Invertebrate Zoology, 2007, 4(2): 111–127 © 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 30–33‰. 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, (7.5–64 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 oral–aboral 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 1A–C, 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 and similarities with other pro- by an external layer of clear ectoderm covering a cesses small core of darker endoderm. During the free stage, IFSP swam in a rotary manner by means of Lambert’s “cysts” a ciliate layer of ectodermic cells resembling In his description of the “Hydra Tuba” stage, planula larvae. After release, they spent two to Lambert (1935) mentioned that it can produce 114 A.A. Vagelli

Fig. 1. Aurelia aurita (Linnaeus). A — scyphistoma carrying three internally produced free swimming propagules (IFSP) in lower part of the stalk. In contrast to buds, these compact ciliated masses of cells are originated internally. B — scyphistoma with four IFSP close to release time, localized in the upper part of the gastrovascular cavity. C — five IFSP migrating inside of the scyphistoma stolon towards the oral region. IFSP normally took between one and three days to reach the oral cavity. Ðèñ. 1. Aurelia aurita (Linnaeus). A — ñöèôèñòîìà ñ òðåìÿ ñâîáîäíîïëàâàþùèìè ïðîïàãóëàìè (IFSP), âûäåëÿåìûìè â ãàñòðîâàñêóëÿðíóþ ïîëîñòü â íèæíåé ÷àñòè íîæêè.  îòëè÷èå îò íàðóæíûõ ïî÷åê ýòè êîìïàêòíûå ñêîïëåíèÿ ðåñíèò÷àòûõ êëåòîê âûäåëÿþòñÿ â ãàñòðîâàñêóëÿðíóþ ïîëîñòü. B — ñöèôèñòîìà ñ ÷åòûðüìÿ ãîòîâÿùèìèñÿ ê âûõîäó ïðîïàãóëàìè IFSP â âåðõíåé ÷àñòè ãàñòðîâàñêóëÿðíîé ïîëîñòè. C — ïÿòü ïðîïàãóë IFSP, ïåðåìåùàþùèõñÿ âíóòðè ñòîëîíà ñöèôèñòîìû ê ðîòîâîìó îòâåðñòèþ. Äâèæåíèå ê ðîòîâîìó îòâåðñòèþ ïðîïàãóëû IFSP çàíèìàåò îò îäíîãî äî òðåõ äíåé. numerous buds, send out shoots, “and in Aure- eggs have, and take much longer to develop lia push out cysts, a sort of egg (as with the into scyphistomae. freshwater Hydra), which can develop into a On the other hand, it seems that “Lambert’s Hydra tuba in fourteen days.” cysts” are not related to podocysts either. Al- It is uncertain what Lambert meant by though Lambert compared the “cysts” with Hy- “cysts.” Hydra releases its eggs by extrusion of dra eggs, Hydra eggs grow from the stalk and its wall tissue (Hyman, 1940) and not through not from the attachment disk where podocysts its oral opening; it is unlikely that Lambert originate. observed the release of internally produced In his review of Scyphomedusae develop- propagules. Furthermore, IFSP are ciliated, do ment, Berrill (1949 pp 399) stated “locomotion not have a “cyst-like cover” (theca) as Hydra of the scyphistoma has led to a special method New asexually produced propagules for Aurelia aurita 115

Fig. 2. Aurelia aurita (Linnaeus). A — scyphistoma showing internally produced free swimming propagules (IFSP) with larger power. B — two IFSP released simultaneously. C — an IFSP is released through the scyphistoma oral opening. The expulsion process takes no more than two seconds. D — an IFSP began to develop its first tentacle (t). Before settling and transforming into scyphistomae it spent about 14 days in a free-swimming stage. Ðèñ. 2. Aurelia aurita (Linnaeus). A — ñöèôèñòîìà ñ ïðîïàãóëàìè IFSP, áóëüøåå óâåëè÷åíèå. B — äâå ïðîïàãóëû IFSP, âûñâîáîæäàþùèåñÿ îäíîâðåìåííî. C — ïðîïàãóëà IFSP, âûõîäÿùàÿ ÷åðåç ðîòîâîå îòâåðñòèå ñöèôèñòîìû. Âûõîä ïðîïàãóëû çàíèìàåò íå áîëåå äâóõ ñåêóíä. D — ïðîïàãóëà IFSP íà íà÷àëüíîì ýòàïå ðàçâèòèÿ ïåðâîãî ùóïàëüöà (t). Ñâîáîäíîïëàâàþùàÿ ñòàäèÿ äëèòñÿ îêîëî 14 äíåé è çàâåðøàåòñÿ îñåäàíèåì è ïðåâðàùåíèåì â ñöèôèñòîìó. 116 A.A. Vagelli

Fig. 3. Aurelia aurita (Linnaeus). A — internally produced free swimming propagule (IFSP) two days after settlement, with the first two tentacles (t) and oral cavity (o) already developed. B–C — externally produced free swimming propagules (EFSP) were originated by extrusion of the body wall tissue in a “budding-like” process. EFSP never developed adult scyphistomae structures while attached to the scyphistoma parent. EFSP larger, less consistent in shape and size, and less motile than the IFSP. Ðèñ. 3. Aurelia aurita (Linnaeus). A — ïðîïàãóëà IFSP ÷åðåç äâà äíÿ ïîñëå îñåäàíèÿ ñ äâóìÿ ùóïàëüöàìè (t) è ðîòîâûì îòâåðñòèåì (o). B–C — ïðîïàãóëà EFSP îáðàçóåòñÿ ýêñòðóçèåé ñòåíêè òåëà ïîäîáíîé ïî÷êîâàíèþ. Ïðîïàãóëû EFSP íå ïðåâðàùàþòñÿ âî âçðîñëûõ ñöèôèñòîì âî âðåìÿ èõ ïðèêðåïëåíèÿ ê ìàòåðèíñêîé îñîáè. Îíè â îòëè÷èå îò ïðîïàãóë IFSP êðóïíåå, áîëåå èçìåí÷èâû è ìåíåå ïîäâèæíû. of reproduction” and mentioned the production not include Lambert’s observations on “cyst” of cysts by Chrysaora hyoscella and the obser- production. Chapman (1966: 60), who made the vations of Herouard (1907), Hadzi (1912), and first detailed description of the nature, produc- Chuin (1930) on statoblasts. However, he did tion, and historic review of podocysts (includ- New asexually produced propagules for Aurelia aurita 117 ing the observations made by Verwey, 1960 in three to six weeks to regenerate new scyphis- Cyanea, and by Chuin, 1930 in Chrysaora), did tomae. Complete or final scyphistoma form was not mention Lambert “cysts” either, although defined as “when regenerates had attached to he did point out Lambert’s observations on the the substrate, formed a mouth encircled by a capacity of scyphistoma to tolerate stagnant ring of 4–8 newly developed tentacles and were water conditions. capable of feeding”. Several times during this study, small pieces Pseudoplanula tentacularies of scyphistomae (commonly from tentacles) were Morphologically, IFSP resemble the cut off during transfers of scyphistomae from “pseudoplanula tentacularies” described by plastic sheets to culture dishes. After isolation Herouard (1913). He observed scyphistomae of in “planuloid” dishes, they were always trans- Chrysaora passing through a “depression peri- formed into spherical ciliated masses, very sim- od”, losing their tentacles, and transforming ilar (except their larger size) to IFSP. themselves into “pseudoplanulas” by reducing In spite of their different origin and mode of their volumes. However, IFSP occurred only production, IFSP (after release) behaved simi- during periods of scyphistomae growth under larly to regenerating scyphistomae fragments, favorable environmental conditions (good wa- and took approximately the same time to trans- ter quality and intense feeding). Furthermore, form themselves into adult scyphistomae. IFSP were released as undifferentiated masses of cells that increased rather than decreased Production of EFSP their volumes during their transformation into scyphistomae. Differences and similarities with other de- scribed processes Regeneration In his experiments on regeneration of scyph- Berrill’s Type I budding istomae of Aurelia aurita, Gilchrist observed Berrill (1949) classified the budding modes that “entodermal pieces round up into ciliated of Scyphomedusae into six types. He defined balls, which may remain alive and rotating for his Type I as: “Buds grow as a wide diverticula several days, but which do not regenerate. Piec- of the body wall; they are set free and swim away es of ectoderm, on the other hand, round up, and before any significant morphogenesis, original within a period of 7 to 11 days regenerate small, proximal end becoming the oral disc.” Berrill complete polyps” (Gilchrist, 1937: 111). included Cotylorhiza tuberculata, C. xamacha- In experiments on the effect of attachment na, and (citing Lambert’s 1935 work) “possibly on polyp regeneration, Kakinuma (1975) ob- occurring at times in Aurelia aurita.” However, served that small pieces of polyp tissue after two Lambert’s 1935 budding classification is not days cohered into spherical and ciliated masses. clear. He described “hydra tubae” budding in If the masses were allowed to attach, one third of three ways, i. e., “(1) by direct growth from the them formed polyps and developed tentacles outer wall of the body with, generally, early after seven–eight days, and all masses became liberation. (2) By means of the lateral process polyps by the tenth day. with immediate liberation; and (3) By means of Lesh-Laurie and Corriel (1973: 888) de- stolonic outgrowths, the buds sometimes being scribed the locomotion of isolated tentacles as liberated but more often remaining as colonies “discontinuous circular movement about the surrounding the parents.” Lambert stated that substrate with the proximal end always in ad- all three forms of budding are found in Aurelia; vance.” They found that isolated tentacles that that Chrysaora and ‘Rentoni’ (referring to the survived for five weeks all regenerated success- unspecified scyphistoma whose budding pro- fully, and depending upon their origin (oral- cess Renton described) buds by lateral process ring, whole or distal third), tentacles took from alone (Lambert #2); that Cyanea capillata buds 118 A.A. Vagelli chiefly by stolons (Lambert #3), and that in ‘C. soglea, septal muscles, and they swim by rotat- Lamarckii’ the buds move away. ing around the longitudinal axis of their body Budding in both Chrysaora and ‘Rentoni’ (Hofmann et al., 1978; Lesh–Laurie, Suchy, (Lambert #2) had been described in detail, e. g., 1990; Van Lieshout, Martin, 1992; personal Perez (1922), Renton (1930), Gilchrist (1937) observations). In contrast, propagules from A. and none of these descriptions agree with an aurita do not have a distinct mesoglea or septal “immediate liberation” of buds. Thus, Lam- muscles; Aurelia’s EFSP are much less motile, bert’s Type 2 budding mode corresponds to swim without direction, and lack any clear Berrill’s Type 3, not Type 1 (Berrill 1949). In body axis. addition, Lambert’s Type 3 is associated with The production of IFSP and EFSP by Aure- outgrowth of pedal stolons (Berrill’s Type 4 not lia aurita and planuloids by rhizostomids share Type 1). two basic characteristics that differentiate this Hence, when Berrill included Aurelia aurita type of vegetative multiplication from typical (citing Lambert’s observations) together with budding processes described in semeaostomes Cotylorhiza tuberculata and Cassiopea xam- and other groups, including the production of achana, which both produce typical rhizosto- lateral buds, stolonic buds, pedal stolons, hy- mid free-swimming planuloids, in his budding dra-type buds, and fission buds. First, neither Type I, he probably was referring to Lambert’s IFSP or EFSP develop adult scyphistomae struc- “cysts,” not to Lambert’s classification of buds. tures while they are attached to the parent; second, once released IFSP and EFSP adopt a Free-swimming planuloids in rhizostomids planula like appearance and swim for a variable The production of free-swimming planu- period of time before settling and transforming loids is well known in rhizostomids, e. g., into a new scyphistomae. In addition to these Cassiopea andromeda (Hofmann et al., 1978), morphological and developmental differences, Cassiopea xamachana (Bigelow, 1900; Cur- the production of free-swimming propagules tis, Cowden, 1971; Van Lieshout, Martin, can be expected to have important ecological 1992), Mastigas papua (Sugiura, 1963), and implications having to do with dispersal, re- Cotylorhiza tuberculata (Claus, 1893). Hof- cruitment, and intraspecific competition. Thus, mann et al. (1978 pp.172) pointed out that the the production of free-swimming planuloids budding process described for most rhizosto- described in most rhizostomid and the produc- mid species is “an entirely different type” than tion of free-swimming propagules in Aurelia those described for semaeostomids. However, aurita should be considered a distinct asexual they mentioned that “strict classification ac- reproductive mechanism instead of another type cording to the mode of asexual reproduction is of budding. It is proposed the term “gemma- not possible, since Rhizostoma pulmo, as indi- tion” for referring to this mechanism and “gem- cated by the observations of Paspaleff (1938), mae” should be used for the products of this seems to exhibit almost every known type of mechanism. This will avoid confusion with the vegetative polyp formation” including planu- term “budding” that has been used to refer to a la-like buds, Hydra-type buds, and stolonial large number of unrelated vegetative multipli- buds. Also, Calder (1973) found that Rhopile- cation processes in all groups of cnidarians ma verrilli differs from the other rhizostomids (Fautin, 2001). in producing stolons and podocysts, but not free-swimming buds. Review of Aurelia aurita life cycle and its Several differences exist between free- adaptive significance swimming propagules produced by Aurelia aurita and those produced by the above de- The life cycle of Aurelia aurita includes the scribed rhizostomids; e. g., Cassioipea xam- alternation of two dimorphic generations, me- achana planuloids possess a well-defined me- dusa and scyphistoma, that are also very distinct New asexually produced propagules for Aurelia aurita 119 ecologically and physiologically. In addition, Sexual phase one generation reproduces sexually, while the other reproduces asexually (metagenesis). Most Sex determination studies on life cycles, reproductive strategies It seems that the issue of the point in Aurelia and dispersal of marine clonal species do not aurita’s life cycle where sex first differentiates include organisms with complex life cycles and its potential implications has been mainly like that of Aurelia aurita (e.g., Ayre, 1984; overlooked. As far as it is known, no studies Jackson, 1986; Jackson, Coates, 1986; Jaeck- have been done to establish the genetic, physi- le, 1994; Mc Fadden, 1997; Thorson, 1950; ological, and / or environmental mechanisms of Vance, 1973). Despite debating the dispersal sex determination in either the medusa or scyph- contribution of asexually vs. sexually produced istoma phenotypes. propagules of a variety of species, the resulting If scyphistoma germinal stem cells do not different genetic structures within (clonal and participate in gonad formation, gametogenetic aclonal) populations, and their adaptive signif- tissue would develop anew in the medusa phe- icance, these studies are all based on organ- notype and sex would be determined at some isms for which (a) adult individuals are sessile point during the medusa development. In this or have minimal dispersal capabilities (except case, if sex were genetically controlled, and rafting), (b) sexual reproduction occurs in fixed since all medusae originating from a given scy- locations (parental habitat), (c) dispersal relies phistoma share the same genotype, then all almost completely on larval forms, sexually or medusae produced by such scyphistoma should asexually produced, that only last from a few have the same sex. On the other hand, if pheno- minutes to a few weeks. typic sex were environmentally determined at In contrast, the life history of Aurelia aurita: the medusa stage, it would be expected that (a) combines sessile and free-living planktonic populations of scyphistomae strobilating under adults1 , (b) sexual reproduction is independent the same environmental conditions, would pro- of the benthic-sessile stage and potentially oc- duce ephyrae that would develop the same type curs over continuous wide-ranging geographi- of gonad. It has been reported that temperature cal areas, and (c) both larval and adult stages determines the phenotypic sex in the dioecious have dispersal capabilities which extend from a Hydra oligactis (Littlefield, 1986), and Carre few days (planula), to weeks (IFSP, EFSP, and Carre (2000) showed how temperature at ephyra), to several months or more (medusa). strobilation time significantly (but not com- Once alternation of generations (and metagene- pletely) determines the phenotypic sex in medu- sis) is taken into consideration, theories dealing sae of Clytia hemisphaerica, a marine dioecious mainly with benthic invertebrates do not pro- hydrozoan with alternation of generations. vide an accurate description of the adaptive Spanenberg (1965) raised 96 medusae of significance of different life stages of organisms Aurelia aurita until sexual maturation under like most scyphozoans with an alternation of laboratory conditions. The medusae derived generations. from scyphistomae that in turn originated from planulae released by female medusae collected 1Both the scyphistoma and the medusa forms are in the wild. All ephyrae and medusae were kept considered here as distinct phenotypes with their own in artificial seawater and at 21–24ºC. Sexual ontogeny. Thus, the medusa phenotype passes through a series of morpho-physiological changes from the newly maturity was observed in about 42% of the metamorphosed ephyra to the mature and to the senes- medusae. Sperm sacs were found at 38, 39 and cence stage; and the scyphistoma phenotype from the 112 days, and planula larvae on days 88 and various stems forms such as planula, cyst, free swimming propagule, and bud to the adult stage, i.e., with complete 153. In contrast, only male medusae were ob- number of tentacles and capable of reproducing. For served to reach sexual maturity in our laborato- theories dealing with ontogenetic and phylogenetic se- ry. The main difference from Spanenberg’s hold- quence of life cycle stages, see Hyman (1940), Hadzi (1953), Hand (1959), Thiel (1966), and Chapman (1966). ing conditions was our lower water temperature, 120 A.A. Vagelli about 17ºC during the first four months after medusae phenotypic sex in A. aurita is deter- strobilation, and about 22ºC thereafter. mined at the scyphistoma stage, rather than at These observations may suggest that the medusae stage. If the medusa phenotypic sex is phenotypic sex at the medusa stage to be mostly determined at the scyphistoma stage, and it is environmental controlled, e. g., under lower genetically controlled, all ephyrae that meta- temperatures only male gonads develop, where- morphosed into medusae should have the same as in warm conditions germinal tissue has the genetic composition of the particular strobila potential to differentiate into both gonads equal- from which they derived. It is possible that we ly. Altough lower temperature decreases medu- had started with an only male population of sae growing rates, and female medusae seems to scyphistomae, and all derived ephyrae devel- need longer to achieve sexual maturation than oped male gonads, independently of the envi- males, it is highly improbable that the absence ronmental conditions (our original population of female medusae in our facility was related to consisted of five plastic sheets 10 x 5 cm carry- developing time. Several works have shown a ing attached scyphistomae, and it was never lack of relationship between gonad develop- mixed with scyphistomae from other sources). ment, size and age. For instance, whereas our Lesh-Laurie and Suchy (1990) mentioned medusae attained a bell diameter of at least the observations by Komai (1935) and Werner between 80–100 mm before being replaced (usu- (1970) on germ cell formation on scyphistomae ally after five–six months), Lucas (1996) found of the coronate Stephanoscyphus. The only females as small as 19–20 mm carrying eggs and known instance of gametogenesis occurring in a planula larvae in Horsea Lake (England). In scyphopolyp. Mature germ cells were incorpo- addition, Spanenberg’s largest medusae reached rated into the ephyra during strobilation, but no a bell diameter of only 55 mm, and she found no gametes were found in such ephyrae. Chapman correlation between age and development of (1966) pointed out the tendency for scyphis- morphological structures (subgenital pits were tomae to form gonads, which may even persist observed to develop between 25 and 66 days). in the strobila and ephyra. He described the Similarly, Lucas and Lawes (1998) found that formation of sex cells, which were intermediate size at maturity is not correlated with either age or between sperm and ova (neutral gonad), but he bell diameter in wild populations. Ripe females also suggested that germ cell development in were found at such small size as 19 mm in bell scyphistomae was weakly genetically deter- diameter and as early as 90 days after strobila- mined. tion. Therefore it seems that our medusas would Also, it could be possible that the medusa have had enough time to develop female gonads phenotypic sex be determined at the scyphis- if they were genetically determined. tomae stage but remain under environmental On the other hand, both Spanenberg’s labo- control. In this case it would be expected that all ratory work, and Lucas and Lawes’ field study medusae derivate from the same scyphistoma (where individuals are subjected to similar envi- will have the same sex, but genetically identical ronmental conditions, and a temperature range scyphistomae maintained under different ambi- between 5.5 and 23ºC) show that under same ent conditions will produce medusae of differ- environmental conditions both sexes develop, ent sex. which would indicate that phenotypic sex is most likely genetically determined. Gonad and embryo development If sex differentiation in medusae is geneti- It is well known that sexual reproduction is cally determined and gonad development is not carried out by the gonochoristic medusa pheno- closely related to age, then one possible expla- type. Studies on lab-raised specimens showed nation for the observations of only male medu- that sexual maturity of medusae can be attained sae sexually maturing (and no detection of fe- in about 40 days for males and 90 days for male medusae) in our facility could be that females at 21–24ºC (Spanenberg, 1965), al- New asexually produced propagules for Aurelia aurita 121 though field observations by Lucas (1996) in brood pouches located in the walls of the fe- Horse Lake suggest that medusae growing at males’ oral arms (Agassiz, 1862; Russell, 1970, lower temperatures and exposed to periods of Kakinuma, 1975). Planula larvae have been food limitations likely take significantly longer reported measuring from about 20 to 80 µm to mature. In their study of growth and degrowth (Lucas, Lawes, 1998), and up to 300 µm for in a population of A. aurita from Tomales Bay larvae before settlement (Agassiz, 1862, Kaki- (California), Hamner and Jenssen (1974) found numa, 1975). Planula metamorphosis into scy- that gonads from mature medusae deprived of phistoma has been described in detail by Agas- food regressed to immature state within five to siz (1862). eight days. After 40 days of starvation, the It appears that Aurelia aurita can adjust its medusae that were fed grew to full size and reproductive output in accordance with particu- become sexually mature again. During their 130- lar environmental situations. Lucas and Lawes day laboratory study, they observed some medu- (1998) found that medusae inhabiting a severely sae spawning and becoming sexually mature food-limited locality invested less energy into again within a two-week period, without post- reproduction and produced a low number of spawning gonadal or somatic deterioration. large planula larvae (k-strategy). In contrast, Eckelbarger and Larson (1988) found that medusae from another locality with much great- the process of yolk deposition was both auto- er food availability were able to direct more synthetic and heterosynthetic, and vitellogene- energy to reproduction, and produced a large sis was completed in less than four days if number, but smaller planula larvae (r-strategy). abundant food is available. Oogenesis is asyn- chronous, without a maturation gradient, and Asexual phase oogonia differentiate without a pattern within the endoderm. There is a high degree of vari- The asexual part of the life cycle is complet- ability in oocyte and planula larvae size com- ed by the scyphistoma phenotype, which is position within populations; yolk deposition starts capable of asexually reproducing (cloning) in at in oocytes of about 75 µm in diameter, and least three principal modes, i.e., (1) budding: a mature oocytes range between about 75 and 180 scyphistoma produces external outgrowths of µm (Widersten, 1965; Eckelbarger, Larson, 1988; various types that develop tentacles and other Avian, Sandrini, 1991; Lucas, Lawes, 1998). adult structures before detaching and becoming Spermatogenesis is synchronous; takes about new scyphistomae (Perez, 1922; Renton, 1930; eight days at 17ºC and is independent of devel- Gilchrist, 1937; Berrill 1949; Kakinuma, 1975); opmental control mechanisms that regulate cel- (2) strobilation: a scyphistoma transforms into lular phenomena in the rest of the organism; strobila that produce several free-swimming once spermatogenesis begins, germ cells com- ephyrae (Spanenberg, 1965, 1967, 1971; Kato plete differentiation in spite of gonad and organ- et al., 1973; Olmon, Webb, 1974; Kakinuma, ism regression (Hamner, Jenssen, 1974). Sperm 1975); (3) production of free-swimming develops in follicles located in the genital me- propagules = gemmation: a scyphistoma pro- soglea; after release, it is transported by ciliary duces a spherical mass of cells internally from currents though the female gastrovascular cav- the lower stalk and stolons, or produces out- ity and fertilization takes place at the ovarian growths externally; after a free-swimming stage, genital sinus (Widersten, 1965). both spherical masses and outgrowths transform Ishii and Takagi (2003) described the em- themselves into new scyphistomae (this study). bryo development. Cleavage was holoblastic The production of podocysts may be consid- and time from zygote to gastrula varied from ered another cloning mechanism in Aurelia au- 116 h at 12ºC to 50 h at 22ºC, and from gastrula rita (Chapman, 1968; Lesh-Laurie, Suchy, to planulae release about 154 h at 12ºC to 120 h 1990). Podocysts are encapsulated cuticular at 22ºC. Development of planulae occurs within structures containing tissue of ectodermal and / 122 A.A. Vagelli or amebocyte origin formed at the scyphistoma that some planula larvae developed into scyph- attachment disk (Chapman, 1968, 1970). Scy- istomae, but a higher proportion of planulae phistomae produce two or three podocysts in (released by the same medusa) developed into about two days. Exposure to poor water quality ephyrae, bypassing the scyphistoma stage. Mean and accumulation of algae and debris increase values of planulae developing into ephyrae were the cyst production, but even during favorable 76% for medusae collected in April (size range: environmental conditions scyphistomae often 15–26 cm); 62% (collected in May, size range: produce cysts. The excystment process takes 20–30cm); and 57% (collected in June, size one or two days, and the further development range: 15–20 cm). The time required for planu- into complete scyphistoma is similar to that lae to develop into ephyrae after settlement already described for gemmae (personal obser- varied between 3 and 11 days depending on vations). temperature, and the egg size varied between In addition, Aurelia aurita has ample re- 260–300 µm. Moreover, Kakinuma (1975) in generating capabilities, particularly from iso- one experiment observed that about 90% of the lated ectodermal fragments and tentacles, and planulae extracted from medusae collected in from pedal stolons, into new complete scyphis- Mutsu Bay, Japan and maintained in Petri dish- toma (Gilchrist, 1937; Steinberg, 1963; Kaki- es differentiated into ephyrae. numa, 1975; Lesh-Laurie, Suchy, 1990). Lesh- The life cycle of Aurelia aurita includes Laurie and Corriel (1973) suggested that the two principal larval forms; these different life complete regeneration of scyphistomae from forms increase flexibility in dispersal and adap- isolated tentacles represents another method of tability during a critical period of ontogeny asexual reproduction. when the highest mortality may occur (Vance, 1973). The first type, the rather phylopatric and Larval diversity and direct development lecithotrophic sexually produced planula larva is released by the planktonic medusoid phase Significant differences in egg size have been and spends a short period as part of the plankton, reported and the effect of different egg sizes on consequently decreasing the time to predation particular embryo development has been dis- exposure, and avoiding dependence on external cussed. Agassiz (1862) observed an important food supply. Although planulae dispersal is variation on the size of planula reaching brood limited, at the time of larvae release, the parent pouches, but he did not follow planulae of medusae may have been drifting away from different sizes through metamorphosis. Haeck- their localities of origin for several months. The el (1881) observed that Aurelia aurita produce second larval form, the free-swimming plank- eggs of different sizes, the smallest of which totrophic ephyra that normally are produced gastrulated by ingression and developed into asexually through the metamorphic process of the free-swimming planula larva. However, strobilation (transversal fission), but they also somre of the largest eggs gastrulated by incom- can originate from the sexual part of the cycle plete invagination and developed directly into from the direct development of planula and ephyrae (hypogenesis) (Haeckel, 1881 pp. 28, actinula larvae. Depending upon ambient tem- 29. Figs 21–24), while other large eggs devel- perature, ephyrae normally take between 10 and oped directly into a free-swimming actinula 25 days before becoming young medusae (Agas- (Haeckel, 1881 pp. 20. Fig. 7). In addition, an siz, 1862; Spanenberg, 1965; personal observa- intermediate size egg developed into a large tions). Ephyrae are the source of the primary planula larva that produced more planulae by dispersal stage of A. aurita, the medusae. budding before settling (Haeckel, 1881 pp. 20. In addition, A. aurita may produce planula Figs 4–6). larvae capable of asexual reproduction. Haeck- Yasuda (1971) working with medusae col- el (1881, pp. 19) described the vegetative mul- lected in Urazoko Bay (Japan Sea) observed tiplication of “gastrulae-larvae”. He observed New asexually produced propagules for Aurelia aurita 123 the production of larvae by splitting and bud- The cosmopolitan distribution2 of A. aurita ding of other larvae held in an aquarium during suggests that its populations have adapted to a winter, although there was a large variation in broad range of environmental parameters, (e. g., settling time. By increasing the number of lar- Miyake et al., 1997; Lucas, 2001) as well as vae that survive until settlement, this kind of having endured significant paleogeographic larval reproduction enhances the probabilities changes, likely through many vicariant and dis- of recruitment (Jaeckle, 1994). Furthermore, persal events. Fossils of scyphomedusae have under the strawberry-coral model, which is in- been recovered from the lower Cambrian, and tended for sessile organisms that multiply veg- fossil Semaeostomatida are reported in Upper etatively in continuous habitats, and that sexual- Jurassic (Moore, 1956); standard molecular clock ly produce widely dispersed propagules (Will- analysis suggests that speciation in the genus iams, 1975), evolutionary success will require Aurelia dates at least from tens of millions years that vagile propagules establish themselves be- before present and possibly up to 50–120 MYBP yond clonal boundaries, and that they will need (Dawson , Jacobs, 2001). This evolutionary suc- to be sexually produced. As Williams stated cess may be explained in part on its complex life “only by genetically diversifying the wide- history, (Fig. 4) which involves not only metagen- spread propagules is there any hope of produc- esis, i. e., the occurrence of both sexual and ing any with sufficiently high local fitness” asexual generations, (Kramp, 1943) and hypo- (Williams, 1975: 31). Thus, by multiplying the genesis, i.e., the direct transformation of gastru- same genet, larval reproduction offers an in- lae into ephyrae (Haeckel, 1881), but also be- valuable increase in the likelihood that a par- cause it includes two very distinct ecological ticular genetic combination will successfully types, i.e., a planktonic, highly dispersed, sexual- complete metamorphosis and will establish a ly produced medusa phenotype, and a benthic, new local adapted clone. sessile, scyphistoma phenotype that may com- bine various reproductive mechanisms, each as- Life history strategy and evolutionary sociated with different dispersal capabilities: success 1. Various budding processes increase the clone population (genotype) without varying its Aurelia aurita’s widespread geographical gene pool, which is already adapted to local distribution includes all oceans, and extends conditions. As Francis (1979) pointed out, a from equatorial, and tropical latitudes (Kramp, genotype dispersed is less likely to be extermi- 1955: Gulf of Guinea; Vanucci, 1957: Brazil; 2Recent studies have focused on the taxonomic status Rao, 1913: Andaman Islands, Indian ocean) to of Aurelia aurita (Dawson, Jacobs, 2001; Dawson, Mar- beyond the Arctic Circle in the Northern hemi- tin, 2001; Schroth et al., 2002; Dawson, 2003). These sphere (LeDanois, 1913: Iceland; Kramp, 1961 molecular studies support the idea of a polytypic Aurelia composed of several cryptic species, cast doubts about the after Mac Ginitie, 1955: Point Barrow, Alaska). ubiquitous nature of A. aurita, and even suggest that life- In the Southern hemisphere its reaches at least to history variability found in this species may be a reflection the 38th parallel in the South Atlantic (personal of different species adapted to local conditions. However, at least one of the identified molecular clades in each of the observations), and to South Australia in the above mentioned studies had a cosmopolitan distribution, Pacific ocean (Southcott, 1958). In addition, A. most of the other clades are very restricted geographically aurita inhabits several seas that have been near- (some proposed clades inhabit areas that have been avail- able for less than 10,000 years), and genetic differentiation ly isolated for long periods, e. g., the Red Sea was not found to be correlated with isolation by geographic (Ranson, 1945), the Baltic Sea (Ranson, 1945, distances. Even if the genetic differentiation found among Barz et al. 2006), the Black Sea (Kramp, 1961 the molecular clades (most of which were defined on a very limited sampling) represents distinct phylogenetic lineag- after Valkanov, 1957), the Mediterranean Sea es (some of which have been hypothesized to have recently (Kramp, 1961 after Ranson, 1945), the Adriatic evolved through hybridization and even introgression Sea (Vucetic, 1957), and the White Sea (Kramp, events), there is no evidence that any of these putative species have developed localized physiological special- 1961 after Yashnov, 1948). izations or changes in their life cycles. 124 A.A. Vagelli

Fig. 4. The life cycle of Aurelia aurita (Linnaeus). It encompasses metagenesis, and the alternation of two dimorphic generations. In addition, it includes the presence of larval polymorphism, direct development, and several asexual reproductive mechanisms each associated with distinct dispersal capabilities. Ðèñ. 4. Æèçíåííûé öèêë Aurelia aurita (Linnaeus). Îí îõâàòûâàåò ìåòàãåíåç è ÷åðåäîâàíèå äâóõ äèìîðôíûõ ïîêîëåíèé. Æèçíåííûé öèêë òàêæå âêëþ÷àåò ëè÷èíî÷íûé ïîëèìîðôèçì, ïðÿìîå ðàçâè- òèå è íåñêîëüêî ñïîñîáîâ áåñïîëîãî ðàçìíîæåíèÿ, îòëè÷àþùèåñÿ ñïîñîáíîñòüþ ê ðàññåëåíèþ. nated. However, Tardent (1984) showed that tomae strobilate they will produce several genetic heterogeneity in cnidarians can also ephyrae that, when mature, will carry gametes result from asexual reproduction. A mutation with the mutant gene. can “slip” into a forming bud; this mechanism 2. Strobilation and the development of a eventually could lead to a sub-clone that con- well-adapted phenotype to planktonic and drift- tains only mutant cells, thus originating geno- ing conditions allowed a widespread geograph- and phenotypic heterogeneity within a previ- ic dispersal, and the permanent colonization of ously isogenetic clone. The same could be ex- zones no well suited for the benthic phenotype pected in relation with the other vegetative (Barz et al., 2006). Furthermore, the medusa modes of reproduction, i.e., production of FSP form was able to exploit habitats richer in food (gemmation), strobilation and production of and with greater gamete nourishing and distrib- cysts. In addition, if mutations affect scyphisto- uting capacity (Chapman, 1966; Chapman, 1966 ma stem germinal cells, each time such scyphis- after Naumov, 1961). New asexually produced propagules for Aurelia aurita 125

3. The production of free-swimming Ayre D.J. 1984. The effects of sexual and asexual repro- propagules combines characteristics of both duction on geographic variation in the sea anemone Actinia tenebrosa // Oecologia. Vol.62. P.222–229. budding and strobilation. Similar to budding, Balcer L., Black R. 1991. Budding and strobilation in scyphistomae produce new ramets, but FSP Aurelia (Scyphozoa, Cnidaria): (gemmae) are originated more rapidly and in functional requirements and spatial patterns of nucleic larger quantities. And, like strobilation, the new acid synthesis // Rouxs’s Archives of Developmental Biology. Vol.200. P.45–50. organisms (FSP) pass directly to the plankton Barz K., Hinrichsen H., Hirshe H. 2006. Scyphozoa in the and disperse from the original population. How- Bornholm Basin (central Baltic Sea) — the role of ever, in this case dispersal is restricted to a few advection // Journal of Marine Systems. Vol.60. Iss.1– weeks and therefore FSP will colonize relative- 2. P.167–176. Berrill N. 1949. Developmental analysis of Scyphomedu- ly similar environments. sae // Biological Reviews. Vol.24. P.393–410. In addition, scyphistomae of Aurelia auri- Bigelow R. 1900. The anatomy and development of Cas- ta, as other sessile organisms, face challenging siopea xamachana // Proceedings of the Boston Soci- situations such as vulnerability to predators ety of Natural History. Vol.5 (6). P.191–236. Calder D.R. 1973. Laboratory observations on the life (Watanabe, Ishii, 2001), high levels of in- history of Rhopilema verrilli (Scyphozoa: Rhyzos- traspecific competition (Grondahl, 1988), and tomeae) // Marine Biology. Vol.21. P.109–114. a very restricted capacity of tropic response to Carre D., Carre C. 2000. Origin of germ cells, sex determi- a deteriorating environment. In such circum- nation, and sex inversion in medusae of the genus Clytia (Hydrozoa, Leptomedusae): The influence of stances the production of cyst like structures temperature // Journal of Experimental Zoology. Vol. (podocysts) has probably been an important 287. P.233–242. survival factor. Finally, the occurrence of dif- Chapman D. 1966. Evolution of the scyphistomae // Rees ferent larval forms with particular develop- W.J. (ed.) The cnidaria and their evolution. Sympo- sium of the Zoological Society of London. Vol.16. ment, phenotype differentiation, and ecologi- P.51–75. cal role, offers additional flexibility to colo- Chapman D. 1968. Structure, histochemestry and forma- nize new habitats and confront spatio-tempo- tion of the podocyst and cuticule of Aurelia aurita // ral environmental fluctuations. Journal of Marine Biology Association of the United Kingdom. Vol.48. P.187–208. Chapman D. 1970. Further observations on podocyst Acknowledgments formation // Journal of Marine Biology Association of the United Kingdom. Vol.50. P.107–111. Chuin T. 1930. Le cycle évolutif du scyphistome de I express my gratitude to Estela Lopretto for Chrysaora: étude histophysiologique Trav.Stat.biol. her advice, fruitful discussions and for helping Roscoff. Vol.8. P.1–179. to localize valuable bibliographic material. I Claus C. 1893. Uber die Entwicklung des Scyphistoma von Cotylorhiza, Aurelia, und Chrysaora. I–II Art // thank all staff and volunteers from the NJAAS Zoologischen Institut der Universität Wien. Research Lab that helped me during several Curtis S.K., Cowden R.R. 1971. Normal and experimental- years with the maintenance of the scyphistomae ly modified development of buds in Cassiopea // Acta and medusae in the laboratory. Embryologiae Experimentalis. Vol.3. P.239–259. Dawson, M.N. 2003. Macro-morphological variation among cryptic species of the moon jellyfish, Aurelia References (Cnidaria: Scyphozoa) // Marine Biology. Vol.143. P.369–379. Dawson M.N., Jacobs D.K. 2001. Molecular evidence for Agassiz L. 1860. Contribution to The Natural History of cryptic species of Aurelia aurita (Cnidaria, Scypho- The United States of America. Vol.III. Part I. Acalephs zoa) // Biological Bulletin. Vol.200. P.92–96. in General. Boston: Little, Brown & Co. London: Dawson M.N., Martin L.E. 2001. Geographic variation Trubner & Co. and ecological adaptation in Aurelia (Scyphozoa, Agassiz L. 1862. Contributions to The Natural History of the Semaeostomeae): some implications from molecular United States of America. Vol.IV. Part III. Discophore. phylogenetics // Hydrobiologia. Vol.451. P.259–273. Boston: Little, Brown & Co. London: Trubner & Co. Dawson M.N., Gupata A., England M. 2005. Coupled Avian M., Rottini Sandrini L. 1991. Oocyte development biophysical global ocean model and molecular genetic in four species of Scyphomedusae in northen Adriatic analyses identify multiple introductions of cryptoge- Sea // Hydrobiology. Vol.216/217. P.189–195. nic species // Proceedings of the Natural Academy of 126 A.A. Vagelli

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Responsible editors: F.D. Ferrari & V.N. Ivanenko

Accepted October 24, 2007

Published online February 11, 2008