The body plan of the cnidarian medusa: distinct differences in positional

origins of polyp tentacles and medusa tentacles

Hiroshi Shimizu�,a and Hiroshi Namikawab

aDepartment of Developmental Genetics, National Institute of Genetics, 1111 Yata, Mishima, 411-8540 Shizuoka, JapanbShowa Memorial Institute, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, 305-0005, Ibaraki, Japan�Author for correspondence (email: bubuchin2006@yahoo.co.jp)

Cnidarians have two typical body forms, the attached form

(polyp) and the swimming form (medusa) (Fig. 1). The polyp

has a mouth with tentacles closely surrounding it at the apical

end of a cylindrical body column (Fig. 1A). The morphology

of a medusa is characterized by a body like an inverted bowl,

termed the umbrella (Fig. 1B). The umbrella has tentacles

hanging down from its margin (marginal tentacles). The

mouth is located at the end of a columnar structure termed

the manubrium, which is located at the center of the umbrella.

Despite these significant differences in morphology, zoology

textbooks typically state that ‘‘the medusa is the upside down

form of a polyp,’’ implying that the two forms have basically

the same body plan (Ruppert and Barnes 1996). As a result, it

has generally been assumed that the tentacles of the polyp and

the marginal tentacles of the medusa are homologous. How-

ever, it remains unknown whether the textbooks’ description

is correct or not. Based upon classical observations and recent

results of molecular studies, we present a simple but novel

answer to this question by showing that animals that belong

to Cnidaria have two areas in the body where tentacles

are formed, one at the oral end, and the other in an aboral

location on the animal.

We focused our analysis on the differences in positional

origins of hydropolyp tentacles and hydromedusa marginal

tentacles in this study. Although the medusa form occurs

in three cnidarian classes (viz., Scyphozoa, Cubozoa, and

Hydrozoa), of these about 75% of the species that have the

medusa stage belong to Hydrozoa (Brusca and Brusca 1990;

Boero et al. 1992; Bouillon and Boero 2000). Furthermore,

Hydrozoa is currently the only class where molecular analysis

has been performed, although extensive gene expression stud-

ies have been carried out mostly with polyps.

The term tentacle is generally used to describe the flexible

appendages that are located near the mouth opening in cnid-

arians and are involved in capturing prey using nematocytes

(Ewer 1947). If a tentacle produced in the polyp showed

developmental continuity into the medusa, this would be

direct evidence that the polyp tentacles and the medusa

tentacles are essentially the same structure. This continuity,

however, is not seen. Instead, medusa tentacles are newly

formed during the process of medusa formation (namely,

asexual budding in Hydrozoa).

The morphology ofHydra, a hydrozoan research model, is

characterized by the solitary polyp form with the hypostome

surrounded by tentacles at the oral end, a large body column/

gastric region, and with the peduncle and foot region at the

aboral end (Fig. 1C). Hydra has been considered to represent

the typical solitary polyp form of this class. However, some

hydrozoans have polyps in which tentacles emerge in two

regions. A polyp of the hydrozoan family Corymorphidae

(Fig. 1D) has tentacles that are at a glance concentrated at

the oral end, suggesting that the morphology of the animal

is basically similar to Hydra. This view is, however, entirely

erroneous. The digestive region (denoted by DR) of a hydra

polyp, which is pink in color because of digested food content,

occupies about 3/4 of the body column length, whereas the rest

(about 1/4) corresponds to the peduncle region (Fig. 1C). In

contrast, the digestive region of a corymorphid polyp is the

region that lies between the two tentacle rings occupying only

about 1/10 of the body. The rest of the polyp (about 9/10) is

occupied by the peduncle region (Fig. 1D), demonstrating that

the two polyps have different proportions of the body parts in

apparently similar cylindrical morphology. Therefore, the po-

sition of the secondary tentacle ring of the corymorphid polyp

corresponds, in a hydra polyp, to the boundary between the

digestive region and the peduncle region, which is located on

the aboral side of the animal. Because the secondary tentacle

ring of the corymorphid polyp is located aboral to the digestive

region of the animal, the tentacles in the secondary ring should

be considered aboral tentacles. This implies that there are two

tentacle regions in the corymorphid polyp, one on the oral side

of the digestive region and the other in the aboral side of this

region. It should be noted that the tentacles in the two regions

are involved in capturing prey in a cooperative manner.

When three subclasses of Hydrozoa (Limnomedusae,

Anthmedusae [Athecata], and Leptomedusae [Thecata]) are

EVOLUTION & DEVELOPMENT 11:6, 619 –621 (2009)

DOI: 10.1111/j.1525-142X.2009.00368.x

& 2009 Wiley Periodicals, Inc. 619

surveyed based upon the results of Petersen (Petersen 1990)

according to the position of tentacles on the polyp form

termed hydropolyp, we find that in the Limnomedusae and

Leptomedusae, and order Filifera of Anthomedusae, tentacles

occur solely as one tentacle ring closely surrounding the

mouth of polyps, that is as oral tentacles. In contrast, we

find in the order Capitata of subclass Anthomedusae that

the majority of animals have tentacle rings in two regions of

hydropolyps, whereas some like Hydra have only one ring.

Despite this diversity, hydropolyps tend to be considered as

polyps having only one tentacle region at the oral end, as seen

with Hydra.

Formation of a hydromedusa occurs by an asexual repro-

ductive process termed budding (Boero et al. 1992). A min-

iature medusa-like structure is formed on the side of the body

column of a polyp. When this miniature medusa detaches

and becomes independent, it grows directly into the mature

medusa form. It is often the case in a hydromedusa that ten-

tacles are formed in two regions, first around the mouth as

‘‘oral tentacles’’ and second around the margin of the um-

brella as ‘‘marginal tentacles’’ (Fig. 1E). The oral tentacles of

hydromedusae are usually thinner and shorter than marginal

tentacles, and hence are sometimes unnoticed or ignored.

The formation of tentacles in two regions that occurs in

the hydropolyp and hydromedusa is, in fact, observed even in

the juvenile form of the animal termed the planula larva that

appears during development from the fertilized embryo to

the polyp form in some but not all species of hydrozoans. In

Tubularia mesembryanthemum for example, a larva having

tentacles on opposite sides of the animal appears (Fig. 1F)

and is termed an actinula (Hawes 1958). When the actinula

larva metamorphoses into a polyp, the short tentacles develop

into the oral tentacles of the polyp whereas the long tentacles

on the other side develop into the aboral tentacles, suggesting

that hydrozoans have two regions of tentacle formation in a

wide range of developmental stages.

We have presented several cases where there are two

tentacle regions in the polyp, the medusa, and the actinula

larva. As a natural outcome, the possibility arises that the oral

and aboral tentacles in the polyp are homologous to the oral

and marginal tentacles in the medusa. There is currently little

information on the molecular biology of medusae that is

relevant to this hypothesis. However, a study of one gene,

which encodes the homodomain-containing protein Otx, does

provide insight into the relationship between polyp and

medusa tentacles.

Otx plays a crucial role in specifying the forebrain and

midbrain of vertebrates (Millet et al. 1996). CnOtx, an

orthologue of Otx in Hydra, is expressed in the epithelial cells

in the digestive region of the body column (Smith et al. 1999).

If the pattern of CnOtx expression in hydropolyps that have

two tentacle regions is similar to the pattern in Hydra, the

predicted area of expression is the area between the two

tentacle regions. In Podocoryne carnea a marine hydrozoan,

the muscular tissue in the inner surface of the umbrella

expresses the Otx orthologue (Muller et al. 1999). This area of

tissue is located between the oral tentacles and the marginal

tentacles. Thus, the two tentacle regions, one in the polyp and

the other in the medusa, sandwich the CnOtx expressing tis-

sue. These results are consistent with the view that the tentacle

rings in the polyp and the medusa are homologous structures.

Based upon this view, we can simulate a virtual surgical

operation on a medusa (Fig. 2). By removing the thick ex-

tracellular matrix layer that resides in the extracellular space

Fig. 1. Morphological patterns in Cnidaria. (A) Textbook view of the attached form (polyp), (B) the textbook view of the swimming form(medusa), (C) a hydra polyp, (D) a corymorphid polyp, (E) a hydromedusa of Cladonema pacificum, (F) an actinula of Tubulariamesembryanthemum. In the hydra polyp (C), the digestive region and the peduncle region can be distinguished from each other by thesmaller body column diameter in the peduncle region, and by the food vacuoles found in the digestive region, but not in the peduncle region.In the corymorphid polyp (D), thin structures emerging near the aboral end of the animal are not tentacles but anchoring rootlets. DR,digestive region; OT, oral tentacle; AT, aboral tentacles; M, manubrium; MT, marginal tentacle. Bars represent 1mm (C), 5mm (D),0.5mm (E), and 100mm (F). (A and B after Ruppert and Barnes (1996); D after Sassaman and Rees (1978); F after Yamashita et al. (2003).)

620 EVOLUTION & DEVELOPMENT Vol. 11, No. 6, November--December 2009

of the umbrella, followed by detaching the outer layer and the

inner layer of tissue of the umbrella from each other, and by

extending along the oral aboral axis to fit onto a cylindrical

framework (Fig. 2C), the overall morphology of the medusa

(Fig. 2B) becomes similar to the morphology of a hydropolyp

(Fig. 2A) of the type with two tentacle rings as in Fig. 1D,

having CnOtx expressing tissue between the two rings. The

illustration in Fig. 2C therefore seems to give a more realistic

view of the relation between the body plan of the polyp and

the medusa than the classical one in Fig. 1, A and B.

To summarize, zoology textbooks have neglected aboral

tentacles of polyps and oral tentacles of medusae, and con-

cluded that the remaining oral tentacles of polyps and mar-

ginal tentacles of medusae are homologous (Fig. 1, A and B).

This misunderstanding has remained unchallenged because of

the lack of studies on the body plan of medusae. In addition,

research using hydrozoans has focused on Hydra as the rep-

resentative model organism, which has led researchers to

neglect aboral tentacles. Although the present analysis was

based largely upon morphological observations in published

studies, future molecular analyses are likely to provide further

evidence that aboral tentacles and marginal tentacles are

homologous.

AcknowledgmentsThe authors wish to thank Dr. Yamashita at Sessile ResearchCorporation Inc. for providing the photographs of Actinula. Theyalso wish to thank Prof. Diane Bridge at Elizabethtown Collegeand Prof. Robert E. Steele at University of California at Irvine forvaluable comments and discussions.

REFERENCES

Boero, F., Bouillon, J., and Piraino, S. 1992. On the origins and evolution ofhydromedusan life cycles (Cnidaria, Hydrozoa). Sex origin and evolu-tion. In R. Dallai (ed.). Selected Symposia and Monographs U.Z.I.. 6.Mucchi, Modena, pp. 59–68.

Bouillon, J., and Boero, F. 2000. Synopsis of the families and genera of thehydromedusae of the world, with a list of the worldwide species.Thalassia Salentina 24: 47–296.

Brusca, R. C., and Brusca, G. J. 1990. Invertebrates. Sinauer Associates,Massachusetts, pp. 211–214–217.

Ewer, R. F. 1947. On the functions and mode of action of the nematocystsof Hydra. Proc. Zool. Soc. London 117: 365–376.

Hawes, F. B. 1958. Preliminary observations on the settlement of actinulalarvae of Tubularia larynx (Ellis and Solander). Annu. Mag. Nat. Hist.13: 147–155.

Millet, S., Bloch-Gallego, E., Simeone, A., and Alvarado-Mallart, R. M.1996. The caudal limit of Otx2 gene expression as a marker of themidbrain/hindbrain boundary: a study using in situ hybridisation andchick/quail homotopic grafts. Development 122: 3785–3797.

Muller, P., Yanze, N., Schmid, V., and Spring, J. 1999. The homeobox geneOtx of the jellyfish Podocoryne carnea: role of a head gene in striatedmuscle and evolution. Dev. Biol. 216: 582–594.

Petersen, K. W. 1990. Evolution and taxonomy in capitate hydroids andmedusae (Cnidaria: Hydrozoa). Zool. J. Linn. Soc. 100: 101–231.

Ruppert, E. E., and Barnes, R. D. 1996. Invertebrate Zoology. 6th Ed.Saunders College Publishing, Ft. Worth, Texas, p. 104.

Sassaman, C., and Rees, J. T. 1978. The life cycle of Corymorpha(5Euphysora) bigelowi (Maas, 1905) and its significance in thesystematics of corymorphid hydromedusae. Biol. Bull. 154: 485–496.

Smith, K. M., Gee, L., Blitz, I. L., and Bode, H. R. 1999. CnOtx, a memberof the Otx gene family, has a role in cell movement in hydra. Dev. Biol.212: 392–404.

Yamashita, K., Kawai, S., Nakai, M., and Fusetani, N. 2003. Larvalbehavioral, morphological changes, and nematocyte dynamics duringsettlement of actinulae of Tubularia mesembryanthemum, Allman 1871(Hydrozoa: Tubulariidae). Biol. Bull. 204: 256–269.

Fig. 2. Comparison of Otx orthologue expression in a hydra polyp(A), a hydromedusa (B), and a hypothetical tissue converted from ahydromedusa (C). The area of tissue that expresses the Otx or-thologue is denoted by the thick part of the outline. OT, oraltentacles; MT, marginal tentacles.

The body plan of the cnidarianmedusa 621Shimizu and Namikawa