Field of Science

Black Yeasts, Black Lichens and Rotting Wood: the Chaetothyriomycetidae

Pyrenula cruenta, copyright Gary Perlmutter.


There is no denying that the advent of molecular phylogenetic analysis has been a boon for fungal systematics. It has allowed a much greater resolution of relationships than was previously possible (especially for comparisons between asexually- and sexually-reproducing fungi), and has even lead to the identification of a number of major lineages that probably could have never been recognised from morphological data alone. One such lineage is the Chaetothyriomycetidae, whose members vary from lichens on tropical tree trunks, to saprobes living in the deep sea, to pathogens in the brains of humans.

The Chaetothyriomycetidae (or Chaetothyriomycetes in many older references: the botanical code goes rather all out in the rather irritating practice of changing the endings of names to indicate arbitrary taxonomic ranks) has been divided by Gueidan et al. (2014) into four major lineages. Two of these, the Pyrenulales and Verrucariaceae, are mostly comprised of lichens. Lichenised fungi in the Pyrenulales associate with green algae of the family Trentopohliaceae (which, despite being 'green algae', are generally orange in colour), and are most commonly found on tree bark in tropical forests. Only one lichenised genus, Strigula, is also found growing on leaves; non-lichenised Pyrenulales are found on bark, leaves or wood (Geiser et al. 2006).

Verrucaria maura on coastal rocks, copyright A. J. Silverside.


The Verrucariaceae, in contrast, associate with different symbiotic algae, and prefer to grow on rocks. Lichens of this family are often blackish; their hyphae are darkened by a melanin-like compound which allows them to tolerate quite exposed conditions. Certain species are particularly prominent around the marine shoreline. Gueidan et al. (2014) also identified a small as-yet-unnamed lineage close to Verrucariaceae including rock-dwelling and moss-associated non-lichenised fungi, but support for this grouping requires further testing.

Another somewhat novel lineage identified by Gueidan et al. (2014) was the Celotheliaceae. The type genus, Celothelium, is a lichenised fungus that associates with the alga Trentepohlia in the manner of Pyrenulaceae. Other members of the Celotheliaceae, however, are quite different in ecology, being mostly pathogens of woody plants. Phaeomoniella chlamydospora is a causative agent of grapevine trunk disease, resulting in conditions such as esca, and the rather ominously named 'black goo decline' (so-called because the stems become filled with 'black goo', as the xylem vessels become clogged with fungal hyphae). Dolabra nepheliae causes canker in lychee and rambutan trees. These pathogenic taxa are commonly largely anamorphic (that is, they produce asexual reproductive structures).

Culture of black yeast Exophiala dermatitidis, from here.


The last and most diverse lineage (so far as we know, anyway) is the Chaetothyriales. Like the Verrucariaceae, the Chaetothyriales have melanised hyphae and often grow on exposed substrates such as rocks. Indeed, molecular analyses have supported a closer relationship between Verrucariaceae and Chaetothyriales than the other major lineages. However, members of the Chaetothyriales are not lichenised. Many are saprobic; others, such as the Chaetothyriaceae, grow on plant leaves but in many cases it is unclear whether they are saprobic or parasitic. The mostly saprobic family Herpotrichiellaceae also includes a number of asexually-reproducing forms that grow as yeasts and are opportunistic pathogens, including in humans. Infections by black yeasts (Exophiala) are most commonly cutaneous and relatively superficial, but they can also cause severe and life-threatening infections of deeper organ systems. These infections are most common in patients with pre-existing conditions affecting the immune system, but at least one species, E. dermatitidis, has been recorded causing fatal brain infections in otherwise healthy individuals.

And I referred at the beginning of this post to the deep sea? Well, the Chaetothyriomycetidae samples from there are, I believe, yet to be described. It is possible that this diverse group of fungi still has surprises for us.

REFERENCES

Geiser, D. M., C. Gueidan, J. Miadlikowska, F. Lutzoni, F. Kauff, V. Hofstetter, E. Fraker, C. L. Schoch, L. Tibell, W. A. Untereiner & A. Aptroot. 2006. Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98 (6): 1053-1064.

Gueidan, C., A. Aptroot, M. E. da Silva Cáceres, H. Badali & S. Stenroos. 2014. A reappraisal of orders and families within the subclass Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol. Progress 13: 1027-1039.

Teasels and Scabious: the Dipsacaceae

Scabiosa cretica, copyright Ori Fragman Sapir.


As recognised plant families go, the Dipsacaceae is not a particularly large one. It includes only a few hundred species, of which the majority are found in arid regions around the Mediterranean and the remainder elsewhere in Africa and Eurasia. The economic significance of the family is also relatively low. Some species are cultivated as ornamental plants. Dipsacus fullonum, teasel, gets its vernacular name because its bottle-brush-like flower-heads were used to tease the fibres of woollen cloth. Various species of Dipsacaceae, particularly the genus Scabiosa, are known as 'scabious' because they were apparently once used somehow in treating scabies. I also came across a reference in Duke (2008) to Syrian scabious Cephalaria syriaca having had a certain notoriety in the past due to its seeds being similar in appearance to wheat grain, meaning that they could be inadvertently sown into fields, or impart an unpleasant taste if ground into flour.

Flowers and fruits of Sixalix atropurpurea, copyright Manuel M. Ramos. Members of this genus grow on sand; their fruits have a reduced membranous wing, and disperse by rolling.


Nevertheless, the Dipsacaceae are not without their points of interest. One intriguing characteristic of the family is that they bear numerous small flowers clustered onto a single shared receptacle, similar to those of the much more diverse Asteraceae. Like Asteraceae, there may even be a differentiation in the appearance of flowers on the inner part of the receptacle from those around the outer rim. The Dipsacaceae are not directly related to the Asteraceae; rather, the two families have developed their capitate flower-heads independently. Which is not to say that they are incomparable: species of both Asteraceae and Dipsacaceae exhibit duplications of genes that are believed to affect the development of floral symmetry (Carlson et al. 2011), and it is possible that similar processes have lead to the evolution of compound flower-heads in both.

Flowers and fruits of Scabiosa sicula, copyright Jose Rodriguez. The fruiting head in focus shows the membranous wings that function in dispersal.


Past authors have divided the Dipsacaceae into three tribes, largely on the basis of characters related to seed dispersal. Each of the small flowers on a dipsacacean flower-head develops into a dry fruit containing a single seed. The epicalyx (an outer protective layer of the flower base) persists as an outer coating of the mature fruit, like a second skin. In the largest of the three previously recognised tribes, the Scabioseae, the epicalyx is often modified for wind dispersal, either by plumose hairs on top of a dorsal tube (the same sort of set-up as seen in dandelions) or by a membranous wing around the fruit. In contrast, the fruit of the genus Knautia, widow flowers, which has been placed in its own separate tribe, bears an elaiosome, a fleshy, hemispherical lump. The elaiosome attracts ants, who carry the fruit away to their nest; after the ants have eaten the elaiosome, the remaining seed is able to germinate where they leave it. Finally, the third tribe Dipsacaceae includes only the genera Dipsacus and Cephalaria; the mature fruit of these genera lack adaptations for either wind or ant dispersal, and seed dispersal is largely controlled by the break-up of the flower-head itself.

Bassecoia bretschneideri, copyright Dave Boufford.


More recent molecular analyses, however, have not entirely supported this three-way division of the Dipsacaceae (Carlson et al. 2009). While Knautia and the Dipsaceae are both likely to be monophyletic, the Scabioseae are not. Instead, a small clade including the eastern Asian genus Bassecoia is sister to the remaining members of the family. These fall into two major clades: one, that has been referred to as the Scabioseae 'sensu stricto', includes the majority of the taxa previously included in the Scabioseae, such as Scabiosa, Lomelosia and Pterocephalus. The other clade, which has been dubbed the 'dipknautids', includes Knautia and the Dipsaceae, together with a few smaller 'ex-Scabioseae' genera. While the original Dipsacaceae may have been wind-dispersed, they have not been above looking at alternatives.

REFERENCES

Carlson, S. E., D. G. Howarth & M. J. Donoghue. 2011. Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evolutionary Biology 11: 325. doi:10.1186/1471-2148-11-325.

Carlson, S. E., V. Mayer & M. J. Donoghue. 2009. Phylogenetic relationships, taxonomy, and morphological evolution in Dipsacaceae (Dipsacales) inferred by DNA sequence data. Taxon 58 (4): 1075-1091.

Duke, J. A. 2008. Duke's Handbook of the Medicinal Herbs of the Bible. CRC Press.

Friend and/or Foe: Separating Rhizobium and Agrobacterium

Roots of cowpea Vigna unguiculata with nodules containing Rhizobium, copyright Dave Whitinger.


For as far back as we have records to know, farmers have recognised the value of crop rotation: varying the crops grown on a particular patch of land in order to avoid exhausting the soil of nutrients. It also did not take these ancient farmers long to realise the value of one of these rotated crops being a legume, the group of plants including peas, beans, lentils and the like. What these pioneers of agriculture did not know was that the rejuvenating effect that legumes seemed to have on the soil was due to bacteria living in their roots, the organisms that we now know as Rhizobium.

The value of Rhizobium to agriculture comes from its ability to fix nitrogen. Nitrogen compounds are essential for all living organisms (proteins, for instance, contain nitrogen). But while nitrogen is also the most abundant element in our planet's atmosphere, most of it exists in a form that cannot be used directly by most organisms. Nitrogen-fixing bacteria are the exception, able to extract the nitrogen directly from the atmosphere and 'fix' it into more tractable compounds. Rhizobium is not the only genus of bacteria able to fix nitrogen, but it is certainly one of the most predominant. One of the limitations of nitrogen fixation is that it generally involves enzymes that do not work well in the presence of oxygen. Rhizobium cells induce the growth of nodules on legume roots, within which they are sheltered from that polluting gas. Not all Rhizobium live in legumes, however: they may also be found in large numbers free in the soil, with concentrations of tens of millions of cells per gram of soil having been recorded (Kuykendall et al. 2005).

Crown gall caused by Agrobacterium tumefaciens, copyright Christoph Müller.


Rhizobium has been regarded as closely related to another bacterial genus called Agrobacterium, whose significance for agriculture has been seen somewhat less favourably. As classically distinguished, Agrobacterium species do not fix nitrogen like Rhizobium, but they do resemble Rhizobium in causing growths on plant roots. These might be tumours, as in Agrobacterium tumefaciens (which can also cause galls to form elsewhere on the plant), or an overabundance of small rootlets, as in A. rhizogenes. While not necessarily fatal to the host plant, these deformities do often stunt growth, causing a loss in yield. A third species, A. radiobacter, has been recognised for non-pathogenic Agrobacterium.

However, as microbiologists gained a better understanding of the underlying genetics of Rhizobium and Agrobacterium, the picture became more complicated. The ability of Rhizobium to fix nitrogen, and of Agrobacterium to cause root deformities, is due to particular sets of genes in each. These genes are not contained in the main chromosome of each bacterium, but are held in little 'mini-chromosomes' called plasmids. And plasmids can be readily transferred from one bacterial cell to another. Through the transfer of the right plasmids, an Agrobacterium might gain the ability to fix nitrogen, or a Rhizobium might start inducing tumours. Phylogenetic analyses of the genera also indicated that some 'Rhizobium' were more closely related to 'Agrobacterium', and vice versa. As a result, at least one group of researchers has proposed uniting the two genera into one, Rhizobium. But others have been loathe to abandon a name as long-used in both the microbiological and agricultural literature as Agrobacterium (Farrand et al. 2003). There are recognisably distinct phylogenetic lines within the family Rhizobiaceae that includes the two genera, and even differences in plasmids are not entirely uninformative: not all strains can utilise all plasmids.

Cells of Rhizobium trifolii on root hair of clover, copyright Frank Dazzo.


There are also some significant genomic differences involved. Some of you may have learnt in biology class that the normal arrangement for bacterial cells is to have the bulk of the genome contained in a single circular chromosome, possibly with a scattering of small plasmids. The difference between the two is that the cell can function without the plasmids, but not without the chromosome. Rhizobium leguminosarum, the type species of Rhizobium, keeps to this arrangement, as do most other Rhizobium (though the plasmid containing the nitrogen-fixation genes is a bit of a whopper by usual standards). However, Agrobacterium tumefaciens*, the type species of its genus, is more unusual in having not one but two chromosomes: some of its vital genes have been transferred to what was originally a large plasmid (Slater et al. 2009). What is more, this second chromosome is not formed as a circle like other bacterial chromosomes, but is linear like the chromosomes of eukaryotes. Another 'Agrobacterium' species, A. vitis, has the second chromosome like A. tumefaciens but it remains circular. The type strain of A. rhizogenes, on the other hand, has only a single circular chromosome, and appears to be closer to Rhizobium.

*The type strains of 'Agrobacterium tumefaciens' and 'A. radiobacter' are close enough that the two names should be synonymised into a single species. However, there seems to be an on-going dispute over which of the two names should be used for the combined taxon. I'm using A. tumefaciens for convenience, but I wouldn't be able to judge which of the sides is correct.

Phylogenetic analysis also supports the recognition of a further genus of Rhizobiaceae, Ensifer, sitting outside the clade including Rhizobium and Agrobacterium. The type species of Ensifer, E. adhaerens, is a soil-dwelling bacterium that can live as a predator of other bacteria. It attaches to them end-wise (when multiple E. adhaerens attach to a single target cell, they may form a palisade) and causes them to burst open. Ensifer adhaerens is not an obligate predator—when suitable prey is not available, it can survive on free nutrients in the soil—and when analysed it turns out to be related to a clade of nitrogen-fixing bacteria previously recognised as the genus 'Sinorhizobium'. Indeed, one species of this genus turned out to be simply a non-parasitic form of E. adhaerens (Young 2003).

REFERENCES

Farrand, S. K., P. B. van Berkum & P. Oger. 2003. Agrobacterium is a definable genus of the family Rhizobiaceae. International Journal of Systematic and Evolutionary Microbiology 53 (5): 1681-1687.

Kuykendall, L. D., J. M. Young, E. Martínez-Romero & H. Sawada. 2005. Genus I. Rhizobium Frank 1889, 337AL. In: Garrity, G., D. J. Brenner, N. R. Krieg & J. T. Staley (eds) Bergey's Manual of Systematic Bacteriology vol. 2. The Proteobacteria, Part C. Springer.

Slater, S. C., B. S. Goldman, B. Goodner, J. C. Setubal, S. K. Farrand, E. W. Nester, T. J. Burr, L. Banta, A. W. Dickerman, I. Paulsen, L. Otten, G. Suen, R. Welch, N. F. Almeida, F. Arnold, O. T. Burton, Z. Du, A. Ewing, E. Godsy, S. Heisel, K. L. Houmiel, J. Jhaveri, J. Lu, N. M. Miller, S. Norton, Q. Chen, W. Phoolcharoen, V. Ohlin, D. Ondrusek, N. Pride, S. L. Stricklin, J. Sun, C. Wheeler, L. Wilson, H. Zhu & D. W. Wood. 2009. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. Journal of Bacteriology 191 (8): 2501-2511.

Young, J. M. 2003. The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an Opinion. International Journal of Systematic and Evolutionary Microbiology 53 (6): 2107-2110.

The Gordian Mouse

North American deer mouse from near Santa Fe, New Mexico, possibly Peromyscus sonoriensis. Copyright J. N. Stuart.


The North American deer mouse Peromyscus maniculatus has been recognised as one of the most widespread mammal species in North America. It has been recorded from most of the continent, with the main areas of absence being northern Canada and Alaska, the south-eastern corner of the United States (where it is replaced by a closely related species, the smaller Oldfield deer mouse Peromyscus polionotus) and coastal regions of Mexico. They are highly adaptable animals, eating a wide range of foods, and their tendency to gnaw just about anything available for food or nesting has not always endeared them to their human compatriots. In recent years, they have also received their fair share of unwelcome attention as vectors for pathogens such as the Sin Nombre hantavirus*, which causes a devastating (and commonly fatal) pulmonary disease in humans. It is therefore not surprising that the deer mouse has become one of the most extensively studied mammal species out there (not quite in house mouse or black rat territory, maybe, but still definitely up there). A search for 'Peromyscus maniculatus' on Google Scholar brings back well over 16,000 results. Surely with this degree of attention, this is at least one taxon for which I cannot deploy my usual 'the taxonomy is uncertain'?

*'Sin nombre' is, of course, Spanish for 'without name'. The reason for this coy appellation is that the virus in question was first labelled the 'Four Corners' virus after being identified from patients in that region of the United States in 1993, but was renamed after residents of the region protested.

Of course it isn't. Quite the opposite, in fact. With a range this large, it is not surprising that a fair amount of variability has been recognised in the North American deer mouse over the years. Over sixty subspecies of Peromyscus maniculatus have been recognised from various regions. This variability has also been part of the deer mouse's appeal as a study animal, as evolutionary scientists have examined the relationships between subspecies. The problem comes when you realise that in some places you may find two distinct 'subspecies' of deer mouse in a single locality. If a 'subspecies' is defined as a geographical sub-unit of a reproductively coherent species (as it traditionally has been), then that ain't right. Two taxa occupying a single range and not interbreeding should be separate species, surely? But travel to another location nearby, and you'll find the two 'species' interbreeding and merging into one. One case that has been cited as a classic example of a 'ring species' is around the Rocky Mountains, where the subspecies P. maniculatus artemisiae and P. m. nebrascensis do not interbreed with each other, but both interbreed with other subspecies to the north and south.

Part of the problem, of course, is that the 'species' is just a horrendously messy concept. There are a wealth of different species concepts out there, but the essential ideal underlying most is that a 'species' represents the point at which the reticulating relationships between interbreeding individuals become less important for understanding relationships than the branching relationships between population lineages. Which is not a point at all. Lineages diverge at multiple, quasi-independent levels in the process of speciation—they separate geographically, behaviourally, genetically, morphologically—and there is no magic point at which they suddenly change from 'one species' to 'separate species'. Nevertheless, as the recent trend has been to recognise species on a finer level than in the past, it seems likely that the future will see a subdivision of the current Peromyscus maniculatus.

Figure showing distributions of lineages of Peromyscus maniculatus from Kalkvik et al. (2012).


Over much of its range, Peromyscus maniculatus can be divided between two main morphotypes: a forest form with larger ears and a longer tail, and an open-country form with smaller ears and a shorter tail. Where the two forms are found in one region, they maintain their ecological distinctiveness. However, because of the aforementioned hybridisation between geographically adjacent populations, it is unlikely that any subdivision of P. maniculatus will be directly between these two morphotypes. One split that has already been widely accepted was proposed by Hogan et al. (1993), who found that certain populations in coastal north-west North America were genetically quite distinct from other P. maniculatus, and recommended the recognition of a separate species P. keeni. Peromyscus keeni is also generally larger and longer-tailed than P. maniculatus. However, more recent studies of the phylogeography of North American deer mice by Dragoo et al (2006) and Kalkvik et al. (2012) have found that even with the removal of P. keeni, P. maniculatus remains paraphyletic to both that species, to the south-west species P. polionotus (whose distinction from P. maniculatus has not generally been questioned), and possibly to the Mexican P. melanotis. Both the later studies identified six major lineages within P. maniculatus, and Dragoo et al. (2006) suggested that it may need to be divided between at least three species. The 'true' Peromyscus maniculatus, under this scheme, includes the two lineages found in the north-east of North America (the original type locality of the species being in Labrador). A coastal lineage found in the south-west was identified by both studies as related to P. keeni, and it remains to be seen whether it would be better included in that species or recognised as its own separate species. A lineage identified in southern New Mexico could be recognised under the name of Peromyscus blandus. The remaining two lineages, one found around the Rocky Mountains and one in the Great Plains, formed a clade that Kalkvik et al. (2012) identified as the sister lineage of P. polionotus. Dragoo et al. suggested that the name Peromyscus sonoriensis was available for this clade. However, Kalkvik et al. recognised that the Rocky Mountain lineage was a forest form and the Great Plains lineage a open-country form, so there may be grounds for their recognition as distinct species.

While the correlation between these studies appears promising, it must be stressed that both were analysing the same gene (cytochrome b) and it remains to be seen whether the lineages they identified continue to be supported by other sources of data. It also needs to be seen whether they stand up to the inclusion of further populations: western Canada and Mexico stand out as poorly sampled areas in both studies. Peromyscus maniculatus in its current form may represent one species, it may represent four, or it may yet refer to even more than that.

REFERENCES

Dragoo, J. W., J. A. Lackey, K. E. Moore, E. P. Lessa, J. A. Cook & T. L. Yates. 2006. Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses. Journal of General Virology 87: 1997-2003.

Hogan, K. M., M. C. Hedin, H. S. Koh, S. K. Davis & I. F. Greenbaum. 1993. Systematic and taxonomic implications of karyotypic, electrophoretic, and mitochondrial-DNA variation in Peromyscus from the Pacific Northwest. Journal of Mammalogy 74 (4): 819-831.

Kalkvik, H. M., I. J. Stout, T. J. Doonan & C. L. Parkinson. 2012. Investigating niche and lineage diversification in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group. Ecography 35: 54-64.

Bits of Cucumber in the Fossil Record

Aggregation of Eocaudina septaforminalis sclerites from Boczarowski (2001). Scale bar = 200 µm.


Echinoderms are a dream group of animals for invertebrate palaeontologists (that's palaeontologists who study invertebrates, not palaeontologists who are invertebrates). Their calcified skeletons mean that their fossil record is extensive and detailed. When most of the body is covered in plates, looking at the fossil can give you an instant idea of what the animal looked like when alive. But as with all things in biology, there are notable exceptions. The sea cucumbers are one group of echinoderms that has significantly reduced the original skeleton, sacrificing a hard outer skeleton for increased flexibility. Instead of solid plates, the sea cucumber skeleton is made up of many minute sclerites embedded in the skin. And while this may be all well and good for the sea cucumber, it is not so convenient for the palaeontologists. In the fossil record, these minute sclerites become separated, and one separated sclerite does not tell you much about the appearance of the sea cucumber as a whole.

As a result, palaeontologists looking at sea cucumber remains have found themselves presented with a conundrum. The classification of modern sea cucumbers is largely based on features of the soft body that are usually not preserved in the fossil record, making comparison of living and fossil cucumbers difficult. Also, the skeleton of a single sea cucumber may include different forms of sclerite, performing different roles. If two different types of sclerite are found close together in the fossil record, did they come from a single sea cucumber or from two different sea cucumbers that died close together? To bypass these barriers, palaeontologists have often used what are referred to as 'parataxa'. A single type of sclerite is treated as a single 'parataxon', with the recognition that there may not be a perfect correlation between the parataxon and the theoretical taxon that it originally came from.

Individual calclamnine sclerite, Priscocaudina crucensis, from Boczarowski (2001).


The Calclamnidae has been recognised as one such 'parafamily' of sea cucumber sclerites. As defined by Frizzell & Exline (1966), the Calclamnidae grouped together rounded or polygonal sclerites that are perforated with holes like a sieve, and that don't have any sort of stalk or other ventral protrusion. This is a very common sort of sclerite for echinoderms: 'calclamnid' sclerites have been identified as far back as the Ordovician (Boczarowski 2001), and sclerites of this sort are still found in sea cucumbers today (just to confuse matters, the skeletons of some brittle stars also include very similar sclerites, raising the spectre of misidentification). Boczarowski (2001) recognised two subfamilies of Calclamnidae: in one, the Eocaudininae, the perforations of the sclerite are all more or less even in size, while in the other, Calclamninae, the pores towards the centre of the plate are larger and arranged in a cross-shape. The eocaudinines include the earliest calclamnid plates, with the calclamnines appearing during the Devonian.

Recognition of parataxa is a convenient tool for keeping records of things like biostratigraphy without getting bogged down, but what sort of sea cucumber did calclamnids actually come from? The calclamnids resemble sclerites found in the group of modern sea cucumbers called the Dendrochirotacea, so they have often been classified with this group. However, a number of features of the dendrochirotaceans, including perforated calclamnid-like sclerites, have been suggested to be primitive for sea cucumbers, so similarities between calclamnids and dendrochirotaceans may represent shared ancestral features rather than true affinities. Haude (1992) commented on a number of cases of sclerites found preserved in assemblages that he believed represented original life associations, including some containing calclamnids. One of these contained sclerites that Haude identified as similar to Calclamna germanica, the type species of the family, in association with large hook-shaped sclerites. Hooks are not characteristic of dendrochirotaceans, but of Apodacea, a different group of sea cucumbers characterised by the loss of tube feet (with the hooks working to provide mobility in their place). Haude suggested the possibility that Calclamna might represent a stem-group apodacean that retained some primitive sclerite features. In other fossil groups such as conodonts, the identification of preserved assemblages has allowed palaeontologists to progress beyond the use of parataxa and integrate more recognition of evolutionary relationships. Hopefully we get the same opportunity with sea cucumbers.

REFERENCES

Boczarowski, A. 2001. Isolated sclerites of Devonian non-pelmatozoan echinoderms. Palaeontologia Polonica 59: 1-219.

Frizzell, D. L., & H. Exline. 1966. Holothuroidea—fossil record. In: Moore, R. C. (ed.) Treatise on invertebrate Paleontology pt U. Echinodermata 3 vol. 2, pp. U646-U672. The Geological Society of America, Inc., and The University of Kansas Press.

Haude, R. 1992. Fossil holothurians: sclerite aggregates as 'good' species. In: Scalera-Liaci, L., & C. Canicatti (eds) Echinoderm Research 1991, pp. 29-33. Balkema: Rotterdam.

The Mighty Limpets

The limpet Nacella concinna on bull kelp Durvillea, copyright David Cothran.


I am Clamp the mighty limpet,
I am solid, I am stuck.
I am welded to the rockface
with my super-human suck.


The hero of Pam Ayres' "Clamp the Mighty Limpet" is a misanthropic Napoleon, threatening would-be harassers with lost fingernails and the danger of attachment (if they would only be willing to stand in one place for two weeks). In reality, 'limpet' is a name that has been applied to a number of unrelated groups of gastropod with cap-like, more-or-less uncoiled shells. The most prominent group of limpets, however, and the one that Ayres almost certainly had in mind, is the 'true limpets' of the Patellogastropoda.

Owl limpet Lottia gigantea, copyright Jerry Kirkhart.


The Patellogastropoda are a mostly marine group of molluscs, though one species in south-east Asia, Potamacmaea fluviatilis, is found in rivers and brackish waters adjoining the Bay of Bengal (Lindberg 2008). The group takes its name from the north-east Atlantic genus Patella, which has been featured on this site in an earlier post. Patellogastropods are particularly prominent in the intertidal zone, where they can be found clinging to rocky surfaces, but there are also many subtidal or deep-water limpets. Some limpets are specialised for living on macro-algae or marine vegetation; one such species, the North Atlantic Lottia alveus, has previously been mentioned on this site due to its unfortunate extinction as a result of the wasting epidemic that devastated sea-grass populations in the 1930s. Deep-water patellogastropods may be found on sunken wood, or they may live in association with hydrothermal vents or cold seeps. One such genus, Serradonta, is restricted to the tubes of vestimentiferan worms (Nakano & Sasaki 2011).

Whitecap limpet Acmaea mitra, copyright Mary Jo Adams.


Phylogenetically speaking, patellogastropods are a very interesting group indeed. Morphological studies have identified them as the sister group to all other living gastropods. They have a distinctive radula morphology, known as 'docoglossan', with each tooth-row of the radula containing a median tooth flanked by a small number of relatively simple lateral and marginal teeth (up to three pairs of each). This contrasts with the radulae of other gastropods, in which the teeth are more numerous and/or more specialised, but resembles the radula of other molluscan groups such as chitons. As such, patellogastropods may retain the plesiomorphic radula morphology of gastropods as a whole. Patellogastropods also have a shell microstructure that differs from that of other gastropods, and they have their gonads in a ventral position relative to the visceral mass instead of the dorsal position of other gastropods (Lindberg 2008). Some have even suggested that patellogastropods may represent a remnant lineage that never underwent the coiling that characterises other gastropods, but this seems unlikely. Patellogastropods do have some features, such as an asymmetrical position of the protoconch (larval shell) on the mature shell, that suggest coiled ancestors. Molecular studies, on the other hand, have been more equivocal in positioning the patellogastropods. Some have given results consistent with the morphological analyses, but a few have failed to place patellogastropods with the other gastropods at all (e.g. Giribet et al. 2006), while many have placed them in a more nested position deeper within the gastropods (Zapata et al. 2014).

Ringed blind limpet Cryptobranchia concentrica, copyright L. Schroeder.


At face value, the fossil record might actually appear to support a more nested position for patellogastropods. The fossil record for gastropods as a whole extends back to the Cambrian, but the oldest definite record of patellogastropods goes back no further than the late Triassic (Frýda et al. 2009). If patellogastropods were indeed the earliest surviving gastropod lineage to diverge, where were they hiding for the intervening 200 million years or so? One possibility is that they were there, but did not get preserved. Phylogenetic analysis of living limpets suggests that the immediate ancestors of the patellogastropods clung to rocks in high-energy environments, with deep-water lineages occupying more nested positions in the tree (Nakano & Sasaki 2011). Such environments are not favourable to the fossil record, as the shells of dead limpets tend to get broken up by wave action before they have the chance to be fossilised. Another, more likely, possibility is that we have failed to recognise the coiled ancestors of the Patellogastropoda for what they are. The Palaeozoic gastropod fauna included a number of groups that are not present in the modern day; it is quite possible that one of these groups gave rise to the patellogastropods. One group that has specifically been nominated as a possible relative of the patellogastropods is the euomphaloids. But for now, Clamp the Mighty Limpet is holding the secrets of his affinities well hidden, and it will not be easy prising them off him.

REFERENCES

Frýda, J., P. R. Racheboeuf, B. Frýdová, L. Ferrová, M. Mergl & S. Berkyová. 2009. Platyceratid gastropods—stem group of patellogastropods, neritimorphs or something else? Bulletin of Geosciences 84 (1): 107-120.

Giribet, G., A. Okusu, A. R. Lindgren, S. W. Huff, M. Schrödl & M. K. Nishiguchi. 2006. Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences of the USA 103 (20): 7723-7728.

Lindberg, D. R. 2008. Patellogastropoda, Neritimorpha, and Cocculinoidea. In: Ponder, W. F., & D. R. Lindberg (eds) Phylogeny and Evolution of the Mollusca, pp. 271–296. University of California Press.

Nakano, N., & T. Sasaki. 2011. Recent advances in molecular phylogeny, systematics and evolution of patellogastropod limpets. Journal of Molluscan Studies 77 (3): 203-217.

Zapata, F., N. G. Wilson, M. Howison, S. C. S. Andrade, K. M. Jörger, M. Schrödl, F. E. Goetz, G. Giribet & C. W. Dunn. 2014. Phylogenomic analyses of deep gastropod relationships reject Orthogastropoda. Proceedings of the Royal Society of London Series B 281: 20141739.

Sybra punctatostriata

Sybra punctatostriata, from here.


Just a very brief post today, because once again I've drawn a species that I haven't been able to find too much about. Sybra punctatostriata is a member of the Cerambycidae, the longicorn beetles, a diverse but (usually) fairly distinctive group of beetles whose larvae burrow into wood and plant stems. This species was first described by H. W. Bates in 1866 as part of a collection of beetles from Taiwan. Since then, it has been recorded over a wide area stretching from Japan in the north to Hainan in the south (though mostly in Japanese and Chinese sources that I don't have access to, and probably couldn't follow if I did). However, Samuelson (1965) indicated that S. punctatostriata was one of a number of very similar species in the genus Sybra, hinting that its range may require revision. Samuelson himself only identified a single specimen of S. punctatostriata from Okinawa in collections of beetles from the Ryukyus, which he described as showing some small differences from Taiwan specimens.

Another view of Sybra punctatostriata from the same site.


Sybra punctatostriata has been recorded feeding on Gossypium, the genus that includes cotton. However, other Sybra species are known to have wide host ranges. Sybra alternans, a species that has been recorded infesting bananas, has also been known to feed on fig trees, pineapple plants, passionfruit vines, beans... (Chen et al. 2001). It is possible that S. punctatostriata's host range may also be wider than recorded.

REFERENCES

Bates, H. W. 1866. On a collection of Coleoptera from Formosa, sent home by R. Swinhoe, Esq., H.B.M. Consul, Formosa. Proceedings of the Zoological Society of London 1866: 339-355.

Chen, H., A. Ota & G. E. Fonsah. 2001. Infestation of Sybra alternans (Cerambycidae: Coleoptera) in a Hawaii banana plantation. Proc. Hawaiian Entomol. Soc. 35: 119-122.

Samuelson, G. A. 1965. The Cerambycidae (Coleopt.) of the Ryukyu Archipelago II, Lamiinae. Pacific Insects 7 (1): 82-130.