Suprageneric Classification of Collembola Entomobryomorpha

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1 SYSTEMATICS Suprageneric Classification of Collembola Entomobryomorpha FELIPE N. SOTO-ADAMES, 1 JEAN-AUGUSTE BARRA, 2 KENNETH CHRISTIANSEN, 3 AND RAFAEL JORDANA 4 Ann. Entomol. Soc. Am. 101(3): 501Ð513 (2008) ABSTRACT The suprageneric classiþcation of the order Entomobryomorpha (families Isotomidae, Tomoceridae, Oncopoduridae, Actaletidae, Coenaletidae, Paronellidae, Entomobryidae, Microfalculidae, Oncobryidae, and Praentomobryidae) is examined and revised. The families are placed in four superfamilies: Isotomoidea; Coenaletoidea, new status; Tomoceroidea; and Entomobryoidea. One new subfamily, Capbryinae, and two new tribes, Nothobryini and Bessionellini, are proposed. Entomobryoidea is examined in more detail at the level of subfamilies and tribes. The characteristics used for this classiþcation are discussed and a scheme is presented. The rationale for the divisions used is discussed. KEY WORDS Collembola, Entomobryomorpha, classiþcation, Coenaletoidea, new superfamily All taxa above the species level are to a large degree arbitrary. The points at which taxa are considered separate are arbitrary, even when involving cladistic analysis based on both morphological and molecular data. In addition, once we consider taxa above the species levels, this kind of combined data are rarely available. Thus, tribes, subfamilies, and families become largely a matter of opinion and popularity, Þrst with taxonomists in the Þeld and eventually with writers of textbooks and people who use specimens of the groups involved. As a result, different people may treat the same taxon as a subgenus, genus, tribe, subfamily, or family at the same time. This arbitrariness has recently led to the development of the Phylocode (Cantino and de Queiroz 2006), which seeks to abolish all existing supraspeciþc Linnaean categories and substitutes them for names attached to clades. Although the aim seems worthwhile, the proposed code is so complex, confusing and Þlled with problems, that widespread adoption remains questionable (Nixon and Carpenter 2000, Nixon et al. 2003). Thus we feel it is important to attempt some clariþcation in the context of the presently ßawed, but ever evolving, Linnaean system. Rationale for creating a new suprageneric taxon can be a matter of opinion only. However, we believe that producing a new suprageneric taxon for a particular genus or, more rarely, group of genera can be useful if including the genus in an extant taxon so broadens the diagnosis of this taxon as to make it difþcult to use or to group genera. It is, 1 Corresponding author: Illinois Natural History Survey, 1816 S. Oak St., Champaign, IL ( fsoto@uiuc.edu). 2 Université Louis Pasteur, Laboratoire de Zoologie, F Strasbourg, France. 3 Department of Biology, Grinnell College, Grinnell IA, Department of Zoology and Ecology, University of Navarra, P.O. Box 177, Pamplona, Spain. of course, always hoped that the new taxon would constitute a monophyletic group, but that is most often merely a hope and not backed by solid evidence. Evidence for monophyly can be afforded by morphological data from extant taxa and fossils, or molecular sequence data analysis. However, the former is not readily available for Collembola and the latter all too scarce. It is thus with some trepidation that anyone should go about creating new suprageneric categories in Collembola. We have examined the relationships among the possible members of the Entomobryomorpha Collembola in the hope of establishing a more stable suprageneric classiþcation for the Entomobryoidea that is currently available. The results of this work are presented below. History of Classification of Entomobryomorpha Tömösvary (1886) created the family Entomobryidae (actually Degeeridae) to encompass genera including Tomocerus, Lepidocyrtus, Seira, Orchesella, Degeeria (later Entomobrya), and Isotoma. Schäffer (1896) divided the family in three subfamilies: Entomobryinae, Tomocerinae, and Isotominae. Börner (1913) elevated each subfamily to family and classiþed Entomobryidae into subfamilies Entomobryinae, Paronellinae, and Cyphoderinae. Börner (1913) further divided the Entomobryinae into tribes Orchesellini and Entomobryini. This classiþcation was widely followed for many years although BörnerÕs subfamilies were often treated as families and his tribes as subfamilies. Subsequently, this suprageneric classiþcation was widely accepted, except for most workers treating tomocerids as a subfamily of Entomobryidae. Yosii (1961) dealt with the phylogenetic signiþcance of chaetotaxy in Collembola and treated the /08/0501Ð0513$04.00/ Entomological Society of America

2 502 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 subfamily Cyphoderinae as a family, while retaining in Entomobryidae subfamilies Orchesellinae, Entomobryinae, Paronellinae, and the newly created Seirinae. Seirinae was created to accommodate scaled species with accessory setae around the botriothrica and short, bidentate or falcate mucrones. The analysis of Cassagnau (1971) of Collembola on the basis of the neuroendocrine system considered Entomobryomorpha to be one of three monophyletic lineages deriving directly from Protocollembola, having Rhyniella as its basal genus. His grouping of the members of Entomobryomorpha differs from YoshiÕs Entomobryoidea only in the placement of Microfalculinae and Cyphoderinae, neither of whose neuroendocrine systems he examined. In his epic work on entomobryid chaetotaxy, Szeptycki (1979) raised Paronellinae and Microfalculinae to families and divided Seirinae into Seirinae and Lepidocyrtinae. Yoshi and Suhardjono (1989) demoted Seirinae and Lepidocyrtinae to tribes and created a new tribe: Willowsini. They divided Seirinae into two groups: Seira group (species with falcate mucrones, i.e., Seira s.l.?) and Lepidosira group (mucrones bidentate), with Lepidosira, Epimetrura, Lepidocyrtoides, and Acanthocyrtus. Hopkin (1997) considered the superfamily Entomobryoidea ( Entomobryomorpha) to include families Actaletidae, Coenaletidae, Cyphoderidae, Entomobryidae (with subfamilies Entomobryinae and Orchesellinae), Isotomidae, Microfalculidae, Oncopoduridae, and Tomoceridae. Deharveng (2004) considered Entomobryoidea as encompassing Cyphoderidae, Microfalculidae, Paronellidae, and Entomobryidae, with families Actaletidae and Coenaletidae incerta sedis. Deharveng also accepted the division of Entomobryidae into subfamilies Entomobryinae, Lepidocyrtinae, Orchesellinae, and Seirinae, whereas including Tomoceridae and Oncopoduridae in superfamily Tomoceroidea. In none of the works, after Börner, is there a complete listing of the genera belonging to each of these suprageneric categories. Only Mari Mutt (1980), in his treatment of the tribal classiþcation of Orchesellinae, assigned genera to each tribe. Different authors have used these different suprageneric categories differently but Paronellidae, Cyphoderidae, Orchesellidae(inae), Entomobryinae, and Entomobryidae, variously deþned, have been widely used. Many authors have distinguished between Entomobryidae s.l. (i.e., sensu Börner 1913) and s.s. (i.e., sensu Yosii 1961 and Szeptycki 1979). The subfamilies or tribes Seirinae and Willowsini have not become widely used, except by Yosii, although Lepidocyrtini, as encompassing all the scaled Entomobryinae, has been often used. The classiþcation scheme we propose is shown in Table 1. This scheme is very similar to that presented by Deharveng (2004). The major differences are that Cyphoderidae is subsumed in Paronellidae as a subfamily; the status of Lepidocyrtinae and Seirinae is changed to tribes; and the tribe Willowsini is added. Actaletidae is placed in Isotomoidea and a new status Table 1. a Extinct family. Classification of Entomobryomorpha Entomobryomorpha Superfamily Family Subfamily Tribe Isotomoidea Isotomidae Actaletidae Coenaletoidea new status Coenaletidae Tomoceroidea Tomoceridae Tomocerinae Lepidophorellinae Oncopoduridae Entombryoidea Paronellidae Paronellinae Bromachanthini Cremastocephalini Callyntrurini Paronellini Troglopedetini Cyphoderinae Entomobryidae Capbryinae new subfamily Orchesellinae Bessionellini new tribe Corynothricini Heteromurini Mastigocerini Nothobryini new tribe Orchesellini Entomobryinae Entomobryini Lepidocyrtini Seirini Willowsini Microfalculidae Oncobryidae a Praentomobryidae a is established for Coenaletidae. The characteristics we have considered most important in separating the superfamilies and families of this order are shown in Table 2. Justification of Superfamilies for Extant Genera Entomobryoidea Extant members of this superfamily are united by the presence of a trochanteral organ composed of three or more setae (usually 15 or more). A similar organ is found in many Tomoceridae, but here it almost always consists of a single seta and/or is also found on the base of the femur. Members of Entomobryoidea are also united by the presence of a postocular botriothricum. They are the only Entomobryomorpha having papillate male genital plates in some (although not all) members of all families, and they are the only Entomobryomorpha having type 1 and 2 setae (Christiansen 1958), although again not all genera have these. With the exception of Corynothrix of the subfamily Orchesellinae, all have the fourth abdominal segment distinctly longer than the third

3 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 503 Table 2. Superfamily and family characteristics of Entomobryomorpha Characteristic Entomobryiomorpha Isotomoidea Coenaletoidea Tomoceroidea Entomobryoidea Tomoceridae Isotomidae Actaletidae Coenaletidae Oncopoduridae Praentomobryidae Oncobryidae a Microfalculidae Paronellidae Entomobryidae Tomocerinae Lepidophorellinae Ratio abdominal segments 4/3 1.5 or 4Ð6 fused 5 (4Ð6 fused) 3Ð4 fused 0.3Ð1 1 1Ð3.5 2Ð Ð 3 PAO ( ) ( ) Clavate tenent hair Scales Mucro Falcate, bidentate, 3Ð5 teeth 3 teeth Long Falcate, 3 teeth (long) Long Bidentate Long Varied Bidentate, falcate b Dens Crenulate smooth Smooth Smooth Smooth Smooth Smooth Crenulate, smooth Smooth Crenulate Smooth Crenulate Ð 15 Setae trochanteral organ Varied, often on femur Antennal segments Ð5 4Ð6 c,, Terminal antennal segment to subterminal Botriothrica abdomen 2Ð4 Most none; never 2:3:2 0:0:3Ð4 0:2:3 0:2:1 0:1:2 1:1:1 0:1:0?? 1:3:1 Varied 2:3:2 2:3:3 Male genital plate d C, M O M e M C O?? P P, C Varied Complex microsetae with botriothrica Postocular botriothrica? Tenacular setae 1Ð Ð30 1Ð8?Ð13??? 0 0Ð1 0Ð4 a The placement of Oncobryidae is problematic. b Bessionella has a mucro intermediate between tridentate and falcate. c One exception: genus Cephalotoma. d O, oligochatotic; M, multisetaceous; C, circinate; and P, papillate. e Intermediate between circinate and multisetaceous.

4 504 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 and except for the other members of this putatively primitive subfamily all have the fourth segment 1.7 times as long as the third at midline. This feature is shared with Actaletidae and some Oncopoduridae, but in the former case there is fusion of abdominal segments 4Ð6 not seen in Entomobryoidea, and the real length of the fourth segment is not evident. Another feature that serves to unite the members of Entomobryoidea is the absence of cylindrical or swollen, moderately long, blunt setae on the fourth antennal segment. This serves to separate them from the Oncopoduridae and most Isotomidae. They are also the only extant groups of the Entomobryomorpha with some forms having more than four antennal segments. Extinct Members of Entomobryoidea The two extinct families placed in the Entomobryoidea, Praentomobryidae (Christiansen and Nascimbene 2006) and Oncobryidae (Christiansen and Pike 2002), have some of the most important features of the superfamily not visible on specimens so far available; however, there are sufþcient visible features, including type 1 setae, to make their placement here justi- Þable. The absence of a typical trochanteral organ, in both, is the most problematic feature, but in the Praentomobryidae, there are only four or Þve short normal acuminate setae on the inner face of then trochanter and they are in position much as the three trochanteral organ setae in Capbrya. The presence of a postocular botriothricum-like seta in the late Cretaceous Oncobrya, and its absence in the mid Cretaceous Praentomobryidae, presents the possibility that this is an apomorphic feature. ClariÞcation of this must await more fossil evidence. Table 3. Features of subfamilies of Paronellidae Character Paronellinae Cyphoderinae Botriothrica on abdominal 232 2Ð3/2Ð3 Segments 2Ð4 3Ð4 Scales Mucro Varied Elongate Antennal segments 4Ð5 4 Tenaculum setae 0Ð1 1 Male genital plate Papilate, circinate Circinate Tomoceroidea As deþned here, this superfamily includes families Tomoceridae and Oncopoduridae. The circumscription of Tomoceridae is problematic, but traditionally has included the mostly septentrional Tomocerinae and austral Lepidophorellinae. Until recently, Tomocerinae was considered to contain a single genus with several subgenera. Recently most workers have elevated these to generic level so that the subfamily contains nine genera. Lepidophorellinae contains Þve genera, two of which are monobasic. Oncopoduridae comprises the genus Oncopodura (52 species) and the monobasic Harlomillsia. The families we place in Tomoceroidea have few features in common. All, except Harlomillsia, have at least one botriothricum on the mesothorax and one or two botriothrica on the third abdominal segment. Except for a few genera of the subfamily Lepidophorellinae, all have body scales and spines on the dentes. Except for Lepidophorellinae, they have long complex mucrones. The best argument for linking the three taxañlepidophorellinae, Tomocerinae, and OncopoduridaeÑis the subdivided dentes. The Tomoceridae all have the third abdominal segment subequal to or greater than the fourth, but the reverse is true in the Oncopoduridae. Extinct Members of Tomoceroidea Almost all extinct members of the Tomoceroidea probably belong to the subfamily Tomocerinae. This includes all fossils from the Eocene and earlier, one fragment seen in amber from the Late Cretaceous and two fragments seen in amber from the Mid- Cretaceous. The one genus described from the Late Cretaceous (Entomocerus mirus Christiansen and Pike 2002) is problematic. It has scales similar to Tomoceridae, subequal third and fourth abdominal segments and a mucro unlike any extant tomocerids but more similar to Tomocerinae than to most Lepidophorellinae. The antennae are like those of Lepidophorellinae, but they have cylindrical multilaterally minutely ciliate setae, similar to the type 2 setae of Entomobryidae. However, because several molecular phylogenetic studies (Lee et al. 1995, DÕHaese 2002) have suggested a closer relationship of Tomoceridae to the Isotomidae than to the Entomobryidae, this last feature is probably best interpreted as convergence. Entomocerus seems unlikely to be a candidate for a common ancestor for the two subfamilies of Tomoceridae and its placement must await the study of additional material. The family Oncobryidae has been placed in the Entomobryoidea, and although it bears some features similar to Oncopoduridae the absence of scales and dental spines, as well as the Þve antennal segments and tapered curved dentes suggest a close relationship is unlikely. Isotomoidea Here, we include families Isotomidae and Actaletidae. Isotomidae is the most varied family in Entomobryomorpha and as such extremely difþcult to delimit. They all lack scales, trochanteral organs and postocular botriothrica. They have four antennal segments and a fourth abdominal segment usually subequal to or smaller than the third (except Folsomia, Folsomina, Pectenisotoma, etc., where abdominal segments 4Ð6 are fused). Most species lack botriothrica and no extant genera have setae resembling the entomobryid type 1 or 2 setae. The distinction between the subfamilies and genera are clearly spelled out by Potapov (2001), and they will not be dealt with further here.

5 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 505 Table 4. Features of subfamilies and tribes of family Entomobryidae Characteristic Capybryinae Orchesellinae Entomobryinae Capbrya Hispanobrya Nothobryini Bessoniellini Heteromurini a Orchesellini Corynothricini Seirini Entomobryini Lepidocyrtini Willowsini Botriothrica abdomen 2Ð Trochanteral organ setae 3 3Ð4 3Ð PAO, Clavate tenent hair,,, Ratio abdominal segments 4/3 1.7Ð Ð Ð Ð Scales,, Mucronal shape Falcate Falcate Falcate Tridentate b Bidentate Bidentate Bidentate Bidentate, falcate Bidentate, falcate Bidentate, falcate Antennal segments Mucronal basal spine,,,, Tenaculum setae 1Ð Ð16 0Ð Male genital plate Papillate Oligochaetotic?? Circinate (multisetaceous) Complex microsetae with botriothrica Circinate (multisetaceous) Circinate Circinate, papillate Papillate Circinate, multisetaceous Venter of dens Setae Setae Setae Setae Setae and/or scales Setae and/or scales Setae Scales Setae Scales Setae Bidentate, falcate Papillate a As diagnosed here, Heteromurini includes tribes Mastigocerini and Heteromurini (see Appendix). Mastigocerini is characterized by having fusiform, denticulate scales restricted to the body, trunk terga with abundant supplementary microsetae, tenaculum without setae, and head row S with 2 2 macrosetae; Heteromurini includes species with scales ribbed, rounded or truncate and covering the furcula and terga, and head row S with at least 4 4 macrosetae. b The mucro is falcate with two extremely weakly developed posterior teeth.

6 506 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 Table 5. Characteristics distinguishing Seirini and Lepidocyrtini Character Seirini Lepidocyrtini Scale shape Some or most pointed All rounded or truncate Scale sculpture Coarsely striate or ridged Finely striate or indented Macrosetae Numerous on whole body Few beyond mesothoracic collar Male genital plate Circinate or papillate Most multisetaceous, few circinate Mucro Falcate or bidentate Most bidentate, few falcate Actaletidae is a small family of nine described species all of which live on rocky shores or mangrove swamps. The characters used to circumscribe Isotomidae will include Actaletidae. However, Actaletidae can be distinguished from all genera of Isotomidae by the presence of a tracheal system, the subdivision of the dentes, and possibly the leaf-shaped tenent hair (Soto-Adames 1988). Other characters of Actaletidae are present in Isotomidae, for example the fusion of abdominal segments 4Ð6 (although abdominal shape in Actaletidae differs greatly from Folsomia and the condition is clearly convergent); botriothrica on abdominal segments 4Ð6 (shared with Archisotoma, Isotomurus, Axelsonia, etc.); and mucronal shape (shared with Archisotoma). Coenaletoidea, New Status The single member of this superfamily, Coenaletidae, is characterized by a strongly sclerotized, dorsoventrally ßattened body; abdominal segments 3Ð4 fused but with segments 5Ð6 distinct; a characteristic mandible with well developed molar plate but with a single acuminate apical tooth; and a large lateral ungual tooth that Þts in a groove at the tip of the tibiotarsus. The phylogenetic afþnities of Coenaletes are unclear. The placement of this family in Entomobryomorpha is based on the presence of an elongate body, and the reduction of the pronotum. Within Entomobryomorpha, Bellinger (1985) suggested a relationship to Isotomidae based on the absence of scales and ciliate setae. Bellinger further suggested a distant relationship to Axelsonia based on the shared distribution of abdominal botriothrica (2 2 on abdominal segments 2Ð4Ñin Coenaletes Fig. 2. Ciliate setae typical of Entomobryoidea. the large segment presumably formed by the fusion of abdominal segments 3Ð4 carries 2 2 anterior and 2 2 posterior botriothrica), the presence of supplementary sensilla on the third antennomere sense organ, and by having two to three very Þne dorsal tibiotarsal hairs. Two characters suggest that the phylogenetic afþnities of Coenaletidae may lay outside Entomobryomorpha. The almost square manubrium and c-shaped (as opposed to ll-shaped) dentes of Coenaletes (cf. Palacios-Vargas et al. 2000) closely resemble the structures seen in Podura and some Symphypleona. In addition, the arrangement of modiþed setae on the second and third antennae of males (Jacquemart 1980, Mari Mutt 1994) shows remarkable similarities to those in some Sminthurides. However, these characters also may be explained as convergence. The structure of the furcula and male antennae may reßect an ancient adaptation of the ancestor of Coenaletes to living on water surface. A detailed analysis of the phylogeny of this family is needed to decide between these hypotheses. Separation of Families and Subfamilies Table 2 shows the separation between the families of Entomobryomorpha. Tomoceroidea Families. The Oncopoduridae can be readily separated from the Tomoceridae by the presence of complex spines on the distal half of the dens, generally Fig. 1. Smooth and unilaterally ciliate setae typical of Isotomoidea. Fig. 3. Coenaletidae, pattern of trunk segmentation.

7 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 507 Isotomidae with all abdominal segments dis- Fig. 4. tinct. relatively longer fourth abdominal segment as well as the botriothrical pattern on abdominal segments 2Ð4 not seen in the Tomoceridae. Subfamilies. The separation between Tomocerinae and Lepidophorellinae is difþcult. The best separation is that tomocerins always have an elongate mucro and a fourth antennal segment much shorter than the third, whereas lepidophorellins never have both together. Fig. 6. Actaletidae, pattern of trunk segmentation. families; however, their similarities are so great (Table 3) that we consider best to include them as part of the same family. Entomobryoidea, Extant Members Families. The monospeciþc family Microfalculidae is easily separated by the absence of a mucro. The Paronellidae and Entomobryidae can be easily separated by the presence of a crenulate and strongly tapered dentes in the latter and a smooth nearly cylindrical dentes in the former. In addition, mucronal shape is extremely varied in Paronellidae but always bidentate or falcate in Entomobryidae. All entomobryids have botriothrica on each side of abdominal segments 2Ð4 (the pattern in most Seira is 2-3-3, but the posterior botriothrica is not present in the Þrst instar and is, thus, secondarily derived; Soto-Adames, 2008), whereas in Paronellidae there are a variety of arrangements (including the pattern). The genera we place in the various suprageneric categories of this superfamily are shown in the Appendix. Note that in the Appendix we do not show all generic synonyms, but only those that have been used in recent times. Paronellidae subfamilies (Table 3) Separation between Paronellinae and Cyphoderinae is based on the presence of fringed dental scales in the latter and their absence in the former. All cyphoderines are eyeless, whereas the majority of paronellines have eyes. In addition, all cyphoderines have scales, whereas many paronellines lack these scales. These two subfamilies are often considered separate Fig. 5. Isotomidae with abdominal segments 5Ð6 fused. Fig. 7. Actaletidae, anterior view of tenet hair.

8 508 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 Fig. 10. Paronellidae, dens morphology. Orchesellinae Tribes As treated here, this subfamily includes Þve tribes, two of which are deþned below for the Þrst time. Fig. 8. Position of post-ocular botriothrica. Entomobryidae (Table 4) The separation of Entomobryinae from the other subfamilies is easy, because only members of this subfamily have the fourth abdominal segment at least twice as long as the third at mid-line. In addition, all members have complex microsetae around some abdominal botriothrica, and only one species among all other subfamilies has these microsetae. Most species of the Orchesellinae have more than four antennal segments, whereas all members of other subfamilies have only four. The distinction between the Entomobryinae and Orchesellinae is unambiguous but that between Capbryinae, new subfamily, and Orchesellinae is less clear due to the intermediate nature of Nothobrya. All members of Orchesellinae have adult trochanteral organs with at least 11 setae, whereas Nothobrya has only four, as do members of Capbryinae. The presence of six antennal subsegments, as well as recurved labral setae, features seen in some other Orchesellinae but not in Capbryinae, places it Þrmly with the Orchesellinae and leads us to consider it as part of this subfamily. Entomobryinae Tribes The Entomobryini is the easiest to separate from all the others, because it is the only one lacking scales. Among the scaled tribes, the Willowsini is easiest to distinguish because it is the only lacking scales on the venter of the dentes. The Lepidocyrtini and Seirini are more difþcult to separate, but Table 5 shows some of the differences between the tribes. In addition to these, the Lepidocyrtini are generally smaller than the Seirini, rarely being 1.5 mm long, whereas the Seirini are rarely 1.7 mm long as adults. Nothobryini New Tribe This tribe includes all Orchesellinae with falcate mucro, postantennal organ and trochanteral organ with three to four setae. Additional characters are listed in Table 4. Bessoniellini New Tribe This tribe is the only among Orchesellinae in having tridentate mucro, trochanteral organ with 12 setae and modiþed supplementary setae around the botriothrical complexes. See Table 4 for additional characters. Most members of Orchesellinae belong to the tribe Orchesellini. Indeed, almost all other tribes are monospeciþc. Heteromurini is easily separated from Orchesellini by having only Þve segmented antenna. As deþned here, Heteromurini includes six or seven genera, Heteromurus and related genera comprise forms with apically rounded scales covering the body and ventral face of the furcula; in Mastigoceras scales are fusiform and present only on the body; Orchesellides and Australotomurus are polychaetotic and lack scales. Corynothricini ( Corynothrix) is similar to Orchesellini and Heteromurini in having a multisetaceous trochanteral organ, bidentate mucro, and circinate male genital plate, but differs in having four antennal segments, a pleurochaetotic body lacking mesothoracic macrosetae, and abdominal segments 3Ð4 subequal. Bessionellini ( Bessionella) is a highly troglomorphic genus of unclear afþnities. The peculiar mucro, intermediate between falcate and bi- or tridentate, as well as the presence of complex microsetae around some botriothrica clearly separate it from other tribes of the Orchesellinae. Nothobryini ( Nothobrya) has been discussed already. Fig. 9. Entomobryidae, dens morphology. Fig. 11. Inner view of metatrochanter showing trochanteral organ.

9 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 509 Fig. 14. Four segmented antenna. Fig. 12. Scale morphology in Seirini and Willowsini. Capbryinae new subfamily This subfamily includes all Entomobryidae with a combination of the following characters (Table 4): ratio of Abd. 4/Abd. 3 ranging from 1.7 to 2.0, four antennal segments, postantennal organ present, mucro falcate and trochanteral organ with a maximum of four setae. This combination of characters distinguishes Capbrynae from Nothobryini and Corynothricini as discussed above. There are only two genera in this subfamily, and they are so similar that no tribal separation is merited. The only real differences between the two are the claw morphology, sensory organ on antennal segment III, eye number, PAO, and male genital plate. The last is the most striking difference with Capbrya having the most highly evolved papillate type and Hispanobrya having the putative most primitive oligochaetotic type. The unguis of Hispanobrya has three dorsal longitudinal ridges extending beyond the level of the basal teeth, with the central ridge longer than the others. There are two inner unpaired ungual teeth, the basal tooth arises from one lamella but the apical tooth is formed at the point the inner lamellae fuse. In contrast, Capbrya lacks the dorsal ungual ridges and the inner lamellae meet at the subapical unpaired tooth. The extant taxa of Entomobryomorpha we have considered can be separated as shown in the key below: Key to Extant Suprageneric Taxa of Entomobryomorpha 1. Body seta usually smooth or unilaterally ciliate, multilaterally ciliate macrosetae always acuminate, scales absent 5 (Fig. 1). 2 Most head and body setae ciliate, macrosetae sometimes multilaterally ciliate and cylindrical, usually truncate or broadened at the tip (Fig. 2), with or without scales Ratio abdominal segments III/IV 1.5 or segments 4Ð6 fused...isotomoidea 3 Abdominal segment 3Ð4 fused (Fig. 3) Coenaletidae 3. Abdominal segments 4 Ð 6 distinct (Fig. 4), but if fused then shorter than length of mesothorax to abdominal segment 3 (Fig. 5); tenet hair variously shaped but never leaf-like...isotomidae Abdominal segments 4Ð6 fused and 1.4 the length of mesothorax to abdominal segment 3 (Fig. 6); tenet hair leaf-shaped (Fig. 7).....Actaletidae 4. Without postocular botriothrica; Abdominal segments 2/3 with 0Ð1/1Ð2 botriothrica, never with 2/3 botriothrica TOMOCEROIDEA 5 With postocular botriothrica (Fig. 8); Abdominal segments 2/3 with 2/3 botriothrica ENTOMOBRYOIDEA 6 5. Dens with spines on distal one-fourths Oncopoduridae Dens without spines or with them only on basal one-half...tomoceridae 6. Dens crenulate and tapering (Fig. 9)... 7 Dens smooth and cylindrical (Fig. 10) Paronellidae Mucro present...entomobryidae 8 Mucro absent...microfalculidae 8. Trochanteral organ with 3Ð4 setae and four antennal segments (Fig. 11)......Capbryinae new subfamily Trochanteral organ with 3Ð4 setae; if trochanteral organ with 3Ð4 setae, then antennae with 5Ð6 segments...9 Fig. 15. Heteromurini, Þve segmented antenna. Fig. 13. Scale morphology in Lepidocyrtini. 5 Neophorella, a Tomoceridae so far known only from South Africa, will key out here, but it can be identiþed by having the fourth antennal segment shorter than the third, smooth dental spines, and an elongate mucro with two setae and four teeth aligned on the dorsal lamella.

10 510 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 these characters bespeak a close relationship with other families in the superfamily. Fig Ratio abdominal segments III/IV at midline 2...Entomobryinae 10 Ratio abdominal segments III/IV at midline Orchesellinae Ventral face of dens with scales...11 Ventral face of dens without scales Scales with coarse ribs or denticles, some pointed (Fig. 12)... Seirini Scales ribless, Þnely denticulate, apically rounded (Fig. 13)... Lepidocyrtini 12. Body without scales...entomobryini Body with scales (Fig. 12)... Wilowsini 13. Trochanteral organ with 3Ð4 setae (Fig. 11).... Nothobryini new tribe Trochanteral organ with 5 setae Trochanteral organ with aproximately 12 setae, mucro weakly tridentate Besoniellini new tribe Trochanteral organ with 15 setae, mucro bidentate Ð6 antennal segments...16 Four antennal segments (Fig. 14) Corynothricini 16. Five antennal segments (Fig. 15) Heteromurini 7 Six antennal segments (Fig. 16).. Orchesellini 17. Dens with fringed scales (Fig. 17) Cyphoderinae Dens without fringed scales.. Paronellinae Extinct Entomobryoidea We place two extinct Families in this order. Praentomobryidae Members of this family have very elongate fourth abdominal segment, curved slender, sometimes crenulate dens and bidentate mucro with basal spine. All Fig. 17. Orchesellini, six segmented antenna. Cyphoderinae, dens chaetotaxy. 6 According to Yoshi (1989), Lepidosinella lacks ventral dental scales and will key out to Willowsini; however, we place this genus in Seirinae because Yoshi indicates that in scale and mucro morphology, and in general body shape Lepidosinella most closely resembles Seira. 7 Including tribe Mastigocerini. Oncobryidae The placement of this family is problematic. The tapered dentes, Þve antennal segments, mucro similar to that of Cyphoderinae, and presence of at least one cylindrical Þnely multilaterally ciliate all seem to place it in the Entomobryoidea; however, many of the features which would allow a more certain placement are not visible on the presently known specimen. Acknowledgments The research was made possible by research grants from Grinnell College. Stephanie Peterson assisted in the preparation of the manuscript. We thank two anonymous reviewers for providing comments that helped improve this manuscript. National Science Foundation grant DEB supported F.S.-A. during the initial phase of this work. References Cited Börner, C Die Familien der Collembolen. Zool. Anz. 41: 315Ð322. Bellinger, P. F A new family of Collembola (Arthropoda, Tracheata). Caribb. J. Sci. 21: 117Ð123. Cantino P., and K. de Queiroz PhyloCode: a phylogenetic code of biological nomenclature version 3. ( Cassagnau, P La phylogénie des collemboles â la lumière des structures endocrine rétrocérébrales. Premiere Symposium Internationale Zoophylogenie, Salamanca: 333Ð349. Christiansen, K The Nearctic members of the genus Entomobrya (Collembola). Bull. Mus. Comp. Zool. 118: 1Ð545. Christiansen, K., and E. Pike Cretaceous Collembola (Arthropoda, Hexapoda) from the Upper Cretaceous of Canada. Cretaceous Res. 23: 165Ð188. Christiansen, K., and P. Nascimbene Collembola (Arthropoda, Hexapoda) from the Mid-Cretaceous of Myanmar (Burma). Cretaceous Res. 27: 318Ð363. Deharveng, L Recent advances in Collembola systematics. Pedobiologia 48: 415Ð433. D Haese, C Were the Þrst springtails semi-aquatic? A phylogenetic approach by means of 28S rdna and optimization alignment. Proc. R. Soc. Lond. B 269: 1143Ð Hopkin, S The biology of springtails. Oxford University Press, Oxford, New York. Jacquemart, S Un collembole noveau de Papouasie, Actaletes vangoethemi sp. n., associé au bernard lõermite Coenobita rugosa Milne Edwards. Ann. Soc. R. Zool. Belg. 109: 67Ð75. Lee, B.-H., U.-W Hwang, W. Kim, K.-H. Parkand and J. P.-T. Kim Phylogenetic study of the suborder Arthropleona (Insecta Collembola) based on morphological characters and 18S rdna sequence analysis. Polski Pismo Entomol. 30: 261Ð277. Mari Mutt, J. A A classiþcation of the Orchesellinae with a key to the tribes, genera and subgenera (Collembola: Entomobryidae). Ann. Entomol. Soc. Am. 73: 455Ð 459. Mari Mutt, J. A A Caribbean male Coenaletes, and new records from the Dominican Republic and St. Croix,

11 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 511 USVI (Hexapoda: Collembola: Coenaletidae). Caribb. J. Sci. 30: 272Ð274. Mitra, S. K Chaetotaxy, phylogeny and biogeography of Paronellinae (Collembola: Entomobryidae). Rec. Zool. Surv. India Occas. Pap. 154: 1Ð107. Nixon, K. C., and J. M. Carpenter On the Ôother phylogenetic systematicsõ. Cladistics 16: 298Ð318. Nixon, K. C., J. M. Carpenter, and D. W. Stevenson The PhyloCode is fatally ßawed and the ÔLinneanÕ system can easily be Þxed. Bot. Rev. 69: 111Ð120. Palacios-Vargas, J. G., L. Q. Cutz, and C. Maldonado Redescription of the male Coenaletes caribaeus (Collembola: Coenaletidae) associated with hermit crabs (Decapoda: Coenobitidae). Ann. Entomol. Soc. Am. 93: 194Ð 197. Potapov, M Synopses of Palearctic Collembola, vol. 3 Isotomidae. Abh. Ber. Naturkundemus. Görlitz. 73: 1Ð603. Schäffer, C Die Collembolen der Umgebung von Hamburg und benachtbaren Gebeite. Mitt. Natur. Mus. Hamburg 13: 147Ð216. Soto-Adames, F. N Revisión de la familia Actaletidae Börner, 1902 (Insecta, Collembola). Caribb. J. Sci. 24: 161Ð196. Soto-Adames, F. N Postembryonic development of the dorsal chaetotaxy in Seira dowlingi (Collembola, Entomobryidae); with an analysis of the diagnostic and phylogenetic signiþcance of primary chaetotaxy in Seira. Zootaxa. 1683: 1Ð31. Szeptycki, A Chaetotaxy of the Entomobryidae and its phylogenetical signiþcance, pp. 1Ð219. In Morphosystematic studies of Collembola, IV. Polska Akademia Nauk, Zaklad Zoologii Systematycznej Doswiadczalnej.Krakow, Poland. Tömösvary, Ö Újabb adatok hazánk ThysanuraÐ fauna jához. Mathematische Temeresz Közl. 19: 47Ð58. Yosii, R Phylogentische Bedeutung der Chaetotaxie bei den Colembolen. Contrib. Biol. Lab. Kyoto Univ. 12: 1Ð37. Yoshii, R Finding of Lepidosinella armata Handschin from East Java, pp. 89Ð91. In R. Dallai [ed.], 3rd International Seminar on Apterygota. University of Siena, Siena, Italy. Yoshii, R., and Y. Suhardjono Notes on the collembolan fauna of Indonesia and its vicinity. I. AZAO 1: 23Ð90. Received 28 December 2006; accepted 15 January Appendix Tribe and subfamily assignment of Entomobryoidea genera. Synonymy is limited to most recent usage. Tribal assignment of Paronellinae genera follows Mitra (1993). Genera of Tomoceroidea Family Oncopoduridae Harlomillsia Bonet, 1944 Oncopodura Carl & Lebedinsky, 1905 Family Tomoceridae Subfamily Lepidophorellinae Antennacyrtus Salmon, 1941 Lasofinius Ireson & Greenslade, 1990 Lepidophorella Schäffer, 1897 Millsia Womersley, 1942 Lepidophorella Neophorella Womersley, 1934 Novacerus Salmon, 1942 Pseudolepidophorella Salmon, 1941 Lepidophorella? Subfamily Tomocerinae Aphaenomurus Yosii, 1956 Lethemurus Yosii, 1970 Monodontocerus Yosii, 1955 Plutomurus Yosii, 1956 Pogonognathellus Paclt, 1944 Tomocerina Yosii, 1955 Tomocerus Nicolet, 1842 Tomolonus Mills, 1949 Tritomurus Frauenfeld, 1854 Genera of Entomobryioidea Family Entomobryidae Subfamily Capbryinae Capbrya Barra, 1999 Hispanobrya Jordana & Baquero, 2005 Subfamily Entomobryinae Tribe Entomobryini Aposinella Paclt, 1971 Coecobrya Botryanura Tshelnokov, 1987 Entomobrya Calistella Schött 1893 Entomobrya Calx Christiansen, 1958 Cavernobrya Yosii, 1956 Sinella Coecobrya Yosii, 1956 Drepanura Schött, 1891 Entomobrya Rondani, 1861 Entomobryoides Maynard, 1951 Haloentomobrya Stach, 1963 Mesentotoma Himalanura Baijal, 1958 Homidia Börner, 1906 Isotobrya Womersley, 1934 Isotobryoides Maynard, 1951 Entomobrya Marginobrya Yoshii, 1992 Mesentotoma Salmon, 1942 Parasinella Bonet 1934 Sinella Prodrepanura Stach, 1963 Sinella Brook, 1882

12 512 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 3 Tribe Lepidocyrtini Acanthurella Börner, 1906 Allocyrtus Yoshii & Suhardjono, 1989 Acrocyrtus Yosii, 1959 Ascocyrtus Yosii, 1963 Carocyrtus Yoshii & Suhardjono, 1989 Cinctocyrtus Yoshii & Suhardjono, 1989 Acrocyrtus? Discocyrtus Yoshi 1959 Ascocyrtus Dahlcyrtus Yoshii & Suhardjono, 1989 Acrocyrtus? Lepidiaphanus Salmon, 1949 Pseudosinella Lepidocyrtus Bourlet, 1839 Metasinella Denis, 1929 Onerocyrtus Yoshii & Suhardjono, 1989 Pseudocyrtus Salmon, 1956 Lepidocyrtus Pseudosinella Schaäffer, 1897 Rambutsinella Deharveng & Bedos, 1996 Setogaster Salmon, 1951 Sulcuncus Mills 1938 Tribe Heteromurini Alloscopus, Börner, 1906 Australotomurus Stach, 1947 Heteromurodes Absolon, 1901 Heteromurus Heteromurtrella Mari Mutt, 1979 Heteromurus Wankel, 1860 Indoscopus Prabhoo, 1971 Alloscopus Luoheteromurus Yongqin & Zhongcheng, 1999 Heteromurus? Orchesellides Bonet, 1930 Orchezelandia Salmon, 1937 Orchesellides? Propemesira Salmon, 1942 Heteromurus Typhlopodura Absolon, 1900 Heteromurus Verhoeffiella Absolon, 1900 Tribe Mastigocerini Mastigoceras Handschin, 1924 Tribe Seirini Acanthocyrtus Handschin, 1925 Acanthurella? Afroseira Yosii, 1959 Seira Austroseira Yoshii & Suhardjono, 1992 Seira Ctenocyrtinus Arlé, 1959 Seira Epimetrura Schött, 1925 Lepidocyrtinus Börner, 1903 Seira Lepidocyrtoides Schött, 1917 Lepidokrugeria Coates, 1969 Seira Lepidoregia Delamare-Deboutteville, 1948 Seira Lepidosinella Handschin, 1920 Lepidosira Schött, 1925 Najtsira Yoshii 1989 Lepidosira Seira Lubbock, 1870 Sinelloides Bonet, 1942 Sundasira Yoshii & Suhardjono 1989 Lepidosira Vietsira Yoshii, 1994 Urewera Salmon, 1938 Lepidosira Tribe Willowsini Americabrya Mari Mutt & Palacios-Vargas, 1987 Drepanosira Bonet, 1942 Desertia Tshelnokov, 1979 Hawinella Bellinger & Christiansen, 1974 Janetschekbrya Yosii, 1971 Lepidobrya Womersley, 1937 Parasira Bonet, 1930 Drepanosira Willowsia Shoebotham, 1917 Subfamily Orchesellinae Tribe Bessoniellini Bessoniella Deharveng & Thibaud 1989 Tribe Corynothrichini Corynothrix Tullberg, 1876 Tribe Nothobryini Nothobrya Arlé 1961 Tribe Orchesellini Dicranocentrella Wray, 1953 Dicranocentrus Dicranocentrus Schött, 1893 Dicranorchesella Mari Mutt, 1977 Heteromuricus Imms, 1912 Dicranocentrus Itheocerus Bourlet, 1842 Orchesella Neorchesella Mari Mutt, 1981 Orchesella Templeton, 1835 Pseudodicranocentrus Mari Mutt, 1981 Family Paronellidae Subfamily Cyphoderinae Calobatinus Silvestri, 1918 Cephalophilus Delamare-Debouteville, 1948 Cyphoda Delamare-Debouteville, 1948 Cyphopderus Cyphoderinus Denis, 1942 Cyphoderodes Silvestri, 1910 Cyphoderus Nicolet, 1842 Delamarerus Mitra, 1977 Megacyphoderus Delamare-Debouteville, 1948 Mimoderus Yosii, 1980 Paracyphoderus Delamare-Debouteville, 1948 Pseudocyphoderus Imms, 1912 Serroderus Delamare-Debouteville, 1948 Setoderus Yosii, 1959 Borecus Folsom, 1923 Mimoderus Subfamily Paronellinae Tribe Bromacanthini Bromacanthus Schött, 1925 Lepidonella Yosii, 1960

13 May 2008 SOTO-ADAMES ET AL.: CLASSIFICATION ENTOMOBRYOMORPHA 513 Tribe Callyntrurini Aphysa Handschin, 1925 Callyntrura Callyntrura Börner, 1906 Chaetoceras Handschin, 1926 Plumachaetas Dicranocentroides Imms, 1912 Idiomerus Imms, 1912 Irianella Yoshii & Suhardjono, 1992 Pseudoparonella Istanaphysa Yosii, 1981 Callyntrura Japonphysa Yosii, 1982 Callyntrura Javaphysa Yosii, 1992 Callyntrura Lawrenceana Mitra, 1993 Pseudoparonella Kudatphysa Suhardjono, 1989 Callyntrura Microphysa Schött 1903 Callyntrura Murphysa Ellis & Bellinger, 1984 Callyntrura Najtnella Yosii, 1989 Pseudoparonella Oceaniella Yosii, 1989 Pseudoparonella Parachaetoceras Salmon, 1941 Pericrypta Schött Callyntrura Phorophysa Salmon, 1945 Callyntrura Plumachaetas Salmon, 1951 Pseudoparonella Handschin, 1925 Sultanaphysa Yosii, 1982 Callyntrura Tribe Cremastocephalini Akabosia Kinoshita, 1919 Coelura Schött, 1917 Metacoelura Glacialoca Salmon, 1941 Metacoelura Salmon, 1951 Micronellides Salmon, 1944 Paronellides Narisa Yosii, 1981 Salina Paronana Womersley, 1939 Paronellides Schött, 1925 Parasalina Salmon Paronana Pseudoparonellides Salmon, 1941 Pseudosalina Mitra, 1974 Salina MacGillivray, 1894 Salinilla Uchida, 1943 Akabosia Silana Yosii & Suharjono, 1992 Salina Yosiia Mitra, 1967 Tribe Paronellini Campylothorax Schött, 1893 Dicranocentropha Wray, 1953 Campylothorax Paronella Schoett, 1893 Tribe Troglopedetini Cyphoderopsis Carpenter, 1917 Dicranocentruga Wray, 1953 Trogolaphysa Microparonella Carpenter, 1916 Troglopedetes Tricorypha Schoett, 1893 Troglobius Palacios-Vargas & Wilson, 1990 Troglopedetes Absolon, 1907 Trogolaphysa Mills, 1938 Family Microfalculidae Microfalcula Massoud & Betsch, 1966 Family Praentomobryidae Cretacentomobrya Christiansen & Nascimbene, 2006 Preantomobrya Christiansen & Nascimbene, 2006