A Parasitic Eel?

The following post was inspired by an e-mail that I was sent recently by Sebastian Marquez. He told me about a friend of his catching a trevally when fishing, then cutting it open to find a snake eel inside the body cavity (but outside the stomach), wrapped around the trevally's internal organs. According to Sebastian, the lead suspicion for what had happened was that the eel had somehow burst out of the trevally's stomach before it was caught, and he wanted to know if I'd ever heard of anything similar. I didn't have an explanation for him, but his story did get me thinking about the snub-nosed eel.

Snub-nosed eel Simenchelys parasitica, from Jordan (1907).

The snub-nose eel Simenchelys parasitica is a small deep-sea eel, about 20 to 35 centimetres long. It has attracted note by being found a number of times burrowed into the body cavity of larger fishes with perhaps the most renowned case being two juveniles that were found nested inside the heart of a mako shark. This lead to the description of S. parasitica as an endoparasite (hence the species name). However, acceptance of this tag has been far from universal. The snub-nosed eel has been caught free-living more regularly than it has been found in other fish and because of its deep-sea habitat it has never been observed in life. An alternative suggestion has been that Simenchelys is normally a scavenger; because many of its recorded 'hosts' have been collected through non-targeted methods such as trawls, it is not impossible that the snub-nosed eels may have burrowed into their body cavity after they were already deceased.

It was with this conundrum in mind that the cranial anatomy of the snub-nosed eel was described by Eagderi et al. (2016). The jaws of Simenchelys are relatively short and muscular (hence its 'snub nose'). It also has teeth arranged in such a way that they form an even cutting edge (in contrast to the more spaced and uneven teeth of other eels). Eadgeri et al. came to the conclusion that the snub-nosed eel probably feeds by biting out plugs of flesh, in a similar manner to a cookie-cutter shark. Simenchelys also resembles a cookie-cutter in having large, fleshy lips that are probably used to form a seal between jaws and food source. A large hyoid ('tongue') apparatus probably works to provide suction to maintain the seal. The snub-nosed eel may also rotate while biting, a behaviour known from both cookie-cutters and other eels.

So is Simenchelys a parasite? It is probably not a habitual endoparasite, lacking as it does any clear adaptations to the endoparasitic lifestyle. There are fish that could be described as ectoparasites, in that they habitually feed on live animals larger than themselves in a manner that does not normally lead to the host's death. The cookie-cutter is one such fish; another is the candiru Vandellia cirrhosa, a small freshwater catfish from the Amazon basin that feeds on blood from the gills of other fish. It is possible that the snub-nosed eel could have a similar lifestyle to one of these. However, recorded evidence of its habits is even more consistent with scavengers such as hagfish and the candiru-açu Cetopsis candiru (another South American catfish) that tear flesh from the submerged bodies of dead animals, and may often burrow their way into the corpse's body cavity as they do so.

Of course, the two modes of feeding are not mutually exclusive. The only difference between predator and parasite in this scenario is whether the attacked animal is alive or dead, and the thing about flesh-feeders is that they're not always picky. A habitual scavenger may easily choose the opportunity to take a nibble from a still-living host, especially is said host is in some way incapacited (as a result of being swept up by a trawl, for instance). The snub-nosed eel may not be a habitual parasite, but it may be an opportunistic one.

REFERENCE

Eagderi, S., J. Christiaens, M. Boone, P. Jacobs & D. Adriaens. 2016. Functional morphology of the feeding apparatus in Simenchelys parasitica (Simenchelyinae: Synaphobranchidae), an alleged parasitic eel. Copeia 104 (2): 421–439.

Life Among a Shrimp's Gills

Female of Schizobopyrina bombyliaster from Williams & Boyko (2004), with red box added on ventral view to indicate position of small male.

For today's random subject, I drew the marine isopod genus Schizobopyrina. Schizobopyrina is a genus in the family Bopyridae, and females of this genus were distinguished by Markham (1985) from those of the related genus Bopyrina by the presence of palp on the maxilliped (part of the mouthparts), by its more elongate oostegites (the lamellae forming the brood pouch in which eggs and larvae are incubated), and by the fusion of the pleomeres (posterior segments) on one side of the body. About ten or so species have been assigned to this genus from warmer waters around the world.

Mature bopyrids are parasites of shrimps and other crustaceans (Schizobopyrina has been found on hosts of the families Palaemonidae, Gnathophyllidae and Hippolytidae). Schizobopyrina and related genera are found in the branchial (gill) cavities of their host. Shrimp gills are developed from side-branches of the base of the legs, and are covered by an overhanging shelf of the carapace (if anyone is familiar with the process of preparing a crayfish or lobster, the gills are the 'dead man's fingers' that you have to remove before serving the crayfish). In a shrimp that is host to Schizobopyrina, the branchial cavity will become greatly protruding, as can be seen in this photo of a bumblebee shrimp Gnathophyllum americanum parasitised by Schizobopyrina bombyliaster (from Williams & Boyko 2004; scale bar equals 1.0 mm):

Bopyrids are released from the parent host as larvae that initially attach themselves to copepods. When they are approaching maturity, they leave the copepod and find an appropriate adult host. The first larva to attach itself to an appropriate shrimp will develop into a female, while any subsequent larva to attach itself will develop into a male (Cash & Bauer 1993). As can be seen in the figure at the top of this post, the female is considerably larger than the male. She is also noticeably asymmetrical in her body form, though a single species may include individuals bent to either the left or the right (Markham 1985). The female bopyrid attaches herself to her host before it reaches maturity: this puts her at risk of losing her place as the host moults, but studies of another branchial parasite bopyrid, Probopyrus pandalicola, indicate that as the host cuticle tears away during the process of moulting, the female is able to reattach herself to the new cuticle underneath and keep her place (Cash & Bauer 1993). The smaller male looks very different to the female, and is much more symmetrical. He attaches himself to the female, but whether or how he feeds is unknown. In Probopyrus pandalicola, the female moults, then produces eggs, after each moult of her host; the male has been observed crawling at this point into the brood pouch of the female, where he presumably fertilises her eggs.

Just as a further aside, the recent description of the species featured in the figures used in this post, Schizobopyrina bombyliaster Williams & Boyko 2004, was of further interest because the type specimen of this parasitic isopod was itself host to a hyperparasitic isopod, the cabiropid Cabirops bombyliophila. Which gives me an idea for a matryoshka design...

REFERENCES

Cash, C. E., & R. T. Bauer. 1993. Adaptations of the branchial parasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology 13 (1): 111-124.

Markham, J. C. 1985. A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises 7 (3): 1-156.

Williams, J. D., & C. B. Boyko. 2004. A new species of Schizobopyrina Markham, 1985 (Crustacea: Isopoda: Bopyridae: Bopyrinae) parasitic on a Gnathophyllum shrimp from Polynesia, with description of an associated hyperparasitic isopoda (Crustacea: Isopoda: Cabiropidae). Proceedings of the California Academy of Sciences 55 (24): 439-450.

Ormyrids: Attacking the Gall

Female of Ormyrus nitidulus, photographed by Penny Metal.

Everyone knows about God's supposed inordinate fondness for beetles, but it is my opinion that the true poster children for insect diversity should be the wasps. Wasps, admittedly, do not have as many described species as beetles (there are some who suspect that the actual number of species of wasp may eventually be higher, but that remains in the realm of the hypothetical). However, many species of beetle are very difficult to distinguish except by skilled specialists, being otherwise small, brown, and conservative. Wasps, on the other hand, come in a kaleidoscopic array of colours and shapes, such that even a novice may look at an array of wasps (see the top of this post, for instance) and be immediately struck by the disparity.

An unnamed species of Ormyrus, photographed by Simon van Noort.

The Chalcidoidea, commonly referred to as chalcids, are one of the largest subgroups of wasps, a clade of mostly small (often minute), mostly parasitoid wasps (some have larvae that feed on plants). Members of the Ormyridae, one of the commonly recognised families of chalcids, are generally about two to three millimetres long. Ormyrids are distinguished from other chalcids by their robust body form, with a strongly sclerotised gaster* (ormyrids and perilampids tend to look like steroid-abusing pteromalids). The segments of the gaster are usually ornamented by rows of coarse foveae (pits) that give it a distinctive rough appearance, though in some species these foveae are less obvious or are replaced by longitudinal ribs (Bouček 1988). Ormyrids are often recorded in association with plant galls, but are not gall-formers themselves: rather, they are parasites of the insect larvae that formed the galls (usually flies or other wasps). Some ormyrids are associated with figs and parasites of fig wasps.

*Wasp researchers generally refer to the sections of the body behind the head by terms such as 'mesosoma' and 'gaster' (or metasoma), rather than 'thorax' and 'abdomen'. This is because the section of the body that is the first segment of the abdomen in other insects has become the last segment of the mesosoma in Hymenoptera.

A female of Ormyrus on a knopper gall (a type of gall that develops when a developing acorn of the pedunculate oak Quercus robur is parasitised by the cynipid wasp Andricus quercuscalicis), photographed by Tristram Brelstaff.

There are about 125 known species of ormyrid (making this a quite small family by chalcid standards) according to the Universal Chalcidoidea Database (an absolutely wonderful resource). However, there isn't yet a really good classification system within the family. Ormyrids vary to a fair degree, particularly in the form of the antennae or the ornamentation of the gaster, but most authors have placed almost all species within the single genus Ormyrus. Attempts to subdivide this diverse group (for instance, that of Doğanlar, 1991, who recognised four genera of ormyrids with three subgenera within Cyrtosoma) have suffered from not considering the full range of ormyrid diversity. Some of the Australian forms referred to by Bouček (1988), for instance, may not be placeable in Doğanlar's system. Until an appropriately large-scale review is conducted, most authors will probably continue to recognise an all-purpose Ormyrus.

REFERENCES

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

Doğanlar, M. 1991. Systematic positions of some taxa in Ormyridae and descriptions of a new species of Ormyrus from Turkey and a new genus in the family (Hymenoptera, Chalcidoidea). Türkiye Entomoloji Dergisi 15 (1): 1-13.

Gordians

Long-term followers of this site may recall this video, linked to over four years ago:

The animal emerging from the unfortunate cricket in the video is a Gordian or horsehair worm, Nematomorpha. Gordian worms spend most of their lives as internal parasites: either of insects (in the freshwater/terrestrial order Gordiida) or of shrimps and crabs (in the marine genus Nectonema). Of the two commonly used vernacular names for this group, 'Gordian worm' refers to the famed Gordian knot, and is derived from the appearance of mating tangles of these elongate animals. 'Horsehair worm' refers to the long-held belief (again, inspired by appearance) that the adult worms developed from horse hairs decaying in water. So persistent was this belief that Leidy felt compelled to report in 1870 on an attempt to generate horsehair worms by this method, explaining that, "I need hardly say that I looked at my horse-hairs for many months without having had the opportunity of seeing their vivification". He also scuttled the fear, which even Linnaeus had reported as fact, that a horsehair worm could inflict a nasty bite on anyone careless enough to handle one. In fact, Gordian worms (being internal parasites absorbing nutrients directly from the host when young and not feeding as adults) do not even possess a mouth. Instead, the males of many species possess a bifurcated tail end, used in copulation, that may have been mistaken for jaws. The complete absence of active feeding has the interesting side effect that adult Gordians may completely lack an internal bacterial flora (Hudson & Floate 2009).

Representative nematomorphs: Gordius (Gordiida) on the left and Nectonema on the right, from Biodidac.

The primary division within the Nematomorpha between the marine Nectonema and the terrestrial Gordiida is universally agreed upon. The two branches are ecologically, morphologically and molecularly divergent (Bleidorn et al. 2002). Adults of Nectonema have dorsal and ventral double rows of swimming bristles, while those of Gordiida lack bristles (except for, in some species, minute patches of bristles in front of the cloacal opening). Mature adults of Gordiida emerge from their insect host when the latter approaches or enters water. It has been suggested that the worm is able to cause its host to actively seek out water, but it seems more likely that the worm simply causes erratic but non-directional behaviour that may make the host more likely to come into contact with water than if it had remained in its preferred microhabitat (Thomas et al. 2002). Once the host does come close to water as a result of random movement, the worm may be able to induce a last suicidal jump; alternatively, it may simply be that the addled host does not recognise the water as dangerous and makes no attempt to avoid it.

Female Chordodes wrapped around a stick, laying a white egg string. Photo from the Hairworm Biodiversity Survey.

Once in the water, the adult Gordians will mate with any others present; when multiple adults emerge in close proximity, they may begin mating before they have even finished emerging from their host (Hanelt & Janovy 2004). The females lay their eggs in long strings: one female may lay nearly six million eggs, making them one of the potentially most fecund animals on the planet. The larvae that hatch from the eggs look nothing like their parents, being kind of sausage-shaped with an eversible, spiny proboscis. A larva will find itself an aquatic animal host such as an insect larva or mollusc to burrow into and form a cyst. If the aquatic secondary host is then eaten by a suitable terrestrial primary host (for instance, after an aquatic insect larva matures into a terrestrial adult), the cyst will hatch out and the Gordian will complete its development within the terrestrial host. The Gordian larva may also bypass the secondary host if a primary host drinks water containing Gordian larvae. The larva or mode of transmission of Nectonema remains unknown,but, as Nectonema adults live in the same habitat as their primary host, they probably do not require a secondary host.

Larva of Chordodes encased in a cyst, from the Hairworm Biodiversity Survey.

Phylogenetically, Gordians have usually been regarded as related to nematodes, with which they share a number of morphological features. However, a molecular analysis by Sørensen et al. (2008) suggested a relationship between Gordians and loriciferans (albeit with support that was not overwhelming). The Gordian larva (which has no equivalent in the direct-developing nematode life-cycle) does bear a vague resemblance to an adult loriciferan, though it is debatable whether the resemblance is more than superficial. Loriciferans have not appeared in many phylogenetic analyses to date, and further investigation is required to establish whether it is the adults or the larvae of the Gordians that hold the clues to their affinities.

REFERENCES

Bleidorn, C., A. Schmidt-Rhaesa & J. R. Garey. 2002. Systematic relationships of Nematomorpha based on molecular and morphological data. Invertebrate Biology 121 (4): 357-364.

Hanelt, B., & J. Janovy Jr. 2004. Untying a Gordian knot: the domestication and laboratory maintenance of a Gordian worm, Paragordius varius (Nematomorpha: Gordiida). Journal of Natural History 38: 939-950.

Hudson, A. J., & K. D. Floate. 2009. Further evidence for the absence of bacteria in horsehair worms (Nematomorpha: Gordiidae). Journal of Parasitology 95 (6): 1545-1547.

Leidy, J. 1870. The gordius, or hair-worm. The American Entomologist and Botanist 2 (7): 193-197.

Sørensen, M. V., M. B. Hebsgaard, I. Heiner, H. Glenner, E. Willerslev & R. M. Kristensen. 2008. New data from an enigmatic phylum: evidence from molecular sequence data supports a sister-group relationship between Loricifera and Nematomorpha. Journal of Zoological Systematics and Evolutionary Research 46 (3): 231-239.

Thomas, F., A. Schmidt-Rhaesa, G. Martin, C. Manu, P. Durand & F. Renaud. 2002. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology 15 (3): 356-361.

Just When You Thought It Was Safe

Smalltooth cookiecutter shark Isistius brasiliensis, photographed by Joshua Lambus.

Sometimes, you can get pretty much everything you need to know from the title of an article alone. To whit:

First documented attack on a live human by a cookiecutter shark (Squaliformes, Dalatiidae: Isistius sp.)

The article itself is in a journal I don't have access to, but I can read the abstract: the person attacked was a long-distance swimmer in Hawaii and was bitten twice. The bite was treated with skin grafts, but still took nine months to finish healing.

Cookiecutter sharks are one of the more fascinatingly evil fish out there. They are small, as sharks go (up to about 50 cm, tops) but have proportionately oversized teeth that are arranged in a tight, single-row array that can be protruded outwards to take a neat plug out of the flesh of a larger animal: hence the name of 'cookiecutter'. The effectiveness of the cutting tooth row is maintained by being replaced all at once, rather than individual teeth being replaced piecemeal as in other sharks. Cookiecutters are rarely encountered by humans as they are generally deep sea fish, living below the light zone, but like many mesopelagic animals they appear to migrate closer to the surface at night (Papastamatiou et al. 2010). Bioluminescent photophores behind the head have been suggested to function as a lure, drawing larger fish, dolphins, etc. into range of an ambush. Cookiecutters have very catholic tastes, and evidence of bites has been recorded from just about any decent-sized pelagic animal. They will even bite the external insulation on submarines.

Fish with cookiecutter bites, from Rick Macpherson (who, it turns out, covered this event when it was first happened).

Given their lack of pickiness, it is hardly surprising that a cookiecutter would take a bite out of a human. Of course, humans very rarely venture into the pelagic environment in which cookiecutters can be found. The very fact that the Hawaii indicent is the first confirmed attack indicates how extremely rare this would be expected to be. The Wikipedia page on cookiecutters refers to possible attacks on shipwreck survivors (though the source page linked to does not provide citations for such reports), and the body of a drowned fisherman was recovered in Hawaii with cookiecutter bites. But unless you happen to be swimming in the open ocean at night, your chances of being bitten by a cookiecutter are low.

REFERENCE

Papastamatiou, Y. P., B. M. Wetherbee, J. O’Sullivan, G. D. Goodmanlowe & C. G. Lowe. 2010. Foraging ecology of cookiecutter sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds. Environmental Biology of Fishes 88 (4): 361-368.

Life in the Fast Lane (Taxon of the Week: Astigmata)

Amongst the bewildering diversity of mites inhabiting this world, the Astigmata include some of the most significance to humans. This group of 5000+ species (with doubtless many more waiting to be described) has become specialised for rapid development and high fecundity. Originally scavengers on decomposing organic matter, members of some lineages have become parasites on vertebrates.


Dust mites Dermatophagoides pteronyssinus on a bedsheet. Dust mites are common inhabitants of human houses where they feed on particles of organic matter such as flaked skin. For the majority of people, their presence in the house is of no consequence; an unfortunate minority suffer allergies to dust mite waste products. Photo from Time.

Curiously, the soft-bodied, fast-living astigmates are most closely related among other mites to the heavily-armoured, long-lived Oribatida. In fact, both morphological and molecular phylogenetic studies have indicated that astigmates are derived from within oribatids (though recovering this result in molecular analyses is dependent on the analytical method used due to the much faster evolutionary rate of astigmates; Dabert et al., 2010*). Astigmates have been derived from oribatids by a process of neoteny where the characters of nymphal oribatids have been carried over to the adult astigmate (OConnor, 2009). Astigmates have also developed a highly modified deutonymph (the second nymphal stage of development) that is specialised for dispersal through phoresy (hitching a lift on some flying insect). The astigmate deutonymph (referred to by many authors as a hypopus) is generally non-feeding and the well-developed mouthparts present in the earlier protonymph become rudimentary, only to reappear when the mite moults through to the next stage, the tritonymph. In many species, if conditions are favourable and dispersal unnecessary, a protonymph may moult directly into a tritonymph, bypassing the deutonymph stage. Other species will only develop into deutonymphs if a suitable host for dispersal is available. The Psoroptidia, the main vertebrate-associated lineage of astigmates, have dropped the deutonymph from their life cycle entirely.

*And a thank-you to Macromite for notifying me of this paper).


Deutonymphs of Chaetodactylus micheneri on a specimen of the bee Osmia californica. Though it may not look pretty, most phoretic organisms do not actually parasitise their hosts, only using them for transport. Photo from here.

While some phoretic astigmates will attach themselves to any old host, others may be very specialised. The members of the subfamily Ensliniellinae (family Winterschmidtiidae) associate solely with nest-building wasps and bees. The early stages of the enslinielline life cycle occur in the host's brood cell and the mites reaches their phoretic stage when the host larva has matured and is ready to leave the brood cell as an adult wasp (or bee). At that point, the mites cluster in specialised pockets on the host's body called acarinaria. In the wasp Ancistrocerus antilope, only the male wasps emerge from the cell carrying mites in acarinaria behind the wings (the females kill any mites in their brood cell while larvae); when the male mates with a female, its mite passengers abandon him to enter acarinaria around the female's genitalia (Houck & OConnor 2001). In other wasp species, the females carry mites in acarinaria from when they emerge. When the female lays its eggs, the mites leave the acarinaria to be sealed in the new brood cells where they will mate and lay their own eggs.


The scabies mite Sarcoptes scabiei. The Sarcoptidae are a family of parasitic mites that burrow into the skin of mammals. Most species are specialists on a small range of hosts, most commonly bats (for some reason, bats carry an extraordinary diversity of parasites), but S. scabiei is a generalist species that has been found on a wide range of hosts, from humans to wombats. Photo by Louis De Vos.

You might be wondering what the wasp gets out of this arrangement as it is hard to see why it would have developed specialised structures to transport the mites if it was not benefiting somehow. And yet, at best, the mites seem to have no significant effect on their hosts; at worst, they are actively harmful, feeding on the food stores left for the developing larva or on the larva itself (though no parasitic ensliniellines have been known to cause the death of their host). Klimov et al. (2007) have suggested that acarinaria have developed not to facilitate the mites' development but to contain them. The mites cannot break through the walls of the brood cells themselves; they can only be carried by an emerging host. If the mites cluster into acarinaria before the host emerges, they remain with already-infected individuals rather than spreading to their potentially mite-free siblings. Perhaps adaptation is not always a matter of achieving an optimum; perhaps it is sometimes simply a form of damage control.

REFERENCES

Dabert, M., W. Witalinski, A. Kazmierski, Z. Olszanowski & J. Dabert. 2010. Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Molecular Phylogenetics and Evolution 56 (1): 222-241.

Houck, M. A., & B. M. OConnor. 1991. Ecological and evolutionary significance of phoresy in the Astigmata. Annual Review of Entomology 36: 611-636.

Klimov, P. B., S. B. Vinson & B. M. OConnor. 2007. Acarinaria in associations of apid bees (Hymenoptera) and chaetodactylid mites (Acari). Invertebrate Systematics 21 (2): 109-136.

OConnor, B. M. 2009. Cohort Astigmata. In: Krantz, G. W., & D. E. Walter (eds). A Manual of Acarology, 3rd ed., pp. 565-657. Texas Tech University Press.

The Hard Way to be a Bloodsucker (Taxon of the Week: Ixodidae)

A mature gorged female of Ixodes ricinus, the sheep tick or castor bean tick, ready to lay her eggs. Photo by Jarmo Holopainen.

Ticks are probably the most familiar of all mite groups. Not only do they include by far the largest mite species but they also feed on the blood of vertebrates, a habit guaranteed to bring them to our attention. The ticks themselves would usually be more irritating than dangerous, except on occasions when they attack in large numbers, but many ticks are vectors of some very unpleasant diseases. Ticks are classified into three families of which the largest is the Ixodidae or hard ticks with a little under 700 species (Horak et al., 2002). Hard ticks are distinguished from members of the Argasidae or soft ticks by the presence of a hardened scutum at the front of the dorsum (the third tick family contains a single species, the African Nuttalliella namaqua). In males the scutum can cover almost the entire dorsal surface while the female scutum is restricted to the front part of the body over the legs. Hard ticks also have the capitulum (the 'head') directed forward so that it is easily visible from above while soft ticks have the capitulum pointed downwards (Nicholson et al., 2009).


A female of the cattle tick Rhipicephalus microplus laying her not inconsiderable brood of eggs. Photo from here.


Cattle ticks removed from a single calf. Photo from here.

The hard tick life cycle contains four stages of a single instar each - egg, larva, nymph and mature adult (soft ticks have multiple nymphal instars). Eggs are laid in large clusters of hundreds or thousands - the record number of eggs laid by a single female is 34,000 for a specimen of Amblyomma variegatum (Nicholson et al., 2009). Like other mites, larval ticks have only six legs when they first hatch out; the fourth pair doesn't appear until the nymphal stage. In both the larval and nymphal stages the young ticks will find a suitable host and feed then usually drop off and moult away from the host* (a small number of species don't leave the host before moulting and remain on a single host for their entire life). Some tick species are very choosy about their hosts (the best-known of which being the cattle tick, Rhipicephalus microplus [aka Boophilus microplus]) while others such as the sheep tick Ixodes ricinus are far more catholic. Some species feed on different hosts at different life stages. Even if suitable hosts are few and far between, some ticks can survive for over a year without feeding while they wait for one to turn up (some soft ticks can survive for several years without food). Males of Ixodes do not feed after reaching maturity and usually mate with females before they attach themselves to the final host (though some may mate on the host) while mature males of other ixodid genera do feed and copulation between the sexes takes place on the host (all together now - ewww). After copulation, the attached female gorges herself on her host's blood, swelling up to many times her original size. Once her eggs are mature, she drops off the host, lays her eggs in a suitable sheltered site, and dies (in contrast, female soft ticks can find another host and mate with another male, eventually surviving for several years).

*I have to admit to being surprised when I learnt that ticks didn't just latch onto their final host right away, even though in retrospect it should have been bloody obvious. After all, they would hardly be as much concern as disease vectors if they only ever attacked a single individual.


Back when she was skinny - a female lone star tick Amblyomma americanum sitting on vegetation waiting for a host. Photo by James Gathany.

Phylogenetic analysis supports a basal division in Ixodidae between Ixodes and other genera which is consistent with the differences in life cycles between the two groups (Murrell et al., 2003).

REFERENCES

Horak, I. G., J.-L. Camicas & J. E. Keirans. 2002. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. Experimental and Applied Acarology 28: 27-54.

Murrell, A., N. J. H. Campbell & S. C. Barker. 2003. The value of idiosyncratic markers and changes to conserved tRNA sequences from the mitochondrial genome of hard ticks (Acari: Ixodida: Ixodidae) for phylogenetic inference. Systematic Biology 52 (3): 296-310.

Nicholson, W. L., D. E. Sonenshine, R. S. Lane & G. Uilenberg. 2009. Ticks (Ixodida). In Medical and Veterinary Entomology, 2nd ed. (G. R. Mullen & L. A. Durden, eds) pp. 483-532. Academic Press.

Name That Bug: Stoecharthrum giardi

From Kozloff (1992).

Meet my favourite orthonectid (because we've all got one, right?) Orthonectida are twenty-odd species of uncommon parasites of marine invertebrates. The host of Stoecharthrum giardi is the annelid worm Scoloplos armiger; most orthonectid species are only recorded from one host, but closely related species can be found in hosts of quite different phyla (other Stoecharthrum species, for instance, are found in bivalves and ascidians). As you can see from the scale bar in the drawing of a sexually mature individual above, they are extremely small- Stoecharthrum giardi, for instance, grows up to 0.8 mm in length and less than 0.02 mm in width. To match this small size, mature orthonectids have a very simple anatomical organisation; an outer layer only one cell deep contains an inner mass of developing gametes, with only a very thin layer of a small number of muscle cells between the two (Slyusarev, 2003b). Sexually reproducing individuals leave their host upon maturity to release their gametes in open water. The resulting larvae re-enter a host and produce multinucleate plasmodia within which new individuals develop from germinative cells. However, there appears to still be some disagreement whether the plasmodium represents the parasite itself (Sliusarev, 2003a) or a pathological product of dissolved host cells (Kozloff, 1997). The relationships of orthonectids with other animals are pretty much unknown - they are often classified in the Mesozoa along with the Rhombozoa, another group of marine invertebrate parasites that also have a simple two-cell-layer organisation, but the detailed nature of the cell layers is decidedly different between the two groups and their simple organisations are just as likely (if not more likely) to be the results of convergence as relationship. Similarly, authors have disagreed whether the simple organisation of 'mesozoans' indicates that they are relatively basal within animals or whether it represents a secondary simplification as a result of their parasitic lifestyle. A molecular phylogenetic analysis by Hanelt et al. (1996) placed orthonectids as sister to all other Bilateria while rhombozoans were placed separately within Bilateria, but their topology shows every sign of long-branch attraction when considered in light of subsequent advances in bilaterian phylogeny.

The orthonectid family Rhopaluridae contains four genera, Rhopalura, Intoshia, Ciliocincta and Stoecharthrum*. The genera are primarily distinguished by the arrangement and morphology of the external cells. The first twenty or so rings of cells from the front of the animal (exact number depending on species) more or less alternate between bands of ciliated and non-ciliated cells (the cilia are the animal's main motile organs after it leaves the host). After that, all cell bands are ciliated, but Stoecharthrum and female Ciliocincta are the only rhopalurids really long enough to have a significant extension of the fully ciliated region. With more than sixty cell rings, Stoecharthrum is more than twice as elongate as most other orthonectids; the average number seems to be about thirty rings (oh, and in case you were wondering, the little arrangement of small cells on ring fifteen is the location of the genital pore). Stoecharthrum and female Ciliocincta also differ from other rhopalurids in having the majority of ciliated and non-ciliated cells about the same length; in Rhopalura and Intoshia, the non-ciliated bands are noticeably narrower than the ciliated bands. The primary difference between Stoecharthrum and Ciliocincta, other than Stoecharthrum's greater length, is that Stoecharthrum is the only orthonectid genus in which individuals are hermaphroditic rather than having separate male and female sexes.

*The only non-rhopalurid genus assigned to Orthonectida is Pelmatosphaera, for which I haven't seen a figure. Kozloff (1992) doubted whether Pelmatosphaera was truly related to Rhopaluridae but didn't suggest any alternative placement.

REFERENCES

Hanelt, B., D. van Schyndel, C. M. Adema, L. A. Lewis & E. S. Loker. 1996. The phylogenetic position of Rhopalura ophiocomae (Orthonectida) based n 18S ribosomal DNA sequence analysis. Molecular Biology and Evolution 13: 1187-1191.

Kozloff, E. N. 1992. The genera of the phylum Orthonectida. Cahiers de Biologie Marine 33: 377-406.

Kozloff, E. N. 1997. Studies on the so-called plasmodium of Ciliocincta sabellariae (Phylum Orthonectida), with notes on an associated microsporan parasite. Cahiers de Biologie Marine 38 (3): 151-159.

Sliusarev, G. S. 2003a. [Orthonectida's life cycle]. Parazitologiia 37 (5): 418-427.

Slyusarev, G. S. 2003b. The fine structure of the muscle system in the female of the orthonectid Intoshia variabilis (Orthonectida). Acta Zoologica 84: 107-111.

If They Only Wood (Taxon of the Week: Diaporthales)

Perithecia (fruiting bodies) of Cryphonectria cubensis, the cause of eucalyptus canker. Photo by Edward Barnard.

Most people, when they think of fungi, will think of mushrooms. However, the majority of fungi do not produce such large and obvious structures as mushrooms; the majority of fungi are microscopic decomposers, whose minute fruiting bodies would be easily overlooked by those not looking for them. But tiny as these organisms are, they can have a significant effect on your life.

The Diaporthales are one order of these microfungi. They are a well-defined order of ascomycetes with brown or black perithecia (almost entirely enclosed fruiting bodies with only a single pore at one end and the spores produced inside) submerged either within a stroma (mass of hyphal tissue) or in the surrounding substrate on which they are growing (Rossmann et al., 2007). In many Diaporthales, the opening pore of the perithecia is on a long neck that may or may not also be submerged; it is the combination of round perithecium and elongate neck that lead the authors of one recently-described genus to dub it Lollipopaia (Inderbitzin & Berbee, 2001).


Pycnidia of Cryphonectria parasitica protruding from chestnut bark. Pycnidia resemble perithecia, but differ in containing asexually- rather than sexually-produced spores. Photo from here.

Most Diaporthales are decomposers of rotting wood. As such, they rarely come to humanity's attention, though it probably wouldn't take us long to notice if they disappeared. A small but significant number of Diaporthales, however, have earned a great deal of attention from humans because, while they grow on wood just like their relatives, they don't have the courtesy to wait for the tree to die first. The most famous (or notorious, depending on your preferred choice of adjectives) of Diaporthales is undoubtedly Cryphonectria parasitica, the cause of chestnut blight and famed as the bane of the American chestnut, C. dentata. According to Wikipedia, C. dentata may have made up as much as a quarter of the forest in the Appalachian region of eastern North America prior to the arrival of chestnut blight around 1905; by 1940, it was almost extinct. To this day, the position of the American chestnut across most of its original range remains tenuous; complete extinction has been staved off by the chestnut's ability to produce subsidiary shoots from its base, meaning that a number of trees survive despite being reduced to the central boles. However, complete regrowth is likewise prevented by the fungus attacking any new shoots before they achieve significant growth. Meanwhile, attempts to breed blight-resistant strains of American chestnut are hampered by the tree's slow growth rate.


Three views of American chestnut (Castanea dentata). On the left, American chestnut trees as they could still be found in 1910. In the centre, American chestnut as it survives today - an understorey regenerating shrub, prevented from reaching full growth by the inevitable onset of blight. On the right, the intermediary stage in a grown chestnut felled by the fungus. Images from Ellison et al. (2005).

When chestnut blight was recorded in European chestnut trees (Castanea sativa) in Italy in 1938, people expected a repeat of the American experience. And at first, that was almost exactly what happened - chestnut blight spread rapidly through western Europe, slowed only by the more scattered distribution of its host (C. sativa was not originally native to most parts of Europe, but introduced by the Romans; as a result, it does not form continuous forests in Europe as C. dentata did in America, but is largely only found where it has been deliberately planted by humans). However, during the 1950s and 1960s, reports started coming in of stands of chestnuts that appeared to be coping surprisingly well despite the obvious presence of blight (Heiniger & Rigling, 1994), with the damage from the blight extending only a short way into the wood (as it does in the Asian chestnut Castanea crenata, the original host of the fungus). What was more, when fungal hyphae from these wimpier infections were transplanted into further chestnut trees amongst more normal raging infections, the more virulent infections began to heal. The reduced virulence turns out to be due to a virus infecting the fungus - the disease being cured by a disease of its own. The spread of reduced virulence among chestnut blight in Europe has massively reduced the European epidemic. Attempts to implement the same cure in North America, however, have mostly resulted in failure (Milgroom & Cortesi, 2004). Transmission of reduced virulence between fungal colonies is slow and ineffecient, and in most cases seems to require direct human intervention to be truly effective. While this direct intervention is feasible with the more scattered European chestnut, it offers little hope of restoring the prior forests of American chestnut.

Other species of Diaporthales cause diseases in other crop trees and plants (including butternut canker caused by Sirococcus clavigignenti-juglandacearum, which I'm sure is a terrible thing to be afflicted by, even if it does sound like the name of some sort of confectionary). Dogwood anthracnose is caused by Discula destructiva, recently shown to be an anamorphic (asexual) member of the Diaporthales. Cytospora species attack Eucalyptus, while Greeneria uvicola causes bitter rot in grapes. If you feel enticed to explore the systematics and characteristics of the various subgroups of Diaporthales, there's an impressively detailed coverage on the U.S. Department of Agriculture's Diaporthales page, including a big interactive tree where clicking on a clade brings up descriptions and images to help you while away the hours.

REFERENCES

Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliott, C. R. Ford, D. R. Foster, B. D. Kloeppel, J. D. Knoepp, G. M. Lovett, J. Mohan, D. A. Orwig, N. L. Rodenhouse, W. V. Sobczak, K. A. Stinson, J. K. Stone, C. M. Swan, J. Thompson, B. Von Holle & J. R. Webster. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3 (9): 479-486.

Heiniger, U., & D. Rigling. 1994. Biological control of chestnut blight in Europe. Annual Review of Phytopathology 32: 581-599.

Inderbitzin, P., & M. L. Berbee. 2001. Lollipopaia minuta from Thailand, a new genus and species of the Diaporthales (Ascomycetes, Fungi) based on morphological and molecular data. Canadian Journal of Botany 79: 1099-1106.

Milgroom, M. G., & P. Cortesi. 2004. Biological control of chestnut blight with hypovirulence: a critical analysis. Annual Review of Phytopathology 42: 311-338.

Rossmann, A. Y., D. F. Farr & L. A. Castlebury. 2007. A review of the phylogeny and biology of the Diaporthales. Mycoscience 48: 135-144.

Multifarities Most Horrid (Taxon of the Week: Braconidae)

Braconid wasp of the subfamily Aphidiinae laying an egg in a hapless aphid. Photo from BioMed Central.

We all know that J. B. S. Haldane is supposed to have remarked that God seemed to have an "extraordinary fondness for beetles". What Haldane may not have realised was the possibility that the beetles were just a means to an end. As the current rate of taxonomic description is considered, some researchers have come to the suspicion that the true objects of the Creator's affection are not beetles, but parasitoid wasps*. Which, when you consider the natures of parasitoid wasps, kind of explains some things about life.

*Personally, I'm still taking the long odds and backing the nematodes.


Microgastrinae larvae emerging from a host caterpillar. Photo from here.

The Braconidae are just one of the stupidly diverse lineages of Hymenoptera (another group, the Proctotrupomorpha, was covered at this site here). According to ToLWeb (in 2004), there are some 12,000 described species of braconids, with estimates of up to 50,000 in total. Braconids form the living sister group to the similarly diverse Ichneumonidae, though braconids tend to be smaller in size (still, some of them are more than big enough). Braconids include both exoparasitic and endoparasitic taxa, parasitoids of eggs, larvae or adult insects, and a small number of gall-forming plant-parasitic taxa for added variety. The usual opinion is that the exoparasitic taxa represent the ancestral lifestyle for the family, but the actual phylogeny of the family is still being hammered out (and the "usual opinion" may yet turn out to be the wrong opinion). About forty subfamilies are currently recognised, but most authors (e.g. Shi et al., 2005) divide those subfamilies between three main lineages, the cyclostomes, microgastroids and helcionoids, with some subfamilies of uncertain position relative to the three. The microgastroids and helcionoids are all koinobiont endoparasitoids (after the wasp has laid its eggs in the host, the host continues to grow and develop), while the cyclostomes include both exoparasitoids and endoparasitoids, with exoparasitoids usually paralysing the host before laying their eggs (Wharton, 1993). The microgastroids are fastidious in their tastes, restricting their diet to Lepidoptera (Murphy et al., 2008), while helcionoids attack a wide variety of hosts, including hemimetabolous as well as holometabolous insects. Early phylogenetic studies suggested that the cyclostomes (which possess a distinctive mouthpart morphology) were paraphyletic with regard to the other braconids, but more recent studies support a monophyletic cyclostome clade (Shi et al., 2005). The monophyly of a microgastroid + helcionoid clade is supported by molecular data (Shi et al., 2005), but remains short on morphological support (Quicke et al., 1999).


An individual of the genus Atanycolus (subfamily Braconinae in the cyclostome group). Photo by Richard Bartz.

The Aphidiinae are the largest group of braconids to not fit comfortably within the three-way division. Aphidiinae are parasitoids of aphids. Morphological data supports a relationship between aphidiines and the cyclostome group (Quicke et al., 1999), but the molecular analysis of Shi et al. (2005) suggested a relationship between the Aphidiinae and the Euphorinae, members of the helcionoids. The intriguing feature of this result is that Aphidiinae and Euphorinae both have the unusual characteristic (for insect parasitoids) of parasitising adult hosts rather than larvae - albeit with different host ranges in the two subfamilies. Euphorinae were probably originally parasitoids of beetles, but some species have since become parasitoids of hosts as diverse as grasshoppers or Psocoptera. (A more recent combined morphological and molecular study whose authors argued against an Aphidiinae-Euphorinae relationship in favour of an Aphidiinae-cyclostome connection [Zaldivar-Riverón et al., 2006] actually did not test anything either way, because the authors' choice of taxa and outgroup effectively forced an a priori cyclostome position).


An adult of Microgastrinae. Photo by Scott Justis.

Finally, some would think it rather remiss of me to write about braconids without making some mention of polydnaviruses, but I don't see why I should when a much better description of such things than I could produce has already been written by Merry Youle at Small Things Considered. After you read the main article there, though, make sure you scroll down the comments to Merry's description of the differences between polydnaviruses in Braconidae and Ichneumonidae suggesting the independent origins of the polydnavirus system in the two families. As well as the differences described by Mary, it also turns out that polydnaviruses are not characteristic of braconids as a whole, but are in fact only found within the microgastroid clade (Wharton, 1993), so an independent origin from ichneumonid polydnaviruses has phylogenetic as well as biochemical support.

REFERENCES

Murphy, N., J. C. Banks, J. B. Whitfield & A. D. Austin. 2008. Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Molecular Phylogenetics and Evolution 47 (1): 378-395.

Quicke, D. L. J., H. H. Basibuyuk & A. P. Rasnitsyn. 1999. Morphological, palaeontological and molecular aspects of ichneumonoid phylogeny (Hymenoptera, Insecta). Zoologica Scripta 28 (1-2): 175-202.

Shi, M., X. X. Chen & C. van Achterberg. 2005. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA, 28S rDNA D2, 18S rDNA gene sequences and morphological characters. Molecular Phylogenetics and Evolution 37 (1): 104-116.

Wharton, R. A. 1993. Bionomics of the Braconidae. Annual Review of Entomology 38: 121-143.

Zaldivar-Riverón, A., M. Mori & D. L. J. Quicke. 2006. Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): a simultaneous molecular and morphological Bayesian approach. Molecular Phylogenetics and Evolution 38 (1): 130-145.

Of Gregarines

An assortment of lecudinid eugregarines. The front end of the cell is towards the lower left in each individual. Image from Leander (2007) via Brian S. Leander.

The Sporozoa are perhaps the most famous group of protozoan parasites. As well as being one of the few protozoan groups distinctive enough to be well-characterised prior to the advent of electron microscopy and molecular analysis (albeit with a few hangers-on such as microsporidians and myxozoans that have since been cast aside from the sporozoan community), distinguished by their lack of motile organelles and intracellular invasion of their hosts, sporozoans include the causative agents of such maladies as malaria and toxoplasmosis. In many references, you may find the Sporozoa referred to as Apicomplexa, a name that refers to the apical complex, an organelle at the front end of the cell that is used to invade the cells of the sporozoan's host. However, as the apical complex is also found in some flagellates that are closely related to sporozoans (such as Colpodella), the name Apicomplexa is better used for the larger clade including these taxa while the name Sporozoa is restricted to the nested aflagellate clade (Cavalier-Smith & Chao, 2004).

Sporozoans have been divided into three classes, the invertebrate parasites Gregarinae (or Gregarinea), Coccidia (intestinal parasites of vertebrates) and Hematozoa (parasites of vertebrate blood cells). Phylogenetic analyses have indicated that the basal division in Sporozoa is between the vertebrate-parasitic Coccidia and Hematozoa on one branch (the Coccidiomorpha), and the Gregarinae on the other, though the Gregarinae is less well supported as monophyletic than the Coccidiomorpha and may yet be paraphyletic (Leander & Ramey, 2006; Leander et al., 2006). One notable exception is that the vertebrate parasite Cryptosporidium, previously regarded as a coccidian, may in fact be related to the gregarines or even derived from within them. Not surprisingly, their choice of hosts means that the Coccidiomorpha are by far the better studied of the two clades, while the Gregarinae have kind of been the poor relation. Nevertheless, it is the gregarines that are my focus today.

Gregarines have been divided into three groups, the archigregarines, eugregarines and neogregarines (Leander, 2007), but it seems more than likely that these represent a series of grades, with eugregarines paraphyletic to neogregarines and archigregarines paraphyletic to the eugregarine + neogregarine clade. In contrast to the complex life-cycles of some coccidiomorphs, gregarines have fairly simple life histories with only a single host. Transmission from one host to another is usually via oocysts released with the host faecal matter, but some gregarine oocysts hitch a ride with their host's gametes during copulation as protozoan STDs. Once inside the host, the oocysts hatch out into infective sporozoites that attach to or invade host cells and develop into feeding trophozoites. Some gregarines can reproduce asexually; the majority cannot. Sexual reproduction occurs by two trophozoites joining together as reproductive gamonts and becoming enclosed within a gametocyst; within the gametocyst they will each divide into hundreds of gametes that will fuse to form oocysts, ready for release.


Selenidium sp., showing the wriggling movement. From Leander (2007).

As I said before, the "archigregarines" probably represent the basal grade of gregarines. They are all intestinal parasites of marine invertebrates, and as such have been unfairly condemned as of little interest to anyone. Archigregarines have very similar sporozoites and trophozoites that are vermiform (worm-shaped) and generally move by wriggling (go here for videos of gregarine movement). Some archigregarines have cells with numerous longitudinal folds, others are smooth. Archigregarines also retain the ancestral characteristic of feeding on their host by using their apical complex to pierce the host cell and sucking out its contents.

The 'eugregarines' include the majority of gregarines (at least, the majority of described gregarines), and include parasites of freshwater and terrestrial as well as marine invertebrates. Again, their study has been biased towards those species that are parasites of insects, with the remainder being generally snubbed. Most marine eugregarines have been lumped together as the genus 'Lecudina', with little to unite them other than that they are marine eugregarines (Leander, 2007). Eugregarines differ from archigregarines in having morphologically quite distinct sporozoites and trophozoites. Their cell walls also became very rigid, and they lost the wriggling ability of archigregarines. Instead, eugregarines developed a system of gliding motility, with an actinomyosin skeleton running along the edge of the numerous surface folds. Ancestrally, eugregarines are intestinal parasites like archigregarines, but instead of the active feeding process of eugregarines, eugregarines absorb nutrients from the host through micropores on the cell surface (Leander et al., 2006).


Two conjoined gamonts of the polychaete coelom parasite Pterospora floridiensis. From Leander (2007).

Neogregarines are a derived subgroup of eugregarines with reduced trophozoites that specialise on terrestrial hosts (mostly insects) and mostly live in non-intestinal tissues. Another group of eugregarines, the urosporidians, became parasites of their host's coelom. Urosporidians lost their direct attachment to host cells, and became free-floating within the tissue as united gamont pairs. The gliding motility and longitudinal folds of other eugregarines were lost, and instead urosporidians move by pulsations of the cell walls. Cells became branched - many are V-shaped with two primary branches that each divide distally into a number of smaller "fingers".

Archigregarines in particular retain a number of features that are believed to be ancestral for sporozoans as a whole (such as sucking feeding), and Leander et al. (2006) suggest that they may constitute the ancestral group not just for eugregarines, but also for coccidiomorphs and hence sporozoans as a whole. Interestingly, gregarines (including archigregarines), so far as is known, lack the residual plastid found in coccidiomorphs. It is currently a subject of some debate as to whether the sporozoan (really coccidiomorph) plastid is homologous with that found in the related dinoflagellates or not (see here for an earlier take of mine on the issue), and the position of the plastid-less 'archigregarines' could have significant implications for this debate.

REFERENCES

Cavalier-Smith, T., & E. E. Chao. 2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.) European Journal of Protistology 40: 185-212.

Leander, B. S. 2007. Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24 (2): 60-67.

Leander, B. S., S. A. J. Lloyd, W. Marshall & S. C. Landers. 2006. Phylogeny of marine gregarines (Apicomplexa) — Pterospora, Lithocystis and Lankesteria — and the origin(s) of coelomic parasitism. Protist 157: 45-60.

Leander, B. S., & P. A. Ramey. 2006. Cellular identity of a novel small subunit rDNA sequence clade of apicomplexans: description of the marine parasite Rhytidocystis polygordiae n. sp. (host: Polygordius sp., Polychaeta). Journal of Eukaryotic Microbiology 53 (4): 280-291.

Christmas Is Coming

Western Australian Christmas tree, Nuytsia floribunda, in flower. Photo from Esperance Blog.

In the last few weeks, the Christmas trees near our house have begun flowering. Nuytsia floribunda, the Western Australian Christmas tree, is without doubt one of the most remarkable plants found in the Perth region. Even coming into my fourth summer here, the sight of a Christmas tree still never fails to catch my attention. Why are they so remarkable?

First, there's the appearance of the tree itself. For most of the year, a Christmas tree is a fairly insignificant, often decidedly scraggly, dark green tree. It can reach a height of about ten metres, but I don't think most of the ones I've seen (and they're not uncommon in remnant bush patches) have been anywhere near so tall. You could be quite readily forgiven for overlooking them. But all that changes about the beginning of November, when they begin to flower - heavily. What was a point of scraggly green becomes a blazing firebrand of burnished gold, as the entire tree becomes covered in individually tiny, but collectively magnificent, yellow flowers. The flowers remain during the next few months, past the end of December (hence, of course, the name), blazing like a beacon all the while.

As noteworthy as this blazing cheer alone would be, Nuytsia has even more points worthy of fascination to draw the attention. Despite its attraction, Nuytsia is rarely grown as a garden plant, and most attempts to do so meet with little success. Why is Nuytsia so recalcitrant? Because this showy shrub is something of a floral femme fatale, with dark secrets hidden beneath the soil. Nuytsia is a parasite, with a double Christmas connection - it is the world's largest mistletoe.


Plant roots with attached white Nuytsia haustoria. Photo from here (which also has a photo of Nuytsia haustoria attached to roots of broomrape, Orobanche minor, itself a holoparasite).

Mistletoes of the family Loranthaceae belong to a clade called Santalales that also includes such plants as sandalwoods. Most Santalales, including mistletoes, are hemiparasites - that is, they derive at least some of their nutrient requirements from other plants, but still retain chlorophyll and produce some of their nutrients themselves. The Santalales also include some non-parasitic species that form the paraphyletic outgroup to the parasitic clade (Nickrent & Malécot, 2001), and recent studies suggest that the holoparasitic (entirely parasitic) Balanophoraceae may also belong to the Santalales (Nickrent et al., 2005). As it is, the parasitic Santalales are, by any measure, the most successful clade of plant-parasitic angiosperms in existence.

The majority of mistletoes are aerial parasites, growing directly on the trunk or branches of the host tree. Nuytsia, however, is a root parasite. It grows in the ground like a normal tree, but its roots hunt through the soil in search of the roots of other plants to latch onto and parasitise. Once the roots come into contact with a potential host, they start growing a pair of lateral projections that wrap around the host root, forming a doughnut-shaped haustorium (nutrient-absorptive tissue). On the inside of the haustorium, a sharp, hard structure develops shaped like a pair of horns, or the blades of a pair of scissors (Calladine & Pate, 2000). The sharp inside edges of this structure quickly cut through the host root (exactly like a pair of scissors), severing it into two parts, and the haustorium then grows over the exposed ends of the roots, diverting the flow of nutrients and water away from the host and into the waiting Christmas tree. Nuytsia does not seem to be choosy when it comes to hosts - it may parasitise any trees within a radius of up to 150 m, but it may also parasitise smaller plants, even grass (allowing it to survive in locations without other trees). Nuytsia have also been recorded attempting to grow haustoria around buried twigs, small stones, and even electrical cables!


Cross-section of a Nuytsia haustorium, showing the hardened structure used to cut through the host root. Photo by Stephan Imhof.

Phylogenetic analysis shows that root parasitism represents the basal condition for parasitic Santalales, with multiple origins of aerial parasitism within the clade (Vidal-Russell & Nickrent, 2008). In fact, the root-parasitic Nuytsia, as well as being the largest member of the family, is also the sister taxon to all other Loranthaceae, making it a fascinating taxon phylogenetically as well as ornamentally and ecologically. So the next time any of you see a Christmas tree in flower, stop for a moment and consider how there's a lot more to it than you can see, hidden below the surface.

REFERENCES

Calladine, A., & J. S. Pate. 2000. Haustorial structure and functioning of the root hemiparastic tree Nuytsia floribunda (Labill.) R.Br. and water relationships with its hosts. Annals of Botany 85: 723-731.

Nickrent, D. L., J. P. Der & F. E. Anderson. 2005. Discovery of the photosynthetic relatives of the "Maltese mushroom" Cynomorium. BMC Evolutionary Biology 5: 38 (http://www.biomedcentral.com/1471-2148/5/38).

Nickrent, D. L., & V. Malécot. 2001. A molecular phylogeny of Santalales. In Proceedings of the 7th International Parasitic Weed Symposium (A. Fer, P. Thalouarn, D. M. Joel, L. J. Musselman, C. Parker, and J. A. C. Verkleij, eds.) pp. 69-74. Faculté des Sciences, Université de Nantes, Nantes, France.

Vidal-Russell, R., & D. L. Nickrent. 2008. The first mistletoes: origins of aerial parasitism in Santalales. Molecular Phylogenetics and Evolution 47 (2): 523-537.

Epsilon of the Deeps – Coming to an Organ System near You

The Pompeii worm (Alvinella pompejana), an inhabitant of deep-sea hydrothermal vents, with a covering of filaments composed of symbiotic ε-proteobacteria. Photo by Alison Murray.

The can be no denying that the direct analysis of DNA sequence data sparked a revolution in bacterial systematics. Previously-recognised taxa were reinforced or struck down, while entirely new groups were raised to recognition. The Proteobacteria were definitely one of the most significant of these new groups. By far the largest of the commonly-recognised major bacterial subdivisions, the Proteobacteria encompass a wide variety of taxa, including photosynthetic, colonial and heterotrophic forms. Indeed, the very name "Proteobacteria" reflects this diversity, naming the group after the shape-shifting Greek sea-god Proteus (the inclusion in the Proteobacteria of the the genus Proteus, named after the same polymorphic god, seems to have been purely a coincidence). Within the Proteobacteria, molecular data distinguished five major subdivisions, which have been rather prosaically dubbed the Alpha, Beta, Gamma, Delta and (surprise, surprise) Epsilon groups. Recent analyses have generally continued to support the distinction of these groups (though the boundary between the β and γ groups may sometimes be a little fuzzy), but it is with the last group, the Epsilonproteobacteria, that we are concerned today.

In terms of recognised species, the ε group is by far the smallest class of the proteobacteria, with only about fourteen described genera. The most-studied members of the group are mammalian pathogens such as Campylobacter and Helicobacter, species of the first of which can cause food poisoning, while species of Helicobacter have become famous for their role in the production of stomach ulcers and potentially increasing the risk of gastric and liver cancers. Other genera are also animal-associated - Wolinella succinogenes, for instance, is a non-pathogenic inhabitant of the cattle gut. However, the isolation of environmental DNA samples, as with so many other bacterial groups, demonstrated that our understanding of ε-proteobacterial diversity has been significantly biased by our ability to culture only a relatively small proportion of species. Epsilonproteobacteria, it turns out, are one of the predominant groups of extremophiles in marine systems. In one environmental DNA sample taken from a hydrothermal vent, Epsilonproteobacteria represented nearly 50% of the inferred diversity (Sogin et al., 2006). As I mentioned previously in a post on another group of extremophilic bacteria, the Aquificae, members of the Epsilonproteobacteria and Aquificae include the only known bacteria that are able to oxidise hydrogen in energy production (Takai et al., 2003). Epsilonproteobacteria have also been shown to be abundant in anaerobic hydrogen sulphide-rich cave springs (figure below from Engel et al., 2003).



Those few members of the Epsilonproteobacteria that have been cultured from hydrothermal vents don't appear to reach quite the thermophilic heights of Aquificae - Sulfurimonas is a mesophile (Inagaki et al., 2003), while Caminibacter and Hydrogenimonas showed optimum growth at 55°C (enough to kill a human with long-term exposure, but still small apples compared to the 100°C-plus temperatures reached by some hyperthermophiles – Miroshnichenko et al., 2004; Takai et al., 2004). A number of undescribed species are ectosymbionts of hydrothermal vent animals, such as the tube worms Alvinella pompejana and Riftia pachyptila or the shrimp Rimicaris exoculata.

Inasmuch as all bacterial phylogenies should be trusted as much as a grinning lunatic with one hand behind their back, the terrestrial Epsilonproteobacteria do appear to be nested within the extremophilic taxa, and the question of how deep-sea extremophiles potentially gave rise to terrestrial animal endosymbionts would be an interesting one. Do the Campylobacter and Helicobacter groups form a single clade, with the animal gut being colonised only the once, or where there multiple invasions? Lines are now open.

REFERENcES

Engel, A. S., N. Lee, M. L. Porter, L. A. Stern, P. C. Bennett & M. Wagner. 2003. Filamentous “Epsilonproteobacteria” dominate microbial mats from sulfidic cave springs. Applied and Environmental Microbiology 69 (9): 5503-5511.

Inagaki, F., K. Takai, H. Kobayashi, K. H. Nealson & K. Horikoshi. 2003. Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ε-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology 43: 1801-1805.

Miroshnichenko, M. L., S. L’Haridan, P. Schumann, S. Spring, E. A. Bonch-Osmolovskaya, C. Jeanthon & E. Stackebrandt. 2004. Caminibacter profundus sp. nov., a novel thermophile of Nautiliales ord. nov. within the class ‘Epsilonproteobacteria’, isolated from a deep-sea hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology 54: 41-45.

Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta & G. J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proceedings of the National Academy of Sciences of the USA 103 (32): 12115-12120.

Takai, K., S. Nakagawa, Y. Sako & K. Horikoshi. 2003. Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. International Journal of Systematic and Evolutionary Microbiology 53: 1947-1954.

Takai, K., K. H. Nealson & K. Horikoshi. 2004. Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the ε-proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. International Journal of Systematic and Evolutionary Microbiology 54: 25-32.