© 2000, Annual Reports of the Zoological Institute RAS.

Hydrida composition and place in the system of Hydroidea (Cnidaria: Hydrozoa)

Sofia D. Stepanjants, Boris A. Anokhin & Valentina G. Kuznetsova

Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, St. Petersburg, 199034, Russia
 

Introduction

As previously stated (Anokhin et al., 1998) many questions taxonomy of Hydrida remain unresolved. There is no clear evidence on the number of families in Hydrida as well as on the number of genera and species in the family Hydridae. There are difficulties in interpreting the taxonomic status of Hydrida and the relationship of this group with the other Hydroidea. According to the Russian and German taxonomists Hydrida are defined as a higher taxon, such as an order or a suborder (Naumov, 1960; Holstein, 1995). In the last decades Hydrida have been revised anew and now they are considered both as a family in the suborder Moerisiida, or as a family in the superfamily Moerisioidea, or even as the genus in the family Moerisiidae (Bouillon, 1985; Petersen, 1990).

Many taxonomists accept Hydrida consisting of two families Hydridae and Protohydridae (Naumov, 1960; Werner, 1984; Holstein, 1995; Schaefer, 1996). Petersen (1990) supposes Protohydridae to be the closest family to Hydridae, however classifies the former as a incertae sedis group. Bouillon (1985) includes Hydridae, Protohydridae and Moerisiidae as equal families into the superfamily Moerisioidea. Thus, the trend is to relate Hydridae and Protohydridae with Moerisiidae.

As for the number of genera included into the Hydrida, it is a maximum of 4 (Hydra, Pelmatohydra, Chlorohydra and Protohydra) and a minimum of the only Hydra. Consideration of Boreohydra within Hydrida (Ewer, 1948) was by accident.

The challenge now is to state our opinion on the above questions, based on some new data, including those on the external morphology, on a number of thin structures and karyotypes.

Material and methods

Only living specimens of the species presently attributed to Hydrida and Protohydra were used in the study.

Hydrida species, such as oligactis, vulgaris, circumcincta, oxycnida, viridissima were collected in different places of the north-western and southern parts of Russia and Belarus. Protohydra leuckarti was collected on the White Sea, in the places of the freshwater inflows into the sea.

Hydra species have been reared in the laboratory culture by the procedure described elsewhere (Anokhin et al., 1998). Specimens of P. leuckarti were kept in the refrigerator at +5 °C in the vessels with ground.

External morphology, including coloration of the living specimens, life history, budding, sexual reproduction as well as some thin structures and karyotypes were analyzed.

Techniques for preparing cytological slides and karyotyping were described elsewhere (Anokhin & Kuznetsova, 1999).

Results

To approach the problem of Hydrida composition the genera Hydra and Protohydra were compared. The representatives usually referred to these groups share some common features, the predominant of which is the development of gonads in the body wall epidermis. There are however much more substantial differences than similarities between these taxa (Table 1, Fig. 1).

Such characters as the absence of tentacles and desmonemes, diffuse nematocyst distribution, and presence of macrobasic mastigophores allow excluding Protohydra from the Hydrida. This conclusion is also well supported by a fairly important difference in the karyotype patterns between Hydra and Protohydra. All so far studied Hydra species were found to display the conservative chromosome number 2n = 30 and symmetrical karyotypes in which the chromosomes are about the same size (Ovanesjan & Kuznetsova, 1995; Anokhin & Kuznetsova, 1999). Although chromosome number in P. leuckarti is not yet definitely determined it is clearly lower being equal to 28 or 26, besides in this species we encounter an asymmetrical karyotype in which there are two size classes of chromosomes, the first consisting of a fairly large chromosome pair and the second being represented by the chromosomes of about the same size (unpublished data).

Table 1. Differences in the general characters of Protohydra and Hydra.

Table 2. Differences in the general characters of Hydra, Pelmatohydra and Chlorohydra.

Some of the morphological characters including diffuse nematocyst distribution, mastigophores (anisorhizas?) presence and desmonemes absence (partly) bring Protohydra closer to some Corymorphidae, especially to their aberrant representatives (Broch, 1937; Kramp, 1948-1949; Salvini-Plawen, 1987). Until the present time no karyological investigations have been conducted of Corymorphidae. Therefore the immediate task is to study the karyotypes of the representatives of this group, Boreohydra included.

Although the majority of the present taxonomists include the only genus Hydra in the family Hydridae, in the Russian literature the genera Pelmatohydra and Chlorohydra are sometimes considered as the valid ones (Naumov, 1960; Babitsky, 1995). Comparatively recently these generic names were used in the monograph "The Biology of Hydra and Some Other Coelenterates" (Lenhoff & Loomis, 1961). Campbell (1987) even using only the Hydra name for all species, distinguishes however "oligactis group" of species - the so-called "stalked hydras" - thus actually accepting the Pelmatohydra validity.

Although the present-day knowledge on the karyotype of H. oligactis (2n = 30, symmetrical, the second chromosome pair is nucleolus-bearing, C-heterochromatin blocs are located in the centromere loci) does not yet allow distinguishing this taxon from Hydra, a series of other characters indicate that the differences between Hydra and Pelmatohydra are of the generic level (Table 2). The most sufficient of these are the length and form of tentacles, stalk presence or absence, number of gonads, the thread coiling into isorhiza capsule. Based on the above characters we are inclined to declare Pelmatohydra (for the present with P. oligactis only) as a valid genus. This reestablishment is supported by R. Campbell, who also supposes that the genus Chlorohydra should be reestablished as well (personal communication). Although a number of discriminative characters, including two fairly essential (coloration and structure of the embriotheca surface: Table 2, Fig. 1) are characteristic of Chlorohydra (with a single species viridissima) they are presently in sufficient to consider Chlorohydra as a valid genus. Besides, karyotype of viridissima was shown to be of symmetrical type and includes 2n = 30 as in the case of all so far studied Hydra species (Ovanesjan, 1994). This taxon needs further investigation both by the traditional morphological methods and karyological ones including chromosomal banding techniques.

Summarizing, Hydrida is perceived to consist of the only family Hydridae with 2 (probably 3) genera Hydra, Pelmatohydra (probably Chlorohydra). Hydrida display a sufficiently large set of solid characters allowing us to consider it noticeably distinct from the other hydroid groups. Below a new diagnosis of Hydrida as a separate order is provided.

Fig. 1. Comparison of the general morphological characters of Protohydra, Pelmatohydra, Hydra and Chlorohydra (?) * - photo by Ovanesjan I.G. (1994).

Order Hydrida. Solitary, lacking skeleton polyps with the sole whorl of the hollow filiform tentacles around the hypostom. Asexual reproduction by the way of lateral budding is characteristic. Sexual reproduction exists, gonads developing in the epidermis of the polyp walls. Brien (1965) showed that the gonad development follows the medusoid nodule type. This testifies to medusoid nature of the hydras' gonads allowing to suggest the earlier embryonization in the hydras' life history. No free medusae. No planulae and parenchimulae in life history. Winter resting stages, covered with chitinous coat - embryotheca. Cnidome consists of 4 types of nematocysts: stenoteles, atrichous isorhizas, holotrichous isorhizas, and desmonemes. Karyotypes include as many as 30 chromosomes in all species studied. Karyotypes are symmetrical with chromosomes representing a regular gradation in size. Morphologically distinguishable sex chromosomes are absent. Chromosomes are predominantly meta -and submetacentric, while in separate species one-two acrocentric chromosomes occur (H. circumcincta). The conspicuous C-blocks (those of the constitutive heterochromatin) revealed by C-technique show a general tendency to be placed adjacent to the centromeres. There is mainly one pair of nucleolar chromosomes while in some species two pairs occur (H. vulgaris), the nucleolar organizers being more frequently placed distally on the second or on the third chromosome pairs. Meiosis is chiasmatic, one-two chiasmata are formed in every bivalent.

We believe that the current evidence does not favour the view that Hydrida are closely related to the Moerisioidea group. The same is that Moerisiidae belong into the Capitata group, which question would require the special consideration. Hydrida are suggested to have been derived as a separate aberrant line of Corymorphidae actinulae, parallel with the development of aberrant line of corymorphids, which could have led to Protohydra.

Conclusions

1. Composition and place of Hydrida in the Hydroidea system is still not adequately investigated.
2. Studies of the external morphology of the living polyps, life history, nematocysts, and karyotypes of different species, allow improving the generic composition of Hydrida: to recognise Hydra and Pelmatohydra as valid genera and to exclude the genus Protohydra (family Protohydridae) from Hydrida.
3. The reliable characters allowing to declare Hydrida as an independent order are established.
4. A series of the most typical Hydrida characters are thought to be a result of aberration.

Acknowledgements

The authors are thankful to all colleagues who helped to obtain the living Hydra material. We thank Prof. Dr. R. Campbell for the consultations concerning the Hydrida taxonomy. We would like to express our thanks to T. Platonova for languagecorrections. Our investigations were supported by the Russian Foundation for Basic Research (grants 00-04-48747 and 00-04-63069).

References

Anokhin, B.A., Stepanjants, S.D. & V.G. Kuznetsova. 1998. Hydra fauna of Leningrad Region and adjacent territory: taxonomy with the karyological analysis. Trudy Zool. Inst. Ross. Akad. Nauk 276: 19-26.

Anokhin, B.A. & V.G. Kuznetsova. 1999. Chromosome morphology and banding Patterns in Hydra oligactis Pallas and H. circumcincta Schulze (Hydroidea, Hydrida). Folia biol. Kraków 47 (3-4): 91-96.

Babitsky, Â.À. 1995. Ethological aspects and rate of a feeding of stalked hydra Pelmatohydra oligactis (Hydrida). Zool. Zh. 74 (4): 22-33. (In Russian).

Bouillon, J. 1985. Essai de classification des Hydropolypes-Hydromeduses (Hydrozoa - Cnidaria). Indo-Malayan Zool. 2 (1): 29-243.

Brien, P. 1965. L'embriogenese et la senescence de l'hydre d'eau douce. Mém. Acad. R. Belg., Cl. Sci. 36: 1-113.

Broch, H. 1937. Hydroidenuntersuchungen. VII: Corymorpha (Euphysa) annulicornis M. Sars 1859. Avh. norske VidenskAkad. Oslo, mat.-naturvid. Klasse 8: 1-32.

Campbell, R.D. 1987. A new species of Hydra (Cnidaria: Hydrozoa) from North America with comments on species clusters within the genus. Zool. J. Linn. Soc. 91: 253-263.

Ewer, R.F. 1948. A review of the Hydridae and two new species of Hydra from Natal. Proc. zool. Soc. Lond. 118 (1): 226-244.

Holstein, T. 1995. Cnidaria: Hydrozoa. In: Susswaserfauna von Mitteleuropa (J. Schwoerbel and P. Zwick. Eds.). Jena, Gustav Fischer Verl. 110 S.

Kramp, P.L. 1948-1949. Origin of the Hydroid Family Corymorphidae. Vidensk. Meddr dansk. naturh. Foren. 3: 183-215.

Lenhoff, H.M. & W.F. Loomis (Eds.). 1961. The biology of Hydra and of some other coelenterates. Univ. Florida, Miami Press. 467 pp.

Naumov, D.V. 1960. Hydroids and Hydromedusae of marine, brackish and freshwater basins of USSR. In: Opredeliteli po faune SSSR [Keys of the fauna of USSR]. Vol. 70. Moskva/Leningrad. 585 pp. (In Russian).

Ovanesjan, I.G. 1994. The karyotypes of Hydra vulgaris Pall. and Hydra viridissima Pall. (standard and Ag-NOR-differential staining) and the survey of the karyotype data on other Hydridae species (Cnidaria, Hydrozoa, Hydroidea, Hydrida): Graduate paper. St. Petersburg State University. (In Russian).

Ovanesjan, I.G. & V.G. Kuznetsova. 1995. The karyotype of Hydra vulgaris Pall. and the survey of the karyotype data on other Hydridae species (Cnidaria, Hydrozoa, Hydroidea, Hydrida). In: Cnidaria. Modern and perspective investigation. (S. Stepanjants. Ed.). Vol. 2. pp. 95-102. St.Petersburg. (Trudy Zool. Inst. Ross. Akad. Nauk 261).

Petersen, K.W. 1990. Evolution and taxonomy in capitate hydroids and medusae. Zool. J. Linn. Soc. 100: 101-231.

Salvini-Plawen, L. 1987. Mesopsammic Cnidaria from Plymouth (with systematic notes). J. mar. biol. Ass. U. K. 67: 623-637.

Schaefer, W. 1996. "Coelenterata", Cnidaria, Ctenophora. In: Speziellen Zoologie (W. Westheide and R. Rieger. Eds.). pp. 143-187. Jena, Gustav Fischer Verl.

Werner, B. 1984. Stamm Cnidaria. In: Lehrbuch der speziellen Zoologie (H.-E. Grüner. Ed.). Bd. 1 (2). pp. 11-305. Jena, Gustav Fisher Verl.