Salpidobolus

The photo above (copyright Dmitry Telnov) shows a millipede of the genus Salpidobolus, photographed in West Papua. Salpidobolus is a genus of the family Rhinocricidae (in the order Spirobolida) that is found over a range from the Philippines, Sulawesi and Lombok in the west to Fiji in the east and Queensland in the south. There are also a handful of species that have been described from northern South America as part of Polyconoceras, a genus now regarded as synonymous with Salpidobolus, but Hoffman (1974) expressed the expectation on biogeographical grounds that future revision will show these species to be misplaced. Salpidobolus species are scavengers of vegetable matter and most active at night. When threatened, they can release a caustic spray from glands on the body segments that can cause irritation if it contacts mucous membranes such as around the eyes (Hudson & Parsons 1997). There are also reports (albeit unconfirmed) of production of bioluminescence by Salpidobolus (see here); observations on other millipedes suggest such bioluminescence could be related to the aforementioned caustic spray.

As has been mentioned in an earlier post, most millipedes tend not to be extravagant in their external variation, and spirobolidan millipedes look about as millipede-y as you can get. Notable features of the spirobolids as a whole include the presence of only a single pair of legs on each of the first five body rings, and modification of the eight and ninth pairs of legs into the gonopods (Milli-PEET). The Rhinocricidae are characterised by a broad collum (the first segment behind the head) with a rounded ventrolateral margin, and the anterior gonopods forming a single, more or less triangular, transverse plate. Sensory pits called scobinae are often present on the dorsal segments (Marek et al. 2003). Below the family level, as with other millipedes, it all comes down to genitalia. In Salpidobolus, the distal section of the posterior gonopods is flagellate and divided into two branches, one branch carrying the seminal channel (Hoffman 1974).

Gonopods of Salpidobolus meyeri, from Hoffman (1974).

The status of Salpidobolus was most recently reviewed by Hoffman (1974). The majority of species now included in the genus had previously been placed in the separate genera Dinematocricus or Polyconoceras. Salpidobolus was initially restricted to the type species, S. meyeri from Sulawesi, which differs from other species in the presence on the first three pairs of legs of distinct processes on some of the leg segments. Dinematocricus and Polyconoceras were supposed to differ on the basis of the number of sensilla at the end of each antenna: four in Dinematocricus, more than four in Polyconoceras. Hoffman felt that none of these differences warranted generic separation in light of the consistency of gonopod structure between the three 'genera', and united them all under the oldest available name.

REFERENCES

Hoffman, R. L. 1974. Studies on spiroboloid millipeds. X. Commentary on the status of Salpidobolus and some related rhinocricid genera. Revue Suisse de Zoologie 81(1): 189–203.

Hudson, B. J., & G. A. Parsons. 1997. Giant millipede ‘burns’ and the eye. Transactions of the Royal Society of Tropical Medicine and Hygiene 91: 183–185.

Marek, P. E., J. E. Bond & P. Sierwald. 2003. Rhinocricidae systematics II: a species catalog of the Rhinocricidae (Diplopoda: Spirobolida) with synonymies. Zootaxa 308: 1–108.

Water Moulds

Salmonid infected with Saprolegnia, from the Scottish Government.

In the 1970s and 1980s, stocks of salmon and trout around the North Atlantic Ocean took a sizeable hit. Mature fish entering fresh water had their skin break out in lesions that eventually became covered in a slimy, cottony growth. With the lesions eventually eating into the underlying tissue, many fish died from these infections before they could spawn.

The disease became known as ulcerative dermal necrosis, and its underlying cause remains unknown. The cottony growth so often associated with the disease, however, was made up of a mould-like organism called Saprolegnia. Saprolegnia belongs to a family Saprolegniaceae in a group of organisms known as the Oomycetes, commonly referred to as 'water moulds'. Most Saprolegniaceae function as saprobes, living off decaying organic matter. A few, however, can occasionally function as pathogens. In the case of the aforementioned necrosis outbreak, the Saprolegnia would have been a secondary infection that exacerbated the progress of the disease. Another genus, Aphanomycese, includes species that can cause root rot in vegetables such as peas or beets (Johnson et al. 2002).

Mature and developing oogonia of Saprolegnia, copyright George Barron.

In habit and lifestyle, water moulds resemble fungi, and were long classified as such. When they were first described in the 1700s, however, they were identified as algae due to similarities in their cell and spore morphology to freshwater algae such as Vaucheria. In recent decades, it has become clear that it was these original observers that were closer to the mark. Oomycetes are not directly related to the true fungi, but belong to a lineage known as the heterokonts or stramenopiles. Most heterokonts are microbial, but they also include algal forms such as the brown algae and (yes) Vaucheria. The heterokont affinities of water moulds become apparent during asexual reproduction when they produce motile zoospores bearing a pair of flagella (though many 'water moulds' are terrestrial rather than aquatic, these zoospores do require water to spread). As is typical of heterokonts, these two flagella differ in appearance: the anterior flagellum bears a series of lateral side-branches whereas the posterior flagellum in smooth. Other significant differences between oomycetes and true fungi are that oomycetes are diploid through the greater part of their life cycle (fungi are haploid), and their cell walls are composed not of chitin but of other compounds such as glucans and/or cellulose.

Drawing of zoospores of Saprolegnia, showing divergent flagella, from here.

Characteristic features of the Saprolegniaceae in particular include their possession of relatively broad hyphae, up to 150 µm in some cases (Dick 2001), that are not divided into cells by septae. Other distinguishing features relate to the production of reproductive cells. Most oomycetes are capable of both asexual and sexual reproduction, though one genus of Saprolegniaceae, Aplanopsis, is only known to reproduce sexually. In asexual reproduction, the motile zoospores are produced within a distinct zoosporangium (some other oomycetes do not separate the zoosporangium from the adjoining hypha until after zoospore formation). When first released, the zoospores move relatively little and soon transform into an immotile cyst. This cyst will eventually revert back into a zoospore, and it is at this stage that the greater part of dispersal happens. This secondary zoospore will then transform again into a cyst, from which will grow the mature hyphae.

Hyphae of an Achlya-like oomycete, with clusters of encysted zoospores at the ends of emptied zoosporangia, from here.

Sexual reproduction involves the production of distinct oogonia and antheridia, with the latter fertilising the former to produce oospores (some species can produce oospores parthenogenetically). These differ from zoospores in being aflagellate and immobile, with thick walls that make them more resistant to adverse conditions. Oospores of Saprolegniaceae contain oil globules that probably function as an energy store (like the endosperm of a plant seed). Depending on the species, the distribution of oil globules may vary between numerous small globules evenly distributed around the periphery of the centrally located cytoplasm (referred to as 'centric'), or one large globule pushing the cytoplasm off to one side ('eccentric'). An oospore may geminate into hyphae alone, or it may produce hyphae topped by zoosporangia.

Oogonium of Saprolegnia, with associated antheridium, copyright George Barron.

The genera of Saprolegniaceae have been primarily distinguished by features of the zoosporangia, such as the manner of release of the zoospores. In some genera, the initial zoospores may have already progressed to encystment or the secondary zoospore stage by the time they fully emerge. In genera such as Achlya, the spores are released from a single terminal opening and form a clump at the end of the emptied sporangium. In others such as Saprolegnia, they disperse individually as soon as they escape. And in genera such as Dictyuchus, the zoosporangium wall opens in multiple places and the spores are all sent out by their own distinct orifice. However, more recent phylogenetic studies have cast doubt on the integrity of some of these genera: the Achlya type of zoospore dispersal, for instance, is probably basal for the Saprolegniaceae as a whole and this genus is polyphyletic.

REFERENCES

Dick, M. W. 2001. Straminipilous Fungi: Systematics of the Peronosporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and other similar organisms. Kluwer Academic Publishers.

Johnson, T. W., Jr, R. L. Seymour & D. E. Padgett. 2002. Biology and systematics of the Saprolegniaceae. http://dl.uncw.edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book/.

The Hawaiian Honeycreepers: Diversity in Danger

'Apapane Himatione sanguinea, copyright Peter LaTourette.

In 1938, avian malaria was discovered to have affected pigeons in the city of Honolulu (Amadon 1950). This might have seemed like a minor detail—except among breeders, pigeons do not normally elicit much concern from the average person—but it was to prove a disaster. From the pigeons, the disease spread into native birdlife of the Hawaiian archipelago and wreaked havoc. Many species living at lower elevations were wiped out, unable to withstand the disease's effects. Others were forced into remnant populations above an elevation of 1500m, where the disease's mosquito vectors were unable to survive.

Among the malaria's victims were several species of the Hawaiian honeycreepers, a group of small birds unique to the archipelago. The honeycreepers have become recognised as one of the classic examples of an island adaptive radiation, like the Madagascan vangas or the Galapagos finches. From the original colonisation of the archipelago by what was probably a fairly generalised finch-like bird, perhaps some five or six million years ago (Lerner et al. 2011), the Drepanidini have diversified into a disparate array of seed-eaters, insectivores and nectar-feeders. Some have evolved massive reinforced bills to crush the seeds of local trees such as koa or naio. Other have long slender bills that they use to reach into the depths of flowers or prise insect larvae from holes in bark. Currently, about fifty species of honeycreeper are known to have been present in the Hawaiian archipelago prior to human settlement; new ones continue to be described from fossil or subfossil remains. Sadly, due to factors such as habitat loss, competition with and predation by introduced fauna, and diseases such as the aforementioned malaria, only about twenty species remain alive today and many of those are critically endangered.

Maui 'alauahio Paroreomyza montana, copyright Markus Lagerqvist.

Older references will refer to the Hawaiian honeycreepers as their own family, the Drepanididae, due as much to long-standing uncertainty about their relationships to other birds as to their own distinctiveness. Many authors, such as Amadon (1950), argued for a connection between the honeycreepers and the South American flowerpiercers of the tanager family, believing that the nectar-feeders among the Drepanididae were closer in appearance to the group's original ancestor. However, recent studies, both molecular and morphological, have been unified in supporting a connection between the honeycreepers and the finches of the Fringillidae, leading to the demotion of the 'family' Drepanididae to a 'tribe' Drepanidini of the fringillids. In his original studies on the honeycreepers, Perkins recognised two subgroups: the 'melanodrepanines' were mostly nectar-feeders and were largely black and/or red in coloration, whereas the 'chlorodrepanines' were mostly seed-eaters or insectivores and usually yellow or greenish. Recent studies have supported the 'melanodrepanines' as a clade but identified the 'chlorodrepanines' as paraphyletic.

Po'o-uli Melamprosops phaeosoma, copyright Paul Baker.

One unusual feature of many Drepanidini is that they carry a distinctive scent that has been referred to as the 'drepanidine odour' (this site describes it as a sweet, musty smell). Two primarily insectivorous genera, the po'o-uli Melamprosops phaeosoma and the ʻalauahios Paroreomyza, lack this 'drepanidine odour', and on the basis of this and a couple of other points it has been questioned whether they are properly assigned to the Drepanidini. However, the osteological analysis of Drepanidini by James (2004) confirmed their position as drepanidines, a result that has since been corroborated by molecular analyses. It seems likely that Melamprosops and Paroreomyza are basal drepanidines outside an 'odoriferous' clade (Pratt 2014). Together with the akikiki Oreomystis bairdi, these species form a basal grade of generalist feeders with fairly slender bills. It is possible that the akikiki and the Maui ʻalauahio Paroreomyza montana are the only members of this grade surviving.

Laysan finches Telespiza cantans, copyright S. Plentovich.

The next clade of drepanidines to diverge in molecular phylogenies includes the Hawaiian finches, an assemblage of often seed- or fruit-eating species with thick, strong bills (Pratt 2014). James' (2004) osteological analysis did not resolve the finches as a single clade, instead intermingling them with the aforementioned grade. Again, the finches have been hard hit by extinction, with the only survivors being the palila Loxioides bailleui, the Laysan finch Telespiza cantans and the Nihoa finch T. ultima. Amadon (1950) noted that the Kona grosbeak Chloridops kona was extremely rare even when first discovered in the late 1800s, being restricted to an area of only 'a few square miles' in the Kona district of Hawai'i. The grosbeaks of the genus Chloridops and the koa finches of the genus Rhodacanthis had particularly strongly developed bills for cracking seeds, looking almost parrot-like in the case of Chloridops (James 2004). Of uncertain relationships to the finches are two unusual extinct species, the 'o'u Psittirostra psittacea and the Lanai hookbill Dysmorodrepanis munroi. The 'o'u was a fruit-eating, large-billed bird that was once widespread on the main islands of the Hawaiian archipelago (in contrast to most other honeycreeper species, which were mostly restricted to a single island). It was last definitely recorded in 1989 and continued survival is considered unlikely. The Lanai hookbill was a particularly bizarre species in which the mandible and maxilla were curved toward each other, so that the base of the bill gaped open even when the beak was closed. The single known specimen is unusual enough that Amadon (1950) did not accept that it represented an actual species, expressing the opinion that it was probably a deformed 'o'u specimen; current authors accept it as a good species.

Crested honeycreeper Palmeria dolei, from the US Geological Survey.

As noted above, the nectar-feeding 'melanodrepanines' form a well-supported clade including three surviving species: the 'i'iwi Drepanis coccinea, the crested honeycreeper or akohekohe Palmeria dolei and the 'apapane Himatione sanguinea, the last of which is one of the more abundant living honeycreepers. The melanodrepanines have slender bills, which in the species of Drepanis (the 'i'iwi and two extinct species of mamo) are long and downcurved. Also probably belonging to the melanodrepanines is the extinct ʻula-ʻai-hawane Ciridops anna, which shared their black and red plumage despite being a fruit- rather than a nectar-feeder.

Kaua'i 'akialoa Akialoa procerus (front) and Kaua'i nukupuu Hemignathus hanapepe (rear), from Keulemans (1890).

The final group of drepanidines to be considered here is also the largest, and contains the most surviving species: the 'amakihis of the genus Chlorodrepanis, the 'akepas Loxops, and related taxa. These are slender-billed insectivorous forms with the more generalist species being similar in appearance to the basal genera Paroreomyza and Oreomystis. Indeed, the classification of drepanidines by Amadon (1950), which was decidedly more lumpy than the current norm, subsumed the latter two genera in an expanded Loxops. Possibly related to this group are the extinct 'akialoas of the genus (wait for it...) Akialoa, which had an extremely long down-curved bill. Two other genera of this group, Hemignathus (including the ʻakiapolaʻau Hemignathus wilsoni) and the Maui parrotbill Pseudonestor xanthophrys, are unique among passerines in having a maxilla that significantly overhangs the much shorter mandible. The Maui parrotbill, despite being primarily an insectivore, has a heavier bill somewhat reminiscent of the finch group, and James' (2004) morphological analysis (which was primarily based on skull features) associated it with Psittirostra and Dysmorodrepanis rather than with Hemignathus; the latter association, however, is supported by molecular analyses, indicating a single origin for the unequal bills.

The loss of this remarkable radiation can be regarded as nothing short of a tragedy. Only two species of Hawaiian honeycreeper are currently regarded as not threatened (as given in the IUCN listings at Wikipedia), the 'apapane and the common 'amakihi Chlorodrepanis virens. Even these species could become endangered as a warming climate allows malaria-carrying mosquitoes to encroach further on their highland refuges. And something truly wonderful could be lost from the world.

REFERENCES

Amadon, D. 1950. The Hawaiian honeycreepers (Aves, Drepaniidae). Bulletin of the American Museum of Natural History 92 (4): 151–262.

James, H. F. 2004. The osteology and phylogeny of the Hawaiian finch radiation (Fringillidae: Drepanidini), including extinct taxa. Zoological Journal of the Linnean Society 141: 207–255.

Lerner, H. R. L., M. Meyer, H. F. James, M. Hofreiter & R. C. Fleischer. 2011. Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Current Biology 21: 1838–1844.

Pratt, H. D. 2014. A consensus taxonomy for the Hawaiian honeycreepers. Occasional Papers of the Museum of Natural Science, Louisiana State University 85: 1–20.