Field of Science

Ending Life in a Puddle of Ichor (Taxon of the Week: Coprinopsis herbivora)

This is an auspicious moment in the history of the Taxon of the Week series, because for the first time in nearly two years, the chosen taxon is an individual species rather than some more supraspecific. So you'd think I'd open the post with a nice big picture of the species in question, wouldn't you? Sorry, you'd be wrong, because I haven't been able to find a picture of Coprinopsis herbivora. In fact, I've been able to find next to diddly on Coprinopsis herbivora. All I've been able to establish is that it was described by Rolf Singer in 1973 from Argentina as Coprinus herbivorus (and I don't have access to the original publication), and it looks like it might be found worldwide: I've found references to what look like records from Australia and Finland. And as far as C. herbivora specifically goes, that is it.

Coprinopsis picacea. Like C. herbivora, C. picacea has been included in Coprinus subsection Alachuani (morphologically defined by the cellular structure of the cap), so the two species are likely to be closely related (NB. Because of the obscenely complicated way in which botanical subgeneric nomenclature works, I can't just say "Coprinopsis subsection Alachuani", because that name probably doesn't exist). Photo by Pau Cabot.

So let's widen the field of view a little. Those of you who didn't immediately recognise the names "Coprinopsis" and/or "Coprinus" were doubtless getting decidedly frustrated by the last paragraph, seeing as I had declined to mention just what, exactly, I was talking about. To explain, Coprinopsis and Coprinus are genera of mushrooms. Until recently, Coprinus included the mushrooms known as ink-caps. When an ink-cap first pops out from the ground, it looks like a fairly undistinguished mushroom. However, as the mushroom matures, the spore-bearing gills begin to liquefy. The mushroom's cap progressively dissolves into a puddle of vile black goo, like some sort of Z-grade horror effect. As the cap dissolves from the outside in, the spores mature in the same direction, so the progressive dissolution means that mature spores are always on the edge of the cap, well exposed to be caught and carried off by the wind. At least some species of ink-cap are edible (that is, if picked before they turn into sludge) but reports differ - many species contain a compound called coprine that can react violently with alcohol. To quote Edible Wild Mushrooms of North America: "It is important to note that coprine leaves the body primed for poisoning for several days (even a week by some reports) after eating the mushroom. Therefore, it is not only the consumption of a coprine-containing mushroom and an alcoholic drink at the same time that can cause coprine poisoning. Symptoms can also occur if someone drinks wine, for instance, two or more days after the meal or eats a coprine-containing mushroom after consuming alcohol" (emphasis in the original).

Another shot of Coprinopsis picacea specimens, showing various degrees of dissolution. Photo by Marino Zugna.

Well over a hundred species of Coprinus had been identified and described from around the world, but all that began to change in the late 1990s, with the advent of molecular phylogeny. A number of studies (most notably Hopple & Vilgalys, 1999) found that the genus Coprinus was polyphyletic, with at least two widely separated clades. The deliquescent cap, it turns out, had evolved on more than occasion. The great majority of species of Coprinus belonged to a clade containing other genera that had been assigned to the family Coprinaceae, though the Coprinus species were not monophyletic within this clade - the positions of species assigned to the genus Psathyrella divided them up into three smaller clades. A very small number of Coprinus species, however, fell within the family Agaricaceae, so more closely related to the common field mushroom Agaricus bisporus (i.e. the only mushroom that many British people and their equally mycophobic descendants are willing to believe is edible) than to other "Coprinaceae" species. This wouldn't have really been a problem, except that one of those agaricaceous defecters just happened to be the type species of Coprinus, C. comatus. This meant that the name "Coprinus" had to be associated with the small segregate, not with the clade containing the vast majority of species, and Coprinus went from including over a hundred species to including two or three. Similarly, the family containing that large clade could no longer be called Coprinaceae, because it no longer contained the genus Coprinus.

The taxonomic implications of all this were worked through by Redhead et al. (2001). They renamed the no-longer-Coprinaceae clade Psathyrellaceae, and divided the ex-Coprinus species into three genera corresponding to the three smaller clades found by Hopple & Vilgalys (1999). This was not an easy process, for a number of generic names had been synonymised with Coprinus over the years, and they all had to be checked to see if they applied to the "new" genera (the results are long and tortuous, and anyone reading Redhead et al., 2001, who does not have a particular enthusiasm for mycological taxonomy is likely to suffer severe cranial implosion). For two of the segregate genera, Coprinopsis and Coprinellus, Redhead et al. dredged up ancient and little-used generic names that had been used for species in each of these clades (and when I say ancient and little-used: Coprinopsis, for instance, had been named in 1881, its own author had abandoned it by 1889, and it had it never been used between then and 2001). The third clade had no suitable generic name, and so Redhead et al. proposed the new genus name Parasola. An older name, Pselliophora, did exist for the genus Redhead et al. dubbed Coprinopsis, but they recommended that that name be quashed - on the somewhat unsteady grounds that a change from "Coprinus" to "Coprinopsis" was easier to remember than one from "Coprinus" to "Pselliophora".

Coprinopsis xenobia, another member of 'Coprinus' subsection Alachuani. Photo by Hans Bender.

As can be imagined, the prospect of wholesale name changes for over a hundred species was not greeted with unalloyed enthusiasm from all quarters. While Redhead et al. put in their request for the conservation of Coprinopsis, Jørgensen et al. (2001) put in a counter-request to change the type species of Coprinus to a species in the largest of the segregate clades - Coprinopsis - so minimising the number of species needing name changes. The decisions on these proposals were published in 2005 (Gams, 2005), with what can only be described as a distinctly grumbling tone. The name Coprinopsis was conserved over Pselliophora - but it was made clear that this proposal would not have been supported if Redhead et al. (2001) had not gone ahead and published no less than 98 new combinations in Coprinopsis and so presented the Committee with something of a do-or-be-damned situation. The proposal to change the type species of Coprinus was turned down, on the grounds that, as well as being the type, Coprinus comatus is one of the better-known species in the old genus - and its vernacular name in French is "le coprin".

And can I note that this seems to be an extraordinary degree of kerfuffle over who gets to keep a name that, loosely translated into English, means "like a turd"?


Gams, W. 2005. Report of the Committee for Fungi: 12. Taxon 54 (2): 520-522.

Hopple, J. S., Jr & R. Vilgalys. 1999. Phylogenetic relationships in the mushroom genus Coprinus and dark-spored allies based on sequence data from the nuclear gene coding for the large ribosomal subunit RNA: divergent domains, outgroups, and monophyly. Molecular Phylogenetics and Evolution 13 (1): 1-19.

Jørgensen, P. M., S. Ryman, W. Gams & J. A. Stalpers. 2001. (1486) Proposal to conserve the name Coprinus Pers. (Basidiomycota) with a conserved type. Taxon 50 (3): 909-910.

Redhead, S. A., R. Vilgalys, J.-M. Moncalvo, J. Johnson & J. S. Hopple Jr. 2001. Coprinus Pers. and the disposition of Coprinus species sensu lato. Taxon 50 (1): 203-241.

Singer, R. 1973. Diagnoses fungorum novorum Agaricalium. III. Beihefte zur Sydowia 7: 1-106.

A Quick Primer on Arthropod Growth

Successive instars of a generalised bug (Heteroptera). Image from here.

One of the trickiest things to wrap one's head around about insects and other arthropods* is also one of the most basic - how they grow. We tend to forget just how different arthropod growth is from our own - I've even known people who work with arthropods regularly to have it slip their mind.

*Other than that a scorpion's anus is at the very end of its tail next to the sting, not under the base of the tail as we chordates might tend to imagine.

For us as vertebrates, growth to maturity is fairly continuous. We start out small, we get steadily bigger. Take a balloon, blow it up, and you've got a fairly good representation of how we grow (yes, I'm massively simplifying things, but bear with me for a moment). Arthropod growth, on the other hand, is more like a series of balloons of different sizes all one inside the other, with the smallest balloon on the outside and the largest balloon at the centre. Start blowing up the balloons, and you'll only be able to blow it up to the size of the smallest balloon. If that smallest balloon breaks open (like an insect moulting its skin), then the balloons can inflate to the size of the second-smallest balloon. And so on and so forth, until you reach the largest size. Instead of growing in size continuously like we do, arthropods grow in steps - an extended period of no obvious increase in size, then a moult followed by a near-instantaneous increase as the animal swells up to fill its new skin, then another period without obvious growth. The change between moults can be drastic, as most obviously shown by the holometabolous insects with their radically different larval and adult stages. Even if the differences in morphology are not so drastic, separate instars (life cycle stages) may occupy distinctly different size ranges, with little or no overlap, and may have very distinct ecologies.

Internal pupal development of Rhagoletis pomonella (apple maggot fly), from a newly developed pupa on the left, to a pharate adult (fully developed adult still enclosed within the pupa) on the right. Photos by John Fuller, via here.

It's not that the arthropod is not growing at all between moults. A new layer of cuticle is being grown inside the old layer, albeit sort of crinkled up so that it can fit. Once the new cuticle has finished growing, the animal enters the pharate ("cloaked") state until the old cuticle is shed to reveal the new. Sometimes, the pharate period will be minimal, and the old cuticle will be shed pretty much as soon as the new one is ready. At other times, though, the pharate period will last for a considerable time. If conditions aren't right for the arthropod to move on to the next stage in its life, its growth may be effectively put on hold. Desert spiders may remain as subadults almost indefinitely, waiting for the rains to come before they moult into mature adults (and if the rains don't come one year, they can wait as subadults until the next). Caterpillars may moult into pupae at the beginning of autumn, but not emerge as butterflies until some time in the next spring when the flowers they feed on are beginning to bloom. If environmental conditions suddenly deteriorate, vertebrates are forced into the awkward position of having to maintain growth despite their reduced food supply. Arthropods, on the other hand, can afford to wait things out.

Supermajor worker of the ant Pheidologeton affinis, surrounded by minor workers. Both sizes are fully adult - the small ants will not grow into the big ones. Photo by Alex Wild.

On the other hand, vertebrates have some liberties that arthropods do not. Most arthropods have a set number of moults in their life cycle, and as a rule they do not reach maturity until the very last moult. The flipside, of course, is that once an arthropod does reach maturity, that's it. They are unable to resume growth should the occasion arise (this is not necessarily a problem because many, if not most, arthropods do not live long as mature adults). [Update: A couple of readers have pointed out that some arthropods do continue to grow and moult after maturity, but this is not the norm. Arthropods being such a mind-bogglingly enormous group, any attempt to make generalisations leaves one bound to make an idiot of oneself.] Contrary to what the cartoons may suggest, little ants do not grow into big ants. Both are fully adult, both are as big as they're going to get. In those ant species that have different sized castes, it's easy to imagine otherwise, but that's simply not the case. Big ants hatched out from their pupa as big ants, little ants hatched out as little ants. Similarly, if the queen of an ant colony were to die, it would not be possible for one of the workers to develop a functional reproductive system and take her place - sterility is a one-way trip.

My Flower is a Trumpet (Taxon of the Week: Solanales)

Fruit of Physalis alkekengi var. franchetii, the Chinese lantern plant. In species of Physalis, the persistent calyx that is characteristic of Solanales has become greatly expanded to form a protective covering for the (rather tasty!) fruit. Photo from here.

While intrafamilial relationships among flowering plants have a reputation for being contentious, one concept that has long been supported by most authors is a close connection between the Solanaceae (nightshades) and the Convolvulaceae (morning glories). Originally united on the basis of features such as similar flower structure and internal phloem in most species (the phloem is the nutrient-carrying tissue in a plant's stem, and in these taxa it is found mixed in with the central water-carrying xylem as well as around the outside of the stem as in other plants), molecular analyses have continued to support their relationship (Bremer et al., 2001). In the most recent APG classification, the two families form the greater part of the order Solanales, along with three smaller families - Montiniaceae (a family of trees and shrubs found in southern Africa and Madagascar) and the isolated genera Sphenoclea and Hydrolea (two pantropical families of small shrubby plants both found growing near or in water) (APG II, 2003).

Montinia caryophyllacea, a shrub of the Montiniaceae found from South Africa to Angola. Photo from Aluka.

The three small families, which remain outside the Solanaceae-Convolvulaceae clade (which I'll call the "core Solanales"), are placed in the Solanales largely on the basis of molecular analyses only, and so far few or no morphological features have been identified that support their referral. Peter Stevens' Angiosperm Phylogeny Website does suggest a couple of features - some shared secondary metabolites, and the fact that the calyx persists on the mature fruit (you've all seen this - it's the sepals around the stalk of a tomato). Erbar et al. (2005) identified features of flower development shared between Hydrolea and the core Solanales, but not the other two families. Most Solanales are, like other members of the Asteridae clade to which they belong, sympetalous - that is, the petals are to some degree joined together at their base. One of the distinctive features of many Convolvulaceae and Solanaceae flowers, in fact, is that they take sympetaly to its extreme - the petals are entirely fused to form a bowl or trumpet. However, while the core Solanales and Hydrolea are "late sympetalous", where the petals initially start growing separately in the bud and are only joined later by the growth of connecting bridges, Sphenoclea is "early sympetalous", where the petals are connected pretty much right from the start. Montiniaceae are not sympetalous at all, but have entirely separated (and not very big) petals.

Kumara or sweet potato, Ipomoea batatas. Photo from here.

Within the core Solanales, the Convolvulaceae are mostly vines (though the basalmost member of the Convolvulaceae, Humbertia madagascariensis, is a large tree), while the Solanaceae range from small herbaceous plants to large trees. As well as being a tree, Humbertia also differs from other Convolvulaceae in lacking internal phloem. This is intriguing, because Humbertia's sister relationship to all other Convolvulaceae means that it is just as parsimonious for internal phloem to have developed independently in the two families as for it to be a true synapomorphy of the core Solanales. The herbaceous vines of the Convolvulaceae are commonly referred to as morning glories, referring to the time of opening of their large but often short-lived flowers, but other common names are just as evocative - trumpet vine, or railway creeper (the latter because many species have become widely distributed as adventives inadvertently carried by human activity). They are also, somewhat less poetically, known as bindweeds. One such plant, Ipomoea batatas, grows large tubers that are the world's second-most important root crop, the sweet potato (Stefanović et al., 2002).

Dodder, Cuscuta epithymum, overgrowing a sage plant. Photo from Kingston University.

One particularly distinctive genus of Convolvulaceae are the dodders, Cuscuta, twining parasites of other plants. Dodders contain little or no chlorophyll of their own, and their roots degenerate early on in life so the mature plant is not connected to the ground. The leaves are minute, and one might be forgiven for thinking that they were not there at all. Cuscuta has been placed in its own family in the past, but most of the characters this has been based on are uniquely derived features resulting from its parasitic lifestyle. Neyland (2001) and Stefanović et al. (2002) confirmed that Cuscuta is nested among normal photosynthetic Convolvulaceae. Cuscuta also provides a remarkable example of convergent evolution - in its general appearance, it is almost indistinguishable from the genus Cassytha, also commonly called "dodder". Cassytha, however, is not closely related to Cuscuta at all, but is instead a member of the distant family Lauraceae, and so more closely related to magnolias.

The Solanaceae also include a number of significant taxa. As a group, most Solanaceae are decidedly toxic (at least from a human perspective), and the family includes such infamous plants as deadly nightshade (Atropa belladonna), Jerusalem cherry* (Solanum pseudocapsicum) and Jimson weed (Datura stramonium). On the other hand, the family also includes a number of plants widely grown for human consumption, such as potatoes (Solanum tuberosum), tomatoes (Solanum lycopersicum**) and eggplants (Solanum melongena). A few Solanaceae manage to be both toxic and grown for human consumption - most notably good old tobacco (Nicotiana tabacum). The question arose recently at the Te Papa blog as to whether the common black nightshade (Solanum nigrum) is toxic or not - while it is widely supposed to be, it is actually eaten in some parts of the world (Edmonds & Chweya, 1997). Fruit are eaten when ripe or cooked (the huckleberry of North America is either Solanum nigrum or a close relative), while leaves are boiled and eaten as a pot herb. It seems that, just to confuse matters, toxicity of this plant varies from place to place.

*No, I don't know why they're calledd that.

**For those who are wondering what happened to 'Lycopersicon esculentum', it has been well established that 'Lycopersicon' species fall phylogenetically within Solanum (as Solanum section Lycopersicum), and in fact are very closely related to potatoes (somatic hybrids between potatoes and tomatoes have been succesfully produced, though it looks like produce-wise they're a bit of a second Raphanobrassica***). If the tomato is included in Solanum, then its name reverts back to that originally given to it by Linnaeus way back in 1753.

***Raphanus (radishes) and Brassica (cabbages) are also closely related to each other, and a lot of time and effort was invested by the early Soviets into producing a hybrid between the two that would possess the root of a radish with the leaves of a cabbage - two crops for the price of one! The Raphanobrassica cross was successfully produced in the 1920s - sadly, it turned out to have the root of a cabbage and the leaves of a radish.


APG II (Angiosperm Phylogeny Group). 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: 399-436.

Bremer, K., A. Backlund, B. Sennblad, U. Swenson, K. Andreasen, M. Hjertson, J. Lundberg, M. Backlund & B. Bremer. 2001. A phylogenetic analysis of 100+ genera and 50+ families of euasterids based on morphological and molecular data with notes on possible higher level morphological synapomorphies. Plant Systematics and Evolution 229: 137-169.

Edmonds, J. M., & J. A. Chweya. 1997. Black nightshades. Solanum nigrum L. and related species. Promoting the conservation and use of underutilized and neglected crops 15. Institute of Plant Genetics and Crop Plant Research, Gatersleben/International Plant Genetic Resources Institute, Rome, Italy.

Erbar, C., S. Porembski & P. Leins. 2005. Contributions to the systematic position of Hydrolea (Hydroleaceae) based on floral development. Plant Systematics and Evolution 252: 71-83.

Neyland, R. 2001. A phylogeny inferred from large ribosomal subunit (26S) rDNA sequences suggests that Cuscuta is a derived member of Convolvulaceae. Brittonia 53 (1): 108-115.

Stefanović, S., L. Krueger & R. G. Olmstead. 2002. Monophyly of the Convolvulaceae and circumscription of their major lineages based on DNA sequences of multiple chloroplast loci. American Journal of Botany 89 (9): 1510-1522.

Big Suckers

Reconstruction by Werner Kraus of the palaeodictyopteran Scepasma mediomatricorum. "Flügelspannweite" means "wingspan" - the model is life size.

Last week, it was wolves, this week I am once again going to present a previously promised post, pertaining to a presentation on Palaeodictyopteroidea.

Palaeodictyopteroids were Palaeozoic pterygotes (okay, I'll stop now) that include what was until recently the very earliest known winged insect, the Early Carboniferous Delitzschala bitterfeldensis (a slightly older wing fragment described by Prokop et al., 2005, has since managed to nudge it from the record-holder's spot). It was, without a doubt, the beginning of a glorious show. All palaeodictyopteroids were large in comparison to modern insects (those with wingspans of one centimetre were among the smallest), while the largest were spectacular by anybody's standards, up to around 55 centimetres for the aptly-named Mazothairos enormis. Patterning preserved on wings in the form of light and dark bands indicates that at least some palaeodictyopteroids were strikingly coloured. The palaeodictyopteroids were also the first plant-feeding insects, with a long piercing beak superficially similar to that of modern hemipterans.

Drawing by Woodward (1876) of a fossil of Lithomantis carbonaria. Many palaeodictyopteroids (and a number of other Palaeozoic insects) possessed a pair of broad paranotal lobes on the first segment of the thorax, which has lead to their being described as "six-winged". However, the paranotal lobes differ from true wings in not being articulated. Image via Tree of Life.

Ancestral palaeodictyopteroids possessed what are called palaeopterous wings. The majority of modern insects (all except dragonflies and mayflies) belong to a clade called Neoptera, characterised by the ability to fold the wings neatly back over the abdomen when not in use. Non-neopteran (i.e. palaeopterous) insects are unable to fold their wings back flat against the body, only move them up and down, so their wings are permanently open*. One group of palaeodictyopteroids, the Diaphanopterodea, did evolve the ability to fold the wings back, but they did so independently of neopterans. Their palaeopterous wings and early appearance have led to a general agreement that palaeodictyopteroids were one of the earliest lineages of winged insect to diverge**. This is also consistent with their development - palaeodictyopteroids had the closest thing to ametabolous development possible for a winged insect, with the wings extended (but curved backwards) in the terrestrial nymphs and growing and straightening incrementally until they reached adulthood (Kukalová-Peck, 1991). As such, palaeodictyopteroids were quite possibly able to fly before they reached full maturity. Among modern insects, mayflies are the only ones to continue growth (undergoing a single moult) after extending their wings.

*Damselflies get around this limitation by having a steeply-angled thorax, so that moving the wings "up" effectively moves them back. They still can't close them flat like a neopteran.

**A notable exception can be found in the Russian school of palaeoentomologists (Sinitshenkova, 2002). The Russian school, who differ from other entomologists in regarding the neopteran ability to fold the wings as primitive and the palaeopterous orders as derive, regard the palaeodictyopteroids as related to modern hemipterans and psocopterans on the basis of the sucking beak.

Fossils of two megasecopterans, Mischoptera nigra above and Sphecoptera brongniarti below, showing the extremely narrowly attached wings on the elongate body. From Carpenter (1951).

Palaeodictyopteroids would have certainly been among the most spectacular features of the Carboniferous coal forests. Broad-winged forms such as the Palaeodictyoptera would have been reasonably fast fliers, but perhaps not particularly graceful ones, and probably resembled nothing so much as a miniature World War II bomber plane. Other palaeodictyopteroids, the Megasecoptera, developed elongate wings with very narrow bases. Megasecopterans probably did not fly as quickly as the palaeodictyopterans, but would have been very agile, possibly even able to hover in some forms. One subgroup of the Megasecoptera, the Dicliptera or Permothemistida, were also among those insects to lose the hind pair of wings.

While palaeodictyopteroids did not become extinct until the end of the Permian, they were in decline long before then (Shcherbakov, 2008). Correlations have been pointed out between the decline of the palaeodictyopteroids and increasing abundance of dragonflies - the speedy dragonflies seemingly finding the relatively slow palaeodictyopteroids to be a flying smorgasbord. Other factors may have been competition from the also-diversifying Hemiptera, and the replacement of early plants such as progymnosperms with more advanced forms with better protection against herbivores. Like the Silurian giant fungus Prototaxites, palaeodictyopteroids had initially diversified when they were pretty much the only game in town, and perhaps they were simply unable to handle the increasing heat. Whatever the reason for their disappearance, they were the most fabulous animals of their time, and the world is all the poorer for their loss.


Carpenter, F. M. 1951. Studies on Carboniferous insects from Commentry, France: Part II. The Megasecoptera. Journal of Paleontology 25 (3): 336-355.

Kukalová-Peck, J. 1991. Fossil history and the evolution of hexapod structures. In The Insects of Australia, 2nd ed. (CSIRO) pp. 141-179. Melbourne University Press.

Prokop, J., A. Nel & I. Hoch. 2005. Discovery of the oldest known Pterygota in the Lower Carboniferous of the Upper Silesian Basin in the Czech Republic (Insecta: Archaeorthoptera). Geobios 38 (3): 383-387.

Sinitshenkova, N. D. 2002. Superorder Dictyoneuridea Handlirsch, 1906 (=Palaeodictyopteroidea). In History of Insects (A. P. Rasnitsyn & D. L. J. Quicke, eds) pp. 115-124. Kluwer Academic Publishers: Dordrecht.

Jonathon Livingstone's Cousin (Taxon of the Week: Sterna)

The Arctic tern, Sterna paradisaea. This is the species famed for making the longest annual migration of any bird, all the way from the Arctic to the Antarctic. Photo by Roberto Lerco.

The terns are the gulls' more refined relations. They have become superb aerialists, spending most of their lives on the wing, feeding on fish delicately plucked from the water's surface as they fly above. Depending on where you look, the clade that the terns comprise may be dubbed the Sternini, Sterninae or Sternidae, but this is purely a quibble over ranking - there seems to be no disagreement about what is, or isn't, a tern.

At the lower level (naturally), a little more disagreement ensues. There is a clear distinction between the mostly smaller, tree-nesting tropical noddy terns of the genera Anous, Gygis and Procelsterna (sometimes all combined in Anous) and the larger, ground-nesting true terns of Sterna and related genera. The spectacular cave-nesting Inca tern, Larosterna inca, also seems to be universally placed in its own genus. However, authorities differ on whether they would prefer to include all the ground-nesting terns in a single genus Sterna, or whether they would prefer to peel off some of the more distinctive taxa into what might be called Sterna's satellite genera, such as Hydroprogne caspia* (the Caspian tern), Chlidonias (the marsh terns) or Gelochelidon nilotica** (the gull-billed tern).

*Hydroprogne, as it happens, translates into English as "water swallow", which seems a rather apropos description for any tern..

**As well as being morphologically distinct, Chlidonias and Gelochelidon (the "laughing swallow") both differ from most other terns in being much more likely to be found inland. Here in Australia, Gelochelidon nilotica can travel almost to the centre of the continent, visiting temporary salt lakes when they are filled by the rains. There is something very surreal about being in the centre of the desert, hundreds of kilometres from the coast, and looking up to see terns passing overhead.

The New Zealand fairy tern, Sternula nereis davisae. With a surviving population of only about thirty-five individuals, this is one of the world's rarest terns, and indeed one of the rarest of all birds. Photo by John Kendrick.

The only proper phylogenetic study that appears to have been published recently on terns was a mitochondrial DNA analysis by Bridge et al. (2005). Sternini were also included in the supertree analysis of Charadriiformes by Thomas et al. (2004), but a look through their source trees suggests that their data for Sternini were almost entirely derived from a 1984 PhD thesis. Bridge et al. (2005) found that Larosterna inca was nested well within Sterna sensu lato, and suggested the recognition of nine genera within this clade (including Larosterna) - as well as those already mentioned, these were Onychoprion for the brown-winged terns, Sternula for the little terns, Phaetusa simplex (the large-billed tern) and Thalasseus for the crested terns, with Sterna restricted to a group labelled the "typical black-capped terns". Most of the genera recognised by Bridge et al. (2005) correspond to groups recognised previously on morphological grounds. The one arguable exception is, ironically enough, their Sterna sensu stricto, which also remained poorly supported in Bridge et al.'s analysis, though a smaller core of species within Sterna was well-supported.

Phylogeny of terns from Bridge et al. (2005). Note that, with only two exceptions, the colour pattern of the head corresponds closely with the phylogeny, though beak coloration appears to be more labile.

One interesting detail of Bridge et al.'s results is how closely the proposed phylogeny correlates with patterns of breeding plumage coloration on the head (it is worth noting that the two exceptions, Sterna sumatrana and S. trudeaui, have breeding plumages similar to the non-breeding plumages of related species). On the other hand, the correlation drops significantly when one considers overall coloration. This is most obvious in the genus Chlidonias - the great similarity in the head views of Chlidonias species in the figure above disguises the fact that these four species vary from almost entirely black (Chlidonias niger) to mostly white with only the cap of the head black (Chlidonias hybrida)*. The main point is that while there is a common assumption that colour patterns are a priori of little use as characters for phylogenetic analysis because they are supposedly too evolutionarily labile, this is not necessarily the case. Some details of colour pattern may indeed be very variable and prone to homoplasy, others may prove to be evolutionarily very conservative (and what is labile in one clade might be conservative in another) - much as one might find in just about any other possible character complex.

*As an aside, a comparison of different sources suggests that there has been confusion over whether the genus Chlidonias is masculine or feminine (and hence what is the appropriate spelling for the species in this genus). According to David & Gosselin (2002), Chlidonias is masculine - hence C. niger, C. leucopterus and C. albostriatus, but C. hybrida, because in this case "hybrida" is a noun in apposition, not an adjective. Thanks are due to Alan Peterson's Zoonomen page for clearing this up.


Bridge, E. S., A. W. Jones & A. J. Baker. 2005. A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution. Molecular Phylogenetics and Evolution 35: 459-469.

David, N., & M. Gosselin. 2002. Gender agreement of avian species names. Bulletin of the British Ornithologists' Club 122 (1): 14-49.

Thomas, G. H., M. A. Wills & T. Székely. 2004. A supertree approach to shorebird phylogeny. BMC Evolutionary Biology 4: 28.

Wolf and Wolf and Wolf and Wolf and Cub

Canis rufus, the controversial red wolf of North America. Photo from Steven Hoelzer.

Despite the fact that I've been posting on this site for nearly two years now, I think this is just about a first - I'm actually going to write about something I've said I was going to write about. I'd better not let it become a habit - people might begin to think that I'm reliable.

In the post just linked to, I considered writing on "the taxonomy of dingoes and singing dogs, and of the wolf complex in general, [and] the origins of the red wolf (and how the ICZN fumbles on hybrids)". This is that post. To write about the wolf complex, though, first I'll have to define it. The phylogenetic analysis of Bardeleben et al. (2005) found a primary division of the genus Canis between the side-striped (Canis adustus) and black-backed (Canis mesomelas) jackals on one hand, and a clade containing the golden jackal (Canis aureus), coyote (Canis latrans), wolf (Canis lupus) and domestic dog (Canis familiaris) on the other. This latter clade was also supported by Zrzavý & Řičánková (2004), who also included therein Canis simensis, the Simien jackal or Ethiopian wolf. These five species, therefore, can be referred to as the wolf complex (or Canis 'sensu stricto', if one were to accept Zrzavý & Řičánková's suggestion of moving the other two species to separate genera, but I don't know of anyone who has). Relationships within the clade are not yet clearly resolved.

The Indian wolf, Canis pallipes, one of the "subspecies" of Canis lupus that has been regarded as a separate species in recent years. Photo by Rajpal Singh.

Though the four main species of Canis aureus, C. lupus, C. latrans and C. simensis all seem to be safe enough, beyond this it all becomes hazy*. At their broadest circumscriptions, three of the four species are extremely polytypic. Mech (1974) listed thirty-two subspecies for Canis lupus, Bekoff (1977) gave nineteen for Canis latrans, and while I haven't found a full listing of subspecies for Canis aureus, I think it's safe to say that there's a few. Even C. simensis manages to fit in two subspecies (Sillero-Zubiri & Gottelli, 1994), despite having a distribution not much larger than a cereal box (the two subspecies are divided by a minor geographical hiccup known as the Rift Valley). Needless to say, a number of these "subspecies" have been recognised as distinct species at one time or another, particularly various wolf populations such as the eastern North American Canis lycaon, the Indian C. pallipes or the Japanese C. hodophilax. The North African C. lupaster doesn't seem to be clamouring for separate species status, but authors disagree whether it's a subspecies of C. aureus or C. lupus. And yes, this is one of those "species concept" things - all members of the wolf clade seem to be pretty much fully interfertile, though behavioral differences may slow down cross-breeding where species overlap.

*It occurs to me that this line is becoming something of a cliché for this site. Honestly, is there any group of organisms out there for which the taxonomy is not hazy?

The Egyptian Canis lupaster, the one that doesn't know if he's a wolf or a jackal. Photo by Thomas Krumenacker.

The most hotly contested issue of interfertility in the wolf clade is undoubtedly that involving 'Canis rufus', the red wolf. The name 'Canis rufus'* has been applied to a form of Canis once found over a large part of the south-eastern United States, from Texas to Florida (Paradiso & Nowak, 1972), but which became extinct in the wild by 1980, before a re-introduced population was established from captive animals in North Carolina in the late 1980s. However, numerous authors have made the suggestion that C. rufus is not a valid 'species', but represents a hybrid between C. lupus (or C. lycaon) and C. latrans (Brownlow, 1996). As 'pure' red wolves became fewer and further between, hybridisation with coyotes became common, further muddying the waters.

*Older references use the name Canis niger, originally applied to the now-extinct Florida red wolf (Canis rufus floridanus). While niger is the older name by some sixty years, the book that it was published in, the Travels of W. Bartram, was declared by the ICZN to be invalid for the purposes of nomenclature, so the next-oldest name swings into use.

The original Canis lupus lupus. The species status of this one, at least, is safe. Photo by Milan Kořínek.

The red wolf was perhaps the academic victim of two malign influences - an unjustified preconception about how speciation works, and the ability of politics to interfere with scientific inference. While no law explicitly states as much (Brownlow, 1996), the general policy for conservation in the United States (and, for that matter, most other places in the world) has been that "hybrids" aren't worth conserving. Instead, there is generally a focus on maintaining "pure" lineages that is sometimes at odds with reality. Also, hybridisation has generally been assumed to be of little importance in animal evolution. The stereotypical view that hybrids between species are infertile (not the case with members of the wolf clade) means that hybrids are assumed to be dead-end oddities. Even the ICZN previously regarded names based on hybrids as invalid, and while this rule was most likely introduced to prevent names based on one-off, individual hybrid specimens (such as a mule), it was also invoked to declare names for populations of hybrid origin to be invalid (the current Code has changed the rules somewhat to remove this ambiguity). This is in stark contrast to the situation in botany, where hybridisation has long been recognised as a major player in the origin of new species, and where the Botanical Code of Nomenclature even has a specific concept of "nothospecies" for taxa of hybrid origin. As a result, the debate over the red wolf became unnecessarily polarised into an argument over whether it was of hybrid origin or a valid species - the possibility that it could be both seems to have never entered consideration.

The taxonomy of the wolf clade is further confused, of course, by the question of how to deal with domestic dogs and their wild derivatives. I'll refer you to a post by Darren Naish from a couple of years ago on the question of domestic dog origins. Darren refers in that post to the pariah dogs - wild populations of generalised domestic dog-type that are found from southern Asia to Australia, where, of course, they are represented by the dingo.

The New Guinea singing dog, Canis hallstromi (sometimes). Photo by Patti McNeal.

There is no doubt that populations such as the dingo and the New Guinea singing dog are ultimately derived from dogs that arrived in Australasia with the original human settlers. On this basis, the majority of authors have tended to include them with with domestic dogs as Canis familiaris and Canis lupus familiaris. However, these dogs have been living wild in their respective countries for a very long time, and have become morphologically distinct from their ancestors, leading others to separate them as the species Canis dingo and Canis hallstromi (Koler-Matznick et al., 2003)*. Again, the difference seems to be more one of philosophical approaches to what should be regarded as a "species", with a soupçon of the artificial distinction between "natural" and "altered" conditions. How long does it take for a "feral" population to become a "wild" one?

*One further point (which I'm putting in a footnote because I couldn't work out how to integrate it into the paragraph) is that these dogs quite possibly became part of the "wild" environment very soon after their arrival with humans, if not immediately (and while there's a lot of disagreement about when exactly that was, it was at least many tens of thousands of years ago). After all, the modern intensive management of domestic animals did not always apply - in many cases, animals were largely left to roam free, dogs especially so, and their presence was more encouraged than controlled. The dogs that originally arrived in New Guinea and Australia could have been more commensals than domesticates of humans.


Bardeleben, C., R. L. Moore & R. K. Wayne. 2005. A molecular phylogeny of the Canidae based on six nuclear loci. Molecular Phylogenetics and Evolution 37 (3): 815-831.

Bekoff, M. 1977. Canis latrans. Mammalian Species 79: 1-9.

Brownlow, C. A. 1996. Molecular taxonomy and the conservation of the red wolf and other endangered carnivores. Conservation Biology 10 (2): 390-396.

Koler-Matznick, J., I. L. Brisbin Jr, M. Feinstein & S. Bulmer. 2003. An updated description of the New Guinea singing dog (Canis hallstromi, Troughton 1957). Journal of Zoology 261: 109-118.

Mech, L. D. 1974. Canis lupus. Mammalian Species 37: 1-6.

Paradiso, J. L., & R. M. Nowak. 1972. Canis rufus. Mammalian Species 22: 1-4.

Sillero-Zubiri, C., & D. Gottelli. 1994. Canis simensis. Mammalian Species 485: 1-6.

Zrzavý, J., & V. Řičánková. 2004. Phylogeny of Recent Canidae (Mammalia, Carnivora): relative reliability and utility of morphological and molecular datasets. Zoologica Scripta 33 (4): 311-333.

Further Readings from the Rocks (Taxon of the Week: Graptolithina)

Colony of the crustoid graptolite Hormograptus sphaericola, showing the triad mode of branching. Image via Graptolite Net (Warning: While an excellent resource for all things graptolite-y, for an unknown reason some pages of Graptolite Net do try to play elevator music at you. Click link at own risk.)

Today, I'm going back to Graptolithina, the graptolites. For those of you who aren't familiar with graptolites, you can read my previous post on the subject.

As mentioned in that post, it is by now universally accepted that the closest living relatives of the Palaeozoic graptolites are to be found in the Pterobranchia. Pterobranchs are, admittedly, a fairly obscure group in their own right, being minute colonial animals that feed by means of a tentacled lophophore*. Despite their obscurity, though, pterobranchs are not devoid of interest, belonging as they do to the phylum Hemichordata and hence among the closer invertebrate relatives to ourselves. The most basic character uniting graptolites and pterobranchs is that they both have an external covering of chitinous fuselli - their skeleton is constructed in bands, a bit like the bandages wrapping a mummy.

*Yes, you heard me - lophophore.

Despite the two groups usually being treated as separate classes, the distinction between graptolites and pterobranchs is a little vague. Okay, it's a lot vague. The problem doesn't lie so much with the graptolites as it does with the pterobranchs. There are three living genera of pterobranchs, each of theme very distinct from each other. In fact, the genera Rhabdopleura and Cephalodiscus are easily more distinct from each other than either is to the graptolites. Rhabdopleura forms a long, linear colony with individual zooids budding off one by one, zooids remaining permanently attached to each other by a stolon, and with a skeleton of only a single banded fusellar layer. Cephalodiscus colonies bud irregularly to form irregular-shaped colonies, zooids do not remain permanently attached to each other but remain in loose association, and the fusellar layer of the skeleton is covered over by an external unbanded cortex. The third genus, Atubaria, has zooids very similar to those of Cephalodiscus, but doesn't secrete a colonial skeleton at all.

Modern pterobranchs - Cephalodiscus above, Rhabdopleura below. Image from here.

Graptolites combine the regular colony structure and permanent stolon of Rhabdopleura with the external cortex of Cephalodiscus. In Cephalodiscus, cortex is produced by individual zooids crawling out of the colony to plaster cortex on from outside, but it is difficult to imagine how graptolites would have managed this with their permanent stolon. Some authors have suggested that graptolites possessed an extensive evagination of the outer epithelium emerging from the colony openings, partially or entirely converting the exoskeleton into an endoskeleton. To further confuse matters, cortex-like structures have also been identified in fossil rhabdopleurids (Mierzejewski & Kulicki, 2001). Overall, it is highly possible that graptolites should really be included within pterobranchs (some authors have used the name "Graptolithoidea" for such a grouping). There are five well-established graptolite orders*. The Graptoloidea are the familiar planktic graptolites, the Dendroidea were upright-branching benthic forms, and the Crustoidea, Tuboidea and Camaroidea were all horizontally-growing encrusting forms. Among these orders, there is a clear division between the Tuboidea and Camaroidea on one hand (in fact, the distinction of these two orders is a little doubtful), and the Crustoidea, Dendroidea and Graptoloidea on the other (Mierzejewski, 2001). Colonies of Tuboidea and Camaroidea exhibit diad branching as in modern Rhabdopleura, with zooids branching off the stolon one by one**. The other three orders, in contrast, possess triad branching. Instead of only one zooid branching at a time, two zooids branch alongside each other, a larger autotheca and a smaller bitheca (most graptoloids later showed a secondary reduction or loss of bitheca production). Many different suggestions have been made as to what the distinction between the two zooid forms could have been in life - feeding vs. reproductive zooids, males vs. females, feeders vs. cleaners, etc. - but, of course, there's really no way of knowing (modern pterobranchs don't show such inter-zooid specialisations). Many tuboids and camaroids also possessed distinct autothecae and bithecae, but bithecae were distributed irregularly within the colony rather than in regular association with autothecae. A collection of stolon fragments described as early crustoids by Mierzejewski et al. (2005) shows an effectively triad branching pattern but with a slight lag between side-branches, suggesting that the triad pattern could have derived from an ancestral diad pattern by simple shortening of the gap between regular autothecal and bithecal branchings.

*Bulman (1970) recognised six, but the Stolonoidea have not been universally accepted as graptolites. Other authors have recognised further orders such as Dithecoidea, but these have usually been poorly characterised and/or possibly not graptolites.

**Technically, the colony produces one lateral theca at a time. Being soft and squishy, the zooids themselves are not preserved as fossils, but it seems a reasonably safe assumption that each thecal opening housed an individual zooid.

The holotype of the camaroid graptolite Tubicamara coriacea. Camaroids had autothecae divided into an inflated basal camara (chamber) and an upright collum. From Kozłowski (1949), via Graptolite Net. Kozłowski (1949), offhand, is one of the books that has most made me wish I could read French.

Records of the three encrusting orders are decidedly limited compared to the dendroids and graptoloids, and all three are only known from the Ordovician and Silurian (camaroids are Ordovician only). However, it is debatable to what extent this lower record reliably indicates the encrusting graptolites to have been rarer. The graptolite fossil record is heavily biased towards remains preserved in low-energy environments (Kirk, 1979), with the relatively frail graptolite skeleton rapidly being destroyed in high-energy environments. Perhaps the rarity of encrusting forms reflects a higher-energy habitat preference rather than true lack of abundance.


Bulman, O. M. B. 1970. Graptolithina with sections of Enteropneusta and Pterobranchia. In Treatise on Invertebrate Paleontology Part V, 2nd ed. (C. Teichert, ed.) pp. V1-V149. The Geological Society of America, Inc.: Boulder (Colorado), and the University of Kansas: Lawrence (Kansas).

Kirk, N. H. 1979. Thoughts on coloniality in the graptolites. In Biology and Systematics of Colonial Organisms (G. Larwood & B. R. Rosen, eds.) pp. 411-432. Academic Press: London.

Kozłowski, R. 1949 ("1948"). Les graptolithes et quelques nouveaux groupes d’animaux du Tremadoc de la Pologne. Palaeontologica Polonica 3: I-XII, 1-235.

Mierzejewski, P. 2001. A new graptolite, intermediate between the Tuboidea and the Camaroidea. Acta Palaeontologica Polonica 46 (3): 367-376.

Mierzejewski, P., & C. Kulicki. 2001. Graptolite-like fibril pattern in the fusellar tissue
of Palaeozoic rhabdopleurid pterobranchs. Acta Palaeontologica Polonica 46 (3): 349-366.

Mierzejewski, P., C. Kulicki & A. Urbanek. 2005. The world’s oldest crustoid graptolites from the upper Tremadocian of Poland. Acta Palaeontologica Polonica 50 (4): 721-724.

Colonies on the Move

First off, the latest edition of the plant blogging carnival Berry Go Round is up at A Neotropical Savanna, so go take a look.

Secondly, Susannah of Wanderin' Weeta has presented a nice overview of bryozoans. Bryozoans, for those as don't know 'em, are tiny colonial aquatic animals, and are one of the groups of organisms that I personally think are most unfairly overlooked. A great many people will have probably never heard of them, but they are not uncommon, they or the remains of their colonies are easily found attached to rocks, shells, etc. at any beach, and their delicately structured colonies can be exceedingly attractive, as indicated by their sometimes-used common name of "lace animals".

As a follow-on from Susannah's post, I just thought I'd present you with one of the more unusual and eye-catching types of bryozoan. Modern lunulitiform bryozoans belong to three families, Lunulitidae, Selenariidae and Cupuladriidae. Unlike other bryozoans, lunulitiforms colonies are not anchored to their substrate, but lie unattached on the surface of the sediment. While free-living bryozoan colonies sometimes grew quite large during the Palaeozoic, the rise of a well-developed infauna (burrowing animal assemblage) and the resulting bioturbation rather did it in for the large forms, and modern lunulitiforms are small, only about a centimetre and a half across at most. They are disc-shaped and raised in the centre, so they look not unlike a Southeast Asian fieldworker's hat, with the zooids all emerging on the outer surface. As shown in the picture near the top of this post from Aaron O'Dea, lunulitiform colonies are generally highly integrated, with zooids growing in a strict radial pattern.

So highly integrated are these colonies, in fact, that some are able to move as if they were a single organism, as shown in the photo of Selenaria maculata just above by P. L. Cook. The zooids around the edge of the colony develop exceeding long setiform avicularia (to find out what an avicularium is, read Susannah's post) that the colony can use like legs to walk on. Selenaria maculata colonies can reach speeds of about one metre per hour, which may not sound particularly fast until you consider that most bryozoan colonies don't move at all.