East Asian Forest Frogs

Black-striped frog Sylvirana nigrovittata, from here.

One group of animals that has somewhtat flown (or at least hopped) under the radar here at Catalogue of Organisms is the frogs. Frogs are perhaps one of the most instantly recognisable of all terrestrial animal groups, with a combination of features that is truly unique (see this post at an older iteration of Tetrapod Zoology for a list of some of their eccentricities—I mean, the things don't have a rib-cage. Maybe fish can get away with those sorts of shenannigans, but I expect any vertebrate crawling around on land to be fully skeletoned up, thank you.) Frogs come in a wide range of shapes and sizes, but perhaps the group most often thought of as the classic 'frogs' are the members of the family Ranidae. A large proportion of these mostly smooth-skinned, long-legged frogs were classified until recently in a single genus Rana. This was always seen as something of a generalised group, characterised as much by the absence of the derived features of other ranid genera such as the torrent-dwelling Amolops as by anything else. As such, it was long expected that more detailed studies of ranid relationships would lead to the Rana monolith being broken down somehow. In 1992, Alain Dubois presented a classification of the Ranidae in which he divided Rana between a number of subgenera, some of which were further divided into sections and species groups. This classification was presented by Dubois as explicitly provisional: the arrangement of taxa was based on overall similarities rather than any explicit analysis, and was largely intended to provide some sort of starting point for future analyses.

One of the new taxa recognised by Dubois (1992) was Sylvirana, which he erected as a new subgenus of Rana containing an assortment of species found in southern and eastern Asia. Members of this group had a foot with an external metatarsal tubercle, suction pads on digit III of the fore foot and digit IV of the hind foot but often not on fore digit I, and males with a humeral gland and internal or external subgular vocal sacs. Their tadpoles had long papillae along the edge of the lower lip, and often had dermal glands. As indicated by the name, species of Sylvirana were mostly found in forests.

Günther's frog Sylvirana guentheri, copyright Thomas Brown.

When the broad genus Rana was later carved up by Frost et al. (2006), they recognised Sylvirana as a separate genus (albeit without quite the same composition as Dubois' version). Since then, the status of Sylvirana has shifted around a bit; some authors have sunk it into a broader Old World tropical genus Hylarana on the grounds of non-monophyly. Oliver et al. (2015) conducted a molecular phylogenetic analysis of the Hylarana group that lead them to propose Sylvirana as the name for a clade of southeast Asian frogs that they recovered. A number of Indian species previously assigned to Sylvirana formed a separate clade that they recognised as a distinct genus Indosylvirana. Morphological differences between Sylvirana and Indosylvirana are slight, but males of the former have a larger humeral gland: three-quarters the length of the humerus vs two-thirds the length in Sylvirana. It's worth noting that, although Dubois (1992) recognised a number of ranid taxa as lacking a humeral gland, most if not all of them do indeed possess this gland, just not raised and readily visible externally as in Sylvirana.

The species of Sylvirana sensu Oliver et al. (2015) are generally medium-sized, robust frogs with a shagreenate back and smooth or slightly warty sides. They generally have a dark stripe along the side of the body, becoming broken into dark spots lower down. Widespread species include Sylvirana nigrovittata, commonly known as the black-striped frog (a completely non-distinct name, I have to say, considering that it could apply to any one of dozens of ranid species; Wikipedia calls it the sapgreen stream frog, which on the one hand is a much more distinctive name, but on the other hand suffers from the point that all the individuals I've seen photographed of this species look more brown than green). This species is found over pretty much the entire continental range of the genus, from eastern India and Nepal to Vietnam and Malaysia. Also widespread is Günther's frog S. guentheri, which is found in southern China, Taiwan and Indochina. This species is also found in Guam where it was first recorded in 2001 and has since become well-established (Christy et al. 2007). It is believed to have made its way there as a stowaway in shipments of aquaculture stock though, as it is itself captured for food in its native range, it is not impossible that it may have been introduced deliberately.

REFERENCES

Christy, M. T., J. A. Savidge & G. H. Rodda. 2007. Multiple pathways for invasion of anurans on a Pacific island. Diversity and Distributions 13: 598–607.

Dubois, A. 1992 Notes sur la classification des Ranidae (Amphibiens Anoures). Bulletin Mensuel de la Société Linnéenne de Lyon 61 (10): 305–352.

Frost, D. R., T. Grant, J. Faivovich, R. H. Bain, A. Haas, C. F. B. Haddad, R. O. de Sá, A. Channing, M. Wilkinson, S. C. Donnellan, C. J. Raxworthy, J. A. Campbell, B. L. Blotto, P. Moler, R. C. Drewes, R. A. Nussbaum, J. D. Lynch, D. M. Green & W. C. Wheeler. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370.

Oliver, L. A., E. Prendini, F. Kraus & C. J. Raxworthy. 2015. Systematics and biogeography of the Hylarana frog (Anura: Ranidae) radiation across tropical Australasia, Southeast Asia, and Africa. Molecular Phylogenetics and Evolution 90: 176–192.

Harvestmen and their Hairy Pedipalps

A selection of harvestmen, showing a variety of pedipalpal morphologies, from Wolff et al. (in press). The upper two are Laniatores with spiny pedipalps; the lower two are Palpatores with leg-like pedipalps.

Wolff, J. O., A. L. Schönhofer, J. Martens, H. Wijnhoven, C. K. Taylor & S. N. Gorb (in press) The evolution of pedipalps and glandular hairs as predatory devices in harvestmen (Arachnida, Opiliones). Zoological Journal of the Linnean Society.

I'm happy to say that a new paper on which I am an author has just been made available. It's been a while (long-term unemployment has not profited my publication record, I must admit), but there are a few things still bubbling below the surface. This last entry is a study of the evolution of harvestmen's pedipalps, the more-or-less leg-like appendages on either side of the mouth that they use for collecting, capturing and manipulating food, and particularly the sticky hairs that many harvestmen have on them. My part in this publication was fairly minimal: I provided specimens and data on Neopilionidae, and assisted with the English-language composition. Full credit goes to my co-authors, particularly our lead author Jonas Wolff who drove it all.

I've learnt some interesting things myself working on this paper. When I first started researching harvestmen, most of the sources I read described them as scavengers, content to get by on decaying remains that they chanced upon in their wanderings. For some harvestman species, that is indeed their chosen diet. But some other species are not content with mere leavings, preferring their meat fresh and wriggling. These species are active predators, using their pedipalps to seize springtails and other small invertebrates. As a result of their use for this and other activities, harvestmen pedipalps show a wide range of shapes and sizes: some simple and presumably multi-purpose, others strikingly modified. Many species (particularly within the Laniatores, or 'short-legged' harvestmen) carry long spines on the pedipalps, and one might presume these to be the more blood-thirsty harvestmen. But, as reported by Wolff et al., there are many species no less active in their hunting (if not even more so) that not only have their pedipalps unadorned with spines but have even lost or reduced the claws that usually tip the pedipalps. What is going on here?

The answer lies in these species' possession of an alternative to spines: glandular setae. These are little hairs attached to a gland secreting a sticky glue that sits in a globule on a cluster of micro-hairs at the end of the seta, and are found in various species of the Palpatores ('long-legged' harvestmen). In some species the micro-hairs may be on one side, like a tooth- or a boot-brush; in others they may form a ring around the end. Using glue to capture prey can be even more effective than using spines or claws: springtails and such are often covered with scales or other loose structures that can slide off when the animal is seized, allowing the prey to escape and leaving the would-be predator with a handful of dust. Attacking the prey with multiple points of sticky glue, however, increases the chance of holding onto it, as the glue works around the scales and adheres to the body.

Two harvestmen showing convergent 'tentacle' pedipalps, the dyspnoan Mitostoma chrysomelas on the left and the ballarrine Ballarra longipalpis on the right, from Wolff et al. (in press).

Most harvestmen have not gone the whole hog for glandular setae; there is presumably scope for compromise with the use of the pedipalps for other purposes such as mating (the genital opening for harvestmen is around the mid-point of the underside of the body, so harvestmen mate 'face-to-face' and may use the pedipalps to hold onto each other). Many Palpatores possess a smattering of glandular setae at certain points on the inner side of the pedipalps only, and otherwise have a fairly underived leg-like pedipalp with a well-developed claw. One particularly interesting example that I hadn't heard of before was the Asian species Metagagrella minax, which possesses glandular setae as a juvenile but progressively loses them as it matures. Nevertheless, there are two groups, the Dyspnoi and Ballarrinae, that possess what Wolff et al. dub the 'tentacle' form of pedipalp: the pedipalps are elongate with glandular setae along the entire length and lack the claw entirely. The Dyspnoi is a purely Northern Hemisphere lineage, whereas the Ballarrinae are restricted to the Southern Hemisphere. The two groups sit nested on opposite sides of the primary divide within Palpatores, so there is no question that the 'tentacle' pedipalp has evolved independently in the two groups (which is also reflected by differences in each in the relative proportions of the segments making up the pedipalp). However, there is a bit of a question about whether the 'tentacle' has appeared even more often: Wolff et al. assume a single origin of the Ballarrinae but this has recently been cast into doubt. This is a question that interests me directly because of something else I've currently got on the boil... but that's a topic for another day.

Hagfish: Probably the World's Most Disgusting Vertebrates

South African hagfish Myxine capensis, copyright Andy Murch.

I say "probably" not the title not because there's any question about whether hagfish are disgusting–they are, they really are–but because there's been some debate in the past about whether hagfish are vertebrates. Hagfish, as you may already know, are superficially eel-like marine animals that, together with the lampreys, are one of the two living lineages of 'jawless fish'. Their skeleton is both completely cartilaginous decidedly rudimentary: they even lack a developed spine, instead retaining the fluid-filled notochord throughout their life. They do possess a brain-case, as well as some appendicular cartilages that provide support for the fins. Around the mouth are a set of muscularly-controlled tooth-plates together with short sensory tentacles. Hagfish have no eyes; instead, they find their way about primarily through the use of a single large nostril in the middle of the head. Along the underside of the body run a series of glands capable of producing a truly mind-bending amount of mucus. As noted by Martini & Flescher (2002), "A single live individual hagfish can turn a 2 gallon pail of water into a gelatinous mass within a few minutes". Most hagfish seem to be in the one or two feet range size-wise, but the New Zealand species Eptatretus goliath was described from a single monster specimen a bit over 1.25 metres long (Mincarone & Stewart 2006). In contrast, the hydrothermal vent inhabitant Eptatretus strickrotti is only just over a foot long and built like a swimming shoelace (Møller & Jones 2007).

A demonstration of a hagfish's slime-producing capabilities, copyright Andra Zommers.

Martini & Flescher (2002) summarised the lifestyle of the Atlantic hagfish Myxine glutinosa (or probably the western Atlantic hagfish M. limosa which they regarded as synonymous with the eastern Atlantic M. glutinosa), which I'm guessing is fairly typical of the group. Atlantic hagfish spend most of their lives buried in burrows in muddy sea-bottoms (the technical term for the type of sediment they prefer is 'flocculent', which is a wonderful word to say), emerging primarily to feed. A large part of their diet is obtained by predating small animals such as crustaceans. They are most notorious, though, as scavengers. Hagfish will emerge in large numbers to feed on any animal corpses that sink within their range. Though they are capable of tearing off external chunks of flesh (more on that in a moment), they are not able to do so efficiently so they prefer to focus on the softer internal organs when they can. This they do by worming their way into the carcasse through a convenient orifice such as the mouth or anus and enjoying the laid-on buffet within. The reproduction of hagfish is poorly known. The Royal Academy of Copenhagen offered an award in 1864 to the first person to describe the details of hagfish nooky; the offer was withdrawn in the 1980s, still unclaimed. Female hagfish have been caught with developing eggs, up to 30 at a time, connected in a string by velcro-like hooks. The absence of any sort of obvious intromittent organ in the male suggests that fertilisation is external, but anything beyond that is a mystery.

Their lack of a rigid skeleton makes hagfish capable of some behaviours that would be beyond other vertebrates. One of these is referred to as 'knotting' and it is exactly what it sounds like. The hagfish makes a loop with its body through with it sticks its tail, quite literally tying itself in a knot. By pulling itself through itself, it can move the knot up the body until the head pops out at the other end. One reason it may do this is to clean itself; for instance, a hagfish may drown in its own mucus if not given the opportunity to remove it (so that single live individual in the two-gallon bucket is probably not live any more). Another reason is that the knot can be used to push against something, such as when the hagfish wants to escape from an enclosed space. When feeding on something large and solid (such as the aforementioned external scavenging), the hagfish will latch on with its tooth-plates and then form a knot to push against it until eventually it tears away with a mouthful of food.

Hagfish can be abundant in some areas, make them an important part of the local ecosystem. They may be regarded as a nuisance in fisheries, attacking fish caught on lines and traps and reducing their commercial value. However, hagfish are also caught for food in some parts of the world (particularly in east Asia) and their skins are cured to produce a soft textile known somewhat euphemistically as 'eelskin'.

Pacific hagfish Eptatretus stoutii, photographed by Linda Snook.

About sixty species of hagfish are currently recognised around the world, usually classified in a single family Myxinidae. Most are divided between two subfamilies (sometimes recognised as separate families), the Myxininae and Eptatretinae. Myxininae have a single external gill opening whereas Eptatretinae have multiple gill openings. A phylogenetic analysis of the hagfish by Fernhom et al. (2013) found a couple of species previously assigned to Eptatretus to probably sit outside the Myxininae-Eptatretinae clade and transferred them to a new genus Rubicundus in its own small subfamily, differing from other hagfish in having the single nostril on a short tubular snout.

As alluded to above, there has been some debate about the affinities of hagfish. Though superficially similar to the other living group of 'jawless fishes', the lampreys (largely through both being eel-like in form), hagfish are very different in the anatomical details, and at the very least the two lineages have been separate for a very long time. Because of their lack of a number of derived features, hagfish were suggested to be the sister lineage of all other vertebrates, leading to the observation that it was not really appropriate to classify a lineage that did not have and probably never had vertebrae as 'vertebrates'. As such, hagfish became regarded as the closest relatives of vertebrates rather than vertebrates themselves. However, molecular studies of vertebrate phylogeny have pretty much universally identified hagfish as forming a clade with lampreys after all, implying that the 'primitive' features of hagfish probably represent secondary losses. When constrained as a clade in morphological analyses, nevertheless, the hagfish-lamprey group remains basal in vertebrates: most if not all of the fossil groups of 'jawless fish', particularly those with an outer covering of bony plates, are more closely related to the jawed fishes than to hagfish or lampreys.

The most likely fossil hagfish (and even then it's not much), Myxinikela siroka, copyright RCFossils.

Not surprisingly for something without much of a skeleton, the fossil record of hagfish is pretty minimal. A species from the Carboniferous Mazon Creek lagerstätte, Myxinikela siroka, is likely to be a stem-hagfish; a couple of other fossils from the same formation have also been suggested as candidates. Myxinikela was broadly similar to a modern hagfish, the most obvious difference being that it was shorter and more cigar- or banana-shaped than eel-like (I can't really imagine it being able to tie itself in knots). Some authors have also suggested similarities between the braincase of hagfish and that of Palaeospondylus, an unusual eel-like vertebrate from the Middle Devonian of Scotland whose confusing assortment of features has lead to it being seen at one time or another as a jawless fish, a degenerate bony fish that failed to develop bone, or even a larval amphibian (Janvier 2015). The most obvious difference between Palaeospondylus and a hagfish is that Palaeospondylus possessed a complete cartilaginous skeleton, but the molecular phylogenies suggest that may not be the problem it would have previously been assumed to be...

REFERENCES

Fernholm, B., M. Norén, S. O. Kullander, A. M. Quattrini, V. Zintzen, C. D. Roberts, H.-K. Mok & C.-H. Kuo. 2013. Hagfish phylogeny and taxonomy, with description of the new genus Rubicundus (Craniata, Myxinidae). Journal of Zoological Systematics and Evolutionary Research 51 (4): 296–307.

Janvier, P. 2015. Facts and fancies about early fossil chordates and vertebrates. Nature 520: 483–489.

Martini, F. H., & D. Flescher. 2002. Hagfishes. Family Myxinidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder's Fishes of the Gulf of Maine 3rd ed. pp. 9–16. Smithsonian Institution Press: London.

Mincarone, M. M., & A. L. Stewart. 2006. A new species of giant seven-gilled hagfish (Myxinidae: Eptatretus) from New Zealand. Copeia 2006 (2): 225–229.

Møller, P. R., & W. J. Jones. 2007. Eptatretus strickrotti n. sp. (Myxinidae): first hagfish captured from a hydrothermal vent. Biol. Bull. 212: 55–66.

Small Waters

Female Bryocamptus minutus, from here.

For this week's semi-random post topic, I drew the copepod genus Bryocamptus. Copepods have made an appearance on this site before (see here, here and here), seeing as these minute crustaceans inhabit almost all the world's waters. Bryocamptus belongs within the harpacticoids, one of the three main groups of free-living copepods (the others are the calanoids and cyclopoids), and like other harpacticoids members of this genus have a more-or-less parallel-sided, somewhat wormlike form, though Bryocamptus species are shorter than some. Within the harpacticoids, this genus belongs to the family Canthocamptidae, members of which have the first segment of the body bearing swimming legs fused to the cephalothorax (Caramujo & Boavida 2009).

There are over 100 recognised species of Bryocamptus, found in a wide range of fresh-watery habitats (Lee & Chang 2006). They may be found in mountain streams, in springs and temporary pools, or in subterranean groundwaters. Some may even be found 'terrestrially', living in the water film around leaf-litter, mosses or within the soil (Fiers 2013). One type of habitat that I haven't found reference to Bryocamptus living in is larger water bodies such as lakes. This is not particularly unusual: nutrients and micro-organisms tend to accumulate along boundaries, so habitats with a high proportion of edges tend to attract a higher diversity than the relative deserts that are larger water bodies.

Sometimes these habitats can be very small indeed. Groundwater species, for instance, may be restricted to the cracks within formations only some tens of metres in extent. Cottarelli et al. (2012) described Bryocamptus stillae from Conza Cave near Palermo in Sicily. This species was found in seasonal rimstone pools within the cave: temporary pools that would be filled by water dripping from the ceiling during the winter, only to dry up in the summer. However, the copepods are unable to survive out of water, and canthocamptids do not have a resistant phase in their life cycle that could survive the ppols drying out. Cottarelli et al. therefore inferred that the pools were not the copepods' primary habitat; rather, the copepods normally lived in the epikarst, the layer of limestone above the cave. Despite being only a few metres thick, this limestone layer retained enough pockets of moisture to provide a home for the copepods. During the rainy season, when water was more actively flowing through the epikarst, some of the more unfortunate copepods would be carried by the water as it dripped through the cave ceiling into the pools below. They would survive (and even breed) so long as the pools remained wet but they would be doomed to die off over the summer, with the following year's copepods representing an entirely new batch. Interestingly, though, Cottarelli et al. found B. stillae in only one group of pools in the cave. In a second group of pools, only about ten or fifteen metres away, an entirely different copepod species was found. Cottarelli et al. collected in the cave over three separate seasons, and each time the same species was found in the same pools. The evidence indicated that, even though these pools were so close, the water dripping into them came from separate, isolated epikarst formations, each one home to its own species of highly localised copepods.

REFERENCES

Caramujo, M.-J., & M.-J. Boavida. 2009. The practical identification of harpacticoids (Copepoda, Harpacticoida) in inland waters of central Portugal for applied studies. Crustaceana 82 (4): 385–409.

Cottarelli, V., M. C. Bruno, M. T. Spena & R. Grasso. 2012. Studies on subterranean copepods from Italy, with descriptions of two new epikarstic species from a cave in Sicily. Zoological Studies 51 (4): 556–582.

Fiers, F. 2013. Bryocamptus (Bryocamptus) gauthieri (Roy, 1924): a Mediterranean edaphic specialist (Crustacea: Copepoda: Harpacticoida). Revue Suisse de Zoologie 120 (3): 357–371.

Lee, J. M., & C. Y. Chang. 2006. Taxonomy on freshwater canthocamptid harpacticoids from South Korea V. Genus Bryocamptus. Korean J. Syst. Zool. 22 (2): 195–208.

These Ants Must Be Crazy

Black or longhorn crazy ant Paratrechina longicornis, copyright Efram Goldberg.

I have to admit that my ant-identifying skills are fairly rudimentary. I can recognise some of the more distinctive and/or common varieties—meat ants, bull ants, strobe ants, maybe even green-headed ants—but that's about as far as it goes. One ant species that I would have a decent chance of recognising right off the bat, however, is the black crazy ant Paratrechina longicornis.

Black crazy ants are an excellent example of what ant experts refer to as 'tramp species'—generalist species that have spread over a wide range in association with humans. Indeed, the black crazy ant is believed to be the most widespread of all ant species (Wetterer 2008): in tropical regions, it is nigh-on ubiquitous, and in cooler regions it lives within buildings and other warm structures built by humans. So widespread is it, and so readily does it spread, that we can't say for absolute certain where it originally came from: most likely it originated somewhere in south-east Asia, but other possibilities have been considered over the years.

Black crazy ants belong to the ant subfamily Formicinae; as such, they lack the sting carried by ants of other subfamilies and instead have a nozzle-like pore in its place that they use to spray formic acid at perceived threats. They are distinguished from other ants by their slender appearance, with numerous upright bristles on the body, and long legs and antennae. The antennae are most distinctive, with a particularly long scape (the first antennal segment, before the sharp 'elbow'). Paratrechina longicornis are known as 'crazy' ants because of their erratic mode of foraging, wandering about seemingly aimlessly and not following clear trails. Other ants with similar modes of behaviour have also been dubbed crazy ants, such as the yellow crazy ant Anoplolepis gracilipes, but they are not close relatives.

Effectiveness in numbers: black crazy ants bring down a Florida carpenter ant Camponotus floridanus, from AntWeb.

Black crazy ants may form large or small colonies as circumstances allow; part of the secret of their success is that these colonies can be found in man-made marginal habitats such as on ships at sea. Crazy ant colonies may reach plague proportions; this website relates an account of students at a Florida primary school being so beset by crazy ants that food and other possessions had to be kept in sealed bags on tables at all times with the table legs set in bowls of water to prevent the ants crawling up them. Black crazy ants produced winged reproductives like other ants, but the new queens remove their wings before they expand and emerge from the nest already wingless. While at first glance this seems counter-productive, I can see this behaviour being another factor in their success as a tramp. Colonies living in isolated habitatssuch as the aforementioned ships and buildings in cold climates will tend to persist in that location, rather than losing all their reproductive potential in fruitless exploratory nuptial flights.

In recent times, P. longicornis has been recognised as one of a number of species in the genus Paratrechina (of which it is the effective type). However, a phylogenetic study by LaPolla et al. (2010) of the group of genera to which Paratrechina belongs has found that the genus as then recognised was polyphyletic. Rather than being directly related to other 'Paratrechnina', P. longicornis was most closely related to two south-east Asian genera Euprenolepis and Pseudolasius. This lead to the resurrection of two older generic names, Nylanderia and the cringe-inducingly named Paraparatrechina, into which all Paratrechina species other than P. longicornis were transferred.

REFERENCES

LaPolla, J. S., S. G. Brady & S. O. Shattuck. 2010. Phylogeny and taxonomy of the Prenolepis genus-group of ants (Hymenoptera: Formicidae). Systematic Entomology 35: 118–131.

Wetterer, J. K. 2008. Worldwide spread of the longhorn crazy ant, Paratrechina longicornis (Hymenoptera: Formicidae). Myrmecological News 11: 137–149.