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.