàãóëû, âûõîäÿùèå ÷åðåç ðîòîâîå îòâåðñòèå è ïðîõîäÿùèå ïåðåä îñåäàíèåì è ìåòàìîðôîçîì ïëàíêòîííóþ ñòàäèþ ðàçâèòèÿ. Âî âòîðîì ñëó÷àå îáðàçóþòñÿ ñâîáîäíîïëàâàþùèå ïëàíóëîèäû, âûäåëÿåìûõ ÷åðåç íàðóæíûé ïîêðîâ òåëà ñöèôèñòîìû.  îòëè÷èå îò ðàçíîîáðàçíûõ ñïîñîáîâ áåñïîëîãî ðàçìíîæåíèÿ èçâåñòíûõ ó ñöèôîçîéíûõ, îáà íîâûõ ñïîñîáà áåñïîëîãî ðàçìíîæåíèÿ âåäóò ê îáðàçîâàíèþ îñîáåé, ïðèîáðåòàþùèõ îáëèê âçðîñëîé ñöèôèñòîìû íå ïåðåä îòäåëå- íèåì îò ìàòåðèíñêîé îñîáè, à ïîñëå ïðîõîæäåíèÿ ñâîáîäíîïëàâàþùåé ñòàäèè, äëèòåëüíîñòü êîòîðîé ìîæåò äîñòèãàòü íåñêîëüêèõ íåäåëü. ÊËÞ×ÅÂÛÅ ÑËÎÂÀ: ïëàíóëîèä, ðàññåëåíèå, ìåòàãåíåç, áåñïîëîå ðàçìíîæåíèå. 112 A.A. Vagelli Introduction submerged in four 30-l tanks (four sheets in each tank). As the scyphistomae reproduced by The life stages and various reproductive mech- budding and spread along the plastic sheets, anisms of Aurelia aurita (Linnaeus) have been portions were transferred to more plastic sheets the classic example of the scyphozoan life cycle and to forty 10-cm Petri dishes (polyp dishes). for invertebrate textbooks , and the subject of The new plastic sheets and Petri dishes were many scientific papers on development and re- equally divided into two 100-l tanks. All six productive mechanisms (Agassiz, 1860, 1862; tanks flowed together in a recirculating system Haeckel, 1881; Lambert, 1935; Berrill, 1949), consisting of a pump, a 120-l sump, a biofilter budding (Perez, 1922; Renton, 1930; Gilchrist, and a chiller. Artificial seawater was used 1937), strobilation (Spangenberg, 1971, 1974; throughout the study for both tanks and Petri Olmon, Webb, 1974; Kato et al., 1973; Balcer, dishes. The salinity range was 3033. The pH Black, 1991) life stages (Spanenberg, 1965; Lu- varied between 7.8 and 8, while nitrites and cas, 2001), and recruitment of planula larvae ammonia remained at 0 mg/l. Water tempera- (Grondal, 1989). Also, several works have been ture was maintained at 22°C except when stro- published on podocyst production (Chapman, bilation was being induced. The system was 1966, 1968, 1970), and regeneration (Lesh-Lau- kept covered from light to avoid algae growth, rie, Corriel, 1973; Steinberg, 1963) for this spe- and no aeration was provided. Scyphistomae cies. However, the production of free-swimming were fed (ad lib.) four times a week with newly propagules was not previously documented for hatched Artemia salina. A. aurita. Moreover, despite detailed reports of important variations on A. aurita ontogeny (e.g., Scyphistomae observations and collection Haeckel, 1881; Berrill, 1949; Thiel, 1966, Kaki- of gemmae and free-swimming buds numa, 1975), its life cycle is still commonly An Olympus SCH dissection microscope depicted in a simplified manner (e.g., Grondahl, (7.564 x) was utilized to regularly observe 1988; Pechenik, 1991) even when it is utilized to scyphistomae attached to the polyp dishes. Mi- base models of dispersion and patterns of distri- crophotographs were taken with an Olympus bution (Dawson, et al., 2005). PC 35 mm camera attached to the microscope, Scyphistomae of Aurelia aurita have been and an Olympus SH2 (1000 x) light-microscope kept in culture for ten years with the goal of was used to observe planuloid development. To obtaining medusas for public display. During follow daily migration of internal produced this time, strobilation has been induced and the propagules, individual scyphistomae were dis- processes of budding, regeneration, cyst pro- tinguished by marks on the polyp dish bottoms. duction, and production of free-swimming Once propagules were observed in a particular propagules observed several times. This paper scyphistoma, they were photographically docu- reports two previously undocumented asexual mented, and a fine mark was made on the polyp reproductive mechanisms in scyphistomae of A. dish bottom to note the current position of each aurita, in which the internal and external pro- propagule. duction of free-swimming planuloid propagules To collect internally produced propagules are involved. In addition, the life cycle of this from the scyphistomae gastrovascular cavity, a species as it is known to date is reviewed, as well fine tuberculin needle was used to gently touch as discusses its adaptive significance. the oral area. This produced a quick reflex consisting of a stalk shortening and the opening Materials and methods of the oral cavity. A 400 µm glass pipette was then used to remove the propagules, which were General conditions isolated into 5-cm Petri dishes (planuloid dish- Scyphistomae of Aurelia aurita were kept es) containing salt water filtered through a 0.45 attached on sixteen 10 x 5 cm plastic sheets µm membrane filter. Also, free (non-artificially New asexually produced propagules for Aurelia aurita 113 extracted) internally generated propagules and three weeks in as a free-swimming stage before free-swimming externally produced planuloids settling down and attaching. found in polyp dishes, were transferred to indi- Metamorphosis began with an oralaboral vidual planuloid dishes to facilitate the study of elongation followed by the opening of the gas- their individual development. trovascular cavity. Soon thereafter, the first two All planuloid dishes were kept floating in tentacles developed (Figs 2D, 3A). Generally both 100-l tanks. When propagules developed the first tentacle began to differentiate, while the gastrovascular openings and the first tentacle, second followed one or two days later . Four to they were fed rotifers (Brachionus plicatilis), six days afterward, two more tentacles began to and after the development of the second tenta- develop simultaneously. Depending upon the cle, they were fed newly hatched Artemia sali- availability of food and on water quality, new na nauplii. Water was replaced daily by new scyphistomae developed eight tentacles in three filtered sea water, approximately three hours to four weeks and sixteen tentacles after three after feeding. more weeks. Results External production of Free-Swimming propagules (EFSP) Internal production of Free-Swimming Propagules (IFSP) The production of EFSP by scyphistomae of Aurelia aurita was characterized by the release IFSP were produced from the internal body of large free-swimming planuloids from the ex- wall of the gastrovascular cavity and stolons. ternal surface of scyphistomae. The EFSP devel- Scyphistomae liberated several IFSP (usually oped as outgrowths protruding usually from the between three and five) at the same time. Inter- lower half of the stalk and stolons (Fig. 3B,C). nal FSP slowly migrated from stolons and the Although they had a broad range of forms and aboral region to the oral region (Figs 1AC, sizes, reaching up to one half of the scyphistoma 2A). The time necessary for the propagules to size, most EFSP measured between 200 and 800 migrate from the aboral region to the oral open- µm. They usually have a spherical shape, although ing was between one and three days and depend- cylindrical and polyhedral also were observed. ed primarily on the distance from where they Besides the different location of origin, EFSP were produced. differed from IFSP by their compact and massive After reaching the gastrovascular cavity, consistency, their brown-orange coloration, and IFSP remained up to three days before they were their low motility. In addition, they require a released. The actual process of expulsion was considerably longer time to settle and develop very rapid (Fig. 2B,C). The opening of the oral adult structures once detached from the scyphisto- cavity and release of IFSP did not take more ma parent. It was common for EFSP to start than one or two seconds. The number of IFSP metamorphosis four or five weeks after detaching. observed in any scyphistomae varied between three and six, and all migrated and were released Discussion simultaneously. Internal FSP were spherical-ovoid structures Production of IFSP of approximately 200 µm in diameter. They were very consistent in shape and size, and were formed Differences
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