Australia and South America, and the smallest number from Africa. ..... and Australia are quite specific (e.g., Frey, 1973, .... M. tenuicornis Sars, 1896 (Australia).
191
Hydrobiologia 321 : 1 9 1-204, 1996. © 1996 Kluwer Academic Publishers. Printed in Belgium.
How many species of Cladocera are there? (Dedicated to the memory of Professor D. J. Frey)
N. M. Korovchinsky A.N. Severtsov Institute of Animal Evolutionary Morphology and Ecology, Russian Academy of Sciences, Leninsky prospect, 33, Moscow 117071, Russia Received 22 December 1994 ; in revised form 24 May 1995 ; accepted 2 August 1995
Key words : Cladocera, taxonomy, species estimation, world fauna
Abstract An estimation of the number of taxa within families, genera and local faunas of Cladocera reveals that only c . 129 species (17% of all known species) may be considered as sufficiently well described (valid species), and c . 146 as rather well described (fair species) but needing further study using modern methods of investigation . The status of all other species is vague . The families Chydoridae, Daphniidae and Sididae and genera Diaphanosoma, Daphnia, (including Daphniopsis), Megafenestra, Scapholeberis, Eurycercus, Chydorus, Ephemeroporus and Pleuroxus have been comparatively studied best . The largest number of valid species is known from Europe, North America, Australia and South America, and the smallest number from Africa . Presence of large number of vague species of Cladocera negatively affects faunistic, zoogeographic, and ecological studies of continental waters .
Introduction Over twenty years have passed since the publication of Frey's (1973) work on the taxonomy of three species of Eurycercus opened a new era in Cladoceran classification . He introduced new methods and the first serious evaluation of the theory of cosmopolitanism . This and follow-up investigations used a population approach, the study of large groups of specimens, ideally containing all sex and age stages, numerous characters, morphological variability, ontogenetic change, experimental crosses and the use of electron microscopy and electrophoresis (Frey, 1982a, 1987 ; Korovchinsky, 1992a) . It was shown that previous descriptions often concerned either species complexes, or intraspecific units (ecomorphs) . On the whole, most described species needed revision . Many new data published during recent years have further changed the Cladoceran system, and the time has come to review it from a theoretical and practical point of view, to reveal some future tasks and perspectives for Cladoceran taxonomy . Some recent reviews
(Dussart et al., 1984 ; Frey, 1987 ; Shiel & Williams, 1990 ; Dodson, 1991 ; Dumont, 1994) pay attention to breadth, not to the quality of the material studied, or they analyse only separate groups (e .g . the Chydoridae) . Besides, an important new view on the Cladocera as artificial taxon, to be divided into a number of orders (Ctenopoda, Anomopoda, Onychopoda and Haplopoda or Daphniiformes, Polyphemiformes and Leptodoriformes) (Fryer, 1987 ; Starobogatov, 1986) must be cited . The last author even considers them to represent two different subclasses . On the other hand, the use of the term Cladocera continues to be practically convenient.
Materials and methods Estimation of the known Cladoceran species number An enumeration of species listed in identification books, beginning with Behning (1941) (Table 1), and
1 92 Table 1 . List of identification books Group
Region (species number)
Author(s)
Cladocera
Caucasus (93)
Behning,1941
Cladocera Cladocera Cladocera
Czechoslovakia (105) USSR (177) USA (140)
Sramek-Husek et al., 1962 Manuilova, 1964 Brooks, 1966
Cladocera Moinidae Chydoridae
Great Britain (92) World fauna (18) World fauna (174) Germany (107)
Scourfield & Harding, 1966 Goulden, 1968 Smirnov, 1971
Cladocera Macrothricidae & Moinidae Cladocera Cladocera Cladocera
World fauna (85) European part of the USSR (61) USA (138) China (111)
F16ssner, 1972 Smirnov, 1976 Smirnov, 1977 Pennak,1978 Chiang & Du, 1978
Cladocera Cladocera Cladocera
Roumania (114) Australia (125) Italy (109)
Negrea, 1983 Smirnov & Timms, 1983 Margaritora, 1985
Polyphemiformes & Leptodoriformes Macrothricidae Sididae & Holopediidae
World fauna (34) World fauna (56) World fauna (42)
Mordukhai-Boltovskoi & Rivier, 1987 Smirnov, 1992 Korovchinsky, 1992
Table 2 . Species diversity of Cladocera Daphniiformes Family Species number (genera number) Sididae (8) Holopediidae (1)
40 2
Daphniidae (5) Moinidae (2) Macrothricidae (15) Ilyocryptidae (1)
134 26 56 18
Chydoridae (38) Bosminidae (2) General species number
274 18 568
taxonomic revisions and descriptions of new species revealed a number of species (568) in 8 families (Table 2) . This number differs rather strongly (by more than 100 species) from those published previously (Frey, 1966 ; Smirnov & Timms, 1983 ; Smirnov, 1986 ; Dumont, 1994), not only because of the continued addition of new species, but mainly because of our approach of the evaluation of the number of Daphniid species . According to modem data, there are more than 50 species of Daphnia (including Daphniopsis)
Polyphemiformes & Leptodoriformes Family Species number (genera number) Podonidae (7) Polyphemidae (1) Cercopagidae (2) Leptodoridae (1) General species number
17 2 14 1 34
(Glagolev, 1986 ; Benzie, 1986 ; Hann, 1986 ; Sergeev, 1990a, b) . In addition, we took into consideration all described species of Simocephalus and Ceriodaphnia (32 and 35 respectively), two genera which have not been revised yet . In the Macrothricidae, as a result of recent revision (Smirnov, 1992), the number of species has decreased, but this is mostly due to the creation of a new family, the Ilyocryptidae, with 18 species, and to the abolition
1 93 Table 3 . Main criteria of species' estimation
Species
1
Eurycercus lamellatus s . str.+
+
E. glacialis s . str.++ E. pompholygodes+ E. macracanthus++ E. microdontus++
-
E.longirostris+ E. vernalis+ E. nigracanthus+ Ilyocryptus cuneatus+
+
2
3
4
+
+ -
-
+ + +
I. spinosus++ I. silvaeducensis++ I. vitali+ I. paranaensis+ I. elegans+ I. cornutus++ I. gouldeni+++ . I. alexandrine I. raridentatus+++ I. samsuni++
Criteria : 5 6 7
• • • • • • •
• • • +
+ -
+ +
-
+
8
9
•
+ + - Smirnov, 1971 ; Frey, 1973 ; Duigan & Frey, 1987 ; Duigan, 1992 + - Hann, 1990 + + Frey, 1975
• -
+ + + + +
10
+ + + + +
-
Sources
Frey, 1973 Frey, 1978 Hann, 1982 Hann, 1982 Hann, 1990
- + - Stifter, 1988 + Stifter, 1988 • + + - Stifter, 1984 + + + +
+ Chirkova, 1982 + Paggi, 1989 + Paggi, 1992 + Mordukhai-Boltovskoi
+ - -
11
-
+
& Chirkova, 1973 + Williams, 1978 Negrea, 1987 + Smimov, 1989 Gundiiz, 1990
Criteria: 1 . Parthenogenetic and gamogenetic specimens ; 2 . Only parthenogenetic females ; 3 . Much material from different populations ; 4 . Much material from one population ; 5 . Few specimens from different populations ; 6 . Few or single specimen(s) from one population ; 7. Variability, ontogenesis ; 8. Type material or topotypical material ; 9 . Ecological data; 10. Detailed description based on many features ; 11 . Superficial description based on few features . Species : + - valid, ++ - fair, +++ - poor.
of the genus Echinisca, incorporated into the genus Macrothrix . Another 16 species were rejected. The family Chydoridae is the most speciose, and some of its genera (Eurycercus, Chydorus, Pleuroxus) became more speciose upon being revised (Frey, 1973, 1980, 1988, 1991, 1993 ; Hann, 1982, 1990) . The family Sididae, is an intensively studied group (Korovchinsky, 1986, 1987, 1992a, b) . Because of parallel tendencies in the number of newly described and abolished species, its general species richness remains almost unchanged . The families Moinidae, Ilyocryptidae, Bosminidae have been studied less thoroughly, though a steady addition of new species in these groups is to be noted .
Estimation of the valid number of Cladoceran species The next step is to examine how many of the c . 600 named taxa at the species level may be valid according to modern standards . As mentioned above, we need to reject classiccal typology, and reach a population level of investigation, based on large amounts of specimens, many taxonomic features, and knowledge of their variability . The morphological (or taxonomic) species concept accepts that species may be separated by means of ecological adaptations as well as by reproductive isolation. Its application depends on the degree of study of the material (intraspecific variability, range, population structure, ecology) . If the material is poorly studied (variability not known) this concept degenerates into typology (Severtsov, 1988) .
1 94
Fig. 1. Total number of valid and fair species (black and dotted columns) in different families of Daphnuformes .
too
60
20-
Fig. 2. Percent of valid and fair species in different families of Daphniiformes . Indications and sequences as in Fig. 1 .
An example of an analysis according to the criteria enumerated in Table 3 is given for representatives of genera Eurycercus (Chydoridae) and Ilyocryptus (Ilyocryptidae), In this, each species was incorporated into one of three categories, designated as `valid' (well described), `fair' (rather well described) and `poor' (inadequately described) . Valid species are usually characterized by scoring for criteria 1, 3 (5), 7, 10, but may also include species described only from parthenogenetic females from different populations and related to groups in which the taxonomic
weight of gamogenetic specimens seems not very high . The second group is mainly characterized by criteria 2, 5 (6), 10 and includes species well described mainly as parthenogenetic females, often without a study of variability, otherwise inadequately described species with peculiar diagnostic features. Representatives of these two groups (adding up to 126 and 146, respectively) (Table 4), described more or less in accordance with modern requirements, were judged to be valid at the species level .
1 95 "a
100
15
137
I"
se
I$8
NAM
Aft
SAD
SAM
Au
20
10
SI
U
Lat
Las
Sam
a
ps
30
1j, !
10
H#LM
Fig. 4. Percent of valid and fair species of Daphnliformes in different geographical regions . From left to right: Europe and Northern Asia, North America, Africa, South Asia, South America, Australia . Indications as in Fig . 1 . Figures on top of the column indicate total numbers of known species in particular regions . oaph
Msg
Sc
cer
Sin
Fig. 3. Total numbers of valid and fair species in different genera of the families Sididae (A) (From left to right : Sida-Si, Limnosida-Li (no such species), Latona-Lat, Latonopsis-Las, Sarsilatona-Sars, Diaphanosoma-Di, Pseudosida-Ps ; Daphniidae (B) : Daphnia-Daph, Megaphenestra-Meg, Scapholeberis-Sc, Ceriodaphnia-Cer, Simocephalis-Sim (no such species) ; Chydoridae (C) : Eurycercus-Eu, Pleuroxus-Pl, Alonella-Alla, Chydorus-Ch, Alona-Al, Acroperus-Ac, Camptocercus-Cam, Leydigia-Ley (no such species), Biapertura-Bi, Ephemeroporus-Eph. Indications as in Fig. 1 .
The taxonomic status of all other named species, mainly characterized by criteria 2, 6 (5), 11 is vague (poor species) . It is appropriate to note the exclusion of L alexandrinae (Table 3), described rather extensively on parthenogenetic and gamogenetic females, but without designation of clear diagnostic features (Stifter, 1991) . This case illustrates the persistant degree of subjectivity of the analysis . Widely distributed, often morphologically variable pantropical, panholarctic and panpalearctic taxa were incorporated into the `poor' group because they may in fact represent groups of species . The Cladoceran faunas of North and South America, the Far East, and Australia are quite specific (e .g., Frey, 1973, 1980, 1987 ; Paggi, 1978, 1979 ; Smirnov & Timms,
1983 ; Korovchinsky, 1986) . For this reason, many widespread species (e.g ., Sida crystallina, Daphnia obtusa, D. cucullata, Bosmina longirostris) were not included in Table 4 . They too may be well defined locally, but conspecificity of their populations over a wide range needs further confirmation, since it has been shown that even within Western Europe closely related species, not separated before, may co-occur (Frey, 1975 ; Duigan, 1992) . The estimation of species within each family requires an individual approach . Thus, the treatment of Chydorids should be detailed and whenever possible include an analysis of gamogenetic specimens and ontogenetic stages (Frey, 1980, 1987 ; Duigan & Murray, 1987) . The same is true of many Daphnia (Alonso, 1985 ; Glagolev, 1986; Kokkin & Williams, 1987), Moinidae (Goulden, 1968 ; Smirnov, 1976) and Bosminidae (Paggi, 1979 ; Kerfoot & Peterson, 1980 ; Korovchinsky, 1992a) . On the other hand, gamogenetic and juvenile specimens are not so important in Sidid taxonomy (Korovchinsky, 1987, 1992b), but these require a knowledge of intra- and interpopulation variability.
Results The Chydoridae comprise about half of all valid and fair species (121) . Daphniidae, Sididae and Moinidae follow them in that order (Fig . 1) . There are no valid species among the Holopediidae and Macrothricidae .
196
Table 4 . List of valid and fair Cladoceran species Valid species
Sarsilatona serricauda (Sars, 1901) Diaphanosoma mongolianum Ueno, 1938 D. lacustris Korinek, 1981 D. D. D. D.
orghidani Negrea, 1982 senegal Gauthier, 1951 celebensis Stingelin, 1900
chilense Daday, 1902 D. fluviatile Hansen, 1899 D. spinulosum Herbst, 1975 D. brevireme Sars, 1901
Fair species Sididae Latona parviremis Birge, 1910 Latonopsis australis (Sars, 1888) s . str. Sarsilatona papuana (Daday, 1900) S. behningi Korovchinsky, 1985 Diaphanosoma unguiculatum Gurney, 1927 D. chankensis Ueno, 1939 D. dubium Manuilova, 1964 s . str. D. modigliani Richard, 1894 s. str. D. orientalis Korovchinsky, 1986 D. excisum Sars, 1885 D. sarsi Richard, 1894 D. australiensis Korovchinsky, 1981 D. dentatum Herbst, 1968 D . polyspina Korovchinsky, 1982 D . volzi Stingelin, 1905 Pseudosida australiensis Korovchinsky, 1983 P ramosa Daday, 1904
Daphnia pusilla (Serventy, 1929)
Daphniidae Daphnia queenslandensis (Sergeev, 1990)
D . australis (Sergeev & Williams, 1985) D . quadrangulus (Sergeev, 1990) D . chilensis (Hann, 1986) D . ephemeralis (Schwartz & Hebert, 1985)
D . carinata King, 1853 s .l. (only in Australia) D . jollyi Petkovski, 1973 D . curvirostris Eylmann, 1887 D . brooksi Dodson, 1985
D . similis Claus, 1876 s. str. (only in Europe) D. similoides Hudec, 1991 D . nivalis Hebert, 1978
D . cristata Sars, 1862 D. gessneri Herbst, 1968 D . retrocurva Forbes, 1882 D . deserti Gauthier, 1927
D. D. D. D. D.
cephalata King, 1853 (only in Australia) lumholtzi Sars, 1885 (only in Australia) mediterranea Alonso, 1985 hispanica Glagolev & Alonso, 1989 occidentalis Benzie, 1986
Megafenestra aurita (S . Fischer, 1849) Scapholeberis rammneri Dumont & Pensaert, 1983 S. microcephala Sars, 1890
D. parvula Fordyce, 1901 D. catawba Coker, 1926 D. dubia Herrick, 1883 Megafenestra nasuta (Birge, 1879) Scapholeberis mucronata (O .F. Miller, 1776) S. kingi Sars, 1888
S. erinaceur Daday, 1903 S. spinifera (Nicolet, 1849) S. armata Herrick, 1882
Moina australiensis Sars, 1896 M. wierzejski Richard, 1895 M. affinis Birge, 1893 M. minuta Hansen, 1899 M. hutchinroni Brehm, 1937 M. reticulata (Daday, 1905)
Moinidae Moina belli Gurney, 1904 M. brachycephala Goulden, 1968 M. tenuicornis Sars, 1896 (Australia) M. lipini N. N . Smirnov, 1976 M. fexuosa Sars, 1897 (Australia) M. eugeniae Olivier, 1954 (S . Amer.)
1 97
Table 4 . (continued) Valid species M. rostrata McNair, 1980 M. orizae Hudec, 1987
Fair species M. baylyi Forro, 1985 M. kaszabi Forro, 1988 M. gouldeni Mirabdullaev, 1993 Macrothricidae Ophryoxus zini N . N . Smirnov, 1992 (Far East) Parophryoxus tubulatus Doolittle, 1909 (North America) Macrothrir pseudospinosa N. N. Smirnov, 1992 M. breviseta N. N . Smirnov, 1976
• indistincta N. N. Smimov, 1992 M. palearis Harding, 1955 (S. America) • carinata (N . N. Smirnov, 1976) • longiseta N. N . Smirnov, 1976 (Australia) M. schauinslandi Sars, 1904 M. flagellata (Smirnov & Timms, 1983) (Tasmania) M. williamsi Smirnov & Timms, 1983 (Australia) • timmsi (N . N . Smirnov, 1976) (Australia) M. .superaculeata (N . N. Smirnov, 1982) M. flabelligera N . N . Smirnov, 1992 s . str. (only in Australia) M. paulensis (Sars, 1900) M. mira (N . N. Smirnov, 1982) (South America) M. pectinata (N . N . Smirnov, 1976) (Australia) M. sibirica Daday, 1901 (Omsk, Siberia) M. capensis (Sars, 1916) M. sioli (N. N . Smirnov, 1982) (South America) M. malaysiensis Idris & Fernando, 1981 M. cornuta Daday, 1904 (Centr. Asia) M. pennigera Shen, Sung & Chen, 1964 (China) Wlassicsia pannononica Daday, 1904 W kinistinensis Birge, 1910 (North America) Onchobunops tuberculatus Frey & Paggi, 1972 (South America) Pseudomoina lemnae (King, 1853) Neothrix armata Gurney, 1927 N. superarmata N . N. Smirnov, 1989 (Australia) N. paucisetosa N. N . Smimov, 1989 (Australia) Cactus cactus (Vavra, 1900) (South America) Streblocerus pygmaeus Sars, 1901 (only in South America) S. inexpectatus Dumont, 1981 (Africa) Ilyocryptidae Ilyocryptus cuneatus Stifter, 1988 IL vitali Chirkova, 1982 I paranaensis Paggi, 1989 I. elegans Paggi, 1992
Ilyocryptus cornutus Mordukhai-Boltovskoi & Chirkova, 1973 I. .spinosus Stifter, 1988 I. samsuni Gundtiz, 1990 IL silvaeducensis Romijn, 1919
198
Table 4. (continued) Valid species
Eurycercus lamellatus (0 . F. Miuller, 1785) E. pompholygodes Frey, 1975 E. longirostris Hann, 1982 E. vernalis Hann, 1982 E. nigracanthus Hann, 1990 Saycia cooki (King, 1866) (only in Australia) Pleuroxus caca Harding, 1955 P. straminius Birge, 1879 P laevis Sars, 1862 s. str. P. chiangi Frey, 1988 P. aduncus (Jurine, 1820) s. str. P inermis Sars, 1896 P. hastirostris Sars, 1903 P .foveatus Frey, 1991 P. pigroides (Lilljeborg, 1901) P. wittsteini Studer, 1878 P. macquariensis Frey, 1993 P. scopuliferus Ekman, 1900 P. paraplesius Frey, 1993 P. varidentatus Frey, 1993 Archepleuroxus baylyi Smirnov & Timms, 1983 Plurispina chauliodus Frey, 1991 Planicirclus alticarinatus Frey, 1991 Dunhevedia odontoplax Sars, 1901 Alonella pulchella Herrick, 1884 Phrixura rostrata (Koch, 1841) s . str. P. leei (Chien, 1970) Chydorus sphaericus (0 . F. Muller, 1785) s . str. C. brevilabris Frey, 1980 C. biovatus Frey, 1985 C. invaginatus Frey, 1982 • linguilabris Frey, 1982 • bicornutus Doolittle, 1909
• bicollaris Frey, 1982 C. faviformis Birge, 1893 C. obscurirostris Frey, 1987 C. opacus Frey, 1987 C. sinensis Frey, 1987 C. pizarri Alonso, 1986 C,. ventricosus Daday, 1898 Dunhevedia serrata Daday, 1898 D. americana Rajapaksa & Fernando, 1987 Alona verrucosa Sars, 1901 A. setosocaudata Vasiljeva & Smirnov, 1969
Fair species Chydoridae Eurycercus glacialis Lilljeborg, 1887 s . str. • macracanthus Frey, 1973 E. microdonthus Frey, 1978 Pleuroxus halvenacus Frey, 1991 P. jugosus (Henry, 1922) P pamirensis (Werestchagin, 1923) (Pamir) P. triocellatus N. N. Smirnov, 1989 (Australia) Plurispina multituberculata Frey, 1991 Chydorus reticulatus Daday, 1898 C. canadensis Chengalath & Hann, 1981 C. angustirostris Frey, 1987 • nitidulus (Says, 1901) C. parvireticulatus Frey, 1987 • arcticus Roen, 1987 Dadaya macrops (Daday, 1898) (only in Sri Lanka) Anchistropus ominosus Smimov, 1985 Alona ovata Rey & Vasquez, 1986 A . setuloides Smirnov, 1983 (Australia) A . macracantha Smirnov, 1983 (Australia) A . smirnovi Petkovski et Fliissner, 1972 A . bromelicola Smirnov, 1988 (Nicaragua) A . setulosa Megard, 1967 A . macronyx Daday, 1898 A . simonei Dumont, 1981 A . nuragica Margaritora, 1971 A . taraporevalae Shirgur & Nike, 1977 A. fabricii Roen, 1992 Biapertura rigidicaudis N . N . Smimov, 1971 (Australia) B . longinqua N . N . Smirnov, 1971 (Australia) B . willisi N . N . Smimov, 1989 (Australia) Kurzia longirostris (Daday, 1898) (only in tropical Asia) Acroperus elongatus (Sars, 1862) s . str. A. americanus Kubersky, 1977 Kozhowia primigenia Vasiljeva & Smirnov, 1969 K. gajewskajae Vasiljeva & Smirnov, 1969 • brevidentata N. N . Srnimov, 1971 • kozhowi Vasiljeva & Smirnov, 1969 Camptocercus oklahomensis Mackin, 1930 Euryalona orientalis (Daday, 1898) E. fasciculata Daday, 1905 Bryospilus repens Frey, 1980 B . bifidus Frey, 1980 Ephemeroporus hybridus (Daday, 1905) E. tridentatus (Bergamin, 1939)
1 99
Table 4 . (continued) Valid species A. labrosa Vasiljeva & Smirnov, 1969 A, lapidicola Chengalath & Hann, 1981 A . borealis Chengalath & Hann, 1981 A . phreatica Dumont, 1983 A. iberica Alonso & Pretus, 1989 A. rectangula Sars, 1862 s . str. A . weinecki Studer, 1878 A . azorica Frenzel & Alonso, 1988 A. hercegovinae Brancelj, 1990 A. skew Brancelj, 1992
Fair species E. acanthodes Frey, 1982 E. epiaphantoii Alonso, 1987 Rak obtusus N. N . Smirnov & Timms, 1983 (Australia) R. labrosus N. N. Smimov & Timms, 1983 (Australia) Australochydorus aporus N . N . Smirnov & Timms, 1983 (Australia) Leberis aenigmatosa N . N . Smirnov, 1989 (Australia) Monospilus biocellatus N . N. Smirnov, 1994 (Australia)
A. bicolor Frey, 1965 A. diaphana King, 1853 s . str. A . alsafadii Dumont & Brancelj, 1994 Kurzia brevilabris Rajapaksa & Fernando, 1986 Kozhowia baikalensis Vasiljeva & Smirnov, 1969 Tretocephala ambigua (Lilljeborg, 1901) T colletti (Sacs, 1895) Oxyurella tenuicaudis (Sars, 1862) s . str. O. brevicaudis Michael & Frey, 1983 Notoalona globulosa (Daday, 1898) N. freyi Rajapaksa & Fernando, 1987 Estateroporus gauthieri Alonso, 1990 Ephemeroporus phintonicus (Margaritora, 1969) E. archboldi Frey, 1982 E. margalefi Alonso, 1987 CeLsinotum parooensis Frey, 1991 C. hypsilophum Frey, 1991 C. platamodes Frey, 1991
Bosmina chilensis Daday, 1902 B. hagmanni Stingelin, 1904 B. huaronensis Delachaux, 1918 Bosminopsis macaguensis Rey & Vasquez, 1986
Evadne anonyx Sars, 1897 Podonevadne trigona (Sars, 1897) P. angusta (Sars, 1902) P camptonyx (Sars, 1897) Cornigerius meoticus (Pengo, 1879)
Bosminidae Bosminopsis negrensis Brandorff, 1976 B. brandorffi Rey & Vasquez, 1989
Podonidae Pleopis schmackeri (Poppe, 1889) Evadne prolongata Behning, 1938 Cornigerius lacustris (Spandl, 1923) C. arvidi Mordukhai-Boltovskoi, 1967 C. bicornis (Zernov, 1901) Caspievadne maximowitschi (Sars, 1902) Polyphemidae
Polyphemus exiguus Sars, 1897
200 Table 4. (continued) Valid species
Fair species Cercopagidae
Bythotrephes longimanus Leydig, 1860 Cercopagis socialis (Grimm, 1877) C. pengoi (Ostroumov, 1891) C. spinicaudata Mordukhai-Boltovskoi, 1968 • micronyx Sars, 1897 • anonyx Sars, 1897
Cercopagis neonilae Sars, 1902 C. prolongata Sars, 1897 • longiventris Mordukhai-Boltovskoi, 1964 • robusta Sars, 1897 C. ossiani Mordukhai-Boltovskoi, 1968 • cylindrata Sars, 1897 • beklemishevi Mordukhai-Boltovskoi, 1964 C. longicaudata Sars, 1902
The remarks in parenthesis indicate insufficiently described species with peculiar diagnostic features or area where species were studied properly. Most of listed Polyphemiformes are Caspian or Ponto-Caspian endemics .
Fair species also dominate in the Sididae, and they are numerous in Chydoridae . The percent valid species in specific families shows an opposite trend . Beside Bosminidae, it is smallest in Daphniidae and Chydoridae and largest in Sididae and Moinidae (on average 48%) (Fig . 2) . The proportion of valid species only exceeds 30% in Moinidae, is 20% in Sididae, Chydoridae and Bosminidae and, on average, is not more than 17% for all families combined . Particular genera have been studied at different levels (Fig . 3) . The genus Diaphanosoma is best studied among Sidids (Paggi, 1978 ; Korinek, 1987 ; Korovchinsky, 1986, 1987, 1992a, b, 1993a, b), the genera Daphnia, Megafenestra and Scapholeberis among Daphniids (Alonso, 1985 ; Glagolev, 1986 ; Benzie, 1988 ; Dumont & Pensaert, 1983), and Eurycercus, Chydorus, Ephemeroporus, Pleuroxus in Chydoridae (Frey,1973,1975,1980,1982a, 1973,1975,19 1993 ; Hann, 1982, 1990, Alonso, 1987) . Other genera have been studied only superficially or have been completely neglected . It is rather paradoxical that Europe and North America have been studied practically at the same level as South America and Australia (Figs 4, 5) . The last continent exceeds the others in terms of its valid and fair species number (67, versus 46 and 43 in Europe and North America, respectively) . At the same time, many Australian species fall in the `fair' group . The number of valid and fair species is small in South Asia, and smallest in Africa . Recorded North Asian species include the Baikalian endemic chydorids (5 species of Kozhowia and 2 Alona) . On the whole the fraction of valid and fair species in different regions varies from
12 to 42%, and that of valid species from 5 to 20% (Fig . 4) . The abovementioned regions have also been studied at different intensities . The east side of North America has been investigated best, as well as India, Sri Lanka and Malaysia in Asia, Argentina and parts of the basins of the Orinoco and Amazon in South America, and the south-eastern region of Australia . The fauna of East Asia is believed to include a good share of endemics, according to the few modem data, but in spite of some monographs (Ueno, 1937 ; Chiang & Du, 1979), it is still little known . Chydoridae and Daphniidae are relatively best studied everywhere except in Africa, Sididae in Eurasia and South America, Moinidae and Macrothricidae in North America, South America and Australia, and Bosminidae in South America whence revisions of Bosmina (Paggi, 1979) and descriptions of endemic Bosminopsis (Brandorff, 1976, etc .) were published . Most representatives of the Polyphemiformes (26 species) have been comparatively well studied, because they are endemic of the Ponto-Caspian basin, often co-occur, and have distinctive taxonomic characters and a restricted distribution (e.g ., Pleopis schmackeri in the Western Pacific) . On the other hand, the taxonomic status of marine species with wide ranges (e .g ., Penilia avirostris), as well as species with holarctic distribution (e .g ., Leptodora kindti) is quite vague . Species have often been well studied over a small part of their range, such as, for example Daphnia lumholtzi and D. cephalata in Australia, and D. sim-
20 1
[5 SP .
Fig. 5. Total numbers of valid and fair species of Daphniiformes in different geographical regions . Indications as in Fig . 1 . In each row from left to right: Sididae, Daphniidae, Moinidae, Macrothricidae, Ilyocryptidae, Chydoridae, Bosminidae .
and Chydorus sphaericus s . str. in some European countries . His
Discussion More than 200 years have passed since the beginning of investigations on Cladocera by O . F. Miiller (Frey, 1982a). During that time, a large amount of work, including a number of monographs, have been published. This fact misleads many hydrobiologists, who believe that the Cladocera have been well studied taxonomically . The present analysis refutes this suggestion . Insufficient study is characteristic of all orders, families and local faunas . One may accept the validity of many European species, studied first among Cladocera and which are the type species of many genera . Subsequently they were often recorded for other continents on evidence of a superficial analysis, and in the belief that they are cosmopolitan in distribution (Frey, 1982a, 1987) . But
today it is no longer possible to be sure of an identification, even in Europe, where species have been studied most extensively. Many descriptions are inadequate and closely related species may co-occur, e.g ., Eurycercus lamellatus and E. pompholygodes (Frey, 1975), members of Chydorus sphaericus complex (Duigan, 1992), and species of Diaphanosoma (Korovchinsky, 1987) . Few European species have been redescribed in detail, and their revaluation often represents a major part of the revision of genera and species groups . Further, most well described species are known from few localities only (e .g., Eurycercus pompholygodes has been recorded from 5 points in Sweden only ; Chydorus sphaericus s. str. from some points in Denmark and Ireland, Daphnia hispanica from 9 points in Spain) . It is also necessary to stress that many taxonomists have paid most attention to forms living in the littoral zone and in small and temporary water bodies (Chydoridae, Macrothricidae, Moinidae, subgenus Ctenodaphnia, including Daphniopsis), not to the typical pelagic species which represent the traditional object of freshwater ecology . Thus the taxonomic status of the
202 species groups Daphnia longispina, D. atkinsoni and D. carinata s .l. remain unsolved on a broad geographic scale, though they have sometimes been successfully resolved locally (Glagolev, 1986 ; Flossner & Kraus, 1986 ; Benzie, 1988) . The same is characteristic for the complex of Diaphanosoma brachyurum (Korovchinsky, 1992a, b), and for the species of Bosmina (Paggi, 1979 ; Lieder, 1983) . In fact, only three species of Diaphanosoma and five species of pelagic Daphnia may be considered as comparatively well studied in Europe and North America. Even the well known and popular Daphnia magna is insufficiently studied from a taxonomic point of view . The transmutation of Cladoceran taxonomy at a modern level has hereby been outlined, but its further development will take a long time . Strictly speaking, even most species listed in Table 4 as valid cannot be considered well studied according to the criteria of the morphological concept of taxonomy, because they are known only from few localities, and their ranges and limits of morphological variability have not been established . Correct species identification usually is the first but important prerequisite to biological studies. But we have to conclude that all identification books (Table 1) are obsolete (Korovchinsky, 1992a) and even the most recent (Smirnov, 1992 ; Korovchinsky, 1992b) are already in need of updating.
Acknowledgements I thank Prof. D . Berner (Temple University, Philadelphia, USA) and Prof. H . J . Dumont (Institute of Ecology, University of Ghent, Belgium) for the correction of the English text and valuable comments, Prof . P. Larsson (Institute of Zoology, University of Bergen, Norway), Dr L . Weider (Max-Plank-Institut fur Limnologie, Plon, Germany), and two anonymous reviewers who helped me to revise the manuscript . I also thank Drs S . Maas (Institute of Ecology, University of Ghent, Belgium) for her kind assistance . This work was partly supported by the International Science Foundation (USA) .
References Alonso, M ., 1985 . Daphnia (Ctenodaphnia) mediterranea: A new species of Hyperhaline waters, long confused with D. (C.) dolichocephala Sars, 1895 . Hydrobiologia 128 : 217-228 .
Alonso, M ., 1987. Morphological Differentiation of two new Ephemeroporus species (Cladocera, Chydoridae) belonging to the barroisi complex : E. margalefi and E. epiophantoii, in Spain . Hydrobiologia 145 (Dev . Hydrobiol. 35) : 131-146 . Behning, A. L., 1941 . Kladotsera Kavkaza. Tbilisi, 384 pp . (Cladocera of Caucasus). Benzie, J . A . H ., 1986 . Phenetic and cladistic analysis of the phylogenetic relationships within the genus Daphnia worldwide. Hydrobiologia 140 : 105-124 . Benzie, J. A . H., 1988 . The systematics of Australian Daphnia (Cladocera: Daphniidae). Species descriptions and keys . Hydrobiologia 166 : 95-161 . Brandorff, G.-O ., 1976 . A new species of Bosminopris (Crustacea, Cladocera) from the Rio Negro. Acta Amazonica 6 : 109-114. Brooks, J . L ., 1957. The systematics of North American Daphnia . Mem. Conn . Acad. Arts Sci. 13 : 1-180 . Brooks, J . L ., 1966 . Cladocera . In : W. T. Edmondson (ed), H . B . Ward & G . S . Whipple's Freshwater Biology, 2nd Edn . J. Wiley & Sons, N .Y. : 587-656 . Chiang, S . C. & N . S . Du, 1979. Freshwater Cladocera . Fauna Sinica, 6, Crustacea . Academia Sinica, science Press, Peking, 297 pp. Chirkova, Z. N ., 1982. Ilyocryptus vitali sp .n . (Cladocera, Macrothricidae) iz ozjor tundry Kolskogo poluostrova . Zoologitchesky J . 61 : 699-706 . (Ilyocryptus vitali sp .n . (Cladocera, Macrothricidae) from tundrian lakes of Kola peninsula) . Dodson, S ., 1991 . Species richness of crustacean zooplankton in European lakes of different sizes . Verh. int . Ver. Limnol . 24 : 1223-1229. Duigan, C . A ., 1992 . The ecology and distribution of the littoral freshwater Chydoridae (Branchiopoda, Anomopoda) of Ireland, with taxonomic comments on some species . Hydrobiologia 241 : 1-70. Duigan, C . A . & D . G . Frey, 1987 . Eurycercus glacialis in Ireland (Cladocera, Chydoridae) . Int. Rev . ges. Hydrobiol . 72: 235-249. Duigan, C . A. & D . A . Murray, 1987. A contribution to the taxonomy of C. sphaericus sens. lat . (Cladocera, Chydoridae) . Hydrobiologia 145 (Dev. Hydrobiol . 35) : 113-124 . Dumont, H. J ., 1994. On the diversity of the Cladocera in the tropics . Hydrobiologia 272 (Dev. Hydrobiol. 92) : 27-38 . Dumont, H. J . & J. Pensaert, 1983 . A revision of the Scapholeberinae (Crustacea, Cladocera) . Hydrobiologia 100 : 3-45. Dussart, B . H., Fernando, C . H ., Matsumura-Tundisi, T . & R. J. Shiel, 1984. A revision of systematics, distribution and ecology of tropical freshwater zooplankton . Hydrobiologia 113 (Dev. Hydrobiol 23) : 77-91 . Fltissner, D ., 1972 . Kiemen- and Blattfusser, Branchiopoda . Fischliiuse, Branchiura. Tierwelt Dtl ., 60, 501 pp . F1Sssner, D . & K . Kraus, 1986. On the taxonomy of the Daphnia hyalina-galeata complex (Crustacea: Cladocera). Hydrobiologia 137 : 97-115 . Frey, D. G ., 1966 . Cladocera in space and time . Mar. Biol. Assoc . India, Proc . Symposium Crustacea 1 : 1-9 . Frey, D . G., 1973 . Comparative morphology and biology of three species of Eurycercus (Chydoridae, Cladocera) with a description of Eurycercus macracanthus sp .nov. Int. Revue ges. Hydrobiol . 58 :221-267 . Frey, D . G ., 1975 . Subgeneric differentiation within Eurycercus (Cladocera, Chydoridae) and a new species from northern Sweden. Hydrobiologia 46 : 263-300 . Frey, D . G ., 1980 . On the plurality of Chydorus sphaericus (0 . F. Miiller) (Cladocera, Chydoridae) and designation of a neotype from Sjaelso, Denmark. Hydrobiologia 69 : 83-123 . Frey, D. G., 1982a. Questions concerning cosmopolitanism in Cladocera. Arch. Hydrobiol . 93 : 484-502 .
203 Frey, D . G ., 1982b . Relocation of Chydorus barroisi and related species (Cladocera, Chydoridae) to a new genus and description of two new species . Hydrobiologia 86 : 231-269 . Frey, D . G .,1987 . The taxonomy and biogeography of the Cladocera . Hydrobiologia 145 (Dev. Hydrobiol . 35) : 5-17 . Frey, D . G., 1988 . Separation of Pleuroxus laevis Sars, 1861 from two resembling species in North America : Pleuroxus straminius Birge, 1879 and Pleuroxus chiangi n .sp . (Cladocera, Chydoridae) . Can J. Zool. 66 : 2534-2563 . Frey, D . G ., 1991 . The species of Pleuroxus and of three related genera (Anomopoda, Chydoridae) in Southern Australia and New Zealand . Rec . Australian Mus . 43 : 291-372 . Frey, D. G., 1993 . Species of Pleuroxus (Anomopoda, Chydoridae) from the subantarctic islands and southernmost South America : a partial unravelling of the Pleuroxus aduncus problem . Hydrobiologia 262: 145-188 . Fryer, G., 1987 . Morphology and classification of the so-called Cladocera . Hydrobiologia 145 (Dev. Hydrobiol . 35): 19-28. Glagolev, S . M., 1986. Species composition of Daphnia in Lake Glubokoe with notes on the taxonomy and geographical distribution of some species. Hydrobiologia 141(Dev . Hydrobiol. 36) : 55-82. Goulden, C. E ., 1968. The systematics and evolution of the Moinidae . Trans . Amer. Phil. Soc., Philadelphia, N .S. 58 : 1-101 . Gundtiz, E ., 1990 . A new species of Ilyocryptus (Crustacea : Anomopoda) from Bafra Balikg6ltl, Turkey . Hydrobiologia 199 : 237-241 . Hann, B . J ., 1982. Two new species of Eurycercus (Bullatifrons) from Eastern North America (Chydoridae, Cladocera) . Taxonomy, ontogeny, and biology . Int . Revue ges . Hydrobiol. 67 : 585610. Hann, B . J., 1986. Revision of the genus Daphniopsis Sars, 1903 (Cladocera, Daphniidae) and a description of Daphniopsis chilensis, new species, from South America . J. Crust. Biol . 6: 246-263 . Hann, B. J ., 1990. Redescription of Eurycercus (Teretifrons) glacialis (Cladocera, Chydoridae), and description of a new species, E. (T) nigracanthus, from Newfoundlend, Canada . Can. J. Zool . 68 : 2146-2157. Kerfoot, W. C . & C. Peterson, 1980. Predatory copepods and Bosmina : replacement cycles and further influences of predation upon prey reproduction . Ecology 61 : 417-431 . Kokkin, M. J . & W. D . Williams, 1987 . Is ephippial morphology a useful taxonomic descriptor in the Cladocera? An examination based on a study of Daphniopsis (Daphniidae) from Australian salt lakes . Hydrobiologia 145 (Dev. Hydrobiol . 35) : 67-73 . Korinek, V., 1987 . Revision of three species of the genus Diaphanosoma . Hydrobiologia 145 (Dev. Hydrobiol . 35) : 3545 . Korovchinsky, N. M ., 1986. On the taxonomy and geographical distribution of the superfamily Sidoidea Baird, 1850 (Crustacea : Cladocera) . Hydrobiologia 140: 243-253 . Korovchinsky, N. M., 1987. Study of Diaphanosoma species of the mongolianum group (Crustacea, Cladocera) . Int . Revue ges . Hydrobiol. 72 : 727-758 . Korovchinsky, N . M., 1992a . Sovremennoje sostoyanie i problemy systematiky vetvistousyh racoobraznyh . In N. N . Smirnov (ed), Sovremennye problemy izutchenya vetvystousyh rakoobraznyh . Gidrometeoizdat, St.-Peterburg: 4-45 . (Modem state and problems of Cladoceran taxonomy) . Korovchinsky, N. M ., 1992b. Sididae and Holopediidae . Guides to the identification of the Microinvertebrates of the Continental Waters of the World 3, SPB Acad . Publ ., The Hague, 82 pp . Korovchinsky, N . M ., 1993a Description of the male, analysis of morphological variability and geographical distribution
of Diaphanosoma senegal Gauthier, 1951 (Crustacea : Daphniiformes : Sididae) Hydrobiologia 259 : 9-16. Korovchinsky, N. M ., 1993b . New records of Diaphanosoma celebensis Stingelin, 1900 (Crustacea: Daphniiformes : Sididae) in tropical Asia with remarks on the morphological variability and biology of the species . Rev. Hydrobiol. trop . 26 : 119-125 . Lieder, U., 1983 . Die Arten der Untergattung Eubosmina Seligo, 1900 (Crustacea, Cladocera, Bosminidae). Mitt . Zool . Mus . Berlin 59 : 195-292 . Manuilova, E. F., 1964 . Cladocera fanny SSSR. Fauna of the USSR, 88, Nauka, Leningrad, 326 pp . Margaritora, F. G ., 1985 . Cladocera. Fauna d'Italia 23 . Ed. Calderini, Bologna, 399 pp . Mordukhai-Boltovskoi, F. D . & Z . N . Chirkova, 1973. Description of Ilyocryptus cornutus Mordukhai-Boltovskoi & Chirkova, 1972, Macrothricidae) . Crustaceana 25 : 119-128. Mordukhai-Boltovskoi, F . D . & I . K . Rivier, 1987 . Hyshnye vetvistousye Podonidac, Polyphemidae, Cercopagidae i Leptodoridae fanny mire. Nauka, Leningrad, 182 pp. (Predatory Cladocerans Podonidae, Polyphemidae, Cercopagidae and Leptodoridae of the world fauna) . Negrea, S ., 1983. Cladocera . Fauna Republ . Social . Romania 4, Edit. Academ ., Bucuresti, 399 pp. Paggi, J . C ., 1978. Revision de la especies argentinas del genero Diaphanosoma Fischer (Crustacea, Cladocera) . Acta zool . lilloana 33: 43-65. Paggi, J . C., 1979. Revision de la especies argentinas del genero Bosmina Baird agrupodas an el subgenero Neobosmina Lieder (Crustacea: Cladocera) . Acta zool. lilloana 35 : 137-162 . Paggi, J . C ., 1989 . A new species of Ilyocryptus (Crustacea : Anomopoda) from the river Parana basin, Argentina . Hydrobiologia 182 : 239-248 . Paggi, J . C ., 1992 . A new species of Ilyocryptus (Anomopoda: Macrothricidae) from Argentina . Hydrobiologia 231 : 141-151 . Pennak, R . W., 1978 . Fresh-water invertebrates of the United States . 2nd edn . Wiley, N .Y, 803 pp . Severtsov, A. S ., 1988. Sovremennye concepcii vida. Bull . Mosc . obschestva ispytat. prirody 93 : 3-15 (The modern concepts of species) . Sergeev, V., 1990a. A new species of Daphniopsis (Crustacea: Anomopoda: Daphniidae) from Australian salt lakes . Hydrobiologia 190 : 1-7 . Sergeev, V., 1990b . The ephippial female of a new species of Daphniopsis Sars, 1903 (Anomopoda, Daphniidae) from Queensland, Australia. Crustacean 59 : 146-155 . Shiel, R . J. & W. D. Williams, 1990. Species richness in tropical freshwaters of Australia. Hydrobiologia 202 : 175-183 . Smirnov, N. N., 1971 . Chydoridae fauny mira . Fauna SSSR 1, vyp . 2, nov .ser., N 101, Nauka, Leningrad, 531 pp . (Chydoridae of the world fauna) . Smimov, N. N., 1976 . Macrothricidae i Moinidae fauny mira . Fauna SSSR 1, vyp . 3, nov.ser., N 112, Nauka, Leningrad, 237 pp . (Macrothricidae and Moinidae of the world fauna) . Smirnov, N . N., 1977 . Cladocera. Opredelitel' presnovodnyh bespozvonochnyh Evropeyskoy chasti SSSR . Gidrometeoizdat, Leningrad: 219-241 . Smirnov, N . N., 1986 . Itogi izutchenya vetvistousyh racoobraznyh v SSSR . Vestnik zool ., N 5 : 3-9 . (Results of the Cladoceran investigation in the USSR) . Smirnov, N. N ., 1989 . Tropicheskie Cladocera . 2 . Novye vidy semeistv Chydoridae, Macrothricidae i Moinidae tropicheskoi Avstralii. Zoologitchesky J . 68 : 51-59 . (Tropical Cladocera . 2 . New species of the families Chydoridae, Macrothricidae and Moinidae of the tropical Australia) .
204 Smirnov, N . N ., 1992 . The Macrothricidae of the world . Guides to the identification of the microinvertebrates of the continental waters of the world 1, SPB Acad . Publ ., The Hague, 143 pp . Smirnov, N. N . & B . V. Timms, 1983 . A revision of the Australian Cladocera (Crustacea) . Rec. Austr. Mus . Suppl . 1 : 1-132 . Scourfield, D. J. & J. P. Harding, 1966. A key to the British species of freshwater Cladocera . Freshwat. biol . assoc . Sci. Publ. 5, 55 pp . Sramek-Husek, R., M . Straskraba & J . Brtek, 1962 . Lupenonozci Branchiopoda. Fauna CSSR 16, 470 pp . Starobogatov, Ya. I ., 1986. Systema racoobraznyh. Zoologitchesky 165 : 1769-1781 . (The system of Crustacea) . Stifter, P., 1984 . Redescription of llyocryptus silvaeducensis (Cladocera, Macrothricidae) . Vests. cs . spolec. zool. 48 : 132-136.
Stifter, P., 1988 . Two new species of the genus Ilyocryptus (Cladocera, Crustacea) confused with IL sordidus Lievin . Vests . cs . spolec . zool . 52 : 290-301 . Stifter, P., 1991 . A review of the genus Ilyocryptus (Crustacea: Anomopoda) from Europe. Hydrobiologia 225 (Dev. Hydrobiol. 71) :1-8. Ueno, M ., 1937 . Order Branchiopoda (Class Crustacea) . Fauna Nipponica, 135 pp . Williams, J . P., 1978. Ilyocryptus gouldeni, a new species of water flea, and the first American record of I. agilis Kurz (Crustacea: Cladocera : Macrothricidae) . Proc. Biol . Soc. Wach . 91 : 666-680.
