Field of Science

A South American Paradox (Taxon of the Week: Sellocharis)

Aspects of Sellocharis paradoxa (Papilionaceae) as illustrated by Polhill (1976): "1, habit; 2, node with stem cut away to show leaf-arrangement; 3, flower; 4, calyx, opened out; 5, standard; 6, wing; 7, keel; 8, stamens, spread out; 9, anthers; 10, pistil; 11, same with ovary-wall cut away to show ovules".

A brief entry today, because Taxon of the Week this week is a bit of a mystery. The southern Brazilian leguminous subshrub Sellocharis paradoxa was first described in 1889, but for a very long time was known solely from the original isotypes*. It has only been rediscovered in scrubby grasslands and rockfields of the Brazilian state of Rio Grande do Sul within the last ten years or so (Conterato et al., 2007). Without having seen the original description, I can't tell you for certain what earned Sellocharis the name of 'paradoxa', but I suspect it was probably the unique arrangement of its leaves. As you can see in the figure above**, S. paradoxa has its leaves arranged in regular whorls of five to seven. The individual "leaves" are more similar to the leaflets of other leguminous plants, and Polhill (1976) tentatively suggested that that might be what they were - that instead of having whorls of six leaves, S. paradoxa might have only a single leaf that had lost its basal stalk so completely that it had merged with the main stem.

*For the non-botanists among you, "isotypes" are two or more type specimens that have been taken from the same original individual, such as two branches from a single tree.

**Now possibly the only depiction of Sellocharis available freely online. Not that I'm bragging or anything (especially considering I just scanned it out of the original book).

As befits its unusual morphology, the relationships of Sellocharis paradoxa are similarly mysterious. The most similar genus is Anarthrophyllum, a genus of Andean 'cushion plants' in which the stipules of the often trifoliate leaves surround the stem, often forming a sheath, and most authors seem to have assumed a relationship between the two genera. Flower morphology and the presence of α-pyridone alkaloids in Anarthrophyllum suggest a position in the Genisteae, the tribe including brooms, gorse and lupins, which I described in a previous post. Within the Genisteae, the flowers of Anarthrophyllum and Sellocharis are most similar to those of the basal Argyrolobium group. A large-scale molecular analysis of Papilionaceae placed Anarthrophyllum as sister to the clade of Lupinus and Genistinae (Wojciechowski et al., 2004), which is consistent with the previously suggested position of the Argyrolobium group (Ainouche et al., 2003) though no other members of the group were included in the later analysis. However, Polhill (1976) noted that, if one interprets the 'leaves' of Sellocharis as leaflets of a single divided leaf, then they bear a certain resemblance to the leaves of lupins and may indicate a relationship to that genus instead.

A genistean position for Sellocharis and Anarthrophyllum is still not un-problematic. As described in the previous post, the Genisteae is a primarily Old World lineage. Lupinus is the only other genus of Genisteae found in the Americas, and as it is found in both the Old and New Worlds it could be a later invader of the latter. Nevertheless, other genera of the Argyrolobium group are found in southern Africa, and the ancestors of Sellocharis may have come from there as other organisms are known to have done (the ancestors of the New World monkeys being perhaps the most famous example). Also potentially problematic is that the number and morphology of chromosomes in Sellocharis is very distinct from those of any other Genisteae; however, the authors who described Sellocharis' karyotype (Conterato et al., 2007) only referred to its differences from Genisteae without comparing it to members of other tribes. Hopefully, now that Sellocharis paradoxa has been re-found, more progress can be made on establishing just what it is.


Ainouche, A., R. J. Bayer, P. Cubas & M.-T. Misset. 2003. Phylogenetic relationships within tribe Genisteae (Papilionoideae) with special reference to genus Ulex. In Advances in Legume Systematics part 10, Higher Level Systematics (B. B. Klitgaard & A. Bruneau, eds.) pp. 239-252. Royal Botanic Gardens: Kew.

Conterato, I. F., S. T. Sfoggia Miotto & M. T. Schifino-Wittman. 2007. Chromosome number, karyotype, and taxonomic considerations on the enigmatic Sellocharis paradoxa Taubert (Leguminosae, Papilionoideae, Genisteae). Botanical Journal of the Linnean Society 155 (2): 223-226.

Polhill, R. M. 1976. Genisteae (Adans.) Benth. and related tribes (Leguminosae). Botanical Systematics 1: 143 - 368.

Wojciechowski, M. F., M. Lavin & M. J. Sanderson. 2004. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. American Journal of Botany 91: 1846-1862.

The Voice of the Turtle (Taxon of the Week: Streptopelia)

Eurasian collared dove Streptopelia decaocto, the most widespread Streptopelia species in Europe. Photo by Rovdyr.

The bird genus Streptopelia comprises the turtledoves or collared doves - thirteen to seventeen species (depending on preferred generic boundaries) of medium-sized, generally pinkish birds that have long garnered human admiration due to their attractive appearance and cooing vocalisations. The name "turtledove" is derived from the Latin turtur, which is itself an imitation of the sound made by the doves. The calls of different species of turtledoves are distinct, and often play a significant part in their identification (Slabbekoorn et al., 1999). Streptopelia doves are native to Africa and the warmer parts of Asia and Europe, but a number of species have been introduced to other parts of the world. Here in Perth, for instance, the laughing dove S. senegalensis and the spotted dove S. chinensis are both abundant (the former particularly so), while S. chinensis is also a successful exotic in Auckland back in New Zealand. Also widely introduced is the African collared dove or Barbary dove Streptopelia risoria*.

*The Barbary dove ("S. risoria") is the domesticated form of the African collared dove ("S. roseogrisea"), and most modern authors no longer regard the two as specifically distinct. S. risoria Linnaeus, 1758 has priority over S. roseogrisea Sundevall, 1857. However, it has become common practice for the name based on a "wild" taxon to be given preference over one based on a domestic taxon because of the often complicated nature of taxonomic concepts in relation to domesticated animals (Gentry et al., 2004), and so many authors have preferred to use S. roseogrisea for the combined taxon. A recent proposal to formalise this situation was turned down by the ICZN (ICZN, 2008), leaving S. risoria as the valid name for this species.

The Madagascar turtle dove Streptopelia picturata (aka Nesoenas picturata). Phylogenetic analysis indicates that this species is closely related to the pink pigeon Nesoenas mayeri (=Streptopelia mayeri) of Mauritius. Though distinct morphologically, the two species have very similar vocalisations. Photo from here.

In the past, Columbidae (pigeons and doves) have mostly been divided between two subfamilies, the Columbinae (standard columbids) and Treroninae (fruit-pigeons and fruit-doves), with separate monogeneric subfamilies for the morphologically distinctive genera Goura and Didunculus (and sometimes Otidiphaps) and a separate family Raphidae for the extinct dodo Raphus cucullatus and solitaire Pezophaps solitaria. This arrangement, never particularly sturdy at the best of times, has been blown out of the water by recent analyses (Pereira et al., 2007), which render the traditional Columbinae paraphyletic to the other subfamilies and Raphidae while the Treroninae becomes polyphyletic. To date, no-one has formally proposed a revised subfamilial classification of Columbidae, though Pereira et al. (2007) did recognise three well-supported clades in the family which they called simply A, B and C*.

*Because I have the comfort of knowing that no-one is going to take any notice of me in this matter, I can reveal that if we were to recognise these three clades as a subfamily each, they would become respectively Columbinae, Claravinae and Raphinae (going by the dates reported in Bock, 1994), and I find a certain pleasant irony in the idea that Raphinae would be the largest of the three.

The collared dove Streptopelia chinensis (=Stigmatopelia chinensis). Originally native to eastern Asia, the collared dove has been widely introduced elsewhere in the world. Photo by Charles Lam.

Whatever the eventual division of the family, Streptopelia will almost certainly remain a part of Columbinae, as it is the most closely related genus to Columba. Molecular analysis of fourteen of the sixteen species generally included in Streptopelia by Johnson et al. (2001) identified three main clades in the genus - a large clade containing the majority of species, a clade uniting S. chinensis and S. senegalensis, and a clade containing the Madagascan S. picturata and the pink dove Nesoenas mayeri of Mauritius. This three-part division is also reasonably consistent with morphological and vocal distinctions within the genus. The two smaller clades were in turn sister to each other, but the monophyly of Streptopelia as a whole was not proven; depending on the chosen method of analysis, either Streptopelia was monophyletic (the maximum likelihood results) or the main Streptopelia clade was sister to a clade containing Old World Columba and the two smaller clades (the maximum parsimony results). New World 'Columba' species were the sister clade to Streptopelia plus Old World Columba whatever the method; their recognition as a separate genus Patagioenas was proposed. Johnson et al. (2001) chose to retain Streptopelia in its previous circumscription, but with 'Nesoenas' mayeri also included. In contrast, Cheke (2005) suggested restricting Streptopelia to the main clade and recognising the smaller clades as separate genera Nesoenas (for mayeri and picturata) and Stigmatopelia (for chinensis and senegalensis). Johnson et al.'s (2001) system has the advantage of minimising the number of name changes involved; Cheke's (2005) system is potentially more robust to the uncertain monophyly of the broader Streptopelia; only time will tell which gains the greater popularity.


Bock, W. J. 1994. History and nomenclature of avian family-group names. Bulletin of the American Museum of Natural History 222: 1-281.

Cheke, A. S. 2005. Naming segregates from the ColumbaStreptopelia pigeons following DNA studies on phylogeny. Bulletin of the British Ornithologists' Club 125 (4): 293-295.

Gentry, A., J. Clutton-Brock & C. P. Groves. 2004. The naming of wild animal species and their domestic derivatives. Journal of Archaeological Science 31: 645-651.

ICZN. 2008. Opinion 2215: Streptopelia risoria (Linnaeus, 1758) (Aves, Columbidae): priority maintained. Bulletin of Zoological Nomenclature 65 (4).

Johnson, K. P., S. de Kort, K. Dinwoodey, A. C. Mateman, C. ten Cate, C. M. Lessells & D. H. Clayton. 2001. A molecular phylogeny of the dove genera Streptopelia and Columba. Auk 118 (4): 874-887.

Pereira, S. L., K. P. Johnson, D. H. Clayton & A. J. Baker. 2007. Mitochondrial and nuclear DNA sequences support a Cretaceous origin of Columbiformes and a dispersal-driven radiation in the Paleogene. Systematic Biology 56 (4): 656-672.

Slabbekoorn, H., S. de Kort & C. ten Cate. 1999. Comparative analysis of perch-coo vocalizations in Streptopelia doves. Auk 116 (3): 737-748.

Archamoebae: The Apogee (or Nadir) of Amoebozoan Evolution

Mastigamoeba aspera, the type species of the mastigamoebids. Photo by Josef Brief.

There's just one group of amoebozoans left for me to cover: the Archamoebae. Among Amoebozoa, the Archamoebae are easily distinguishable by one significant feature - they lack mitochondria. Mitochondria are also absent in Breviata (which was initially identified as an archamoeba as a result), but Breviata has double basal bodies attached to the cilium unlike the single basal body of Archamoebae (Walker et al., 2006). Members of the Archamoebae are either freshwater amoeboflagellates or non-ciliate animal endosymbionts. Because the Archamoebae are primarily defined by a character absence some authors have suggested that their monophyly is suspect, but molecular analyses support their recognition. The lack of mitochondria also lead to Archamoebae being one of the four groups of protists (along with the Diplomonadida, Microsporidia and Parabasalia) that were grouped together as the "Archezoa", and suggested to have diverged from other eukaryotes prior to the origin of mitochondria. The archezoan hypothesis began to fall from favour in the latter half of the 1990s as relationships were proposed between various 'archezoans' and specific groups of mitochondriate protists, such as between Archamoebae and other amoebozoans. Putative mitochondrion-derived organelles such as mitosomes and/or hydrogenosomes have now been identified from most Archamoebae (Walker et al., 2001; Gill et al., 2007).

Molecular data supports the division of Archamoebae into two clades, the Mastigamoebida and Pelobiontida (Cavalier-Smith et al., 2004). Production of pseudopodia in Mastigamoebida is eruptive (Walker et al., 2001), which you may recall is not the usual condition for amoebozoans (other than Archamoebae, eruptive pseudopodium is also found in Leptomyxida). Free-living mastigamoebids are ciliate for at least part of their life cycle, and movement is generally by means of the cilium or by gliding rather than by pseudopodium production. Mastigamoebids may or may not be multinucleate, and the cilium is usually connected to the nucleus. Taxonomy of the free-living amoeboflagellate mastigamoebids is in something of a state of flux - three genera have been distinguished, Mastigamoeba, Phreatamoeba and Mastigella, but opinions differ as to whether the latter two should be distinguished from the first. Phreatamoeba balamuthi has been placed as a separate genus because of its more complex life-cycle alternating between amoeboid and amoeboflagellate stages, with the amoeboid stage predominant, but the flagellate stage is otherwise not distinguishable from Mastigamoeba. Mastigella has been distinguished based on the absence of a connection between the cilium and the nucleus, but the presence or absence of such a connection can be difficult to distinguish in taxa where the connection is very fine (Walker et al., 2001). Part of the problem lies in the genus Mastigamoeba itself - Mastigamoeba contains about forty species of which some are very distinct from each other but many (including the type species) are insufficiently studied. When more of the Mastigamoeba species are studied it may lead to the genus' subdivision.

The giant micro-aerobic amoeboid Pelomyxa palustris, with the larger cell nearly three millimetres in length. The flecks of green inside it are endosymbiotic algae. Photo from here.

The Pelobiontida contain three distinct genera, Pelomyxa, Mastigina and Entamoeba, united by molecular data. Mastigina and Pelomyxa are both free-living amoeboflagellates. Mastigina setosa has one or a few nuclei and a single long cilium; however, movement is by pseudopodia while the cilium contributes little if any propulsion. Pelomyxa palustris is a gigantic amoeboid, up to five millimetres long and often with hundreds of nuclei in a single cell. It possesses small cilia, but it almost goes without saying that they do not contribute to moving the cell's massive bulk. Cytoplasmic movement in Pelomyxa has been described as "fountain streaming" - a wave of cytoplasm moves across the dorsal surface of the cell and spills over the front. Like Trichosphaerium, Pelomyxa can reproduce by budding off a piece of the cell with a few nuclei (Hickson, 1909) - indeed, at one point it was thought that Pelomyxa never underwent mitosis, an error that lead to its brief elevation to the status of an independent phylum, Caryoblastea.

Both of the two archamoebaen clades have given rise to non-ciliate lineages - the Endolimacidae (Endolimax and Endamoeba) among mastigamoebids, and Entamoeba among pelobionts. Both of these taxa are animal endosymbionts, living inside the gut of their host (the name Endolimax means "inner slug") - Endolimax and Entamoeba inhabit vertebrates (including humans), while Endamoeba is found in cockroaches (including termites). Endolimacidae are generally innocuous, but a few species of Entamoeba can cause great trouble for their hosts - among humans, E. histolytica causes dysentery, while E. gingivalis lives in the mouth and can cause gum disease.

Endamoeba blattae, an inhabitant of the digestive system of cockroaches. Photo from here.

Even with the downfall of the idea that Archamoebae are among the most archaic of eukaryotes (which kind of makes the name of clade a bit misleading, but we're stuck with it now), the relationships of this group are still interesting. Archamoebae possess a distinct conical arrangement of microtubules at the base of the cilium; in turn, this cone sits on top of the nucleus like a Vietnamese farmer's hat. The presence of a similar structure in many slime moulds lead Cavalier-Smith to unite Archamoebae and Mycetozoa in a clade called Conosa (or Conosea, depending on which paper you're reading and what rank Cavalier-Smith felt like putting it at at the time). Molecular data generally supports placing the two close together, but not always as an exclusive clade - often various examples of the taxa described in the last post muscle their way in. Many of these other amoebozoans, such as Phalansterium and Multicilia, possess similar (but not identical) microtubular cones, and Cavalier-Smith (2009) recently extended the Conosa to include these taxa as well. This extended Conosa is supported by most molecular analyses, but it has to be noted that all of the taxa involved show elevated rates of evolution - Pelomyxa and Trichosphaerium, in particular, show rates going through the roof - and the possibility of long-branch attraction cannot be entirely ruled out. If I may be allowed a somewhat strained analogy, it's a bit like when an election is held in a culturally diverse area between candidates of various backgrounds and both sexes, and all the winning candidates end up belonging to one particular subgroup. It's entirely possible that this was the valid result, and nothing untoward occurred in the ballot-counting process, but still, you can't help wondering.

And with that, I reach the end of the Amoebozoa (at least for now). If you want to look back on the other amoebozoan posts:

Now if only someone would do the same for Heterolobosea...


Cavalier-Smith, T. 2009. Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. Journal of Eukaryotic Microbiology 56 (1): 26-33.

Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40 (1): 21-48.

Gill, E. E., S. Diaz-Triviño, M. J. Barberà, J. D. Silberman, A. Stechmann, D. Gaston, I. Tamas & A. J. Roger. 2007. Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Molecular Microbiology 66 (6): 1306–1320

Hickson, S. J. 1909. The Lobosa. In A Treatise on Zoology pt. 1. Introduction and Protozoa, first fascicle (R. Lankester, ed.) Adam & Charles Black: London.

Walker, G., A. G. B. Simpson, V. Edgcomb, M. L. Sogin & D. J. Patterson. 2001. Ultrastructural identities of Mastigamoeba punctachora, Mastigamoeba simplex and Mastigella commutans and assessment of hypotheses of relatedness of the pelobionts (Protista). European Journal of Protistology 37 (1): 25-49.

Amoebozoan Oddments

Arachnula, a branched marine amoeboid of uncertain affinities. Photo by D. Patterson et al.

If I am to continue with the Cavalier-Smith et al. (2004) classification of Amoebozoa, the next class I reach would be the Variosea. However, Cavalier-Smith et al.'s Variosea was the weakest of the classes they recognised. The characters it was based upon (usually single cilia or centrosomes, no fruiting bodies, non-eruptive pseudopodia) are almost certainly plesiomorphic for Amoebozoa (or possibly the clade of Amoebozoa excluding Breviata), and even the name 'Variosea' was coined to refer to the diverse morphologies the class covered. Molecular studies have not indicated variosean monophyly, though the majority of 'varioseans' may fall into a paraphyletic series below Archamoebae and Mycetozoa. The Smirnov et al. (2005) classification contained no grouping comparative to Variosea: they simply left the 'varioseans' as "Amoebozoa incertae sedis". Still, this is as good a place as any to introduce the 'varioseans', plus a couple of other amoebozoan taxa that don't fall under the aegis of any of the other groupings I've referred to. In no particular order, these are the 'Varipodida', Centramoebida (or Acanthopodida), Stereomyxa, Corallomyxa, Phalansterium, Trichosphaerium and Multicilia.

The name 'Varipodida' was introduced by Cavalier-Smith et al. (2004) for a grouping of the non-ciliate genera Gephyramoeba and Filamoeba (though as it turns out 'Gephyramoeba' was misidentified; the varipodidan has been redescribed as Acramoeba, while true Gephyramoeba is a member of Leptomyxida and hence tubulinean; Smirnov et al., 2008). Subsequent studies have been equivocal about the monophyly of such a grouping. Generally, the two genera are close to the clade containing Archamoebae and Mycetozoa (more on that clade in the next post), either just outside it or just within it. Filamoeba is a flattened, fan-shaped amoeboid which produces extremely slender, spine-like subpseudopodia that look superficially like filose pseudopodia (hence the name). However, unlike true filose pseudopodia as found in Rhizaria, the subpseudopodia of Filamoeba do not function in movement. Acramoeba has branched cells, with the branches producing slender subpseudopodia like those of Filamoeba. It's also worth mentioning Arachnula, which is similar to Acramoeba but larger and multinucleate. Similar slender subpseudopodia are also produced by dictyostelian slime moulds, adding further support to a relationship between Varipodida and Mycetozoa.

Balamuthia mandrillaris. Photo from here.

The Centramoebida include the flattened soil-living amoebae Acanthamoeba and Balamuthia. Acanthamoeba is similar to Filamoeba in producing slender subpseudopodia (there was a picture in this post), but Balamuthia does not. Both genera can be pathogenic to humans, though that is probably not their main mode of life - Acanthamoeba has been connected to eye infections, while both Acanthamoeba and Balamuthia can cause meningitis. The really interesting thing about the centramoebids, however, is that unlike any of the amoebozoans I've covered in the last few posts, they possess a centrosome. The centrosome is an organelle that is involved in controlling the activity of the microtubules that run through the cytoplasm. The centrosome (or, specifically, the centrioles within the centrosome) is also the organelle responsible for the production of cilia. Up until now, I've been looking at non-ciliate amoebozoans, but the common ancestor of the Amoebozoa would have been ciliate and some amoebozoans remain so. Just how many times cilia have been lost in the Amoebozoa is unknown - at least five, probably more (Nikolaev et al., 2006). Centramoebids have lost the cilium and the centrioles, but they still retain the evidence of their former presence in the centrosome.

Corallomyxa, though without a species name I'm not certain whether this is supposed to be true Corallomyxa or the rhizarian Filoreta tenera, originally misidentified as a Corallomyxa. Photo by David Patterson.

A similar centrosome to that of Centramoebida is also found in the marine genera Stereomyxa and Corallomyxa, and the three taxa may form a clade (Cavalier-Smith et al., 2004). Stereomyxa and Corallomyxa have slender branched, reticulate pseudopodia, making them look at first glance a bit like a small plasmodial slime mould (though they differ in lacking fruiting bodies). A recent study suggesting that Corallomyxa, at least, may be rhizarian rather than amoebozoan has turned out to be based on another misidentification (Bass et al., 2009).

Trichosphaerium in the naked phase. Photo by David Patterson.

Trichosphaerium is perhaps the most bizarre of all the amoebozoans - and not merely because of its ability to happily chow down on plastic. Trichosphaerium is a relatively large, multinucleate marine amoeboid that lives enclosed in a membranous test. The test is pierced by numerous openings, and the amoeboid extends its pseudopodia through those openings for feeding and locomotion (this differs from the situation in Pellita because the openings are permanent, rather than each individual pseudopodium forcing its way out through the covering). The life cycle of Trichosphaerium alternates between asexual and sexual generations; in the asexual generation, the test has a covering of sharp spicules, but in the sexual generation it is smooth. Reproduction in the asexual stage is by division, but division is generally unequal - a relatively small piece of cytoplasm containing a few nuclei is pinched off to become a separate cell, and the nuclear membrane does not break down during division. In the sexual generation, asexual division may occur as in the asexual generation while the cell is growing, but when the cell finishes growing it forms a cyst. Within the cyst, the cell divides rapidly so that each individual nucleus is contained within its own individual biciliate cell; when the cyst breaks open, these uninucleate cells fuse to give rise to the next generation (Hickson, 1909). Under crowded conditions, normal multinucleate cells have also been recorded fusing to give rise to gigantic amoeboid cells up to three millimetres in diameter, with over a thousand nuclei, that break apart into more normal multinucleate within the course of a week.

Phalansterium - drawing of a colony and of an individual cell embedded in its matrix. Image by Stuart Hedley & David Patterson.

Phalansterium is another highly unusual amoebozoan, for the simple reason that it is not an amoeboid (Cavalier-Smith et al., 2004). It's not even an amoeboflagellate. At one time, Phalansterium was united with the choanoflagellates, which it resembles in having a collar around the base of its single cilium and by living in colonies; however, in Phalansterium the collar is a single undivided fold while in choanoflagellates it is divided into microvilli, while Phalansterium has only a single centriole at the base of its cilium to choanoflagellates' two. Molecular analysis firmly plonks Phalansterium among the amoebozoans. Cavalier-Smith has made some pretty big calls in relation to unassuming little Phalansterium, claiming it is the closest known organism to the probable ancestral morphology for all eukaryotes. This, however, is based on his assumption that the unikont morphology is ancestral.

Drawing of Multicilia instructa. Image by Won Je Lee.

Finally, Multicilia is a marine amoebozoan with a covering of numerous radially-arranged cilia. Mikrjukov & Mylnikov (1998) found that movement in Multicilia was by irregular, uncoordinated beating of the flagella, causing the cell to roll over the substrate without any obvious organisation into front or back or up or down. Short pseudopodia are extended to capture Multicilia's favoured food - other amoebozoans. Generally cells are roughly globular, but in certain unfavourable conditions large branched cells can develop. Cavalier-Smith et al. (2004) suggested that Multicilia was related to the Flabellinea due to the presence of glycostyles in the cell coat, but Nikolaev et al. (2008) placed it closer to other ciliate amoebozoans.


Bass, D., E. E.-Y. Chao, S. Nikolaev, A. Yabuki, K. Ishida, C. Berney, U. Pakzad, C. Wylezich & T. Cavalier-Smith. 2009. Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160 (1): 75-109.

Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40 (1): 21-48.

Hickson, S. J. 1909. The Lobosa. In A Treatise on Zoology pt. 1. Introduction and Protozoa, first fascicle (R. Lankester, ed.) Adam & Charles Black: London.

Mikrjukov, K. A., & A. P. Mylnikov 1998. The fine structure of a carnivorous multiflagellar protist, Multicilia marina Cienkowski, 1881 (Flagellata incertae sedis). European Journal of Protistology 34: 391-401.

Nikolaev, S. I., C. Berny, N. B. Petrov, A. P. Mylnikov, J. F. Fahrni & J. Pawlowski. 2006. Phylogenetic position of Multicilia marina and the evolution of Amoebozoa. International Journal of Systematic and Evolutionary Microbiology 56: 1449-1458.

Smirnov, A. V., E. S. Nassonova & T. Cavalier-Smith. 2008. Correct identification of species makes the amoebozoan rRNA tree congruent with morphology for the order Leptomyxida Page 1987; with description of Acramoeba dendroida n. g., n. sp., originally misidentified as ‘Gephyramoeba sp.’ European Journal of Protistology 44 (1): 35-44.

Smirnov, A. V., E. S. Nassonova, E. Chao & T. Cavalier-Smith. 2007. Phylogeny, evolution, and taxonomy of vannellid amoebae. Protist 158 (3): 295-324.

Building a Home of Your Own (Taxon of the Week: Hydroides)

Close-up of the front end of the tubeworm Hydroides elegans, showing the double-level operculum. Photo by John Lewis.

This week's highlight taxon is the worm genus Hydroides. Hydroides unites about eighty species of the family Serpulidae, the tubeworms, an easily-found component of many a beach all over the world. Serpulids (previously commented on here) are a distinctive group of annelid worms that secrete themselves a tubular shell of calcium carbonate in which they live permanently attached to a rock or some other substrate (not uncommonly, that "other substrate" will be another tubeworm, leading to the production of tangled masses of worm tubes). Many authors have divided serpulids between two families, Serpulidae proper and Spirorbidae, but phylogenetic studies place spirorbids as a derived subgroup of Serpulidae rather than their sister group (Kupriyanova et al., 2006; Lehrke et al., 2006). Hydroides is not a spirorbid, so it remains in Serpulidae whatever the preferred arrangement.

With more than eighty species, Hydroides is a reasonably large assemblage, and it is distributed worldwide. Among the more distinctive features of the genus is the division of the spinose operculum into two tiers, a lower (rather daisy-like, in my opinion) ring called the funnel and an upper ring of spines called the verticil. The features and arrangement of the verticil spines are often the main distinguishing characters between species, but this can be complicated somewhat by changes in spine morphology over the course of growth and regeneration (ten Hove & Ben-Eliahu, 2005). It is also notable that at least one Caribbean species, Hydroides spongicola, has been recorded as showing a tendency towards reduction of the operculum; this species lives in close association with the highly toxic touch-me-not sponge (Neofibularia nolitangere) and presumably the host sponge's irritating spicules offer all the protection the tubeworm needs (Lehrke et al., 2006).

The first species of Hydroides to be described was H. norvegica (now Hydroides norvegicus to match the gender of the genus) in 1768 by Johan Ernst Gunnerus, Bishop of Trondhjem*. An English translation of Gunnerus' original description was published by Moen (2006); as shown in the reproduction above from Moen (2006) of the first few lines, the original is not among the easiest of reads. Interestingly enough, Gunnerus bestowed a different name on the animal ("Hydroides norvegica") from the tube that it lived in ("Serpula norvegica") - I suspect that this may represent a different philosophy from the present about how to deal with animals versus their products, as opposed to any doubt about whether the one had produced the other. In a letter to Linnaeus (or von Linné as he'd become by then), Gunnerus also described his doubt about just what type of animal it was he'd described - a hydrozoan, or possibly a sea cucumber? It seems that its sessile lifestyle had quite put him off the idea of it being a worm**.

*Among other animals described by Gunnerus are the basking shark and Lineus longissimus, the world's longest ribbon worm and possibly the longest of all living animals.

**Remember, Gunnerus and Linnaeus were both working in a largely non-evolutionary paradigm. As such, their classifications were not intended to reflect an organism's "affinities" in the sense that we'd understand them, but rather to reflect how their overall features compared to other animals.

Congregation of Hydroides ezoensis on the side of a ship. Image from Science in Salamanca.

These days, Hydroides species are among the most intensely studied of all marine annelids. The motives for this interest are primarily economical - not surprisingly, Hydroides have often earned the ire of humans through their penchant for attaching themselves to the humans' nice clean boats and jetties. A number of Hydroides species have been transported and established outside their native ranges by human agency - probably in ballast water for the most part, though H. ezoensis was transported from Japan to France on the shells of oysters imported to stock oyster farms (Thorp et al., 1987). With this economic focus, it is not surprising that the majority of studies appear to have been on factors affecting larval development and settlement. One interesting point is that Hydroides larvae are far more likely to settle somewhere already inhabited by tubeworms than on a completely fresh surface (Scheltema et al., 1981), a common pattern among sessile organisms that do not reproduce by budding. After all, there's safety in numbers.


Hove, H. A. ten, & M. N. Ben-Eliahu. 2005. On the identity of Hydroides priscus Pillai 1971 – taxonomic confusion due to ontogeny in some serpulid genera (Annelida: Polychaeta: Serpulidae). Senckenbergiana Biologica 85 (2): 127-145.

Kupriyanova, E. K., T. A. Macdonald & G. W. Rouse. 2006. Phylogenetic relationships within Serpulidae (Sabellida, Annelida) inferred from molecular and morphological data. Zoologica Scripta 35: 421-439.

Lehrke, J., H. A. ten Hove, T. A. Macdonald, T. Bartolomaeus & C. Bleidorn. 2006. Phylogenetic relationships of Serpulidae (Annelida: Polychaeta) based on 18S rDNA sequence data, and implications for opercular evolution. Organisms Diversity & Evolution 7 (3): 195-206.

Moen, T. L. 2006. A translation of Bishop Gunnerus’ description of the species Hydroides norvegicus with comments on his Serpula triqvetra. Scientia Marina 70S3: 112-123.

Scheltema, R. S., I. P. Williams, M. A. Shaw & C. Loudon. 1981. Gregarious settlement by the larvae of Hydroides dianthus (Polychaeta: Serpulidae). Marine Ecology Progress Series 5: 69-74.

Thorp, C. H., S. Pyne & S. A. West. 1987. Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. Journal of Natural History 21 (4): 863-877.

Discosea: Keeping a Low Profile

Various views of Vannella devonica, a representative of the Vannellidae. Photos by A. Smirnov.

Having covered the Tubulinea, it's time to move on to some of the less familiar Amoebozoa. At this point, however, the competing classifications of Cavalier-Smith et al. (2004) and Smirnov et al. (2005) begin to part ways - at least superficially. Cavalier-Smith et al.'s class Discosea is roughly comparable to Smirnov et al.'s class Flabellinea, but the two are not identical. Rather, Flabellinea is a subgroup of Discosea, the latter also including a few taxa that Smirnov et al. listed as Amoebozoa incertae sedis. As such, I'll use Discosea for the larger group and Flabellinea for the smaller group. Monophyly of the Flabellinea has been recovered in a number of analyses (including both the studies just cited), monophyly of the Discosea is more doubtful. Kudryavtsev et al. (2005) found a monophyletic Discosea, but all other molecular analyses including non-flabellinean 'Discosea' show 'Discosea' as polyphyletic. The morphological characteristics of Discosea cited by Cavalier-Smith et al. (2004) ("highly flattened, often discoid amoebae that move slowly by a leading lamellipodium", and a tendency to secrete some sort of thickened protective covering or membrane) are not unique to members of the group. Nor is the other feature cited by Smirnov et al. (2005) as distinguishing Flabellinea from Tubulinea, that cytoplasmic flow in pseudopodia does not form a single central axis. Discoseans produce only a single anterior pseupodium when moving (which may or may not produce subpseudopodia), and no discosean has an adhesive uroid.

As well as the Flabellinea, Cavalier-Smith et al.'s Discosea included the Cochliopodiidae and Thecamoebida. Later analysis (Kudryavtsev et al., 2005) suggested the polyphyly of Thecamoebida, and the discosean component was restricted to the genus Dermamoeba (nevertheless, because Dermamoeba and Thecamoeba are ultrastructurally similar, I may as well cover both in this post). Subsequent studies have continued to indicate the polyphyly of 'Thecamoebida', but Pawlowski (2008) refers to unpublished data that might restore monophyly to the group. Cavalier-Smith et al. (2004) also suggested that the multiciliate Multicilia was a discosean, but Nikolaev et al. (2006) have since shown otherwise (Multicilia will feature in the next Amoebozoa post; with its removal, Discosea becomes an entirely non-ciliate group). Finally, though its authors refrained from saying so, it seems entirely possible that, if the Discosea should be monophyletic, the recently described distinctive genus Pellita (Smirnov & Kudryavtsev, 2005) may be discosean.

Thecamoeba striata. I suspect that the front of the cell is towards the lower left. Photo by Keisotyo.

A general characteristic of Amoebozoa that I have not yet had cause to mention is the presence of a glycocalyx, a protective covering of proteins and polysaccharides that lies outside but is connected to the membrane of the cell. The nature of the glycocalyx has often been used in differentiating amoebozoan taxa in the past, but recent studies suggest that it may be more variable than previously thought (e.g. Smirnov et al., 2007), so glycocalyx-based features should probably be treated with caution. Both 'Thecamoebida' and Flabellinea have particularly well-developed glycocalyces. In 'Thecamoebida', the glycocalyx is amorphous (probably the ancestral condition for Amoebozoa) but extremely thick. Thecamoebids on the move are generally oval or oblong in shape without anterior subpseudopodia. Thecamoeba has the dorsal surface of the cell shaped into longitudinal folds or wrinkles, while Dermamoeba has no dorsal folds or wrinkles (Smirnov & Goodkov, 1999).

Paramoeba aestuarina. The large dark spot is the "parasome" (or the endosymbiont Perkinsela amoebae, however you want to put it). Image from here.

In Flabellinea, the glycocalyx is usually differentiated into a covering of column-like glycostyles, though a number of flabellineans have lost the glycostyle coat (Smirnov et al., 2007). Flabellinea are divided into three families - Vanellidae, Paramoebidae and Vexilliferidae, with the latter two more closely related to each other than to Vanellidae. The basic form of Flabellinea is broad and fan-shaped; Vanellidae have a smooth leading edge without subpseudopodia, while Paramoebidae and Vexilliferidae produce subpseudopodia - short and blunt in Paramoebidae, long and slender in Vexilliferidae. Paramoebids were also distinguished in the past by their possession of a distinctive organelle known as the parasome. However, this distinction has been reworked in recent years - not because of doubts about the reality of the parasome, but because the parasome is now regarded as a separate organism in its own right, an endosymbiont rather than an organelle of paramoebids.

Diagram of Pellita, showing how the subpseudopodia extend through the thick cell coat. Figure from Smirnov & Kudryavtsev (2005).

The recently discovered Pellita (Smirnov & Kudryavtsev, 2005) resembles Flabellinea in possessing a cell covering of glycostyles. This covering is particularly thick in Pellita, and almost resembles a test rather than a coat. So thick is Pellita's covering that the normal means of amoebozoan movement and feeding via the projection of pseudopodia are not possible for it. Instead, Pellita produces short subpseudopodia with a covering of basic cell membrane only that muscle their way between the glycostyles until they project outside the coat. These subpseudopodia engulf individual bacteria if feeding, while for movement subpseudopodia produced near the leading edge of the cell adhere to the substrate and the cell rolls forward over the top of them.

Cochliopodium. Photos from here.

Finally, the Cochliopodiidae also possess an external covering, but in their case it is a rigid coat that is entirely separate from the cell membrane. In the genus Cochliopodium the coat consists of carbohydrate scales, while in the genera Gocevia and Paragocevia the coat is filamentous. The cochliopodiid coat differs from the test of Arcellinida in that it is restricted to the dorsal surface of the cell, not surrounding it as in arcellinidans. Also, the coat is divided between the daughter cells when the cochliopodiid divides; in Arcellinida, one daughter cell keeps the test while the other has to make an entire new test from scratch.


Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40 (1): 21-48.

Kudryavtsev, A., D. Bernhard, M. Schlegel, E. E-Y. Chao & T. Cavalier-Smith. 2005. 18S ribosomal RNA gene sequences of Cochliopodium (Himatismenida) and the phylogeny of Amoebozoa. Protist 156: 215-224.

Nikolaev, S. I., C. Berny, N. B. Petrov, A. P. Mylnikov, J. F. Fahrni & J. Pawlowski. 2006. Phylogenetic position of Multicilia marina and the evolution of Amoebozoa. International Journal of Systematic and Evolutionary Microbiology 56: 1449-1458.

Pawlowski, J. 2008. The twilight of Sarcodina: a molecular perspective on the polyphyletic origin of amoeboid protists. Protistology 5 (4): 281-302.

Smirnov, A. V., & A. V. Goodkov. 1999. An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1: 20-29.

Smirnov, A. V., & A. A. Kudryavtsev. 2005. Pellitidae n. fam. (Lobosea, Gymnamoebia) – a new family, accommodating two amoebae with an unusual cell coat and an original mode of locomotion, Pellita catalonica n.g., n.sp. and Pellita digitata comb. nov. European Journal of Protistology 41 (4): 257-267.

Smirnov, A., E. Nassonova, C. Berney, J. Fahrni, I. Bolivar & J. Pawlowski. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129-142.

Smirnov, A. V., E. S. Nassonova, E. Chao & T. Cavalier-Smith. 2007. Phylogeny, evolution, and taxonomy of vannellid amoebae. Protist 158 (3): 295-324.

Tubulinea: The Paragons of Amoeboids

The basal tubulinean Echinamoeba. If you look very closely at the lower end of the cell, you can see the filaments of the adhesive uroid. Photo by David Patterson et al.

Due to popular demand (does two count as popular?), I'm continuing with the Amoebozoa series (previous installments are here and here). The two major classifications of Amoebozoa that have been published in recent years are those of Cavalier-Smith et al. (2004) and Smirnov et al. (2005). While at first glance the two systems appear quite different, there are few real significant differences between them. Mostly it's a matter of different names being used for similar concepts, plus the Cavalier-Smith et al. classification assigns positions to a number of taxa that the more conservative Smirnov et al. classification is content to list as Amoebozoa incertae sedis. The Cavalier-Smith et al. classification divides amoebozoans between seven 'classes', which offers a good basis for dividing my posts. One of Cavalier-Smith et al.'s classes currently includes a single species, the strange (and not necessarily amoebozoan) Breviata anathema, which has previously been covered here and here, while the two classes of their infraphylum Mycetozoa (slime moulds) include the first three entries for this post here. So that leaves four classes that I haven't yet covered in detail. In the coming posts, I'll start with the Tubulinea, move to the Discosea, waft through the 'Variosea' and finish with the Archamoebae. And if that seems like a lot to you, just be glad I didn't choose to do my amoeboid series on Foraminifera - we could have been here well into the next century.

The "Tubulinea" of Smirnov et al. (2005) are the same grouping as the "Lobosea" of Cavalier-Smith et al. (2004). I prefer to use the name Tubulinea because Lobosea has been used in the past for a much larger grouping, effectively all amoebozoans except Mycetozoa and (sometimes) Archamoebae. Also, the name Tubulinea refers to one of the characteristic features of this group, the production of tubular rather than flattened pseudopodia, with cytoplasmic flow within the pseudopodia or entire cell along a single axis. All Tubulinea lack cilia at all stages of the life cycle. The Tubulinea include the Tubulinida (Amoeboidea of Cavalier-Smith et al.), Arcellinida, Copromyxidae, Leptomyxida and Echinamoeba, and both the papers cited above produced identical phylogenies for this class.

Leptomyxa, type genus of the Leptomyxida. Note the branched morphology. Don't ask me to tell you which way this one's going - I think that might be the uroid towards the bottom right, but I'm not sure. Photo by David Patterson et al.

Echinamoeba forms the basalmost clade within the Tubulinea, together with the species 'Hartmannella' vermiformis (erroneous comments on the relationships of the family Hartmannellidae in Cavalier-Smith et al., 2004, are due to the use of H. vermiformis to represent Hartmannella; it wasn't until later that Smirnov et al., 2005, showed that H. vermiformis is not closely related to other Hartmannella species. The normal cell shape of Echinamoeba is "acanthopodian" - flattened with short, spinelike subpseudopodia (Smirnov & Goodkov, 1999); it only produces a more typically tubulinean cylindrical, monopodial form under particular conditions. The form it takes in these conditions is one produced by many amoeboids called the 'limax' form. Limax is a genus of slugs, and a microscopic slug is exactly what this form looks like. 'Hartmannella' vermiformis, on the other hand, is habitually worm-like, and has gained a certain notoriety as an unwitting vector for bacteria causing respiratory diseases in humans, particularly Legionnaire's disease (Brieland et al., 1997).

The Leptomyxida are the next group to branch off. The four genera of leptomyxidans - Leptomyxa, Rhizamoeba, Flabellula and Paraflabellula - resemble Echinamoeba by normally being flattened, and only adopting a tubular limax-like form occasionally. The normal form of Leptomyxa is reticulate, with a anastomosing net of pseudopodia. In the other three genera, the uroid (the trailing end of the moving cell) is adhesive, so when the cell is moving the posterior end is drawn out into smeared streaks. Rhizamoeba is monopodial, while the other two genera are fan-shaped. Paraflabellula produces short subpseudopodia from the anterior edge of the cell, Flabellula doesn't.

The fruiting body of Copromyxa arborescens, which grows up to 2.5 mm in height. Figure from Nesom & Olive (1972).

The Copromyxidae were placed by Cavalier-Smith et al. (2004) among the Tubulinea on the basis of their morphology (but were not represented in the molecular analysis), but were not even mentioned by Smirnov et al. (2005). Copromyxids include two little-studied genera, Copromyxa and Copromyxella. Cavalier-Smith et al. suggested that they are closer to Arcellinida and Tubulinida than other Tubulinea as these three groups are habitually rather than only intermittently tubular. Copromyxids differ from other Tubulinea in having a slime-mould type life cycle (I overlooked them in my earlier slime mould post). Life for copromyxids really is a pile of crap - their chosen habitat is animal dung. Fruiting bodies are produced by previously separate cells aggregating together to form a mound. Newly-arriving cells clamber over their confederates to reach the top of the pile, and the eventual result is a small, vaguely tree-like fruiting body (Bonner, 1982). Copromyxids are very similar in appearance to the non-amoebozoan acrasid slime moulds, and many earlier references combine the two.

The Arcellinida are the most speciose subgroup of Tubulinea (at least, as far as we know). Arcellinida are the testate Amoebozoa - they possess are hardened test of either secreted proteinaceous material or agglutinated mineral grains. The test is roughly vase-shaped, with a single opening through which the organism extends its pseudopodia. Phylogenetic studies (Nikolaev et al., 2005) confirm that the testate Amoebozoa form a monophyletic group (which, as I noted earlier, forms an interesting contrast to the polyphyletic testate Rhizaria), but the same cannot be said for proteinaceous- versus agglutinated-test formers, with lineages apparently switching between the two a number of times.

Nebela tubulosa, a member of the Arcellinida. Photo by Antonio Guillen.

Finally, the Tubulinida includes Amoeba itself and its nearest and dearest (such as Chaos, Saccamoeba and true Hartmannella). Tubulinida differ from Echinamoeba and Leptomyxida in being permanently tubular, never flattened. The cell may move limax-wise as a single pseudopodium (Saccamoeba, Hartmannella, sometimes Amoeba) or may form multiple pseudopodia (Chaos, other times Amoeba). Both Cavalier-Smith et al. and Smirnov et al. placed Chaos and Amoeba closest to one another, and indeed phylogenetically mixed together. As the only difference between the two seems to be the number of nuclei (one in Amoeba, more in Chaos) it would perhaps not be surprising if one or the other, or both, turned out to be polyphyletic.

Finally, I'd like to end this post on a bit of speculation. In the first Amoebozoa post, I described the ridiculously large genome of Tubulinida species (thanks to commentor George X for pointing out that the species I referred to as Amoeba dubia is now known as Polychaos dubium). I tried to find if any studies had been done on the detailed genetic structure of these species, to see if there was any clue as to just why Tubulinida have such enormous genomes, but I couldn't find any. Indeed, when searching on Amoeba in Google Scholar, I was struck by the dates shown for most of the results - a significant proportion dating back to the period from the 1940s to the 1960s. It looks like Amoeba proteus, so popular as a model organism in the early days of cell biology due to its large size making it easy to observe and manipulate, may have since fallen in popularity. I can guess at some reasons why that might be - I get the impression that Amoeba's rarity makes it tricky to find, that it is difficult to maintain in culture once you do find it, and I wonder if, in a time when electron microscopy has become almost routine, Amoeba is large enough that its size has become a positive disadvantage rather than advantage.

In the absence of much information about Amoeba's genome beyond its size, speculation becomes ill-founded. The large size of the genome doesn't necessarily indicate a proportionally large number of genes - it could be that Amoeba is carrying a particularly heavy load of non-coding DNA. Also, the previously-mentioned cyclic nature of the Amoeba genome, with the amount of DNA increasing and decreasing over the course of the division cycle by a factor of nearly three (Parfrey et al., 1998), suggests that Amoeba proteus is at least hexaploid. Again, it might not be - perhaps instead of the entire genome being replicated three times, a smaller number of chromosomes are replicated many times (as we know happens with such things as B chromosomes in animals). But, with all those caveats, I still can't help wondering if the cyclic Amoeba genome is related to its unusual success as an asexual organism. Let us assume that the entire genome is replicated in the cell cycle, and that it is random which of the resulting replicate chromosomes gets retained and which disposed of prior to division. The result would be that the effective mutation rate of Amoeba would probably be noticeably higher than in organisms with more straightforward genetic cycles. Could this be what has allowed Amoeba to survive for so long seemingly without the benefit of recombination?


Bonner, J. T. 1982. Evolutionary strategies and developmental constraints in the cellular slime molds. American Naturalist 119 (4): 530-552.

Brieland, J. K., J. C. Fantone, D. G. Remick, M. LeGendre, M. McClain & N. C. Engleberg. 1997. The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire's disease. Infection and Immunity 65 (12): 5330-5333.

Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40 (1): 21-48.

Nesom, M., & L. S. Olive. 1972. Copromyxa arborescens, a new cellular slime mold. Mycologia 64 (6): 1359-1362.

Nikolaev, S. I., E. A. D. Mitchell, N. B. Petrov, C. Berney, J. Fahrni & J. Pawlowski. 2005. The testate lobose amoebae (order Arcellinida Kent, 1880) finally find their home within Amoebozoa. Protist 156: 191-202.

Parfrey, L. W., D. J. G. Lahr & L. A. Katz. 2008. The dynamic nature of eukaryotic genomes. Molecular Biology and Evolution 25 (4): 787-794.

Smirnov, A. V., & A. V. Goodkov. 1999. An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1: 20-29.

Smirnov, A., E. Nassonova, C. Berney, J. Fahrni, I. Bolivar & J. Pawlowski. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129-142.

There's Something on Your Back (Taxon of the Week: Prioninae)

The Palo Verde borer, Derobrachus hovorei, a member of the Prioninae from North America. Photo by Alex Wild.

A brief respite from Amoebozoa to present the new Taxon of the Week, the beetle subfamily Prioninae.

The Prioninae are a subgroup of the Cerambycidae, the longicorn beetles. The common name refers to the elongate, back-swept antennae that are a feature of most members of this family. Cerambycidae are a simply huge family - over 20,000 species have been described, of which about 700 belong to the Prioninae (Bílý & Mehl, 1989). The most familiar longicorns are large beetles, but longicorns come in all sizes from the very large to the very small. Larvae of most longicorns live in and feed on dead wood (females may oviposit in live wood; the process of oviposition kills off the oviposition site and rot spreads through the tree allowing the larva to feed, making some of these species serious horticultural pests), and can take as long as two years to develop. Adults, in contrast, are relatively short-lived.

The most obvious feature distinguishing Prioninae from other longicorns is the presence of a sharp lateral keel on either side of the pronotum (the anterior shield of the thorax). Prioninae are large longicorns, dark in colour and crepuscular or nocturnal in habits. Adult Prioninae probably don't feed (Willemstein, 1987), but they nevertheless possess impressive jaws with which the males engage in vicious battles to win females. The larvae are generally polyphagous (that is, they're not particularly picky over exactly what type of wood they're eating), though some exceptions occur, and oviposition by the females is usually little more complicated than pushing the eggs into already rotting wood (Bílý & Mehl, 1989).

Witchety grubs, dressed for the table. Photo by David Hancock.

Among the better-known members of the Prioninae are the witchety grubs of the genus Cnemoplites which were eaten by Australian Aborigines (Lawrence & Britton, 1991) - still are, in fact, by those who have the nous to know where to find them (I've tried them on one occasion, cooked in wood ash. To be honest, I thought they tasted a bit like snot, but the woman who had brought them assured us that they were wonderful when spread across bread in lieu of butter). The most notorious of all Prioninae, however, is probably the rather self-explanatorily named Titanus giganteus, the Titan beetle of northern Amazonia. At twenty centimetres in length, Titanus is one of the largest of all insects - technically, the Goliath beetles of the scarabaeid genus Goliathus are larger, but for some reason - probably their more compact build and less prominent mandibles - Goliath beetles don't seem quite so bowel-openingly intimidating as Titanus. Titan beetles are a rare sight even within their native range (outside Amazonia, they have only ever been recorded as specialised parasites on time-travelling comediennes) which may just be all for the best; I suspect that even an avid entomophile like myself would be hard-pressed not to go into a blind panic and start screaming like a little girl if one of those suckers started crawling up my arm.

Titanus giganteus, the largest of the Prioninae. Photo by Bruno Ramos.

David Attenborough, who is seemingly a braver man than I, did handle a specimen of Titanus giganteus on an episode of Life in the Undergrowth. In that episode, Attenborough commented on the point that the larval stage of Titanus has not yet been conclusively identified. It might seem unusual that something as doubtlessly impressive as a Titanus grub would be should go unnoticed, but when you consider the concealed habitat of the larvae, the short lives of the adults, and the extreme difficulty of identifying a holometabolous larva with its corresponding adult, this situation becomes much less surprising. The words of Francis Pascoe, commenting in 1866 on a collection of longicorns from Penang in Malaysia, are just as appropriate today as they were 140 years ago:

If we consider that the Longicorns in their perfect [i.e. adult] state are generally short-lived, and that a great majority of the species frequent particular plants or families of plants, so that only where these plants occur can we expect to find the insects, it will be readily understood how this limited range and brief existence make it almost impossible for any collector to obtain more than a portion of those that inhabit even a moderately extensive district. And thus it is that sometimes perhaps half the species of a large collection are represented each by one or two individuals only. The number of species, therefore, and the many superb novelties which Mr. Lamb has had the good fortune to capture, whilst it excites our imagination, shows us how much more might be expected if all those rich tropical lands were as thoroughly worked by entomologists as Europe has been.


Bílý, S., & O. Mehl. 1989. Longhorn beetles (Coleoptera, Cerambycidae) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica 22. E. J. Brill.

Lawrence, J. F., & E. B. Britton. 1991. Coleoptera. In The Insects of Australia vol. II (CSIRO, ed.) pp. 543-683. Melbourne University Press.

Pascoe, F. P. 1866. Catalogue of longicorn Coleoptera collected in the island of Penang by James Lamb, Esq. Part I. Proceedings of the Zoological Society of London 1866: 222-267.

Willemstein, S. C. 1987. An Ecological Basis for Pollination Ecology. E. J. Brill.

Amoebozoan Classification: Putting the Formless in Formation

Chaos carolinense, the species generally regarded today as the main exemplar of the genus Chaos (see the note below). In case you were wondering, this individual is moving towards the right. Photo by David Patterson.

In my last post, I described some of the oddities of the well-known micro-organism Amoeba. In this post, I'll expand the field of view to look more generally at the clade of Amoebozoa. Study of amoeboids has certainly been going on for a long time - an amoeboid was among the few micro-organisms listed by Linnaeus (1758), under the name of Volvox chaos*. But how, you may be wondering, does one go about characterising a shapeless blob? And how does one distinguish one type of shapeless blob from another?

*Later raised by Linnaeus to the status of a separate genus, Chaos. The name Chaos is still in use for a genus very closely related to Amoeba (the main difference is that Chaos is multinucleate, while Amoeba has a single nucleus) but it pays not to look to carefully at the taxonomy. Debate about the identity of the original Volvox chaos raged down the years - whether it was the modern Chaos, the modern Amoeba, or something else entirely - but the debate was largely futile, because the original description cited by Linnaeus illustrates little more than a shapeless blob with a few dots over it. Many authors included the modern 'Chaos' in the genus Pelomyxa, another large multinucleate amoeboid, but Pelomyxa is an entirely different beast. King & Jahn's (1948) argument for recognition of the three genera Amoeba, Pelomyxa and Chaos with those names is in accord with the modern usage, but has the air more of arbitrary pragmatism rather than adherence to priority - the genus that is now Chaos needed a name, and the name Chaos was going begging. The modern usage is now well-established, and it wouldn't really benefit anyone to go stirring things up now.

If you are wondering exactly that, then I'm sorry to point out to you that you're under something of a misunderstanding about the nature of cellular structure. Not that I blame you, because it's an easy enough misunderstanding to develop. Most basic descriptions of intra-cellular structure might suggest that the interior of a cell is basically liquid (or at most jelly-like) with the nucleus and other organelles freely floating about like so many chunks of carrots and peas in a vegetable soup. But while the cytoplasm is fluid, it's not water. It's a complex mixture of all sorts of molecules - actin filaments, microtubules, etc. - almost more like an enormous bowl of noodles than a broth. It is the interactions between these molecules that give a cell its shape, and also that make it move. The movement and shape-changes of an amoeboid are not random, but follow a pattern. And different types of amoeboid will move according to a different pattern. The form and manner that the amoeboid adopts while moving is generally one of the first things to observe in its identification.

Jahn et al. (1974) divided amoeboid micro-organisms into two classes based on the mode of pseudopodium formation. In one class (as shown in the figure from Jahn et al., 1974, above), the cytoplasm was liquified and pushed forward by contraction, re-coagulating at the front of the resulting broad, lobose pseudopodium. In the second class (shown in the figure below), long filamentous pseudopodia were extended with each side of the pseudopodium moving against the other in an opposite direction.

The distinction between lobose and filose amoeboids has been reinforced with further study, though as it turns out both modes have evolved multiple times (filose pseudopodia more often than lobose pseudopodia). Filose pseudopodia are found among such organisms as the Rhizaria (including foraminifers and radiolarians), while Amoebozoa are characterised by lobose pseudopodia (in those amoebozoans that don't produce distinct pseudopodia, the entire cell moves in this way). Lobose pseudopodia are also found among the Heterolobosea, another group of micro-organisms not closely related to Amoebozoa (heteroloboseans include Naegleria, the causative agent for amoebic meningitis, and acrasid slime moulds). Nevertheless, pseudopodium formation differs between the two in that in amoebozoans, movement is smooth and continuous, while heteroloboseans produce pseudopodia eruptively, cycling between periods of extension and periods of "resting" (heteroloboseans also have a distinct mitochondrial structure from amoebozoans).

Acanthamoeba, a common amoebozoan in soil and fresh water, occasionally causing eye infections in humans. Acanthamoeba produce distinctive short, narrow subpseudopodia from the single flattened cell-wide pseudopodium, as seen in this photo by David Patterson.

Among amoebozoans except testate forms, archamoebae and slime moulds, Smirnov & Goodkov (1999) recognised nineteen "morphotypes" distinguished by their mode of movement - whether the amoeboid extends multiple pseudopodia, or moves as a single unit; the form of the uroid (the posterior end of the cell while the amoeboid is moving); whether the surface of the cell is ridged or smooth; and other such details. Though Smirnov & Goodkov (1999) explicitly established their morphotype distinctions as identification characters only, without necessarily indicating higher classification, molecular phylogenetic studies have indicated a rough (but not exact) correlation between locomotive mode and phylogeny (Smirnov et al., 2005). For instance, Tubulinea, the class of amoebozoans including Amoeba and Chaos, generally produce tubular or subcylindrical pseudopodia with cytoplasm streaming down a distinct single central axis. Members of another class, Flabellinea, have flattened pseudopodia without a single central axis.

Vannella simplex, a member of the Flabellinea. Note the single broad flat fan-shaped pseudopodium. Photo from here.

Not everything is movement, of course. Other features distinguishing amoebozoans include the texture and ornamentation (if any) of the outer cell surface; the shape, distribution and number of the nucleus/nuclei and other organelles; and the presence and nature of a protective test (interestingly, while the testate filose amoeboids do not appear to form a monophyletic group among the Rhizaria, the testate lobose amoebae do seem to be monophyletic among the Amoebozoa - Nikolaev et al., 2005). There is a good detailed online guide at Alexey Smirnov's website (and a hat-tip to Psi Wavefunction for pointing the site out to me). A number of the higher taxa among the Amoebozoa have become reasonably robust in the last few years - if you're not too completely sick of amoeboids, I may introduce you to a few over the next few posts.


Jahn, T. L., E. C. Bovee & D. L. Griffith. 1974. Taxonomy and evolution of the Sarcodina: a reclassification. Taxon 23 (4): 483-496.

King, R. L., & T. L. Jahn. 1948. Concerning the genera of amebas. Science 107: 293-294.

Nikolaev, S. I., E. A. D. Mitchell, N. B. Petrov, C. Berney, J. Fahrni & J. Pawlowski. 2005. The testate lobose amoebae (order Arcellinida Kent, 1880) finally find their home within Amoebozoa. Protist 156: 191-202.

Smirnov, A. V., & A. V. Goodkov. 1999. An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1: 20-29.

Smirnov, A., E. Nassonova, C. Berney, J. Fahrni, I. Bolivar & J. Pawlowski. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129-142.

Amoeba: Much Wierder than You Think

Amoeba proteus extending pseudopodia to feed on a hapless ciliate. Note how the pseudopodia completely surround the ciliate, cutting off any escape, before they close in on it. A fantastic photo by Wim van Egmond - you owe it to yourself to visit that link.

I have been challenged (or at least, I think I have been challenged) to write some posts on amoebozoans, the clade of eukaryotes that includes such organisms as Amoeba and most slime moulds. As amoebozoans are unequivocally neat organisms, I'm happy to take up the challenge, but I thought Id start by focusing on the most famous amoebozoan genus of all, Amoeba itself. There are about five or so species of Amoeba (at least that I'm aware of), but most of what I'm going to say in this post applies equally to all of them. I think I'm safe in claiming that Amoeba is not just the most famous amoebozoan, it's also the most famous of all unicellular eukaryotes. Almost all general biology textbooks will include two examples of 'protists', and one of them will always be Amoeba (the other will be either Euglena or Paramecium). The funny thing about this ubiquity of the Amoeba exemplar, however, is that as unicellular protists go, Amoeba is actually (a) apparently not that common, and (b) seriously wierd*.

*Euglena and Paramecium aren't that typical either.

What makes Amoeba so odd? For a start, Amoeba is amoeboid* (kind of by definition, really). This might not seem so unusual at a glance (many micro-organisms are amoeboid), but the thing is that Amoeba is always amoeboid. It never possesses cilia. Many (if not most) other amoeboid eukaryotes transform into amoeboflagellates or flagellates for at least part of their life-cycle, or possess flagellated gametes, while the majority of unicellular eukaryotes are permanently flagellated**. Even among amoebozoans, cilia are not that unusual; they're still present in Breviata, Multicilia, Phalansterium, Mastigamoebidae, Pelomyxa and many Mycetozoa, though cilia have been entirely lost among amoebozoans at least nine times (Cavalier-Smith et al., 2004).

*Simply for the sake of avoiding confusion, I prefer to avoid the common use of the name "amoeba" to refer to any organism with an Amoeba-like morphology.

**A brief explanation about the terms "cilium" and "flagellum". Originally, the term "cilium" was used for small hair-like locomotory structures, usually present in large numbers, while "flagellum" referred to larger whip-like structures of which a cell would usually only have one or a few. As our knowledge of unicellular diversity broadened, the boundary between the two became increasingly blurred, and fundamentally they're all the same structure. On the other hand, "flagella" in bacteria, though superficially resembling flagella in eukaryotes, are structurally very different (eukaryote flagella are organelles formed of membrane-bound microtubules, while bacterial flagella are formed of a single protein strand). As a result, recent authors have tended to restrict the term "flagellum" to bacteria, and expand the term "cilium" to cover all eukaryote locomotory structures (a replacement term "undulipodium" never caught on [thankfully]). However, terms such as "flagellate" are still pretty well entrenched in their old sense.

Amoeba 'radiosa', photo by David Patterson & Aimlee Laderman. Despite the use of the name, there is not really such a species as 'Amoeba radiosa'. Rather, the name is used to indicate amoebae that have become detached from the substrate and are free-floating in the water column, where they abandon their usual flattened form and adopt a form with slender pseudopodia radiating from a spherical centre. Once they come back into contact with a solid surface, they will return to their normal morphology.

The second unusual thing about Amoeba (which is perhaps not unconnected to the first thing) is its reproductive habits. Most people are aware that Amoeba reproduce by division. That happens to be the only way that Amoeba reproduce (Chapman-Andresen, 1971); they are (so far as anyone knows) entirely asexual. While asexual reproduction is normal for many organisms, exclusively asexual lineages are something of a rarity. Most asexually reproducing organisms have more aphid-like life cycles - they reproduce asexually as long as conditions are favourable for doing so, but convert to sexual reproduction when times get tough. Even bacteria, which mostly don't engage in sexual reproduction per se, are able to engage in processes such as conjugation that still allow for gene flow.

And the third wierd thing about Amoeba has to be its genetics. Amoeba genomes are simply huge - the largest genomes known to exist, in fact. We humans have a genome that clocks in at a little under three billion base pairs of DNA. Amoeba proteus, the best-known species of Amoeba, has a genome containing closer to three hundred billion base pairs. And even that effort pales in comparison to Amoeba dubia, which carries around a whopping six hundred and seventy billion base pairs. That's right - the difference in genome size alone between the two species is larger than the total genome size of any other organism! The actual genetic structure of Amoeba, however, appears to be little-known. The genome of A. proteus is divided between more than five hundred chromosomes, which is hardly surprising considering its size. By means unknown, however, this enormous genome can be reduced to nearly a third of its normal size over the course of cell division (Parfrey et al., 2008). Presumably the normally polyploid amoeba jettisons excess chromosomes prior to division then recreates them from the remainder afterwards.

Amoeba proteus on the move (towards the top left of the photo). Note the knobbly bit at the bottom right corner. This is the uroid, and represents the trailing end of the cell. The form of the uroid has turned out to be surprisingly useful in identifying amoeboids. Another photo by David Patterson.

One other feature of the Amoeba nucleus is worth mentioning. The nucleus contains a number of stellate aggregations of condensed helical structures just inside the nuclear envelope that, when first observed, were not unreasonably thought to represent condensed chromosomes. However, further study showed that the nuclear helices were composed of a mixture of proteins and RNA (not DNA) and seemed to be able to be transported out of the nucleus into the surrounding cytoplasm (Minassian & Bell, 1976). The helices disappear over the course of cell division, but are regenerated afterwards. The exact function of these helices is still unknown. Minassian & Bell (1976) seem to have suggested (in a rather cagy way that would have allowed for ready back-tracking if they turned out to be wrong, and which I may have easily misinterpreted) that they could be related to ribosome formation. Gągola et al. (2003), in contrast, note the attachment of actin filaments to the helices, and imply that they may play a role in cell motility (Amoeba with removed nuclei are unable to move*, while amoeboid animals cells can continue to move even without their nuclei).

*Removing the nucleus from an Amoeba is as simple as slicing it in half.


Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40 (1): 21-48.

Chapman-Andresen, C. 1971. Biology of the large amoebae. Annual Review of Microbiology 25: 27-48.

Gągola, M., W. Kłopocka, A. Grębecki & R. Makuch. 2003. Immunodetection and intracellular localization of caldesmon-like proteins in Amoeba proteus. Protoplasma 222: 75-83.

Minassian, I., & L. G. E. Bell. 1976. Studies on changes in the nuclear helices of Amoeba proteus during the cell cycle. J. Cell Sci. 20: 273-287.

Parfrey, L. W., D. J. G. Lahr & L. A. Katz. 2008. The dynamic nature of eukaryotic genomes. Molecular Biology and Evolution 25 (4): 787-794.