Phylogenetic relationships between the families of recent Thysanoptera (Insecta)

Zoological Journal of the Linnean Society, 69: 1 11-14 1. With 43 figures June 1980 Phylogenetic relationships between the families of recent Thysanoptera (Insecta) L. A. MOUND British Museum (Natural History), Cromwell Road, London S W7 5 BD B. S. HEMING Department of Entomology, University of Alberta, Edmonton, Canada AND J. M. PALMER British Museum (Natural History), Cromwell Road, London S W7 5 BD Accepted for publication July 1979 One family, the Phlaeothripidae, is recognized in the suborder Tubulifera, whereas extant species of Terebrantia are classified into seven families : Uzelothripidae, Merothripidae, Aeolothripidae, Adiheterothripidae. Fauriellidae (stat. n.), Heterothripidae and Thripidae. A phylogenetic analysis of the relationships between these families is given, based on consideration of 35 imaginal characters; however, the relationships of Uzelothripidae and Phlaeothripidae to the rest of the Thysanoptera remain equivocal. The Phlaeothripidae are either derived independently from Protothysanoptera, or else are the sister-group of the Thripidae, the most specialized family of Terebrantia. Diagnostic characters, diversity, distribution and relationships of each family are discussed. Keys to family and, in Fauriellidae, to genus are provided. Holarthrothnps Bagnall (= Adihetrrothrips Ramakrishna, syn. n.) and Oligothrips Moulton are removed from Heterothri idae to Adiheterothripidae and Fauriclla Hood, Opisthothrips Hood and Ropotamothrips Pefikan (= Osmanothnps Priesner, syn. n.) from Heterothripidae to Fauriellidae (stat. n.). These transfers leave Aulacothnbs Hood, Heterothrips Hood and Scutothrips Stannard as the only genera in Heterothripidae. KEY WORDS :-Systematics-cladistics-Tubulifera-Terebrantia-comparative anatomy. CONTENTS Introduction...................... 112 Diagnostic characters.................... I 14 Tentorium..................... 114 Antennae...................... 1 14 Mouth parts..................... I 17 Ill 0024-4082/80/0601 I1 + 3 1$02.00/0 0 1980 The Linnean Society of London

112 L. A. MOUND ET AL Forewings....,.,,, Mesospinasternum...... Metanotum........ Tarsi,,....,,.. Abdominal tergo-pleurotergal sutures. Abdominal wing-holding setae... Abdomenofmale...... Abdominal sternites VII-VIII of female Tenth abdominal segment of female. Ovipositor........ Pupal cocoons...,,.. Life style......... Fossil history.....,.. Phylogenetic analysis....... Evolutionary origin of the Phlaeothripidae Hypothetical Protothysanopteran... Family classification...,... Key to families...,... UzelothripidaeHood, 1952,... MerothripidaeHood, 1914,... AeolothripidaeUzel, 1895.... Adiheterothripidae Shumsher Singh, 1946 Fauriellidae Priesner, 1949, stat. 8... HeterothripidaeBagnall, 1912... ThripidaeStephens, 1829.... PhlaeothripidaeUzel, 1895.,.. Acknowledgements...,,.. References............................................ _..................................... I.....................,. _...................................................................... _..................,........ i18 1 I8 120 120 120 121 121 121 123 124 125 125 125 126 128 133 133 133 135 13.5 136 136 137 138 138 139 139 140 INTRODUCTION Insects of the Order Thysanoptera are characterized by possession of a protrusible sac-like arolium at the apex of each leg (Heming, 197 l), and by their asymmetric punch and suck mouth-parts in which the mandible of the lefthand side only is developed (Figs 1-4) (Heming, 1978). Since the time of Haliday ( 18361, two suborders have been recognized : the Terebrantia, whose females have an external ovipositor of four saw-like valves, and the Tubulifera, in which the ovipositor is a flexible internal, but eversible structure. The Tubulifera includes a single family, the Phlaeothripidae, whereas extant Terebrantia are here classified into seven families : Uzelothripidae, Aeolothripidae, Adiheterothripidae, Fauriellidae, Heterothripidae and Thripidae. Phlaeothripids are abundantly distinct from all terebrants in numerous characteristics which are discussed extensively below. This constellation of characters, emphasizing the uniqueness of the family, reinforces the view of the Tubulifera as a distinct suborder and has even led some workers to consider the possibility of regarding the two groups as distinct Orders. Heming (1979) regarded the Tubulifera as probably arising from an early off-shoot of the stem group of Thysanoptera, and considered the Phlaeothripidae and Uzeiothripidae as the sister-group of the rest of the Thysanoptera. Wilson (1975) similarly considered (in diagrammatic form) the Phlaeothripidae and Merothripidae as an offshoot of the rest of the Thysanoptera. In contrast, Stannard (1957, 1968) considered the Phlaeothripidae the most highly evolved group of Thysanoptera, derived from the Thripidae - Panchaetothripinae; and Schliephake 8c Klimt (1979) also accept this view. If this were so, then the Thripidae and Phlaeothripidae would be regarded as sister-groups, and, although the Tubulifera would be a monophyletic group, the Terebrantia could not be so

FAMILIES OF THYSANOPTERA 113 M Figures 1 to 4. Heads of adult Thysanoptera (ventral aspect). Fig. I. Merothrips wiliiamsi (Merothripidae). Fig. 2. Melanlhrips juscus (Aeolothripidae). Fig. 3. Haplothrips verbasci (Phlaeothripidae). Fig. 4. Chilochrips pini (Thripidae). regarded. Hennig (1969) apparently subscribed to this view and indicated that the Terebrantia are probably paraphyletic, i.e., the diagnostic characters of the group would have been present in the common ancestor of all present-day Thysanoptera. Schliephake ( 19751, in pointing out this situation, concluded that the Aeolothripidae should be placed in one suborder (Aeolothripidea) and the rest of the Thysanoptera including the Phlaeothripidae in a second suborder (Thripidea).

114 L. A. MOUND Er AL The objective of the present paper is not only to examine the phylogenetic relationships of the seven families of Terebrantia, but also to investigate their relationships to the Phlaeothripidae. Discussions and analysis are limited to adult members of extant families because most characters cannot be studied on fossil specimens, and because juvenile members of too few taxa are known. Patterson 8c Rosen ( 197 7 1 discuss the phylogenetic methodology by which fossils may be classified with Recent organisms but at the same time treated in a different way. This methodology has yet to be applied to Thysanoptera. DIAGNOSTIC CHARACTERS Tentorium The tentorium varies in its degree of development among the families. It is most complete and best developed in uzelothripids and aeolothripids : the transverse bridge and posterior arms-connecting laterally with the head capsule-are stout, and the anterior arms are well developed (Figs 2, 6). A similar but less stoutly developed tentorium is visible in some merothripids (Damerothrips, Erotidothrips and Merothrips williamsi Priesner, Fig. 11 but most species of Merothrips have the tentorial bridge interrupted medially or else the tentorium is considerably reduced and difficult to evaluate. In adiheterothripids (Holarthrothrips and Olzgothrips), the tentorial bridge is developed together with slender posterior arms, but only the bases of the anterior arms are visible. Finally in heterothripids, fauriellids, thripids (Fig. 4) and phlaeothripids (Fig. 3) no tentorium is developed apart from rudiments of the anterior arms to which the extrinsic antennal muscles are attached (Heming, 1975). Presence of a fullydeveloped tentorium has to be regarded as a plesiotypic character because it is found in a fully-developed state in representatives of all more generalized insect orders, including the Psocoptera (Kim 8c Ludwig, 1978). However, absence of a tentorium is clearly subject to ambivalence in interpretation (see Hecht, 1976). Either the tentorium has been modified progressively during evolution of the Thysanoptera and lost only once, if so, the thripids and phlaeothripids are closely related; or else the tentorium has been lost more than once, if so on this evidence these two families may be more distantly related. Antennae The plesiotypic number of antennal segments in Thysanoptera appears to be nine, although Scaphothrips antennatus Strassen, from Cretaceous Amber, has ten. Multiple division of the terminal antennal segment found in some fossils (Mound, 1968; zur Strassen, 1973) is not accepted here as true segmentation any more than the multiple division of the maxillary and labial palpi in some Aeolothripidae is accepted as segmentation (Mound, 1967). Nine-segmented antennae are found in merothripids (Fig. 12) (eight in the genus Merothrips, Fig. 11 ). adiheterothripids (Fig. 241, fauriellids (Fig. 13) (eight in Opisthothrips), heterothripids (Fig. 211, aeolothripids (Figs 14-16) and a few thripids. In contrast, uzelothripids (Fig. 10) have seven-segmented antennae, and representatives of most species in the two largest families, Thripidae (Figs 19, 20) and Phlaeothripidae (Figs 17, 181, have seven or eight-segmented antennae.

FAMILIES OF THYSANOPTERA Figures 5 to 9. Uzelothrips scabrosus (Uzelothripidae). Fig. 5. Head and pronotum of macropterous 9 (dorsal). Fig. 6. Head (dorsal aspect showing tentorium). Fig. 7. Forewing. Figs 8, 9. Sternites VIII-X (8, 9 with egg). Antenna1 segments III-VIII frequently bear rings of sculpture each carrying a row of rnicrotrichia (Figs 13-16, 19, 21-24). However, in the genus Merothrips only M. williamsi Priesner shows this ornamentation, and in phlaeothripids it is always undeveloped. In merothripids and fauriellids sensoria on the third and fourth antenna1 segments are transverse, band-like, pale areas, which even at their greatest

n f 3 7 abstract/69/2/111/2658699

FAMILIES OF THYSANOPTERA 117 15). Sensoria of heterothripids are continuous porous bands, transverse in most members of Heterothrips (Fig. 21, but see Fig. 23) but convoluted in Aulacothrips (Fig. 26) species, wrapping completely around segments three and four. In contrast, sensoria of members of other families are emergent trichomes (Figs 10, 17-20) although these could have been derived from the Merothrzps condition through an intermediate stage such as is found in adiheterothripids (Fig. 24). The trichomes of phlaeothripids (Figs 17, 18) are unbranched as are those of adiheterothripids (Fig. 24) and some panchaetothripines, whereas the trichomes of most higher thripids are forked (Fig. 19). The plesiotypic number of sensoria is evidently one on each of segments three and four, although members of both Orothrips (Fig. 16) and Ekplectothrips (Aeolothripidae) have two sensoria on both segments. Phlaeothripids frequently have three or four sensoria on both of these segments (Figs 17, 18) but the plesiotypic condition in this family is probably one sense cone on the third segment, and three on the fourth. In this connection it is interesting to note that some panchaetothripines (Anisopilothrips, Astrothrips, Dinurothrips) have an elongate and thin-walled seta on antenna1 segment four, with an enlarged base and looking like a second trichome. Mouth parts The plesiotypic condition of the maxillary palpi appears to involve three segments (Figs 1, 2, 4) with reduction to two segments in phlaeothripids (Fig. 3) as well as in some thripids and fauriellids. In some aeolothripids, the distal palpal segment is variably subdivided into six small units (Mound, 1967) but these do not appear to be homologous with true segments. The labial palpi are primitively two-segmented (Figs 1-41, but again in some aeolothripids the distal segment is subdivided. The plesiotypic condition of the mandibular and paired maxillary stylets is regarded as being short and retained within the mouth cone (Figs 1, 2). In aeolothripids and some thripids the mouth cone, and hence also the stylets, is elongate but the stylets are still retained within the mouth cone (Fig. 4). However in many phlaeothripids (Fig. 3), the stylets are elongate and deeply retracted into the head, in members of many taxa reaching the compound eyes and in a few even arranged into coils (Mound, 1970). The increasing length of the mouth cone and stylets result in an extreme opisthognathous condition in many phlaeothripids. However increased length of stylets in some aeolothripids and thripids (Fig. 41, without these stylets being retractable into the head capsule, results in increased asymmetry of the mouth cone and clypeofrons. In the phlaeothripids, the mandible is arched at its base (Fig. 3) whereas in terebrants the mandible is relatively straight (Figs 1, 2, 4). The difference is correlated with differences in musculature and in mode of operation of this stylet. In terebrants the head is nodded during mandibular protraction and retraction and the mouth cone is foreshortened by a group of muscles whose homologues are absent from the head of phlaeothripids (Reyne, 1927; Heming, 1978). Moreover, the maxillary levers in phlaeothripids appear to originate on the genal wall of the head capsule outside the mouth cone (Fig. 3) instead of articulating with the stipital lobes of the maxillae as in all terebrants (Figs 1, 2, 4), thus allowing the deeper retraction of these stylets dorsal to the brain (Reyne, 1927; Mickoleit, 1963). The large mandibular gland of terebrants (Rider, 1957) appears to be absent from

118 L. A. MOUND ET AL. phlaeothripids (Heming, 1978). The cibarial pump of phlaeothripids is smaller than in terebrants, having lost the first and fourth clypeo-epipharyngeal muscles, but apparently functions more efficiently (Figs 1-4) (Heming, 1978). Forewings The broad forewing with several cross veins, typical of aeolothripids, has generally been assumed to be the most plesiotypic wing condition in Thysanoptera. Mound & O Neill (1974) point out the lack of evidence for this assumption and suggest that these broad wings may be related to the larger body size of many aeolothripids, the additional cross veins being a functional necessity for the larger area. The relatively narrow forewing of merothripids could equally well be considered the most plesiotypic. Sharov (1972) erected the family Karataothripidae for a single specimen from the Jurassic with broad forewings bearing a short fringe, but the thysanopterous nature of this specimen is not completely certain. Forewings of phlaeothripids exhibit a constellation of characters which can only be regarded as apomorphies : longitudinal veins absent, veinal setae absent, wing membrane with no microtrichia, and marginal cilia not arising from sockets. The forewings of all other thysanopterans, including uzelothripids (Fig. 71, exhibit the plesiotypic state of each of these four characteristics. This remarkable difference in wing structure is taken by other authors to reinforce the view that the Phlaeothripidae are so distinct they should be segregated to the separate suborder Tubulifera. However, Mound 8c O Neill (1974) suggest that the distal three-quarters of the wing in phlaeothripids is neogenic, not directly homologous with the wings found in the rest of the Thysanoptera. They reached this conclusion because of the essential uniformity, throughout the whole of the Order, of the bases of the wings including the wing coupling apparatus (Fig. 25). This apparatus is retained in many micropterous individuals, and it is suggested that the Phlaeothripidae evolved from micropterous, subcortical ancestors, the effective wings being new developments. The wings of Aulucothrips (Fig. 25) also appear to have gone through a rather similar evolutionary phase. The basal part of the wing is evidently homologous with that found in other Thysanoptera, and is particularly similar to that of Scutothrips peruuiunus (Hood). However the distal, parallel-sided part of the wings of Aulacothrips apparently lacks longitudinal veins and major setae, although microtrichia and socketed cilia are present. Ellington (19801, in discussing the functional significance of socketed wing cilia in Thrips, has indicated that it is difficult to regard the wings in the two suborders of Thysanoptera as homologous. Mesospinasternurn The mesospinasternum is well developed as a transverse, rectangular sclerite between the median coxae in members of Aeolothripidae, Adiheterothripidae, Heterothripidae and Fauriellidae. However this sclerite is not differentiated in merothripids, uzelothripids nor phlaeothripids, and although it is present in many thripids it is also absent from several genera of Panchaetothripinae. Stannard (1957) used this character to relate Phlaeothripidae to Panchaetothripinae, but its plesiotypic condition cannot be distinguished

FAMILIES OF THYSANOPTERA 119 Figures 25 to 29.- Heterothripidae. Figs 25-28. Aulucothrips dictyotus. Fig. 25. Base of wing. Fig. 26. Antenna. Fig. 27. Head. and pronotum. Fig. 28. Tergite IV. Fig. 29. Scutothrips peruuiunus, metanotum. satisfactorily. Possibly, the sclerite was differentiated for some functional reason when thysanopterans first evolved onto flowers from the leaf-litter habitat. It may have been lost once again in the leaf-inhabiting evolutionary line involving the Panchaetothripinae, and this could be interpreted as evidence supporting the view that this group gave rise to the subcortical ancestors of Phlaeothripidae. 8

120 L. A. MOUND ET AL. Metanotum Primitively, there appear to have been two metanotal sclerites, although these are broadly fused in Merothrips macropterae (Merothripidae). However, all phlaeothripids, as well as macropterous Uzelothrips and many apterous thripids, have only a single metanotal sclerite. This fusion and reduction is probably related to wing reduction, the posterior metanotal sclerite being poorly developed even in apterous aeolothripids, and the condition in phlaeothripids possibly supports the suggestion that this family has evolved from micropterous ancestors. The anterior metanotal sclerite usually bears a pair of median setae. These are near its posterior margin in merothripids (when present), aeolothripids, fauriellids (when present), adiheterothripids, heterothripids, and a very few thripids (e.g. Monilothrips-Panchaetothripinae; Synaptothrips-Thripinae). In most thripids, the median pair of setae arise medially or close to the anterior margin of the sclerite, and in phlaeothripids they arise medially but are frequently duplicated. This median position of these setae is consistent with the hypothesis that Phlaeothripidae are derived from panchaetothripine-like ancestors. Tarsi The tarsi are two-segmented in merothripids, aeolothripids, adiheterothripids, fauriellids, and heterothripids (Heming, 197 1 : figs 1-5). It appears reasonable to assume that this is their plesiotypic condition. Only in uzelothripids, thripids and phlaeothripids have the tarsi been reduced to one segment, although in the representatives of the latter two families this reduction has evidently happened on several occasions. Many phlaeothripids are remarkable in having 1-segmented fore tarsi but 2-segmented mid and hind tarsi. The apical margin of the distal tarsal segment on the fore leg is produced ventrally into a hook-like tooth (the hamus) in aeolothripids (except melanthripines), adiheterothripids, fauriellids and heterothripids, although it is usually rather small in members of the last named family. This hamus is presumed to be used to cut the silken pupal cocoon prior to adult emergence. However, in phlaeothripids, a similar hamus is developed slightly more ventrally on the tarsi of all three pairs of legs. This is probably an independent development associated with life in the sub-cortical habitat. Adult phlaeothripids lack the gland about the unguitractor apodeme which is found in thripids and aeolothripids (Heming, 197 1 : fig. 8); moreover, only adult phlaeothripids have a well developed, coiled, femoral gland in each leg (Heming, 197 1). Abdominal tergo-pleurotergal sutures In merothripids, a pair of pleurotergites and pleurosternites is developed on most abdominal segments, that is, the tergo-pleurotergal sutures are complete. However, amongst aeolothripids, only individuals of such genera as Melanthrips have these sutures present and then only weakly; all the more derived members of this family have their tergites and pleurotergites completely fused. In this characteristic, fauriellids resemble merothripids, and adiheterothripids resemble Melanthrips, but heterothripids, phlaeothripids and many panchaetothripines

FAMILIES OF THYSANOPTERA 121 (Thripidae) resemble higher aeolothripids. This sequence suggests that evolution may have resulted in progressive fusion of pleurotergites with the tergites. However, in higher thripids, this trend is reversed and the tergo-pleurotergal sutures are well developed. Abdominal wing- holding setae Adult phlaeothripid macropterae usually bear one or more pairs of sigmoid wing-retaining setae on the median abdominal tergites. The only other Thysanoptera to bear similar setae are members of a group of small genera in the Thripidae - Panchaetothripinae : Dinurothrzps, Hoodothripoides, Sigmothrips (Fig. 4 1) and Tryphactothrips (Wilson, 19751, although the tergites of Aulacothrips (Heterothripidae) also have a group of setae apparently used for wing holding (Fig. 28). Abdomen of male In more specialized Thysanoptera the sternites of the male often bear glandular areas or areae porosae (Bode, 1978). Male Heterothripidae have these structures on most sternites, although in males of Opisthoth~ps (Fauriellidae) they are present only on VII-VIII. In males of these two families as well as in Adiheterothripidae, the glandular areas are anterior to the sternal antecostal ridge. Male Thripidae have glandular areas on the median sternites frequently (rarely only on I1 or 1111, always posterior to the antecostal ridge, whereas male Phlaeothripidae have them on sternite VIII (rarely VII and VIII). However males of some Phlaeothripidae (Adelothrips and related genera) also have reticulate glandular areas on the median sternites which do not seem to be homologous with areae porosae. The first abdominal tergite in males is normally a simple, transverse sclerite, essentially similar to other abdominal tergites. However in male Aeolothripidae, the first tergite is elongate with two longitudinal ridges, and in most phlaeothripids (of both sexes) the first tergite is reduced to a small median sclerite, the pelta. Males of Phlaeothripidae also differ from those of other families in having long, single follicled testes with the sperm arranged in many, longitudinally-disposed sperm bundles, and also in having four accessory glands (Heming, 1970b). Most male Thripidae transfer sperm within a spermatophore that is eventually lodged within the spermatheca of the female (Heming, 1970a). In contrast, phlaeothripid males apparently transfer sperm directly into the opening of the female spermathecal duct (Heming, 1970b). Priesner (1964) has given a comparative account of the male external genitalia in Aeolothripidae, Thripidae and Phlaeothripidae. Unfortunately only a single, fully cleared, male uzelothripid has been available for the present study. The genitalia of this specimen have a well developed endotheca with paired rows of small spines and a chitinized aedeagus, however the 'primitive aedeagus' (Heming, 1970b) is apparently not developed. Abdominal sternites VII- VIZI of female Among the terebrantian families, only female Merothripidae retain a well developed eighth abdominal sternite (Mound & O'Neill, 1974). This is represented by a pair of large overlapping sclerites, each bearing two pairs of setae, in females

122 L. A. MOUND ET AL. 40 41.,,_- -_- Figures 30 to 41. Abdomens of female Thysanoptera. Figs 30-37. Sternite VII. Fig. 30. Opisthothrips elytropappi. Fig. 3 1. Fauriella natalensis. Fig. 32. Ropotamothrips buresi. Fig. 33. Heterothrips sp. Fig. 34. Oligothrips oreios. Fig. 35. Erotidothrips sp. Fig. 36. DamerothripJ gemmatus. Fig. 37. Anisopilothrips sp. Fig. 38. Sternites VII & VIII, Hoplandrothrips jauipes. Fig. 39. Tergite X, Merothrips tympanis. Fig. 40. Tergite X, Melanthrips sp. Fig. 4 1. Tergite VI, Sigmothrips aotearoana. of each of the three extant genera of the family, Damerothrips, Erotidothrips and Merothrips (Figs 35, 36). In Damerothrips females, the two pairs of setae arise medially on the sclerites (Fig. 36), whereas in the other two genera they arise near the anterior border (Fig. 35) (Mound & O'Neill, 1974). In all remale Aeolothripidae, there are two pairs of presumably homologous setae near the

FAMILIES OF THYSANOPTERA posterior margin of the seventh sternite (Mound, 1967), although these are readily confused with the sternal discal setae in females of many genera. Moreover, in females of other terebrantian families, it is not unusual for two pairs of minute (1-3 pm) setae or pores to be found in this same position (Figs 30-34, 371, although they are not present in those species of Heterothrips (Heterothripidae) which have a posteromarginal fringe of microtrichia. It is difficult to consider this character other than exhibiting a progressive reduction sequence from Merothripidae, through Aeolothripidae, to Fauriellidae and Thripidae. That is, the condition of sternite VIII in merothripids is with respect to that of the rest of the Thysanoptera - Terebrantia, an Rlesiotypic moreover the extreme reduction or absence of sternite VIII setae in fauriellids and thripids is apotypic with respect to the condition found in aeolothripids. The median area of sternites I-VI of Uzelothrips females (Uzelothripidae) is weakly sclerotized, but there are three pairs of small posteromarginal setae present on each sternite. Sternite VII (Figs 8, 9) is uniformly sclerotized with two pairs of posteromarginal setae and one pair of median discal setae; the latter are probably homologous with the median pair of posteromarginal setae on the preceding segments. Sternite VIII is represented by a uniform area of membranous, finely striated cuticle which apparently surrounds the gonopore (Figs 8, 9). Thus neither sternite VII nor VIII in uzelothripids can be related to the sequence described above in terebrants. Female Phlaeothripidae have sternites 11-VIII remarkably uniform throughout the family, each with a posteromarginal series of elongate setae and a discal series of small setae (Fig. 38). Sternite VIII is directly comparable with preceding sternites, unlike those of all other Thysanoptera, although the posterior margin is often developed into a flange-like craspedum, the sub-genital plate (Heming, 1970a1, which bears one or more pairs of setae submarginally (Fig. 38). This subgenital plate may have some protective function during oviposition, and it is interesting to note that the posterior margin of sternite VII in females of some Thripidae - Panchaetothripinae ( AstrothTip~; Anisopilothrzps) has a similar structure (Fig. 37). Thus it is not possible to trace any homologies of the posterior abdominal sternites between females of Uzelothripidae, Phlaeothripidae and the terebrantian families. The condition found in merothripids can be regarded as plesiotypic to the rest of the Terebrantia; but the conditions of sternite VIII in uzelothripids and phlaeothripids cannot be determined readily as either apotypic or plesiotypic in relation to that found in merothripids. The presence of a series of eight equivalent sternites in the protothysanopteran, which would have been necessary if the phlaeothripid condition is plesiotypic, seems unlikely in view of the fact that sternite VIII is reduced in merothripids as well as in psocids which probably share a common ancestor with Thysanoptera (Hennig, 1969; Kim & Ludwig, 1978). An alternative view, as mentioned in the section concerning abdominal segment X, is the possibility that the phlaeothripid condition is the result of neoteny, although this requires the added complication of heterochrony in development of the genitalia. I23 Tenth abdominal segment of female Males and females of Merothripidae bear a pair of long trichobothria on the tenth abdominal tergite (Fig. 391, although these are reduced or absent from

124 L. A. MOUND ET AL. Merothrips brunneus and from apterae of M. mirus (Mound & O Neill, 1974). These trichobothria are also present in aeolothripids (Fig. 40) but are very reduced in members of the most derived genera such as Aeolothrips. Similar structures are not present in any other Thysanoptera. In female Phlaeothripidae the tenth abdominal tergite is more or less cylindrical, without any longitudinal division, the anus being at the apex of the tube, and the gonopore sited ventrally between sternites VIII and IX. Stannard ( 1957 1 postulated that this tubuliferous condition, so characteristic of the family, was related in some way to the elongate, semi-tubular condition of the tenth abdominal segment found in females of several panchaetothripine genera, although these thrips have a typically thripoid ovipositor. The larvae of Panchaetothripinae sometimes have a well developed tubular tenth abdominal segment, and the condition found in Phlaeothripidae could have been derived by neotenic retention of this characteristic. However, despite the attraction of this simple hypothesis, the fundamental differences between the structure of the genital segments in female Thripidae and Phlaeothripidae do not support it (see Heming, 1970a for additional differences). Ovipositor The large, upturned ovipositor of female Aeolothripidae has generally been regarded as primitive for Thysanoptera. No evidence appears to have been presented to support this view which seems to be derived from subconscious analogy to the Orthoptera. Paradoxically, most authors accept that the Thysanoptera share a common ancestor with the Psocoptera and Zoraptera, although Heming (1977) relates the latter group to the Isoptera and Dictyoptera. Mound & O Neill (1974) suggest that Thysanoptera evolved orginally as fungus feeders in detritus, under which conditions a large saw-like ovipositor would have been unnecessary. Moreover, if the merothripid condition of sternite VIII is accepted as plesiotypic to the aeolothripid condition, then the protothysanopteran presumably must have had a less well developed ovipositor than that of aeolothripids. The greatly enlarged, saw-like ovipositor, found in females of most Terebrantia, appears to be a functional necessity for laying eggs within the tissue of green plants, and can be interpreted as evidence for monophyly of this group. However, the ovipositor of female aeolothripids, and also of Erotidothrips (Merothripidae) curves upwards whereas that of Thripidae and the other families curves downwards, apparently resulting in a different orientation of the egg within the host plant tissue relative to the laying female. An alternative interpretation of these observations could be that the ovipo sitors in females of these two families represent parallel redevelopments from the plesiotypic condition in merothripids, that is, they represent alternative responses to the difficulty of ovipositing in plant tissue rather than evidence of close kinship. The ovipositor in female Phlaeothripidae is a delicate, eversible, chute-like structure which has a paired origin from the hind margin of sternite VIII (Heming, 1970a); hence the phlaeothripid progenitor must have possessed at least the anterior ovipositor valves. Female Terebrantia with a well developed ovipositor also possess a well developed accessory gland which is not found in phlaeothripids (Heming, 1970a).

FAMILIES OF THYSANOPTERA 125 Pupal coccoons Heming (1973) points out that known second instar larvae of Aeolothripidae, Adiheterothripidae, Heterothripidae and Merothripidae spin cocoons prior to pupation. Unfortunately nothing is known of the life history of representative Uzelothripidae and Fauriellidae, but cocoon spinning is not known in Phlaeothripidae, and is not strongly developed in most Thripidae although Odontothrips species produce a cell of soil particles held together with silk (Lewis, 1973). It seems likely, therefore, that coccoon spinning is a plesiotypic characteristic of Thysanoptera larvae, but has been lost from more advanced forms as the result of an increasing tendency to pupate on the host plant or under bark. Lye style The plesiotypic habitat of thysanopterans is presumed to have been leaf-litter, where they fed on fungal-hyphae (or hyphal breakdown products) and pupated in the soil. From this habitat, the group appears to have moved into flowers, the most obvious source of soluble nitrogen apart from plant meristems and other arthropods. The Fauriellidae and Adiheterothripidae are probably relict groups from this level of evolution, but Heterothrips and the Aeolothripidae are highly successful flower-living groups, both of which have retained the habit of pupating in soil. The Aeolothripidae have also produced numerous facultative (or even obligate?) predators, but none are known to feed on plant meristems or leaf tissue. Panchaetothripines are generally regarded as the most primitive of Thripidae (Stannard, 1957 ; Wilson, 19751, despite their structural apomorphies, and larvae and adults of all species in this subfamily apparently feed on exposed and expanded leaves, many pupating in situ. Thripines have a range of life styles, but the less specialized appear to be either leaf-feeding (Thripini -Aptinothripina) or associated with Gramineae (Chirothripini), and the most advanced are mainly flower-feeding (Thripini - Thripina) although members of a fav specialized genera have reverted to leaf feeding (Mycterothrips). Some of the more advanced thripids (Dendrothrips, Scirtothrips) feed on young leaves close to plant meristems, and Scolothrips species are obligate predators. Phlaeothripids exhibit all possible life styles although dorsoventral flattening of the body suggests they evolved initially as fungus feeders under bark. Individuals of one subfamily (Idolothripinae) feed on fungal spores; those of the other (Phlaeothripinae) include species which feed on fungi (in litter, on twigs, or under bark), lichens, mosses, flowers, mature leaves, young leaves (causing galls) and on other arthropods. Apart from those of spore-feeding species, the stylets do not appear to be modified for feeding on these different substrates (Mound, 197 1). Fossil history Most fossil specimens of Thysanoptera are too poorly preserved for serious analysis, and many important characters are not available for study on such material. Sharov (1972) has rejected Permothrips as a thysanopteran and placed this fossil in the homopterous family Archescytinidae; however, Karaotothrips

126 L. A. MOUND ET AL. jurarsicus Sharov is itself doubtfully a member of the Thysanoptera. The largest recorded sample of fossil specimens was the Baltic Amber inclusa studied by Bagnall (see Mound, 1968) and Priesner (1924, 1929). These authors described a total of 58 species from amber of the Oligocene Period (35-40 million years B.P.) with the following family distribution: Merothripidae, 2 ; Heterothripidae, 6; Aeolothripidae, 7 ; Thripidae, 33; and Phlaeothripidae, 10. Moreover, zur Strassen (1973) has recently described five new families placed in the Heterothripioidea on seven specimens from Cretaceous Amber of Lebanon (120-140 million years B.P.). If the Phlaeothripidae had evolved early in a subcortical habitat one might have expected a rather higher representation of them in amber. However amber inclusa probably reflect the aerial population of Thysanoptera of their period; they cannot be interpreted as giving sound evidence of total faunal diversity any more than an aerial sample could be used as a measure of the present day fauna. Fossil material therefore gives little evidence at present on family relationships within the Thysanoptera, and families known only from fossil material have been excluded from consideration. PHYLOGENETIC ANALYSIS Table 1 lists the characters discussed above together with their presumed plesiotypic and apotypic states. Table 2 gives the distribution of these character states throughout the eight families recognized here. Two families, the Phlaeothripidae and Thripidae, are evidently more highly derived than the other six and have the largest number of apotypic character states (see totals at bottom of Table 2). However this is not, in itself, evidence of a close relationship. According to orthodox principles of phylogenetic analysis (Hennig, 19661, in order to regard these two families as sister-groups it would be necessary to demonstrate at least one uniquely derived characteristic (or synapomorphy) which they have in common. This is discussed further below. The Merothripidae and Aeolothripidae are evidently closely related, and can be considered sister-groups because of the presence of an upturned ovipositor in females of Erotidothrips and Aeolothripidae (Figs 42, 43). Moreover, this pair of families appears to be the sister-group of the four families Adiheterothripidae, Fauriellidae, Heterothripidae and Thripidae (Fig. 43). The Adiheterothripidae, whose members retain a tentorial bridge, is probably a relict group (Figs 42, 431, and it is interesting to note that similar conical antenna1 sensoria (Fig. 24) are found in Thysanoptera from Lebanese (Lower Cretaceous) and Baltic (Oligocene) Amber. The Fauriellidae and Heterothripidae appear to be sistergroups, from the Old and New Worlds respectively, and together apparently constitute the sister-group of the Thripidae (Fig. 42). Relationships of the Uzelothripidae remain equivocal. Presence of a complete tentorium (Fig. 6) suggests that this family was not derived subsequently to the Merothripidae and Aeolothripidae, and the presence of a single metanotal sclerite as in Merothr$s species indicates the possibility of a sister-group relationship to this pair of families (Fig. 42). However, the wing structure of Uzelothrips scabrosus (Fig. 7) appears to be derived from that of other terebrants, and the family could represent a highly specialized relict offshoot from the Protothysanoptera (Fig. 43). It cannot be regarded as a subfamily of Thripidae and the sister-group of Thripinae as given in Ananthakrishnan ( 1979).

FAMI1.IF.S OF THYSANOPTERA 127 Table 1. Analysis of imaginal characters in Thysanoptera Character Plesio typ ic Character State Apotypic I. Tentorium 2. Dorsal ocelli 3. Antenna] segments 4. Sensoria on 111-IV 5. Antenna1 segment surface 6. Maxillary palpi 7. Labial palpi 8. Stylet length 9. 10. 1 I. 12. 13. 14. 15. 16. Wing cilia 17. 18. Mouth cone Mouth part symmetry Cibarial pump Mandibular stylet Forewing width Forewing longitudinal veins Forewing cross veins Forewing surface Mesospinasternurn 19. Metanotum 20. Metanotal median setae 21. Tarsal segments - complete (A) - 3 present (A) - 9, all separated (A) -transverse, linear 01 expanded (A) - annulae and microtrichia present on most segments (A) - 3-segmented (A) - 2-segmented (A) -short (A) - hypognathous (A) -almost symmetric, apart from absence of right mandible (A) -merothripoid (A) -straight (A) -intermediate (A) - 4 present (A) - 3 present (A) -straight, socketed (A) -with mirrotrichia (A) - transverse, rectangular (A) - 2 separate sclerites (A) - near posterior margin (A) (absent A') - 2 segments on all legs (A) -bridge missing (B) - bridge and posterior arms present (C') - only bases of anterior and posterior arms present (C2) -only bases of anterior arms present (D) -only 2 present (B) - reduced or variable (C) -absent (D) - > 9 (B) - 9, terminal segments close (C) - < 9 (D) -longitudinally linear (B) -conical (C') -linear, continuous around segment (Cz) -slender trichomes (D') - uzelothripine (D*) - annulae and microtrichia on reduced no. of segments (B) - annulae only (C) -glabrous (D) - >3 segments (BI - < 3 segments id) -> 2 segments (B) -intermediate (B, C) -long, restricted to mouth rone (D1) -long, retracted deeply into head (DZ) - opisthognathous (B, C, D) -intermediate (B, C) -highly asymmetric (D) - phlaeothripoid (D) -arched basally (D) -broader (BI-D') - narrower (Bz-D2) - < 4 present (B, C) - 0 present (D) - > 3 present (Bl, C1) - < 3 present (Bz, Cz) - 0 present (D) -wavy, sockrted (B, C) -straight, unsocketed (D) -intermediate (B, C) -without microtrichia (D) - intermediate (B, C) - simple transverse thickening (D) - 2 sclerites fused (B, C) - 1 srlerite with posteromarginal craspedum (D) - near middle of sclerite (B, C) -near anterior margin (D) - 1 segment on forelegs, 2 on others (C) - 1 segment on all legs (D)

128 L. A. MOUND ET AIL Table 1. continued Character Plesiotypic Character State Apotypic 22. Hamus 23. d glandular areas 24. external genitalia 25. accessory glands 26. Testes 27. 8 tergite I 28. Trichobothria on Q tergite X 29. Pleurotergal sutures 30. Ovipositor 3 1. Q sternite VIII -present on fore tarsi (A) -absent (A) - merothripoid (A) - 2 present (A) -elongate, with sperm in spermatodesms (A) -transverse (A) -well developed (A) -well developed (A) - psocopteroid (A) -present as two separate sclerites (A) 32. Spiracles - small; on meso- and metachorax, also abdominal segments I & VIII (A) 33. Tergal wing-retaining -absent (A) setae 34. Life-style -fungus feeding in litter (A) 35. Cocoon spinning by -present (A) larva 11 -absent from all tarsi (B) - present on all tarsi (C) -present in front of antecosta on sternites 2 (or 3) -8 (B) - present in front of antecosta on sternites 5-8 (B') - present in front of antecosta on sternites 7-8 (Bz) -present on sternites 3-7 or less, behind antecosta (C) -present on sternite 8 only (D) - melanthripine-(b) - aeolothripine-(c) - phlaeothripine4d') - uzelothripine-(dz) - 4 present (D) -short, with sperm singly disposed (D) -elongate (C) -reduced to pelta (D) -present but reduced (B, C) -absent (D) -present but reduced (B, C) -absent (D) -well developed, upturned (B', C') -well developed, downturned (BP, Cz) -membranous, protrusile (D') - phlaeothripoid (D') -secondarily psocopteroid (D3) -present, but fused to VII (B) -absent, but setae or pores present on VII (C) -absent (D') -present, structure similar to sternite VII (DP) -intermediate size (B, C) - peritremes enlarged (D) - intermediate (B, C) -present (D) -fungus feeding under bark (B) - phytophagous on leaves (C') - phytophagous on flowers (CP) -predatory (D) -cocoon weakly developed (B) -absent (C) ~ ~ ~ ~ (A) indicates plesiotypic state; (B),(C), etc., levels of derived character states. See Figs 42.43 and Table 2. Evolutionary origin ofthe Phlaeothripidae Many of the apotypic character states which are listed in Table 2 as shared among thripids and phlaeothripids involve reduction of pre-existing structures, e.g. loss of tentorium, fusion of antenna1 and palpal segments, loss of mesospinasternum and abdominal pleurotergites, etc. These synapomorphies, although suggestive of a relationship, are not as convincing as are shared,

Antenna/ FAMILIES OF THYSANOPTERA Table 2. Imaginal character states in recent families of Thysanoptera + Chorocter 1; ~ surface Moxillory polpi Labial polpi Stylet length Mourh ccme I29 Metonoturn Sprrocles life style A A K-. A- I A 1 A A A A,(C) A,C-D, A-D A A., A A,B C2 1 C,D C C C2 C,C2,D! A-D 3 7 A I ~ / A 7 A B,D,D Totolr Apotypic Chorocter 8.5 8. 2 c=2 CL 2 D=4 D : 1 la B;B B=l c= 4 fg6 D=4 D = 1-24 1 B=ll C=15 c: 2 cg 4 D=14 D : 3 D2= 1 DL 1 I - 51 8.4 C: 8 D: 2t D = 3 0 : 4 44 uniquely-derived characters (Hecht, 1976). For example, only thripids and phlaeothripids among the Thysanoptera have slender, emergent trichomes on the third and fourth antenna1 segments (Figs 17-20), and only phlaeothripids and members of certain genera of Thripidae - Panchaetothripinae have more than one trichome on the fourth segment. At first sight this appears to be strong evidence for a close relationship between Phlaeothripidae and Thripidae. However, thin-walled trichomes are found in many other groups of insects and could be considered as plesiotypic in the phlaeothripids. Apart from Aulacothrips individuals (Heterothripidae, Fig. 281, sigmoid wing-retaining setae are only

130 L. A. MOUND ET AL. TEREBRAN TIA I 1 - m TUBUL IFERA Character States U A r n B E 3 c r n D I 5,14,16,17,19,24 11,12,25 22 21 26 27 30,31 Figuie 42. Reconstructed phylogeny of the recent families of Thysanoptera, scheme A. Phlaeothripidae is shown as the sister-group of the Terebrantia and Uzelothripidae of the Merothripidae and Aeolothripidae.

FAMILIES OF THYSANOPTERA I TEREBRANTIA TUBUL IFERA in 0) 0 x._ 0. L f P 0) 0 a.- n L f - 0 $ 5" a 3 4,13 11,12,25,27 29 26 B 23 5.16 14 15,30 17 19 21 22.24 31 4 23 22 Character States I A r n B e c r n D Figure 43. Reconstrurted phylogeny of the recent families ol Thysanoptera, scheme B. Phlarothripidae is shown as the sister-group of the Thripidae and Uzelothripidae of the rest of the Thysanoptera. (Note: in this scheme the Plilaeothripidae is actually the sister-group of thr subfamily Panrhartothripinae of the Thripidae-see text for details.)

132 L. A. MOUND Er A[.. found in phlaeothripids and a few species of Thripidae - Panchaetothripinae (Wilson, 19751, and moreover these panchaetothripines resemble phlaeothripids in having their metanotal setae placed medially, their abdominal pleurotergites fused, and their tenth abdominal tergite relatively elongate and tubular (although fully divided longitudinally on the ventral surface). These apparent synapomorphies suggest a phylogenetic relationship between Panchaetothripinae and Phlaeothripidae, but if these are sister-groups then the Thripidae itself must be paraphyletic. For the purpose of Fig. 43 the Phlaeothripidae are regarded as sister-group to the entire Thripidae. However, in contrast to the above conclusion, phlaeothripids dif er from all other Thysanoptera in a number of characters which suggests that the family is independently derived from the Protothysanoptera, and is the sister-group of the rest of the Thysanoptera (Fig. 42). These characters include mandibular and maxillary stylet articulations, cibarial pump, wing structure, presence of complete sternite VIII in females, and the structure of the ovipositor, external male genitalia, testes and male accessory glands. Most of these characters do not form part of any transformation series which includes Thripidae, or any other terebrantian, although most of them, such as changes in the head, thorax and genitalia, appear to be important adaptations to the sub-cortical habitat and could constitute a functionally integrated character complex (Hecht, 1976). Thus, this phylogenetic analysis clarifies, but does not solve, the problem of the relationship between the Thripidae and Phlaeothripidae. Either, the Phlaeothripidae are independently evolved from an early offshoot of the Protothysanoptera, and the apparent synapomorphies with Thripidae are all due to convergence (Fig. 42). Or, the Phlaeothripidae are the sister-group of the Thripidae, and their unique characteristics are the result of adaptation to life under bark (Fig. 43). The suggestion that the Phlaeothripidae are independently evolved from the Protothysanoptera is open to the following objections : The remarkable homogeneity of members of the Phlaeothripidae, despite the large size of the family and the range of life histories involved, is not typical of an ancient group, particularly in the absence of relict species. The synapomorphies between Thripidae and Phlaeothripidae are not likely to be due to convergence because of differences in plesiotypic life-styles between members of these families. No phlaeothripids have 9-segmented antennae, nor bear trichobothria on tergite X, both of which are presumed plesiotypic characters for all Thysanop tera. A complete sternite VIII as in phlaeothripids, and a psocopteroid ovipositor as in merothripids are not both likely to be plesiotypic. The suggestion that the Phlaeothripidae are the sister-group of the Thripidae is open to the following objection: The many structural differences between the families suggest, in the absence of any transformation series, an example of saltational evolution for which it is doubtful if neoteny and heterochrony can account satisfactorily. As a result of the above observations, the phylogeny of the Phlaeothripidae remains obscure. No adult member of the family retains any characteristic which is definitely plesiotypic except for testicular structure in males, and so there is no

FAMILIES OF THYSANOPTEKA 133 hard evidence that the group has evolved independently from primitive Thysanoptera. On the other hand, present interpretation of structural differences suggests that evolution from a common ancestor with Thripidae is not possible. HYPOTHETICAL PROTOTHYSANOPTERAN Judging from our analysis of character states in Table 1, the protothysanopteran would have lived in leaf-litter, exhibited wing polymorphism and pupated in the litter within a loose cocoon spun from posterior glands in the abdomen of the second instar larva. Its head would have had a complete tentorium, 9- segmented antennae with annulae and microtrichia on all segments and with sensoria on I11 and IV as in Damerothrips, 3-segmented maxillary and 2- segmented labial palpi, and a short, hypognathous mouthcone symmetric except for the absence of the right mandible. The sucking mechanism would have been weakly developed and similar to that of Damerothrips. In macropterae, the wings would have been intermediate in width, with four longitudinal and three crossveins, straight but socketed fringe cilia, and the surface covered with microtrichia. All legs would have had two tarsal segments, the fore tarsi equipped with some kind of cocoon-cutter. Areae porosae would have been absent from the abdominal sternites of males, abdominal pleurites would have been well-developed in both sexes, the ovipositor would have been psocopteroid (as in Damerothrips) and tergite X would have borne two long trichobothria. Abdominal sternite VIII would have been present, well-developed, paired and separate from sternite VII. The male would have had two large, single-follicled testes each containing longitudinally-disposed sperm bundles and two pairs of accessory glands involved in production of a spermatophore. The female would have had two ovaries each of four panoistic ovarioles, a relatively small spermatheca, and would probably have lacked an accessory gland because of weak development of its ovipositor. FAMILY CLASSIFICATION The family-group classification of recent Thysanoptera proposed here involves re-arrangement of the generally accepted Heterothripidae into three distinct families-heterothripidae, Adiheterothripidae and Fauriellidae. Moreover, contrary to some recent workers, Uzelothripidae is retained as a distinct family. Key to families 1. Tergite X tubular in both sexes, with no ventral longitudinal division; wings, when present, with no longitudinal veins or veinal setae, wing surface without microtrichia, and wing fringe-cilia not arising from sockets; sternite VIII of 9 similar in structure and chaetotaxy to sternitevi1 (Fig. 38) (suborder Tubulifera)................. Phlaeothripidae - Tergite X not tubular, divided or incomplete ventrally; wings, when present, with longitudinal veins which usually bear setae, wing surface covered with microtrichia, wing cilia arising from sockets ;

134 L. A. MOUND ET AL. sternite VIII of 0 absent medially at least, if developed then differing considerably from sternite VII in structure and chaetotaxy (suborder Terebrantia)..................... 2 2. Sternite VIII of 9 developed as a pair of overlapping lobes each bearing a pair of setae (Figs 35, 36); tergite X usually with a pair of well-developed trichobothria on posterior margin (Fig. 39).................. Merothripidae - Sternite VIII of 9 not developed as a distinct sclerite; tergite X without, or with a pair of very small trichobothria (Fig. 40)..................... 3 3. Cephalic tentorium with a well developed transverse bridge (Fig. 2)..................... 4 - Cephalic tentorium reduced to bases of anterior (and sometimes posterior) arms, transverse bridge absent..................... 6 4. Only bases of anterior tentorial arms present; antennal segments I11 and IV each with a broadly based conical trichome (Fig. 24)................ Adiheterothripidae - Tentorium with both anterior and posterior arms well developed (Figs 2,6); sense organs on 111-IV not conical trichomes..................... 5 5. Antennae 9-segmented (Figs 14, 15, 16); 9 with a large upturned ovipositor of four saw-like valves; forewing broad with well developed cross veins................. Aeolothripidae - Antennae 7 -segmented (Fig. 10); 9 with ovipositor membranous and protrusible (Figs 8,9); forewing without cross veins, but with at least one longitudinal vein bearing small setae (Fig. 7).................. Uzelothripidae 6. Antennal segments 111-IV bearing slender, emergent, forked or simple trichomes (Figs 19, 20)................... Thripidae - Antennal segments 111-IV with sensory areas linear and encircling the segments..................... 7 7. Sensory areas on antennal segments Irr-Iv continuous around each segment, usually a simple, apical, porous band (Fig. 211, sometimes convoluted (Figs 23, 26)................. Heterothripidae - Sensory areas on antennal segments 111-IV not continuous around either segment (Figs 13,221.................. Fauriellidae

FAMILIES OF THYSANOPTERA 135 Uzelothripidae Hood, 1952 The single species of this family, Uzelothrips scabrosus Hood, was described from apterous males, and macropterous and apterous females collected in southern Brazil. Recently, however, Dr S. Okajima of Tokyo University has collected about 100 macropterous and apterous females, also one second instar larva, of this species in Singapore from dead twigs and litter (July-August). Moreover, one of the present authors (L.A.M.) has collected 23 female apterae and 8 larvae of this genus at four sites in Singapore about 4.8 km apart (15 January 1979). Unfortunately, the body structure, including the antennae (Fig. 101, is so highly specialized that the relationships of Uzelothrips remain conjectural. Since the tentorium is more fully developed than that in any other Thysanoptera (Fig. 6) the genus may well represent an early but highly aberrant and specialized offshoot from the protothysanopteran (Fig. 43) or the sister-group of the Merothripidae and Aeolothripidae (Fig. 42). Mound & O Neill (1974) as well as Heming (1979) suggest a close relationship to the Phlaeothripidae, but this is contrary to evidence provided by the tentorium. Wilson ( 1975 : 13) considered the forewing to be Liothrips-like, but unlike that of any phlaeothripid (and contrary to Wilson, 1975: 201) the wing of Uzelothrips has a well developed marginal (? costal) vein extending the full length of the wing (Fig. 7). Moreover this vein bears four small (6 pm) major setae along its length (as well as two large setae with expanded apices near the wing base), the surface bears numerous microtrichia, and the marginal cilia arise from sockets (Fig. 7). Thus there is no evidence for relating Uzelothripidae to Phlaeothripidae apart from lack of an external ovipositor, and even this does not necessarily indicate a relationship because the genital opening of female Uzelothrips (Figs 8, 9) appears to be quite unlike that of Phlaeothripidae (Heming, 1970a). Wilson (1975) considered Uzelothrips to be related to Kurtomathrips (Thripidae) whose members have a remarkably similar general appearance and body sculpture, but have a fully developed ovipositor, the tentorium reduced to the bases of the anterior arms and other characters as in other thripids. Merothripidae Hood, 1914 About 15 species in three Recent genera are recognized in this family. Damerothrips gemmatus Hood and most Merothrips species are known only from the Neotropics, although Erotidothrips mirabilis Priesner and several Merothrips species are widespread but uncommon throughout the tropics, possibly being introduced by man. Mound 8c O Neill (1974) suggest that the Merothripidae represent the most primitive of extant Thysanoptera, producing as evidence in support of this the structure of abdominal sternite VIII of females in comparison with that found in members of other families (Figs 35, 36). However, the other diagnostic characters discussed above can also be interpreted as being consistent with this hypothesis. The three genera in the family are divergent in structure of the head and thorax. However, they are similar in structure of the abdomen including sternite VIII (Mound & O Neill, 1974), in structure of the antennae (Figs 11, 121, and also in the presence of a well developed tentorium (Fig. 1) despite the absence of the tentorial bridge from members of most Merothrips species. All merothripids occur in litter and on dead twigs, probably the habitat of the earliest Thysanoptera. 9

136 L. A. MOUND Er AL. Aeolothripidae Uzel, 1895 About 220 species in 20 genera are recognized in this family. Most aeolothripids live in temperate regions, in both the northern and southern hemispheres, although members of several small genera are restricted to the tropics. Sternite VII of females usually bears two pairs of setae near the posterior margin submedially (Mound, 196 7 1 which are here regarded as homologous both with the sternite VIII setae of female Merothripidae and with the two pairs of microsetae on sternite VII of some thripids (Fig. 37). Moreover tergite X of most females bears a pair of small trichobothria (Fig. 40) similar to, but smaller than, those found in merothripids (Fig. 39). The tentorium is fully developed, but the anterior arms are stout only in members of Melunthrips (Fig. 2) and related genera; these structures are more slender in species of Aeolothrips and Mymurothrips and weak in those of Franklinothrips and Eqthrothrips. The antennae of adult Melanthrips (Fig. 14) and related genera are similar to those of Merothrips with the segments all separated and the sensoria on 111 and IV transversely linear. The antennal segments of adult Orothrips and Ekplectothrips are similar to those of Melanthrips but in members of both genera segments I11 and IV bear two sensoria which are weakly emergent and suggestive of the way in which trichomes might have evolved (Fig. 16). Orothrips species occur in western North America and those of Ekplectothrips in Spain, and these distributions curiously reflect the distribution of the two genera of Adiheterothripidae, as well as the two families Fauriellidae and Heterothripidae. Adults of aeolothripine genera have the terminal antennal segments reduced, and the sensoria on I11 and IV linear (Fig. 151, although sometimes curving around the segment apex, and more rarely convoluted. Adiheterothripidae Shumsher Singh, 1946 This family was erected for the Indian genus Adiheterothrips Ramakrishna because of the unusual structure of the antennae (cf. Fig. 24). However, similar antennae are found in adults of Holurthrothrips Bagnall and Oligothrips Moulton. Moreover members of Adiheterothrips can only be distinguished from those of Holarthrothrips through the relative shortness of the pronotal setae, and in view of the many fundamental similarities between them they are here treated as congeneric. As a result, only two genera are recognized in the Adiheterothripidae, Holarthrothrips (= Adiheterothrips syn. n.) whose members occur between the eastern Mediterranean and India, apparently in the flowers of Date Palms, and Oligothrips from western North America, apparently on Arctostaphylos. The head, tentorium, antennae and wings as well as the mesospinasternum and pleurotergal sutures are similar in adults of both genera, and the metanotum usually bears a pair of postero-median setae. However, metanotal sculpture in adults of Holurthrothrips resembles that of most Heterothrips in having concentric rings of microtrichia, and abdominal tergites VII-VIII bear a posteromarginal comb of microtrichia. In contrast, the metanotum of Oligothrips specimens is weakly reticulate and tergites VII-VIII do not have a posteromarginal comb. Two males of Oligothrips from Oregon in the collections of the British Museum (Natural History) have a transversely elongate glandular area on sternites V-VIII anterior to the antecostal ridge.

FAMILIES OF THYSANOPTERA 137 Fauriellidae Priesner, 1949, stat. n. Priesner ( 1949 : 40) erected this group as a tribe of the Heterothripidae for two monobasic genera Fauriella and Opisthothrips described by Hood ( 1937 1 from South Africa. Subsequently, two further monobasic genera were placed in this group, Ropotamothrips Pelikan (1958) and Osmanothrips Priesner (1961), both from Europe between Spain, Germany and Turkey. According to the International Code of Zoological Nomenclature ( 1961, Article 361, tribal names are coordinate in status with family names. Therefore the name Fauriellini is available for use as Fauriellidae with the original date and authorship. Adults of this family are readily distinguished through the presence of antennae which are similar to those of Merothrips and Melanthrips (Figs 13, 221, and also through the presence of a well developed, fore tarsal hamus. The rest of the body is remarkably like that of a thripid, and the head has three pairs of ocellar setae as in adiheterothripids, heterothripids and most of the less specialized thripids. The tentorium is represented simply by the bases of the anterior arms (cf. Fig. 41, and, as in heterothripids, the sternite VIII setae are either absent or represented by minute pores (Figs 30-32). Adults of Osmanothrips were distinguished from those of Ropotamothrips by Priesner through the presence of 2 -segmented maxillary palpi and the absence of a pair of elongate, posteroangular, pronotal setae. A female paratype of 0. ressli has been compared during the present study with a female from Spain which was identified as R. buresi by the late Dr Erich Titschack. This specimen agrees well with the description of buresi hut has the maxillary palpi 2-segmented as in 0. ressli instead of 3-segmented as in the description of buresi. Chaetotaxy and sculpture of the head, thorax and abdomen of buresi and ressli is very similar, and the only obvious difference is in the length of the pronotal posteroangular setae. Osmanothrips Priesner (syn. n.) is therefore placed here in synonymy with Ropotamothrips Pelikan, and the resulting three genera of the Fauriellidae can be distinguished by means of the following key. 1. Antennae 8 -segmented; ovipositor weakly developed, not extending beyond apex of body; sternite VII of female with three pairs of posteromarginal setae arising close together and close to the posterior margin (Fig. 30); forewing, distal to the first cross vein, with 4 setae on the first vein and 3 setae on the second vein................ Opisthothrips Hood - Antennae 9 -segmented (Fig. 13); ovipositor straight to down-curved, extending beyond apex of body; sternite VII with at least one pair of setae arising at more than its own length from the posterior margin (Figs 3 1, 32); forewing, distal to the first cross vein, with 5 or 6 setae on the first vein and 4 or 5 setae on the second vein..................... 2 2. Pleurotergal sutures relatively broad with several longitudinal lines; sternite VII of female with two pairs of setae (Fig. 32); metanotum without a pair of setae near the posterior margin............... Ropotamothrips Pelikan (Osmanothrips Priesner syn. n.)

138 L. A. MOUND ET AL. - Pleurotergal sutures narrow and weakly developed, without longitudinal lines; sternite VII of female with three pairs of setae (Fig. 31); metanotum with a pair of small setae near posterior margin.....,,.......... Faurieh Hood Heterothripidae Bagnall, 19 12 Only three Recent genera are here accepted in this family; the other genera previously placed here (Jacot-Guillarmod, 19 70) being removed to the Adiheterothripidae and Fauriellidae, q.v. As a result, the Heterothripidae is restricted to the New World. Aulacothrips contains a single species, dictyotus Hood from southern Brazil (Figs 25-28), Scutothrips contains four species from South America (Stannard, 19721, but Heterothrips includes rather more than 50 species from South, Central and parts of North America. In adults of all three genera, the sensoria on the third and fourth antennal segments are continuous around each segment, but in Heterothrips and Scutothrips the sensoria constitute a simple band, whereas in Aulacothrips the band is convoluted (Figs 21, 26). In adults of Heterothrips (Lenkothrips) sensitivus Santis 8c Sureda ( 1970) the sensoria are also looped, extending about half the length of both segments (Fig. 231, although the rest of the body is typical of other members of Heter0thrip.s. Aula~othrips (Figs 25-28) appears on first examination to be quite distinct from Heterothrips and Scutothrips. However S. peruuianus (Hood) has a sculptured metanotal triangle as in A. dictyotus (Fig. 291, and several HeterothrzpJ have the median abdominal tergal groove with stout setae laterally (Fig. 281, as well as the swollen base to the forewing (Fig. 251, which are so strongly developed in Aulacothrips. The first vein of the forewing in Aulacothrips is only visible in the basal, swollen part of the wing; the distal three-quarters of the forewing apparently lacks veins. Sternite VII of females bears a pair of minute pores or indentations (Fig. 33) in those species of Heterothrips which lack a posteromarginal fringe of microtrichia on the sternites. Thripidae Stephens, 1829 There are about 1500 species in 230 genera recognized at present in this family, but these figures can be expected to rise considerably with increased collecting and improved studies in tropical areas. The Thripidae includes all those Thysanoptera with emergent, slender trichomes on the third and fourth antennal segments, but whose abdominal segment X is not entirely tubular. The antennal trichomes are forked in adults of most species, one on each segment (Fig. 191, but simple sense cones are not uncommon (Fig. 20). Adults of certain genera of Panchaetothripinae (Anisopilothrips, Astrothrips, Dinurothrips) have an elongate, thin-walled seta with an enlarged base on the fourth antennal segment looking very like a second simple trichome. The plesiotypic number of nine antennal segments occurs in adults of several species, but adults of most species have only eight (Fig. 19) or seven antennal segments, and some have even fewer (Fig. 20). Of the two subfamilies recognized, the Panchaetothripinae include only about 1 10 species in 34 genera (Wilson, 19751, and members of all of these apparently feed on green leaves. In contrast, the Thripinae include the most specialized flower-

FAMILIES OF THYSANOPTERA 139 living species, and the diversity of life-styles in this subfamily is indicated above in the section on life-styles (p. 125). The suggestion that Panchaetothripinae represent an earlier stage of evolution than the Thripinae is maintained here despite the fact that both adult and larval panchaetothripines exhibit a considerable number of apomorphies. The group includes relatively few species but a considerable number of genera, several of which are restricted in distribution to southern land masses. This is typical of an ancient group. In contrast, groups like the Chirothripini, Sericothripini and Dendrothripini include many species in few genera, and are found mainly in the northern hemisphere. Phlaeothripidae Uzel, 1895 At present, there are about 2700 species recognized in this family. However their classification is not satisfactory; the genera are frequently ill-defined and the concept of what constitutes a species is inadequately studied particularly in the gall-forming and fungus-feeding groups which evidently include the majority of taxa. Recent interpretations of variation (Palmer & Mound, 1978) suggest that much synonymy remains to be established, but an alternative interpretation (Mound, 1972) could multiply the number of recognized species considerably. This large number of species, together with the structural uniformity of the group, suggests that the Phlaeothripidae is a relatively modern taxon which is still actively evolving. Unfortunately, the family is mostly tropical and few species have been studied in the field. Adults of the great majority of species have eight antennal segments (Fig. 181, reduction to seven (Fig. 17) or even less is uncommon, and no species has nine segments. Unlike most terebrants, phlaeothripids usually have more than one sensorium on antennal segments three and four (Figs 17, 18); the basic arrangement appears to be one trichome on segment three, and three trichomes on segment four. The plesiotypic life-style in Phlaeothripidae probably involves fungal-hyphae-feeding under bark, judging from the dorso-ventral compression of the body and other characteristics. Members of the majority of extant species are probably fungusfeeding; however those of a large number of species feed on plant leaves (often inducing galls, Ananthakrishnan, 19781, those of many species of the genus Haplothrzps live in flowers (Pitkin, 1973; 19761, and those of various unrelated species appear to be predatory. Members of one subfamily of about 400 species (Mound & Palmer, in prep.), the Idolothripinae, have exceptionally broad maxillary stylets and feed on fungal spores. ACKNOWLEDGEMENTS The authors are grateful to Dr Douglas R. Miller of the U.S. Department of Agriculture, Beltsville, Maryland, to Dr Richard zur Strassen of the Senckenberg Museum, Frankfurt, to Professor Luis de Santis of La Plata University, and to Dr J. S. Bhatti of Delhi Universi for the loan of specimens. We are particularly grateful to Dr Shuji Okajima o 9 Tokyo University who not only loaned material of Uzelothrips scabrosus but allowed us to publish his remarkable record of the species from Singapore. Adrian Pont of the B.M.(N.H.), London generously made available his English translation of Hennig, 1969, and Jack Scott of the University

140 L. A. MOUND ET AL. of Alberta prepared the final drafts of Table I1 and Figures 42 and 43. Dr George Ball of the University of Alberta and Dick Vane-Wright of the B.M.(N.H.), London read the manuscript and made many positive suggestions for its improvement. REFERENCES ANANTHAKRISHNAN, T. N., 1978. Thrips galls and gall Thrips. Zoological Suruey oflndia, Technical Monograph, 1: 1-69. ANANTHAKRISHNAN, T. N., 1979. Biosystematics of Thysanoptera. Annual Review of Entomology. 24: 159-1 83. BAGNALL, R. S., 1912. Some considerations in regard to the classification of the Order Thysanoptera. Annah 6. Magazine ofnatural History (8) 10: 220-222. BODE, W., 1978. Ultrastructure of the sternal glands in Thrips validus Uzel (Thysanopcera, Terebrantia). Zoomorphologie, 90: 53-65. ELLINGTON, C. P., 1980. Wing mechanics and take-off preparation of Thrips (Thysanoptera). Journal./ ExperimentalBio/ogy, 85: 129-136. HALIDAY, A. H., 1836. An epitome of the British genera of the Order Thysanoptera, with indications ofa few of the species. Entomo/ogical Magazine,3: 439-45 1. HECHT, M. K., 1976. Phylogenetic inference and methodology as applied to the vertebrate record. Evolutionary Biology, 9: 335-363. HEMING, B. S., 1970a. Postembryonic development of the female reproductive system in Frankliniellafwca (Thripidae) and Haplothnps verbasn' (Phlaeothripidae) (Thysanoptera). Miscellaneous Publications of the EntomologicalSociety of America, 7: 197-234. HEMING, B. S., 1970b. Postembryonic development of the male reproductive system in Frankliniellafusca (Thripidae) and Haplothrips uerbasci (Phlaeothripidae) (Thysanoptera). Miscellaneous Publications of the Entomok@dSociety ofamerica, 7: 235-27 2. HEMING, B. S., 197 1. Functional morphology of the thysanopteran pretarsus. CunadianJourna[ OfZooloy, 49: 91-108. HEMING, B. S., 1973. Metamorphosis of the pretarsus in Frankliniellafusca (Hinds)(Thripidae) and Haplothnps uerbasci (Osborn)(Phlaeothripidae)(Thysanoptera). CanadianJournal OJZoology, 5 1: 1211-1234. HEMING, B. S., 1975. Antenna1 structure and memorphosis in Frankliniella ficu (Hinds) (Thripidae) and Haplothrips uerbasci (Osboin)(Phlaeothripidae) (Thysanoptera). Quaestiones Entomologicae, I I : 25-68. HEMING, B. S., 1977. [Book review.] Matsuda, R. 1976, Morphology and evolution of the insect abdomen. Quaertioms Entomologicae, 13: 75-8 1. HEMING, B. S., 1978. Structure and function of the mouthparts in larvae of Huplothrips uerbusci (Osborn) (Thysanoptera, Tubulifera, Phlaeothripidae).Journa[ of Morphology, 156: 1-38. HEMING, 8. S., 1979. Thysanoptera. Chapter for a projected work on Immature Insects, edited by F. W. Stehr and L. D. Anderson. HENNIG, W., 1966. PhylogeneticSystematics. Translated by D. D. Davis & R. Zangerl, 263 pp. Urbana: Universityof Illinois Press. HENNIG, W., 1969. DieStammesgeschichlederfnseRten, 436 pp. Frankfurt: W. Kramer. HOOD, J. D., 1914. Notes on North American Thysanoptera, with descriptions of a new family and two new species. lnsecutor Inscitiae Memtruus, 2: 17-22. HOOD, J. D., 1937. New genera and species of Thysanoptera from South Africa. Annals k Magazine 0fNdural History, (10) 19: 97-1 13. HOOD,J. D., 1952. Brazilian Thysanoptera 111. Proceedings ofthe Biological Society ofwashington, 65 : 14 1-1 76. JACOT-GUILLARMOD, C. F., 1970. Catalogue of the Thysanoptera of the world, 1. Annals ofthe Cape Provincial Museums, 7: 1-218. KIM, K. C. & LUDWIG, H. W., 1978. Phylogenetic relationships ofparasitic Psocodea and taxonomic position of the Anoplura. A n d ofthe Entomological Society OJAmnic~, 71: 9 10-922. LEWIS, T. R., 1973. Thrips. Their Biology, Ecoh~, and Economic Importme, 349 pp. New York: Academic Press. MICKOLEIT, E., 1963. Untersuchungen zur Kopfmorphologie der Thysanopteren. Zoologkche Juhrbucher (Anatomie), 81: 101-150. MOUND, L. A. 1967. A taxonomic revision of the Australian Aeolothripidae (Thysanoptera). Bulletin 4th British Museum (Natural HistorYj (Entomology), 20: 43-74. MOUND, L. A., 1968. A review of R. S. Bagnall's Thysanoptera Collections. Bulletin of the British Museum f"atura1 History) (Entomology), SllpP~cmrnl I I : 3-1 72. MOUND, L. A. 1970. Convoluted maxillary stylets and the systematics of some Phlaeothripine Thysanoptera from CUSUQT~TZU trees in Ausrralia. A~lstralian JoUdOfZoology, 18: 439-463. MOUND, L. A. 197 1. The feeding apparatus of hips. Bulletin of Entomological Research, 60: 547-548. MOUND, L. A. 1972. Species complexes and the generic classification of leaf-litter thrips of the tribe Urothripini (Phlaeothripidae). Australian Jouml./Zoology, 20: 83-103.

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