The Surprisingly Mysterious Eels

European eel Anguilla anguilla, photographed by Ron Offermans.

The eels are, without a doubt, one of the more distinctive groups of bony fishes, with their elongate snake-like bodies and linearised fins. And among the eels, perhaps the most familiar to many people are the freshwater eels of the genus Anguilla. Being able to wriggle across land on damp nights, eels can be found in a wide variety of water bodies, even small and isolated ones (such as cattle troughs). But the very familiarity of the freshwater eels disguises what are, in some ways, very poorly known animals.

First off, though, I have to provide something of a correction. Way back in 2007, in one of my earliest posts at this site, I made the comment that the deep sea gulper eels were 'not real eels', on the basis that they were placed in a separate order Saccopharyngiformes from the true eels of the Anguilliformes (referred to in many older texts as the Apodes, the 'legless ones'—which is a bit of a funny feature to be focusing on when talking about a fish). Witness the misleading nature of non-phylogenetic classifications! For, as turns out, phylogenetic studies have demonstrated that gulpers are indeed 'real eels', with Saccopharyngiformes well-nested among the Anguilliformes (Inoue et al. 2010). Their previous separation was due not to phylogenetic distinctiveness, but just to their individual wierdness.

New Zealand long-finned eel Anguilla dieffenbachii, photographed by Gusmonkeyboy. This species is known to grow surprisingly large: the largest on record being about 24 kg (so sayeth Wikipedia). It is generally believed that such giants are females that have, for some reason, failed to develop to reproductive maturity and instead remain as juveniles.

Anywho, back to Anguilla. This genus includes some fifteen species, most of which are found around the Pacific, with four species around the Indian Ocean and two around the North Atlantic (Lecomte-Finiger 2003). Contrary to one of the opening statements in the just-quoted review, Anguilla species are not the only freshwater eels: the Indo-Pacific moray Gymnothorax polyuranodon also enters fresh water* (Ebner et al. 2011). All freshwater eels also return to the sea to breed; this is referred to as a catadromous life-cycle (as opposed to an anadromous life-cycle as found in salmon, where the fish spend part of their lives in the sea and return to fresh water to breed**). It wasn't until the 1990s that it was discovered that some Anguilla eels spend their entire lives in the sea, and never enter fresh water (Tsukamoto et al. 1998).

*Just to confuse matters, there are also the pantropical freshwater swamp eels and spiny eels. Despite the name (and despite their superficial appearance), these are members of the percomorph radiation.

**I mention this because personally I can never remember which is which.

Marbled eel Anguilla marmorata, in the evidently excited hands of Seishi Hagihara (the eel, presumably, was somewhat less impressed). This is the only species to be found in both the Indian and Pacific Oceans.

Where the eels go once they return to the sea was long an unknown, and it wasn't until the Danish biologist Johannes Schmidt traced the leptocephalus larvae of the European eel Anguilla anguilla across the Atlantic in the early 1920s that it was realised that they travel all the way across the Atlantic to the Sargasso Sea, close to North America. Even now the breeding locations are known for only three of the fifteen Anguilla species: the European eel Anguilla anguilla and the American eel A. rostrata both breed in the Sargasso Sea, and the Japanese eel A. japonica breeds in the Marianas Trench. Molecular dating suggests that the two Sargasso species diverged between 3.8 and 1.9 million years ago, and it has still not been established how the species became distinct. Certainly such a date would be far too recent for the once-popular suggestion that they might be the descendants of an ancestral population divided by the widening of the Atlantic. There is also evidence of a hybrid zone between the two species: eels collected from Iceland, though predominantly belonging to the European species, have been shown to have 2-4% derivation from the American species.

Polynesian long-finned eel Anguilla megastoma, from Bernhard Höller. The eel in the photo is estimated to be about 12 kg in weight. Both this species and A. marmorata are found in French Polynesia: A. marmorata is found in downstream, low-gradient parts of rivers while A. megastoma is found in upstream, higher-gradient stretches. A third species in the region, A. obscura, prefers still estuaries (Lecomte-Finiger 2003).

All fifteen Anguilla species were included in the phylogenetic analysis of Anguilliformes by Inoue et al. (2010). This analysis supported a relationship of Anguilla with a clade of mesopelagic eels containing the Serrivomeridae (sawtooth eels) and Nemichthyidae (snipe eels). Sister to all of these were our old friends the gulpers. The (admittedly limited) available evidence about the habits of Anguilla during the marine phase of their life suggests that these three lineages may form a single ancestrally pelagic clade, contrasting with the near-bottom habits of most other eels (members of the Derichthyidae, the longneck eels, represent an independent origin of pelagism).

REFERENCES

Ebner, B. C., B. Kroll, P. Godfrey, P. A. Thuesen, T. Vallance, B. Pusey, G. R. Allen, T. S. Rayner & C. N. Perna. 2011. Is the elusive Gymnothorax polyuranodon really a freshwater moray? Journal of Fish Biology 79 (1): 70-79.

Inoue, J. G., M. Miya. M. J. Miller, T. Sado, R. Hanel, K. Hatooka, J. Aoyama, Y. Minegishi, M. Nishida & K. Tsukamoto. 2010. Deep-ocean origin of the freshwater eels. Biology Letters 6: 363-366.

Lecomte-Finiger, R. 2003. The genus Anguilla Schrank, 1798: current state of knowledge and questions. Reviews in Fish Biology and Fisheries 13: 265-279.

Tsukamoto, K., I. Nakai & W.-V. Tesch. 1998. Do all freshwater eels migrate? Nature 396: 635-636.

The Horns of Ammon

Goniatite of the genus Girtyoceras, showing the relatively simple zig-zag sutures of this group, from here.

Ammonites are one of the few groups of fossil invertebrates that are known to the general public as animals with coiled shells, some of them reaching significant sizes. The name Ammonites means 'image of Ammon': Ammon was an Egyptian god whose sacred animal was the ram, the curled horns of which ammonites were supposed to resemble. Ammonites were Mesozoic representatives of a larger group of cephalopods, the Ammonoidea, which also included a number of Palaeozoic lineages.

Specimen of Ceratites, a Triassic ammonoid with a greater number of suture lobes than Girtyoceras, but with the lobes still relatively simple (if you look very closely, you may be able to see small crenulations in the lobes). From Drow male.

Among extant cephalopods, only extant members of the Nautilidae, the chambered nautiluses, have permanent external shells. Nautilus shells bear a general resemblance to those of ammonoids, and as a result ammonoids have often been assumed to have resembled nautiluses in life. However, there are numerous reasons to think that this may not have been the case. Ammonoids are more closely related to the other living cephalopods, the shell-less coleoids (octopods and squid). Study of the fossil record indicates that the coiled shells of ammonoids and nautiluses are due to convergence: both groups derived separately from straight-shelled ancestors. Soft-body remains of Michelinoceras, a straight-shelled cephalopod that was related to the ammonoid + coleoid clade, suggest that ammonoids probably possessed ten relatively large tentacles like modern squid, rather than the very numerous small tentacles of a nautilus (Jacobs & Landman 1993). Jacobs & Landman (1993) also argued that ammonoids are likely to have had an expansive mantle like that of coleoids, and could probably extend the body partially out of the shell. Many ammonoids had lateral extensions of the shell at the aperture that would have required some forward extension of the mantle to grow, and some even show evidence of external shell deposition. Palaeozoic ammonoids often have a sinus on the lower edge of the aperture like that of a nautilus: in the nautilus, this marks the position of the siphon used to propel the animal. Mesozoic ammonites, however, lack such a sinus, and may have had a more dorsally placed siphon, closer to the shell's centre of buoyancy. This would have allowed more direct, steady propulsion than that of a nautilus, but would have restricted the nautilus' ability to bend the siphon and use it to propel itself forwards as well as backwards.

The ammonite Phylloceras (Goretophylloceras) subalpinum, with greatly subdivided lobes, from here.

As generally presented, the story of ammonoid evolution is the story of sutures. The septa dividing the chambers within the shells of ammonoids had a tendency to become increasingly complex over time, and the form of the sutures between septa and shell are one of the main characteristics used in distinguishing ammonoids. In many species of goniatites, one of the more basal Palaeozoic ammonoid groups, the sutures had only a small number of simple lobes. In other ammonoids, the number of lobes increased, and the individual lobes tended to develop their own complications. By the appearance of the ammonites, the sutures had become massively complicated, with almost fractal-appearing folds and folds within folds. The reasons for this complexity are uncertain: one possibility is that, if the ammonoids were more mobile than the modern nautilus, the crenulated sutures may have helped the animal in withstanding the hydrodynamic pressures involved with faster movement, by breaking up the flow of water within the body chamber (Hewitt & Westermann 2003).

REFERENCES

Hewitt, R. A., & G. E. G. Westermann. 2003. Recurrences of hypotheses about ammonites and Argonauta. Journal of Paleontology 77 (4): 792-795.

Jacobs, D. K., & N. H. Landman. 1993. Nautilus-a poor model for the function and behavior of ammonoids? Lethaia 26: 101-111.

The Corotocini in their Gut-Swollen Glory

Specimen of Thyreoxenus brevitibialis, photographed by Taro Eldredge.

Staphylinids are one of the most diverse groups of beetles out there, despite not looking like what most people would identify as beetles. But that's okay, because there are staphylinids that don't look much like what most people would identify as staphylinids, like the beautiful beasty in the photo above. Thyreoxenus brevitibialis is a member of the staphylinid tribe Corotocini, a distinctive grouping of termite inquilines.

Inquilines are animals that live in association with social insects such as ants, bees or termites. A number of staphylinid lineages have adopted the inquiline lifestyle; another group of termite inquilines, the Termitusina, was briefly covered in an earlier post. The Corotocini are the largest group of termite-inquiline staphylinids, living in association with termites of the pantropical subfamily Nasutitermitinae. Distinguishing features of the corotocins include fusion of the mentum and submentum (two plates on the underside of the head) and distinctive sensilla on the antennae (Seevers 1957). Most notable, however, is that all members of the Corotocini show some degree of physogastry, swelling of the abdomen*. In most species, the greatly inflated abdomen is recurved and held upwards, often overtopping the front part of the body (exceptions are in the subtribe Timeparthenina, in which the swelling is concentrated towards the front of the abdomen and hence it cannot be recurved). They also have relatively long legs for staphylinids, though this may be correlated with supporting their enlarged abdomens. Corotocins appear to make their living by imitating the nymphs of the termites they live amongst, and being fed and looked after by the adult termites.

*The development of the physogastric abdomen is something that may be worthy of attention. Stenogastric individuals (without swollen abdomens) have been identified for some corotocin species; for Thyreoxenus major, a series of specimens was identified by Seevers (1957) that he felt indicated that adults initially emerged as stenogastric, then developed physogastry over time. However, physogastric and stenogastric individuals differ not only in the size of the abdomen, but also in the shape and proportions of leg segments. This could be a problem, because insect growth generally doesn't work that way.

Line drawing of Timeparthenus, showing the non-reflexed abdomen. Note also how the elytra have been pushed forward above the pronotum. From Seevers (1957).

How they achieve this trick has been subject to some discussion, but is still not really resolved. Inquilines, by their very nature, tend to be uncommon and difficult to find, so many aspects of their biology remain mysterious. Many authors have assumed that the physogastric abdomen is associated with the production of chemical exudates or other substances that mimic those produced by the termite nymphs, and termitophilous staphylinids in other lineages have been shown to produce the same cuticular hydrocarbons as their termite hosts (Howard et al. 1982). However, it has been suggested that members of one particular corotocin subtribe, the Corotocina, may take the mimicry a step further. In some species of this subtribe, the abdomen is not only swollen but possesses odd sausage-like appendages:

Lateral view of Coatonachthodes ovambolandicus, from Kistner (1968).

In one species possessing such appendages, Spirachtha mirabilis, its host termites have been observed licking them, suggesting that they may be a focus for exudate production. However, Kistner (1968) suggested that they may serve a further function, the possibility of which becomes most clear when they are seen from above:

Dorsal view of Coatonachthodes ovambolandicus, from Kirstner (1968).

The appendages, together with strategically placed abdominal constrictions, may turn the beetle's abdomen into a tactile facsimile of one of the termites themselves! So close was the mimicry, Kistner felt, that he used differences between the abdomens of Coatonachthodes ovambolandicus and another corotocin, Spirachthodes madecassus, to predict morphological differences between their respective hosts. Kistner's predictions were later tested by Sands & Lamb (1975), who showed that Kistner had been both wrong and right. Workers of the host species of S. madecassus, Kaudernitermes kaudernianus, did not possess the features predicted by Kistner. However, the second-instar nymphs did! Sands and Lamb refined the mimicry hypothesis to suggest that it was the nymphs, not the workers, that the beetles were imitating. An interesting corollary of this refinement is that very young termite nymphs apparently do not yet exhibit the chemical characteristics of their home colony, so a first- or second-instar-imitating beetle would not necessarily have to mimic the host chemistry itself.

Termitophya emersoni, a less morphogically specialised corotocin, from Seevers (1957).

For those Corotocini without the abdominal appendages of the Corotocina, of course, the chemical mimicry hypothesis perhaps remains the most likely. It is worth noting, too, that tactile and chemical mimicry are not mutually exclusive. Tactile mimicry is also not exclusive of a third suggested function for the abdominal appendages, that they may function as decoys if one of the host termites was to attack the beetle, in the same way that some lizards drop their tails. Whatever the explanation, there can be no doubt that these are truly remarkable beasts.

REFERENCES

Howard, R. W., C. A. McDaniel & G. J. Blomquist. 1982. Chemical mimicry as an integrating mechanism for three termitophiles associated with Reticulitermes virginicus (Banks). Psyche 89: 157-168.

Kistner, D. H. 1968. Revision of the African species of the termitophilous tribe Corotocini (Coleoptera: Staphylinidae). I. A new genus and species from Ovamboland and its zoogeographic significance. Journal of the New York Entomological Society 76 (3): 213-221.

Sands, W. A., & R. W. Lamb. 1975. The systematic position of Kaudernitermes gen.n. (Isoptera: Termitidae, Nasutitermitinae) and its relevance to host relationships of termitophilous staphylinid beetles. J. Ent. (B) 44 (2): 189-200.

Seevers, C. H. 1957. A monograph on the termitophilous Staphylinidae (Coleoptera). Fieldiana: Zoology 40: 1-334.

The Grapsidae: From Sea to Shore

Sally Lightfoot, Grapsus grapsus, photographed by Victor Burolla. The vernacular name refers to their walking on the points of their legs.

In a post from back in 2008, I wrote about the group of crabs known as the Grapsoidea. As described in that post, the classification of the Grapsoidea has been shuffled in recent years, and the subjects of today's post, the Grapsidae, would have previously been classed as the Grapsinae within a larger Grapsidae. The more restricted Grapsidae has been supported by numerous recent analyses, both morphological (Karasawa & Kato 2001) and molecular (Schubart et al. 2000). Morphologically, grapsids are united by having an expanded anterolateral corner to the merus* of the third maxilliped, oblique ridges on the lateral surfaces of the meri of the pereiopods, and (in many species) oblique ridges on the dorsum of the carapace (Karasawa & Kato 2001). Studies of the larvae of grapsids have also identified distinctive characters by which grapsid larvae can be distinguished from those of other grapsoids (Cuesta & Schubart 1999).

*The merus is the first elongate segment of crustacean appendages, corresponding to the femur of other arthropods. The maxillipeds are feeding appendages; the pereiopods are the walking legs.

The Columbus crab Planes major, photographed by Denis Riek. This species comes in a wide range of colours, from brown to blue to almost white; the page linked to shows a number of examples.

Most grapsids are intertidal shore-dwellers, but there are some exceptions. Species of the genus Planes, known as Columbus crabs, are small oceanic forms. They live on objects floating in the open water: seaweed, driftwood and other debris, or even other animals such as by-the-wind sailors or turtles (Spivak & Bas 1999). Columbus crabs differ from other grapsids in having flattened pereiopod meri for swimming, and two of the three species lack oblique ridges on the carapace. The aforementioned phylogenetic analyses also agree in placing Planes as the sister group to other grapsids analysed.

Geograpsus grayi, from here.

Also distinctive are species of the genus Geograpsus, which are one of a number of crab groups to have developed a terrestrial lifestyle, found on islands of the Indo-Pacific and Atlantic. In the Indo-Pacific G. crinipes, it has been shown that dense bunches of setae between the second and third walking legs are long enough to contact the ground when the animal sits back on its haunches (McLay & Ryan 1990). Water on the surface of the ground is drawn up through the setae by capillary action and conducted into the gill chamber, keeping the gills damp and functioning. Terrestrial Geograpsus retain marine larvae as do many other terrestrial crabs; the larval development has been studied for the eastern Pacific G. lividus which goes through nine larval stages (eight zoeae and the megalopa) over the period of two months (Cuesta et al. 2011). This happens to be the longest developmental pathway of any known crab: the previous confirmed maximum was eight larval stages.

REFERENCES

Cuesta, J. A., G. Guerao, C. D. Schubart & K. Anger. 2011. Morphology and growth of the larval stages of Geograpsus lividus (Crustacea, Brachyura), with the descriptions of new larval characters for the Grapsidae and an undescribed setation pattern in extended developments. Acta Zoologica 92 (3): 225-240.

Cuesta, J. A., & C. D. Schubart. 1999. First zoeal stages of Geograpsus lividus and Goniopsis pulchra from Panama confirm consistent larval characters for the subfamily Grapsinae (Crustacea: Brachyura: Grapsidae). Ophelia 51 (3): 163-176.

Karasawa, H., & H. Kato. 2001. The systematic status of the genus Miosesarma Karasawa, 1989 with a phylogenetic analysis within the family Grapsidae and a review of fossil records (Crustacea: Decapoda: Brachyura). Paleontological Research 5 (4): 259-275.

McLay, C. L., & P. A. Ryan. 1990. The terrestrial crabs Sesarma (Sesarmops) impressum and Geograpsus crinipes (Brachyura, Grapsidae, Sesarminae) recorded from the Fiji Is. Journal of the Royal Society of New Zealand 20 (1): 107-118.

Schubart, C. D., J. A. Cuesta, R. Diesel & D. L. Felder. 2000. Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 15 (2): 179-190.

Spivak, E. D., & C. C. Bas. 1999. First finding of the pelagic crab Planes marinus (Decapoda: Grapsidae) in the southwestern Atlantic. Journal of Crustacean Biology 19 (1): 72-76.

Biantidae: The Importance of Titillators

An unidentified member of Biantinae, photographed in Singapore by WJ.

Long-time readers of this site will be familiar with my rants about the influence of early 20th-century arachnologist Carl-Friedrich Roewer on Opiliones taxonomy (just enter 'Roewer' into the search box near top right on this page). One of Roewer's larger errors (but an understandable one in context) involved the species he included in the family Phalangodidae. As Roewer had it, this was an almost cosmopolitan family, with representatives on all continents. However, as research has progressed, it has become clear that Roewer's Phalangodidae was a polyphyletic assemblage of a number of different lineages of relatively generic-looking Laniatores (short-legged harvestmen). Firm distinction of some of these lineages (now recognised as separate families) often requires examination of the male genitalia, something Roewer never did.

Specimen of Lacurbs, from A. B. Kury.

The Biantidae are one of these families of ex-phalangodids. They are a pantropical family, with representatives in South America, Africa and Asia. Biantids have eyes well-separated on the carapace instead of on a common central eye-mound, and they bear a strong external resemblance to another family of Laniatores that I've covered before, the South American Stygnidae. Distinguishing biantids from stygnids depends on two features: the presence of a process of the tarsi of the third and fourth legs in Stygnidae, and the presence of a ventral sclerotised plate on the penis of the Stygnidae versus no plate and dorsal processes called titillators (named for an obvious possible function) on the penis of Biantidae. However, despite the strong external similarity, stygnids and biantids are not closely related: a recent molecular phylogenetic analysis of Laniatores places them in separate superfamilies, with stygnids in the Gonyleptoidea and biantids in the Samooidea (Sharma & Giribet 2011).

Representative biantid penes, from Kury & Pérez González (2007). Left: Caribbiantes (Stenostygninae), dorsolateral view; right: Biantes sherpa (Biantinae), lateral and dorsal views. Ti = titillators; Co = conductors.

Biantidae are divided between four subfamilies (Kury & Pérez González 2007). The African genera Lacurbs and Zairebiantes are more divergent than the other two subfamilies: Lacurbs has the scutum (dorsal shield) of the opisthosoma (the rear part of the body) widest in the middle and narrowing towards the front and back, while other biantids are more or less straight-sided, and has the tibiae and metatarsi of the hind legs armed and swollen. Zairebiantes has its eyes placed closer together and further forward than other biantids, and Pinto-da-Rocha (1995) suggested that its classification as a biantid may require re-evaluation. The other two subfamilies, the South American Stenostygninae and the African and Asian Biantinae, contain the great majority of biantids and share the presence of dense scopulae (pads of hairs) on the third and fourth tarsi. Apart from their distribution, the latter two subfamilies are distinguished by genital morphology: in Stenostygninae, the titillators are rigid and sit forward to cover the capsula interna of the penis, while in Biantinae they are soft and fold back and out so that they don't cover the capsula interna.

REFERENCES

Kury, A. B., & Pérez González, A. 2007. Biantidae Thorell, 1889. In Harvestmen: The Biology of Opiliones (R. Pinto-da-Rocha, G. Machado & G. Giribet, eds) pp. 176-179. Harvard University Press: Cambridge (Massachusetts).

Pinto-da-Rocha, R. 1995. Redescription of Stenostygnus pusio Simon and synonymy of Caribbiantinae with Stenostygninae (Opiliones: Laniatores, Biantidae). Journal of Arachnology 23 (3): 194-198.

Sharma, P. P., & G. Giribet. 2011. The evolutionary and biogeographic history of the armoured harvestmen—Laniatores phylogeny based on ten molecular markers, with the description of two new families of Opiliones (Arachnida). Invertebrate Systematics 25: 106-142.

A Bizarre New Shark

Live goblin shark Mitsukurina owstoni, from here.

It's a bit unusual for me to be posting anything on a Sunday, but I've just received notice of something so incredibly cool that I couldn't wait to tell you all about it. A new paper has just come out describing a truly remarkable new species of shark:

Takahashi, N., & N. Yuasa. 2012. First recorded use of weaponised light by an elasmobranch. National Daiei Journal 7: 17-87.

The new species, Neomitsukurina nodai, is most closely related to the unusual goblin shark Mitsukurina owstoni, and the resemblance between the two is clearly visible in the head region:

Photo of the new shark species from Takahashi & Yuasa.

Nevertheless, it possesses several remarkable differences. First there is the distinctive fin array, somewhat more extensive than that found in most shark species. The denticles in the skin are much reduced, giving the body an almost rubbery appearance. Furthermore, in a remarkable case of life imitating art, Neomitsukurina differs in its jaw morphology. The vast majority of depictions of goblin sharks show it with protruding jaws but, as can be seen in the photo at the top of the post, this is not the usual appearance of this species: the jaws are generally only protruded when the shark is picking up food. In Neomitsukurina, however, the jaws are seemingly permanently protruded, and the upper jaw has been modified into a sharpened beak. The most interesting distinction of all, however, is the presence of a massively enlarged photophore on the underside of the rostrum, above the jaws:

Close-up of the head of Neomitsukurina nodai, from Takahashi & Yuasa.

The photophore contains a unique lens structure that focuses the light it produces. So strongly focused is the light, in fact, that it can be used in prey capture by the shark. Through a mechanism not yet fully understood, but possibly a shock reaction to its brightness, the light causes potential prey animals to become stunned, after which they can be easily picked off. Preliminary observations of Neomitsukurina suggest that it may be willing to take on quite large prey: even turtles have not proven immune to stunning, though the shark did not always immediately ingest stunned prey animals. Neomitsukurina has also been observed gliding above the surface of the water through the use of its enlarged pectoral fins.

It might be wondered how such a distinctive and mobile predator eluded discovery until the present, but Neomitsukurina's strict nocturnality might have something to do with it. It is also worth noting that sightings of what may, in hindsight, have been Neomitsukurina have been described in the past (a particularly famous sighting occurred in 1971, near the island of Niemonjima), but attempts to follow up such records have so far only collected other animals such as sea bass.