Morphology and Evolution of the Tarsal Plantulae in Hymenoptera (Insecta), Focussing on the Basal Lineages

BlackwellMorphology Science, Ltd and evolution of the tarsal plantulae in Hymenoptera (Insecta), focussing on the basal lineages

SUSANNE SCHULMEISTER*

Accepted: 5 June 2002 Schulmeister, S. (2003). Morphology and evolution of the tarsal plantulae in Hymenoptera (Insecta), focussing on the basal lineages. — Zoologica Scripta, 32, 153–172. The morphology of the plantulae (= tarsal pulvilli = plantar lobes), structures attached to the underside of the tarsus in Hymenoptera, was examined in 55 genera from all 14 families of the basal lineages of Hymenoptera (‘Symphyta’) and a few species of Apocrita, using scanning electron microscopy. Two distinct types of plantula were found: (1) integrated, an unsclerotized patch positioned ventro-distally on each tarsomere, and (2) distal, a membranous vesicle attached to the apical end of each tarsomere. The evolution of these two types is discussed in the light of current phylogenetic hypotheses. The plantulae exhibit an astonishing variety of form and structural details; their potential phylogenetic and taxonomic value is discussed. Susanne Schulmeister, Institute of Zoology and Anthropology and Zoological Museum, Berliner Str. 28, 37073 Göttingen, Germany. E-mail: [email protected].

Introduction the plantulae to characterize some of his taxonomic groups, A multitude of different structures attached to the tarsi and but did not discuss their evolution. Due to the lack of a com- pretarsi of insects has evolved. A comparative study on the parative study, there has been no attempt to use the plantulae ordinal level was recently undertaken within a cladistic as a character in phylogenetic analysis. Königsmann (1977) context by Beutel & Gorb (2001), in which they concluded mentions their presence or absence in certain groups and that that the plantulae found in the Hymenoptera are unique to they probably belong to the groundplan of Hymenoptera, this insect group. The plantulae (plantar lobes, tarsal pulvilli) but did not use them in his phylogeny of lower Hymenoptera. are membranous structures on the underside of the tarsus, Vilhelmsen (1997) mentions the plantulae (‘plantar lobes’) integrated in or attached to the ventro-distal part of each as potentially informative characters, but did not use them tarsomere. because they were insufficiently surveyed; in more recent It has been known for a long time that two distinct types phylogenetic treatments (Ronquist et al. 1999; Vilhelmsen 2001), of tarsal plantulae, integrated and distal, are found in the the plantulae are not mentioned at all. Hymenoptera (Börner 1919; Benson 1945a, 1954). In spite of The present study has been written with the aim of bring- this, they have not been the subject of a comparative study. ing these structures to the attention of both morphologists Due to the broad scope of their investigation, Beutel & Gorb and systematists. (2001) examined only two species of Hymenoptera with plantulae, both of which have the distal type. It seems that Materials and methods the existence of these structures has been overlooked by Classification (following Vilhelmsen 2001) and names of the morphologists. species included in the present study, as well as the methods The presence of two types of plantulae raises a number of of preservation and examination of the specimens study, are questions about their evolution. Whether they are homologous, given in Table 1. and if so, which type is plesiomorphic and which apomorphic. Most specimens were fixed in Bouin’s fluid following How they might have originated and their potential value as collection and subsequently stored in 70% ethanol. They a source of phylogenetic information. These problems have were examined with a stereomicroscope (Zeiss Stemi SV 11, also escaped the attention of systematists. Börner (1919) used maximum magnification 66×). One hind tarsus of each specimen chosen for scanning electron microscopy was cut off and cleaned twice using ultrasound. Alcohol concentration *Present address: Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th St., New York, NY 10024, USA. was slowly raised to 100% in 5% steps over the course of E-mail: [email protected] several days in order to avoid collapsing of the plantulae. The

Tarsal plantulae in Hymenoptera • S. Schulmeister

Table 1 Taxa examined in the present study. The column ‘Pres.’ speciﬁes the preservation method: p.a. = pure alcohol; Bouin = kept in 70% alcohol after Bouin ﬁxation; pinned = pinned and dried museum specimen. SEM = scanning electron microscopy and stereo light microscopy, SLM = stereo light microscopy only.

Species Sex Pres. M. 1 2 3 4 5 6 7

MECOPTERA Panorpa communis f Bouin SEM 0 — 0 2 — — — HYMENOPTERA XYELOIDEA Xyelidae Macroxyela ferruginea (Say, 1824) m Bouin SEM 1 — 1 0 1 0 0 Xyelecia nearctica Ross, 1932 f pinned SEM 3 0 1 0 0 0 0 Xyela sp. f + m Bouin SEM 1 — 1 2 ? 0 0 Pleroneura bruneicornis Rohwer, 1910 f + m pinned SEM 0 — 1 0 — — — TENTHREDINOIDEA Blasticotomidae Runaria reducta Malaise m p.a. SEM 3 0 0–1 0 1 0 0 Tenthredinidae Monophadnoides sp. m Bouin SEM 3 ? 1 0 0 1 0 Strongylogaster xanthocera (Stephens, 1835) f Bouin SEM 3 1 1 0 0 1 0 Selandria serva (Fabricius, 1793) m Bouin SEM 3 1 1 0 0 2 0 Taxonus agrorum (Fallén, 1808) m Bouin SEM 3 0 1 0 0 4 0 Allantus didymus (Klug, 1818) m Bouin SEM 3 ? 1 0 0 4 0 Dolerus pratensis (Linnaeus, 1758) m Bouin SEM 3 1 1 0 0 1 0 Dolerus sp. m Bouin SEM 3 1 1 0 0 5 0 Dolerus gonager (Fabricius, 1771) m Bouin SEM 3 1 1 0 0 0 0 Tenthredo campestris Linnaeus, 1758 m Bouin SEM 3 1 1 0 0 2 0 Tenthredo mesomela Linnaeus, 1758 m Bouin SEM 3 1 1 0 0 1 0 Aglaostigma lichtwardti (Konow, 1892) m Bouin SEM 3 ? 1 0 0 1/4 0 Tenthredopsis stigma (Fabricius, 1798) m Bouin SEM 3 1 1 0 0 1 0 Tenthredopsis tarsata (Fabricius, 1804) m Bouin SEM 3 1 1 0 0 1 0 Siobla sturmii (Klug, 1817) m Bouin SEM 3 1 1 0 0 5 0 Athalia rosae (Linnaeus, 1758) m Bouin SEM 3 1 1 0 0 0 0 Athalia sp. m Bouin SEM 3 ? 1 0 0 0 0 Nematus sp. f Bouin SEM 3 1–2 1 0 0 1 0 Hoplocampa fulvicornis (Panzer, 1801) m Bouin SEM 3 ? 1 0 0 1 0 Cladius pectinicornis (Geoffroy, 1785) m Bouin SEM 3 ? 1 0 0 1/4 0 Diprionidae Monoctenus juniperi (Linnaeus, 1758) f Bouin SEM 3 2 1 0 3 3 0 Gilpinia sp. f Bouin SEM 3 2 1 0 1 3 0 Diprion sp. (pini or similis) f + m Bouin SEM 3 2 1 0 3 3 0 Macrodiprion nemoralis (Enslin, 1917) f Bouin SEM 3 2 1 0 3 3 0 Cimbicidae Corynis crassicornis (Rossi, 1790) m Bouin SEM 3 0 1 0 1 5 0 Cimbex connatus (Schrank, 1776) f pinned SEM 3 1 1 ? 5 3 0 Zaraea sp. f p.a. SEM 3 1 1 2 5 3 0 Abia fasciata (Linnaeus, 1758) f p.a. SEM 3 1 1 0 5 3 0 Abia nitens (Linnaeus, 1758) m pinned SEM 3 ? ? ? 5 6 0 Argidae Arge ochropus (Gmelin, 1790) m Bouin SEM 3 1 1 0 0 0 0 Arge cyanocrocea (Forster, 1771) m Bouin SEM 3 ? 1 0 0 0 0 Arge gracilicornis (Klug, 1814) m Bouin SEM 3 ? 1 0 0 0 0 Sterictiphora furcata (Villers, 1789) m Bouin SEM 3 1 1 0 0 0 0 Pergidae Perga sp. m pinned SLM 3 1 1 ? 1 0 0 Lophyrotoma analis (Costa) m Bouin SEM 3 1 1 0 1 0 0 Neoeurys sp. m Bouin SEM 3 ? 1 0 2 0 0 Decameria sp. m Bouin SEM 3 3 0 ? 2 0 0 Phylacteophaga froggatti Riek f p.a. SEM 3 ? 0 0 0 0 0 PAMPHILIOIDEA Pamphiliidae

154 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters

S. Schulmeister • Tarsal plantulae in Hymenoptera

Table 1 Continued.

Species Sex Pres. M. 1 2 3 4 5 6 7

Neurotoma fasciata (Norton, 1862) m pinned SLM 2 — ? ? ? ? ? Pamphilius hortorum (Klug, 1808) f p.a. SEM 2 — 1 0 1 0 0 Onycholyda amplecta (Fabricius, 1804) f + m Bouin SEM 2 — 1 0 1–2 0 0 Cephalcia sp. m Bouin SEM 2 — 1 0 2 0 0 Acantholyda sp. m Bouin SEM 2 — 1 0 2 0 0 Megalodontesidae Megalodontes cephalotes (Fabricius, 1781) f + m Bouin SEM 2 — 1 0 0 0 0 Megalodontes panzeri (Leach, 1817) m Alkohol SEM 2 — 1 0 0 0 0 CEPHOIDEA Cephidae Cephus pygmeus (Linnaeus, 1767) m Bouin SEM 3 0 0 1 0 4 0 Calameuta filiformis (Eversmann, 1847) f + m Bouin SEM 3 0 1 0 0 0/4* 0 Hartigia trimaculata (Say, 1824) f + m Bouin SEM 3 0 1 0 0 0 0 Janus integer (Norton, 1861) m Bouin SEM 3 0 0 0 + 1 0 4 0 Caenocephus sp. m Pinned SLM 3 0 0? ? ? ? ? Pachycephus sp. m Pinned SLM 3 0 1? ? ? ? ? ANAXYELOIDEA Anaxyelidae Syntexis libocedrii (Rohwer, 1915) f Bouin SLM 0 — 0 ? — — — SIRICOIDEA Siricidae Urocerus gigas (Linnaeus, 1758) f + m Bouin SEM 1 — 1 2 0 0 1 Xeris spectrum (Linnaeus, 1758) m Bouin SEM 0 — 1 2 — — — Sirex noctilio Fabricius, 1793 ? p.a. SEM 1 — (1) 2 0 0 1** Tremex columba (Linnaeus, 1763) f p.a. SEM 1 — 1 2 4 0 1 XIPHYDRIOIDEA Xiphydriidae Xiphydria camelus (Linnaeus, 1758) m Bouin SEM 4 1 1 0 0 0 0 Xiphydria prolongata (Geoffroy, 1785) f Bouin SLM 4 1 1 ? ? ? ? Derecyrta lugubris Westwood f pinned SEM 0 — 0 ? — — — Steirocephala sp. m pinned SEM 2 — 0 2 0? 0 0 ORUSSOIDEA Orussidae Orussus abietinus (Scopoli, 1763) m Bouin SEM 0 — 1 2 — — — APOCRITA STEPHANOIDEA Schlettererius cinctipes (Cresson, 1880) m pinned SLM 0 — 1? ? — — — MEGALYROIDEA Megalyra sp. m pinned SLM 0 — 0? ? — — — TRIGONALIOIDEA Orthogonalys sp. m pinned SLM 3 0? 0? ? ? ? ? EVANIOIDEA Aulacidae Pristaulacus sp. m pinned SLM 0 — 0 ? — — — ICHNEUMONOIDEA Braconidae sp. ? Bouin SEM 0 — 0 2 — — — Ichneumonidae sp. m Bouin SEM 0 — 0 2 — — — CYNIPOIDEA Ibaliidae Ibalia sp. m pinned SLM 0 — 0 ? — — — ACULEATA CHRYSIDOIDEA Chrysididae Chrysis sp. ? pinned SLM 0 — 0 ? — — — Bethylidae Rhabdepyris sp. m p.a. SLM 0 — ? ? — — — APOIDEA ‘Sphecidae’ Crabronidae sp. f Bouin SEM 3 ? 0 0 0 4 0

Tarsal plantulae in Hymenoptera • S. Schulmeister

Table 1 Continued.

Species Sex Pres. M. 1 2 3 4 5 6 7

Apidae Anthophora sp. Bouin SEM 0 — 1 2 — — — VESPOIDEA Pompilidae unidentiﬁed genus Bouin SEM 3 1 1 0 0 4 0 Vespidae Polistes sp. m Bouin SLM 0 — 0 ? — — — Scoliidae Scolia sp. f Bouin SLM 0 — 0 ? — — — Formicidae Cataglyphis sp. Bouin SLM 0 — 0 ? — — —

*Only on basal plantulae, **only very few and only on the plantulae of the two distal tarsomeres.

tarsi were dried in a Balzers CPD 030 critical point dryer and 3 Plantulae (e.g. Bohart & Menke 1976). The Latin coated with gold in a Balzers SCD 050 sputter coater for ‘plantula’ is the diminutive of ‘planta’ and means ‘small sole’ 300–500 s. The micrographs were taken in a Zeiss/Leica (Kenneth 1960; von Kéler 1963). LEO 435 VP scanning electron microscope. The presence or 4 Euplantulae (e.g. Schedl 1991). According to Beutel & Gorb absence of denticles on the plantulae of the front and middle (2001), the plantulae of Hymenoptera are not homologous to tarsi of some Tenthredinidae was examined with a light the euplantulae found in basal neopterans; the term microscope. euplantulae should therefore not be used for hymenopteran The Steirocephala and Derecyrta specimens examined in this plantulae. study are deposited in the American Museum of Natural 5 Sohlenbläschen (e.g. Börner 1919; Königsmann 1977). This History, New York. The Xyelecia and Pleroneura specimens German word means ‘vesicle of the sole’. belong to the Canadian National Collections, Ottawa. Perga, In order to use a Latin term which is not easily confused with Caenocephus, Pachycephus, Syntexis, Schlettererius, Megalyra, those for other structures, I chose the term ‘plantulae’. For Orthogonalys, Pristaulacus, and Ibalia were loaned by the the purposes of this paper, the terms ventral, dorsal, and Smithsonian Museum of Natural History, Washington D.C. lateral are used with respect to the leg, i.e. ventral and dorsal The remaining specimens are in the private collection of indicate the lower and upper side of the leg, lateral refers to the author. the sides of the leg.

Terminology Results A number of terms have been applied to the structures In agreement with previous studies, two basic types of tarsal attached to the ventro-distal end of each tarsomere in plantulae were found in Hymenoptera: integrated and distal. Hymenoptera: An integrated plantula is formed by the unsclerotized ventro- 1 (Tarsal) pulvilli (e.g. Benson 1945a,b, 1954; Arora 1956; distal part of the tarsomere (Fig. 1A and B) and is hence Middlekauff 1958; Königsmann 1977; Smith 1988). The broadly connected to the sclerotized part. A distal plantula is Latin ‘pulvillus’ is the diminutive of ‘pulvinus’ and means a vesicle attached to the ventro-distal end of the tarsomere ‘small cushion’ (Kenneth 1960; von Kéler 1963). [The word and so has only a small connection to the rest of it (Fig. 1C ‘pulvillus’ is also used for the paired (basi) pulvilli of the and D). Each of these two basic types shows modiﬁcations. pretarsus in some insects, situated below the claws]. Integrated plantulae can be simple (Fig. 1A) or bilobed According to Richards (1977), some authors use ‘pulvillus’ to (Fig. 1B). Distal plantulae are usually singular, i.e. one on indicate the arolium, a pad between the pretarsal claws (see each tarsomere (Fig. 1C); double distal plantulae are found also Gauld & Bolton 1988). only in Xiphydriidae (Fig. 1D). 2 Plantar lobes (e.g. Richards 1977; Gauld & Bolton 1988; Simple integrated plantulae were found in the xyelid Goulet & Huber 1993). Derived from the Latin ‘planta’ (sole Macroxyela (Fig. 2E and F) and the siricids Urocerus, Sirex, of the foot) which has been used for the underside of the and Tremex (Fig. 3A and C), bilobed integrated plantulae in all tarsomeres. ‘Planta’ is also used to indicate a sclerite on the examined Pamphilioidea (e.g. Fig. 4A−D) and the xiphydriid arolium and the basal tarsomere of the hindleg of worker bees Steirocephala (Fig. 7B). The xyelid Xyelecia and all examined (von Kéler 1963). exemplars of Tenthredinoidea sensu lato (e.g. Fig. 5) and

156 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters

S. Schulmeister • Tarsal plantulae in Hymenoptera

Fig. 1 A–D. Types of plantulae; integrated (A, B) and distal (C, D). —A. Simple integrated plantulae in the xyelid Macroxyela. —B. Bilobed integrated plantulae in the pamphiliid Cephalcia. —C. Singular distal plantulae in the tenthredinoid Arge. —D. Double distal plantulae in Xiphydria.

Tarsal plantulae in Hymenoptera • S. Schulmeister

Fig. 2 A–F. Tarsomeres in Mecoptera and Xyeloidea. —A. Panorpa communis. —B, C. Xyela sp. —D–F. Macroxyela ferruginea. Intersegmental membrane arrowed.

158 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera

Fig. 3 A–D. Tarsomeres in Siricoidea. —A. Urocerus gigas. —B. Xeris spectrum. —C. Tremex columba. —D. Surface structure near the rim of the plantula of Tremex.

Fig. 4 A–D. Tarsal plantulae in Pamphilioidea. —A. Megalodontes cephalotes (Megalodontesidae). —B. Cephalcia sp. (Pamphiliidae) —C. Pamphilius hortorum (Pamphiliidae). —D. Onycholyda amplecta (Pamphiliidae, male).

160 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera

Fig. 5 A–F. Tarsal plantulae in Tenthredinoidea sensu lato. —A. Runaria reducta (Blasticotomidae). —B. Arge ochropus (Argidae). —C. Phylacteophaga froggatti (Pergidae). —D. Tenthredopsis tarsata (Tenthredinidae). —E. Zaraea sp. (Cimbicidae). —F. Monoctenus juniperi (Diprionidae).

Cephidae (e.g. Fig. 6) have singular distal plantulae, while No plantulae exist in the xyelid Pleroneura, the siricid Xiphydria has double distal plantulae (Fig. 7A). The state in Xeris (Fig. 3B), the xiphydriid Derecyrta (Fig. 7C), the anax- Xyela shows some variability, even on one and the same tarsus, yelid, the orussid (Fig. 7D), and all examined apocritan taxa but most examined tarsi have vestigial plantulae (Fig. 2B,C). (e.g. Fig. 8E and F) except for the pompilid (Fig. 8A and B),

Fig. 6 A–D. Tarsal plantulae in Cephoidea. A. Cephus pygmeus. —B. Calameuta ﬁliformis. —C. Hartigia trimaculata. —D. Janus integer.

162 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera

Fig. 7 A–D. Tarsomeres in Xiphydrioidea (A−C) and Orussoidea (D). —A. Xiphydria camelus. —B. Steirocephala sp. —C. Derecyrta lugubris. —D. Orussus abietinus.

Fig. 8 A–D. Tarsomeres in Apocrita. —A, B. Pompilidae sp. —C. Crabronidae sp. —D. Braconidae sp. —E. Ichneumonidae sp. —F. Anthophora sp.

164 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera

Table 2 Character state descriptions for 1 Plantulae: (0) absent; (1) integrated, simple; (2) integrated, bilobed; (3) one distal plantula; (4) two distal plantulae. Table 1. 2 Sclerotization on dorsal side of distal plantula: (0) absent; (1) disc-shaped; (2) ring-shaped; (3) triangular, pointed; (–) not applicable. 3 Membrane between plantula and following tarsomer: (0) not protruding; (1) protrudes beyond the rim of the tarsomer, forming a cushion. 4 Denticles near plantulae : (0) on membrane between plantula and following tarsomer; (1) on rim of tarsomer, lateral of plantula; (2) absent. 5 Surface structure on plantulae : (0) none; (1) honeycomb pattern; (2) large parallel lineation; (3) areolate; (4) papillous; (5) ﬁne parallel lineation; (–) not applicable. 6 Denticles on plantulae of hind tarsus : (0) absent from all plantulae; (1) patch of bristle-shaped denticles present on ventral face of all plantulae; (2) patch of bristle-shaped denticles present on ventral face of the plantulae on the two distal tarsomeres, absent from the two proximal plantulae; (3) denticles along rim of plantula, but not on ventral face; (4) denticles present on base of plantulae; (5) no denticles on ventral face or rim of plantula, but very small, ﬁne denticles on the back of the plantula; (6) plantula on basal tarsomere covered with bristles, the distal plantulae increasingly less; (–) not applicable. 7 Secretion pores : (0) absent; (1) present; (–) not applicable.

crabronid (Fig. 8C), and trigonalid exemplars, which have specimen has only very few pores, and these occur only on the distal plantulae. A peculiar and unique structure was found in plantulae of the two distal tarsomeres. a braconid (Fig. 8D). In several species, the plantulae were found to be equipped Distal plantulae appear transparent ventrally. Dorsally, the with denticles. Dense patches of bristle-shaped denticles on distal plantulae of Tenthredinoidea s.l. are often strongly the ventral face of the plantula (i.e. the one in contact with sclerotized, as is shown by the dark colour (not discernable in the substrate), were found only in some tenthredinids (e.g. the SEM); the sclerite can be disc-shaped and cover the entire Fig. 5D, see Table 2, character 6) and one cimbicid. Remark- back (dorsal side) of the plantula, it can be U-shaped and run ably, only the plantulae on the two distal tarsomeres of each along the rim of the back of the plantula, or it can be trian- leg of Selandria serva were equipped with denticles; those on gular and cover only the base of the back of the plantula (see the two proximal tarsomeres were glabrous. The same pattern Table 2, character 2). is found on the hind legs of Tenthredo campestris, but not on The ventral surface of the plantulae (examined in the scan- the fore and middle legs, where all four plantulae have ning electron microscope) is usually smooth (e.g. Figs 4A, patches of denticles. Monophadnoides sp., Strongylogaster 5B, C, 6A−C and 7A), with a few exceptions. The plantulae xanthocera, Dolerus pratensis, Tenthredo mesomela, Tenthredopsis of Macroxyela ferruginea exhibit a remarkable honeycomb stigma and T. tarsata, Nematus sp., Hoplocampa fulvicornis, and pattern (Fig. 2D); similar patterns are found in Pamphilius Abia nitens have patches of denticles on all four plantulae on hortorum (Fig. 4C) and in some Tenthredinoidea, viz. Runaria all six legs. Taxonus agrorum and Allantus didymus have a few reducta (Fig. 5A), Gilpinia sp., Corynis crassicornis, and Lophy- denticles around the bases of the plantulae, similar to the rotoma analis. The plantulae of Neoeurys sp., Decameria sp., cephid shown in Fig. 6D. In Aglaostigma lichtwardti and Cephalcia sp. (Fig. 4B) and Acantholyda sp. show parallel line- Cladius pectinicornis, the plantula on the proximal tarsomere ation, and those of Onycholyda amplecta show a pattern that is resembles that illustrated in Fig. 6D, while the plantula on intermediate between honeycomb and parallel lineation the distal tarsomere is ﬂat and covered ventrally with a patch (Fig. 4D). Minute parallel lines are found on the plantulae of of denticles. The tenthredinids Dolerus gonager, Dolerus sp., the cimbicids Zaraea sp. (Fig. 5E), Abia fasciata, and Cimbex Athalia rosae, Athalia sp. and Siobla sturmii do not have connatus. The surfaces of the plantulae of the diprionids patches of denticles on the ventral face of any of their plan- Monoctenus juniperi, Diprion sp., and Macrodiprion nemoralis tulae, as did all nontenthredinid exemplars included in this (but not Gilpinia sp.) show a unique areolate structure study. A band of small denticles borders the rim of the plan- (Fig. 5F), which is clearly different from the honeycomb tulae of the cimbicids Zaraea sp. (Fig. 5E), Abia fasciata and pattern mentioned above. Cimbex connatus, as well as the diprionids Monoctenus juniperi The plantulae of the siricid Tremex columba have a remark- (Fig. 5F), Diprion sp., and Macrodiprion nemoralis, but not of able surface structure found in no other examined hymenop- the cimbicid Corynis and diprionid Gilpinia. These two species, teran: they are densely covered with papillae, leaving small like Dolerus sp. and Siobla sturmii, only show small scattered gaps only where there are pores (Fig. 3C and D). The pores denticles on the upper side of the plantulae, as are found in are also present in two other siricids, Urocerus gigas and Sirex other Tenthredinidae. Dolerus gonager, Athalia rosae, and noctilio, but not the papillae (Fig. 3A). The examined Sirex Athalia sp. are the only examined species of Tenthredinidae,

Diprionidae and Cimbicidae whose plantulae are completely taxa they did not examine. Arora (1956) mentions structures bare, like those of all examined Blasticotomidae, Argidae, and in Tipulidae (Diptera) similar to the distal plantulae in Pergidae. The proximal plantulae on the hind legs of Selan- Hymenoptera. For the present, however, the assumption of dria serva are also completely bare, but the distal ones are not. Beutel & Gorb (2001) is assumed to be correct. Small scattered denticles were found on the proximal part The plantulae probably serve to enhance the attachment of of the plantulae of the cephids Cephus pygmeus, Calameuta the tarsus to the substrate. Because of their flexible surface, filiformis, and Janus integer (Fig. 6A,B, and D) as well as in they can achieve a tight contact with the surface by passive Pompilidae and Crabronidae (Fig. 8A−C). deformation, which possibly enables molecular adhesion Sexual dimorphism is exhibited by the plantulae in some (Beutel & Gorb 2001; and references therein). In many species. In the examined Urocerus gigas female, for example, tenthredinoid taxa and a few other Hymenoptera, one pair of the three distal plantulae cover almost the entire tarsomere, setae is longer and often directed more ventrally than the whereas they cover only the distal part in the male. Also, the others (Fig. 5B and D−F); this pair might have a special female has a much higher number of pores on the plantulae. tactile function correlated with the plantulae. Normally, the membrane between the distal rim of a tar- Two distinct types of tarsal plantulae, integrated and distal, somere and the base of the next one runs straight between are found in Hymenoptera (Börner 1919; Benson 1945a, them and can only be seen if the leg is viewed obliquely (e.g. 1954). The present study showed that Pamphiliidae and Fig. 2A and E, arrowed). However, in conjunction with a Siricidae (except Xeris) all have integrated plantulae, while all plantula, whether it is integrated or distal, this membrane is Tenthredinoidea s.l., Cephidae, and some Apocrita have usually modified to extend distally, often beyond the rim of distal plantulae. In Xyelidae and Xiphydriidae there are both the tarsomere, forming a cushion-like structure, often fur- types as well as a complete lack of plantulae. Syntexis, Orussus, nished with denticles, and henceforth called ‘cushion’ (e.g. and most Apocrita lack plantulae as well. Figs 2F, 3A, and C, 4, 5B and F, 6B and C and 7A). The distal rim of integrated plantulae is directly connected Evolutionary aspects to the cushion (cf. Figs 2F, 3A and C, and 4A–D). Distal The first question to be addressed is whether the integrated plantulae insert directly on the cushion (cf. Figs 5B and F, 6B and distal plantulae evolved independently or whether one and C, and 8C), but often very close to the sclerotized wall of type was derived from the other. The alternative hypotheses the tarsomere. In the SEM pictures, the difference between of a homologous or convergent (analogous) origin are dis- sclerites and membranes is, unfortunately, often very subtle. cussed in the following sections. If viewed with a stereomicroscope, the area in which the The discussion is based on the phylogenetic relationships distal plantulae insert is clearly white or translucent, whereas shown in Fig. 9. The relationships between the ‘families’ of the surrounding region is usually dark and heavily sclerotized. lower Hymenoptera in this cladogram are derived from The results are summarized in Table 2. The coding always the hypothesis of Vilhelmsen (2001); some nodes have been refers to the hind tarsus. The table is not intended as a collapsed and a few taxa have been added. The relationships character matrix for phylogenetic analysis, only to present within Siricidae are based on Gauld & Mound (1982). the morphological results in detail. To be incorporated in a The relationships within Apocrita are taken from a review phylogenetic analysis, it should be modified in relation to the by Ronquist (1999), in order to use the most conservative level of the analysis. For example, in a cladistic analysis of estimate. The relationships within Xyelidae are based on the Hymenoptera, character 1 might be more useful phylogenet- tentative phylogeny shown in Fig. 10 derived from character ically if coded with only three states (as in Fig. 9), and char- information in Benson (1945b), Vilhelmsen (1996, 2001), acter 6 with two states (absence or presence of any denticles and Smith & Schiff (1998). on the plantulae), while others should be excluded, except if If the character ‘plantulae’ is coded with three states used with a much larger taxon sample. (absent, integrated, and distal), and the character transformations are mapped onto the cladogram, the hypotheses Discussion of homology and analogy both require 10 transformations General points (Fig. 9). (The Apocrita are not relevant to this question and According to Beutel & Gorb (2001), the plantulae of will be ignored until later.) This means that neither of the two Hymenoptera have no homolog in other insects. However, scenarios can be preferred over the other at present. they examined only very few representatives of each ordinal- To decide between the two hypotheses (without weighting level insect group, so that it is possible that they missed the transformations differently), it would be helpful to something. For example, they saw only distal plantulae in examine the phylogeny and the evolution of the plantulae Hymenoptera and none of the integrated type (see below). It within Xiphydriidae. If plantulae have to be assumed for the is therefore possible that there are similar structures in insect groundplan and the lack of plantulae is secondary within the

166 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera

Fig. 9 A, B. The (‘family’ level) relationships of most Hymenoptera included in this study, after Vilhelmsen (2001), Gauld & Mound (1982), Ronquist (1999) (see also Fig. 10). 0 = plantulae absent; 1 = integrated plantulae; 2 = distal plantulae. To assume a homologous origin of integrated and distal plantulae would require 10 steps (A) within the lower Hymenoptera; a convergent origin of the different types of plantulae requires 10 steps as well (B). The two cladograms are the same, except that in (B) a number of taxa have been summarized with their family name. family, the hypothesis of analogy would require one step bilobed or double plantulae are found in all Xiphydriinae, more than the hypothesis of homology. Alternatively, if pres- in Brachyxiphus, and in Steirocephala. If both Derecyrtinae ence were to be assumed to be secondary, homology would be and Derecyrtini are monophyletic and the plantulae of Brach- less parsimonious. Xiphydriidae therefore play a key role in yxiphus are integrated (Benson did not distinguish between determining the evolution of the plantulae in lower the two types), the lack of plantulae in Derecyrta would have Hymenoptera. A detailed analysis of the plantulae and rela- to be taken as secondary within Xiphydriidae and both tionships of more xiphydriid genera might also show whether integrated and distal plantulae as homologous. the bilobed integrated plantulae of Steirocephala (Fig. 7B) and The Siricidae is another important family for the deter- the double distal plantulae of Xiphydria (Fig. 7A) should be mination of homology. If the phylogeny of Siricidae were assumed to be homologous or not. different from that in Fig. 9 and Xeris instead of Tremex was Xiphydriidae are commonly divided into the subfamilies the sister taxon of the other siricids, absence of plantulae in Xiphydriinae and Derecyrtinae; the latter has been subdivided Xeris could be interpreted as primary in Fig. 9B and presence into Brachyxiphini (= Brachyxiphus) and Derecyrtini a synapomorphy of Tremex + Urocerus + Sirex. This would (= Derecyrta and Steirocephala) (Benson 1954 and references make the hypothesis of an independent origin of the inte- therein; Abe & Smith 1991). According to Benson (1954), grated and distal plantulae one step shorter. However, the

integrated plantulae might have extended more and more distally, while the base of the plantulae became sclerotized again. It is possible that singular distal plantulae derived from simple integrated plantulae this way. The fact that the honeycomb pattern on the integrated plantulae of Macroxyela (Fig. 2D) is also present on the plantulae of Pamphilius (Fig. 4C) and those of the most basal tenthredinoid, Runaria (Fig. 5A), seems to support a common origin of the plantulae of these three superfamilies, i.e. homology of distal and integrated plantulae. However, the optimization of the character ‘honeycomb pattern absent/ present’ is ambiguous at the base of these three superfamilies, and morphological similarity alone cannot be used to decide the question of homology; even if two structures agree in detail, they could still have evolved independently.

The hypothesis of analogy If it is hypothesized that integrated and distal plantulae are not homologous, the assumed origin of the integrated Fig. 10 Tentative phylogeny of the five extant genera of Xyelidae. plantulae can remain as described above. A new evolutionary scenario is only needed for the origin of the distal plantulae. Beutel & Gorb (2001), apparently unaware of the existence of hypothesis that absence in Xeris is secondary is not only sup- integrated plantulae (see below), suggested that the (distal) ported by the phylogeny of Gauld & Mound (1982), but also plantulae of Hymenoptera were derived from tarsal ‘thorns’. by the fact that the ventral area of the tarsomeres of Xeris They do not mention how they derived this hypothesis, lacks bristles entirely and that the area where there is a but I assume it was based on a similar position of the distal plantula in Urocerus and Tremex is elevated in Xeris (ridges plantulae and spines/bristles (which was what they probably arrowed in Fig. 3B). Hence, it seems justified to assume that meant by ‘thorns’). It can be imagined that the middle spine the absence of plantulae in Xeris is secondary. of the three long spines in Fig. 7D could evolve into a structure similar to the plantula shown in Fig. 8B. However, closer The hypothesis of homology inspection reveals that the insertion positions of these two If integrated and distal plantulae are homologous, which is structures are only superficially similar. While spines and the plesiomorphic state? The scenario of an integrated plan- bristles insert on sclerotized areas, distal plantulae insert tula in the groundplan of the Hymenoptera requires 10 steps directly on the membrane connecting the distal rim of a (Fig. 9A). The assumption that integrated plantulae were tarsomere with the base of the following one (see above). In derived from distal plantulae requires one step more. Accord- the pompilid specimen (Fig. 8B) this is not quite as clear as ing to the hypothesis of homology, integrated plantulae must in the crabronid shown in Fig. 8C, or the sawflies shown in therefore be assumed in the groundplan of the Hymenoptera. Figs 5C and D, and 6B and C. Examples of spine-like struc- In this case, they might have originated as a weakly sclero- tures which insert on the membrane include the apical tibial tized area in the wall of the tarsomere. spurs, although these are found only on the tibiae, not on the According to the hypothesis of homology, the integrated tarsomeres. Beutel & Gorb (2001) erroneously assumed plantula would have been transformed into a distal plantula that the distal plantulae insert on the sclerotized part of the in the branch leading to the Tenthredinoidea s.l., at the base tarsomere (see their fig. 3i). Because this is not the case, their of the Cephidae, and within Xyelidae and Xiphydriidae. It is hypothesis of a homology of the distal plantulae and tarsal intriguing that both types occur in a simple and a bilobed spines is highly questionable. form, suggesting that plantulae like those in Fig. 1A evolved An alternative evolutionary scenario of the origin of the into something resembling those in Fig. 1C, while those in distal plantulae should be considered. The fact that cushions Fig. 1D were derived from something resembling those in are present with both types of plantulae suggests that even Fig. 1B. It can easily be imagined that integrated plantulae if integrated and distal plantulae were nonhomologous, the similar to those shown in Fig. 4A evolved into the kind of cushions might be homologous. If the presence or absence plantulae illustrated in Fig. 7B, which further transformed of a cushion is mapped on the cladogram (Fig. 11), it is more into distal plantulae like those in Fig. 7A. Similarly, simple parsimonious to assume that all cushions are homologous

168 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera than that they originated independently. This leads to the a membranous vesicle covered with folds. Peculiarly, the tip hypothesis that a cushion developed in the common ancestor of this structure ﬁts into a groove on the next tarsomere. It of the Hymenoptera. If this was the case, it possibly provided would be interesting to examine the tarsal structures of more a slight enhancement of the attachment properties of the Ichneumonidae and Braconidae to determine the distribu- tarsus and likely constituted a predisposition for the sub- tion within these families. sequent, independent development of integrated and distal In addition, Börner (1919) mentions plantulae not only for plantulae in different taxa. Under this scenario, the distal Trigonalidae, Pompilidae, and certain Sphecidae and Crab- plantulae developed simply as a vesicle ‘budding’ off from ronidae, but also for Thynninae (Tiphiidae). It is possible the cushion. that plantulae will be discovered in more apocritan families. Hence, the presence of plantulae might turn out to be plesi- Origin of plantulae within the Apocrita omorphic within Apocrita. A detailed study of the plantulae Within Apocrita, plantulae were found only in Trigonalidae, in Apocrita is needed in order to make an estimate of their Pompilidae, and Crabronidae. With most cladograms, this evolution. pattern would be most parsimoniously explained by three independent origins (considering only the taxa examined in Plantulae and phylogenetic systematics the present study). Hymenoptera. As discussed above, it is unclear where inte- Under the hypothesis that plantulae evolved at the base of grated plantulae originated; this means that no phylogenetic the hymenopteran tree and were reduced at the base of the conclusions can be drawn from their presence. The distal Vespina (= Orussidae + Apocrita (Rasnitsyn 1988)), one could plantulae, however, must be hypothesized as derived, either assume that the occurrence of plantulae would be explained as modiﬁcations of integrated plantulae or de novo; their pres- by reversals to the original state, which could be brought ence within the basal lineages of Hymenoptera is hence likely about by ‘switching on’ an old gene which had been ‘switched to be interpreted as a synapomorphy of Tenthredinoidea s.l. off’ at the base of the Vespina. However, this explanation is as well as Cephidae. contradicted by the fact that the original state that would The presence of (distal) plantulae within Apocrita must have been reduced at the base of the Vespina would likely be currently be assumed to be apomorphic as well, but the an integrated rather than a distal plantula, which is the only apocritan sample of this study is too meagre to derive an state found in Apocrita. evolutionary scenario for this part of Hymenoptera. If The occurrence of plantulae is more widespread (and plantulae are apomorphic within Apocrita, they could be a variable) within Apocrita than indicated by the present study. synapomorphy of some or all Trigonalidae and perhaps for Of the former ‘Sphecidae’, only Crabronidae were examined, Pompilidae (see above). but other ‘sphecids’ also have plantulae, for example some Sphecidae s.s. (i.e. the former Sphecinae) (M. Ohl, J. Car- Xyelidae. While the plantulae of Macroxyela and Xyelecia are penter, pers. comm.). According to Bohart & Menke (1976), well developed (see above and Benson 1945b), those of Xyela plantulae are present in Sceliphrini, but not in Sphecini are very much reduced, but still present. I did not see plantu- and Ammophilini. Of three examined Rhopalosomatidae, lae in Pleroneura bruneicornis, but there was a small bulbous Liosphex varius has plantulae, while Rhopalosoma nearcticum structure on some of the cushions, which could be a remnant and R. guianense do not ( J. Carpenter, pers. comm.). of a distal plantula. Xyelidae thus show three different con- Depending on the phylogenetic relationships, plantulae ditions. According to Benson (1945b), those of Megaxyela are could have appeared at the base of the ‘Sphecidae’ + Apidae ‘minute and the apical ventral excisions of tarsi scarcely (Brothers & Carpenter 1993; Brothers 1999), at the base of longer than broad’. the Pompilidae + Apoidea (Ronquist et al. 1999), or, if ‘Sphe- cidae’, Pompilidae, and Rhopalosomatidae are a monophy- Pamphiliidae. According to Benson (1945a), the Cephalcii- lum (Ronquist et al. 1999), potentially at the base of this nae Acantholyda and Cephalcia have long plantulae which monophylum. If mapped on the cladograms of Brothers & cover more than half the length of the tarsomere, whereas Carpenter (1993) and Brothers (1999), the presence of plan- those of the Pamphiliinae Neurotoma and Pamphilius are tulae must be assumed as a synapomorphy of the Pompilidae much shorter. My observations of Cephalcia, Acantholyda, and (or part of them). Pamphilius are consistent with his, but the plantulae of According to Gauld & Bolton (1988), a few Ichneumoni- Neurotoma fasciata cover (almost) the entire length of the dae also have plantulae. The braconid specimen examined in tarsomere. This could mean that the size of the plantulae is this study exhibits a structure at the ventro-distal end of the variable within Neurotoma. The form of the plantulae differs tarsomere which is unlike anything else found in this place in strongly between the Pamphiliidae examined in this study (cf. the other examined hymenopterans (Fig. 8D). It seems to be Fig. 4B−D). Both the size and form of the plantulae should

Fig. 11 Most parsimonious evolutionary scenario of the cushion-like structure mapped on the cladogram in Figure 9. 0 = absent; 1 = present.

therefore be studied in a much larger taxon sample. However, other insect groups, and in some they have been shown to be it should be noted that the form can also vary between the secretion pores whose secretions serve to enhance attach- sexes: in the male of Onycholyda amplecta (Fig. 4D), the distal ment (Beutel & Gorb 2001; and references therein). It is ends of the plantulae are drawn out to form pointed tips, quite likely that the pores found in Siricidae have the same while those of the female have rounded and much shorter function. The structures seen in some of the pores (Fig. 3D) ends. might be remnants of the secretions. Considering the absence of pores on the plantulae in all other examined Siricidae. Within Hymenoptera, pores were found only in Hymenoptera and their presence within Siricidae, they are Siricidae. They have been found on attachment structures in likely a synapomorphy of all Siricidae. The presence of

170 Zoologica Scripta, 32, 2, March 2003, pp153–172 • © The Norwegian Academy of Science and Letters S. Schulmeister • Tarsal plantulae in Hymenoptera papillae on the plantulae is a potential autapomorphy of which is found in this form only in Tenthredinidae, Diprion- Tremex, or even of the Tremecinae. It should be very idae, and Cimbicidae (Schulmeister, pers. obs.). More support interesting to examine the plantulae of other siricid genera, for the hypothesis of a monophyletic Tenthredinidae sensu particularly from Tremecinae. Their fine structure could be Rasnitsyn + Cimbicidae was recently found in a completely useful for phylogenetic reconstruction within Siricidae. different character system. This group came out as The plantulae of the presumed Urocerus gigas specimen monophyletic in seven out of nine molecular analyses of depicted by Beutel & Gorb (2001) look quite different from Schulmeister et al. (2002) (including fragments of two mito- those of the two Urocerus gigas specimens (male and female) chondrial and two nuclear genes). However, in eight out of or any other siricid that I examined. In my siricid specimens, nine simultaneous analyses of Schulmeister et al. (2002), in the plantulae are only slightly set off from the rest of the which the molecular data were analysed together with the tarsomere and hardly extend beyond the distal end of the morphological data of Vilhelmsen (2001), Cimbicidae were tarsomere. Those shown by Beutel & Gorb (2001) rather look the sister group of Argidae + Pergidae. like distal plantulae. I believe that this difference is due to a confusion of specimens. The size of the arolium, the size and Diprionidae. The areolate surface structure of the plantulae distribution of the setae on the leg, and the form of the plan- of the diprionid Monoctenus (Fig. 5F) is also present in Diprion tulae themselves show that the leg of the presumed Urocerus and Macrodiprion, but not in Gilpinia. Because the areolate gigas depicted by Beutel & Gorb (2001) is not from a siricid, surface structure is present in both subfamilies of the Dipri- but probably from a cimbicid, most likely Cimbex, as indi- onidae, but in no other hymenopteran family, it is likely a cated by the large size of the leg. If this is correct, this would synapomorphy of the entire family. mean that Beutel & Gorb (2001) examined only species with distal plantulae, and none with integrated plantulae. Unfor- Acknowledgements tunately, I was unable to check their vouchers. I wish to thank the participants of the Scanning Electron Microscopy Course (held by T. Hörnschemeyer and Tenthredinoidea. The presence of denticles on the plantulae R. Willmann) — Christian Hess, Robert Niebergall, was already mentioned by Börner (1919). According to him, Claudia Schluckebier, and most of all Stephan Leu — for the plantulae of Tenthredinidae and Diprionidae are at least producing many of the SEMs. Malte Jänicke, David R. Smith, partially covered with scales or hairs. I found that this is true Mark Dowton, Stephan Blank, Stefan Schmidt, James Carpenter, not only for Tenthredinidae sensu Rasnitsyn (1988) (= Ten- Oliver Niehuis, Manfred Niehuis, and Bodo Falke are thanked thredinidae including Diprionidae; see Schulmeister et al. for gifts and loans of rare specimens. James Carpenter, 2002), but also for Cimbicidae. The distribution of denticles Donald Quicke, Gary Gibson, and Rainer Willmann is quite variable in these families — some plantulae have den- made helpful comments on the manuscript. Rolf Beutel ticles all over, some only on the rim and dorsal face, and some kindly sent me a copy of the proof of his paper before its only very fine dorsal denticles — but they are present in all publication. examined species of Tenthredinidae sensu Rasnitsyn and Cimbicidae except for Athalia rosae and Dolerus gonager. Nei- References ther the blasticotomid nor the four species of Argidae and Abe, M. & Smith, D. R. (1991). The genus-group names of Sym- Pergidae examined in the SEM were found to have any den- phyta (Hymenoptera) and their type species. Esakia, 31, 1–115. ticles. The presence of denticles on the plantulae is hence a Arora, G. L. (1956). The relationship of the Symphyta (Hymenop- potential synapomorphy of Tenthredinidae sensu Rasnitsyn + tera) to other orders of insects on the basis of adult external mor- Cimbicidae. However, the species sample of Blasticotomidae, phology. Research Bulletin of the East Punjab University (Zoology), 90, Argidae, and Pergidae is too poor to permit extrapolation. 85–110. Benson, R. B. (1945a). Classification of the Pamphiliidae A monophyletic Tenthredinidae sensu Rasnitsyn + Cimbi- (Hymenoptera Symphyta). Proceedings of the Royal Entomological cidae was proposed by Rasnitsyn (1969, 1988); this group was Society London (B), 14, 25–33. also found in the trees of Vilhelmsen (1997) and Ronquist Benson, R. B. (1945b). Classification of the Xyelidae (Hymenoptera et al. (1999), who both used many of the characters of Rasnitsyn Symphyta). Proceedings of the Royal Entomological Society London (B), (1988). However, in the most recent analysis of Vilhelmsen 14, 34–37. (2001), which included many more characters, Cimbicidae Benson, R. B. (1954). Classification of the Xiphydriidae (Hymenop- appeared as the sister group of the Argidae + Pergidae. tera). Transactions of the Royal Entomological Society London, 105, 151–162. 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