Rock Mosses

Black rock-moss Andreaea rupestris, photographed by Sture Hermansson.

Upon first examining the picture above, you might think that you were looking at a patch of moss. Which would not be an unreasonable assumption to make, because that is exactly what you are looking at. But this is not just any moss, but perhaps one of the most interesting mosses out there.

The hundred or so species of the genus Andreaea, found in cooler regions around the world, are commonly known as rock mosses or granite mosses in reference to their preferred growth habitat on acidic rocks. They can often look black or red rather than green (presumably relative to how dry they are), and they are often brittle. Glime (2013) notes that a characteristic feature of granite mosses is that a hand brushed over one will come away with small fragments stuck to it, and suggests that this may act as a method of vegetative dispersal. Usually, granite mosses are autoicous: a single plant has both male and female reproductive structures, but they are borne in separate clusters. What makes Andreaea really interesting, though, is how it produces spores. As explained in the diagram I used in an earlier post, mosses produce spores from a sporophyte (diploid plant) that grows supported by the gametophyte (haploid plant) that comprises the green, vegetative stage of the moss life cycle. In most mosses, the sporophyte holds itself up by means of a long stalk called a seta, and spores are released from the terminal capsule by the ejection of a covering operculum.

Capsules of Andreaea, photographed by David Tng.

Andreaea does things differently. In this moss, the capsule is not supported by its own stalk, but is instead lifted up on an extension of the gametophyte called a pseudopodium. And instead of popping off an operculum, the Andreaea capsule splits open longitudinally into a squashed crown. Andreaea shows its difference after the spores are released as well: while the spores of other mosses germinate into a filamentous protonema (the moss 'seedling', as it were), the protonema of Andreaea bears thalloid appendages.

Such is the distinctive of Andreaea that it has been classified in a separate class from most other mosses, the Andreaeopsida. Phylogenetic analysis has demonstrated that Andreaea is one of the earliest diverging of all mosses, being the next to diverge from the main moss lineage after the Sphagnopsida (the group that includes Sphagnum). In some classifications, the class Andreaeopsida is restricted to Andreaea alone, but there are two other small genera that have been grouped with it in the past.

Andreaeobryum macrosporum, photographed by Masaki Shimamura.

Andreaeobryum macrosporum is a single unusual moss species found in north-west North America. Like Andreaea, it is found growing in rocks, though its preference is for basic rocks such as limestone. It also resembles Andreaea in having a spore capsule that opens through slits, though in the case of Andreaeobryum the apex of the capsule eventually wears off as well and the capsule splays fully open. The biggest difference between Andreaea and Andreaeobryum is that the capsule of the latter is not raised on a gametophytic pseudopodium, but possesses its own supporting seta like that of typical mosses (albeit a particularly short and stubby one). The phylogenetic position of Andreaeobryum remains uncertain: a molecular analysis by Chang & Graham (2011) recovered an Andreaea-Andreaeobryum clade, but with very low support.

Takakia lepidozioides, from here.

The real wild-card in basal moss phylogeny, however, is the little green monster known as Takakia. Takakia is a genus of two species found in western North America and eastern Asia. It was first discovered in the Himalayas and described in 1861—as a liverwort. This is a bit like being presented with a new species of snake, and describing it as a type of eel. But it has to be pointed out that Takakia possesses some very un-moss-like features. It has finely divided leaves, a feature common in liverworts but not known from any other moss. Its leaves contain oil bodies: again, unlike any other moss, but like many liverworts. Matters were not helped by the fact that Takakia was first described from vegetative material only, and it was not until the description of sporophytes in the 1990s that Takakia was conclusively accepted as a moss (Renzaglia et al. 1997).

Even so, its position within the mosses remained uncertain. A relationship with Andreaea has been suggested, as the capsule (though borne on a seta rather than a pseudopodium) opens through a single spiral slit. However, recent phylogenetic analyses have not supported a direct relationship between the two. Chang & Graham (2011) found in the analysis of their data that its position was vulnerable to the analytical model used: it could be placed as the sister taxon to all other mosses, or it could be the sister to the Sphagnopsida (with the two together being the basalmost moss clade). We have not heard the last of little Takakia.

REFERENCES

Chang, Y., & S. W. Graham. 2011. Inferring the higher order phylogeny of mosses (Bryophyta) and relatives using a large, multigene plastid data set. American Journal of Botany 98 (5): 839-849.

Glime, J. M. 2013. Bryophyta - Andreaeopsida, Andreaeobryopsida, Polytrichopsida. Chapt. 2-6. In: Glime, J. M. Bryophyte Ecology. Volume 1. Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 29 June 2013 and available at .

Renzaglia, K. S., K. D. McFarland & D. K. Smith. 1997. Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). American Journal of Botany 84 (10): 1337-1350.

The Diversity of Neosauropods, or Pity Poor Camarasaurus

Articulated skeleton of juvenile Camarasaurus lentus in the Carnegie Museum of Natural History, photographed by Daderot.

Let me just get the obvious out of the way first: sauropods were huge. Mind-bendingly huge. In some cases, big enough to reduce a human to a sticky puddle under foot and not even break their stride. For close to 150 million years, they were the largest land animals anywhere in the world, and no other terrestrial animal at any time has come even close to rivalling their largest representatives in size. Being around for so long, it should also be no surprise that they were diverse: a large number of sauropod genera have been named, representing a wide variety of forms. Nevertheless, most people's idea of sauropods is encompassed within just four genera from the late Jurassic of North America: Diplodocus, Apatosaurus, Brachiosaurus and Camarasaurus.

These four genera all belong to the clade Neosauropoda, which has been defined as the smallest clade containing the genera Diplodocus and Saltasaurus (a late Cretaceous South American genus). Upchurch et al. (2004) diagnosed the neosauropods by a number of cranial features, together with a reduction in the fourth hind toe (part of a general trend towards toe reduction in sauropods as their feet became more columnar—see this article by Darren Naish for more on the subject). However, Upchurch et al. were writing before the recognition of the Turiasauria, a European clade that is probably the sister group of neosauropods (Royo-Torres et al. 2006), and I don't know how that clade would affect the synapomorphy distribution*. The neosauropods quickly became the dominant sauropod group after their appearance in the middle Jurassic, and the only non-neosauropod sauropods to make it into the early Cretaceous were the aforementioned turiasaurs and possibly Jobaria, an African genus that varying analyses place either just inside or just outside the Neosauropoda.

*There has been an annoying tendency in recent years for many papers featuring phylogenetic analyses to present us with the character data matrix and the final trees from the analysis, but not do anything to map character changes onto the tree. The only way to find that out would be by transcribing the entire matrix and re-running the analysis yourself.

Mounted skeleton of Amargasaurus cazaui in the Melbourne Museum.

The famed North American genera include representatives of each of the two main lineages within the Neosauropoda. Diplodocus and Apatosaurus belong the Diplodocoidea, and Brachiosaurus and Camarasaurus belong to the Macronaria. Diagnostic features of the diplodocoids according the Upchurch et al. (2004) include restriction of teeth to the front of the jaw and a subrectangular snout. This last feature reaches an extreme in the middle Cretaceous Nigersaurus, which was another of those animals that serves to remind us that, if God did indeed create all of nature, then he was taking the piss. Ludicrous diplodocoids also include the late Jurassic South American Brachytrachelopan, which took one look at the graceful, elongate necks of all the other sauropods and decided that it simply couldn't be having with all that.

Reconstruction of Saltasaurus loricatus, by Lady of Hats.

The name of the other lineage, Macronaria, means 'big nostrils', and one of the notable features of this clade is, indeed, a great expansion in the size of the nares, the opening for the nostrils in the skull (though whether the size of the nares directly corresponds to the size of the actual nostrils is, I suppose, another question). As well as Brachiosaurus and Camarasaurus, this clade includes the Titanosauria, a very successful group that included the last surviving sauropods, but whose significance was overlooked for many years because they had the poor judgement not to achieve their main diversity in North America. At least some titanosaurs, such as Saltasaurus pictured above, sported a skin reinforced by nodules of bone.

Which brings us to Camarasaurus. For some reason, of the 'Big Four' genera, this is the one that gets the least love. While the other three have each in their turn enjoyed roles as stars of stage and screen, I'm not aware of a single film in which Camarasaurus has even been given a name-drop*. In John Sibbick's illustration of Brachiosaurus and Camarasaurus together (scroll down a bit at the link) in Norman's (1985) The Illustrated Encyclopedia of Dinosaurs, Brachiosaurus marches confidently towards the front bearing a goofy leer, while Camarasaurus is forced to sulk towards the back. It's all blatantly unfair. It's not as if Camarasaurus is rare: in fact, Camarasaurus may just be the best known of all sauropods, represented in the Morrison Formation by a whole whack of remains, including what is perhaps the single most beautiful sauropod specimen ever found (the one with which I opened this post). It was no slouch in the size department, either: its maximum length of about 23 metres is similar to that of Apatosaurus, despite it having proportionally shorter appendages than the latter. Nor does it lack distinctiveness: the short, bulldog-like face of Camarasaurus instantly stands out in any neosauropod line-up. So after all this time, doesn't Camarasaurus deserve to be given the spotlight?

*Though it is a pity that the name 'Camarasaurus' won out in the priority stakes over its competitor 'Morosaurus', which to those of us from a New Zealand background suggests a dinosaur made out of chocolate.

REFERENCES

Norman, D. 1985. The Illustrated Encyclopedia of Dinosaurs. Salamander Books: London.

Royo-Torres, R., A. Cobos & L. Alcalá. 2006. A giant European dinosaur and a new sauropod clade. Science 314: 1925-1927.

Upchurch, P., P. M. Barrett & P. Dodson. 2004. Sauropoda. In: Weishampel, D. B., P. Dodson & H. Osmólska (eds) The Dinosauria, 2nd ed., pp. 259-322. University of California Press: Berkeley.

Sleepers

Hawaiian sleeper Eleotris sandwicensis, from the Hawaii Biological Survey.

Fishes of the genus Eleotris are a group of gobioids commonly known as the spinycheek sleepers. I haven't found a definite statement as to why they're called sleepers, but presumably it's because, as sit-and-wait ambush predators, they spend a lot of time lying around on the bottom. Eleotris species are found in tropical and subtropical waters around the world, mostly in estuaries and freshwater. They are smallish fish, with most species seeming to be in the ten to twenty centimetre size range. The 'spinycheek' part of the vernacular name refers to the presence of a hook-like spine on the lower corner of the preoperculum (the bone running between the cheek and the gill cover on the side of the head). This spine may be covered with tissue and so not always readily visible, but Pusey et al. (2004) note that it 'can be easily detected by running a thumbnail lightly, and carefully, along the preoperculum margin'. Carefully, I think, is the operative word here.

Eleotris oxycephala, from Chinese Academy of Fishery Sciences.

The species of Eleotris are mostly a conservative bunch appearance-wise, and the genus seems to have gotten a reputation for being difficult to work with taxonomically (it doesn't help matters that for a long time 'Eleotris' was something of a dumping ground for generalised gobioids). The Japanese species were revised in 1967 by Akihito (yes, that Akihito), the West African species have been revised by Miller (1998), and the North and South American species by Pezold & Cage (2002), but species from the remainder of the Indo-Pacific remain unrevised. There has been some disagreement over the status of a group of New World species classified in the genus Erotelis, which resemble Eleotris species but are generally more elongate and have higher numbers of fin rays (Pezold & Cage 2002). Miller (1998) felt that this genus should be synonymised with Eleotris, but Pezold & Cage (2002) argued that its members were distinct enough to be kept separate. A molecular phylogenetic analysis of the gobioids by Thacker & Hardman (2005) suggested that 'Erotelis' is nested within Eleotris, which may support their synonymisation.

Dusky sleeper Eleotris fusca, photographed by C. Appleby.

The sleepers are amphidromous, meaning they spend part of their life in the sea. Sleepers enter the sea as larvae, returning to fresher waters as they mature. As a result of this marine stage in the life cycle, individual species of Eleotris may be widespread and can often be found in places such as oceanic islands that lack populations of permanently freshwater species. It has even been suggested they may cross oceans: Miller (1998), noting similarities between species on either side of the Atlantic, suggested that this may be the result of trans-Atlantic dispersal. Among the evidence cited in favour of this possibility was the record in 1987 of a specimen of the northern South American species Eleotris pisonis from the island of St Helena in the mid-Atlantic. However, Miller also noted that the amount of time it would take to disperse across the Atlantic is greater that the time it would take for the larva to develop to maturity (and mature Eleotris are not known from the open sea). Pezold and Cage (2002) were more skeptical about the possibility of trans-Atlantic dispersal, even though they admitted to being unable to identify any characters distinguishing the Caribbean E. amblyopsis from the West African E. daganensis. They queried whether the St Helena record may have been an individual transported in ship ballast water, rather than an unaided dispersal.

REFERENCES

Miller, P. J. 1998. The West African species of Eleotris and their systematic affinities (Teleostei: Gobioidei). Journal of Natural History 32 (2): 273-296.

Pezold, F., & B. Cage. 2002. A review of the spinycheek sleepers, genus Eleotris (Teleostei: Eleotridae), of the western hemisphere, with comparison to the West African species. Tulane Studies in Zoology and Botany 31: 19–63.

Pusey, B., M. Kennard & A. Arthington. 2004. Freshwater Fishes of North-eastern Australia. CSIRO Publishing: Collingwood.

Thacker, C. E., & M. A. Hardman. 2005. Molecular phylogeny of basal gobioid fishes: Rhyacichthyidae, Odontobutidae, Xenisthmidae, Eleotridae (Teleostei: Perciformes: Gobioidei). Molecular Phylogenetics and Evolution 37: 858-871.

Raphitoma histrix

The shell in the photo above (from G. & Ph. Poppe) belongs to Raphitoma histrix (Bellardi 1847)*, a small marine gastropod (the shell shown is just over 6 mm long). Raphitoma histrix was first described as a fossil from the Pliocene of north-western Italy, but the name has also been used for Recent shells from the Mediterranean and western Africa. Rolán et al. (1998) implied (but did not state) that the identity of the modern specimens could do with a double-check. Raphitoma histrix is found in soft-bottomed, reasonably calm waters.

*There has been a bit of confusion over the exact name for this species. Many authors have referred to it as 'Raphitoma hystrix (Cristofori & Jan 1832)'. However, as noted by Pusateri et al. (2012), Cristofori & Jan's name was a nomen nudum (meaning that it lacked an accompanying description), making it not validly published. The name was not validated until it was used by Bellardi (1847), who used the spelling 'histrix'.

Raphitoma histrix is the type species of the genus Raphitoma, which is in turn the type genus of the subfamily Raphitominae. Past authors have classified this genus within the family Turridae, and the Raphitominae broadly corresponds with the group that has often been called the 'Daphnellinae' (other 'turrids' have been featured on this site before: Comitas, Antiplanes, Kuroshioturris, Asperdaphne and Paradrillia). However, with the recognition that the old 'Turridae' was largely just a dumping ground for less differentiated members of the superfamily Conoidea, the Raphitominae is now usually treated as part of the Conidae, and so a member of the same family as the cone shells. Like other members of this family, including other species of Raphitoma, R. histrix is probably a predator, possibly feeding on other marine invertebrates such as worms.

REFERENCES

Pusateri, F., R. Giannuzzi-Savelli & M. Oliverio. 2012. Revisione delle Raphitomidae mediterranee 1: su Raphitoma contigua (Monterosato, 1884) e Raphitoma spadiana n. sp., specie sorelle (Gastropoda, Conoidea). Sociedad Espanola de Malacologia—Iberus 30 (1): 41-52.

Rolán, E., J. Otero-Schmitt & F. Fernandes. 1998. The family Turridae s.l. (Mollusca, Gastropoda) in Angola (West Africa), 1. Subfamily Daphnellinae. Sociedad Espanola de Malacologia—Iberus 16 (1): 95-118.

The Araeolaimida: We Barely Know Ye

Axonolaimus sera, from here.

Overall, the nematodes cannot be considered one of the best-known groups of animals. This is not because they are at all uncommon: there is the oft-cited factoid that nematodes are so abundant in every corner of the world that, if everything other than them was somehow instantaneously removed, the ghostly shadow of the planet Earth would supposedly still be visible as a cloud of microscopic worms. Nematodes are even found in places other animals are not: they have been found further beneath the Earth's surface than any other multicellular organism. There are some nematode species that attract attention, such as those that cause diseases, or are notable crop or animal pests. The nematode Caenorhabditis elegans has been a workhorse of developmental biology for many a year. But these well-studied taxa represent only a small proportion of the full nematode diversity out there.

Being very small and soft-bodied, nematodes do not usually present taxonomists with a great variety of clearly defined morphological features. As a result, dividing nematodes into well-supported groupings has not been an easy task (there are some notable exceptions: try looking up the Desmoscolecida one of these days). Take, as an example, the group known as the Araeolaimida. This name spent many years as a bit of a wastebasket for various non-parasitic nematode families. Eventually, it was restricted by Ley & Blaxter (2002) to just four families: the Axonolaimidae, Comesomatidae, Diplopeltidae and Coninckiidae, with many taxa previously treated as Araeolaimida included in a separate order Plectida. Fonseca & Bezerra (2012) include a fifth family, the Bodonematidae, that was not mentioned by Ley & Blaxter. Even in this restricted sense, the Araeolaimida may not represent a coherent group. There is no single feature shared by all araeolaimidans that is not found in other nematodes, and a molecular phylogenetic study of nematodes by van Megen et al. (2009) did not recover a monophyletic araeolaimidan clade. Nevertheless, Araeolaimida normally have the ovaries outstretched within the bodies of females (in many other nematode taxa, they are folded back on themselves), and the amphids (sensory grooves on the sides of the head) are usually spiral or looped in shape. The majority of araeolaimidans are marine, with freshwater and terrestrial environments being home to two genera of Diplopeltidae, and a few species of Axonolaimidae (Fonseca & Bezerra 2012). We don't know much about their diet, but they are probably grazers on micro-algae or bacteria. About 400 species of Araeolaimida have been described, but it would be very surprising if there weren't more out there.

Head end of the freshwater diplopeltid Cylindrolaimus, photographed by Peter Mullin. Note the dark circle near the end: this is the amphid.

The separate families are a bit easier to define (Fonseca & Bezerra 2012). The single known species of Bodonematidae, Bodonema vossi, stands out by having a pharynx with the mid-part differentiated into a series of muscular bulbs, as opposed to the fairly simple pharynxes of other Araeolaimida. Coninckia, the only genus of Coninckiidae, has the amphids sitting on differentiated plaques that are not present in other taxa. The Comesomatidae have spiral amphids, while the Axonolaimidae and Diplopeltidae have simpler looped amphids. The last two families are distinguished by the shape of the buccal cavity, which is larger and more strongly sclerotised in the Axonolaimidae.

One detail which caught my eye when researching this post is that males of some axonolaimids produce two different forms of spermatozoa (Riemann 1986). The sperm cells produced in the anterior testis of Nicascolaimus punctatus are more than three times the size of those produced in the posterior testis. In another axonolaimid species, Axonolaimus helgolandicus, it is the posterior testis that produces the larger cells. Both types of sperm were shown in N. punctatus to be transferred to females, but the reason for the two different sperm types is unknown. Pomponema, a genus belonging to a separate group of nematodes from the Araeolaimida, produces dimorphic sperm in which the larger cells seem to break down before they are transferred to the female, and it is possible that only one sperm type functions to fertilise the female in axonolaimids as well. Perhaps the other sperm type represent some sort of nuptial gift? Or could they somehow interfere with fertilisation by other males? We await the nematode enthusiast who will find out.

REFERENCES

Fonseca, G., & T. N. Bezerra. 2012. Order Araeolaimida De Coninck, 1965. Zoology Online. Berlin, Boston: De Gruyter. Retrieved 3 Jun. 2014, from http://www.degruyter.com/view/Zoology/HBZ-2011-000076.

Ley, P. de, & M. Blaxter. 2002. Systematic position and phylogeny. In: Lee, D. L. (ed.) The Biology of Nematodes, pp. 1-30. Taylor & Francis: Florence (Kentucky).

Megen, H. van, S. van den Elsen, M. Holterman, G. Karssen, P. Mooyman, T. Bongers, O. Holovachov, J. Bakker & J. Helder. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11 (6): 927-950.

Riemann, F. 1986. Nicascolaimus punctatus gen. et sp.n. (Nematoda, Axonolaimoidea), with notes on sperm dimorphism in free-living marine nematodes. Zoologica Scripta 15 (2): 119-124.