Revision of the South African endemic bee genus Redivivoides Michener, 1981 (Hymenoptera: Apoidea: Melittidae)

The South african endemic bee genus Redivivoides Michener, 1981 is revised and redefined. The genus comprises seven species, six of which are described here as new: Redivivoides capensis sp. nov. ♀♂, R. eardleyi sp. nov. ♀, R. kamieskroonensis sp. nov. ♀, R. karooensis sp. nov. ♀♂, R. namaquaensis sp. nov. ♀♂ and R. variabilis sp. nov. ♀♂. A key to species is provided.


Introduction
The bee genus Redivivoides was described by Michener (1981) based on a single species, R. simulans Michener, 1981, collected in the winter rainfall region of western South africa.Two other species were only known from a few female specimens and remained undescribed.Since then much more material of this genus has become available representing now a total of seven species, six of which are described here as new.The morphological diversity of the newly described species required a re-evaluation of the characters defining Redivivoides as a genus.
Redivivoides belongs to the subfamily Melittinae Schenck, 1860 and the tribe Melittini Schenck, 1860 that also includes the genera Melitta Kirby, 1802and Rediviva Friese, 1911(Michez et al. 2009).Michener (1981) suggested that Redivivoides is the sister-group of Rediviva and the close relationship of both genera was later confirmed by phylogenetic studies (Danforth et al. 2006;Michez et al. 2009).however, unlike Redivivoides, the females of Rediviva collect floral oil that is mixed with pollen for nest provisioning from a range of oil-producing flowers, with Diascia (Scrophulariaceae) as their principal floral host (Whitehead & Steiner 2001;Pauw 2006;Whitehead et al. 2008).In several Rediviva species the forelegs are elongate, sometimes longer than the entire body, and the lengths of floral spurs and bee legs in some cases show co-variation at the population level, suggesting co-evolution (Steiner & Whitehead 1990, 1991).Because Melittidae are the most basal bees (Danforth et al. 2006), Redivivoides and Rediviva are a key group for understanding the evolution of oil-collecting in bees (Michez et al. 2009) and they might also help to understand the origin of the unusual bee diversity in the Greater Cape Floristic Region (Kuhlmann 2009).
The goal of this publication is to describe the six new species and to provide a key for species identification to facilitate further research on this fascinating group of bees.Based on the descriptions and the analysis of the morphology of the new species, Redivivoides is redefined as a genus and its relationship to its putative sister group, the oil-collecting Rediviva bees, is briefly discussed.

Material and methods
Terminology for the description of species is based on Michener (2007) for general morphology.Puncture density is expressed as the relationship between puncture diameter (d) and the space between them (i), such as i = 1.5 d or i < d.The following abbreviations were used for morphological structures: T = metasomal tergum S = metasomal sternum Body length was measured from the vertex to the apex of the body.
acronyms for collections (after arnett et al. 1993) from which specimens were borrowed or deposited, are as follows: aMGS = albany Museum, Grahamstown, South africa CuIC = Cornell university Collection, Ithaca, uSa EMuS = Entomological Museum, utah State university, uSa LPCT = Laurence Packer collection, Toronto, Canada SaMC = South african Museum, Cape Town, South africa SANC = South African National Collection of Insects, Pretoria, South Africa RCMK = research collection of Michael Kuhlmann, london, uK Nomenclature of plant names follows Germishuizen & Meyer (2003).If not given on the labels, coordinates of collecting sites are given in square brackets and places were identified using Microsoft Encarta® World atlas (version 10, 2001).Geographical coordinates are given in the following format: degree.minutes.seconds.Distribution maps were generated using DMAP V7. 2 (www.dmap.co.uk).
Scanning electron microscopy (SEM) was carried out using a Leo 1455VP.The backscattered electron images were taken under low vacuum (variable pressure) of uncoated specimens.In this mode electronpoor organic material appears darker than electron-rich material (e.g.soil dust particles) consisting of heavier chemical elements.
The diagnosis of Redivivoides given by Michener (1981) was solely based on R. simulans, which was the only known species of the genus at that time.however, in some respects R. simulans is an exception within the genus so a redefinition of Redivivoides is required in the light of the six new species described in this paper (see discussion).
a comprehensive phylogenetic analysis of Redivivoides and related genera is in preparation to investigate the intra-generic relationships, so for convenience the species are here listed in alphabetical order.

Female
Body length.9.0-10.5 mm.head.head slightly wider than long.Integument black except tips of mandible partly dark reddishbrown.Face sparsely covered with long, whitish-grey to brown, erect hairs intermixed with black hairs especially along the inner eye margins and on vertex (Fig. 2B).Clypeus mostly flat, apically almost impunctate; medially covered with medium-sized punctures that become gradually smaller and denser towards the lateral and upper margins; surface between punctures shiny (Fig. 2B).Malar area medially narrow, almost linear.antenna black, ventrally orange to reddish-brown.
Wings.Yellowish-brown; wing venation dark brown.legs.Integument black to dark reddish-brown.Vestiture of femora whitish-yellow, on tibiae and tarsi dark brown to black, scopae dark brown, ventrally hairs white to greyish-yellow.

Male
Body length.8.5-10.0mm.head.head slightly wider than long.Integument black except tip of mandible partly dark reddishbrown.Face sparsely covered with long, whitish-grey to brown, erect hairs intermixed with black hairs especially along the inner eye margins and on vertex.Clypeus mostly flat, apically almost impunctate; medially covered with medium-sized punctures that become gradually smaller and denser towards the lateral and upper margins; surface between punctures shiny.Malar area medially narrow, almost linear.antenna black, ventrally reddish-brown.
MetasoMa.Integument black, except T1 to a variable extend apically red, T2 red with a black spot anterior-medially, T3 either like T2 or in some specimens only apically with a red margin, T4 in some males with red basal and apical margins (Fig. 3C).T1 completely and T2 -T3 on disc sparsely covered with a few long erect yellowish-white hairs; T4 -T6 covered with short black hairs; apical tergal hair band missing on T1, on T2 -T5 narrow and sparsely white (Fig. 3C).Terga impunctate, finely shagreened with a silky shine (Fig. 3C).

Distribution
This species is only known from a few localities from Clanwilliam to the Nieuwoudtville area (Fig. 4).

Floral hosts
All specimens collected on the farms Papkuilsfontein and Glen Lyon were collected on Polygalaceae: Nylandtia scoparia.

Seasonal activity
July -September.

Diagnosis
Females of R. eardleyi sp.nov.can be separated from other Redivivoides species by a combination of the following characters: metasomal terga black to brown, T2 sparsely punctate with minute punctures and surface between punctures smooth and shiny, white apical tergal hair bands present (Fig. 5D), prepygidial and pygidial fimbria dark brown to black (Fig. 5D).The male is unknown.

Etymology
Named after Connal D. Eardley, Pretoria, who collected this species and to honour his outstanding contribution to african bee taxonomy.head.head wider than long.Integument black.Face sparsely covered with long, whitish-grey, erect hairs, along the inner eye margins and on vertex intermixed with black hairs (Fig. 5B).Clypeus convex in profile, apically impunctate; medially covered with fine punctures that become gradually smaller and denser towards the clypeal margins; surface between punctures smooth and shiny (Fig. 5B).Malar area medially narrow, almost linear.antenna black.

Distribution
There is only a single record of this species from the Karoo in the summer rainfall area (Fig. 9).

Floral hosts
unknown.

Seasonal activity
September.

Diagnosis
Females of R. kamieskroonensis sp.nov.can be separated from other Redivivoides species by their extensively and brightly red metasomal terga (Fig. 6D) in combination with the head that is distinctly wider than long (Fig. 6B).unlike other species the propodeal triangle is weakly shagreened.The male is unknown.European Journal of Taxonomy 34: 1-34 (2012) head.head much wider than long.Integument black except tips of mandible partly dark reddishbrown.Face sparsely covered with long, whitish-grey to brown, erect hairs intermixed with black hairs (Fig. 6B).Clypeus almost flat, slightly convex in profile in the lower part and slightly concave in the upper part, apico-medially and apical margin impunctate; clypeus otherwise densely (i ≤ d) covered with small punctures that become gradually smaller and denser towards the clypeal margins; surface between punctures shiny (Fig. 6B).Malar area medially about 1/4 to 1/5 as long as width of mandible base.antenna black, ventrally reddish-brown.
MetasoMa.Integument mostly black, red are the apical part of T1, all of T2 except for a small black spot anterior-medially, T3 except for a large black spot in the same position and apical margin of T4 (Fig. 6D).T1 and T2 on disc with long erect yellowish-white hairs; T3 -T4 covered with mostly blackish and very short erect hairs; apical tergal hair bands on T1 -T4 medially broad, consisting of short sparse white hairs; prepygidial and pygidial fimbriae black (Fig. 6A, D).Terga impunctate, finely shagreened with a silky shine (Fig. 6D).

Distribution
This species is only known from a single locality near Kamieskroon (Fig. 9).

Floral hosts
unknown.

Seasonal activity
September.

Diagnosis
Females of R. karooensis sp.nov.can be separated from other Redivivoides species by a combination of the following characters: metasomal terga black to brown, T2 densely punctate with large punctures and surface between punctures smooth and shiny, white apical tergal hair bands present (Fig. 7D), prepygidial and pygidial fimbria dark brown to black (Fig. 7D).These characters also apply to males (Fig. 8C) but the genitalia and S6 -S8 (Fig. 8D-h) should be checked to avoid potential confusion with the unknown male of R. eardleyi.

Etymology
named after the Karoo, the arid region in western and central South africa where this species was found.

Female
Body length.9.5-10.5 mm head.head slightly wider than long.Integument black except mandibles and labrum largely dark reddish-brown.Face sparsely covered with long, yellowish-grey, erect hairs intermixed with black hairs especially along the inner eye margins and on vertex (Fig. 7B).Clypeus slightly convex, apically narrowly impunctate; medially densely covered with medium-sized punctures that become gradually smaller and denser towards the lateral and upper margins; surface between punctures shiny or superficially shagreened (Fig. 7B).Malar area medially narrow, almost linear.antenna black, ventrally orange to reddish-brown.
legs.Integument black to dark reddish-brown.Vestiture of femora whitish-yellow, on tibiae and tarsi dark brown to black, scopae very sparse, dark brown to whitish-grey.

Male
Body length.8.5-10.5 mm.head.head slightly wider than long.Integument black except tip of mandible partly dark reddishbrown.Face densely covered with long, yellowish-brown, erect hairs intermixed with black hairs along the inner eye margins and on vertex.Malar area medially narrow, almost linear.antenna black, ventrally yellowish to reddish-brown.

Distribution
The species is known from a few places in southern namaqualand and low lying areas west of the Cedarberg Mountains (Fig. 4).

Seasonal activity
July -September.

Diagnosis
Males and females of R. namaquaensis sp.nov.can be separated from other Redivivoides species by their black to brown metasomal terga in combination with dark brown to black prepygidial fimbria and orange-brown pygidial fimbria (Figs 10D, 11C).

Etymology
named after namaqualand, the arid region in nW South africa where this species occurs.

Type material (71 specimens)
Holotype ♀, V.B. Whitehead, 16 Sep. 1999 head.Head slightly wider than long.Integument black except mandible and sometimes labrum partly dark reddish-brown.Face sparsely covered with long, whitish-grey, erect hairs intermixed with black hairs along the inner eye margins and on vertex (Fig. 10B).Clypeus mostly flat, apical margin almost European Journal of Taxonomy 34: 1-34 (2012) impunctate; medially densely covered with medium-sized punctures that become gradually smaller and denser towards lateral and upper margins; surface between punctures shiny (Fig. 10B).Malar area medially narrow, almost linear.antenna black, ventrally dark orange to reddish-brown.

KUHLMANN M., Revision of the bee genus Redivivoides
MesosoMa.Integument black.Mesoscutal disc between punctures smooth or superficially shagreened and shiny; disc densely (i = 0.5 d) and very finely punctate (Fig. 11B).Mesoscutum, scutellum, metanotum, mesepisternum and propodeum covered with long white to yellowish-grey erect hairs, partly intermixed with a few black hairs.

Distribution
This species has the centre of its distribution on the Bokkeveld Plateau and in the Roggeveld Mountains with a few records southwest of that area (Fig. 9).

Diagnosis
Females of R. simulans can be separated from other Redivivoides species by a combination of the following characters: metasomal terga at least partly red (at least on a narrow stripe on the apical part of the discs of T1 -T3), metasomal terga with surface between punctures smooth and shiny (Fig. 12D), scutum at least on the disc between punctures smooth and shiny (Fig. 12C), and head about as long as wide (Fig. 12B).These characters also apply to males (Fig. 13C) but genitalia and S6 -S8 (Fig. 13D-h) should be checked to avoid potential confusion with the unknown male of R. kamieskroonensis.

KUHLMANN M., Revision of the bee genus Redivivoides
Both sexes of R. simulans were described in detail by Michener (1981).

Diagnosis
Females and males of R. variabilis can be separated from other Redivivoides species by their black to brown metasomal terga which are smooth and shiny between punctures and that lack white apical hair bands (Figs 15E-F, 16E).This is the only Redivivoides species where terga have an intense oily bluish shine.

Etymology
The species is named after the colour variation of the females.

Description Female
Body lengTh.12.0-13.0mm.head.Head slightly wider than long.Integument black except median part of mandible and sometimes labrum partly dark reddish-brown.Face sparsely covered with long, whitish-grey (in the dark form all black, Fig. 15B), erect hairs intermixed with black hairs along the inner eye margins and on vertex KUHLMANN M., Revision of the bee genus Redivivoides (Fig. 15C).Clypeus mostly flat, apically almost impunctate, punctures here large and scattered becoming rapidly smaller and denser towards the upper edge; surface between punctures shiny (Fig. 15C).Malar area medially narrow, almost linear.antenna black, ventrally sometimes partly dark reddish-brown.
legs.Integument black to yellowish-brown.Vestiture yellowish-brown, scopae yellowish-brown.In the dark form hairs of femora and most of tibiae black or dark brown, on tarsi yellowish-brown, scopae darker yellowish-brown (Fig. 15B).

Male
Body length.12.0-13.0mm.head.head slightly wider than long.Integument black except tip of mandible partly dark reddish-brown.Face densely covered with long, whitish-grey to yellowish-brown, erect hairs intermixed with black hairs along the inner eye margins and on vertex.Malar area medially narrow, almost linear.antenna black, ventrally dark reddish-brown.
MetasoMa.Integument black, except apical tergal margins partly narrowly brownish translucent; T1 -T3 with intense oily bluish shine, T4 -T5 less so (Fig. 16a, C).T1 completely and T2 on disc covered with long erect yellowish-white hairs; T2 -T3 densely covered with short erect yellowish-white either yellowish-white or black on T4 and black on T5 -T6; apical tergal hair band missing on T1, on T2 -T5 sparse and narrow, yellowish-white to white (Fig. 16A, C).Terga densely but finely punctate, smooth and shiny between punctures (Fig. 16C).T7 with pygidial plate that is reduced to a narrow longitudinal, slightly elevated and shiny ridge.
European Journal of Taxonomy 34: 1-34 (2012) or processes reduced to small sclerotic structures like in Melitta budensis (Michez & Eardley 2007).In Rediviva and Redivivoides S7 in turn has a small disc with the apex bifid and/or with membranous lobes and the gonostyli are relatively long (Michener 1981(Michener , 2007)).
The differentiation of Rediviva and Redivivoides males is problematic.Michener (1981Michener ( , 2007) ) suggested that the broad, subtrunctate apex of the male S7, with its large laterally attached, vertical, membranous hairy lobes (Fig. 13E) is a unique apomorphy of Redivivoides.however, these characters seem to be species specific for R. simulans and they are either absent (R. karooensis, R. namaquaensis) (Figs 8E,11E) or reduced (R. capensis, R. variabilis) (Figs 3E, 16E) in the other four species (the males of R. eardleyi and R. kamieskroonensis are unknown).Michener (1981) mentioned the weak pygidial plate in male R. simulans as a character differentiating Redivivoides from both Melitta and Rediviva.a pygidial plate is also present in male Macropis and in R. variabilis, where it is reduced to a narrow longitudinal, slightly elevated and shiny ridge but it is missing in all the other three species making it unsuitable as a differentiating character.
Generally, the morphology of S7, S8 and the genitalia of Redivivoides males (Figs 3,8,11,13,16) reflect much of the morphological diversity known from the much more species-rich Rediviva as illustrated in Whitehead & Steiner (2001) and Whitehead et al. (2008).although well characterized as species, the obvious lack of apomorphic characters defining the males of Redivivoides at the genus level make their identification difficult and indicate the close relationship of both genera as suggested by Michener (1981) and Michez et al. (2009).

Origin of oil-collecting
The origin of oil-collecting in bees has been much debated and this behaviour has evolved independently at least five times in the Centridini, Ctenoplectrini, Exomalopsini, Tetrapediini and Melittinae (Buchmann 1987;Vogel 1974Vogel , 1986Vogel , 1990;;Renner & Schaefer 2010).Within the Melittinae floral oil is collected by bees of the genera Macropis and Rediviva (Michener 2007).Melittids are the most basal bees (Danforth et al. 2006) and, thus, they can be a key-group for understanding the evolution of oil-collecting in bees in general.Michener (1981) and later Michez et al. (2009), based on the results of a phylogenetic study, discussed whether oil-collecting has evolved only once in melittids or if there are two independent origins in Macropis and Rediviva.
In both scenarios the phylogenetic position of Redivivoides is crucial to understanding the evolutionary history of early bees.In Michez et al.'s (2009) analysis Redivivoides arose from Rediviva, making the latter paraphyletic, indicating a loss of oil-collecting in Redivivoides.however, only two of the currently 24 described Rediviva species and only R. simulans of the now seven known Redivivoides species were included in the study.A broader approach including more species is required to confirm the paraphyly of Rediviva.
If Redivivoides evolved from Rediviva the question is why Redivivoides is only present in the winter rainfall region in the west of South africa whereas Rediviva also occurs in the summer rainfall area in the east of the country.Either Redivivoides evolved in the winter rainfall region and has not spread to the east of South africa or it became extinct there.an interesting parallel case is the 11 of 35 described species of the Colletes fasciatus-group in western South africa that have a reduced scopa, which is unique in the genus (Kuhlmann 2006(Kuhlmann , 2007)).
Based on the present taxonomic revision there is now additional evidence that Redivivoides species might have lost their oil-collecting structures, as presumably happened in some neotropical Centris species (Michener 2007).With the exception of Redivivoides all non oil-collecting genera of the Melittinae have a slender hind basitarsus and a dense scopa with at least some branched long hairs.In contrast, the KUHLMANN M., Revision of the bee genus Redivivoides hind tibia and basitarsus of oil-collecting Macropis and Rediviva is very broad and the scopa consists of densely plumose, short pilosity for oil-collecting embedded in a matrix of sparse, long, simple, emergent hairs (Fig. 1a-D) (Michener 1981), with the latter reminiscent of Redivivoides (Fig. 1E-F).Thus, the broadened and posteriorly curved hind basitarsus lacking an apical process (present in Melitta, Macropis and in modified form in some Rediviva), the sparse scopa consisting of only simple hairs in Redivivoides and the lack of a penicillus (present in Melitta and modified into a brush-like structure in Rediviva and Macropis) might be remnants indicating a loss of oil-collecting structures.This view is supported by the phylogenetic position of R. simulans, arising from Rediviva, rendering Rediviva paraphyletic (Michez et al. 2009), the similar structure of male genitalia, S7 and S8 and a study of fore and mid leg anatomy by Steiner & Cruz (2006) suggesting that Redivivoides has descended from an oil-collecting ancestor.
The close relationship of Redivivoides and Rediviva is also reflected in flower visitation.Most Rediviva collect floral oil on Scrophulariaceae (Whitehead & Steiner 2001;Whitehead et al. 2008) and pollen from this plant family is also a major constituent of female scopal pollen loads (Kuhlmann unpubl.)but it is rarely used by other Melittidae (Michez et al. 2008).Whilst no information is available on flower visitation of R. eardleyi sp.nov.and R. kamieskroonensis sp.nov.and only a single observation for R. capensis sp.nov.all the other Redivivoides species were found visiting Scrophulariaceae with R. karooensis sp.nov.and R. namaquaensis sp.nov.obviously having a preference for this family.Although Kuhlmann & Eardley (2012) showed that Scrophulariaceae are visited and their pollen collected by a range of bee species it is usually only a minor component in scopal pollen loads (Kuhlmann unpubl.).Thus, the shared preference for Scrophulariaceae even though only based on a small number of observations can be seen as another indicator for the common ancestry of both genera.however, a robust phylogeny including more species of Rediviva and Redivivoides is required to better understand the evolution of oil-collecting and phylogeography of both genera.