The Colletinae: Going to Ground

In a recent post, I considered one of the families of short-tongued bees, the Halictidae. In this post, I'll turn my attention to members of one of the other short-tongued bee families, the Colletidae. Specifically, I'm looking at members of the subfamily Colletinae.

Mating ball of male ivy bees Colletes hederae, copyright Charles J. Sharp.

Members of the Colletidae differ from other bee families in that their glossa, the 'tongue' at the end of the proboscis, is apically bilobed or bifurcate. They are also distinctive in lining their nests with a plasticky, cellophane-like material. It has been thought that this material was made from dry saliva but the bulk of it is now known to come from a large gland in the abdomen that opens near the base of the sting (Almeida 2008). A nesting female will swallow droplets of the glandular secretion from her partially protruded sting then regurgitate it as she licks the wall of the nest cell. This waterproof lining both protects the cell from outside elements while preventing the loss of moisture from within. Many colletids, including colletines, leave the cell food provisions in a semi-liquid state; other bees whose nests are less watertight will dry and compact the provisions, presumably because the bulk of them would otherwise be lost before the larva hatched. In colletines, the egg is attached to the cell lining when laid, suspended above the provisions for the hatching larva to swandive into upon emergence. All colletids are solitary nesters with species nesting either in burrows in the ground or in hollows in vegetation; the majority of colletines are ground nesters*.

*One species, Colletes daviesianus, has apparently taken in Germany to boring its nests in the sandstone and mortar used in building construction.

Female Colletes daviesianus, copyright Donald Hobern.

In his 2007 edition of The Bees of the World, Charles Michener recognised five subfamilies within the Colletidae. The Colletinae were distinguished from three of these subfamilies by their retention of a covering of dense hair over the body (from the last subfamily, the Diphaglossinae, they differ in features of the glossa and wing venation). The hind leg of the female bears a well-developed scopa (dense arrangement of hairs for the carrying of pollen) on the femur and tibia with a corbicula (bare patch within the scopa where a ball of compacted pollen may be carried) on the underside of the femur. Hairiness is an ancestral characteristic for bees and phylogenetic studies have established that the Colletinae as recognised by Michener is a paraphyletic grouping (e.g. Almeida & Danforth 2009). As a result, it has been further subdivided with the name 'Colletinae' now restricted to what Michener had recognised as the tribe Colletini. As such, the Colletinae now includes just two genera of moderate-sized bees (seven to sixteen millimetres in length). The larger of these, Colletes, is found in temperate and tropical regions around the world except for the Indo-Australian region where it is notably absent. The other genus, Maurecolletes, is restricted to South America. One of the most distinctive features of Colletinae in the strict sense compared to other ex-colletines is the lack of the basitibial and pygidial plates, flattened and hardened plates possessed by other hairy colletids at the base of the hind tibia and at the end of the abdomen.

The absence of these plates is intriguing in light of the ground-nesting habits that seem to be the norm for Colletes (the nesting habits of Maurecolletes seem to be unknown). In other ground-nesting bees, the basitibial and pygidial plates are used to press the soil of the nest walls and opening into place. One would think this would mitigate against their loss. An explanation may be provided by the fact that some South American Colletes nest in the hollows of dead, pithy plant stems instead of in the ground, a characteristic shared with members of the less hairy colletid subfamilies belonging to the sister group of the colletines (Almeida & Danforth 2009). Ground-nesting Colletes species also bear noteworthy resemblances to stem-nesting colletids. Nest cells are closed with a layer of the cellophane-like wall membrane rather than the earthen plugs used by other ground-nesting bees. In many species, cells are lined up in a burrow divided by transverse partitions rather than placed in their own individual side branches. The possibility has been suggested that stem-nesting arose within the common ancestors of modern colletines and less hairy colletids. Ground-nesting in Colletes would then represent a secondary reversion by these species to the previous habit. When they did so, they retained the adaptations and habits that had originally been associated with their time in the twigs.

REFERENCES

Almeida, E. A. B. 2008. Colletidae nesting biology (Hymenoptera: Apoidea). Apidologie 39: 16–29.

Almeida, E. A. B., & B. N. Danforth. 2009. Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes. Molecular Phylogenetics and Evolution 50: 290–309.

Michener, C. D. 2007. The Bees of the World 2^nd ed. John Hopkins University Press: Baltimore.

The Halictidae: Short Tongues and Waxy Chambers

In an earlier post, I introduced you to the diverse group of bees known as the Halictinae. In this post, I'm going to take a step back and consider the family of bees to which the halictines belong, the Halictidae.

Nomia sp. feeding at a flower, copyright Graham Wise.

The Halictidae are one of the families of what are known as 'short-tongued bees' (the other short-tongued families recognised by Michener, 2007, are the Andrenidae, Colletidae and Stenotritidae). Bees have their mouthparts modified compared to those of other wasps to form a mobile proboscis. The tongue works in three main sections from base to tip. The first two sections work like the upper and lower parts of your arm, or of the arm of a crane, to extend and fold back the proboscis against the underside of the head. The third section beyond these two includes a flexible structure, the glossa, that may be thought of as working like the tongue proper to collect nectar and pollen from the inside of flowers. Somewhat self-explanatorily, this glossa is extremely long and slender in the families of 'long-tongued bees' (the Apidae and Megachilidae) but relatively shorter and broader in short-tongued bees. Naturally, these differences in tongue structure may be reflected in differences in which types of flowers the different types of bees chose to visit. Just to confuse matters, some species of Halictidae may have relatively long proboscides overall, but in this case the extra length is achieved by extending the length of the middle 'arm' section rather than of the glossa itself. The primary features separating Halictidae from the other families of short-tongued bees relate to the structure of particular sclerites incorporated into the proboscis that I'm not going to go into here, but notable points include that the glossa of Halictidae is pointed at the tip and hairs on it are usually branched or bifid at the tips.

Male Halictus tetrazonianellus with proboscis extended (the glossa is the orange structure at the end of the proboscis), copyright Gideon Pisanty.

For the most part, halictids are moderately built bees: neither remarkably slender nor particularly robust. Halictids vary extensively in size: many are small, even minute, but some may be relatively large by bee standards. Coloration is similarly variable, with both metallic and non-metallic species belonging to the family. Members of the genus Nomia (which tend to be relatively large for halictids) often bear contrasting bright bands across the back of the metasoma. Michener (2007) recognised four subfamilies within the halictids: the Rophitinae, Nomiinae, Nomioidinae and Halictinae, with the Halictinae being considerably more diverse species-wise than the other three. Nomioidines have sometimes been included by other authors within the Halictinae but, as there is a general agreement that nomioidines form the sister lineage of the halictines in the strict sense, the question of whether to combine them or not is purely a matter of semantics. Rophitines differ from other halictids in having a relatively large labrum whose tip remains visible between the mandibles when they are closed (other subfamilies have the labrum hidden by the closed mandibles). Rophitines, as well as kleptoparasitic halictines, also have the tip of the labrum simply truncate or rounded; in other subfamilies, the tip of the labrum in females is produced into a distinct process. Rophitines also have the scopa (the array of long pollen-carrying hairs on the hind leg) less developed on the trochanter and femur than on the tibia whereas other subfamilies (excluding, again, kleptoparasitic forms in which the scopa is reduced) generally have the longest scopal hairs on the femur. Nomiines commonly have the third submarginal cell on the wing (if present) as long as the first submarginal cell or at least more than twice the length of the second. In nomioidines and halictines, the third submarginal cell is much shorter. Another notable feature of the last two subfamilies is that the basal vein (the upper of the three veins radiating from the basal midline of the wing) is much more strongly curved near the base than in other bee families; this feature may or may not be discernable in rophitines and nomiines.

Just to show that bees can sometimes get insane: a male of the Colombian species Chlerogella anchicaya, from Engel et al. (2014).

For the most part, halictids construct their nests in burrows in the ground (some halictines nest in rotting wood). Cells of the burrows are generally lined with a wax-like membrane secreted by the parent bee. The membrane is duller and less watertight in Rophitinae than in other subfamilies; one rophitine genus, the southwest North American Protodufourea, appears to not produce such a membrane. Most non-halictine halictids are solitary nesters though some nomiines are known to work communally, and may even show low levels of division of labour. Kleptoparasitism is not known outside the Halictinae.

REFERENCE

Michener, C. D. 2007. The Bees of the World 2^nd ed. John Hopkins University Press: Baltimore.

The Osmiin Mason Bees

As I'm sure I must have had cause to say before, the world of solitary bees is a spectacularly diverse. Literally tens of thousands of species have been described to date, and no doubt many more remain. The classification of bees was reviewed by in great detail by Charles Michener (2007) in his monumental Bees of the World, and it was there that I turned to learn about the subject of today's post, the osmiins.

Female Osmia ferruginea, copyright Gideon Pisanty.

The Osmiini are currently recognised as a tribe of the Megachilidae, one of the two families of long-tongued bees (the other is the Apidae, including, among others, the majority of social bees). Megachilids are most easily characterised by the position of the scopa, a dense array of hairs used by bees for carrying pollen. In most bees possessing a scopa (it tends to be reduced or lost in kleptoparasitic forms), it is located on the hind legs but in megachilids it covers the underside of the metasoma. Osmiins are distinguished from other megachilids by the combination of a well developed sting, elongate stigma on the fore wing, arolia between the claws, and the lack of a pygidial plate. They are often smaller bees, less than a centimetre in length, though the largest osmiins grow close to two centimetres. Some osmiins are also more or less metallic in coloration, an unusual condition for megachilids. No feature has been identified that is unique to osmiins as a whole and their monophyly relative to other megachilid tribes (particularly the Megachilini) has long been called into question. A number of authors have recognised a division of living osmiins between two subtribes, the Osmiina and Heriadina. Osmiina have generally been distinguished from Heriadina by features such as a smaller stigma in the fore wing, a mesopleuron (a plate forming much of the side of the mesosoma) that is shorter ventrally than dorsally, and a propodeum that generally slopes downward from the base (rather than being initially flat). Again, however, the validity of this division has been questioned as no one feature uniformly distinguishes the two groups. A phylogenetic analysis of the Megachilidae by Gonzalez et al. (2012) did not support monophyly for Osmiini or either of its subtribes, but a proper revision of the group's higher classification remains to be done.

Female Hoplitis parana, copyright Gideon Pisanty.

Like other solitary bees, osmiins nest in cavities (a handful are kleptoparasites that do not construct their own nests). They often do not construct these cavities themselves but occupy pre-existing ones such as abandoned beetle burrows and hollows in wood, or crevices between rocks. Some species of Osmia have a predilection for nesting in empty snail shells. Cells are most commonly demarcated in the nest by walls constructed of chewed leaves, often held together with a sticky substance such as mud, resin or (more rarely) nectar. In some cases, the amount of leaf material used is reduced or abandoned, so the cell walls are made entirely of mud or resin. In some European species of Hoplitis, the cells are lined with petals; the species H. papaveris, for instance, lines its cells with bright red poppy petals. Osmia brevicornis, a species found in southern Europe and central Asia, is unusual in that its nest is not divided into cells. Instead, the nest cavity (an abandoned beetle burrow) is uniformly packed with pollen, with eggs being progressively inserted into the pollen mass as it is laid down. The larvae feed on the pollen around them after they hatch, and cocoons end up randomly scattered through the remains of the mass as they mature.

REFERENCES

Gonzalez, V. H., T. Griswold, C. J. Praz & B. N. Danforth. 2012. Phylogeny of the bee family Megachilidae (Hymenoptera: Apoidea) based on adult morphology. Systematic Entomology 37: 261–286.

Michener, C. D. 2007. The Bees of the World 2^nd ed. John Hopkins University Press: Baltimore.

Agenioideus: Average Spider Hawks

I have commented in earlier posts on the challenges of identifying spider hawks of the family Pompilidae, resulting from this wasp family's combination of high species diversity with a mostly conservative body plan. As a result of this conservatism, pompilid classification has tended to drift towards a situation where the majority of species are included in a relatively small number of somewhat vaguely defined genera. Each of the species included in one of these genera can be associated with other species in the genus, and groups of species approach each other closely enough that clear lines cannot be settled upon, but identifying features shared by all members of the genus can prove difficult. A good example of one such genus is Agenioideus.

Female Agenioideus birkmanni, from the University of Texas at Austin.

Species assigned to Agenioideus can be found pretty much worldwide though the greatest diversity occurs in warmer parts of the Holarctic. Though there does not seem to be a great deal of disagreement over which species should be placed in this genus, it seems a little difficult to say exactly what makes an Agenioideus. If anything, Agenioideus species seem to be associated by how relentlessly average they are, possessing a unique combination of characters that are none of them individually unique. They have wings with three submarginal cells, a broad metapostnotum in front of the propodeum, and legs ending in a small arolium with a weak comb of setae between a pair of long claws, mostly with a single small ventral tooth (Krogmann & Austin 2012). If you don't know exactly what those terms mean, just know that they are all quite unspecialised features for pompilids. Males often have asymmetrical claws on the forelegs, with the inner claw strongly bent and bifid while the outer claw is like those on the other legs, and the pterostigma (the dark node at the front of the fore wings) is relatively large compared to other genera. Females often have a comb of longer spines on the inner margin of the fore tarsi. But these last, more derived, features may not be universally present across all species of the genus.

Female Agenioideus nigricornis with redback spider Latrodectus hasselti as prey, copyright Mark Newton.

As befits their unspecialised appearance, most Agenioideus species (as far as we know) are relatively unspecialised in their nesting behaviour (Shimizu 1997). Like other pompilids, they lay their eggs on paralysed spiders that will provide food for the larva when it hatches. Most Agenioideus species construct simple nests with a single brood cell containing a single spider for each nest. One European species, A. nubecula, is known to produce slightly more extensive nests with up to four cells. The nest may be made by digging in loose soil or by using a pre-existing cavity; whether the wasp is more likely to do one or the other is correlated with whether she possesses a well-developed tarsal comb. A Japanese species, A. ishikawai, is known to at least partially dig a nest before capturing a spider, completing construction after bringing it back. The most specialised provisioning behaviour known for the genus, however, is found in another European species, A. coronatus. This species hunts jumping spiders which she paralyses with her sting as is standard. The paralysis, however, is only temporary, lasting just a few minutes, just long enough for the female to deposit an egg near the base of the spider's abdomen where it cannot easily remove it. The spider is then freed to go about its business without being placed in a nest, until the wasp larva hatches and feeds on its host in the manner of a parasitoid.

REFERENCES

Krogmann, L., & A. D. Austin. 2012. Systematics of Australian Agenioideus Ashmead (Hymenoptera: Pompilidae) with the first record of a spider wasp parasitizing Latrodectus hasselti Thorell (redback spider). Australian Journal of Entomology 51: 166–174.

Shimizu, A. 1997. Taxonomic studies on the Pompilidae occurring in Japan north of the Ryukyus: the genus Agenioideus Ashmead (Hymenoptera). Japanese Journal of Entomology 65 (1): 143–167.

The Ageniellini: Nest Evolution in Spider Wasps

The Pompilidae, commonly known as spider wasps or spider hawks, are a distinctive and often conspicuous group of wasps, well known for their practice of capturing spiders and sealing them paralysed into nest cells to serve as food for their developing larvae. Though spider hawks come in a wide range of sizes and colours, I can say from experience that they are often a challenging group of animals to work with taxonomically. Their superficial diversity often masks a certain structural sameness that makes it hard to develop a reliable system for the family. Nevertheless, one subgroup of the pompilids that has long been recognised as distinct is the subject of today's post, the Ageniellini.

Female Ageniella arcuata carrying a lynx spider, copyright Edward Trammel.

Agniellins are generally smaller spider wasps whose distinguishing features include a more or less constricted base to the metasoma, forming a petiole. Females have a collection of relatively long, forward-directed setae on the prementum, a sclerite on the underside of the head that forms the rear margin of the mouthparts (you could think of it as the wasp's 'chin'). As befits their smaller size, they provision their nests with smaller and medium-sized spiders. As well as paralysing the spider with their sting in the usual way, ageniellins will also often remove its legs before sealing it into a cell, though Barthélémy & Pitts (2012) observed that this might not be done with small spiders. The Ageniellini have been further divided between two subtribes, the Ageniellina and Auplopodina. In Ageniellina, the premental setae are relatively fine and the end of the metasomal dorsum (the pygidium) in females is rounded and hairy. In Auplopodina, the premental setae are further modified into strong, thick bristles and the female pygidium is more or less flattened and smooth. However, the aformentioned characters of Ageniellina are primitive and shared with non-ageniellin spider wasps. A phylogenetic analysis of the Ageniellini by Shimizu et al. (2010) reinforced the suggestion that 'Ageniellina' might be paraphyletic with regard to the monophyletic Auplopodina.

Auplopus carbonarius, copyright Fritz Geller-Grimm.

Ageniellini are of particular interest among spider wasps for the variety of nesting behaviours they exhibit, which were reviewed in detail by Evans & Shimizu (1996). The primitive nesting behaviour for pompilids, shared by species of 'Ageniellina', is to dig nest cells in holes in the ground. 'Ageniellina' construct short holes from pre-existing openings in the soil such as caves, crevices or the burrows of animals. The holes are closed by patting down soil using the end of the metasoma. The origin of the Auplopodina, however, saw a seemingly small innovation that was to have significant consequences: the evolution of the ability to carry a small amount of water in the crop. Initially, this allowed the wasps to nest in firmer ground than was previously possible, using water to soften the soil before digging. Many Auplopodina species still nest in this fashion. They could also carry balls of mud under the head using the basket of premental bristles, using the mud to close up holes. Eventually, they started using mud to build barrel-shaped nest cells above ground, bypassing the need to dig, and/or closing up suitable pre-existing cavities such as hollow plant stems or abandoned cells from other wasps. The most basic mud cells are still vulnerable to damage from rain and water so are built in sheltered locations such as attached to plant rootlets protruding from overhanging banks. However, some Auplopodina species have learnt to cover the outside of the cell with a coating of resin to provide water resistance and so are able to build in more exposed places such as underneath plant branches or leaves. Species of one genus, Poecilagenia, are kleptoparasites, breaking into the nests of other pompilids and closing them back up after depositing their own eggs inside.

Macromerella honesta females on a communal nest, from Barthélémy & Pitts (2012).

The greatest advance in nesting behaviour known from a handful of Auplopodina species is the appearance of communal behaviour, potentially derived from multiple factors. The need for suitable sheltered sites for nest-building places a premium on location, increasing the likelihood of intra-specific encounters. The ability to break down and re-purpose pre-existing nest cells rather than building entirely from scratch makes it worthwhile for females to linger around their own place of hatching. In one eastern Asian species, Machaerothrix tsushimensis, dominance behaviour has been observed around nests with one female largely monopolising cell construction and provisioning while other females remain largely inactive, only constructing their own cells when the dominant female is elsewhere. In other communal Auplopodina species, females will share in the construction and guarding of nest cells.

True eusocial behaviour as found in vespid wasps and bees is unknown in pompilids. It has been suggested that their practice of provisioning brood cells only at the time of the construction, without providing subsequent meals, may be a hindrance to sociability as there is little incentive for females to provide for the larvae of other individuals. Nevertheless, the Ageniellini demonstrate that basic communality is not beyond the abilities of spider wasps.

REFERENCES

Barthélémy, C., & J. Pitts. 2012. Observations on the nesting behavior of two agenielline spider wasps (Hymenoptera, Pompilidae) in Hong Kong, China: Macromerella honesta (Smith) and an Auplopus species. Journal of Hymenoptera Research 28: 13–35.

Evans, H. E., & A. Shimizu. 1996. The evolution of nest building and communal nesting in Ageniellini (Insecta: Hymenoptera: Pompilidae). Journal of Natural History 30 (11): 1633–1648.

Shimizu, A., M. Wasbauer & Y. Takami. 2010. Phylogeny and the evolution of nesting behaviour in the tribe Ageniellini (Insecta: Hymenoptera: Pompilidae). Zoological Journal of the Linnean Society 160: 88–117.

Ants in Bright Velvet

A paper that I've been intermittently working on for a while now finally saw publication last week. Authored by myself, Mark Murphy, Yvette Hitchen and Denis Brothers, the paper describes four new species of velvet ant from here in Western Australia.

Female Aglaotilla chalcea, photographed by yours truly.

Velvet ants are not actually ants but a distinct group of typically hairy wasps forming the family Mutillidae. They are strongly sexually dimorphic: females are wingless like ants but males have fully developed wings. They develop as kleptoparasites in the nests of other wasps, with the velvet ant larva feeding on the prey left to provision the host and/or on the host larva itself. Taxonomically, velvet ants are perhaps one of the more difficult wasp groups to work with. The high sexual dimorphism means that it is often impossible to match males with females unless one is lucky enough to catch them in the act of mating, and the mesosoma of females is highly sclerotised and fused with many of the characters useful for identifying other wasp groups no longer visible. The taxonomy of Australian velvet ants is particularly uncertain, almost to comical levels. A large number of species (possibly numbering in the hundreds) remain undescribed, and many of those species that have been described are yet not readily identifiable. No extensive survey of the Australian fauna has appeared since 1898 and most Australian species have been placed in a single genus Ephutomorpha. This genus was established by French entomologist Ernest André in 1902 with a definition that can basically be summarised as "Ugh, I can't even right now": it was explicitly intended as a dumping ground for Australian velvet ants that André was unable to sort more appropriately at the time. A vague promise to get onto it later never eventuated. Even at its time of establishment, Ephutomorpha included taxa that had already been designated as type species for genus names Bothriomutilla and Eurymutilla that should have taken precedence.

A few years ago, I was engaged in identifying wasp specimens collected by Mark Murphy as part of his research into pollinator ecology in the Western Australian wheatbelt. For those of you unfamiliar with the area, the Wheatbelt refers to a band of land inland from Perth. Most of the wheatbelt is rolling, semi-arid terrain that has been cleared for the growth of the eponymous wheat, with the indigenous forest largely reduced to isolated stands and reserves. Mark was studying the diversity of pollinator wasps in these remnant stands, most of which are dominated by wandoo Eucalyptus wandoo. As an example of the difficulties I was referring to above, I was able to recognise over two dozen morphospecies of velvet ants among specimens collected by Mark, only a couple of which I was able to even tentatively connect to known species. The specimens which formed the basis of the new publication came from a particular one of Mark's study methods, nest traps. Mark would leave wooden blocks into which holes had been drilled out in the field for a number of months, over which time they would hopefully be colonised by nesting wasps and bees (Mark was visiting traps once a month to check for nests). The holes were lined with paper tubes and if Mark found one that contained a nest, he would slide out the tube and take it back to the lab to be reared to maturity. Emerging wasps and bees were identified to species both by morphological examination and via the extraction of DNA for fingerprinting. Mark also found that he reared a number of parasitoids and kleptoparasites that were treated in the same way.

The male of Aglaotilla chalcea, also by yours truly.

I realised that this gave us an excellent opportunity regarding the mutillids, of which four identifiable species had emerged from Mark's nest samples. Because of Mark's rearing experiments, we had host data for all four species. Because of the use of DNA fingerprinting, we were able to identify both males and females of three of the four species (the fourth was recorded from a single nest that only provided us with female specimens). And at least two of the species appeared to be completely new to science. It didn't hurt that they were also all very attractive animals with brilliant metallic colours. So I prepared a manuscript describing all four species with myself, Mark and Yvette (who had done the DNA sequencing for the specimens) as authors and submitted it to the journal Zootaxa for consideration.

It was rejected.

That, as it turned out, was a good thing. One of the original reviewers was Denis Brothers of the University of KwaZulu-Natal, one of the world's leading authorities on velvet ants. Denis agreed that, while the paper couldn't stand as originally submitted, there was a definite value in what we were presenting. So he offered to help us with the composition. As well as correcting some misunderstandings I was guilty of regarding mutillid morphology (see my earlier comment on the difficulty of identifying features of the female mesosoma), Denis was able to confirm that all four of our species was actually new. He also informed us that they could be placed in a group of species that he had identified as part of as-yet unpublished research on Australian velvet ants and suggested that we establish a new genus for this group. This new genus was named Aglaotilla by Brothers (2018). Denis also added a new section to our manuscript summarising the recorded host data for Australian mutillids.

Aglaotilla species are mostly metallic in coloration, predominantly blue, green or purple (describing the colours of metallic wasps can be a challenge because the exact shade observed depends a lot on the incident lighting). One of our species, A. micra, has the mesosoma reddish with a purple gloss whereas an earlier described species A. discolor has the mesosoma entirely red. Females often have prominent spots or bands of clustered white hairs on the metasoma. Depending on the species, the colour pattern of the sexes may be similar or distinct. One of our new species, A. lathronymphos, has a species name that means 'secretly married' because without the DNA fingerprinting we would have had no reason to associate the bright blue males with the reddish-purple females. Females lack the rake-like spines on the fore legs and flattened plate at the end of the metasoma found in many other female mutillids. This almost certainly relates to their life cycle. Female velvet ants parasitising ground-nesting hosts use their fore legs to dig into the host nest and the terminal plate to tap down the ground after closing it back up. Aglaotilla females, where known, parasitise hosts that nest above ground in holes in trees and so do not need adaptations for digging. Three of the species we described, A. chalcea, A. lathronymphos and A. micra, were reared from the nests of crabronid wasps belonging to the genus Pison. The fourth species, A. schadophaga, was reared from the nests of resin bees. Aglaotilla species are very unusual among velvet ants in that more than one larva may grow to maturity in a single host nest cell; in all other mutillids for which host data is available, only a single individual will ever emerge from a single host.

A likely live female of Aglaotilla in search of a suitable host nest, copyright Mark A. Newton.

The Australian mutillid fauna includes a number of enticing taxa that deserve further examination: the strikingly patterned Australotilla species and the weird ant-associated Ponerotilla are just a couple of examples. Not to mention the hordes of new species that don't even have names yet. I have been pleased to make some contribution to this much-neglected family.

REFERENCES

André, E. 1902 Hymenoptera. Fam. Mutillidae. Genera Insectorum 11: 1–77, 3 pls.

Brothers, D. J. 2018. Aglaotilla, a new genus of Australian Mutillidae (Hymenoptera) with metallic coloration. Zootaxa 4415 (2): 357–368.

Taylor, C. K., M. V. Murphy, Y. Hitchen & D. J. Brothers. 2019. Four new species of Australian velvet ants (Hymenoptera: Mutillidae, Aglaotilla) reared from bee and wasp nests, with a review of Australian mutillid host records. Zootaxa 4609 (2): 201–224.

Miscophus littoreus

Face of Miscophus littoreus, from Andrade (1960).

For this post's semi-random subject, I drew the crabronid wasp species Miscophus littoreus. This small, mostly black wasp (about five millimetres in length) was described from Morocco by Nuno Freire de Andrade in 1960, with the original description seeming to still be the only source for information about it. Miscophus is a cosmopolitan genus, found on all continents except Australia and Antarctica (though its presence in South America seems marginal). They are characterised by wings with the outer veins reduced or lost so they have at most two submarginal and two discoidal cells, with the second submarginal cell (if present) triangular and petiolate, and mid-coxae that are very closely placed or touching each other along the midline. Miscophus littoreus is one of a group of closely related species within this genus found between north Africa and central Asia with the fuller complement of wing cells, and the features distinguishing it from other species in this group are rather fine: a slightly longer clypeus, a shinier and less punctate mesosoma. The wings are darker shaded towards the ends, and females have a tarsal comb (a series of longer spines along the front edge of the fore tarsus).

Another species of Miscophus, M. ater, from here.

There don't seem to have been any natural history observations made for M. littoreus itself but we can infer that it is probably similar in behaviour to other species of Miscophus. North American Miscophus species dig nests as short burrows in sandy soil, only a few centimetres in length (Bohart & Menke 1976); this is why the females have the tarsal comb. Nests have at most only a few cells each, often only one. The cells are stocked with small spiders, often juveniles (though I suspect the preference for juvenile spiders has more to do with size preference than anything else. The tendency in many Miscophus species to show a reduction in the wing venation is related to a broader tendency in the genus to not be enthusiastic fliers. Most Miscophus females run along the ground rather than fly when hunting prey, and they do the same when carrying prey back to the nest. At most, they may make only short hopping flights. Miscophus individuals on the ground may be mistaken for ants, which they often hang around while foraging, hoping to avoid attention while they search for unsuspecting spiders.

REFERENCES

Andrade, N. F. de. 1960. Palaearctic Miscophus: bicolor group and isolated species (Hymenoptera, Sphecidae). Memórias e Estudos do Museu Zoológico da Universidade de Coimbra 262: 3–136.

Bohart, R. M., & A. S. Menke. 1976. Sphecid Wasps of the World. University of California Press: Berkeley.

Wasps that don't Give to a Fig

The strategies employed by flowering plants to draw in their pollinators are many and varied. Some have entered into exclusive partnerships, contriving methods by which their rewards are shared with a single animal species and hence presumably increasing the likelihood of that species visiting them. Once remarkable example of such a partnership is found among the figs. To the casual observer, fig trees might appear to never produce flowers. However, immature figs are in fact closed inflorescences called syconia with the flowers produced on the inside of the fig, never exposed to the outside world. The only way for pollinators to reach the fig flowers is through a tiny hole or ostiole at the fig's apex. This ostiole is used by the fig's pollinators, tiny female wasps of the chalcidoid family Agaonidae, who enter the fig in search of places to lay their eggs. The wasp herself does not leave the fig again after laying but her eggs and larvae develop within galls inside the fig, feeding on the tissue of the fig itself. After developing into wingless males and winged females, the next generation of fig wasps mates within the syconium; pollination of the fig tree occurs through the young females leaving the fig to find their own laying places and carrying pollen as they do so.

Female Idarnes nr flavicollis, a typical late-laying sycophagine, copyright Sergio Jansen Gonzalez.

The fig benefits by having an exclusive pollinator, the fig wasp benefits by having a ready-made nursery for its offspring. However, all that tasty fig tissue is bound to prove attractive to others who would circumvent the standard contract. Another group of chalcidoid wasps, the subfamily Sycophaginae, includes prime examples of such freeloaders. Like the true pollinating fig wasps, these non-pollinating fig wasps develop in galls within fig syconia. However, instead of entering the fig through the ostiole, most sycophagines use their ovipositor to pierce the fig's outer skin and lay from outside. In some sycophagines, the ovipositor is relatively short and thick; these species lay their eggs when the fig is only just beginning to develop. In others, the ovipositor is longer and slender, longer in fact than the rest of the wasp, and oviposition happens later when the fig has grown to a larger size. In some of these later-arriving forms, the ovipositing female lays into a gall already induced by the fig's actual pollinator (how she finds it from outside the fig, I have no idea), and as well as feeding on the gall, her larva will eventually feed on the pollinator larva. There are also some sycophagines that enter the syconium through the ostiole and oviposit internally; I haven't been able to find whether these species may function as true pollinators.

Female Sycophaga ovipositing on Ficus sur, copyright JMK.

As noted above, pollinating agaonids exhibit strong sexual dimorphism with only the females having wings, and males never escaping the host syconium. The wingless males cannot be easily recognised as belonging to the same species as the females; indeed, if one does not already know what they are, they can barely even be recognised as wasps. In sycophagines, matters are a bit more complicated. In some species, males are wingless and highly modified as in pollinating fig wasps. In others, males are winged and similar in appearance to females. And in still others, wingless and winged males are both present within a single species. I don't know what determines whether a given larva of these species develops wings or not; both forms may develop within the same syconium. It has been suggested that the presence of the two forms is related to conflicting pressures of gene flow vs speed. Winged males that can look for mates outside the parent syconium have a better chance of finding mates outside the pool of their own siblings, thus avoiding the risk of inbreeding. However, wingless males can mate with females immediately after they emerge within the syconium (if not before, as I'll explain shortly), in which case the winged males may simply find themselves too late to the party. Certainly there is a correlation between winglessness and the size of broods. Early-ovipositing species, which tend to produce smaller broods because the younger host syconium offers less space for egg-laying, are more likely to have winged males whereas males of later-ovipositing species are more likely to be wingless (Cruaud et al. 2011).

Male Apocryptophagus, copyright Centre for Biodiversity Genomics.

Males of the genera Sycophaga and Apocryptophagus (which Cruaud et al., 2011, suggested should probably be synonymised) are invariably wingless and have elongate, flattened, extensible gasters. The terminal pair of spiracles on the abdomen have the surrounding peritremes (supporting rings) extended into a pair of long filaments. In the host figs of these genera, the interior of the syconium becomes filled with liquid after being pollinated by its associated agaonids; the liquid is resorbed when the pollinators emerge. Nevertheless, there are advantages for the sycophagines in emerging before the pollinators: not only could the interior of the syconium become rather crowded, males of some agaonid species have enlarged mandibles that they may use to dispatch any interlopers. So instead of waiting for the syconial fluid to drain away, the male Sycophaga cuts a small opening slit in his gall (too narrow for the surrounding fluid to seep in) through which he partially emerges into the central cavity. The peritremal filaments are used to anchor the end of his gaster within his original gall so that he can continue to breathe from the air-pocket inside it while he stretches out in search of another gall containing a female. When he finds one, he will cut into it in the same way that he cut out of his own, then release the end of his gaster from its anchor-point and quickly slip into the gall of his intended. After a brief mating, he can repeat the process, this time using the female's gall as his air-tank (Ramírez 1996–1997). The female presumably emerges once the syconial fluid is gone.

Male Apocryptophagus emerging from a gall containing a female, from Ramírez (1996–1997).

There have been various viewpoints about the relationships of Sycophaginae to other chalcidoids. Some authors have included almost all the fig-associated wasps in the Agaonidae, whether pollinators or not. Others have restricted the Agaonidae to the true pollinators and classified non-pollinating fig wasps such as the Sycophaginae with the poorly defined family Pteromalidae. An analysis of chalcidoid relationships by Heraty et al. (2013) identified Sycophaginae as a sister group to Agaonidae sensu stricto (while placing other groups of non-pollinating fig wasps elsewhere on the tree). This might lead one to consider the possibility that the gall-making habit seen in both Sycophaginae and pollinating Agaonidae pre-dates the evolution of the wasp-fig relationship as pollinators. Perhaps the evolution of the syconium allowed figs to convert gall-makers that had previously been parasites into partners.

REFERENCES

Cruaud, A., R. Jabbour-Zahab, G. Genson, F. Kjellberg, N. Kobmoo, S. van Noort, Yang D.-R., Peng Y.-Q., R. Ubaidillah, P. E. Hanson, O. Santos-Mattos, F. H. A. Farache, R. A. S. Pereira, C. Kerdelhué & J.-Y. Rasplus. 2011. Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea). BMC Evolutionary Biology 11: 178.

Ramírez, W. 1996–1997. Breathing adaptations of males in fig gall flowers (Hymenoptera: Agaonidae). Revista de Biologia Tropical 44 (3)–45 (1): 277–282.

Sweat Bees

For many people, the common domestic honey bee may be the only bee species that they are aware of. In fact, bees are incredibly diverse, with well over 17,000 species known worldwide (and counting). Not all bees live in social hives like honey bees: the majority are solitary, with individual females each constructing their own nest and stocking it with food stores for their young. One particularly diverse group of bees is the Halictinae.

Foraging Lasioglossum, copyright Beatriz Moisset.

Halictines are mostly small bees, sometimes referred to as 'sweat bees' owing to the predilection of many species for lapping up sweat from the skin of hot humans and other animals (a habit that, while generally harmless, can be rather annoying). They can be distinguished from other bees by a distinctive curve at the base of the basal vein in the forewing. Michener (2007) recognised two tribes within the Halictinae, the cosmopolitan Halictini and the strictly Western Hemisphere Augochlorini. Augochlorins are often bright metallic in coloration; Halictini are less commonly so. Even among bee specialists, halictines can be notorious for the difficulties involved in trying to make sense of them. For instance, the cosmopolitan genus Lasioglossum alone comprises over 1300 known species, and having spent my own time attempting to identify bee specimens back in Australia I can confirm that there are times when it feels like all Lasioglossum, all the time. The majority of halictines construct their nests in burrows in soil; some species build in rotting wood.

Female Augochlora pura mosieri, copyright Bob Peterson.

The Halictinae are a particularly interesting group for studies of bee evolution because they include both solitary and social species. Indeed, some species may be either depending on circumstances. The most common nest type in Halictinae involves a long central tunnel with radiating side branches leading to globular brood cells. In most Augochlorini and species of the genus Halictus, however, the cells are arranged in a single cluster that is suspended within an underground cavity, held in place by earthen struts or by the rootlets of plants. The cells are lined with a protective waxy membrane rich in lactones, secreted by the builder from a gland near the base of the sting. Some species may be communal, with more than one female sharing a single burrow but each building and laying in its own cells (such communality is not necessarily a step on the road towards true sociality but may be a response to a shortage of good nesting opportunities). In social species, the queen is commonly not that different in appearance from associated workers, and if the queen dies the workers may begin producing eggs of their own (if, indeed, they were not already doing so while the queen was alive). Some species, though, may exhibit development of a distinct soldier or major class among the workers with massively enlarged heads and mandibles. In the Australian species Lasioglossum hemichalceum, there may be similarly large-headed males. These big-headed males also have reduced wings, rendering them flightless and bound to the nest. No more than one major male may be present in a colony; if another such male is present, the two will fight to the death. Unlike honey bees, halictine colonies do not often live for more than one season; instead, males and reproductive females usually mate near the end of the growing season, followed by the death of the males. The females hibernate over winter before beginning construction of their own nests the following spring.

Sphecodes albilabris, copyright Fritz Geller-Grimm.

In contrast, a number of halictine species, such as members of the genus Sphecodes, do not construct their own nests but instead lay their eggs in the nests of other bees. This behaviour, known as kleptoparasitism, has arisen in many bee lineages and is usually associated with a recurring set of evolutionary trends. Many kleptoparasites are closely related to their hosts: most kleptoparasitic halictines attack the nests of other halictines though some Sphecodes species mooch off bees in more distant subfamilies and families. Kleptoparasitic bees are commonly less hairy than their self-sufficient relatives, as they have little or no need of the pollen-carrying hairs used by other bees. Many kleptoparasites are more heavily armoured than other bees, to protect them against host resistance. Female Sphecodes have blunt spines on the outside of the hind tibia that may help them push into a host nest. Females of most kleptoparasitic halictines destroy the host egg in a nest cell before laying their own egg; in contrast, bees of other kleptoparasitic lineages usually leave the host egg undisturbed and it is the parasitic larva that executes the host. In most cases, the kleptoparasitic female abandons the nest once she has laid there, but in some species parasitising social hosts, the kleptoparasite may remain in the nest and inveigle herself into society there, continuing to enjoy the fruit's of her hosts' labours.

REFERENCE

Michener, C. D. 2007. The Bees of the World 2^nd ed. John Hopkins University Press: Baltimore.