Bzohgical Journal of the Linnean Society (1993). 48: 239-266. With 5 figures
Zoogeography and life cycle patterns of
Mediterranean hydromedusae (Cnidaria)
Dipartimento di Biologia, Stazione de Biologia Manna, Universita di Lecce,
73100 Lecce, Italy
AND
J. BOUILLON
Laboraioire de <oologie, Universitk Libre de Bruxelles, Ave F.D. Roosevelt 50,
1050 Bruxelles, Belgique
Received July 1990, accepted far publication December 1991
The distribution of the 346 hydromedusan species hitherto recorded from the Mediterranean is
considered, dividing the species into zoogeographical groups. The consequences for dispersal due to
possession or lack of a medusa stage in the life cycle are discussed, and related to actual known
distributions. There is contradictory evidence for an influence of life cycle patterns on species
distribution. The Mediterranean hydromedusan fauna is composed of 19.5% endemic species. Their
origin is debatable. The majority of the remaining Mediterranean species is present in the Atlantic,
with various world distributions, and could have entered the Mediterranean from Gibraltar after the
Mcssinian crisis. Only 8.0% of the fauna is classified as Indo-Pacific, the species being mainly
restricted to the eastern basin, some of which have presumably migrated from the Red Sea via the
Suez Canal, being then classifiable as Lessepsian migrants. The importance of historical and climatic
factors in determining the composition of the Mediterranean fauna of hydromedusae is discussed.
ADDITIONAL KEY WORDS:-Hydrozoa
- hydroid - medusa - dispersal
CONTENTS
Introduction . . . . . . . . . . . . . . . .
The Mediterranean Sea . . . . . . . . . . . .
Zoogeographical regions . . . . . . . . . . . .
Biological features of hydromedusae affecting their distribution . . .
Types of hydromedusan life cycle and their possible relevance to dispersal
The Mediterranean hydromedusan fauna . . . . . . . .
Material and methods.
. . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . .
Circumtropical species . . . . . . . . . . . .
Endemic species . . . . . . . . . . . . . .
Boreal species
. . . . . . . . . . . . . .
Cosmopolitan species . . . . . . . . . . . . .
Tropical-Atlantic species . . . . . . . . . . . .
Mediterranean-Atlantic species . . . . . . . . . .
Indo-Pacific species . . . . . . . . . . . . .
0024-^066/93/030239
+28 $08.00/0
239
Q 1993 The Linnean Society of London
240
F BOER0 AND J. BOUILLON
. . . . . . . . . . . . . .
Discussion
Affinities of the Mediterranean hydromedusan fauna . . . . . . . .
The importance of life-cycle features in the distribution of Mediterranean
hydromedusae . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . .
References
. . . . . . . . . . . . . . .
Appendix
. . . . . . . . . . . . . . .
252
252
253
255
256
256
258
INTRODUCTION
The description and explanation of the distribution of organisms is the main
goal of biogeography. T h e theoretical framework on which biogeographical
analyses are usually based can be divided into two approaches: the historical and
the ecological.
The historical approach implies that the distribution o i a species reflects its
evolutionary history, so that biogeographic and phylogenetic analyses are strictly
related by taking speciation processes into account. The original version of the
historical approach consists of the dispersal theory, typically accepted by
Darwinian and Neo-Darwinian evolutionary biologists. According to this theory
species originate mainly by allopatry due to dispersal of members of the ancestral
population into separate geographic areas. The actual distribution of organisms
is thus the result of the dispersal of their ancestors, being due to the intrinsic
potential of the species, in terms of vagility.
In recent years the theories of historical biogeography have been changed by a
different approach which has led to vicariance biogeography, with the
integration of Croizat's panbiogeography (e.g. Croizat, 1964) and the cladistic
method (e.g. Nelson & Platnick, 1981 ) . Vicariance biogeography postulates that
ancestral species were widely distributed before the fragmentation of the
Pangaea and that continental drift led to physical separation of the original
populations, leading then to speciation. The actual distribution of organisms, in
this case, is due to extrinsic reasons, being caused by the fragmentation of the
areas inhabited by their ancestors. A further development of this second
approach led to cladistic biogeography (e.g. Humphries & Parenti, 1989), with
the construction of cladograms for both phylogenies and areas of distribution.
A contradiction between these two theories is, however, apparent. They take
into account two aspects of the history of life which are not mutually exclusive.
The fragmentation of the Pangaea undoubtedly had a decisive impact on both
speciation and distribution of organisms, but the possession of a wide distribution
throughout the Pangaea ( a starting point in vicariance biogeography) implied
dispersal from a centre of origin or, less probably, instantaneous speciation on a
worldwide scale.
The ecological approach (see, for instance, Davis, 1982; Endler, 1982; Blondel,
1986) states that historical factors are not necessarily linked to actual
distributions, and that species are present in those localities where their
ecological requirements are satisfied. Of course this condition must be valid for
every theory, and also in this case there is not a real conflict with the historical
approaches. Vermeij (1978) attempted to reconcile historical and ecological
approaches in marine zoogeography.
These problems, however, have been tackled mainly in terrestrial organisms.
Marine zoogeography, even in the light of the most modern approaches, is still
MEDITERRANEAN HYDROMEDUSAE
24 1
largely devoted to the determination of actual distributions. The unexplored
portions of the world ocean are so vast that the descriptive stage is far from being
completed (van der Spoel, 1983). Fishes and some invertebrates such as molluscs
have better known distributions, but this is usually not the case for the rest of the
faunas. Especially in invertebrates, marine biologists have mainly stressed the
evolution of life-history traits and their relevance to dispersal (e.g. Valentine &
Jablonski, 1983; Strathmann, 1985; Jackson, 1986), or have based the
explanation of species distributions in terms of adaptations to local conditions
e.g. Vermeij, 1978, 1989). For some groups, such as molluscs, however, lifehistory traits have been used to explain distributions (e.g. Scheltema, 1986) and
evolution (e.g. Jablonski, 1986).
Hydromedusae, in both their hydroid and medusa stages, occur commonly in
all oceans and seas but a synthesis of their world distribution has never been
attempted (see Kramp, 1959, 1961, 1968 for the medusa stage only). They have
much-differentiated cycles (see below), and almost all reproductive and dispersal
strategies of higher animals are already shown at the hydromedusan
evolutionary level.
We have chosen to study the relationships of the hydromedusan fauna of the
Mediterranean Sea because it is one of the better known in the world and
because the geological history of the basin has been recently carefully
reconstructed. The opening of the Suez Canal, connecting the Mediterranean
and the Red Sea, furthermore, constitutes a rare opportunity for 'experimental'
biogeography.
After a general description of the history and the physical conditions of the
Mediterranean, and of the life-cycle types of hydromedusae, we will consider the
affinities of the Mediterranean hydromedusan fauna, trying then to compare the
actual distributions with the results expected by the application of the different
biogeographic theories.
The Mediterranean Sea
The Mediterranean Sea is considered to be a relict of the Tethys Sea, the body
of water separating Gondwana and Laurasia following the fragmentation of
Pangaea. It connected the early Atlantic and Pacific Oceans. During the
Miocene (Pontian) the eastern part of the Tethys Sea closed, and the only
communication left was that with the Atlantic Ocean. When this connection
closed as well, the Messinian crisis (between 6 and 5 Ma BP) led to the almost
complete drying of the Mediterranean. Only the deeper parts of the basin seem
to have retained water (see Maldonado, 1985 for a review of the geological
history of the Mediterranean). Salinity, and probably temperature, were very
high. The opening of the Strait of Gibraltar (5 Ma BP) restored the level of the
sea. The Mediterranean relicts of the Tethys Sea, therefore, would have passed
the Messinian crisis in almost non-marine conditions or in refuge areas. This
possibly led to many local extinctions of both flora and fauna. The sea-grass
Posidonia is the most outstanding case of Tethyan endemism: representatives of
this genus live only in the Mediterranean and in Southern Australia. How the
ancestral stock of the single Mediterranean species, Posidonia oceanica, survived
the Messinian crisis is still debated and the same questions apply to the
remainder of presumed Tethyan species (see Perks, 1985, for a discussion).
242
F. BOERO AND J. BOUILLON
Recent studies (see Por, 1989, for a review) are showing that the Messinian crisis
was perhaps not so drastic throughout the basin as previously thought, so this
topic is to be considered as not completely clarified.
Today the Mediterranean communicates with the Atlantic via the Strait of
Gibraltar and with the Red Sea via the Suez Canal, opened in 1869.
The physico-chemical conditions of the Mediterranean are different from
those of the Atlantic Ocean and the Red Sea. Deep-water temperature is
constant at about 13'C. This is the mean temperature of the whole basin in the
cooler part of the year (January-March), with slightly higher values in the
eastern basin and very low values (4-5%) in the northern Adriatic. Surface
temperature can reach 28OC in August. In shallow waters, then, the temperature
differences between the warm and the cold season can approach 15-20°C.
Salinity is about 37%0, and so is higher than in the Atlantic (about 35Oh) and
lower than in the Red Sea (40-41%). The eastern basin has salinities of up to
39%. Strong seasonality is thus a striking feature of the Mediterranean.
Temperature is the most variable factor, accompanied by variations in a number
of other physical factors, including the concentration of nutrients, water
movement and light penetration. A 'warm' season (May-June to
October-November) thus alternates with a 'cold' season (November December
to AprilMay). Planktonic and benthic primary and secondary production show
sharp seasonal cycles reflecting this alternation of climatic conditions.
~ ~ g e o g r a p h i c aregions
i
Marine zoogeography is fairly advanced in some groups (especially
vertebrates) but lower invertebrates such as Hydrozoa have received scant
attention. The incompleteness of our knowledge even of the overall distribution
of hydromedusae is exemplified by the situation in the Pacific insular area. The
synopsis by Kramp (1968) is the standard work for the area and lists 59 species of
Antho- and Leptomedusae. A long period of observation at a single site in
Papua New Guinea raised the number to 176, with the description of 43 new
species and 96 new records from the area (Bouillon, Clareboudt & Seghers,
1986). Some of these newly described species are now being found in the
Mediterranean! It is hence inadvisable to divide the oceans into detailed regions
and subregions.
The
distribution
patterns
considered
(Mediterranean Endemic,
Mediterranean-Atlantic,
Boreal,
Tropical-Atlantic,
Indo-Pacific,
Circumtropical, Cosmopolitan) are, for convenience, taken to have the
Mediterranean as their centre and are compared with it (Fig. 1). They apply
then to the Mediterranean fauna and consider all the possible relations between
this and other faunas. For instance, we consider as Indo-Pacific the species found
both in the Mediterranean and the Indo-Pacific, even though an Indo-Pacific
species should not necessarily occur in the Mediterranean.
Biological features of hydromedusae affecting their distribution
Hydromedusae are represented by a medusa, a planula and a polyp stage.
The alternation of benthic and pelagic stages is a basic feature of hydromedusae,
though in some orders the polyp is absent (some Narcomedusae and all
MEDITERRANEAN HYDROMEDUSAE
.--.
*"
-
*.
Figure 1 . Zoogeographical regions for the Mediterranean hydromedusan fauna: A,
Mediterranean-Endemic; B, Mediterranea-Atlantic; C, Boreal; D, Tropical-Atlantic; E,
Indo-Pacific; F, Circumtropical; Cosmopolitan not shown. (Redrawn after C. N. Bianchi,
unpublished.)
Trachymedusae). Almost half of the Mediterranean species, however, have lost
the medusa stage by reduction (Table l ) , so that a much varied array of
dispersal strategies is present in this group. In this paper we consider the
planktonic medusa as the sexual, adult stage: it releases the gametes, giving rise
to non-feeding planula larvae from which, in most cases, originate hydroids (a
specialized type of larva) which, then, will produce medusae (see Boero &
Bouillon, 1987; Boero & Sara, 1987; and Bouillon, Boero & Fraschetti, 1991,
for recent discussions). This interpretation, however, is not accepted by other
hydromedusan workers (Cornelius, 1990). When the medusa is present in the
cycle, the adult shows the highest vagility and could be considered as the main
agent of dispersal. This is a reversal of the 'norm' in meroplanktonic animals,
where the larva, and not the adult, has a planktonic life.
F. BOER0 AND J. BOUILLON
244
TABLE
I. Distribution of Mediterranean hydromedusae
7-
Yo
"
%
g
%
mg
Yo
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Circumtropical
Cosmopolitan
Non-classifiable
Total
T,Total number of species referable to a given contingent and %, percentage ofthat contingent in respect to
the total fauna; m, number of species with medusa and %, percentage of such species within the contingent; g,
number of species with fixed gonophores and %, percentage of such species within the contingent; mg, number
of species with liberable eumedusoids and O/', percentage of such species within the contingent. *, Significant
difference ( x 2 test, P < 0.05) between species with medusae and species with fixed gonophores or liberable
eumedusoids; same difference, but highly significant (P < 0.01).
+
Types of hydromedusan life cycle and their possible relevance to dispersal
(Fig. 2 )
( 1 ) Medusa - planula - benthic hydroid - medusa
Dispersal is dependent on several factors: duration of life of the medusa (from
a few days to several months), duration of the free life of the usually hollow and
floating coeloblastula and planula larva (too few data for generalization, but a
maximum of 15 days seems to be possible), dispersal of hydroid via planktonic
propagules (e.g. Halecium pusillurn), life on nectonic (Hydrichthys), or planktonic
(Obelia, Kinetocodium, Pelagiana, parasitic Narcomedusae etc.) organisms, and
settling on floating algae or objects. A particular case is that recently reported by
Bouillon et al. ( 1991 ) in Laodicea indica, a leptomedusa producing planulae which,
according to the season, can give rise to hydroid colonies or short-lived fixed
gonothecae which immediately release a single medusa.
( 2 ) Liberated eumedusoid or swimming gonophore - planula - benthic hydroid - liberated
emedusoid or swimming gonophore
The planktonic life of liberated eumedusoids or swimming gonophores (reevolved medusiform stages) is usually just a few hours (see Boero & Bouillon,
1989) limiting the extent of dispersal. As in the former cases, however, the
hydroid can contribute to dispersal.
(3) Benthic hydroid - planula - benthic hydroid
The coeloblastula is absent and the morula and planula stages of these species
are usually dense and tend to sink. The possibilities for dispersal are thus limited.
In a few species the planula is known to be linked to the mother colony by
mucous threads which break only when settlement occurs. I n some groups a
non-feeding actinula larva occurs, showing some possibilities of dispersal.
Production of asexual propagules, life on pelagic organisms or on floating
objects, are still possible.
MEDUSA
POLYP
encystment possible
-to
+++
feedina
complete
-to ++ +
1 feedina
reduced
+
abolished
DISPERSAL
non-feedina
re-introduced
+
n.f.
n. f.
++
PLANULA .
encystment possible
-to +*+
MEDUSA
1 non -feeding
Figure 2. Life-cycle patterns of hydromedusae, with dispersal possibilities (from- 10
+ 1, presence ( + ) or absence f - ) of asexual reproduction, and trophic value of
the various stages Broken arrows: direi-t development, with no hydroid stage; solid arrows' indirect development, with hydroid stage.
246
F. BOER0 AND J. BOUILLON
(4) Medusa - planula - planktonic hydrozd - medusa
The benthic life is abolished and different dispersal strategies are employed by
planula, hydroid and medusa stages (e.g. Margelopsis, Pelagohydra, Velella, Porpita,
Climacocodon, Evens hexanemalis).
(5) Medusa - planula - medusa
This is considered a primitive type of life cycle and it is characteristic of most
of the Narcomedusae and all Trachymedusae. Besides exceptional benthic forms
(Ptychogastria), all species are holoplanktonic.
Asexual reproduction of medusae
The life span of medusae should set a limit on their dispersive capabilities. But
this is compensated by several ways of asexual reproduction such as fission and
budding of medusae from the manubrium or tentacular bulbs, gonothecae on
the circular or radial canals, polyps on the manubrium or radial canals. In this
way a medusa and its offspring should be able to cover unlimited distances,
provided that food availability and chemico-physical features of the water are
suitable (Kramp, 1959; Bouillon et al., 1986; Mills, 1987).
Encystment
Almost all hydroids are able to produce resting stages represented by dormant
hydrorhizae (Calder, 1990). Several species are known to produce planula
encystment and this phenomenon is probably more widespread than is known.
Recently Carre & Carre (1990) have described the asexual formation of resting
frustules from the medusa of Eucheilota paradoxica. Specimens capable of such
encystments can survive for long periods and become active again under proper
conditions. When the possibility of hydroids settling on floating objects
(including ships) is considered, it is evident that, theoretically, dispersal has no
limit (Cornelius, 1981;Jackson, 1986).
These life-cycle patterns should generate different dispersal possibilities, so
that it might be possible to classify them along an efficiency-of-dispersal
gradient. Picard (1958) and Boero (1984), however, have remarked that lifecycle features seem unimportant in determining the distribution patterns of
hydromedusae.
The most efficient cycle for dispersal we could envisage apriori is one with both
medusa and benthic hydroid. The two completely different dispersal and feeding
strategies, plus the planula stage, enable a wide array of possibilities, even
though not all species presumably can express the maximum theoretical dispersal
potential. The cycle of Laodicea indica, with the possibility of shifting from benthic
hydroid to benthic gonotheca, can be placed in this category. It might be
expected that species with such a life cycle would show a low rate of endemism,
with a high tendency to wide distribution.
The second position might be held by species having free medusae and
planktonic hydroids. They cannot take advantage of settlement and encystment
on floating objects, but are anyway able to disperse with two morphs having
different dispersal and feeding strategies.
Holoplanktonic species, with the medusa stage only, rely on a single morph
which, however, has no limitation due to the finding of a proper substratum for
MEDITERRANEAN HYDROMEDUSAE
247
larval settlement. The possibility of resting stages is only hypothetical and their
distribution is limited by food availability and physico-chemical conditions.
The lowest vagility is shown by species with liberable eumedusoids, swimming
gonophores and, above all, fixed gonophores. Their dispersal is mainly due to
the planula displacement but since their larval stages are solid and usually nonfloating, the covered distances should not be relevant. The dispersal of
propagules and resting stages deriving from the hydroid, however, is still
theoretically rather high.
We are aware that this scenario is oversimplified. The general biology of the
great majority of the species is still unknown and, furthermore, the life cycles of
about 75% of the species are still to be elucidated. It is to be expected that
species with no medusa stages show a greater tendency to dispersal by asexual
propagules or simply by colony rafting, but it is also true that species with
medusae can show planula settlement on substrata such as pteropods, fishes etc.,
so that there should be a certain balance among the different dispersal
mechanisms.
We will try to test the preceding assumptions against the known distribution of
the Mediterranean hydromedusae, assigning them to zoogeographical groups
and considering their life cycles. The analysis will be hindered by incomplete
knowledge of distributions and also by the fact that some areas have been
extensively investigated for medusae but not for hydroids, and vice versa.
It has been impractical to build up a group for each category of life cycle, and
we choose to divide the species into forms with medusae, forms with fixed
gonophores, and forms with liberable eumedusoids or swimming gonophores.
Species with pelagic hydroids and Trachymedusae (with no hydroid stage)
constitute a small fraction of the whole fauna: for ease of analysis they have been
considered as species with both hydroid and medusa stages.
Until now all species of hydromedusae are supposed to have a polyp stage,
with the exception only of some Narcomedusae and the Trachymedusae. But the
life cycles of 82 of the 143 Antho- and Leptomedusae species with medusae are
unknown or poorly known. As suggested by Bouillon et ul. (1991) it could be that
many or at least some species known only as medusae have no 'classical' polyp
stage.
Thus our speculations are based on incomplete knowledge, but it is also true
that the study of Mediterranean hydromedusae has been, and still is, rather
intense and that the Mediterranean is one of the best known hydromedusan
faunas of the world. The number of species treated here probably constitutes a
sufficiently large sample to allow some general considerations. The knowledge of
the distributions of many of them will surely improve, but this will take place
slowly and this is not a sufficient reason to delay delineation of general aspects of
species distribution.
The Mediterranean hydromedusanfauna
By hydromedusae we mean practically all Hydrozoa except Siphonophorae,
that is: Antho-, Lepto-, Laingio-, Limno-, Narco- and Trachymedusae, and the
Actinulidae (see Bouillon, 1985, for definition of orders).
No recent paper, to our knowledge, has treated the complete hydromedusan
fauna of the Mediterranean. Kramp (1959, 1961) treated the medusa stage only
F. BOER0 AND J. BOUILLON
248
.
(65 species), and Ficard (1958) considered both polyp and medusa stages of
Antho- and Leptomedusae (191 species). The preparation of a monograph on
Mediterranean hydromedusae has also contributed to the knowledge of the
group. T h e only part to have been published is that on the
Anthomedusae/Capitata (Brinckmann-Voss, 1970).
Many recent papers have greatly modified the knowledge of the composition
of the hydromedusan fauna of the Mediterranean, with new records and
descriptions of new families, genera, and species. These, at first, were considered
endemic to the basin, but many have since been recorded from other seas and
oceans.
MATERIAL AND METHODS
The distribution of the representatives of the various orders is summarized in
Tables 1 and 2. With the y2 test we tested the significance of the difference in
numbers between species with medusae and species with fixed gonophores,
swimming gonophores and liberable eumedusoids.
We included the species with swimming gonophores or liberable eumedusoids
in the group of species with fixed gonophores for a number of reasons: (1) the
possibility could be high that there are more species of Leptomedusae liberating
TABLE
2. Distribution o f the different orders of Mediterranean hydromedusae.
An~homedusae
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
ndo-Pacific
Circumliopical
Cosmopolitan
Non-classifiable
'total
Leptomedusae
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Circumtropical
Cosmopolitan
Non-classifiable
Total
Anthomedusac~Leptomedusae
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Gircumtropical
Cosmopolitan
Xon-classifiable
Total
MEDITERRANEAN HYDROMEDUSAE
249
Limnomedusae
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Circumtropical
Cosmopolitan
Nan-classifiable
Total
Narcomedusae (all m)
Endemic
.Vedi terranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Circumtropical
Cosmopolitan
Non-classifiable
Total
Trachymedusae (all m)
Endemic
Mediterranean Atlantic
Boreal
Tropical Atlantic
Indo-Pacific
Circumtropical
Cosmopolitan
Non-classifiable
Total
Actinulidae (all g)
Cosmopolitan
Mediterranean Atlantic
Total
Laingiomedusae (all m)
Indo-Pacific
Total
1
1
100
0.2
Abbreviations as in Table I.
gonophores than hitherto thought (Boero & Bouillon, 1989); (2) some species
may switch from fixed gonophores to liberable eumedusoids, according to
environmental conditions, so the two possibilities are not mutually exclusive
(Stefani, 1959); (3) the possibilities of dispersal obtained with a liberable
eumedusoid are presumably more similar to those obtained with fixed
gonophores than to those obtained with medusae.
RESULTS
The number ofhydromedusan species recorded from the Mediterranean is 346
(see Appendix). The number of species with medusae is not statistically different
F. BOER0 AND J. BOUILLON
Distribution
Figure 3. Species numbers of Mediterranean hydromcdusae. E, Endemic; MA,
Mediterranean-Atlantic; B, Boreal; TA Tropical-Atlantic: IP, Indo-Pacific, GI Circumtropical; C,
Cosmopolitan; NC, non-classifiable. T , Total, M, species with medusa; G, species with fixed
gonophorca; MG, species with liberable eumedusoids or swimming gonophores; *, Significant
difference (x2 test, P < 0.05) between species with medusae and species with fixed or swimming
gonophores or liberable eumedusoids; **same difference, but highly significant [P < 0.01).
than that without medusae. The situation, however, is completely different when
the most abundant groups are considered separately. Anthomedusae show a
significant prevalence of species with medusae, whereas in Leptomedusae the
species with fixed gonophores or short-lived medusoids prevail (Table 2).
The different zoogeographical groups (Figs 3-5) .are treated separately in
order of importance.
Czrcumtropical specie's
T h e circumtropical species are the most abundant, with a highly significant
prevalence of species with medusae. The Anthomedusae show a highly
significant difference in favour of the medusa stage; the Leptomedusae show no
significant difference between species with and without medusae; all LimnoNarco- and Trachymedusae have a well-developed medusa stage. The data show
that the medusa stage is dominant in the circumtropical Anthomedusae, but not
in the Leptomedusae.
D Q C 3
T M G M G
Distribution
Figure 4. Species numbers of Mediterranean Anthomedusae. Key as in Fig. 3.
MEDITERRANEAN HYDROMEDUSAE
Distribution
Figure 5. Species numbers o f .Mediterranean Leptornedusae. Key as in Fig. 3.
Endemic species
T h e endemic contingent is almost as important as the circumtropical one.
There is no significant difference between species with and without medusae in
Antho- and Leptomedusae. All Narco- and Trachymedusae have medusae. T h e
presence of a medusa stage in the life cycle of endemic Mediterranean
hydromedusae is rather widespread.
Boreal species
T h e overall difference between species with and without medusae is not
statistically significant. Leptomedusae, however, show a statistically highly
significant difference in favour of fixed gonophores. As in the circumtropical
contingent, Antho- and Leptomedusae show differing life-cycle patterns,
Anthomedusae being 'neutral', whereas Leptomedusae show a relevant
reduction of the medusa stage. I t is suggestive that the orders with prevalence of
the medusa stage (Narco-, Trachymedusae) have no boreal representatives in
the Mediterranean.
Cosmopolitan species
We reluctantly introduce this category which should comprise panoceanic
species occurring from the Polar seas to the Equator, I t is unlikely that such
species really exist, and their records in the literature could be due to insufficient
possibilities of discrimination in current taxonomy. Many of the supposed
cosmopolitan species may turn out to be eurythermic circumtropical, but this
sort of zoogeographical revision is outside the scope of the present paper.
T h e difference between cosmopolitan species with and without medusae is
statistically highly significant in favour of fixed gonophores. Cosmopolitan
Anthomedusae, however, show no significant difference whereas Leptomedusae
show a highly significant difl'erence for fixed gonophores; all Narco-, Limno- and
Trachymedusae have medusae whereas the Actinulidae have fixed gonophores.
The Mediterranean species with the broadest distributions show a sharp
252
F. BOERO AND J. BOUILLON
prevalence of forms deprived of the medusa stage and, again, Antho- and
Leptomedusae behave in an opposite way.
Tropical-Atlantic species
There are no significant differences between species with and without
medusae. This coiltingent does not show a significant prevalence of a given type
of life cycle.
Mediterranean-Atlantic species
There is no overall significant difference between species with and without
medusae. However, the Anthomedusae have a statistically significant difference
in favour of the medusa stage and the Leptomedusae have a statistically highly
significant difference in favour of fixed gonophores; Limno-, Narco- and
Trachymedusae, all have medusae; the only representative of the Actinulidar
has fixed gonophores. The presence of the medusa stage is different in Anthoand Leptomedusae, the two orders showing opposite life-cycle patterns. As in
some of the preceding cases, this is compensated in the overall picture, so that the
presence or absence of the medusa seems unimportant.
hdo-Pacific species
This group of species shows a highly significant difference in favour of the
medusa stage. The difference, however, is not significant for Leptomcdusae. The
presence of a medusa stage in the life cycles is widespread in the Indo-Pacific
species inhabiting the Mediterranean, but not in the Lcptomedusae, in which
the situation is balanced.
DISCUSSION
Affinities o f the Mediterranean hydromedwan j'auna
The endemic group is second only to the circumtropical one. This indicates a
great originality of the Mediterranean fauna. As remarked by Picard (1958),
however, the only certain endemics are those species restricted to particular
habitats not available outside the Mediterranean. Posidonia oceanica meadows
constitute an outstanding example (Boero, 1987). Many endemic species have
been found only once, in spite of intense collection in the basin in recent decades.
Their endemicity could be due to incomplete knowledge of their distribution.
These species could have arrived in the Mediterranean from other, less studied,
areas where they are more abundant but still undetected. Some of the endemic
species seem to be restricted to the Adriatic which, in fact, is a quite peculiar sea.
Its conditions might have facilitated speciation.
The environmental conditions of the Mediterranean, as already mentioned,
are very variable during the year and this should favour forms with a marked
tendency towards seasonality, such as hydromedusae. Warm-water species can
proliferate in the summer and pass the winter as resting stages. Cold-water
species could be active in the winter and spend the summer as resting stages.
This pattern is evident from studies of hydromedusae, of both hydroid and
MEDITERRANEAN HYDROMEDUSAE
253
medusa stages (see Boero, 1984, for a review, and Morri & Bianchi, 1983, for a
discussion of brackish water species).
Some of the endemic species could be relicts of the Tethys Sea. This can apply
to the species typical of Posidonia since this plant is supposed to be itself a
Tethyan relict. Paraco~yneh e i could be a Tethyan relict too, and features of its
life cycle (Bouillon, 1975) could have enabled it to survive the Messinian crisis.
Not many other species are easily classifiable in their endemicity. As already
said, they could be 'false endemics', due to sparse zoogeographical information,
but they could also have originated in the Mediterranean after, or during, the
Messinian crisis (see Pkrks, 1985; Sara, 1985; Tortonese, 1985; Por, 1989, for
recent discussions). Some endemic species are of dubious taxonomic validity,
owing to insufficient description. The difference in salinity between the
Mediterranean and the Atlantic could play a role in the confinement of
stenohaline species which evolved in the Mediterranean Sea. Dispersal of
specimens settled on floating objects or of strictly shallow-water species could be
influenced by the fact that, owing to the differences in density, the Atlantic
water enters the Mediterranean basin from the surface, whereas the
Mediterranean water flows out at a deeper level. Differences in salinity and
features of circulation could be the main causes for the confinement of the species
which evolved in the Mediterranean.
One hundred and twenty-six species are boreal, tropical Atlantic, or
Mediterranean-Atlantic; and 114 species are circumtropical or cosmopolitan.
Almost 70% of the hydromedusan fauna living in the Mediterranean could have
entered through the Strait of Gibraltar, having been found i n t h e corresponding
part of the Atlantic and also elsewhere.
Indo-Pacific species are noteworthy, representing only 8.0% of the fauna.
Picard (1958) stated that no Indo-Pacific species was present in the
Mediterranean, but the studies of Schmidt (1973, 1976), Marinopulos (19791,
Lakkis & Zeidane ( 1985), Goy, Lakkis & Zeidane ( 1 9901, Margulis (1989) and
others have shown that certain Indo-Pacific species are present in the
Mediterranean, mainly in the eastern part. This may be due to Lessepsian
migration through the Suez Canal, even though the absence of information
about the hydromedusan fauna of the Eastern Mediterranean before the opening
of this waterway allows no comparison between the situation before and after the
presence of a connection between the Mediterranean and the Red Sea.
The hydromedusan fauna of the Mediterranean, then, comprises a
conspicuous Atlantic contingent which, presumably, is the result of colonization
through the Strait of Gibraltar. A relatively high number of endemics gives
originality to the fauna, but it is difficult to ascertain their geographical origin,
even though some species could be Tethyan relicts. Lessepsian migration via the
Suez canal is slowly bringing Indo-Pacific species into the basin and it is
expected that this group will become increasingly reported in the near future,
following better exploration of the Eastern Basin. For a detailed treatment of
Lessepsian migration see Por (1989).
The importance of life-cycle features in the distribution of Mediterranean hydromedusae
The hypotheses resulting from our analysis of life-cycle features are only partly
confirmed by our data. Circumtropical species show a prevalence of cycles with a
medusa, but cosmopolitan species behave in exactly the opposite way and fixed
254
F. BOER0 AND J. BOUILLON
gonophores prevail over medusae. T h e endemic species should have shown a
sharp tendency towards medusa suppression. This is true for the species living on
Posidonia leaves, but the whole endemic hydrornedusan fauna shows no
significant difference between the two general types of life cycle. T h e data
regarding the single orders are even more contradictory. T h e opposite
patterns of dominance of species with and without medusae indicate that
Anthomedusae show a sharp tendency to conserve the medusa stage, whereas
most Leptomedusae have suppressed it. This could be explained by some
differences in colony organization between thecate (leptomedusan) hydroids and
athecate (anthomedusan) hydroids. Thecates often have highly integrated
colonies, formed by a high number of small polyps, whereas athecates usually
have bigger polyps and less integrated colonies. A sharp specialization of the
hydroid stage could have led to its prevalence over the medusa stage in
Leptomcdusae. This assumption, however, is probably too simplistic and the
problem calls for a deeper analysis which is outside the scope of the present
paper. T h e presence of the medusa stage, and so high degree of vagility, seems
not to be of importance in the patterns of distribution of the Mediterranean
hydromedusae as already observed by Picard (1 958). Cornelius (1981),
analysing the distribution of boreal hydroids, found that two-thirds lacked a
medusa stage, being, however, widely distributed in cooler parts of the northern
hemisphere.
The tendency to medusa reduction is evident also in the present data on
Mediterranean species of boreal affinity, whereas the species in other
zoogeographical groups do not show this feature. Furthermore, even though not
explicitly stated, it is apparent that Cornelius (1981) dealt mainly with records
of the hydroid stage, and this may limit the general value of his assumptions.
Asking the question if a medusa stage is 'better' for dispersal than fixed
gonophores is comparable to asking if planktotrophic larvae are more efficient
for dispersal than lecithotrophic ones. Following a series of mathematical
expressions Vance (1 973: 35 1 ) summarized his results with this sentence:
'Planktotrophy is more efficient than lecithotrophy when planktonic food is
abundant and planktonic predation is low, and lecithotrophy is more efficient
when either or both of these conditions is reversed'. I t is quite possible that
during daily, lunar, seasonal, annual and pluriannual cycles environmental
conditions might be successively better and worse for the different types of
dispersal mechanisms available to the various species. Over geological time this
should result in a uniform geographical distribution of nearly all marine species,
regardless of their dispersal mechanisms. This has obviously not occurred (see
van der Spoel, 1983, for discussion).
In our opinion the distribution of marine species or, a t least, of hydromedusae
does not depend on their modes of dispersal, but on their limits of environmental
tolerance. I t is possible that, in one of the many different ways listed above,
hydromedusae can widely disperse in the various oceans and seas. The absence
of a given species from a certain area may not depend on its not reaching it, but
on its lack of adaptation to local conditions. Over short periods, however, the
presence of a long-lived pelagic stage seems to be a successful mode of dispersal,
as indicated by the predominance of species with medusae in the Indo-Pacific
contigent that, presumably, is the result of a recent migration of species from the
Red Sea to the Mediterranean.
MEDITERRANEAN HYDROMEDUSAE
255
CONCLUSIONS
Historical factors have undoubtedly been important in recruitment to the
Mediterranean hydromedusan fauna. Species which entered the basin from the
Strait of Gibraltar after the Messiniari crisis largely determined the present day
fauna, together with a set of palaeoendemisms of Tethyan origin. The peculiar
conditions of the Mediterranean, then, led to speciation and neoendemism. This
interpretation is in accordance with the one detected in the Mediterranean
benthos by Fredj (1974) and in the Mediterranean plankton by Furnestin
(19.79).
This overall picture seems to reconcile quite well with the dispersal theory, but
it is notable that the possession of theoretically more or less efEcient means of
dispersal seems not to be important in the determination of the distribution of
the species. Recent migration from the Red Sea through the Suez Canal,
however, shows that efficient dispersal has a great importance in short-term
colonization of newly-available areas. Among Indo-Pacific forms, representing
probable Lessepsian migrants, in fact, species with medusae are significantly
more numerous than species with fixed gonophores, even though this is not true
for Leptomedusae. Por (1981) proposed a Lessepsian Province in the Eastern
part of the Mediterranean in direct contact with the Suez Canal, this Province
being characterized by a high number of Indo-Pacific species which had
migrated to the Mediterranean via the Suez Canal. The migration occurred in
spite of temperature and salinity barriers. Dispersal can clearly play a major role
in determining the distribution of marine species. The same can be said for
environmental features. Lessepsian migrants colonized the Mediterranean
because they were able to reach it and because they are adapted to live in a
'Mediterranean' environment. Efficiency of dispersal is important during the
first stages of colonization (prevalence of species with medusa stage in the group
which entered via Suez) but seems unimportant over geological time ('balanced'
situation in the species which entered via Gibraltar). The theory of vicariance
could possibly apply to the endemic species living on the leaves of Posidonia, but a
comparison of the hydroids of Mediterranean and Australian Posidonia has still to
be done. The two theories explaining biogeographical patterns can both be
applied to subsets of the hydromedusan fauna of the Mediterranean. Climatic
factors, however, play an important role in 'shaping' a given fauna. Recent
advances in biogeography (vicariance and cladistic biogeographies) refer almost
entirely to terrestrial florae and faunae. It is reasonable to assume that oceans
and mountains are almost insurmountable barriers for many terrestrial forms,
but the situation in the seas is completely different, and geographical barriers are
probably much less important in determining speciation and distribution
patterns of marine organisms. Fauchald (1984) rightly stated that, theoretically,
any organism can reach any point in the world ocean, in spite of its 'history'. For
these reasons we consider premature, for instance, the comparison of the wellknown hydromedusan fauna of the western Mediterranean with that of the
eastern Mediterranean or with that of deep waters of the basin: their data sets
are simply not comparable. The same is true for comparisons of the
hydromedusan fauna of the Mediterranean with those of the Red and the Black
seas.
As remarked by Sara (1985) the understanding of the causes of the
256
F. BOER0 AND J. BOUILLON
distributions of marine animals will be possible by taking into account not only
historical aspects (theories of vicariance and of dispersal) but also the
conditioning of the present-day environmental features. The statement by
Strong (1983: 640); 'Until autecological facets of existence are understood, it is
tenuous to infer much about synecological influences' is, in our opinion,
applicable also to marine zoogeography in terms of distribution of single species
vs composition of regional faunas.
ACKNOWLEDGEMENTS
This paper was written with contributions from UNEP, MURST (60% and
40% programs), the Fonds de la Recherche Fondamentale Collective nr.
2.9008.90, C. N. Bianchi (La Spezia), D. Calder (Toronto), P. F. S. Cornelius
(London), K. Mangin (Tucson), C . Morri (Genova), M. Sari (Genova) and
H. Zibrowius (Marseille) read and commented on the manuscript. C. N.
Bianchi (La Spczia) proposed the broad zoogeographical regions here adopted.
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APPENDIX
List of hydromedusan species hitherto recorded from the Mediterranean Sea. g: fixed
gonophores; ni: medusae; mg: liberable medusoids or swimming gonophores; ?: life cycle unknown
or poorly known; E: endemic; MA: Mediterranean Atlantic; B: boreal; TA: Tropical Atlantic; IP:
1ndo-Pacific; CT: circun~tropical;C: cosmopolitan; nc: non classifiable. species marked with an
asterisk (*) were added to the list wlien the present paper was in press and have not been
considered in the text. T h e adopted classification reflects suggestions recently proposed in the
paper by Bouillon et al. (1992).
Class HYDROZOA
Subclass HYDROIDOMEDL'SAE
Order ANTHOMEDCSAE 142: 85 m, 52 g, 5 mg
Suborder Filifera
Superfamily Bougaiiivillioidea
Bougainvilliidae 20: 11 m, 9 g
Bimeria wstita Wright, 1859
(*}Boue(iinviilia aurantiaciz Bouillon; 1980
Boueainvillia britannica (Forbes, 1841)
K o ~ i n i ~ z l l imaniculata
a
Haeckel, 1864
Beuginmiilia multirilia (Haeckel, 1879';
Boqaimillia ma-fcus {Allman, 1863)
Bougainvillia piapgaster (Haeckel. 1879;)
Claiwfiselia michaeli (Berrill, 1948)
Dico~yneconferta (Alder, 1857)
D i c o p e rorybcari (Allman, 1864)
Garseia franciscam (Torrey, 1902)
Garzieia g~i.ieaMotz-Kossowska, 1905
Carveia nutarts (Wright, 1859)
KoetliAerina fasciculata (Pkron & Lesneur, 1810)
Liz& blondina Forbes, 1848
Lizziafulgurwts (A. Agassiz, 1865)
Lzzzia octosIvIa (Haeckel, 1879)
Nubiella mitra Bouillon, 1980
Pachycordyle nafiolitana Weismann, 1883
Rhizorhagium arenosum (Aldcr, 1862)
Thamnostoma dibaiiwn (Biisch, 1851 )
Cytaeidae 6: 4 m, 2 g
Q l a & fmszlla Gcgcnbaur, 1857
Cytaeis tetrastyla Eschscholtz, 1829
Cytaeis vulgaris Agassiz & Maycr, 1899
Parafvtaeis odonia Bouillon, 1981
Perarelia pop(igt;lala Bavestrello, 1987
Perarella schneideri (Motz-Kossowska, 1905)
E
CT
IP
IP
E
E
Superfamily Clavoidae
Clavidae 7: 2 m, 5 g
C1az:a muUicornis (Forskal, 1775)
Car&o#hora caslfia (Pallas, 177 1)
Cor~ylo#horapusilla Motz-Kossowska, 1905
m?
m'?
m?
m?
g
g
.
MEDITERRANEAN HYDROMEDUSAE
Cofydendrium parasiiicum ( L., 1 767 )
Mrrona cornucopiat (Norman, 1864)
Oceania armaiw Koclliker, 1853
Turri~ospisnutriiula McCrady. 1859
Superfamily Eudendrioidea
Eudendriidae 1 3 13 g
Eudmdrium m a t u r n Tichomiroll', I887
Eudendriian ralceolatum Motz-Kossowska, 1905
Eudmdrium capi/lare Alder, 1856
Eudtdrium carneum Clarkc, 1882
Eudefidrkm c u n n k h a m i Kirkpatrick, 1910
Eud&ium Jragile Motz-Kossowska, 1905
EudendtI~tn;glumeratura Picard, 1952
Kudmdrium merulum Watson, 1985
Euder^riurrz ma~&ossowskae Picard, 1952
Eudendrzum rucwt~sum(Gnlelin, 1791)
Euderidrium rameum (Pallas, 1766;
Er~dtndnumramosum (L.,1758)
*ma
amboinense Pictet, 1893
Superfamily Hydractinodea
Hydractiniidae 14: 8 m, 3 g, 3 mg
eydractiuia aaileata (Wagner, 1833)
Hydractinia echwala Fleming, 1828
&drachma j'ucicoiu (M.
Sam, 1857)
Hydrwiinia ornata Bonnevie, 1899
Hfdructomma prmoti (Motz-Kossowska, 1905)
hdacoyne areola& (Alder, 1862)
Psdworyir hurealis (Mayer, 1900)
Podecoyne carnea M. Sars, 1846
Podawrym exigua (Haeckel, 1879)
Podocinyne hartlaubi Neppi & Stiasny, 191 1
Podwmyne minima (Trinci, 1903)
Podocar~inemimla (Mayqr, 1900)
,Y@fdaria inrrmis (Allman, 1872)
Tregoubovia atentaculda Picard, 1958
Ptilocodiidae I: 1 g
77if.cocodium brzeni Bouillon, 1967
Rhysiidae I: 1 g
in'
Rhysiu halecii (Hicksun & Gravely, 1907)
Stylastcridae 1: 1 g
Errina ospcfa (L., 1767)
Superfamily Pandeoidea
Niobiidae 1: 1 m
ffiobia dendratentaculata Mayer, 1900
Calycopsidae 2: 2 m
Bythotiara muwayz Gunther, 1903
Calycapsis simplex Kramp & Damns, 1925
Pandeidae 13: 13 rn
Amphintma dinema (Peron & Lesueur, 1810)
Amphimma rubrum (Kramp, 1957)
A m p h i m rtigosum (Mayer, 19(10)
h j f h i n e m a ium;la (Mayer, 1900)
Leuckariiara nohilis Hartlaub, 1913
Leuckurilara octona (Fleming, 1823)
Merga guileri Brinckmann, 1962
Merga tergoslina (Neppi & Stiasny, 1912)
Merga tregoubovi Picard, 1960
Merga violacea (Agassiz & Mayer, 1899)
.Veotwr& pileala (Forskal, 1775)
Octatiura russelli Kramp, 1953
Pandta conica (Quoy & Gaimard, 1827)
F. BOERO AND J. BOUILLON
260
Protiaridae 2: 2 m
Halitiara formosa Fewkes, 1882
(*) Haliliara inzexa Bouillon, 1980
Protiara kiranana (Pefon & Lesueur, 1810)
Trichydridae 1: 1 m
Trichydra oligonema (Kramp, 1955)
Superfamiiy Rathkeuidea
Rathkeidae 1; 1 m
Rathkea octopnnctata (M. Sara, 1835)
Suborder Capitata
Superfamily Acauloidea
Superfamily Corynoidea
Cladonematidae 1: I m
Corynidac 18: 12 m, 6 g
C q n e caespe.~Allman, 187 1
C o p e epi^oica Stechow, 1921
Cnrynefucicola De Filippi, 1866
C'eryne musmtdcs (L., 1761)
C o p e pusilia Gaertner, 1774
C o p e pintmri Schneider, 1897
Dicodonium adriaticurn Graeffe, 1884
Dicodunium ocellatum (Busch, 1851)
Dipureaa dolichogaster (Hacckel, 1864)
Dipurena haiterafa (Forbes, 1846)
Dtpurma ophiogaster (Haeckel, 1879-80)
D i p u r m reesi Vannucci, 1956
¥Sarsi.a eximia (Allman, 1859)
Sarsia gemmifera Forbes, 1848
Sarsia producta (Wright, 1858)
Sarsia prol@ra Forbes, 1848
Sarsia tubutosa (M.Sars, 1835)
Eleutheriidae 3: 3 m
Eleatheria clapartdei Hartlaub, 1889
Etmlheria dichotorna Quatrelages, 1842
Staurdadia porlmanni Brinckmann, 1964
Superfamily Moerisioidca
Moerisiidae 5: 5 m
Moerisia carinae Bouillon, 1981
MoenSia inkermanka Paltschikowa-Ostroumova,1925
Moerisia lyonsi Boulenger, 1908
Moerisia paltasi (Derzhavin, 1912)
Odessia maeotica (Ostroumoff, 1896)
Protohydridae 1: 1 g
Protohydra feuckarti Greef, 1869
* ) Spaeroeorynidae
)
Spaerocorym bedoti' Picket 1893
Superfamily Tricyclusoidea
Fricyclusidae 1: I g
Tricyclusa singularis (Schulze, 1876)
Superfamily Tubularioidea
Boreohydridae 1: 1 g
Psammafydra nana Schultz, 1950
MEDITERRANEAN HYDROMEDUSAE
Corymorphidae 9: 8 m, 1 g
Branchiocerianthw italicus Stechow, 1923
Coiymorpha nutarns M. Sam, 1835
Eucodoniam brownei Hartlauh, 1907
EupA,sora annulala Kramp, 1928
Euphysora bigelowi Maas, 1905
@ybvcodon prolifer L. Agassiz, 1862
Paragolhea bathybia Kramp, 1942
Plotocnide borealis Wagner, 1885
Vannucctaforbesii (Mayer, 1894)
Euphysidae 2: 1 m, 1 g
Euphysa auratu Forbes, 1848
(*) Euphysaftammea (Linko, 1905)
SifihonoA,dra adriatica Salvini-Plawen, 1966
Halocordylidae 1: 1 mg
Halocordyle tlisttcha (Goldfuss, 1820)
Paracorynidae 1: I g
Paracnryne huvei Picard, 1957
Tubulariidae 9: 6 m, 3 g
Ectspleura dumcrtieri (Van Beneden, 1844)
Eclopleura minerzu Mayer, 1900
Ectopleura sacculifera Kramp, 1957
Ectopleura wrighti Peterscn, 1979
Eugothoea petalina Margulis, 1989
Rhabdomi singularis Keferstein & Ehlers, 1861
Tubularia crocea Agassiz, 1862
Tibuiaria indivisa L., 1758
Tubutaria larynx Ellis & Solander, 1786
%.
Superfamily Porpitoidea
Porpitidae 2: 2 m
Porpiia prplla (L., 1 758)
Velella vefella (L., 1 758)
Superfamily Zancleoidea
Cladworynidae 1: 1 g
Cladoco~ynffloccosa Rotch, 187 1
Halocoryne epizoica Hadzi, 1917
Rosalindidae 1: I m
Rosalinda incruslans (Kramp, 1947)
Zancleidae 2: 2 m
<anclea coslaia Gegenbaur, 1857
m e a sessilis (Gosse, 1853)
Order LEPTOMEDUSAE 154: 57 m, 93 g, 4 mg
Suborder Conica
Infraorder Campanulinida
Superfamily Campanulinoidea
Aeq uomidae 4: 4 m
Aequorea forskalea PCron & Lesueur, 1810
Aequorea conica Browne, 1905
Aequorca pensilis (Eschscholtz, 1829)
Zygocama sp. Babnik, 1948
Blackfordiidac I: 1 m
Biackfoda ukginica Mayer, 1910
262
F. B O E R 0 AND J. BOUILLON
Campanulinidae 4: 4 g
Cdycella M g a (I.., 1767)
Cam~~anulina
hincksii Har tlaub, 1897
Egmundella amiranlen.~~.~
Millard & Bouillon, 1973
Lafoeina f e w & G.O. Sam, 1874
h&tldgazziidae 1: 1 m
Oi-tophtaluciumfunfranum (Quay & Gaimard, 1827)
Phialellidae 1: 1 n1
Phialella qnadrafa (Forbes, 1848)
Superfamily Dipicurosomtoidea
Melicertidae 1: I m
Orfhislumella graejfei (Neppi & Stiasny , 1911)
Superfamily Eirenoidea
Eirenidae 9: 8 m 1 mg
Eirtne viridula (Peron & Lesueur, 1810)
Eusymnanlhea kquilina inquilimi Palombi, 1935
Euiimo pegenbasri (Haeckel, 1864)
Eutima &lis
{Forbes & Goodsir, 1853)
Eutima mira McCrady, 1859
Eutonina sciniillarvs (Bigelow, 1909)
Helgicirrha c a n (Hacckcl, 1864)
Helgicirrho schulzei Hartlaub, 1909
i't'eotima lucullana [Delle Chiajc, 1822)
Laudireidae 8: 8 m
Kramptlia dubia Russell, 1957
Laodicea higeiortii Neppi & Stiasny, 19 12
Laodiceajijiana Agassiz & \layer. 1899
Uodicea oceliata Babnik, 1948
I s o d i ~ e aneptuna Mayer, 1900
Laodicea unduiata (Forbes & Goodsir, 1851')
Melicerlisw adnatica Neppi, 1915
Staurophora mertensii Brand t, 1838
Tiarannidae 1: 1 m
Mooderza rotunda (Quoy & Gaimard, 1827;
riaropsiidae 2: 2 rn
Ocl^gonade mediterranea Zoja, 1896
Tiaropsulium mediterranenm (Metschnikoff, 18861
Superfamily Lovenelloidea
Cirrholoveniidac I: 1 m
Cirrholovenia tetrunema Krarnp, 1959
Eucheilotidae 3: 3 m
Eucheilota maasi Neppi & Stiasny, 1911
Ewheiloia paradiixica Mayer, 1900
Eucheilota zcniricularis MrGrady. 1859
l^iMnella chiquitita Millard, 1959
Losenella cirrata (Hacckel, 1879)
iJiuenella ciausa (Loven, 1836)
Uvaulla pacilis (Clarke, 1882)
Lmmtlla fmniculata 5 .0. Sars, 1873)
Superfamily Mitrocomoidea
Mitrocomidae 2: 2 m
A¥fitrocoma annae Haeckel, 1864
Milrocomella howini (Kramp, 1930)
MKDHERRANEAN HYDROMEDUSAE
Infraorder 1.afoeida
Superfamily Lafoeidea
Hcbcllidae 7: 4 m, 2 g, 1 mg
Hebella hrochi {Hadzi, 1913)
Hebdla JUrax %Hard, 1957
Hebella parasilica ('Ciamician, 1880)
Hebella scadens (Bale, 1888)
Hebdla urrmiata Millard, I964
Arandia gigas ( Pieper, 1884)
Srandia michael-sarsz {Lcloup, 1935)
.4cyptolaria conftrta ( Allman, 1877)
FtUllum serpew (Hamall, 1848)
Filellum serratum (Clarke, 1879)
Laf'a~adumosa (Fleming, 1820)
Lafvea fruti~osa (Sars, 18.51)
Zy^ephylax hiarmak Billard, 1905
111f~orcicr
Haleciida
Superfamily Halecioidt'a
Haleciidac 18: 1 m, 16 g, 1 mg
Campaleciurn medusiferum Torrey, 1902
Hdecium banyuleme Moiz-Kossowska. 1911
Heleciwn beanii ijohnston, 1838)
Halecium coriicum Stcchow, 1919
Hueleriurn halecinm (L., 1758)
HaSerium {airosum Alder. 1859
H e l d lankesteri (Bourne, 1890)
Ildecium medihrraneum Weisinann, 1883
Halecium mnricaium [Ellis & Solander, 1786)
Halrcinm nunum Alder, 1859
Halecium peirosum Stechow, 1919
Hafecium pusillurn (M. Sars, 1857)
Halfcimn sessile Norman, 1867
Halecium tenellam Hincks, 1861
Hydranthea aliysii (Zoja, 1893)
Hydranthea margarica (Hincks, 1863;
Ophiodissa cacinijurmis (Ritchie, 1907'
Ophiodissa mirahilh (Hincks, 1868)
Infraorder Plumulariida
Superfamily Plumularoidea
Aglaophcniidae 15: 15 g
Aglmph~niaacacia Allmian, 1883
Maojheniu elongala Meneghini, 1845
Aglaaphenia harpago Von Schenek, 1963
.4g~aoflAeniakkhenpauer: (Heller, 1868)
Aglaophenia latecarinala Allman, 1877
Aflaophenia lophacarpa Allman, 1877
Aglaophenia picardi Svoboda, 1979
Aglaophmia pluma (L., 1758)
Aglaophnia octodonta (Heller, 1868j
Aglaophenia tuhijomis (Marktanner-Turncretscher, 1890)
.4~~laopACTiu
tubulifira (Hinds, 1861)
Cladocarpus dallfusi BiIlard, 1924
Thecocarpus distans (Allman, 1877)
Thecocarpus mynopAyllum ( I..., 1758)
Thecocarpus phyteuma (Kirchcnpauer, 1876)
Halopteriidae 7: 7 g
Antendla secufida& (Gmelhi, 1791)
Anteniulla siliquosa (Hincks, 1877 )
Halopleris caiharina (Johnston, 1833)
IP
E
c
E
c
B
TA
MA
B
TA
MA
TA
c
c
E
B
CT
MA
m?
g
g
g
K
g
g
B
K
g
g
g
g
g
g
me,
R
g
264
F. BOER0 AND J. BOUILLON
Hafopteris diaphana (Heller, 1868)
Haloptern giutinnsa (Lamouroux, 1816)
Halopteris litchtensterni (Marktanner-Turnerets~her,1890)
S~hi~otricha
frutescens (Ellis & Solander, 1786)
Kirchenpaueriidae 3: 3 g
Kkchenpaueria echinulata (=ricks, 1868)
Kirchmpawria pinnata (L., 1758)
Ventromma haleciaides (Alder, 1859)
Plurnulariidae 7: 7 g
h e r t e s i a aniennina (L., 1758)
Nernertesia ramosa Lamouroux, 1816
ffemertesia tctrasticha (Meneghini, 1845)
Plumularia obliqua (Thompson, 1844)
Plumularia putcheffa Bale, 1882
Plumuluria setacea (L., 1758)
Plumularia syriaca Billard, 1930
Superfamily Sertularioidea
Sertulariidae 22: 22 g
Amphisbeha optrculata (L.,1758)
Diphasia margarcta (Hassall, 1841)
D p m e n a disticha (Bosc, 1802)
Salacia desmoides (Torrey, 1902)
Salacia dubia (Billard, 1922)
Sertufarella arbuscula (Lamouroux, 181 6 j
Sertularella crassicaulis (Heller, 1868;
Sertularella cubica Garcia, Aguirre & Gonzalez, 1980
Strtularella cyldritheca (Allman, 1888)
Sertularclla fusiformis (Hincks, 1861)
Strtularella gaudichaudi f Lamouroux, 1824)
Sertularella gayi fLarnouroux, 1821)
Strtularella picta (Meyen, 1834)
Sertularella potyzonias (L., 1758)
Sertularella robust0 Coughtrey, 1876
Sertularilla simplex (Hutton, 1872)
Sertdartlla tmella (Alder, 1856)
Sertularia distans Lamourous, 1816
Sertularia perpusilla Stechow, 1919
Sertularia marginata (Kirchenpauer, 1864)
Sertularia turbinata (Lamouroux, 1816)
Thyroscyfihusfruticesus (Esper, 1793)
Syntheciidae 1: 1 g
Splhecium tvansi {Ellis & Solander, 1786)
Suborder Proboscoida
Superfamily Carnpanulariidea
Campanulariidae 24: 13 m, 10 g, 1 mg
Campanularia hincksii Alder, 1856
Campanulaha uolubifis (L,,1758)
Ctytia discoidea (Mayer, 1900)
Ctytia gracilis (Sars, 1851)
Clylia hemisphanica (L., 1767)
Qtia linearis (Thornely, 1899)
Clytia mccraityi (Brooks, 1888)
(*) Chtia macrogonia Bouillon, 1984
Ctytia noliformis (McCrady, 1859)
Clytiapaultasis (Vanhoffen, 1910)
Ctytia pentala (Mayer, 1900)
Chtia serrulata (Bale, 1888)
Gonolhyraea h e n i (Allman, 1859)
Hartlaubella gelatinosa (Pallas, 1776)
Laomedea anguiaia Hincks, 1861
Lomedea calceoliftra (Hincks, 1871)
C
B
TA
B
C
CT
CT
IP
TA
C
CT
g
K
m?
m?
m
rn?
m?
m?
m?
rn?
rn ?
IP
m?
C
B
TA
TA
B
K
g
g
MEDITERRANEAN HYDROMEDUSAE
h m e d e a flexwsa Alder, I856
Laomedea neglecta Alder, 1856
Obelia bidentata Clarke, 1875
Obelia dickotomu (I.., 1 758)
* Obeliajimbriata (Dalyell, 1848)
Obelia geniculata (I.., 1758)
Obelia longissima (Pallas, 1766)
O r f h o f i s agmmetrica (Stechow, 1919)
Orlkolyxis crmata (Hartlaub, 1901)
O&opyxts Integra (Macgillivray, 1842)
Order LAINGIOMEDUSAE 1: 1 m
Laingiidae 1: 1 m
Kantiella enigmatics Bouillon, 1978
Order LIMNOMEDL'SAE 9: 7 rn, 1 mg, 1 g
Armohydridae 1: 1 rng
Armhohydra janowzczi Swedrnark & 'I'eisrier, 1958
Microhydrulidae 1: 1 g
Microh~drdapontica Valkanov, 1965
Olindiasidae 6: 6 m
Gospedamia sowerbyi Lankester, 1880
Gonionemus vertens A. Agassiz, 1862
Gossea corynetes (Gosse, 1853)
Matotias inexpecida Ostrournoff, 1896
Olindias phehorica (Delle Chiaje, 1841)
Scolionma suvaensf (Agassiz & Mayer, 1899)
C
CT
MA
I'A
TA
IP
m
m
rn
m
rn
rn
F'roboscidactylidae 1: 1 rn
Proboscidactyia omata (McCrady, 1857)
Order NARCOMEDUSAE 20: 20 m
Aeginidae 2: 2 rn
Aqinia citrea Eschscholtz, 1829
Solmundella bitentaculata (Quay & Gaimard, 1833)
Cuninidae 9: 9 m
Cuninafrugfera Kramp, 1948
Cunina globosa Eschscholtz, 1829
Cunina laiiventris Gegenbaur, 1856 (doubtful, probably C. globosa)
Cunina octonaria McCrad y, 1857
Cunina polyfiinia (Haeckel, 1879) (doubtful)
Cmina poboscidea E. & L. Metschnikoff, 1871
Cunina vitrea Gegenbaur, 1856 (doubtful, probably C. pruboscidea}
Solmissus albescew (Gegenbaur, 1856)
Solmissus incise (Fewkes, 1886)
Solmarisidae 9: 9 m
Pegantha mollicina (Forskal, 1775) (doubtful)
Pegantha ntbiginosa (Koelliker, 1853)
Pegantha triloba Haeckel, 1879
Pegantha mnaria (Haeckel, 1879) (doubtful)
Solmaris corona (Keferstein & Ehlers, 1861)
Solmaris flavescens (Koelliker, 1853)
Solmaris leucostyla (Will, 1844)
Solmaris sofma~is(Gegenbaur, 1856)
Solmaris vanhoeffeni Neppi & Stiasny, 1911
C
CT
err
CT
E
E
E
IP
CT
m
rn
rn
rn
m
m
m
m
m
Order TRACHYMEDUSAE 17: 17 m
Geryoniidae 2: 2 m
Gerysnia poboscidatis (Forskal, 1775)
Liriofu fetraphylla (Chamisso & Eysenhardt, 1821)
err
CT
m
rn
F. BOER0 AND J. BOUILLON
266
Halicreatidae 1: 1 m
ffaltscera tonzca Vanhoffrn, 1W2
* I Hahtrrphes m a w Bigelow, 1909
Pcta$idac 1: 1 rn
5'e~asus a t m Haeckcl, 1879
Ptychogastriidae 1: 1 m
Pwhogastna asternides (Haeckcl, 1879)
Rhopalonematidae 12 12 m
Aglaura hern~~turna
Peron & Liqueur, 1810
Amphagonu puiilla Harttaub, 1909
Ar;ta.podfina ampla (Varihof1en, 1902)
Hornwowma plv&snoa Browne, 1903
Panthachqon hatckelt Maas 1893
Panthiichigan &tare (Maas, 1893)
P e r a 7ncoIarata M~Crddy,185J
Ransonta krumpi ,Ranson, 1932)
Rhopalonema funfranurn Vanhoffcn, 1902
Rhopalonema velaturn Gegenb'~ur, 1856
Smmikea euygastra Gegenbaur, 1856
'letrorcht~eythrngaster Bigrlow , 1909
Order ACTINULIDAE 3: 3 g
Halarnmohydridae 2: 2 g
Halammuhydra vct@odides Remane, 1927
Halamohydra sh&ez Remane, 1927
Otohydridac 1: 1 g
Otuh$ra
vagans Swedmark & Teissier, 1958