Q Zoological Institute, St.Petersburg, 1998

Phylogeny and higher classification of Ephemeroptera

N.Ju. Kluge

Kluge, N.Ju. 1998. Phylogeny and higher classification of Ephemeroptera. Zoosj~s- tematica Rossica, 7(2): 255-269.

The order Ephemeroptera is divlded into Permoplectoptera and Euplectoptera; Eu- plectoptera are divided into two holophyletic taxa - Posteritorna and Anteritorna; An- teritorna are divided into Tridentiseta (which is possibly a paraphyletic group) and a holophyletic taxon Bidentiseta; Bidentiseta are divided into Branchitergaliae and Fur- catergaliae. Characters of these taxa are described and discussed, together with charac- ters of higher taxa in Ephemeroptera suggested by other authors.

N.Ju. Kluge, Department of Enromology, Biological Faculty, St.Petersburg State Uni- versity, Universitetskaya nab. 7, Sr.Petersburg 199034, Russia.

INTRODUCTION were united with some other taxa into a sub- order which was regarded as holophyletic This paper represents a report made at the (Pannota, Furcatergalia, or Rectracheata). VII International Conference on Epheme- But earlier an opposite idea was expressed, roptera in 1992 in Orono, Mine, USA (Klu- according to which Baetiscidae and Prosop- ge, 1992a), and the manuscript was submit- istomatidae separated early from other ted to the Proceedings of the Conference. Ephemeroptera and inherited their unusual Because of a confusion, the paper was not fore wing venation with unforked CuA from published in the Proceedings which appeared the Paleozoic Misthodotidae (belonging to in 1995. In spite of that, the paper was cited the extinct suborder Permoplectoptera), as a published one (Kluge et al, 1995), and while other recent originated from the names of new taxa introduced in this pa- another Palaeozoic family of the suborder per were used (Kluge, 1992b, 1993a, 1993b; Permoplectoptera -- Protereismatidae (Ed- Kluge et al., 1995). Here this paper is given munds & Traver, 1954a; etc.). with some later corrections. In the present paper, a new version of McCafferty & Edmunds (I 979) divided all phylogeny and a new classification of recent Ephemeroptera into two suborders, Ephemeroptera are suggested. It has been al- Schistonota and Pannota. Kluge (1 989) sug- ready published briefly in some papers gested another division of recent Ephe- (Kluge, 1992a, I992b, 1993b; Kluge et al., meroptera into two suborders, Costatergalia 1995). This classification is given below. and Furcatergalia. McCafferty (1 99 1) di- vided recent Ephemeroptera into three sub- TA4XONOMICPART orders: Pisciforma, Setisura and Rectra- cheata. In all these three classifications, one of the suborders (Schistonota, Costatergalia and Pisciforma) is wittingly paraphyletic, while the others (Pannota, Furcatergalia, The order is divided into (1) Permoplec- Setisura and Rectracheata) were regarded to toptera and (2) Euplectoptera. be holophyletic. In these three successive classifications, the volume of the para- 1 . Permoplectoptera Tillyard, 1932 phyletic taxon decreased, while the volume of holophyletic taxa increased. This corre- An extinct (Permian - Triassic) taxon, sponds to the general direction in which all characterized by homonornous wings and classification of organisms changes. In each of the three classifications, the some other plesiomorphies. A paraphyletic families Baetiscidae and Prosopistomatidae taxon ancestral to Euplectoptera. 256 N.Ju. Muge;Classificar,ion oJEphemeroptercr ZOOSYST. ROSSICA Vol. 7 2. Euplectoptera Tilly ard, 1932 Anteritorna are divided into (2.2.1) Tri- dentiseta and (2.2.2) Bidentiseta. Characterized by heteronomous wings: hind wing not exceeds 112 of fore wing 2.2.1. Tridentiseta Kluge et al., 1995 length; in flight, anterior margin of hind wing coupled with posterior margin of fore This group corresponds in its content to: wing. This may be an autapomorphy or a re- - Pisciforma sensu Kluge et al., 1995: 105 sult of convergence (see below). Correspond- (non Pisciforma McCafferty, 1991); ingly, this taxon may be holophyletic or - Tridentiseta Kluge et al., 1995: 105. polyphyletic. Diagnosis. Larval maxilla with 3 (or fewer) Age: Jurassic - Recent. dentisetae (see discussion below). Euplectoptera are divided into (2.1) Pos- Probably a paraphyletic taxon, as one of teritorna and (2.2) Anteritorna. its groups (which one, is unknown) may be a sister group for Bidentiseta. 2.1. Posteritorna Kluge et al., 1995 'Tridentiseta are divided into Tetramero- tarsata Kluge, 1997 and a paraphyletic This group corresponds in its content to: group described as superfamily Siphlonuro- - Larves cryptobranches: Lestage, 19 17: 236; idea sensu Kluge et al., 1995. - Prosopistominae sensu Lameere, 1917: 74; - Prosopistomatoidea sensu Edmunds & 2.2.2. Bidentiseta Kluge, 1993 Traver, 1954b: 240; - Baetiscoidea sensu Peters & Hubbard, This group corresponds in its content to: 1989: 115; - Bidentiseta Kluge, 1993a: 41; Kluge et - Posteritorna: Kluge, 1992a: 10 (publica- al., 1995: 105. tion for temporary usage); Diagnosis. Larval maxilla with 2 (or fewer) - Posteritorna: Kluge, 1992b: 24 (publica- dentisetae (see discussion below). tion for educational usage); A holophyletic taxon. -- Posteritorna Kluge et al., 1995: 105. Bidentiseta are divided into (2.2.2.1) Bran- Diagnosis. Tornus of fore wing behind chitergaliae and (2.2.2.2) Furcatergaliae, apex of CUP(for the phylogenetic signifi- cance of 'this character see discussion below). 2.2.2.1. Branchitergaliae taxon nov. In larval maxilla, number of dentisetae in- definite, more than 3 (see discussion below). This group corresponds in its content to: In addition, a number of autapomorphies -- Setisura sensu Kluge, 1993a: 41; Kluge listed in discussion below. et al., 1995: 105 (non Setisura McCafferty, A holophyletic taxon. 1991). Posteritorna include Baetiscidae' (with a A holophyletic taxon. See apomorphies single genus Baelisca) and Prosopistomsti- discussed below. dae (with a single genus Prosopistoma). Branchitergaliae are divided into the group Eusetisura taxon nov. (which includes 2.2. Anteritorna Kluge, 1993 Isonychiidae sensu Landa, 1973, Coloburis- cidae sensu Landa, 1973 and Oligoneuriidae ?%is group corresponds in its content to: sensu Ednlunds & Traver, 1954b) and the - Larves nudibranches: Lestage, 1917: superfanlily Heptagenioidea sensu Kluge et 244; al., 1995 (which includes Pseudiron, Arthro- - Anteritorna: Kluge, 1992a: 10 (publica- plea and sensu Landa, 1969a. tion for temporary usage); - Anteritorna: Kluge, 1992b: 24 (publica- 2.2.2.2. Furcatergaliae taxon nov. tion for educational usage); - Anteritorna Kluge, 1993b: 35. This group corresponds in its content to: Diagnosis. Tornus of fore wing between - Furcatergalia sensu Kluge, 1993a: 41;. apices of veins CuA and CUP(about phylo- 1993b: 41 ; Kluge et al., 19b5: 105 (non Fur- genetic significance of this character see dis- catergalia Kluge, l 989). cussion below). Larval maxilla with number A holophyletic taxon. See apomorphies of dentisetae determined, not more than 3 discussed below. (see discussion below). Furcatergaliae are divided into Ephe- A hoiophyletic taxon. meroidea sensu Edmunds & Traver, 1954b, iOOSYST. ROSSICA Vol. 7 N.Ju.Mugz: ClarsiJication of Ephemeroptera

Figs ,l4.Wings of Posteritorna. 1-2, Buetisca rogersi Bern.; 3-4, Prosopistoma foliaceum Fourcr. (male). 1,3: fore wing; 2,4: its base.

Caenoidea sensu Edmunds & Traver, 1954b, as PCu); CuA and CUPrun nearly parallel to Ephemerelloidea sensu Koss, 1973 and Lep- each other, without branches or intercalaries tophlebiidae. between them (Figs 1, 3). In Anteritorna, tornus is situated betueen CuA and CUP, DISCUSSION these veins are strongly divergent, with branches of CuA or intercalaries between Posteritorna and Anteritorna them (only in Ametropodidae CUPand Ar terminate verv close to the tornus'l. 'There are different views on the homology In Posteritorna, tornus (the hind angle) of of veins of Baerisca @emoulin, 1969; Ed- the fore wing is situated distinctly behind rnunds & Traver, 1954a) and Prosopisloma Cup, usually behind A 1 (which is also known (Gillies, 1954, 1956). The homologization ac- 258 N.Ju. Huge: L'lassifico~iion oJ Ephemeroptera ZOOSYST. ROSSICA Vol. 7 cepted here is based on comparison of bases Prosopistoma were regarded as not related of concave and convex veins (Figs 1-4). and were placed in different taxa. Eaton The difference in position of tornus in Pos- (1 883- 1888) placed Baetisca in his "Series I" teritorna and Anteritorna is independent of of "Group 111" (together with Siphlonurus the size of hind wings, as Anteritorna in- and others) and placed Prosopisroma in "Se- clude species with hind wings well devel- ries 111" of "Group 11" (together with Caenis oped, or rudimentary, or completely absent. and Tricorythus). Demoulin (1958, 1961) In the cases when the hind wing is rudimen- placed Baetiscidae in Oligoneurioidea and tary or absent, the tomus of fore wing is Prosopistomatidae in Ephemerelloidea; later usually shifted proximally, becomes obtuse (Demoulin, 1969), he regarded Baetiscidae or is lost, but it never changes its position to be related with Oniscigastridae, and Pro- relatively to the terminations of the longitu- sopistomatidae with Ametropodidae. Tsher- dinal veins, being in Anteritorna always be- nova (1970, 1980) placed Baetiscidae in tween CuA and CUP.The difference in posi- Ephemerelloidea, and Prosopistomatidae in tion of tornus in Posteritorna and Anteri- Caenoidea. McCafferty (1991) placed Baeti- torna can be explained by independent ori- scidae in a separate superfamily Baetis- gin of these taxa from Permoplectoptera coidea, and Prosopistomatidae in Caenoidea which had homonomous wings without tor- (together with Caenidae and Ephemerelli- nus. In Posteritorna and Anteritorna, the dae). hind wings have been shortened inde- The monophyly of the Posteritorna, which pendently, and in consequence of this, their include Baetisca and Prosopistoma, can be fore wings got tornus independently twice, at proved by the following synapomorphies: two different places. (1) Tornus is behind CUP(Figs 1, 3) (see The division of all recent mayflies into discussion above). Posteritorna and Anteritorna suggested here (2) While wing venation of Baetzsca and corresponds to the classification by Lameere Prosopisroma is quite different (Figs 1, 3), (1917), who divided all recent mayflies into their vein bases are similar (Figs 2, 4): the two families, Prosopistomatidae (with tribes stem of MA+RS reduced, so RS MA, MPl Baetiscini and Prosopistomatini) and Ephe- and CuA arise from the same point. MP2 in- meridae (which had the same content as An- dependent from MPl and begins close to its teritorna). On the other hand, now it is clear base. CuA and MPl diverging more strongly that the systematic position of the Mesozoic than MPr and MA. CUPindependent from subfamily Hexagenitinae was determined by CuA and its base nearer to CuA than to A). L'ameere incorrectly: he used wrong homolo- In all other taxa of Ephemeroptera, combi- gization of their veins based on the incom- nations of characters are different. plete fossils and placed Hexagenitinae in his (3) All nerve ganglia of the thorax and ab- Prosopistomatidae. Later studies showed domen fused into a single synganglion situ- that Hexagenitidae have venation typical of ated in basisternurn of mesothorax Fig. 8) Anteritorna (Tshernova, 1961; etc.). and furcasternal protuberances of mesot- The here suggested contraposition of Pos- horax in imago contiguous, without median teritorna to all other recent mayflies is based impression between them (Figs 8, 9). In all on the single character (position of tornus), other Ephemeroptera, at least thoracic gan- but it does not contradict all other known glia are not fused together wigs 5-7); in the characters (see discussion below) and thus cases when metathoracic ganglion is more or seems to be true. less brought nearer to mesothoracic gan- glion, metathoracic ganglion is situated be- tween bases of subalar-sternal muscles Monophyly of Posteritorna (SA.Sm), so externally furcasternal protu- berances (FSp) (which contain bases of In some classifications, both families in- SA.Sm) are separated by median longitudi- cluded here in Posteritorna, Baetiscidae and nal furcasternal impression (FSi) (Figs 6, 7). Prosopistomatidae, were regarded as related (For description of thorax structure see and were united in the superfamily Baetis- Kluge, 1994a). coidea (= Prosopistomatoidea) (Edmunds & (4) Structure of larval thorax highly spe- Traver, 1954a, 1954b; Edmunds, 1962; Ed- cialized and unique. Pro- and mesonotum munds, Allen & Peters, 1963; Riek, 1973; completely fused together, strongly enlarged McCafferty & Edmunds, 1979; Kluge, 1989). (covering abdominal terga I-VII), with ven- But in other classifications, Baetisca and tral portions (named epipleura) and with ZOOSYST. ROSSICA Val. 7 N.Ju. Kluge: Class~ficotionof Ephemeroplera

Figs5-10. Pterothorax structure. 5, Potamanthus lureus (L.),ventral view of pterothorax (nerve system shown by in- terrupted line); 6, Leucorhoenanthus maximus (Joly), the same; 7, Caenis mucrtira Steph., the same; 8, Baetisca ro- gersi Bern., the same; 9, Prosopistoma foliaceum Fourcr., male, the same; 10, P.foliacewn, longitudinal section. FSi, furcasternal longitudinal impxtssion; FSp, furcasternal protuberance; SA.Sm, subalar-sternal muscle.

emargination on hind margin. Thoracic pair VI has the same structure as the pairs sterna have a pair of lateral longitudinal 111-V. Operculate tergaliae arose inde- ridges (Eaton, 1883-1888: P1. 43, 52). pendently in several other unrelated mayfly (5) Structure of tergaliae (for explanation groups: Oniscigastridae, Leptohyphinae, of this term see Kluge, 1989, 1996a) unique some Ephemerellidae, some Leptophlebii- and highly specialized, nearly identical in dae, but in these groups they have a differing Baerisca and Prosopistoma: pair I is the structure. longest, with straight outer margin and (6) Bases of hind pairs of tergaliae (espe- fringed inner margin; pair I1 operculate, cially of the pair VI) are turned anterome- quadrangular, prominent; pairs 111-V with dially; abdominal segment VI enlarged, its fringed margins; pair VI elongate, widened hind margin is elevated in its median part; a and rounded apically, not. fringed; pair VII pair of oblique dorsal ridges run from ante- absent (Lafon, 1953: P1. 11; Pescador & Pe- rior-lateral angles to this elevation (Pescador l ters, 1974: Figs 16, 20). This structure of ter- & Peters, 1974: Fig. 20). In addition to galiae has some similarity with that in Baetisca and Prosopistoma, such form of ab- Caenoidea (sensu Edmunds & Traver, dominal segment VI is found only in Co- 1954b) which also have operculate quadran- ryphorris of Tricorythidae (Peters, 1981). gular tergaliae of the pair 11, fringed margins (7) While structure of mouthparts in of tergaliae of the pairs 111-V, and reduced Baetisca and Prosopistoma is different. both pair VII; but in contrast to Posteritorna, in groups have a synapomorphy in the struc- Caenoidea the pair I is rudimentary and the ture of labium: lateral portions of submen- 260 N.Ju. Muge:e.Class~$cationof Ephrmeroptera ZOOSYST. KOSSICA Vo1.7 turn enlarged and turned forward. This char- dentisetae pressed against it (in Fig. 13 they acter is not unique and arose independently are shown artificially moved apart from each in several unrelated mayfly taxa. other). About common characters of Baelisca, In Anteritorna, the number of dentisetae is Prosopisloma and some other taxa, see dis- definite, and dentisetae differ distinctly from cussion below. other setae of the same medio-dorsal row. In 'Tridentiseta, the initial number of dentisetac Structure of larval maxillae in Ephemeroptera is three, usually the thickest dentiseta is the and division of Anteritorna into Tridentiseta most distal one. In Bidentiseta, the initial and Bidentiseta number of dentisetae is two, usually the thickest dentiseta is the proximal one. Both 'lie newly examined structure of the max- in Tridentiseta and in Bidentiseta, there are illae allows some relationships in Anteri- some specialized taxa which have the num- torna to be clarified. ber of dentisetae less than the initial one. The integral distal segment of the maxilla (which is usually regarded to be a result of ~~ctureof maxillae in various Tridentiseta fusion of galea and lacinia) has quite diverse form and structure in differently specialized In Siphlonuridae sensu Kluge et al., 1995 mayfly larvae, but nearly in all cases it has (Fig. 16), Dipteromimidae, Metretopodidae, the following common features. On its inner- Ametropodidae, Oniscigastridae (Kluge et apical (medio-apical) corner, the maxilla al., 1995: Fig. 39) and Tetramerotarsata bears a transverse row of immobile denticles, (Figs 14, 15; Kluge, 1997a: Fig. 3), three usually three in number, which can be dentisetae are present; among them, in named maxillary canines. Two rows of setae Ametropus the number of maxillary canines run from canines towards the base of max- is reduced to two, in others all three canines illa along its inner (median) margin: a are preserved. In some Tetramerotarsata, mrdio-dorsal and a medio-ventral row; be- namely in Cloeon sensu Kluge & Novikova, tween these rows a light (possibly weakly 1992 (Fig. 14) and Callibaelis, the dentisetae sclerotized) narrow area is situated 03gs 11- may be slender and only slightly thicker than 25). It is interesting to note that a similar the setae proxinlal to them. In Baeropus s. 1. structure have the maxillae of larvae and (including Raptobaeropus) which have thc imagoes of Odonata, while other usu- mouth apparatus specialized for predatory ally have a single median row of stout setae habits, the setae proximal to the dentisetae on their lacinia. In Ephemeroptera, the in- are absent. In some other Tetramerotarsata itial number of maxillary canines is three, (Baetis sensu Novikova & Kluge, 1987, this number is preserved in most of mayflies, Uoeodes, Afroplilum), the most distal den- and only in several taxa the number of ca- tiseta is extremely stout and can be pressed nines can be less than three: two, one, or ca- against the canines (Fig. 15). In the same nines can be absent; sometimes canines bear way the most distal dentiseta is modified in additional denticles. Nesameletidae (Kluge et al., 1995: Figs 47, Some setae in the medio-ventral and, espe- 48), but in contrast to Tetramerotarsata, the cially, in the medio-dorsal row may be thick- two other dentisetae are very weak and situ- ened and specialized. A term dentisetae is ated on a common plate. In Rallidens, all suggested for the distinctly thickened and three dentisetae are weak (Kluge et al., 1995: specialized setae of the medio-dorsal row Fig. 53). In Ameletidae, maxillae are highly (Kluge, 1994b, 1996b; Kluge et al., 1995). specialized for filtering, their canines are ab- In the most primitive state, the number of sent, arid only a single small dentiseta is pre- dentisetae is indefinite and the thickest den- sent (Kluge et al., 1995: Figs 20, 21). In tisefae are situated in the distal part of the Acanthametropodidae, maxillae are highly row. while the thinner ones in its proximal specialized for predatory habits, their den- part. Such structure is present in Baetisca tisetae are very stout and completely fused (Figs 11, 12): in the examined specimens of with the corpus of maxilla, thus they look Baefisca carolina, the number of dentisetae like canines; the number of canines and den- varies from 6 to 8. Prosopisloma has a highly tisetae is reduced (Kluge et al., 1995: Figs 23, specialized carnivorous mouth apparatus; 28). The maxillary structure of Ameletidae maxillae are highly specialized, with a single and Acanthametropodidae does not allow long acute canine and few very long acute reconstruction of the number of dentisetae /OOSYST. KOSSICA Vol. 7 a N.Ju Kluge: Classflcarion of Ephemeroptera 26 I

figs 11-16. Apex of left maxilla of Posteritorna and Tridentiseta. 11-12, Baetisca carolina Trav.; 13, Prosopistoma sp.; 14, Cloeon dipterum (L.); 15, Baetis vemur Curt.; 16, Siphlonumsaestivalis Etn. 11, 13, IS, dorsal view; 12, 14, 16, median view. Dentisetae shown by dots, setae of medio-ventral row shown by black. of their ancestors, but it is quite probable horseshoe-shaped row of five long, stout, that their ancestors had three dentisetae, as acute, mobile appendages (Kluge et al., other Tridentiseta. 1995: Figs 59, 60). If these appendages are The position of Ameletopsidae (which are dentisetae, their number is larger than in Tri- attributed to Siphlonuroidea sensu Kluge et dentiseta and Bidentiseta, that leads to con- al., 1995) is not clear. The larvae of all Ame- clusion that Ameletopsidae probably are not letopsidae are carnivorous with identical related to other Anteritorna and can be highly specialized structure of maxillae: ca- placed in a separate taxon. Such conclusion nines are absent, and apex of maxilla bears a is supported by the fact that Ameletopsidae 262 N.Ju. KiugetQassijication ofEphen~eroptera ZOOSYST. ROSSICA Vol. 7 are the only group in Euplectoptera in which dentisetae can be slender and poorly visible larvae have mobile tarsal segments, that is a among long dense setae of the medio-dorsal very archaic character. On the other hand, and the medio-ventral row. Often the most the five maxillary appendages of Ameletop- distal seta of the medio-ventral row is as sidae develop not as true setae (Kluge el al., stout as dentisetae, so it seems that there are 1995), so they cannot be dentisetae, but are three dentisetae, while only two true den- new formations. In this case, their structure tisetae (i.e. dentisetae of the medio-dorsal says nothing about relationships of Amele- row) are present (Figs 21, 23). In some cases topsidae, and this family may belong to Tri- it is very difficult to count dentisetae. In dentiseta. Rhithrogena s. str., both dentisetae are often pressed to one another and look like one Structure of maxillae in various dentiseta. In all Ecdyonurus sensu Kluge, Branchitergaliae 1988, the proximal dentiseta is bifurcate (Figs 21, 22); in the subgenera Ecdyonurus In each of the main phylogenetic branches and Afghanurus sensu Kluge, 1997b, the dis- of Branchitergaliae, two dentisetae are pre- tal dentiseta is simple (Fig. 21); in the sub- sent, at lest in the primitive groups. genera Notacanrhurus, Elecirogena and Among Eusetisura, in Isonychia and Oli- Cinygmina, the distal dentiseta is divided goneuriidae maxillae have only two canines; into several branches (Fig. 22). In Cinygma, canines of Coloburiscidae are secondarily both dentisetae are rudimentary, much serrate, so their number is unclear. In Isony- shorter than setae of medio-dorsal and chia s. str., the distal dentiseta is rudimen- medio-ventral row (Fig. 19). tary, very poorly visible (Fig. 17); in Isony- chia (Prionoides) georgiae McD., it is ab- Structure of maxillae in various sent. In Oligoneuriidae s. str., both den- tisetae are present; they are nearly as slender as setae proximal to them, but differ from Like in Branchitergaliae, in each of the these setae in the structure of their bases niain phylogenetic branches of Furcater- (Fig. 18). In Coloburiscidae, in contrast to gaiiae two dentisetae are present, at lest in all other Bidentiseta, the number of den- the primitive representatives. tisetae is variable: in the same species it can In Ephemeroidea sensu Edmunds & be two or three (specimens with two and Traver, 1954b, three canines and two den- three dentisetae are found among Adur- tisetae are retained in the most primitive phyella needhami Lest. and Coloburiscoides groups, but lost in some derived taxa. All sp.; in 8 examined specimens of Coloburiscus three canines and both dentisetae are devel- humeralis (Walk.), two dentisetae are found). oped in Polamanthidae (Fig. 24), Euthyplo- Probably such indefinite number of den- ciidae (here canines are well developed in tisetae arose in Coloburiscidae secondarily. Eurhyplocia, but rudimentary in Exeuthyplo- In all Heptagenioidea, two dentisetae are cia) and Ichthybotus. Among Ephemeridae present. In Pseudiron, maxillae are special- sensu nov. (i. e. including Hexagenia and ex- ized for predatory habits, with unusually cluding Ichthybotus and Pentagenia), all large proximal dentiseta and with two ca- three canines and both dentisetae are well nines only, so the distal dentiseta looks like a developed in Ephemera, but the distal den- third canine (Fig. 20). In Arthropl~a,the tiseta is vestigial and only two canines are apex of the maxilla bears a single canine; in present in Hexageniinae (Hexagenia limbata Arlhropleu bipunctata McD., two dentisetae Guern. and Eatonigenia chiae Dang exam- are distinctly larger than other setae of the ined). Among Behningiidae, in Pro- medio-dorsal row, but in A. congener Bgtn. tobehningia two canines are present and den- dentisetae are indistinguishable among setae tisetae are absent (Elpers & Tomka, 1994: of this row. In most of the Heptageniidae Fig. 2); in Behningia and Dolania only one sensu Landa, 1969a, maxillae have three canine and only one dentiseta are present slender weak canines (except for Epeorus Glpers & Tomka, 1994: Fig. 15b). In Palin- sensu Edmunds, Jensen & Berner, 1976 geniidae sensu McCafferty & Edmunds, which has three canines strongly enlarged 1976 (both in Pentagenia and Palingeniinae), arid stout, and Cinygma which has a single the maxilla has only one canine and only one slender canine - Fig. 19). All examined Hep- dentiseta. Among Polymitarcyidae, all three tageniidae have two dentisetae, but their canines and two dentisetae are retained in ZOOSYST. ROSSICA Vol. 7 N.Ju. Kluge: Class~j?cationof Ephemeroptera 263

Figs 17-26. Apex of maxilla of 13identiseta. 17, Isonychia ussunca Bajk., left maxilla, dorsal view; 18, Oligoneun'ella paNida [Hag.), the same; 19, Cinygma lynyormir McD., left maxilla, median view; 20, Pseudiron meridionalis Trav., left maxilla, dorsal view; 21, Ecdyonurus sp. n. (gr. venosus), left maxilla, median view; 22, E. abracadabrur Kluge, dentisetae separately, dorsal view; 23, Heptagenia (Kageronia)fuscogrisea (Retz.), left maxilla, dorsal view; 24, Po- tamanthus luteus @.), left maxilla, median view; 25, Leptophlebia marginata (L.),right maxilla, ventral view; 26, Choroterpes (Euthraulus) sumbarensis Kluge, the same. Dentisetae are shown by dots, setae of medio-ventral row are shown by black; dl, d2, distal and proximal dentisetae. 264 N.Ju. h7uge:Classijic ,ation ofEphemeroptera ZOOSYST. ROSSICA Vol. 7 the primitive genus Ephoron; in Campsurus, (3) Eggs have anchors (Fig. 31) each of both dentisetae are retained, but there are which consists of a long cable twisted into a only two canines; in Povilla, all three canines small cylindrical coil and a cap at the end of are retained, but dentisetae are completely the cable; in twisted condition of the anchor, lost. this cap covers the coil apically. Such an- In all Caenoidea sensu Edmunds & Trav- chors are found on eggs of various species of er, 1954b, all three canines and both denti- Heptageniidae, Arlhroplea, Isonychia, Colo- setae are developed. buriscidae. On eggs of Oligoneuriidae s. str., The same is true for most of Ephemerel- the anchors are also present, but they are ru- loidea sensu Koss, 1973, except for some dimentary, very short, mushroom-like, and highly specialized groups. Particularly, in not coiled (Fig. 30). In other Ephemerop- Uracanthella and Cincticostella which have tera, anchors, when present, have a differing specialized filtering maxillae, canines are lost structure. (but both dentisetae are retained). In Dicer- (4) In imago and subimago, the posterior comyzon, maxillae are highly specialized, arms of the prealar bridge of mesothorax scraping, with a single vestigial dentiseta. In (for explanation of this term, see Kluge, Tricorylhus, maxillae are so highly special- 1994) are shortened and do not reach the lat- ized, that they have lost all canines, den- eral margins of scutum (Figs 28, 29; com- tisetae, medio-dorsal and rnedio-ventral pare with Fig. 27). rows of setae. In the most primitive group of the Lepto- Holophyly of Furcatergaliae phlebiidae, i. e. Leptophlebiinae sensu Klu- ge, 1994b, maxillae bear slender rudiments The taxon Furcatergaliae has the follow- of three canines and two dentisetae (Fig. 25; ing apomorphies: Kluge, 1994: Fig. 7). In Habrophlebiinae (1) In imagoes and subimagoes, first tarsal and Atalophlebiinae, canines are lost (Klu- segment (which like in majority of other ge, 1994b: Figs 8, 9); in Atalophlebiinae, the Ephemeroptera is immovably fused with distal dentiseta is also lost (Fig. 26); in some tibia) is strongly shortened. Only in some Atalophlebiinae (Traverella and others), all specialized groups of Furcatergaliae, where dentisetae are lost. legs are non-functional (in Behningiidae, Po- The foregoing account shows that the lymitarcyidae, Palingeniidae), or all tarsal number of dentisetae is very conservative, segments are strongly shortened (in Caenis), and their reduction takes place only in rare the first tarsal segment can be relatively cases. long, that is probably a secondary elonga- tion. Holophyly of Branchitergaliae (2) In the hind wings (if they are present), MA is not forked. This apomorphy is not unique: independently from Furcatergaliae, Branchitergaliae have the following apo- loss of MA fork occurs in some other mayfly morphies: taxa (particularly, fork of MA is absent in (1) Tergaliae have an additional ventral both species of Arrhroplea and in Cinygma (hind) fibrillose portion. Only in few repre- dimicki McD., but is present in two other sentatives (in Arlhroplea, in some species of species of Cinygma). Cinygmula, etc.), this portion is secondarily (3) According to the investigation by lost. This apomorphy in not unique: in addi- Landa (1969), visceral tracheae in all Fur- tion to Branchitergaliae, such a fibrillose catergaliae are lost in the abdominal seg- portion is present in RaNidens and some ment 11, being developed only in the seg- Ameletopsidae (Chiloporrer and Mirawara). ments 111-VIII or IV-VIII, while in other (2) Maxillae with a ventral row of setae mayflies visceral tracheae are developed in parallel to the inner margin. This row is de- all segments 11-VIII. But actually the posi- veloped in Isonychia Fig. 17), Arthroplea, tion and number of visceral tracheae is un- and Heptageniidae (only in Ecdyonurus der individual variability, so future investi- sensu Kluge, 1988, it is transformed into an gations are necessary to clarify whether this irregular field of setae - see Kluge, 1988, apomorphy is reliable. 1993a). In Oligoneuriidae s. str., this row is In my previous paper (Kluge, 1989), it was indistinct and turned laterally; in Coloburis- stated that, in contrast to Costatergalia (a cidae and Pseudiron, it is absent. paraphyletic taxon which is now divided into

Figs 27-31. Details of structure of Branchitergaliae in comparison with Siphlonum. 27, Siphlonumaestivalis Etn., lateral view ofpterothorax; 28, Isonychiaignota Walk., the same; 29, Oligoneuriella sp., the same; 30, vestigial an- chor on egg surface of Oligoneuriella sp.; 31, anchors typical of Branchitergaliae. a, posterior arm of prelllar bridge; b, joining of posterior arm of prealar bridge with scutum; c, secondary dorso-posterior arm of prealar bridge.

Tridentiseta and Branchitergaliae), Fur- these are not apomorphies of Furcatergaliae catergalia (a polyphyletic taxon which is as a whole. Short rudiments of the tergalial now divided into Posteritorna and Furcater- ribs are present in some Ephemeridae and galiae) have apomorphies in the structure of Behningiidae; weak ribs are visible on ter- larval tergaliae (loss of the tergalial ribs) and galiae of some Tricorythidae. Ephemeridae, larval caudal fdaments (loss of the primary Palingeniidae and Behningiidae have pri- swimming hairs). But now I have found out mary swimming hairs (the hairs on the inner that in some representatives of Furcater- margins of cerci and the lateral margins of galiae these apomorphies are absent, so paracercus) which differ in their structure 266 N.Ju. Kluge:Clarsr$c :ation ofEphemeroptera ZOOSYST. ROSSICA Vo1.7 from secondary swimming hairs on the lat- McCafferty & Edmunds (1979) placed eral margins of cerci. Other Furcatergaliae Baetiscidae and Prosopistomatidae in the have no swimming hairs, or have only secon- suborder Pannota based on the structure of dary swimming hairs on both margins of larval mesonotum which is fused with the cerci and paracercus. median margins of fore wing buds. But such a fusion occurs independently from Pannota Systematic position of Buetisca in Oligineuriidae, Coloburiscidae, and the and Prosopbtoma genus Pseudopannola (Baetidae), so this character is not sufficient to prove a rela- tionship between Baetiscoidea and the rest Here Baetisca and Prosopisroma are of Pannota. placed in a separate taxon Posteritorna In contrast to other taxa included in Pan- which is opposed to all other recent mayflies. nota (Caenoidea sensu Edmunds & Traver, This contradicts the former classifications, 1954b and Ephemerelloidea sensu Koss, where Baetiscidae and Prosopistomatidae 1973), Posteritorna retained the primary were united with Caenoidea and Ephemerel- swimming setae on the caudal filaments of loidea into the taxon Pannota (McCafferty the larva: both in Baetisca and Prosopis- & Edmunds, 1979; McCafferty, 1991) or roma, the setae on the median sides of cerci were united with Caenoidea, Ephemerel- and lateral sides of paracercus (the primary loidea, Ephemeroidea and Leptophlebioidea ones) differ in their structure from the setae into the taxon Furcatergalia (Kluge, 1989). on the lateral sides of cerci (the secondary Actually, Baerisca and Prosopistoma have no ones). apomorphies which are present in Furcater- Landa (1969) described a similarity in the galiae: structure of larval Malpighian tubes between (1) In contrast to Furcatergaliae which Baerisca and Neoephemeridae, and between have initially 2 maxillary dentisetae, Baetisca have a primitive structure of maxillae with Prosopistoma and Caenidae. Landa's classi- fication of types of Malpighian tubes is indefinite number of dentisetae (Figs 11, 12). In highly specialized maxillae of Prosopis- based on the number of trunks and presence of branches of these trunks. According to his roma, the number of dentisetae is also more than two (Fig. 13). investigations, various Neoephemeridae and (2) In contrast to Furcatergaliae, the first Baetisca have the type Fba - 2 trunks, each tarsal segments of imago in Baetisca are not with 3 non-branched processes; Caenidae shortened (they are longer than the next and Prosopisroma have the type Fbcx - 2 ones). Imaginal legs of Prosopistoma are non-branched trunks; Potamanthidae, Ephe- non-functional, and their tarsal joints are in- meridae and Polymitarcyidae have the type distinct. Ea - 6 non-branched trunks; Behningiidae (3) In imagoes of Baetisca and Prosopis- have the type B - 8 low buds; and so on. Ac- roma, the ventral surface of mesothoracic tually, the number of trunks and their episternum is completely divided by the branches is strongly variable, it may differ in paracoxal suture into anepisternum and specimens of the same species and in the left katepisternum (Figs 8-9), while in Furcater- and right halves of the same specimen. Most galiae the paracoxal suture usually termi- constant are the longest trunks, while short nates more laterally (Figs 5-7). trunks and short branches can easily arise (4) In contrast to Furcatergaliae, larval and disappear, varying individually. So, it is visceral tracheae of Baerisca and Prosopis- impossible to compare total numbers of toma are developed in all abdominal seg- trunks and branches in different taxa, it is ments 11-VIII (according to Landa, 1969). possible only to compare position of the Other characters of Furcatergaliae (non- longest trunks. Larvae of Baetisca, Prosopis- forked MA of hind wing, reduction of ribs of toma, Neoephemeridae, Caenidae, Ephe- larval tergaliae, development of secondary meridae, Potamanthidae, Behningiidaeand setae on lateral margins of larval cerci) are Isonychia examined by me have 2 long lat- present in Baetisca and Prosopistoma, but eral trunks directed anteriorly (Figs 32-34). these characters are present also in some These long trunks can bear at .their anterior taxa of Tridentiseta and Branchitergaliae, so ends a pair of peculiar straight Malpighian they do not prove relationship of Posteri- tubes which are partly fused with their ducts torna and Furcatergaliae. (Fig. 33); an identical pair of peculiar Mal- ZOOSYST. ROSSICA Vol. 7 . N.Ju. Huge: Classijication oJEpherneroptera

Figs 32-34. Trunks of Malpighian tubes, ventral view (most of Malpighian tubes detached). 34, Ephemera danica Moll.; 35, Leucorhoenanthus maximus (Joly) (Neoephemeridae); 36, Baetisca carolina Trav. AMT, apical Malpighian tube; MT, Malpighian tube.

pighian tubes directed anteriorly is found of ventro-lateral and a pair of dorso-lateral also in some mayflies which have no trunks: trunks) and indefinite number of additional Baetis (Landa, 1968: Fig. 12 BR), Ephe- short trunks or buds (Kluge, 1993: Figs 1- merella, Tricorythodes. So, the lateral paired 19). Thus only three main types of Mal- position of Malpighian tubes is common to pighian tubes are found in Epherneroptera: many groups of Ephemeroptera. Another absence of long trunks, one and two pairs of structure of trunks of Malpighian tubes is long trunks directed anteriorly. As Baetisca, found in all examined Heptageniidae: there Prosopisroma, Neoephemeridae and Caeni- are 4 long trunks directed anteriorly (a pair dae have a widely distributed type of Mal- :ation of Ephemeroptera . ZOOSYST. ROSSICA Vol. 7 pighian tubes (with two long trunks), struc- Acknowledgements ture of their Malpighian tubes does not al- low discussion on their relationships. The author expresses his sincere thanks to Dr. S.K. Burian, Dr. J.W. Early, Dr. M.T. Gillies, Dr. T. Gonser, Dr. W.P. McCafferty, Dr. W.L. Peters, Dr. Status of Rectracheata McCafferty, 1991 T. Soldan, Dr. A.H. Staniczek, Dr. D. Studemann, Dr. I. Tomka, who provided him with the necessary McCafferty (1 99 1) established the subor- material on exotic mayfly species. der Rectracheata McCafferty, 1991 which united the taxon Furcatergalia Kluge, 1989 References and the family Oniscigastridae (for which he Demoilin, G. 1958. Nouveau schema de classifica- established a separate infraorder Vetulata tion des Archodonates et des Ephemeropteres. McCafferty, 199 1). The only character Bull. Inst. roy. Sci. nut. Belg., 34(27): 1-19. which allowed the bringing together Vetu- Demoulin, G. 1969. Remarques critiques sur la posi- lata and Furcatergalia was the presence of tion systematique des Baetiscidae et des Prosopis- tracheal anastomoses in the abdominal seg- tomatidae (Epherneroptera). Bull. Inst. roy. Sci. nat. Belg., 45(17): 1-8. ments IV-VII (Landa, 1969); in all other re- Eaton, A.E. 1883-1888. A revisional monograph of spects, Vetulata have nothing in common recent Ephemeridae or mayflies. Trans. Linn. Soc. with Furcatergalia. In my opinion, this char- Lond., (2) 3: 352 p., 65 pl. acter is not sufficient to prove relationship Edmunds, G.F., Jr. 1962. The principles applied in of these taxa, because it can arise inde- determining the hierarchic level of the higher pendently. For example, in Chiloporter well categories of Ephemeroptera. Syst. Zool., ll(1): developed anastomoses in abdominal seg- 22-31. Edmunds, G.F., Jr., Men, R.K. & Peters, W.P. ments 111-VIII are present, while in other 1963. An annotated key to the nymphs of the Ameletopsidae tracheal anastomoses in the families and subfamilies of mayflies (Ephemerop- segments 111-VII are absent (Landa, 1969). tera). Univ. Utah, biol. Ser., 13(1): 1-49. On this base Landa (1973) established for Edmunds F.F., Jr., Jensen S.L. & Berner L. 1976. Chiloporter a separate family Chiloporteri- The majiflies of North and Central America. 330 p. dae. Rut relationship between Chiloporter Univ. of Minnesota Press, Minneapolis. Edmunds, G.F., Jr. & Traver, J.R. 1954a. The flight and other Ameletopsidae is evident, all of mechanics and evolution of the wings of Ephe- them have identical and quite unusual struc- meroptera, with notes on the archetype ture of mouth apparatus (see Kluge et al., wing. J. Wash. Acad. Sci., 44: 390-400. 1995); because of this, other authors (includ- Edmunds, G.F., Jr. & Traver, J.R. 1954b. An out- ing McCafferty, 1991) do not accept this line of a reclassification of the Ephemeroptera. family. According to Landa's description, Proc. entomol. SOC.Wash., 56: 236-240. Elpers, C. & Tomka, I. 1994. Mouthparts of preda- the tracheal anastomoses of the abdominal ceous larvae of the Behningiidae (Insecta: Ephe- segments I1 and I11 can be present or absent meroptera). Arch. Hydrobiol. Suppl., 99(4): 38 1- in some closely related taxa of Leptophlebii- 413. dae, Ephernerellidae and Tricorythidae; tra- Gillies, M.T. 1954. The adult stage of Prosopistoma cheal anastomoses of the abdominal seg- Latreille (Ephemeroptera), with description of ments VIII-IX are also strongly variable. It two new species from Africa. Trans. Toy. Soc. means that during mayfly evolution tracheal Lond., 105: 355-372. Gillies, M.T. 1956. A supplementary note on anastomoses can easily originate in the Prosopistoma Latreille (Epherneroptera). Proc. same abdominal segments independently roy. entomol. Soc. Lond., 31: 165- 166. in different lineages, so their presence is Kluge, N.Ju. 1988. Revision of genera of the family not sufficient to establish a taxon of high Heptageniidae (Ephemeroptera). I. Diagnoses of rank. tribes, genera and subgenera of the subfamily The larvae of Vetulata have three well de- Heptageniinae. Entomol. Obozr., 67(2): 291 -31 3. (In Russian). veloped maxillary dentisetae. It means that Kluge, N.Ju. 1989. The problem of the homology of Vetulata could not derive from a common the tracheal gills and paranotal processi of the ancestor with Furcatergaliae separately from mayfly larvae and wings of the insects with refer- Branchitergaliae, as both Furcatergaliae and ence to the and phylogeny of the order Branchitergaliae (and most probably their Ephemeroptera. Chteniya pamyati N.A. M~ol- common ancestor as well) have only two odkovskogo [Lectures in Memoriam of N.A. Kholodkovsky], 1988: 48-77. (In Russian). dentisetae. It leads to conclusion, that Kec- Kluge, N.Ju. 1992a. Phylogeny and higher classifica- tracheata is a polyphyletic taxon. tion of Ephemeroptera. Ulth International Con- ZOOSYST. ROSSICA Vol. 7 N.Ju. Kluge: Classi>c ference on Ephemeroptera, August 3-6, 1992, Lafon, J. 1953. Note sur Prosopistoma foliaceum Orono, Maine, USA. Program and Abstracts: 10. Fourcr. (Ephemeroptera). Bull. Soc. zoo!. France, pot properly published in nomenclatural sense]. 77(5/6): 425-436. Kluge, N.Ju. 1992b. Nasekomye-podenki (otryad Lameere, A. 1917. Etude sur l'evolution des Ephe- Ephemerop tera). Chart ' I [Insects-mayflies (order mires. Bull. Soc. zool. France, 42: 41-81. Ephemeroptera). Part I 1. 35 p. St.Petersburg, Landa, V. 1969a. Jepice - Ephemeroptera. Fauna St.Petersburg State University. (In Russian). [Not ~SSR,18. 350 p. Praha. properly published in nomenclatural sense]. Landa, V. 1969b. Comparative anatomy of mayfly Kluge, N.Ju. 1993a. Revision of genera of the family larvae (Epherneroptera). Acta entomol. bohemosl., Heptageniidae (Ephemeroptera). 11. Phylogeny. 66: 289-31 6. Entomol. Obozr., 72(1): 39-54. (In Russian). Landa, V. 1973. A contribution to the evolution of Kluge, N.Ju. 1993b. New data on mayflies (Ephe- the order Ephemeroptera based on comparative meroptera) from fossil Mesozoic and Cenozoic anatomy. In: Peters, W.L. & J.G. (eds). Proc. 1st resins. Palaeontol. J., 27(1A): 35-49. Int. Conf. Ephemeroptera, USA, Florida, 1970: Kluge, N.Ju. 1994a. Pterothorax structure of may- 155- 159. Leiden, Brill. flies (Ephemeroptera) and its use in systematics. Lestage, J.A. 1917. Contribution a I'etude des larves Bull. Soc. entomol. France, 99(1): 41 -61. des Ephemeres palearctiques (ser. I). Ann. Biol. Kluge, N.Ju. 1994b. Habrophlebiinae subfam. n. Lacust., 8: 2 12-458. with description of new species of Habroleptoides MeCafferty, W.P. 1991. Toward a phylogenetic from Caucasus (Ephemeroptera: Leptophlebii- classification of the Ephemeroptera (Insecta): a dae). Zoosyst. ross., 3(1): 35-43. commentary on systematics. Ann. entomol. Soc. Kluge, N.Ju. 1996a. A new suborder of Thysanura Amer., 84(4): 343-360. for the Carboniferous insect initially described as McCafferty, W.P. & Edmunds, G.F., Jr. 1976. Re- larva of Bojophlebia, with comments on charac- definition of the family Palingeniidae and its im- ters of the orders Thysanura and Ephemeroptera. plication for higher classification of Ephemerop- Zoosyst. ross. 4(1) (1 995): 71-75. tera. Ann. entomol. Soc. Amer., 69(3): 486-490. Kluge, N.Ju. 1996b. The Palaearctic Metretopodi- MeCafferty, W.P. & Edmunds, G.F., Jr. 1979. The dae, with description of a new genus and species higher classification of the Ephemeroptera and its from Siberia (Ephemeroptera). Zoosyst. ross., evolutionary basis. Ann. entomol. Soc. Amer., 4(1), (1995): 76-80. 72(1): 5-12. Kluge, N.Ju. 1997a. Classification and phylogeny of Novikova, E.A. & Kluge, N.Ju. 1987. Systematics of the Baetidae (Ephemeroptera) with description of the genus Baetis (Ephemeroptera, Baetidae), with the new species from the Upper Cretaceous resins description of new species from Middle Asia. of Taimyr. Ephemeroptera & Plecoptera. Biology- Vestnik Zoologii, 1987(4): 8-19. (In Russian). Ecology-Systematics (Proc. VIII Int. ConJ on Peseador, M.L. & Peters, W.L. 1974. The life his- Ephemeroptera and XI1 Int. Symposium on Ple- tory and ecology of Baetisca rogersi Berner coptera, August 1995, Losanne). Mauron+Tin- (Ephemeroptera: Baetiscidae). Bull. Florida St. gue1.y & Lacht SA: 527-535. FribourgISwitzer- Mus., biol. Sci., 17(3): 151-209. land. Peters, W.L. 1981. Coryphorus aquilis, a new genus Kluge, N.Ju. 1997b. Order mayflies, Ephemerop- and species of Tricorythidae from the Amazon tera In: Tsalolikhin, S.Ja. (ed.). Opredelitel'pres- basin (Epherneroptera). Aquatic Insects, 3(4): novodnykh bespozvonochnykh Rossii i sopredel'- 209-217. nykh stran [Key to freshwater invertebrates of Peters, W.L. & Hubbard, M.D. 1989. Names and Russia and adjacent lands], 3: 176-220. %.Peters- authorship of two family-groups in the Ephe- burg. (In Russian). meroptera. J. New York entomol. Soc., 97(1): 1 15. Kluge, N.Ju. & Novikova, E.A. 1992. Revision of the Riek, E.F. 1973. The classification of the Ephe- Palaearctic genera and subgenera of mayflies of meroptera. In: Peters, W.L. & J.G. (eds). Proc. the subfamily Cloeoninae (Ephemeroptera, Baeti- 1st Int. ConJ Ephemeroptera. USA. Florida, 1970: dae) with description of new species from the 160-179. Leiden, Brill. USSR. Entomol. Obozr., 71(1): 38-55. (In Rus- Tshernova, O.A. 1961. On taxonomic position and sian). (Engl. translation in Entomol. Rev., 71(9): geological age of the genus Ephemeropsis Eich- 29-54). wald (Ephemeroptera, Hexagenetidae). Entomol. Kluge, N.Ju., Studernarm, D., Landolt P. & Gonssr Obozr., 40(4): 858-869. (In Russian). T. 1995. A reclassification of Siphlonuroidea Tshernova, O.A. 1970. On the classification of the (Ephemeroptera). Bull. Soc. entomol. Suisse, 68: fossil and recent Ephemeroptera. Entomol. 103-132. Obozr., 49(1): 124- 145. (In Russian). Koss, R.W. 1973. The significance of egg stage to Tshernova, O.A. 1980. Order Ephemerida Latreille, taxonomic and phylogenetic studies of the Ephe- 1810. In: Istoricheskoe razvitie klassa nasek- meroptera. In: Peters, W.L. & J.G. (eds). Proc. omykh [Historical developn~entof the class of in- 1st Int. Conf. Ephemeroptera, USA, Florida, 1970: sects]. Trudy paleontol. Inst. Akad. Nauk SSSR, 73-78. Leiden, Brill. 175: 3 1-36. (In Russian). Received 20 January 1998