Contributions to Zoology, 80 (4) – 2011
Transformational homology of the tergal setae during postembryonic development in the Sinella-Coecobrya group (Collembola: Entomobryidae)
Feng Zhang1,3, Daoyuan Yu1, Guoliang Xu2
Keywords: primary homology, larval chaetotaxy, primary setae, s-chaetae.
The homology concept and its recognition criteria are introduced and discussed, with the importance of transformational (primary) homology assessment in phylogenetic analysis emphasized. We use an ontogenetic approach to explore the setal transformational homology in polychaetotic entomobryid genera (Collembola), where tergal chaetotaxy is usually the most informative character for taxonomy. The postembryonic development of setae on terga of three species in the Sinella-Coecobrya group, Sinella curviseta, Coecobrya tenebricosa and C. aokii are studied following Szeptycki’s principle. Different chaetotaxic patterns of each tergite are homologized and classified for more than 50 species of the two genera. The taxonomical significance of chaetotaxy of abdomen V, which has been rarely studied, is evaluated and affirmed here. The system presented here is a revised and updated from Szeptycki’s system.
Taxonomy of Collembola mostly relies on the external morphology, although limited molecular analyses have been attempted (D’Haese, 2002; Porco and Deharveng, 2009). A series of integrated approaches have been used to develop and unify descriptive methods, particularly in setal nomenclature, which has been performed using an evolutionary perspective (Deharveng, 2004). The arrangement of setae (chaetotaxy) in larvae and adults is widely used in descriptive and phylogenetic studies of arthropods, for example in Collembola, as well as Lepidoptera, Coleoptera, Acarina et cetera. (Kitching, 1984; Miller, 1991; Archangelsky, 2004; Beutel and Leschen, 2005; Solodovnikov, 2007). However, the problems of chaetotaxic homology often affect the reliability of species description and phylogenetic analysis.
The concept of homology is the fundamental basis for comparative and evolutionary biology, as well as phylogenetic systematics. ‘Classical’ homology is a similarity due to historical continuity of information, a feature shared because of descent from a common ancestral character. Actually, studies employ different homology concepts in the light of their different interests and goals (Brigandt, 2003). Describing and explaining the adaptive modification of characters in comparative and evolutionary biology is referred to as transformational homology. By contrast, taxic homologies are features that provide evidence of phylogenetic relationships (taxic homology = synapomorphy) (Patterson, 1982, 1988; Rieppel, 1994; Sluys, 1996).
Recognition of homology involves both the establishment of a proposition of homology and the subsequent affirmation through congruence (Rieppel, 1988), which are evidenced respectively by Remane’s criteria (detailed similarity in position and quality of resemblance, see Wiley, 1981), and phylogenetic criteria (congruence test). Embryological, ontogenetic and paleontological evidence are the best-known methods used for transformational homology assessment, which remains contentious and subjective, yet ultimately crucial in any cladistic analysis (Pimentel and Riggins, 1987; Bryant, 1989; Pogue and Mickevich, 1990; De Pinna, 1991; Stevens, 1991; Smith, 1994; Pleijel, 1995; Hawkins et al., 1997).
Collembolans are epimetabolic and moult throughout their lives, where a gradual differentiation occurs during development. Most setae present in adults are secondary (additional), occurring after first instar. The recognition of setal transformational homology of adults usually depends on empirical diagnosis, which often becomes problematic, because it is difficult to discriminate homology of morphologically similar setae that are near to each other in a small area, and setae whose morphology varies during postembryonic development. The improper determination of transformational homology will bring severe confusion in the further phylogenetic analysis. An effective method for determining the setal transformational homologies needs to be applied to Collembola. Ontogenetic observation, which is able to strictly trace the transformation and the addition of setae during the postembryonic development and further establish setal transformational homology, could be a much better choice than traditional empirical diagnosis in adults. This method primarily records developmental changes, and indicates that the numbering system and homologies are just hypotheses and subject to different interpretations.
The chaetotaxy on terga, already described for most entomobryid genera, is a powerful tool in taxonomy and may contribute to the solution of phylogenetic relationships among genera of Entomobryidae (Yosii, 1959; Szeptycki, 1979). Setal transformational homology plays an important role in phylogenetic analyses, and its validity therefore will directly affect the reliability of results. However, the displacement and transformation, and the secondary addition of tergal setae during postembryonic development results in difficulty in establishing setal homology in adults. Szeptycki (1969) was the first one to observe the postembryonic development of Entomobryoides myrmecophila (Reuter, 1886) in Entomobryidae. Later, Barra (1975) observed the same in Pseudosinella decipiens Denis, 1924 and P. impediens Gisin and Da Gama, 1969. Szeptycki (1972, 1979) also made a fundamental contribution to the tergal chaetotaxy in Entomobryoidea, by providing a system of nomenclature where he identified the homologous setae.
However, Szeptycki’s system has not been widely applied in the descriptions or identifications in the past thirty years, because it is complex and lacks sufficient assessment of applicability in most entomobryid genera and species. After observing the postembryonic development of Seira dowlingi (Wray, 1953), Soto-Adames (2008) made some corrections on the homology of partial setae that was originally proposed by Szeptycki (1979). Szeptycki’s hypotheses (1979) on setal homology were only based on a few representatives, not entirely representing the high diversity and variability of chaetotaxic patterns that exists in entomobryid adults. To expand comparisons of homology and avoid the wrong identification of transformational homology in phylogeny, it’s necessary to investigate the setal transformational homology in more taxa using an accurate general method.
Jordana and Baquero (2005) also proposed a chaetotaxic system for Entomobrya and its related genera. They studied some species of Entomobrya, Entomobryoides, Homidia and Drepanura, but Sinella and Coecobrya were not included. Most setal names of nomenclature were identical to those of Szeptycki, but justification for the ‘updated’ reason and changes in setal nomenclature was not explained, not was the prospect for expanding the system to other genera.
The two closely related genera, Sinella and Coecobrya, both having reduced number of ommatidia, 4-segmented antennae but with scales and dental spines absent, are widespread and well defined among Entomobryid genera (Deharveng, 1990). Sinella-Coecobrya group is the second largest group in unscaled Entomobryinae, with more than 90 species reported. Chen and Christiansen (1993, 1997) reviewed the best diagnostic characters for the Sinella-Coecobrya group, designating a series of adult chaetotaxic patterns or groups, which were widely applied during the past fifteen years (Chen and Christiansen, 1997; Ma and Chen, 1997; Wang and Christiansen, 2000; Wang et al., 2002; Chen et al., 2002, 2005; Qu et al., 2007, 2010). After the examination of plenty of species (many undescribed) from East and Southeast Asia, we find that the various patterns defined by Chen and Christiansen (1993, 1997) can’t be applied to all cases, even the conflicts occurring between the known patterns. Because the developmental processes of tergal setae are quite similar in Entomobryinae particularly within genera (Szeptycki, 1979), we study the postembryonic development of the tergal setae of only three species in detail and further present a general hypothesis of setal transformational homologies for the Sinella-Coecobrya group. It is not possible for us to observe development of all species because some were difficult to culture and we didn’t have enough specimens at each stage. In addition, to test the validity of the hypotheses and explore the variation in different species, we examine the adult chaetotaxy of more than 50 species of both genera, and point out the flaws of Chen and Christiansen’s classification with more patterns newly designated.
The complete S-chaetotaxy (chaetotaxy of s-chaetae / sensilla / setulae / sensory setae / sensorial chaetae / setae sensuales) has been described in a few species of Sinella and Coecobrya recently by Zhang and Deharveng (2009) and Zhang et al. (2009). The use and variability of S-chaetotaxy in both genera are investigated here for the first time in the Entomobryoidea.
The chaetotaxy of Abd. V is usually overlooked in the taxonomy of Entomobryoidea and rarely described although potential availability in this character was mentioned by Szeptycki (1979). Most setae on this tergum are usually less differentiated and of great number. The diversification of Abd. V chaetotaxy in Sinella-Coecobrya group is also illustrated in the present study.
Material and methods
The widespread and typical representatives of the group, Sinella curviseta Brook, 1882 and Coecobrya tenebricosa (Folsom, 1902) were collected from leaf litter near Nanjing (China) and Paris (France) respectively, and cultured with dry yeast in the laboratory. The third species endemic to Vanuatu (South-west Pacific), C. aokii (Yoshii, 1995), was taken from the alcohol material at Museum National d’Histoire Naturelle (MNHN). Only the specimens of the 1st-3rd instar larvae and adults were examined, and their chaetotaxy were discussed and illustrated in the present paper, because the homology of most macrosetae in adults, particularly the primary setae (occurring at 1st instar, primary versus secondary/additional), could be observed before the 4th instar. Specimens were mounted after clearing in lactic acid under a coverslip in Marc André II solution, and were examined using a Leica DMLB and Nikon E600 microscope. Illustrations were enhanced with Photoshop CS2.
The adult chaetotaxy of 57 species of two genera, including 21 unpublished new species are also examined in the present study (see Appendix). Most material examined was from the collections of the MNHN, Paris, France and of the School of Life Science, Nanjing University (NJU), P.R. China.
Symbols used in the present paper are shown in Fig. 1. Mesoseta is essentially microseta (common seta) in morphology with larger socket and longer length (even longer than macroseta), but it’s much thinner than macroseta. S-chaetae are of two type, microsensillum and sensillum, similar terms to those used for isotomids. Most primary microsetae in adults are not able to be distinguished from numerous additional microsetae, although most of them in adults are slightly larger than the additional ones; so only partial primary microsetae could be recognized and labeled in the adult figures. The figures of adult chaetotaxy in C. tenebricosa, C. aokii, C. lanna Zhang et al., 2009, C. similis Deharveng, 1990 and C. tukmeas Zhang et al., 2009 are redrawn or modified after Zhang et al. (2009).
Terminology: primary setae-setae occurring at 1st instar; secondary/additional setae-setae occurring after 1st instar; s-chaetae-’specialized’ setae of various morphology and different from ‘ordinary (common)’ setae, often called as sensillar / setulae / sensory setae / sensorial chaetae / setae sensuales (Deharveng, 2004).
Abbreviations: Th.-thoracic segment; Abd.-abdominal segment; mac-macroseta(e); mic-microseta(e); mes-mesoseta(e); ms-microsensillum/a; s-sensillum/a; Gr.-group.
Criteria for homologization of setae: the primary setae are almost identical in different taxa of Entomobryinae and easily established in a fixed way. The position of secondary setae in relation to the primary or and other secondary setae, or to those elements whose homology is easier to establish (e.g. bothriotricha, pseudopores) is the main criteria. To determine some complicated cases which have several possible hypotheses, it’s necessary to find the species with intermediate features of chaetotaxy. In addition, the displacement of a homologous seta is more probable than its reduction together with the existence of a new one while the position of setae between two compared species is different. The absence of (some) secondary setae is more probable than that of primary ones.
Principle of setal nomenclature: the primary setae of each tergum except Abd. IV are designated using the symbol of a letter and a number; the former letter represents the relative position (usually a-anterior, m-median, p-posterior) that have been defined in Szeptycki (1972). The secondary setae are named by a combination of the symbol of nearest primary setae and one or several letters indicating their position in relation to the former primary ones; a (anterior), p (posterior), i (internal) and e (external) are used to describe the relative position. For example, p1 represents a primary seta, p1i a secondary seta located internally to p1, p1ip a secondary seta posterior to p1i. To avoid repeating letters of setae following each other in the same direction, a series of successive numbers are used to indicate these setae; e. g., three setae posterior to p1 are designated respectively as p1p, p1p2 and p1p3 (the first letter p often deleted in a set of the drawings); sometimes, the rows of mac close to the main seta is simply designated as a whole, e.g., m.p1p instead of the above three names. To briefly describe some sets of setae arranged in a more or less regular way, these particular setae are connected to each other with a broken line in the drawings, and designated with the characteristic seta and the symbol ‘+’, e.g. set p1+; the largest setae together with the largest socket among them usually appear earliest.
All figures are located after the references.
Postembryonic development of the tergal setae in S. curviseta, C. tenebricosa and C. aokii
First instar (Fig. 2B). Totally 19 ciliate setae and 3 s-chaetae occur, with a7, m2, m5, m7 and p4-6 as mic and others mac. Two s-chaetae (ms and s) are close to seta m7, ms internal to s; the third s is external to p6.
Second instar (Fig. 2C). The primary setae a7 and m2 are transformed into mac. Additional setae a1a, a3a, a4e, a4e2, m4p, m6i, m6p, m7p, p1a, p1p, p2a and p2e appear as mac, m2i, m5a, m5e as mic. The most postero-lateral 3 additional setae, not labeled as any symbols, are difficult to determine their homology.
Third instar (Fig. 2D). Mac a1p, a4a, a4p, a4e2p, a4e2p2, a6ai, a6i and mic a7e are added to the collar. Additional setae m4i, p1p, p2p and p2ea appear as mac. The primary setae are unchanged.
Adult (Fig. 2E). In the subsequent instars and adults, m2i and p2e2 are transformed into mac and a general increase in the number of mac occurs in most multiplets. The position and shape of mic p5-6 and 3 s-chaetae are unchanged during the postembryonic development.Coecobrya tenebricosa
The development of most setae in C. tenebricosa is similar to that in S. curviseta. The relative position of anterior two s-chaetae is reverse compared to S. curviseta, ms external to s during all instars. Seta m4i rarely changes into a mac in adults (Fig. 1F).
The development of setae in C. aokii is similar to that in the above two species. S-chaeta ms is internal to s as usual. However, the primary setae m2 and p4, and secondary setae m4i and m2i are always ciliate mic (Fig. 2A).
First instar (Fig. 3A). Eighteen ciliate setae and 2 lateral s occur, with a2-6, m6 and p1-3 as mac and others mic. Anterior s is internal to m7, another s postero-external to p6. Seta m5 is located anteriorly between a5 and a6, m6 almost aligning with p5 and p6.
Second instar (Fig. 3B). Two mac, p2e and m6e, and 1 mic, m5i, are added by 2nd instar. Primary setae a1, m5 and p6 change into mac. Seta m6 migrates slightly anteriorly.
Third instar (Fig. 3C). The primary setae are unchanged at this instar. Nine new setae are added, i.e., mac a4i, p1p and p2a, mic m1i, a6i, m5p and p5pi, and two setae of unclear homology. Seta m6 migrates further anteriorly.
Adult (Fig. 3D). A general increase in the number of multiplet mac also occurs during the subsequent instars. Setae a6i and p5 are transformed into mac. An additional mac internal to m6 is homologous to m6i.
Primary seta a6 is a mic at 1st instar (Fig. 3E) and develops into a mac at 2nd instar. Mic a6i appears at 2nd instar instead of 3rd instar as in S. curviseta (Fig. 3F). Mac p2p and a4i also occur at 3rd instar but mic p5pi doesn’t appear at this instar (Fig. 3G). Primary seta p5 remains as a mic for life. Seta m6 always aligns with p5 and p6 and never moves anteriorly (Fig. 3H).
Only a4, a6 and p1-3 are mac at 1st instar, other 13 setae as mic (Fig. 4A). By 2nd instar, primary setae a2, a3 and m6 change into mac (Fig. 4B). The adult chaetotaxy (Fig. 4C) is slightly reduced compared to the above two species; p5, m5i, m6e and m6p never become mac. Seta m6 migrates gradually anteriorly during development and at last almost aligns with a6 and p6.
First instar (Fig. 5A). Twelve ciliate setae and 2 s-chaetae are primary, with m2-4 as mac. S-chaeta ms is external to s and a6, s between p5 and p6.
Second instar (Fig. 5B). No additional setae appear.
Third instar (Fig. 5C). A new mac, obviously smaller than m4 and postero-internal to m4, is designated as m4p. Another 2 additional mic m2i and m6e appear at this instar.
Adult (Fig. 5D). Setae m2i and a3 are transformed into mac. Primary seta a5 remains as a mic for life.
At 1st instar, seta a6 is absent and 11 primary setae occur besides s-chaetae; seta m2 is a mic (Fig. 5E). Only 1 additional seta m5i appears and m2 changes from mic to mac at 2nd instar (Fig. 5F). One mac m4p and 1 mic m6e appear at 3rd instar as in S. curviseta (Fig. 5G). In adults, m2i exists as a mac; a mac often present internal to m4 and antero-internal to m4p is homologous to m4i; seta a3 is observed as a mic for life (Fig. 5H).
Setae a6 and m6 are absent and m2 is also a mic at 1st instar (Fig. 5I). The additional seta m2i appears and m2 remains as a mic at 2nd instar (Fig. 5J). In adults, m2-4 and m4p are mac, m2i, a3 and a5 mic (Fig. 5K).
First instar (Fig. 6A). There are 15 primary ciliate setae, 2 bothriotricha and 2 s; m3 and m5 are mac, others mic. The central s (‘as’ in Szeptycki’s monograph) is located between a2 and a3, the lateral s between p5 and p6.
Second instar (Fig. 6B). The mac m3e and 3-4 additional mic are added posteriorly to row p.
Third instar (Fig. 6C). No obvious changes occur except a few additional mic added.
Adult (Fig. 6D). Setae a3 external to a2 and m3ep posterior to m3e are mac in adults. Seta a2 always remains as mic.
Primary setae a7 and m7 are absent, others similar to those in C. tenebricosa (Fig. 6G).
First instar (Fig. 7A). Fourteen ciliate setae (a few lateral mic of unclear homology not included), 3 (m2, a5, m5) bothriotricha and 2 s appear at this instar. Only m3 is mac, others mic. The central s is internal to m3, lateral s between pm6 and p6.
Second instar (Fig. 7B). More than 10 additional setae are added. Primary setae pm6 and p6 change from mic to mac but am6 remains as mic.
Third instar (Fig. 7C). A general increase in the number of additional mic occurs. Primary setae are unchanged at this instar.
Adult (Fig. 7D). Four mac are present in adults, 1 (m3) central and 3 (am6, pm6, p6) lateral.
Primary setae are identical with S. curviseta at 1st instar. Seta pm6 changes from mic to mac at 2nd instar; the transformation of am6 into a mac occurs at 3rd instar; others never exhibit any changes for life except a general increase of mic (Fig. 7E).
Primary setae are identical with the above two species at 1st instar. Seta am6 changes into a mac at 2nd instar. Setae pm6 and p6 develop into mac in the subsequent instars (Fig. 7F).
First instar (Fig. 8A). There are 29 ciliate setae, 2 bothriotricha and about 18 (sometimes 17) s. Setae B5 and E3 are mac, others mic. Seta C1 is located in alignment with B2 and T1. Two of the s-chaetae are obviously shorter than others, although as long as s on other terga; one is external to T7 and designed as ps by Szeptycki, another is external to B5.
Second instar (Fig. 8B). More than 20 additional setae are added, with 3-4 mic on the midline. Four primary setae A6, B4, B6, and E4 are transformed into mac. Two secondary mac, designated I and M here, appears postero-external to A3 and between B3 and T2, respectively. Setae D3, F1 and F3 are apparently larger than other mic and develop into mes. A mac between D2 and F2 appears at this instar; here we consider it to be homologous to E2 in contrast to the position of ‘E2’ in the 1st instar larvae of Seirinae and Lepidocyrtinae.
Third instar (Fig. 8C). Setae D3 and F1 change into mac. A4 is rarely transformed into mac. Mac E2p is added, aligning with column E1-2. The sockets of mic D3p, E2a, E4p and F2 are larger than other mic.
Adult (Fig. 8D). The number and position of mac are identical to that at 3rd instar. More mes appear on the lateral part with sockets relatively larger but apparently smaller than those of mac. The long s (the complete arrangement is impossibly observed for their loss during specimen preparation) are more than 2 times as long as both ps and another short s external to B5.
At 1st instar (Fig. 9A), about 15 s appear; setae B5 and E3 are mac. Compared to S. curviseta, B4 moves antero-externally, falling into the column C1-2; B5 and B6 also move anteriorly, B5 getting closer to A4; the second short s is postero-external to B5 and internal to C3. By 2nd instar (Fig. 9B), mac E2 and mic E2p occur at the same time; the sockets of mic A6 and B4 are larger than those of other mic. At 3rd instar, A6, B4 and I are transformed into mac; E4 also develops into mes with socket much smaller than that of mac, and into a mac in the subsequent instars (Fig. 9C).
The chaetotaxy of 1st instar larvae is similar to that in C. tenebricosa except S-chaetotaxy (Fig. 9D); B4 and B5 are anterior to their normal position; the second short s is between C2 and B5, aligning itself with them. At 2nd instar (Fig. 10A), E2 and E4 changes into mac, with the addition of secondary mac M and mic I. I, A4, A6, B6, F1, E2p and D3 are transformed into mac in the subsequent instars (Fig. 10B). The homology of a seventh dorso-central mac inner to I and rarely present in adults is unclear.
First instar (Fig. 12B). Fourteen ciliate setae and 3 s occur, including a mic posterior to pp6 designated as ‘el’ here by the present authors. Setae of row m are larger than others. The inner s is located between a3 and m3, middle one between p3 and p4, lateral one internal to p5 (between p4 and p5).
Second instar (Fig. 12C). Six additional mic are added. Among them, one antero-external to a6 is designated as ‘a6a’, the other antero-external to a5 as ‘a5a’.
Third instar (Fig. 12D). Two mic, m3a and p1p, appear.
Adult (Fig. 12E). All the sets are complete as Szeptycki’s definition. Seta p0 on the midline is present.
The chaetotaxy of 1st instar is nearly the same as that in S. curviseta except that the lateral s is located more anteriorly and between a5 and m5; seta el is also present. Three mic, m3a, p6ai and a6a, are added at 2nd instar (Fig. 12A). By 3rd instar, 5 mic occur, i.e., m5a, p3a, p4a, p1p and p3pi. In adults, p0 is also present; set p4a+ is complete; p4p and p5pe are absent in set p4p+ (Fig. 13B).
The chaetotaxy of 1st instar is the same as that in C. tenebricosa; seta el is also present (Fig. 13C). Only 2 mic, a6a and p6ai, are added at 2nd instar. In adults, p0 is also present; set p4a+ is complete; set p4p+ is incomplete with only 1 mic p1p present; sets p4a+ and p3+ are quite close to each other (Fig. 13D).
Revision of homology and chaetotaxic patterns in Sinella-Coecobrya group
Homology of some setae in the nomenclature of Szeptycki’s system (mainly after figures of Coecobrya hoefti) and the present study are shown in Table 1.
Table 1. The nomenclatorial comparison between Szeptycki’s system (mainly after the figures of Coecobrya hoefti) and present study.
Thorax II (Fig. 2B)
Compared to Szeptycki’s nomenclature, the main conflict is the presence or absence of the set a3e+. The chaetotaxy of 2nd instar in the above three species exhibits the addition of two mac (a4e, a4e2) external to a4, which develops into the sets a4e+ and a4e2+ during the subsequent instars. Considering that the mac antero-external to a3 apparently belongs the set a3+ and no more secondary mac in relation to it occur for life, this mac is homologous to a3a instead of a3e. In addition, the fact that the sockets of primary mac a3 and a4 is apparently larger than that of mac a3a, a4e and a4e2, also approves the secondariness of the latter three setae. Szeptycki (1979) exhibited the similar process in the 2nd instar larvae of Orchesella flavescens (Bourlet, 1839), but he used perplexing, wrong names in other species. ‘a4e2, m2e and p2e2’ are newly designated by the present authors.
Chen and Christiansen (1993) divided the setae on medial and posterior areas into 6 groups, whose corresponding homologies are shown in Table 2. Group III-V are of less taxonomical value because the number of additional setae in these areas is variable from juveniles to adults, even in adult instars.
Table 3. Macrochaetotaxic patterns of Gr. I on Th. II in adults (+ present as mac; - absent or present as mic).
Group I. So far, eight patterns are found respectively with 1-6 mac. Seta m1 is always a mac in all patterns, while m2e as a mac only in pattern VIII in S. sp. A. Socket of m1i, if it is a mac, is usually smaller than others.
Group II. Four patterns are found (Table 4). Seta m4 is always a mac in all patterns for life, and m4pi is found to be a mac only in pattern IV in S. sp. A.
Group VI. There are usually 0-2 mac in this area (Table 5). Seta p4p rarely develops into mac in adults. When only one mac is present in the area of Gr. VI, it is homologous to p4 or p2e2 (Fig. 2B), p4 more external to p3 than p2e2; while both mac p2e2 and mic p4 present, p4 antero-external to p2e2 is easy to be recognized for its larger socket than those of ordinary mic. More mac associated to p2e2, all designated as set p2e2+ here, are found in S. sp. C (Fig. 2B). If two mac present in Gr. VI, the homology of the inner one sometimes is difficult to judge; for example, the inner seta in C. tenebricosa, just located internal to p4 and slightly farther from p4 than normal position of p4i, is possibly homologous to p2e2, which is usually considered as p4i (Fig. 1F). Because of the uncertainty of p2e2 in this area, it should be quite careful when giving the names.
The anterior two s-chaetae are close to m7, both internal or both external to m7, or ms internal and s external to m7. The short ms is usually internal to s except that in C. tenebricosa. The posterior s is external to p6.
Thorax III (Fig. 4E)
Setal homology coincides well with Szeptycki’s results. Primary setae m5, p4 and p5 may remain mic in adults; p4 is usually a mic. Primary setae m1, m4, a7 and m7 are always mic for life. The position of two lateral s is stable, respectively internal to m7 and external to p6. Gr. I-IV were divided by Chen and Christiansen (1993), with their homologies shown in Table 6. The number of setae in Gr. I and II is often variable whatever interspecifically or intraspecifically.
Sets a4+ and a5+. Two sets are of great use, usually with 3 patterns present: I, a4, a4i, a5; II, a4, a5; III, a4, a4i, a4i2, a5. The mac a5i is unstable and often absent in adults.
Group III. The group is of great taxonomical importance, with five patterns found (Table 7). Seta a6 is always a mac in all patterns. Seta m5 is observed as a mic only in pattern I in an endemic species C. sp. D (Fig. 4D). Pattern V represents the complete sets m5+ and a6+, which is a most generalized pattern in other Entomobryini and Willowsiini species.
Group IV. Only setae p6 and m6 are always mac in adults; their relative position is stable and of taxonomical value, m6 aligning with p5 and p6 (Fig. 3E-H), or m6 antero-exnternal to p6 (Fig. 4E) or even anterior to p6 (Fig. 4D). Setae p5 and m6e always occur but often remain as mic. Seta m6i is often absent (Fig. 4D).
The postembryonic development of the above three species (Fig. 5) demonstrates that the two mac, both external to m3 and socket of posterior one usually smaller than the anterior one, are m4 and m4p instead of a5 and m4 in Szeptycki’s system, with the substitution of a5i by m4i. Seta a5 never develops into mac for life in the examined three species, and its distance from m4 is much longer than that between m4 and m4p. Primary setae m2-4 are always mac in adults, those lateral to them as mic; the sockets of p6, m6 and m6e are often larger than those of other mic and easily distinguished; mac a1 and a5 are only present in Pattern VIII in S. sp. A (Fig. 5L). The mac m4i and a5i may be present or absent in adults (Pattern I-III, VIII), so no more separate patterns are recognized while they are present (Fig. 5H). Besides 4 patterns defined by Chen and Christiansen (1993), 4 more patterns, V-VIII, are observed in the present study (Table 8). When m4i absent in Pattern II and present in Pattern III, both patterns look to be the same, but actually are different.
Table 8. Macrochaetotaxic patterns of Abd. I in adults (* pattern designated by Chen and Christiansen, 1993).
The position of s-chaetae is interspecifically variable but intraspecifically stable, although the number of s-chaetae (ms and s) on Abd. I is unchangeable. The internal s usually is located between p5 and p6, ms external to a6 and p6. In some species, both s-chaetae move internally, with s closer to p5 and ms internal to p6 (Fig. 5M). Both s-chaetae are reverse in S. sp. A (Fig. 5L).
Abdomen II (Fig. 6H)
The diverse patterns and their stability of dorsal chaetotaxy on Abd. II result in its high taxonomical reliability. Our results on homology agree well with Szeptycki’s system. Setae m3, m3e and m5 are always mac in both genera. Chen and Christiansen (1993) divided the central area into two parts, M3 arch (m3, m3e+) and inner part. A maximum of 4 mac occurs in M3 arch; while 3 in arch, m3ep is always transformed into a mac rather than m3ea. Another difficulty of homology is the discernment of a2 and a3, the former internal and the latter external to as (the central s) (Fig. 6D); while only 1 mac, except m3ei, is present inner to M3 arch, it has two possibilities of homology (a2 or a3). The number and position of s-chaetae on Abd. II are stable, ms absent.
Abdomen III (Fig. 7G)
Primary setae m3 and pm6 are always as mac in adults; a2, a3, am6 and p6 may develop into mac, other primary setae as mic during all the instars. Seta a2 and a3 is respectively internal and external to as.
There are 1+1-4+4 mac possibly present on central Abd. III, respectively designated as Pattern I-IV (Fig. 7H) and the latter two patterns rarely present in both genera.
Three macrochaetotaxic patterns occur on lateral Abd. III: I, am6, pm6, p6 (Fig. 7F); II, am6, pm6 (Fig. 7E); III, pm6, p6 (e.g. C. tetrophthalma). An exception occurs in Sinella yosiia Bellinger and Christiansen, 1974, a mac possibly homologous to a7 occurring external to am6 in the original figure.
Two s are always present on Abd. III, central one (as) between a2 and a3 and lateral one between pm6 and p6 (Fig. 7A-F). A third s-chaeta (ms) occurs in some species (Fig. 7G), internal to lateral s and homologous to d2 (Snider, 1967) in Lepidocyrtinae.
Abdomen IV (Fig. 12A)
Only primary setae B5 and E3 and secondary seta M are always mac in adults. The development of the above examined three species shows that only primary seta B4 may develop into mac between columns A and T on anterior part; seta B3 is always a mic. A mac occurs at 2nd instar between D2 and F2 at the position identical with that of E2 in the 1st instar larvae of Seirinae and Lepidocyrtinae, so that we consider it homologous to E2; at the same instar or subsequent instars, a seta posterior to E2 appears, as a mic (Fig. 9B-C) or as a mac with socket smaller than that of E2 (Fig. 8C-D). Therefore, seta ‘B3’, ‘E2a’ and ‘E2’ in Szeptycki’s figures should be respectively corrected as ‘M’, ‘E2’ and ‘E2p’.
In Szeptycki’s illustrations, A3 and B3 have more probabilities to develop into mac than other setae on anterior part. The above viewpoint grounds on the fact that primary mic have more probabilities of transformation into mac than secondary mic in most examined species, and thus results that two mac present at 2nd or 3rd instar on anterior part are considered to be the transformation of mic ‘A3 and B3’. However, we find that mic A3 and B3 never develop into mac at 2nd and subsequent instars. The relative position particularly their position in relation to s-chaetae may help to understand their homology here. For example, mic A3 in S. curviseta (Fig. 8) at 1st instar locates slightly externally to A2 and closer to midline, with 3 neighbouring s-chaetae around it, anterior one between A2 and B2, external one posterior to B2, and posterior one between A3 and A4; at 2nd instar, the position of A3 in relation to all other closer setae would change if A3 is transformed into mac and moves nearby, and thus a secondary mic would occur at the original location instead of mic A3. Compared to the previous idea, another hypothesis, that is the unchanging mic A3 and additional mac I, performs much better and more reasonable here. Similarly, mac M is an additional one rather than primary B3. The sharp displacement of setae (A3 and B3) in neighbouring two instars (short time) seems unimaginable. The further affirmance could be demonstrated in species having longer distance between A3 and I.
The sharp movement of B4 and B5 in some species often brings confusion to the recognition of their homology. In S. curviseta (Fig. 8), mac B4 and B5 don’t obviously move for life, usually located at the general place as those in most Entomobryini and Willowsiini species. Compared to S. curviseta, B4 in C. tenebricosa and C. aokii moves antero-externally, resulting in the position beyond bothriotrichum T2; B5 transfers antero-internally, often beyond A4. In Coecobrya lanna Zhang et al., central pattern in most specimens is similar to S. curviseta, with slightly forward movement of B5; whereas in a few specimens, B4, B5 and the short s associated with B5 exhibit strongly forward movement so that seta B4 is close to the alignment of B3 and M (Fig. 10C). In a few extreme examples, the forward movement of B4 and B5 results in B4 aligning with I and C1. Chen and Christiansen (1993; 1997), Chen et al. (2002, 2005) and Qu et al. (2007) illustrated many patterns on setal arrangement of central and lateral parts; homology of these patterns are re-examined, some new patterns or explanations also provided here. The exceptional case, with numerous mac on Abd. IV, is not included in the new patterns for the uncertain homology of some setae.
We concentrate on the changes of primary setae in central macrochaetotaxic patterns; those patterns with the addition of a few secondary mac are included as the variety of primary patterns (Fig. 11). Thirteen basic patterns are found in both genera (Table 9). The Pattern III* defined by Chen and Christiansen (1993), in fact, is identical to their Pattern II*, with the sharply forward movement of mac B4 and B5; therefore, the Pattern III* of Chen and Christiansen should be cancelled. The newly defined Pattern III shown in Table 9 is displaced by the Pattern II-A* of Chen and Christiansen, which has mac B6 instead of mic B6 in the Pattern II*. The Pattern IV-A* is homologous to V*, with the forward movement of B5 in the former. Two varieties of Pattern I are provided here (Fig. 11), I-A with a mac of unclear homology internal to I; I-B, homologous to Patterns X* and X-A* of Chen and Christiansen, with a mac Ae7 added.
The lateral chaetotaxy is also of great taxonomical importance, with 14 patterns found (Table 10). Our re-examination of Pattern IV-A* indicated that the original figure was mistakenly drawn; the revised figure is designated as Pattern VIII, with the presence of mac E3 and mic E4. Six new patterns (IX-XIV) are added; mac F3a in Pattern XII is discovered for the first time.
The number and position of s-chaetae are only roughly symmetrical between the two sides of the same specimen (only one specimen of C. similis exhibites perfect symmetry in our material). Microsensillum is absent on Abd. IV. Most s on this segment are much longer (usually more than 2 times) than those on other segments. At least 2 (usually 2) s, are distinctly shorter than others and have normal length; one is the most postero-lateral one (ps), which always occurs external to T7; another one associated with B5 always occurs external to B5, but its position is more or less variable between species and its homology with ‘as’ in Lepidocyrtinae is unclear (Fig. 8-9-10-11). The cases with more short s are observed in some New Caledonia species (Fig. 10D). The only exception is found in S. sp. A, with more than 40 s of normal length but no obvious differentiation among them.
Abdomen V (Fig. 13I)
Most setae drawn in Fig. 13I are not mac in adults, but their sockets are obviously larger than those of ordinary additional mic. The setal number is extremely variable between species. Five sets are defined by Szeptycki (1979). A seta often present external to a3 in adults and named m2a here, is added to the set m2+, with its socket often larger than a3. The lateral two setae of the set m5+ are respectively corrected as a6 and a6a instead of ‘m5e’ and ‘a6’ named by Szeptycki in the light of the relative distance between m5 and a6. A secondary seta antero-external to a5 is also often observed, designated as a5a. Additional seta P0 always occurs in adults. Seta p4p is often overlooked for its socket is subequal to those of ordinary mic and obviously smaller than those of other setae of the set p4p+. The seta el newly added to Szeptycki’s figure is not observed for the first time in Entomobryidae; Deharveng (1979) drawn a seta posterior to ap6 and pp6 in Lepidocyrtus cf. lanuginosus (Gmelin, 1788) but without any nomenclature.
The chaetotaxy of Abd. V is usually overlooked in the description of entomobryid species except some figures in Szeptycki’s monograph. The present work exhibits high diversity of chaetotaxy on Abd. V among Sinella and Coecobrya species. The chaetotaxy of Abd. V provides a new powerful tool for the taxonomy of the two genera, possibly most entomobryid genera.
The movement of some sets (sometimes partial setae of the set) occur in some species. In C. lanna (Fig. 13E), both sets p4a+ and p4p+ move forward, with setae p3a and p4a beyond m2 and m3, and set p4p+ extremely close to p3+. The forward movement of the set p3+ in C. similis almost results in the mixture of the sets p4a+ and p3+ (Fig. 13F).
The reduction of the sets p4a+ and p4p+ is also of taxonomical importance. In C. sp. E (Fig. 13G), p3a and p4a of the set p4a+ and nearly the whole set p4p+ except p3pi are absent or develop into only ordinary mic, whose sockets are not obviously differentiated. The complete set p4p+ is absent in C. similis (Fig. 13F). Only one seta p1p occurs in set p4p+ in C. aokii (Fig. 13D).
There are 3-5 (usually 3) s present on Abd. V, anterior one (as) close to m2 and a3, the middle s internal or antero-internal to p4, the lateral s anterior to p5 (usually internal to m5). A fourth s antero-internal to p3 appears in S. sp. F, while the lateral s moves externally, located externally to m5 (Fig. 13H). Five s are observed in S. sp. A, with the sharp modification of each set.
The S-chaetotaxy has highly intraspecifical stability and interspecifical diversities in number and position. The formulae of s-chaetae (including both s and ms) on half terga from Th. II to Abd. V are 3, 2/ 2, 2, 2(3), ?, 3(4-5), and ms as 1, 0/1, 0, 0(1), 0, 0. The complete s-chaetotaxy of Abd. IV is difficult to observe for the frequent loss of s-chaetae on Abd. IV during specimen preparation; however, the rough range of s-chaetae given in the description could provide relevant useful information. The variety of s-chaetae on each tergite has been already discussed in the above text.
Comments on existing systems
Most nomenclature on tergal setae of Jordana and Baquero’s (2005) system was identical to Szeptycki’s original designations; that is, both their system and our system were derived from Szeptycki’s system. However, they designated the different names without any explanation for the modification and didn’t give the reason why their system was better. For example, the homologization of a4, a5 and m5 on Th. III has been established in Szeptycki (1979), and our present study in Sinella-Coecobrya also affirms his work, whereas Jordana and Baquero still used ‘a4i, a4 and a5’ with m5 absent in their figures. It’s difficult for other collembologists to apply their system, whose rationale is completely unclear. The reconstruction of phylogeny in Collembola should be based on the most accurate transformational homology assessment. We believe that ontogenetic study of postembryonic development is superior to the study of adults alone (as in Jordana and Baquero’s study) as a method for assessing homology of chaetotaxic characters.
Szeptycki’s system has strict principles and detailed explanations for most mac of each terga, and is therefore very useful at species level. The main flaw, as he wrote in his own book, is that the examined species were too few to cover all the cases. Our present study focuses on the revision of homology of the tergal setae in Sinella and Coecobrya and provides more evidence for his hypotheses, and our system is essentially a revised Szeptycki’s system under strict rationale. Because of the lack of sufficient information on Entomobrya, we can’t compare Szeptycki’s system and ours to Jordana and Baquero’s system in detail before the postembryonic development of Entomobrys spp. is studied. A more comprehensive revision of chaetotaxic homology across Entomobryidae should be made using the ontogenetic approach.
The primary setae are almost identical in all entomobryid species, even in the adult chaetotaxy (Szeptycki 1972). Our study of the Sinella-Coecobrya group also demonstrated this point. Further observation of more species in the same group shows strong constancy during postembryonic development. However, the absence of few primary setae in C. tenebricosa and C. aokii exhibits the variation in the 1st instar chaetotaxy of Entomobryidae, at least on Abd. I and II. It seems that the classification of genera or species using chaetotaxy of 1st instar larvae is almost impossible, although it may be possible at tribal or subfamilial level. The larval chaetotaxy could be used for the systematics of high taxa in Entomobryomorpha, where the phylogeny of most families or subfamilies is still unclear.
Szeptycki (1979) made an important advance in the construction of a nomenclatural system for primary and additional setae of representative genera of Entomobryoidea (mainly for Entomobryidae). The greatest difficulty in widely applying his system is in the identification of setal homologies although Szeptycki (1979) provided some larval chaetotaxy; the displacement and transformation of tergal setae between genera are often difficult to trace. Soto-Adames’ (2008) work on Seira showed some distinct differences from Szeptycki’s work (1979) on this genus. Our study of the Sinella-Coecobrya group also modified some of Szeptycki’s plan. Although all the mac in adults could be theoretically named by Szeptycki’s principle, the transformational homology of setae occurring at early instars is easier to establish than that of setae appearing later.
Homologization of all mac is impossible to achieve even among closely related species. For this reason, we focus the homology of the setae that appears at early instars, which are generally considered most important in taxonomy. Ontogenetic studies of setal homology should be expanded across Collembola.
The S-chaetotaxy usually remains stable at species level and perhaps has moderate variability in most entomobryid genera. The limited information in earlier literature indicates that S-chaetotaxy may be useful in the taxonomy of high taxa rather than in species level in Entomobryidae, as is the case in Isotomidae.
Chaetotaxy of Abd. IV
The chaetotaxy of Abd. IV, which is the most complicated among those of all terga in Entomobryidae with the sharp elongation of Abd. IV, is of extreme taxonomical importance in Sinella and Coecobrya (Chen and Christiansen, 1997). The key revision of setal homology on Abd. IV in the present study is I and M, which occur at 2nd instar and usually develop into mac in adults. Our results show that partial primary setae don’t strongly move for life, i.e., they remain located in the same positions as those at early instars. The homology of A3 located in medial area in some entomobryid species is doubtful, probably homologous to secondary seta I. A mac antero-internal to bothriotrichum T2 occurs in most entomobryid species, even in Lepidocyrtinae (‘C1’). In Szeptycki’s monograph (1979), he named a seta anterior to T2 at 1st instar as ‘C1’ in two Lepidocyrtinae species with absence of C1 on this figures; however, his ‘C1’ should be labeled as T1 compared to Entomobryinae species; the early work of Barra (1975) exhibited complete set in P. impediens with the presence of C1, whereas Barra’s figures of 2nd instar showed the seta anterior to T2 is a secondary seta instead of primary seta ‘C1’. The similar nomenclature of anterior setae on Abd. IV in Soto-Adames’ (2008) work is also doubtful. The accurate homology needs to be further explored in a broader scope and compared between genera and higher taxa in Entomobryidae.
The present study was supported by the Ministry of Science and Technology of the People’s Republic of China (2006FY120100) and the National Natural Science Foundation of China (30771704, 40801096).
Received: 21 June 2010
Revised and accepted: 9 February 2011
Published online: 26 September 2011
Editor: J.A. Miller
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Species list and related deposit and collection information (present study).
Coecobrya akiyoshiana Yosii, 1956, Natural History Museum (Geneva), Japan (Akiyoshi)
Coecobrya aokii Yoshii, 1995, NJU, Vanuatu (Espiritu Santo, River Saranata)
Coecobrya communis Chen and Christiansen, 1997, NJU, China (Anhui, Chuxian)
Coecobrya guanophila Deharveng, 1990, MNHN, Thailand (Changwat Chiang Mai: Amphoe Chiang Dao, Tham Chiang Dao)
Coecobrya huangi Chen and Christiansen, 1997, NJU, China (Tibet, Zadaqusongbigong)
Coecobrya indonesiensis Chen and Deharveng, 1997, Museum Zoologicum Bogoriense (Bogor), Indonesia (Propinsi Sulawesi Selatan, Bone-Watampone)
Coecobrya ishikawai (Yosii, 1956), Natural History Museum (Geneva), Japan (Kreis Koti, Kusaka Mura, Saruta Do)
Coecobrya lana Zhang, Deharveng and Chen, 2009, NJU, Thailand (Changwat Chiang Mai: Amphoe Chiang Dao, Doi Chiang Dao)
Coecobrya liui Wang, Chen and Christiansen, 2002, NJU, China (Qinghai, Laoye Mountain)
Coecobrya magyari Chen, Wang and Christiansen, 2002, NJU, Hungary (Páter K. u. l., Gödöllö)
Coecobrya mulun Zhang et al., 2010, NJU, China (Guangxi, Huanjiang)
Coecobrya oligoseta Chen and Christiansen, 1997, NJU, China (Jiangsu, Nanjing)
Coecobrya similis Deharveng, 1990, MNHN, Thailand (Changwat Chiang Mai, Amphoe Chiang Dao, Ban Tham)
Coecobrya tenebricosa (Folsom, 1902), NJU, France (Paris)
Coecobrya tetrophthalma Denis, 1948, MNHN, Vietnam (Lam Dong, Dalat, Lang Bian)
Coecobrya tibetensis Chen and Christiansen, 1997, NJU, China (Tibet, Jilongtuodang)
Coecobrya tropicalis Qu, Chen and Greenslade, 2007, NJU, Australia (Learmonth Limestone Lease, Cape Range)
Coecobrya tukmeas Zhang, Deharveng and Chen, 2009, NJU, Cambodia (Kampot, Tuk Meas)
Coecobrya 2 spp., NJU, China (Guangxi)
Coecobrya 5 spp. (sp. E included), MNHN, Vietnam
Coecobrya sp., MNHN, Thailand
Coecobrya sp. B, MNHN, Thailand (Chaiyaphum, Nong Bua Daeng, Tham Keaw)
Coecobrya sp. D, MNHN, New Caledonia (Kaala-Gomen)
Sinella affluens Chen and Christiansen, 1993, NJU, China (Anhui, Chuxian)
Sinella browni Chen and Christiansen, 1993, NJU, China (Anhui, Yellow Mountain)
Sinella christianseni Ma and Chen, 1997, NJU, China (Anhui, Shitai)
Sinella colorata Zhang et al., 2010, NJU, China (Guangxi, Huanjiang)
Sinella curviseta Brook, 1882, NJU, China (Jiangsu, Nanjing)
Sinella fuyanensis Chen and Christiansen, 1993, NJU, China (Jiangzi, Ruichang)
Sinella insolens Chen and Christiansen, 1993, NJU, China (Jiangsu, Yixing)
Sinella plebeia Chen and Christiansen, 1993, NJU, China (Anhui, Yellow Mountain)
Sinella qufuensis Chen and Christiansen, 1993, NJU, China (Shandong, Qufu)
Sinella quinocula Chen and Christiansen, 1993, NJU, China (Anhui, Chuxian)
Sinella samueli Chen, Leng and Greenslade, 2005, NJU, Australia (South Australia, Mountain Wood)
Sinella sexoculata (Schött, 1896), Grinnell College, USA (California, Berkeley and Alamenda)
Sinella sineocula Chen and Christiansen, 1993, NJU, China (Jiangsu, Yixing)
Sinella termitum Schött, 1917, NJU, Australia (Queensland, Ravenshoe)
Sinella triocula Chen and Christiansen, 1993, NJU, China (Jiangsu, Nanjing)
Sinella trogla Chen and Christiansen, 1993, NJU, China (Guangxi, Guilin)
Sinella umesaoi Yosii, 1940, NJU, China (Jilin, Changbai Mountain)
Sinella wui Wang and Christiansen, 2000, NJU, China (Qinghai, Xining)
Sinella whitteni Zhang and Deharveng, 2009, NJU, China (Guangxi, Yachang Nature Reserve)
Sinella 9 spp. (sp. A included), MNHN, China (Guangxi and Sichuan)
Sinella sp., MNHN, New Caledonia (Lifou island)
Sinella sp. C, MNHN, New Caledonia (Hienghène, Mont Panié)
Sinella sp. F, MNHN, New Caledonia (Bouloupari, Mont Do)
Fig. 1. A) Symbols used in the figures. B-E) Chaetotaxy of Th. II in S. curviseta: B) 1st instar, C) 2nd instar, D) 3rd instar and E) adult. F) Adult chaetotaxy of Th. II in C. tenebricosa.
Fig. 2. A) Adult chaetotaxy of Th. II in C. aokii. B) A diagram of the final chaetotaxy of Th. II in both genera.
Fig. 3. A-D) Chaetotaxy of Th. III in S. curviseta: A) 1st instar, B) 2nd instar, C) 3rd instar and D) adult. E-H) Chaetotaxy of Th. III in C. tenebricosa: E) 1st instar, F) 2nd instar, G) 3rd instar and H) adult.
Fig. 4. A-C) Chaetotaxy of Th. III in C. aokii : A) 1st instar, B) 2nd instar and C) adult. D) Adult chaetotaxy of Th. III in C. sp. D. E) A diagram of the final chaetotaxy of Th. III in both genera.
Fig. 8. Chaetotaxy of Abd. IV in S. curviseta: A) 1st instar, B) 2nd instar, C) 3rd instar and D) adult.
Fig. 9. A-C) Chaetotaxy of Abd. IV in C. tenebricosa: A) 1st instar, B) 2nd instar and C) adult. D) Primary chaetotaxy of Abd. IV in C. aokii.
Fig. 10. A Chaetotaxy of Abd. IV in C. aokii: A) 2nd instar and B) adult. C) Adult chaetotaxy of Abd. IV in C. lanna. D) Adult chaetotaxy of Abd. IV in S. sp. F.
Fig. 12. A) A diagram of the final chaetotaxy of Abd. IV in both genera (few exceptional cases excluded). B-E) Chaetotaxy of Abd. V in S. curviseta: B) 1st instar, C) 2nd instar, D) 3rd instar and E) adult.