Eurotiomycetes: Small but Significant Fungi

Mention the word 'fungi' and most people's thoughts will probably go to images of mushrooms or toadstools. A few may conjure up pictures of lichens. Nevertheless, the great majority of fungal species are microscopic and likely to pass unremarked by most observers. That does not, however, mean that they are of no consequence. Today's post involves one major group that, for all their visual insignificance, include some of the most significant fungal species for modern human society: the Eurotiomycetes.

Developmental stages of Aspergillus glaucus, with cleistothecia as figs 21–23, from Raper & Fennel (1965).

The class Eurotiomycetes has been recognised in recent years as including a diverse assemblage of fungi, associated with a wide range of morphologies and habitats, that are united as a clade by molecular analyses. Réblová et al. (2017) recognised five subclasses within the Eurotiomycetes of which the two largest (or at least the most studied) are the Eurotiomycetidae and the Chaetothyriomycetidae. The Eurotiomycetidae are, for the greater part, saprobes. They were largely recognised as a distinctive group even before the advent of molecular phylogenetic analysis owing to the production by sexually reproducing forms of a distinctive type of fruiting body, the cleistothecium. In cleistothecia, the fruiting body is completely enclosed with no openings to faciliatate the release of spores, which only escape when the fruiting body itself breaks down. Cleistothecia are most commonly produced by fungi that grow in enclosed locations such as underground (the Eurotiomycetidae are not the only group of fungi to produce cleistothecia though they are one of the most diverse). Within the cleistothecium, spores develop within globular asci with a single wall that breaks down shortly after maturity (Geiser et al. 2015).

Penicillium expansum on rotting pear, copyright H. J. Larsen.

For many people, though, the most familiar members of the Eurotiomycetidae are likely to be asexually reproducing forms. This is the clade containing the moulds of the genera Aspergillus and Penicillium. Even before a species of the latter achieved fame as the shource of the first known antibiotic, penicillin, members of these genera had a great impact on human lives. Species of Penicillium are the moulds used in the production of cheeses such as Roquefort and camembert. Species of Aspergillus are used to ferment soy beans and rice in the production of comestibles such as soy sauce and sake. On the flip side, a number of species of Eurotiomycetidae act as pathogens of mammals including humans, causing conditions such as respiratory illnesses or tinea, with the former being of particular concern in immunocompromised individuals. Eurotiomycetid moulds may also cause problems for food storage and the like, particularly as many species are capable of growing under remarkably hot and/or dry conditions. Some Aspergillus moulds produce dangerous toxins, capable of causing acute poisioning or cancer development.

Verrucaria maura, copyright Richard Droker.

The Chaetothyriomycetidae are less clearly defined morphologically than the Eurotiomycetidae but fruiting bodies are mostly produced as perithecia: flask-shaped structures with an apical pore through which spores are released. The asci within the perithecium usually possess a double wall. Like many eurotiomycetids, chaetothyriomycetids have a tendency to be associated with habitats where water availability is a concern such as in very dry and/or saline environments. A number of chaetothyriomycetid species form lichens. One genus, Verrucaria, is often found as a thin black lichen growing on rocks along the seashore. Some species grow within the cavities of myrmecophytes, plants that form mutualistic associations with ants (the plant provides food and/or accomodation for the ants and the ants help keep the plant clear of grazers or sap-suckers). The fungi are cultivated by the ants that use them for food.

The other three subclasses of the Eurotiomycetes are less well known and recognised as containing a single order each. The Sclerococcales were first recognised as such by Réblová et al. (2017) via molecular analysis. Fruiting bodies, where known, are apothecia (open bowls) bearing single-walled asci. Representatives are known from marine and terrestrial habitats, growing on wood or lichens, and some have been isolated from within the digestive tracts of bark beetles. The Coryneliaceae, living as parasites on podocarps, have been considered as morphologically intermediate between chaetothyriomycetids and eurotiomycetids. Molecular analysis positions them as sister to the latter (Wood et al. 2016). Finally, the Mycocaliciales live as parasites or commensals of other fungi, particularly lichens.

There are other representatives of the Eurotiomycetes that I haven't even had the time to gloss over, such as endophytes and ectomycorrhizal truffles. You may not know they're there but that doesn't mean they don't mean anything to you.

REFERENCES

Geiser, D. M., K. F. LoBuglio & C. Gueidan. 2015. Pezizomycotina: Eurotiomycetes. In: D. J. McLaughlin, & J. W. Spatafora (eds) The Mycota 2^nd ed. vol. 7. Systematics and Evolution part B pp. 121–141. Springer-Verlag: Berlin.

Réblová, M., W. A. Untereiner, V. Štěpánek & W. Gams. 2017. Disentangling Phialophora section Catenulatae: disposition of taxa with pigmented conidiophores and recognition of a new subclass, Sclerococcomycetidae (Eurotiomycetes). Mycological Progress 16: 27–46.

Wood, A. R., U. Damm, E. J. van der Linde, J. Z. Groenewald, R. Cheewangkoon & P. W. Crous. 2016. Finding the missing link: resolving the Coryneliomycetidae within Eurotiomycetes. Persoonia 37: 37–56.

The Glyceriforms: Stabby Worms and Grabby Worms

Historically, the annelid worms have been considered a difficult group to classify. Whereas most of the recognised families have been fairly well established, higher taxa uniting these families have tended to be a bit on the vague side. Nevertheless, there are some supra-familial groups that can be considered well established, one such group being the Glyceriformia.

Specimen of Goniadidae (head to the right), from NOAA Fisheries.

The glyceriforms are two families of marine worms, the Glyceridae and Goniadidae. More than a hundred species are known in this clade (over forty glycerids and over sixty goniadids), found in habitats ranging from the intertidal to the abyssal. They range in size from about a centimetre in length to well over half a metre. The front end of the body tapers to a narrow, elongate conical point in front of the mouth, bearing two terminal pairs of small, slender appendages that may correspond to the antennae and palps of other worms. Eyes may be present or absent. The pharynx forms a remarkably elongate, eversible proboscis. In Glyceridae, the proboscis ends in a ring of four hook-shaped jaws, all similar to each other. In Goniadidae, the arrangement of jaws is more complex with the usual arrangement being small micrognaths on one side of the ring and larger macrognaths on the other. Glycerids usually have a transparent skin and an overall red or white colour reflecting the coloration of the internal fluids (red-coloured individuals are sometimes known as 'bloodworms', as are many other similarly coloured worm-like invertebrates). Goniadids have a more opaque cuticle and often have an iridescent sheen (Rouse & Pleijel 2001).

Glycera dibranchiata with everted proboscis, from the Yale Peabody Museum.

Glyceriforms most commonly live as burrowers in muddy or sandy substrates though some live on the surface of rocks. Most are carnivores of active invertebrates such as crustaceans or other worms; some may be detritivores. They may be vagile or they may construct permanent galleries of burrows with multiple entrance and exit openings in which they wait to lunge at anything foolish enough to pass nearby. In glycerids, the stabby jaws are associated with venom glands leading to ducts opening through pores on the jaw's underside. In some species, this venom is strong enough to cause a painful reaction in humans (though I haven't come across any references to long-term consequences). Goniadids lack venom glands and seem to rely on the physical use of their jaws to capture prey. As with many other marine worms, reproduction happens via pelagic epitokes. As a suitable time approaches (Prentiss, 2020, records goniadid epitokes emerging only during a full moon), the glyceriform worm undergoes a metamorphosis involving the break-down of the digestive system and enlargement of the parapodia. The transformed epitokes swim towards the surface where they release gametes through ruptures of the body wall, ending their life in a suicidal orgasm.

Close-up on proboscis of Glycera alba, copyright Hans Hillewaert.

Because of their hardened jaws, which are mostly constructed of protein but partially mineralised, glyceriforms have quite a good fossil record compared to many other worms (Böggemann 2006). Fossilised glyceriform jaws have been found as far back as the Triassic and are little different from those of modern glyceriforms. Body fossils are, unsurprisingly, much rarer but a worm from the Carboniferous Mazon Creek fauna, Pieckonia helenae, has been identified as a stem-group goniadid. The glyceriform body plan seems to have been a very successful one, remaining essentially unchanged over hundreds of millions of years.

REFERENCES

Böggemann, M. 2006. Worms that might be 300 million years old. Marine Biology Research 2: 130–135.

Prentiss, N. K. 2020. Nocturnally swarming Caribbean polychaetes of St. John, U.S. Virgin Islands, USA. Zoosymposia 19: 91–102.

Rouse, G. W., & F. Pleijel. 2001. Polychaetes. Oxford University Press.

Piercing Fruit and Piercing Souls

The moths of the superfamily Noctuoidea are one of the most diverse subsections of the Lepidoptera, with probably somewhere between fifty and seventy thousand species known to date (Zahiri et al. 2012; as with other massively diverse clades, the lack of proper checklists and revisions makes the question of species number surprisingly difficult to answer). For many people, the classic image of a 'moth' will evoke a noctuoid: broad-winged, often nocturnal, often predominantly brown or grey in colour. Obviously, a group this size is going to have a complex taxonomy, and one of the significant subgroups of the noctuoids is the tribe Ophiusini.

Variable drab moth Ophiusa mejanesi, copyright Bernard Dupont.

Historically, the classification of noctuoids has been something of a mess. One researcher commented in 1975 that "It is exceptional to find any two authors who use the same combination of subfamily names within the Noctuidae" and Zahiri et al. admitted in 2012 that the validity of this statement still stood. Until recently, the majority of noctuoids were dumped in a broad family Noctuidae but recent studies (particularly influenced by molecular data) have lead to a significant rearrangement. As a result, the Ophiusini went from being usually placed in the family Noctuidae, subfamily Catocalinae, to the family Erebidae, subfamily Erebinae. A number of genera previously included in the Ophiusini were also transferred elsewhere; most notably, these included all New World representatives so the Ophiusini are now regarded as an exclusively Old World group.

Thyas juno, copyright Alexey Yakovlev.

The Ophiusini are mostly robust-bodied moths with wings of a fairly uniform background colour marked with simple, linear lines on the forewings. The males lack well-developed coremata (eversible structures used for dispersing pheromones) on the genital valves. The caterpillars are elongate semi-loopers with the front two pairs of abdominal prolegs much reduced compared to the rear two pairs. Larvae have been recorded from a wide range of host plant families but the most commonly exploited hosts are members of the Combretaceae and Myrtaceae (Holloway 2005). The pupa lacks the waxy bloom found in many other erebines.

Caterpillar of guava moth Ophiusa disjungens, copyright Robert Whyte.

Many members of the Ophiusini also have a modified apex to the adult proboscis bearing strong, enlarged spines and reversed, erectile hooks (Zahiri et al. 2012). This formidable apparatus is used to pierce the skins of fruits, allowing the moth to feed on their juice. As well as damage caused by browsing caterpillars, ophiusins may therefore also be of concern to horticulture due to damage from this fruit-piercing behaviour. As well as the damage caused by the moth itself, the resulting holes may allow the fruit to be attacked by disease or other insects not capable of breaching the rind themselves. The modified proboscis may also function in what is somewhat daintily referred to as lachrymal feeding: the process of applying the proboscis to the eyes of mammals (more rarely birds) and feeding on secreted fluids. Yes, these are moths that can potentially destroy an orchardist's crop... and then proceed to drink his tears.

REFERENCES

Holloway, J. D. 2005. The moths of Borneo (part 15 & 16): family Noctuidae, subfamily Catocalinae. Malayan Nature Journal 58: 1–529.

Zahiri, R., J. D. Holloway, I. J. Kitching, J. D. Lafontaine, M. Mutanen & N. Wahlberg. 2012. Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Systematic Entomology 37: 102–124.