Big Bears, Little Islands

The archipelago Haida Gwaii lies 80 km off British Columbia and is home to a number of endemics including a subspecies of American Black Bear, Euarctos americanus carlottae (Byun et al. 1997). It seems surprising that a viable population of bears could survive on such isolated and small islands (~10,000 km² total) which is made further remarkable by Haida Gwaii American Black Bears being the largest subspecies (Byun et al. 1997 – citing Foster 1965). Haida Gwaii bears also have distinctive morphology compared with other bears including a more elongate skull, narrower rostrum, less arched cranium and larger teeth with particularly elongate last upper molars (Osgood 1901).

Haida Gwaii Black Bear (left) and a more typical Black Bear, presumably mainland. From Osgood (1901).

Despite their distinctive morphology, an early mtDNA analysis failed to distinguish Haida Gwaii bears from their coastal relatives (Byun et al. 1997). This, coupled with the coastal/island bears clearly grouping away from continental subspecies, was interpreted as indicating that the coastal/island bears had a recent common ancestor from a glacial refuge, probably in the (now submerged) Hecate Strait (Byun et al. 1997). Agnarsson et al. (2010) found similar results with coastal/island bears forming a distinct clade and with its sub-clades having low bootstrap values (i.e. being infrequently recovered). I’m curious why the Haida Gwaii bears themselves formed a clade only half the time – gene exchange with the mainland certainly cannot be common – but perhaps it could indicate just how recently evolved the bears are. Humans have inhabited Haida Gwaii for 8000 years (Reimchen 1998) and it is strange to think that a distinctive subspecies could evolve while sharing an island with our species.

As for how the Haida Gwaii bears got their size, Byun et al. (1997) hypothesized that they represent the ancestral size while other American Black Bears shrunk. Wolverton & Lyman (1998) commented that large bears from the American Midwest assumed to be Pleistocene in age because of their size were actually only a couple hundred of years old, which makes me wonder if similar assumptions led to Byun et al.’s hypothesis. Whether large size was retained or gained, island-dwelling Black and Brown Bears (Ursus arctos) are generally larger than their mainland counterparts (Meiri et al. 2006). One striking example is the Kodiak Bear (U. a. middendorffi) which parallels the Haida Gwaii bears in being the largest subspecies and living on a surprisingly small archipelago (~14,000 km²) in the Pacific Northwest. What factors could there be on islands which allows them to support bears of such size? For Brown Bears, coastal salmon-eating bears were the largest (Hilderbrand et al. 1999) and Haida Gwaii bears consume considerable amounts of Chum Salmon (Oncorhynchus keta) (Reimchen 2000). Of course I haven’t seen a correlation between salmon availability and Black Bear size tested yet and there could very well be a host of other minor factors which allowed Haida Gwaii bears to reach their superlative size. Say, isn’t there supposed to be an ‘Island Rule’ where large mammals get smaller and vice versa? It seems not to apply to carnivorans (Meiri et al. 2006) – so why is it still referred to as a “rule?”?

References:

Agnarsson, I. et al. (2010). Dogs, cats, and kin: A molecular species-level phylogeny of Carnivora. Molecular Phylogenetics and Evolution 54, 726–745. Available.

Byun, S. A. et al. (1997) North American Black Bear mtDNA Phylogeography: Implications for Morphology and the Haida Gwaii Glacial Refugium Controversy. Evolution 51(5), 1647-1653. Available.

Foster, J. B. (1965) The evolution of the mammals of the Queen Charlotte Islands. BC Prov. Mus. 14, 1-30.

Hilderbrand, G. V. et al. (1999) The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Canadian Journal of Zoology 77, 132–138. Available.

Meiri, S. et al. (2006). The generality of the island rule reexamined. Journal of Biogeography 33, 1571–1577. Available.

Osgood, W. H. (1901) Natural history of the Queen Charlotte Islands. North American Fauna 21, 7-50. Available.

Reimchen, T. E. (2000) Some ecological and evolutionary aspects of bear–salmon interactions in coastal British Columbia. Canadian Journal of Zoology 78, 448–457. Available.

Reimchen, T. E. (1998) Nocturnal Foraging Behavior of Black Bears, Ursus americanus, on Moresby Island, British Columbia. Canadian Field-Naturalist 112(2), 446-450. Available.

Wolverton, S. & Lyman, R. L. (1998) Measuring Late Quaternary Ursid Diminution in the Midwest. Quaternary Research 49, 322-329. Available.

Old Six Lobes

_Latimeria chalumnae_ from the Harvard Museum of Natural History. The famous _Kronosaurus_ lurks in the reflection.

What is going on with coelacanths? The first dorsal fin is a typically fishy rayed structure yet the second is fleshy and lobed. Considering that tetrapod limbs are derived lobed fins and the anal fin is also lobate this makes coelacanths hexapedes of a sort. It is baffling how the nickname “Old Fourlegs” got attached to a creature with such bizarrely arrayed and numerous appendages.

A phylogeny of lobed fins from Friedman et al. (2007).

Coelacanths can’t really be said to have “legs” or even proper limbs. Tetrapod limbs are defined as having mobile wrists, ankles and digits (Shubin et al. 2006) whereas coelacanth lobed fins are made out of a series of metapterygia with radials on the anterior and posterior margins (see above). The Devonian coelacanth Shoshonia had pectoral fins with some traits more typical of early tetrapodomorphs than extant coelacanths, most notably by having pronounced asymmetry (Friedman et al. 2007). This indicates that coelacanth lobe fins became less limb-like during their evolution and Friedman et al. (2007) argue that the extant fishes most likely to give insight into early tetrapod limbs are basal actinopterygians such as bichir and sturgeon. Thus extant coelacanths should not be viewed as evolutionarily stagnant and the nickname “Old Fourlegs” somehow manages to be even more wrong.

From Wikipedia Commons.

The medial second dorsal and anal fins of Latimeria are “practically identical” and mirror one another (Forey 1998). These lobed medial fins exhibit skeletal, muscular and innervational similarities with the paired lobed fins (Ahlberg 1992 – citing Millot and Anthony 1958) and all the lobed fins appear capable of considerable rotation (Forey 1998). Judging by videos it appears that the medial lobed fins beat in sync whereas the pectoral and pelvic pair does not. The medial lobed fins particularly resemble the pelvic fins and the basal plate supporting the former appears very similar to the pelvis of the latter rotated 90 degrees (Ahlberg 1992). Ahlberg (1992) suggested that the lobed median fins came into being through a switch in gene expression although noted more fossils and evidence from development and genetics would be needed. Unfortunately so far as I can tell this topic has yet to be explored further.

From Wikipedia Commons

The caudal fin of coelacanths is normally interpreted as a three-part structure (Forey 1998) however in the description of the Jurassic coelacanth Parnaibaia maranhaoensis Yabumoto (2008) interprets it as being composed of a third dorsal, second anal fin and a proper caudal. Third dorsals and second anals are not without precedent (e.g. cod) however the degree of disparity between fins that coelacanths display certainly is. Perhaps the medial lobed fins of coelacanths aren’t true dorsal or anal fins at all but totally novel replications of the pelvic fins. Alternately it could be possible that coelacanths had ancestors with a superfluous number of medial fins or that the caudal fin split into three parts for some reason; either way it seems likely that something very very strange is happening to coelacanths genetically and developmentally.

References:

Ahlberg, P. E. (1992). Coelacanth Fins and Evolution. Nature 358, 459. Available.

Forey, P. L. (1998). History of the Coelacanth Fishes. Natural History Museum: London.

Friedman, M. (2007). First discovery of a primitive coelacanth fin fills a major gap in the evolution of lobed fins and limbs. Evolution & Development 9(4), 329-337. Available.

Millot, J. & Anthony, J. (1958-1965) Anatomy de Latimeria chalumnae. Vol. I-II. Paris.

Shubin, N. H. et al. (2006). The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature 440 (6), 764-771. Available.

Yabumoto, Y. (2008). A new Mesozoic coelacanth from Brazil (Sarcopterygii, Actinistia). Paleontological Research 12(4), 329-343. Available.

Lophenteropneusts and Beyond

Lophenteropneust - the worm that never was. From Pawson (2003).

My younger and more credulous self continuously pored over the Regional Checklist of Mystery Animals and one of the many cryptic entities which captured my imagination were lophenteropneusts, deep-sea chimerical invertebrates known only from photographs. This was during the informational Dark Age of the early 00′s and having that one scrap of information to go on made them all the more tantalizing. Revisiting the topic on a whim led to the shocking discovery that one ‘lophenteropneust’ was captured before the checklist was even composed and that the hypothetical worm was a gross distortion of an already fantastic group.

Unidentified acorn worm. From Wikipedia Commons.

‘Lophenteropneusts’ were initially interpreted as a transitional form between pterobranchs (sea angels) and enteropneusts (acorn worms) and used to argue that the latter had evolved into the former (Holland et al. 2005). Both the angels and the worms are hemichordates, deuterostomes with a three part (proboscis/collar/trunk) body plan and separate coelom in each region (Swalla and Smith 2008 – citing various). Hemichordata has been consistently recovered as the sister clade of echinoderms (e.g. Swalla and Smith 2008) and knowing what the ancestral hemichordate looked like could be very informative about the evolution of echinoderms and even more distant relatives such as vertebrates. The two hemichordate body plans are strikingly disparate as acorn worms are solitary, have numerous gill slits and a strait gut whereas sea angels are colonial tube dwellers, have reduced or absent gill slits, a u-shaped gut and feed with tentacles (Cannon et al. 2009). The ‘lophenteropneust’ looks like an acorn worm with sea angel tentacles glued on and was thus interpreted as a transitional form. Lacking the original source I’m puzzled why the hypothetical worm was interpreted as evidence of an acorn worm to sea angel transition and not vice versa. Despite the dubiousness of ‘lophenteropneusts’ the hypothetical relationship between the hemichordates has some merit.

The sea angel _Rhabdopleura normani_. From Wikipedia Commons.

Cameron et al. (2000) recovered pterobranchs as being within Enteropneusta in a molecular analysis and noted that pterobranchs share a number of traits with harrimaniid sea acorns such as small size, post-anal tail in harrimaniid juveniles, reduction in gill slits, filter feeding in some harrimaniids, and others. Cannon et al. (2009) reached a similar arrangement in their molecular phylogeny yet Osborn et al. (2011) did not. This hypothesis is still very much an open question – invertebrate biology seems to be full of these – and hopefully some sort of consensus will eventually be reached.

'Lophenteropneust'. From Thiel (1979).

After a few botched attempted at collection (Barnes 2004) in 2002 an acorn worm with a broader collar than any other described species was videotaped, collected and formally named Torquarator bullocki (Holland et al. 2005). Wide-collared acorn worms had been observed and photographed previously (but not captured) and in their review Holland et al. (2005) discovered that ‘lophenteropneusts’ showed a similarly wide collar area with no readily apparent tentacles. The Thiel photograph (above) is the highest quality ‘lophenteropneust’ picture (Holland et al. 2005) and it seems to have similar collar morphology to Tergivelum baldwinae (see Holland et al. 2009) with no indication of the looped and feathered tentacles imagined to be present. Holland et al. (2005) conclude that the ‘lophenteropneust’ concept was entirely based on misinterpreted low-quality photographs but that doesn’t mean that the worms behind them are at all boring.

Not concept art from Avatar 2 but an undescribed extra-wide-lipped acorn worm. From Holland et al. (2005).

Holland et al. (2005) found Torquarator bullocki unique enough to warrant its own family, Torquaratoridae, and while one analysis found a wide-collared species to fall within Ptychoderidae (Cannon et al. 2009) the clade was recently confirmed to be separate and monophyletic (Osborn et al. 2011). One issue is that extraction of genetic material from the type species and genus Torquarator bullocki has thus far failed however the family was also rediagnosed on morphology which the species displays (Osborn et al. 2011). Torquaratorids have a reduced to absent proboscis skeleton and an adult stomochord either absent or separated from the buccal cavity of the collar (Osborn et al. 2011). More remarkable traits displayed in Torquaratoridae include a deep sea habitat (acorn worms were previously regarded as primarily shallow water), no burrowing capabilities (the normal mode of life for acorn worms), controlled drifting (using gut contents as ballast, secreting mucous to increase drag in the water column) to travel between locations, the largest invertebrate eggs (outside of cephalopods) which may have something to do with the enigmatic planctosphaera larvae, far more morphological disparity than most acorn worms, and they are very specious with 13 species being added in one study compared to the prior total of 89 for all acorn worms (Osborn et al. 2011).

Going back to the impetus of this article, what does the discovery of torquaratorids mean for cryptozoology? The misinterpretation of ‘lophenteropneust’ pictures was used as a cautionary tale by Dubois and Nemésio (2007); the authors further discussed cryptozoological “problems” resulting from photographs being used to name species such as my old nemesis Cadborosaurus willsi. The sightings and photographs of ‘lophenteropneusts’ and other wide-collared acorn worms prior to 2002 (see Holland et al. 2005 for review) highlights an awkward period between initial observation and discovery which is surprisingly common. But is it cryptozoological? Since the earlier observations (and anecdote) of pre-discovery torquaratorids apparently did not lead to the discovery of Torquarator bullocki I would argue that no, it isn’t. This does not mean that photographs and even anecdotes are useless as tools for discovering new species (they’re not) but they must be treated with caution and restraint. I have a suspicion I’ll be discussing this extensively and excessively in the future.

References:

Barnes, R. S. K. 2004. Kingdom Animalia. IN: The Diversity of Living Organisms. Blackwell Publishing.

Cannon, J. T. et al. 2009. Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Molecular Phylogenetics and Evolution 52, 17–24. Available.

Dubois, A. & Nemésio, A. 2007. Does nomenclatural availability of nomina of new species or subspecies require the deposition of vouchers in collections? Zootaxa 1409, 1–22. Available.

Holland, N. D. et al. 2009. A new deep-sea species of epibenthic acorn worm (Hemichordata, Enteropneusta). Zoosystema 31(2), 333-346. Available.

Holland, N. D. et al. 2005. ‘Lophenteropneust’ hypothesis refuted by collection and photos of new deep-sea hemichordate. Nature 434, 374-376. Available.

Osborn, K. J. et al. 2011. Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea. Proc. R. Soc. B doi: 10.1098/rspb.2011.1916

Pawson, D. 2003. Deep-sea dreams: diary of a mad lophenteropneust watcher. Deep-Sea Newsl. 32, 6–7. Available.

Swalla, B. J. & Smith, A. B. 2008. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Phil. Trans. R. Soc. B 363, 1557–1568. Available.

Thiel, H. 1979. Structural Aspects of the Deep-Sea Benthos. Ambio Special Report 6, 25-31. Available.