Sympiesis

Female Sympiesis, copyright Lyle J. Buss.

We often imagine that parasites select their hosts largely on the basis of type: one parasite prefers caterpillars, for instance, while another prefers flies. However, sometimes what is important is not so much what type of host a parasite attacks, as where they find it. The wasp in the photo above represents Sympiesis, a sizeable genus (the Universal Chalcidoidea Database lists over 130 species) of microscopic parasitoid wasps found worldwide. The majority of Sympiesis larvae attack the larvae of Lepidoptera, but others feed on the larvae of Diptera. A few have been recorded as hyperparasitoids, attacking the larvae of other parasitic wasps. The main thing that all hosts of Sympiesis have in common, though, is that they are all found in secluded, vegetative habitats: either mining in leaves, or in retreats formed by rolling or tying leaves (sometimes boring in stems). Depending on species, Sympiesis larvae may be either ectoparasites or endoparasites: those species feeding on leaf-rolling hosts tend to be ectoparasites, while those targeting leaf-miners are endoparasites (Miller 1970).

Sympiesis is a genus of the chalcid family Eulophidae. Eulophids used to be the subject of some disagreement between myself and a colleague of mine about their ease of recognition. Eulophids are a diverse group in appearance, coming in a bewildering array of shapes and colours. However, I have always maintained that they are nevertheless readily recognisable. Whatever their appearance, eulophids seem to always a distinctive stamp of 'eulophid-ness'. They tend to be slender, relatively soft-bodied wasps, often with a flat top to the gaster. Most identification guides will tell you to look out for their four-segmented tarsi (as opposed to the five-segmented tarsi of most other chalcid wasps); eulophid tarsi are rendered even more recognisable by the point that, though they have less segments than the tarsi of other chalcids, they are not any shorter so the individual tarsal segments are all relatively long. The features distinguishing Sympiesis from other eulophid genera are, of course, finer and require fairly close examination: notably, they have relatively few dorsal setae (only four on the scutellum) (Bouček 1988). As far as I know, they are mostly metallic green in coloration.

Male Sympiesis, showing branched antennae, from here.

As with many eulophids, males of Sympiesis usually differ from females in having long branches on the antennae. However, the first species of the genus to be described, the European Sympiesis sericeicornis, is distinctive in that these antennal branches are much reduced so that the males' antennae look little different from the females' (if you look very closely, they still have just a bit of a finger on each of the middle antennal segments). This led historically to a fair bit of confusion in the recognition of Sympiesis, with many species originally being placed in segregate genera (often with tongue-twistery compound names such as Asympiesiella or Sympiesonecremnus; thank you again, Alexandre Girault). Even now, the status of Sympiesis with regard to some related smaller genera could do with further investigation; we may yet see it grow again.

REFERENCES

Bouček, Z. 1988. Australasian Chalcidoidea (Hymenoptera): A biosystematic revision of genera of fourteen families, with a reclassification of species. CAB International: Wallingford (UK).

Miller, C. D. 1970. The Nearctic species of Pnigalio and Sympiesis (Hymenoptera: Eulophidae). Memoirs of the Entomological Society of Canada 102 (Suppl. S68): 5–121.

The Velvet Spiders: High Society

Communal web of Stegodyphus, copyright V. B. Whitehead.

In John Wyndham's novel Web (published in 1979, some ten years after Wyndham's own death), a group of settlers attempting to establish a utopian society on a remote Pacific island find themselves besieged by spiders. Contrary to the usual solitary habits of their kind, the spiders of Web have evolved a social structure like that of wasps or ants, and form roving packs that can overwhelm and devour animals many times their size. Fortunately for us, no such rapacious beasts exist in real life. But there are social spiders, even if they do not present a threat to anything much larger than a big insect.

The social habit has evolved in spiders on a number of occasions, but is perhaps best developed in some species of the genus Stegodyphus. This is a genus of the family Eresidae, commonly known as the velvet spiders. Eresids are small spiders, distinguished from most others by their subrectangular carapace with the front edge produced into a hood above the chelicerae (Miller et al. 2012). They have the full spider complement of eight eyes, with the posterior median eyes generally enlarged and directed forwards. Together with their covering of plush fur (hence the name 'velvet' spiders), this gives them an appearance distinctly reminiscent of some sort of carnivorous muppet.

Male Eresus cinnaberinus, copyright Ferenc Samu.

There are nine currently recognised genera of eresids, though only Stegodyphus includes social species. The family is mostly restricted to the Old World, with a single species Stegodyphus manaus known from Amazonian Brazil. A second species, S. annulipes, was originally described as Brazilian, but has since been collected from Israel and appears to have been mislabelled (Miller et al. 2010). Members of the temperate Eurasian genus Eresus are commonly known as 'ladybird spiders' as males often have a striking abdominal colour pattern of black spots on a red background. Most eresids live in silken tubes under objects such as stones or underground, whereas Stegodyphus species construct their webs in vegetation (Miller et al. 2012).

Mature Stegodyphus lineatus feeding hatchlings, copyright jorgemotalmeida.

The communal webs of social Stegodyphus species may extend for several metres. When an animal becomes trapped in the web, as many spiders as are able to reach it swarm over, all biting and salivating as they can. As a result, the members of the colony are able to kill and digest much larger prey than they could otherwise handle alone. Sociality in Stegodyphus appears to have arisen as an extension of the parental care found in other eresids. Females of both Stegodyphus and Eresus will regurgitate food for newly hatched young (Kullmann 1972). In social Stegodyphus, young are cared for communally and females will feed the young of their nest-mates as well as their own. Eventually, the young begin feeding directly on the caring female herself, draining her haemolymph to the point of rapid death. Again, in social Stegodyphus, this fate awaits all mature adults in the colony, and there is no overlap between generations (Schneider 2002). After the death of their mother, juvenile Eresus and non-social Stegodyphus remain in a group until they are closer to maturity; social behaviour could have arisen through a simple delay in the time of dispersal.

REFERENCES

Kullmann, E. J. 1972. Evolution of social behavior in spiders (Araneae; Eresidae and Theridiidae). American Zoologist 12: 419–426.

Miller, J. A., A. Carmichael, M. J. Ramírez, J. C. Spagna, C. R. Haddad, M. Řezáč, J. Johannesen, J. Král, X.-P. Wang & C. E. Griswold. 2010. Phylogeny of entelegyne spiders: Affinities of the family Penestomidae (NEW RANK), generic phylogeny of Eresidae, and asymmetric rates of change in spinning organ evolution (Araneae, Araneoidea, Entelegynae). Molecular Phylogenetics and Evolution 55: 786–804.

Miller, J. A., C. E. Griswold, N. Scharff, M. Řezáč, T. Szűts & M. Marhabaie. 2012. The velvet spiders: an atlas of the Eresidae (Arachnida, Araneae). ZooKeys 195: 1–144.

Schneider, J. M. 2002. Reproductive state and care giving in Stegodyphus (Araneae: Eresidae) and the implications for the evolution of sociality. Animal Behaviour 63: 649–658.

The Problem with Sacesphorus

Probably not the subject of today's post: an unidentified assamiid from Thailand, from here.

One of the most frustrating things about many older taxonomic resources can be the shortage of illustrations. Up until the early part of the twentieth century, at least, it was something of a rarity for a publication to include extensive figures of their subject(s). So when I was presented for my semi-random subject of the week with the Burmese assamiid Sacesphorus maculatus, described by T. Thorell in 1889, I was not entirely surprised to discover that this Asian harvestman has never actually been illustrated.

At present, Sacesphorus maculatus is the only recognised species in its genus, known only from the Bago region in southern Burma. Unfortunately, that in itself doesn't necessarily indicate much. The Assamiidae are perhaps the most diverse group of Laniatores (short-legged harvestmen) in the tropics of the Old World, but they are also some of the least studied. The last extensive revision of the family was by our old friend Carl-Friedrich Roewer in 1935, and like many of Roewer's classifications its accuracy is suspect. Roewer divided the assamiids between seventeen subfamilies, but the characters separating most of these subfamilies are fairly superficial and probably do not reflect actual relationships (Staręga implicitly synonymised some of the African subfamilies in 1992 when he synonymised genera from different 'subfamilies' together). Roewer placed Sacesphorus in the Erecinae, which he characterised by features such as the absence of a pseudonychium (a claw-like process between the two true claws at the end of each leg), smooth leg claws, a two-segmented telotarsus on the front legs, and the absence of a median spine along the front edge of the carapace. All of these are fairly generalised characters, and some (such as tarsal segment number) are probably more variable than Roewer realised. Many short-legged harvestmen possess a pseudonychium as nymphs but lose it as they grow into adulthood, and the distribution of this feature in the assamiids may require more investigation.

Similar issues attend the identification of assamiid genera. Thorell (1889) originally distinguished Sacesphorus from the genus Pygoplus, also found in Burma and eastern India, by the presence in the former of a small spine in the middle of the eyemound. Roewer recognised a number of 'erecine' genera in Burma and eastern India, largely on the basis of tarsal segment numbers and armature of the dorsum. The relationship between all these genera deserves a second look. Many other groups of harvestmen have been successfully raised from the Roewerian quagmire in recent years; the assamiids are still waiting.

REFERENCES

Roewer, C.-F. 1935. Alte und neue Assamiidae. Weitere Weberknechte VIII. (8. Ergänzung der “Weberknechte der Erde” 1923). Veröffentlichungen aus dem Deutschen Kolonial- und Uebersee-Museum in Bremen 1: 1–168.

Staręga, W. 1992. An annotated check-list of Afrotropical harvestmen, excluding the Phalangiidae (Opiliones). Annals of the Natal Museum 33 (2): 271–336.

Thorell, T. 1889. Viaggio di Leonardo Fea in Birmania e regioni vicine. XXI.—Aracnidi Artrogastri Birmani raccolti da L. Fea nel 1885–1887. Annali del Museo Civico di Storia Naturale di Genova, Serie 2a 7: 521–729.

Let's You and Me Enter Syzygy

Finally, you and your beloved are together. For the two of you, there are no others; all the world is yours alone. You gaze into each other's eyes, and then you pull your beloved into an embrace. Your lips touch in a passionate kiss. Your arms and legs intertwine in a firm hold. As you press so close to one another, it almost feels like you can no longer tell where the dividing line is between you. The excitement builds, and then... the two of you explode, each dissolving into a cascading avalanche of twitching gobbets of flesh.

Life cycle of Lecudina, from Clopton (2002).

This, roughly, is syzygy, a key event in the life cycle of many of the invertebrate-gut-parasitising protists known as eugregarines. Originally, the term 'syzygy' referred to the conjunction of two heavenly bodies, and provides a very poetic label for the process by which two of these unicellular organisms conjoin, rotating around one another as they produce and outer membrane to contain themselves within a single gametocyst. Once within the gametocyst, each divides into numerous gametes (which are produced through straight mitotic division, as eugregarines are haploid at maturity rather than diploid like ourselves). The resulting gametes will then be released from the gametocyst to fuse with one another in the production of diploid zygotes. Each zygote encloses itself in a resistant oocyst, in which state it may be passed out of the host's digestive system and be swallowed by a new host. While within the oocyst, the zygote divides to produce a number of new haploid individuals. Once the oocyst is in a suitable host, the new eugregarines are released, ready to feed and hopefully to eventually find a syzygy of their own.

Mature individuals of Blabericola in association, copyright R. E. Clopton.

Eugregarines have been referred to at this site before. As described in that post, they are part of the group of protists known as gregarines. Eugregarines differ from the other two major subgroups of gregarines, the archigregarines and neogregarines, in that they do not include an extensive asexually reproducing phase in their life cycle in addition to the sexual phase. All known eugregarines are parasites of invertebrates: their hosts include arthropods, molluscs, annelids and tunicates. Most eugregarines parasitise only a single host species over the course of their life cycle. The only known exception is members of the family Porosporidae, which are believed to spend part of their life cycle in a crustacean, and part in a mollusc. However, the porosporid life cycle has only been observed in its entirety once in 1940, when H. F. Prytherch fed infective spores from an oyster to crabs. It has been suggested that Prytherch may have conflated two separate parasites, with the eugregarine infection observed in the crabs after feeding them the spores actually representing a pre-existing infection that they had been carrying before the start of the experiment (Clopton 2002).

Individual of Schneideria quadrinotatus, from Clopton (2002); scale bar = 100 µm. Offhand, I can't be the only one who can't help seeing the nuclei in these sort of drawings as eyes. And for some reason, they always seem to look a bit wistful.

The eugregarines are usually divided between three suborders. Two of these, the Septatorina and Aseptatorina, include the great majority of species and are distinguished (as their names suggest) by the presence or absence of septae dividing the cell into sections. The third suborder includes the single small genus Siedlickia, parasites of marine annelids, which differs from other eugregarines in that it does not go through syzygy; instead, reproductive cells are budded directly off the mature feeding cells. The relationships between the three suborders are largely unknown; the Aseptatorina in particular seems to be defined largely by plesiomorphies. Clopton (2009) argued for a marine ancestry of eugregarines as a whole, and that the radiation of the septate eugregarines had been driven by adaptations of the gametocyst allowing their transmission in freshwater and terrestrial habitats. However, both the aseptate and septate eugregarines include parasites of marine, freshwater and terrestrial hosts. The fact that Clopton did not refer in 2009 to the marine members of the Septatorina (in the Porosporidae and various families of the Gregarinoidea) is somewhat bemusing as he himself had reviewed them some years earlier in his 2002 chapter on the eugregarines for The Illustrated Guide to the Protozoa. It is possible that he simply assumed the marine species to sit outside the terrestrial-freshwater clade, but it would have been nice for hime to say so.

Multiple syzygy in Hyalospora roscoviana, from Clopton (2002). The one in front doesn't look like it was quite expecting this.

Ignorance of the marine eugregarines does seem to be a theme, though: they're definitely less well-studied than the parasites of terrestrial species. Not that the latter can claim to have been exhaustively studied either: as noted by Clopton (2002), while over 1600 species of eugregarine have been described, only a fraction (much less than one percent) of potential hosts have been investigated for their presence. As almost every investigation of a new host results in the description of new parasite species, it is possible that the total number of eugregarine species out there ranks in the millions. Eugregarines are morphologically and behaviourally diverse. Attachment to the cells of the host's intestinal lining is via a structure called the epimerite, which may be a simple nubbin or may be a complex branching, fingered, collared or dart-like structure. When not attached to the host cell, most eugregarines move by gliding, but the worm-like Selenidiidae move by nondirectional swinging or thrashing. Many taxa are all distinguished by the characteristics of their syzygy. They may connect end to end, or they may lie top-to-tail. Members of the septate superfamily Gregarinoidea form associations some time before entering actual syzygy, so they are often found connected (whereas other taxa that do not become conjoined until the point of syzygy are more often found as isolated cells). Syzygy is most often between two individuals, but some Gregarinoidea regularly form associations of three or more. At least one species, Hirmocystis polymorpha, has been found in head-to-tail chains of up to twelve individuals. Whether such polygamous associations lead to all the individuals involved combining to form one gametocyst, or whether some form of competition occurs to whittle them down to a single victorious pair, is something I haven't yet discovered.

REFERENCES

Clopton, R. E. 2002. Order Eugregarinorida Léger, 1900. In: Lee, J. J., G. Leedale, D. Patterson & P. C. Bradbury (eds) Illustrated Guide to the Protozoa, 2nd ed., vol. 1 pp. 205–288. Society of Protozoologists: Lawrence (Kansas).

Clopton, R. E. 2009. Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comp. Parasitol. 76 (2): 167–190.