Freakishly Big Eyes

To once again shamelessly ride the coattails of research in the news, Nilsson et al. (2012) argued that the enormous eyes of Architeuthis and Mesonychoteuthis are adaptations for detecting Sperm Whales (Physeter). The authors demonstrated that pupils larger than 25 mm are subject to diminishing returns except in the ability to discern large moving objects at great depths from the disturbance to bioluminescent organisms. They calculated that below 600 meters, 90 mm pupils would be able to discern a Physeter 120 m away, allowing the cephalopods an opportunity for “suitably timed and forceful escape behavior”. The data on eye effectiveness are fascinating and the proposed eye function seems plausible, however the paper contains some claims and speculations which are… troubling.

A (barely) living _Architeuthis_. From Wikipedia Commons.

Nilsson et al. claimed that Architeuthis and Mesonychoteuthis have disproportionately large eyes but presented no compelling reason why. They cited Zeidberg (2004) and stated “the allometric growth factor [of eye diameter relative to mantle length] for smaller squid is below 0.7″ but failed to mention the study only covered growth within the species Doryteuthis opalescens. The application of intraspecific allometry from a distant relative is pointless and I see no reason to dismiss the possibility that Giant and Colossal squid eyes are ‘normal’. Comparisons are complicated for Architeuthis due to its (apparent) phylogenetic isolation but compared to other oegopsids it seems positively modest. Mesonychoteuthis is not isolated and other cranchiids (when not stalk-eyed paralarvae) appear to have the largest eyes which can plausibly fit on a head, and beyond. This doesn’t necessarily mean Architeuthis and Mesonychoteuthis aren’t abnormal for their size, but far more interspecific data are needed on adult cephalopod eye size before making any pronouncements. 

_Haliphron atlanticus_ from Wikipedia Commons.

Nilsson et al. imagined a scenario where Physeter predation drove gigantism in squids since large body size would offer more power to escape and would be needed to “build, sustain, and propel a pair of soccer-ball-sized eyes”. They do not appear to have realized that there is another cephalopod with eyes just as big as those of the Giant and Colossal Squids, Haliphron atlanticus. The Mesonychoteuthis measured by Nilsson et al. had an eye 270-280 mm in diameter and the Architeuthis eye diameter calculated from a photograph was “at least” 270 mm; in comparison, the largest Haliphron had eyes “about” 40% of the 0.69 m mantle length (O’Shea 2004) or ~276 mm. The Mesonychoteuthis was apparently the individual with a 2.5 m mantle and weight of 495 kg, compared to only 75 kg for the Haliphron (O’Shea 2004). The mass (and mantle length) of the Architeuthis measured by Nilsson et al. was not given, but is undoubtedly far more than Haliphron as the head width appears to be around 60 cm. Unless there is some fundamental difference between squid and octopus eyes, this suggests that Architeuthis and Mesonychoteuthis could potentially have much larger eyes. Why Haliphron would have some of the proportionally largest eyes for a cephalopod despite already being the largest octopus is puzzling. Like the squids it is prey of Physeter (Santos et al. 2002) but so is the other giant octopus Enteroctopus dofleini (Fiscus et al. 1989) with its modestly-sized eyes, among myriad other deep-sea cephalopods.

This is a rich topic and there are so many other aspects to explore. As hinted at the similar size of Architeuthis, Mesonychoteuthis, and Haliphron eyes – have these species reached some structural or functional limit? How do the eyes of other giant cephalopods (e.g. Galiteuthis phyllura, Megalocranchia fisheri, Onykia robusta, Taningia danae, Dosidicus gigas) compare? One study found the main stomach contents by mass of Southern Sleeper Sharks (Somniosus antarcticus) to Mesonychoteuthis (52%) with Architeuthis present in considerable quantities as well (15%) (Cherel & Duhamel 2004) – how often do the sharks prey on the cephalopods and are they more efficient predators than Physeter due to their much smaller size? Is it possible the eyes have some other, unforeseen function? Alas, Nilsson et al. discuss ichthyosaurs.

_Ophthalmosaurus icenius_ from Wikipedia Commons.

Ichthyosaurs are characterized by greatly enlarged eyes (Sander et al. 2011) with smaller species having an eye diameter/body length relationship comparable to owls and penguins (Motani et al. 1999 – fig 2.). Ophthalmosaurus (above) has the proportionally largest eyes of any ichthyosaur (>220 mm for a 4 m body), frequently shows evidence of the bends, and was calculated to be capable of diving to at least 600 m (Motani et al. 1999) and thus the case seems good that its eyes were functioning similar to those of giant cephalopods. As for what they were detecting, Nilsson et al. suggest giant pliosaurs… I can’t find any other suggestions of pliosaurs cruising the lower end of the mesopelagic zone. Well, at least they didn’t bring up that one Stupid Fucking Hypothesis which I refuse to directly acknowledge. Temnodontosaurus had sclerotic rings 253 mm in diameter relative to a 9 m body length and a similar frequency of the bends as Ophthalmosaurus (Motani et al. 1999) and Nilsson et al. further argue that the laterally-facing orbits and lack of adaptation for improving forward-vision means their objects of interest could appear in any direction, and the authors suggested conspecifics at great depths as the objects of interest. I see no reason to think the large eyes of Temnodontosaurus are due to anything but scaling and it certainly seems that large cetaceans (with the largest extant vertebrate eyes) also have severely reduced or absent forward vision. Nilsson et al. talk about ichthyosaurs in general terms and unfortunately imply that they were all adapted for detecting large objects, which is a shame since eyes rivaling those of giant cephalopods seem to have been restricted to the larger species (and Ophthalmosaurus).

It is worth stating again that I think Nilsson et al. (2012) is fascinating research but it applies its findings to simple scenarios without great justification. I don’t think the research is necessarily wrong – Physeter-detection seems highly compelling – but there is undoubtedly far more to possessing freakishly big eyes than the authors discuss.

References:

Cherel, Y. & Duhamel, G. (2004). Antarctic jaws: cephalopod prey of sharks in Kerguelen waters. Deep-Sea Research I 51, 17–31. Available.

Fiscus, C. H., et al. (1989) Cephalopods from the Stomachs of Sperm Whales taken off California. NOAA Technical Report NMFS 83, 1-10. Available.

Motani, R., et al. (1999) Large eyeballs in diving ichthyosaurs. Nature 402, 747. Available.

Nilsson, D-E., et al. (2012) A Unique Advantage for Giant Eyes in Giant Squid. Current Biology 22, 1-6. DOI 10.1016/j.cub.2012.02.031

O’Shea, S. (2004) The giant octopus Haliphron atlanticus (Mollusca: Octopoda) in New Zealand waters. New Zealand Journal of Zoology 31, 7–13. Available.

Sander, P. M., et al. (2011) Short-Snouted Toothless Ichthyosaur from China Suggests Late Triassic Diversification of Suction Feeding Ichthyosaurs PLoS ONE 6(5): e19480. doi:10.1371/journal.pone.0019480

Santos, M. B., et al. (2002) Additional notes on stomach contents of sperm whales Physeter macrocephalus stranded in the north-east Atlantic. Journal of the Marine Biological Association of the UK 82, 501-507. Available.

Zeidberg, L. D. (2004) Allometry measurements from in situ video recordings can determine the size and swimming speeds of juvenile and adult squid Loligo opalescens (Cephalopoda: Myopsida). The Journal of Experimental Biology 207, 4195-4203. 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.