Revision of the bee genus Capicola (Hymenoptera: Apoidea: Melittidae) distributed in the Southwest of Africa

The bee family Melittidae (Hymenoptera: Apoidea) includes 14 genera. Most have been reviewed but not the small African genus Capicola. The present work aims to fill this gap. Based on the revision of the type material and 1272 additional specimens, we provide a comprehensive synonymic and annotated catalogue of the 12 Capicola species sensu Michener (1981). Lectotypes are designated for the previously established species Capicola braunsiana (= C. obscura syn. n.), C. cinctiventris, C. femorata, C. flavitarsis and C. rufiventris. Moreover, C. danforthi sp. n., C. flavicara sp. n., C. gessorum sp. n., C. micheneri sp. n., and C. richtersveldensis sp. n., are newly described, as well as the previously unknown female of C. nanula, male of C. nigerrima and male of C. rhodostoma. New synonymies are proposed for C. braunsiana (= C. obscura) and C. flavitarsis (= C. cinctiventris). An original dataset of 20 morphological characters is used for the inference of the 12 species’ phylogenetic relationship. A key to species is provided. In addition, the ranges of the 12 taxa are mapped and discussed. This paper contributes to a global revision of the Melit tidae.

Analysis.The dataset (Table 1) was analysed in two ways using PAUP 4.0b10 (Swofford, 2001).A heuristic parsimony search was first made with Dasypoda hirtipes and Hesperapis regularis as outgroups (ingroup = 12 Capicola species).The starting tree was obtained by stepwise addition.10,000 random additional sequences were performed during the search.The branch swapping option was kept as default (TBR).All minimal trees found during branch swapping were kept.The most parsimonious trees yielded were used to compute a strict and a 50% majority rule consensus.The effect of successive weighting method (along ten steps of reweighting) was tested using the same analytical framework.In this case, the most parsimonious trees yielded on the final (tenth) step were used to draw a strict and a 50% majority rule consensus.The bootstrap (150 replicates) support values were computed both considering the characters of equal weight and after the last reweighting step.
Alternatively, an exhaustive search was also performed (ALLTREES).H. regularis (outgroup) and C. rufiventris (ingroup) were cancelled from the dataset, to bring the number of taxa to 12, which is the upper limit for exhaustive search in PAUP.

Biogeography, phenology and host plant affiliation
We synthesised the biogeography, phenology and host plant information in a catalogue.Species are listed following alphabetical order.The synonyms are quoted under the priority species name in chronological order with references to their original description and subsequent citations.In addition, we give the holotype depository and the locus typicus for each species.
The non-type specimens information is also quoted using the following standardisation of the labels' data: locality, coordinates (or conventional coordinates in decimal degrees when not on the label), date, collector, plants visited and depository.
The labelling data provided information for the host plant of 370 specimens of Capicola.Most of these data are from the expeditions of F.W. and S.K. Gess (AMGS), and J.G. Rozen (AMNH).

Cladistic analysis
The heuristic search based on the dataset (Table 1) yielded two equally parsimonious trees of length = 46, CI = 0.6087 and RI = 0.7465.The same search after ten steps of successive weighting of the characters yields one tree with the same topology, length = 21, CI = 0.784 and RI = 0.8821.The strict consensus of the trees from unweighted analysis is displayed in Fig. 100.The exhaustive search produces six trees, length = 44, CI = 0.6364 and RI = 0.7288 (Fig. 101).
Based on the previous trees, three species-groups could be identified within Capicola (of which monophyly was strongly supported by the yielded topologies).The first of these groups include C. aliciae + C. micheneri [= subgenus Capicoloides sensu Michener (1981)] associated with C. braunsiana, C. rhodostoma and C. nanula.The bootstrap value for C. aliciae + C. micheneri was notably high (88, 99 with weighted characters).On the contrary, grouping within the three other species received only low support: 47 (77 after weighting) for basal node and 41 (57 after weighting) for C. nanula + (C.braunsiana + C. rhodostoma) (Fig. 100).This latter clade was not displayed by the consensus of the six trees yielded by an exhaustive search (Fig. 101).In this topology C. braunsiana, C. rhodostoma and C. nanula branched off a basal polytomy.The second group, C. rufiventris, C. flavitarsis, C. richtersveldensis, C. nigerrima, C. gessorum and C. danforthi, was better supported by bootstrap values.The basal node had a bootstrap support = 79 (91 when characters were weighted) and all derived nodes received support higher than 50 (Fig. 100).The topology of this clade was conserved in the exhaustive search (Fig. 101).C. flavicara alone constituted the third group among Capicola.
The first species group is characterized by the derived state of the characters 8 and 9, namely the clypeus punc- tuation and the propodeum declivity.The second species group is characterized by the descriptors 15, apical expansion of Tb3, 17, apical emargination of S6, and 20, presence of hairy grooves on gonostyli.C. flavicara is characterized by the yellow coloration of clypeus (character 4) and the shape of the head, which is longer than wide (character 1).
First -last observations.14.ix to an unspecified date in November.

Capicola flavicara Eardley sp. n.
Diagnosis .& and %.Head longer than wide.Integument of antenna, supraclypeal area, clypeus, labrum, mandible, scutum, scutellum, fore and middle legs yellow or orange.Maxillary palpus a little shorter than labial palpus, the latter not quite reaching end of glossa.Maxillary palpus a little shorter than galea, which is subequal in length to labial palpus.Outer surface of galea sculptured.Compound eyes with upper and lower  Description.&.Head.L = 2.2 mm; W = 2.0 mm.Head longer than wide.Integument of antenna, supraclypeal area, clypeus, labrum and mandible yellow or orange, remainder black.Face, genal area and preoccipital ridge with white hairs.Face shiny, with fine punctation.Maxillary palpus a little shorter than labial palpus, the latter not quite reaching end of glossa.Maxillary palpus a little shorter than galea, which is subequal in length to labial palpus.Outer surface of galea scluptured and mat.Malar area shorter than A2.Face and vertex densely but weakly punctate (i = 2d).Clypeus about twice as wide as long; with many small, shallow punctures, without mediolongitudinal groove.Compound eyes not converging.Mesosoma.L = 2.4 mm.W = 1.6 mm.Integument of pronotum, scutum and scutellum orange, remainder black.Mesoscutum and scutellum shiny, densely but weakly punctate (i = 2d).Mesepisterna and metanotum with long, white hairs.Propodeum seen in profile with horizontal basal area.Propodeal triangle hairless, mostly shiny, with basal reticulate sculpture; remainder of propodeum mat.Legs.Integument of legs 1-2 mostly orange, leg 3 mostly blackish; vestiture white.Inner surface of tarsus 3 with orange hairs.Spurs of Tb2 with about eight very small spines.Wings.Surface transparent.Two submarginal cells, the first longer than the second.Basal vein slightly curved.Metasoma.L = 3.6 mm.W = 2.2 mm.T1-T2 and S1-S2 reddish, remainder of metasoma dull black, with reticulate sculpture and weak punctures.T1-T4 with white, continuous apical fringes.Prepygidial fimbria black.Premarginal lines curved anteriorly medially.Pp shallowly concave, reddish, without medio-longitudinal carinae.%.Head.L = 1.9 mm.W = 1.8 mm.Head slightly longer than wide.Integument of antenna, supraclypeal area, clypeus, labrum and mandible, yellow or orange, remainder dull black.Face, genal area and preoccipital ridge with white hairs.Vertex shiny, with fine punctation.Maxillary palpus a little shorter than labial palpus, the latter not quite reaching end of glossa.Maxillary palpus a little shorter than galea, which is subequal in length to labial palpus.Galea sculptured and mat.Labrum not swollen.Malar area shorter than A2.Clypeus about twice as wide as long, with small, shallow punctures, without a medio-longitudinal groove.Compound eyes converge slightly ventrally.Face and vertex with small, shallow punctures.A3 longer than A4.Mesosoma.L = 2.0 mm.W = 1.3 mm.Integument of scutum, scutellum, propodeum orange; remainder dull black.Vestiture generally long and white (partly damaged and cannot be fully described).Mesoscutum, scutellum, metanotum and propodeum with small, shallow and dense punctures (i < d).
First -last observations.Unspecified date in September to 23.xi.
Host plant.Unknown.First -last observations.17.x -unspecified date in February.
Description.&.Head.L = 1.3 mm; W = 2.2 mm.Head wider than long.Integument mostly black.Mandibles base, labrum and clypeus yellow to reddish.Clypeus, face, genal area, vertex and preoccipital ridge with yellow or orange appressed hairs.Face shiny.Labial palpus three-fourths as long as maxillary palpus, reaching beyond apex of glossa.Maxillary palpus twice as long as galea.Outer surface of galea sculptured.Malar area shorter than A2.Face and vertex densely, but weakly punctate.Clypeus three times as wide as long; with few deep punctures and a medio-longitudinal groove.Compound eyes converging ventrally.Antennae ventrally reddish, dorsally brownish to entirely yellow.Mesosoma.L = 1.5 mm.W = 1.1 mm.Integument black.Mesoscutum and scutellum shiny (some specimens with short appressed hairs), densely but weakly punctate, punctures more than width puncture apart.Mesepisterna and metanotum with long, erect, yellowish hairs.Propodeal triangle hairless, entirely rugose, with basal area horizontal.Propodeum mat.Legs.Integument yellow to reddish.Fore legs with yellowish hairs.Inner surface of mid legs with yellow hairs.Outer side of mid legs with long white appressed hairs.Hind legs with yellowish hairs, scopa sparse.Spurs of Tb2 with about six small spines.Tb3 and Bt3 with red spots at the hair base.Wings.Surface transparent.Two submarginal cells, the first longer than the second.Basal vein slightly curved.Metasoma.L = 2.7 mm. W = 1.4 mm.Terga and sterna reddish.Discs of terga shiny, with weak punctures.T1 apical hair band interrupted medially to continuous.T2-T4 with white continuous apical hair bands.T2-T4 with brown spot on lateral margin.Prepygidial fimbria yellowish.Sterna shiny.Sterna and terga with straight premarginal line.Pp with median subparallel carinae, proximal region of carinae narrow and weakly depressed (Figs 58-59); base reddish; apex red.

Morphology and taxonomy
The species included in Capicola are unambiguously characterized by some morphological structures like proboscis proportions, body size, punctuation of clypeus, propodeal triangle, shape of hidden sterna % (S6-S8) and genitalia %.The shape of the females' pygidial plate is diagnostic for many species, what is notably unusual in melittids (except in Dasypoda females; Michez et al., 2004a).
Our cladistic analysis does not support the former subdivision of Capicola into two subgenera Capicoloides and Capicola (Michener, 1981(Michener, , 2000)).The group described by Michener (1981) as Capicoloides is monophyletic, robust and supported by high bootstrap values (Fig. 100).However, the large species group designated At a higher taxonomic level, our previous proposal leads to the acknowledgement of seven subgenera -all Nearctic -within Hesperapis namely: Amblyapis Cockerell, 1910, Carinapis Stage, 1981, Disparapis Stage, 1981, Hesperapis s. str., Panurgomia Viereck, 1909, Xeralictoides Stage, 1981 and Zacesta Ashmead, 1899.Moreover, the Dasypodaini would then include four genera: Capicola, Dasypoda Latreille, 1802, Eremaphanta and Hesperapis.The phylogenetic relationships among these genera need re-evaluation through a global analysis.Interesting preliminary clues on the result of such analysis were suggested by Engel (2005) who grouped Capicola and Eremaphanta within the subtribe Hesperapina.Several of our own observations give us additional insights supporting this proposal, notably in the C. flavicara morphology (flatness of the female's pygidial plate and the shape of the head).
Other questions concerning the higher taxonomic levels are (1) the taxonomic status of sub-genera of Hesperapis; (2) the nature of the phylogenetic relationships between these taxa, and (3) the relationships between Dasypodaini and the other tribes of the Dasypodainae (Promelittini and Sambini).

Biogeography
Capicola distribution is mostly restricted to the xeric part of south-western Africa (Figs 92-93).The diversity pattern seems unipolar (Figs 94-99) contrary to the bipolar one of species like those in Colletes Latreille, 1802 (Kuhlmann, 2005).The centre of endemism is clearly in the Western Cape Province's Succulent and Nama Karoo biomes, which have the world's highest temperate floral diversities (Kuhlmann, 2005).The distributions of several species extend northward into Namibia and eastward in the Eastern Cape Province.One species that is recorded outside this area is C. micheneri which is an Namibian endemic species.
The narrow range of Capicola is remarkable compared to the distribution of their closest relatives among Dasypodaini: Hesperapis and Eremaphanta, which are respectively Nearctic and Central Asian (Michener, 1981;Michez & Patiny, 2006).The distribution of the group formed by these three taxa includes two large disjunctions, the origins of which could be well explained by a serie of extinction events.The potential causes for these extinctions are likely to be the consequences of major climate changes undergone in these regions during the Quaternary period (Marchant & Hooghiemstra, 2004).
The host plants of Capicola are very common in South Africa.The families Aizoaceae, Asteraceae and Fabaceae are also very attractive to many other oligolectic bee species (Gess & Gess, 2004).

Host plant in the context of Capicola phylogeny
The results of the phylogenetic analysis seem coherent with the host plants ( cola.According to the tree topology, the specialisation on Fabaceae, Asteraceae and Campanulaceae has each evolved once.

as
Capicola s.str. is obviously not monophyletic.The five species originally included in the latter taxon (C.braunsiana, C. cinctiventris (= C. flavitarsis), C. flavitarsis, C. nanula, C. rufiventris) are associated in two distinct clades.Moreover, the relationships of three species (C.braunsiana, C. nanula and C. rhodostoma) remain uncertain based on the available knowledge.Acknowledging subgenera in Capicola based on the previous trees would consequently lead to numerous taxonomical changes, a critical taxonomic inflation and no significant improvement of the systematic relevance.We propose thus to pool the twelve species in one single genus including several (at least three) monophyletic groups of species.

TABLE 1 .
Character-state matrix for cladistic analysis.
Etymology.Named after Prof. C.D. Michener who is an early reviewer of Melittidae.