Field of Science

Blue Moon

Male blue moon butterfly Hypolimnas bolina, photographed by Comacontrol.


My native country of New Zealand is not home to a large diversity of butterflies. Only a couple of dozen or so species are known from the entire country. It would not be unreasonable for a keen butterfly spotter to attempt to track down them all. But one particular species of butterfly generally included in New Zealand lists would a touch of luck: the aptly named blue moon Hypolimnas bolina.

This is because the blue moon is not a regular resident of New Zealand (I've personally never spotted one). It is native to a wide region stretching from Madagascar and India to Japan and northern Australasia where it is usually referred to by the more prosaic name of common or greater eggfly. The only examples found in New Zealand are vagrants who lost their way on southwards migrations. Nevertheless, such vagrants are regular enough for its local appellation to be thought worth coining. Not only does it reflect their rarity, it also describes the appearance of the male, with the wings bearing blue-ringed white spots on a black background.

Two females of Hypolimnas bolina. On the left, a mimetic individual, copyright Greg Hume; on the right, a non-mimetic individual, copyright W. A. Djatmiko.


The appearance of the female is a bit harder to explain because it can vary between individuals. Females of the eggfly genus Hypolimnas are commonly mimics of other, poisonous butterflies of the subfamily Danainae, to which eggflies are only distantly related (both groups belong to the family Nymphalidae but eggflies are placed in the subfamily Nymphalinae). For instance, the diadem or danaid eggfly H. misippus of Africa and Asia (and also introduced into parts of the Americas adjoining the Caribbean) is a mimic of the plain tiger Danaus chrysippus. The chosen model of H. bolina in the western part of its range is the common crow Euploea core and in the region of India almost all females are a remarkably good copy of that species (above left). But as one moves east, one starts seeing females of H. bolina that are not mimics like the individual shown above right; by the time one reaches Australia these make up the greater part of the population. Mimetic females may also vary to resemble different Euploea species, depending on which model is locally present.

Female danaid eggfly Hypolimnas misippus, copyright Raju Kasambe. Males of this species are similar to those of H. bolina but lack the blue rings around the white spots on the wings.

There are about two dozen species of Hypolimnas eggflies found in various parts of the Old World tropics. Hypolimnas misippus is also found in parts of the Americas around the Caribbean where its presence is usually explained as the result of an early introduction (possibly, and somewhat poignantly, in connection to the slave trade). Their vernacular name is probably derived from the unique behaviour (for butterflies) of a number of species whose females stand guard over their eggs, beating their wings over them to protect them from predators until hatching. About two-thirds of Hypolimnas species are mimics. In some of these species, both sexes are mimetic; others resemble H. bolina and H. misippus in that only the females are mimics (Vane-Wright et al. 1977). One might be tempted to ask why this variation exists. One point to be considered is that there are limits on when mimicry is likely to be effective. The mimic needs to be much less abundant than its model, otherwise potential predators may not learn to associate the distinctive coloration with the toxic original. Swinhoe (1896) noted that males of Hypolimnas misippus were very active, aggressively defending their territories from other butterflies, and suggested that this agility might provide males with alternative defences to mimicry. The more sedentary females (especially when egg-guarding) might be expected to benefit more from the passive protection mimicry provides, but mimesis might be expected to disappear in areas where their model is less abundant.

REFERENCES

Swinhoe, C. 1896. On mimicry in butterflies of the genus Hypolimnas. Journal of the Linnean Society, Zoology 25: 339–348.

Vane-Wright, R. I., P. R. Ackery & R. L. Smiles. 1977. The polymorphism, mimicry, and host plant relationships of Hypolimnas butterflies. Zoological Journal of the Linnean Society 9: 285–297.

False Spider Mites

Among the enormous diversity of the world's mites, some families are particularly notorious for the damage that they inflict on commercial plant crops. Among such Acari non grata are the spider mites of the family Tetranychidae or the gall mites of the Eriophyidae. But a third, equally notorious group is the false spider mites or flat mites of the Tenuipalpidae.

Red and black flat mite Brevipalpus phoenicis, false-colour SEM by Christopher Pooley.


False spider mites include about 800 known species of more or less flattened, slow-moving mites. They are closely related to the true spider mites and both families have the chelicerae modified into a pair of long, whip-like retractable stylets that are used to pierce and suck fluids from plant tissues. In the case of the false spider mites, though, their commercial infamy comes not only from the direct damage caused by the feeding mites themselves but also from the effects of transmitted viruses. Viruses transmitted by false spider mites include the causative agents of diseases such as citrus leprosis and coffee ring spot and may cause significant reductions in the yield and lifespan of infected plants.

Morphologically, false spider mites differ from true spider mites in the absence of what is called the 'thumb-claw' process, an arrangement of the tarsus of the pedipalp alongside a claw on the seta (hence the family name which means 'slender palp'). The palps are often reduced, with some species having only the barest remnant. Some species also show reduction in the fourth pair of legs, and females of a number of species are six-legged as adults. This merely stands as another example of how mite morphology functions purely to play silly buggers with anything one might learn in basic animal biology.

Hebe stem gall mites Dolichotetranychus ancistrus inside an open gall, copyright Plant and Food Research.


Parthenogenesis is also common in false spider mites. Species found in cooler climes will often overwinter as females, with a new generation of males not appearing until the next spring. In some species, eggs produced parthenogenetically will hatch into males; in others, they will produce females. A few species almost entirely lack functional males. A small group of these species in the genus Brevipalpus is unique among animals in being both parthenogenetic and genetically haploid.

Almost all forms of seed plant seem to be vulnerable to some form of flat mite or another; some mite species are very catholic in their tastes and will latch onto almost anything green and photosynthesising. Others are more discerning. How false spider mites make their way from one host plant to another is little known but they may be passively carried through the air on the wind. Alternatively, they may be inadvertently carried from place to place by feeding herbivores, or by the very human horticulturalists that suffer so much from their presence.

REFERENCE

Walter, D. E., E. E. Lindquist, I. M. Smith, D. R. Cook & G. W. Krantz. 2009. Order Trombidiformes. In: Krantz, G. W., & D. E. Walter (eds) A Manual of Acarology 3rd ed. pp. 233-420. Texas Tech University Press.

Oily and Salty Trees

The Annonaceae is another one of those plant families like Acanthaceae that, despite containing a high diversity of speceis, tend to be overlooked because that diversity is mostly tropical. A number of species in the type genus Annona produce commercially significant fruits: custard apples, cherimoyas, soursops and the like. However, these are just a few of the 2400+ species of trees and lianes assigned to this family.

Ylang-ylang flowers Cananga odorata, from here.


Taxonomically, the Annonaceae is well established as distinct, readily recognised by a number of distinctive features. Among these is a characteristic 'cobweb' appearance to the wood structure when seen in cross-section, resulting from prominent rays of xylem connected by narrow cross-bands of parenchyma (Chatrou et al. 2012). Relationships within the family have been much harder to work out, not becoming well established until the advent of the molecular era. Recently, Chatrou et al. (2012) have recognised four subfamilies within the Annonaceae. The majority of species are placed in the subfamilies Annonoideae and Malmeoideae (which together form a clade), but a handful of species are placed in two basal subfamilies: one for the single genus Anaxagorea, and the Ambavioideae. Anaxagorea and the ambavioids differ from the annonoid-malmeoid clade in the structure of their seeds. Seeds of Annonaceae have what is called ruminate endosperm: that is, the surface of the endosperm is not smooth, but divided by wrinkles and grooves (the term 'ruminate' literally means 'chewed'). In Annonoideae and Malmeoideae, the ruminations of the endosperm are shaped like spines or lamellae. In Anaxagorea and the Ambavioideae, the ruminations are irregular in appearance. Molecular analyses place Anaxagorea as the sister taxon to all other Annonaceae.

View into the canopy of a salt-and-oil tree Cleistopholis patens, copyright Marco Schmidt.>


The Ambavioideae, despite not being very diverse, are widespread, with species found in the tropics of Africa, Asia and the Americas. Perhaps the best known ambavioid is the ylang-ylang tree Cananga odorata, native to south-east Asia, whose flowers are used as a source of perfume. Other south-east Asian ambavioids belong to the genera Cyathocalyx, Drepananthus and Mezzettia. The type genus, Ambavia, is native to Madagascar; other ambavioids in the genera Meiocarpidium, Cleistopholis and Lettowianthus are found in continental Africa. Finally, a single genus Tetrameranthus is found in South America. Most species of ambavioid are not systematically economically exploited but a number are locally used as sources of wood. The wood is light and not suitable for structural uses, but can be shaped and finished for utensils and other small items. The West African species Cleistopholis patens, whose Ghanaian name has been translated as 'salt and oil tree' (in reference to the taste of the bark when chewed), provides a fibrous bark that is readily stripped from the tree and is used for such purposes as matting and carrying straps (see here).

REFERENCES

Chatrou, L W., M. D. Pirie, R. H. J. Erkens, T. L. P. Couvreur, K. M. Neubig, J. R. Abbott, J. B. Mols, J. W. Maas, R. M. K. Saunders & M. W. Chase. 2012. A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Botanical Journal of the Linnean Society 169: 5–40.

Hydromantes: Salamanders in Different Places

There are times when biogeography is able to throw us some real puzzlers: organisms whose distribution seems to defy expectations. Among these mysteries, special mention must be made of the salamanders of the genus Hydromantes.

Gene's cave salamanders Hydromantes genei courting, copyright Salvatore Spano.


Hydromantes is a genus containing a dozen species from among the lungless salamanders of the family Plethodontidae. Plethodontids are the most diverse of the generally recognised families of salamanders, with over 450 known species found mostly in Central and South America. Hydromantes, however, is a geographically isolated genus in this family with its species found in two widely separated regions: California in western North America, and mainland Italy and Sardinia in Europe. Though some authors have advocated treating the species found on each continent as separate genera, both morphological and molecular studies have left little doubt that the group represents a discrete clade.

Distinctive features of Hydromantes compared to other plethodontids include feet with five, partially webbed toes and a weakly ossified, flattened skull (Wake 2013). Members of this genus capture prey with a projectile tongue which is the most extensive of any amphibian, extending up to 80% of the animal's total body length (Deban & Dicke 2004). There are some differences between North American and European species notable enough for the recognition of separate subgenera (there is something of a gigantic clusterfuck surrounding the names of said subgenera but the details are far too tedious to relate here). The three North American species of the subgenus Hydromantes have bluntly tipped tails that they use as a 'fifth leg' when navigating smooth and/or slippery surfaces, whereas the European species have unremarkable pointed tails. Historically, the North American Hydromantes species have been poorly known, being isolated to restricted ranges. Hydromantes shastae is found in limestone around Lake Shasta whereas H. brunus is found in a small area of mossy talus habitat along the Merced River in the foothills of the Sierra Nevada (Rovito 2010). The third species, H. platycephalus, is found at higher altitudes in the Sierra Nevada, well over 1000 m above sea level. Individuals found living on steep slopes are known to escape predators by tightly coiling their bodies and simply rolling down the slope (García-París & Deban 1995). A molecular analysis of H. platycephalus and H. brunus by Rovito (2010) identified the former species as derived from within the latter, and Rovito suggested that H. brunus may have originated in a remnant population from when H. platycephalus moved into lower altitudes during the Ice Age.

Mt Lyell salamander Hydromantes platycephalus, copyright Gary Nafis.


The seven or eight European species are mostly placed in the subgenus Speleomantes; a single species, Hydromantes genei, is divergent enough to be placed in its own subgenus Atylodes (though most recent studies have indicated that the European Hydromantes overall form a discrete clade). Hydromantes genei and three species of Speleomantes are found in caves on the island of Sardinia; the remaining Speleomantes species on mountains of mainland Italy. Molecular analysis suggests that H. genei became isolated on Sardinia about nine million years ago, with the ancestors of the Sardinian Speleomantes arriving later about 5.6 million years ago when the Mediterranean dried out during what is known as the Messinian Salinity Crisis (Carranza et al. 2008). The absence of any Hydromantes on neighbouring Corsica is something of a mystery, and it has been suggested that they may have been present there in the past before going extinct.

Extinction also seems the most likely explanation for Hydromantes' unusual distribution. The fossil record for the genus is minimal, and provides little information not already available from living species, but molecular dating attempts agree that the division between European and North American Hydromantes happened too recently to be related to the tectonic separation of the two continents. Such a scenario would also leave open the Hydromantes' absence in eastern North America. The description in 2005 of the Korean lungless salamander Karsenia koreana demonstrated the presence of plethodontids in eastern as well as far western Eurasia, and it seems possible that Hydromantes dispersed into Eurasia via the Bering Strait landbridge, becoming widespread across the continent before extinction reduced it to the isolated relicts it is today.

REFERENCES

Carranza, S., A. Romano, E. N. Arnold & G. Sotgiu. 2008. Biogeography and evolution of European cave salamanders, Hydromantes (Urodela: Plethodontidae), inferred from mtDNA sequences. Journal of Biogeography 35: 724–738.

Deban, S. M., & U. Dicke. 2004. Activation patterns of the tongue-projector muscle during feeding in the imperial cave salamander Hydromantes imperialis. Journal of Experimental Biology 207: 2071–2081.

García-París, M., & S. M. Deban. 1995. A novel antipredator mechanism in salamanders: rolling escape in Hydromantes platycephalus. Journal of Herpetology 29 (1): 149–151.

Rovito, S. M. 2010. Lineage divergence and speciation in the web-toed salamanders (Plethodontidae: Hydromantes) of the Sierra Nevada, California. Molecular Ecology 19: 4554–4571.

Wake, D. B. 2013. The enigmatic history of the European, Asian and American plethodontid salamanders. Amphibia-Reptilia 34: 323–336.

Leucicorus: FAKE EYES!

In an earlier post, I told you about the fishes known as brotulas. These are one of the most prominent groups of fish in the deep sea. They tend not to be attractive fish: their lack of outstanding dorsal and tail fins makes them look like something between an eel and a cod, and like many deep-sea fishes they look somewhat flabby and lumpish. There are numerous genera of brotulas out there; the individual in the photo below represents the genus Leucicorus.

Leucicorus atlanticus, from Okeanos Explorer.


Leucicorus belongs to the brotula family Ophidiidae, commonly known as the egg-laying brotulas though Leucicorus' own reproduction has (so far as I have found) not been directly observed. The feature that most immediately sets Leucicorus apart from other brotulas is the eyes: Leucicorus species have very large eyes but the actual lenses are rudimentary or absent (Cohen & Nielsen 1978). It almost looks like they grew bigger and bigger to cope with the low light of the deep sea before they just kind of gave up at some point.

Two species of Leucicorus are currently recognised, each known from separate parts of the world. Leucicorus lusciosus is found in the eastern Pacific, whereas L. atlanticus is known from around the Caribbean. The two species differ in meristic characters and proportions: for instance, L. lusciosus has more dorsal and anal fin rays, but fewer vertebrae and gill rakers, and has a deeper body (Nielsen & Møller 2007). Leucicorus has also been found in the vicinity of the Solomon Islands, but interestingly enough Nielsen & Møller (2007) identified the specimen found as L. atlanticus rather than L. lusciosus, despite the latter species' more proximate distribution. One wonders if perhaps a third species is involved, yet to be recognised.

REFERENCES

Cohen, D. M., & J. G. Nielsen. 1978. Guide to identification of genera of the fish order Ophidiiformes with a tentative classification of the order. NOAA Technical Report NMFS Circular 417.

Nielsen, J. G., & P. R. Møller. 2007. New and rare deep-sea ophidiiform fishes from the Solomon Sea caught by the Danish Galathea 3 Expedition. Steenstrupia 30 (1): 21–46.

Pontodrilus: Earthworms by Sea

Earthworms are primarily a terrestrial and freshwater group, sensitive to changes in the quality of their habitat. But there are some earthworm species that are tolerant of more saline environments. One such species is Pontodrilus litoralis, a widespread earthworm found in warm coastal habitats around the world, being recorded from such far-flung places as the Caribbean, the Mediterranean, Australia and Japan. The species is found in sandy or muddy soils in coastal habitats, including beaches, estuaries and around the roots of mangroves, and is able to tolerate salinities from 5 to 25 parts per thousand—that is, from fresh water to close to the standard salinity of sea water (Blakemore 2007).

Pontodrilus litoralis in its natural habitat, from here.


Pontodrilus litoralis is one of five species currently recognised in the genus Pontodrilus, though many more have been recognised in the past (Blakemore, 2007, listed eighteen species and subspecies now regarded as synonyms of P. litoralis). Characteristic features of the genus include an absence of nephridia in the anterior segments, and tubular prostrate organs opening to male pores on the eighteenth segment. The other Pontodrilus species have more restricted, non-coastal ranges; one, P. lacustris, is found free-swimming in Lake Wakatipu in New Zealand, whereas the other three are found in terrestrial habitats in Sri Lanka, China and Tasmania.

How P. litoralis achieved its wide distribution is currently unknown. If it arose prior to the separation of the land-masses on which it is now found then it would have had to have survived almost unchanged for hundreds of millions of years, which seems on the face of it unlikely. It seems more credible that it has dispersed more recently from its original point of origin, but while its green, spindle-shaped cocoons are often found attached to floating vegetation we do not know how long they can stand immersion in full-strength salt water. Nor do we know just where P. litoralis originated. It was first described in 1855 from the French Riviera so many authors have assumed the species is Mediterranean in origin. However, the distribution of related species seems to make an Indo-Pacific origin more likely. It may well be that P. litoralis was spread from its original home by humans, carried with rocks and sand used for ballast.

REFERENCE

Blakemore, R. J. 2007. Origin and means of dispersal of cosmopolitans Pontodrilus litoralis (Oligochaeta: Megascolecidae). European Journal of Soil Biology 43: S3—S8.

The Asteiids: Overlooked Flies

Flies are incredibly diverse, but they may be one of the least appreciated of the major insect groups. There are many significant fly lineages whose presence goes all but unnoticed by a small number of afficionados.

Asteia amoena, copyright Mick E. Talbot.


One of the largest clades of flies is the Schizophora, including many such familiar animals as house flies, blowflies, and fruit flies (of both varieties). The most distinctive feature marking this lineage is the ptilinal fold, a groove that runs around the face of the flies along the inner margin of the eyes and across above the antennal insertions. This groove marks the position of a large fold of soft cuticle, the ptilinum, that is used by the fly when it emerges from the hardened case, the puparium, in which it metamorphoses from a larva. The ptilinum expands like a bellows as the fly pumps its head full of liquid until the pressure causes the cap of the puparium to pop open. After this, the excess cuticle is folded away inside the head, never to emerge again, but the mark of its presence remains.

House fly Musca domestica emerging from its puparium, showing the inflated ptilinum. Copyright Alex Wild.


Schizophorans have commonly been divided between two main groups, referred to as the calyptrates and acalyptrates. The basis of this division is the presence (calyptrates) or absence (acalyptrates) of the calypters, lobes at the base of the wings that help in controlling flight. This is not an entirely phylogenetic system: the calyptrates are a single clade but the acalyptrates are not. The most familiar flies belong to the calyptrates (which include house flies and blowflies) despite the fact that acalyptrate flies are considerably more diverse. This is in part because many acalyptrates are very small flies, easily overlooked by the casual observer.

The Asteiidae are one such group of overlooked flies. They are found pretty much world-wide and can be very abundant in some habitats. Nevertheless, they are apparently not common in collections: their soft-bodiedness makes them tricky to preserve, and Grimaldi (2009) noted that tropical species living on rolled leaves of herbs such as bananas and gingers were reluctant fliers and so unlikely to be collected by passive intercept traps. Noteworthy features of asteiids compared to similar flies include a reduced wing venation, and an antennal arista bearing alternating rays (Friedberg 2009). In two genera, Polyarista and Anarista, the arista is reduced or lacking, replaced by a collection of long setae arising from the first flagellomere (Papp 2013).

Diagnostic features of Asteia amoena, from Walker's Insecta Britannica Diptera.


Because of their low collection rates, the natural history of asteiids is poorly known. As already noted, a number of species are found in association with vegetation; others have been raised from fungi. Grimaldi (2009) described Asteia species running "over the surface of a leaf in all directions with uniform effort, including backwards and sideways, which gives them an appearance of floating over the surface". Some species have mating rituals involving trophallaxis, in which a male attempts to entice a female by offering her a regurgitated droplet. If his offering meets her standards, they will collaborate to produce a new generation that will carry on in the same obscurity as the last.

REFERENCES

Freidberg, A. 2009. Asteiidae (asteiid flies). In: Brown, B. V., A. Borkent, J. M. Cumming, D. M. Wood, N. E. Woodley & M. A. Zumbado. Manual of Central American Diptera pp. 1093–1096. NRC Research Press: Ottawa.

Grimaldi, D. A. 2009. The Asteioinea of Fiji (Insecta: Diptera: Periscelididae, Asteiidae, Xenasteiidae). American Museum Novitates 3671: 59 pp.

Papp, L. 2013. A new genus of Asteiidae with a key to the Old World genera (Diptera). Annales Historico-Naturales Musei Nationalis Hungarici 105: 199–205.