Billfish Bills - What Are They Good For?

In the prior article, I discussed long-beaked "dolphins" (Eurhinodelphidae) and noted that I couldn't find hypotheses on the function of their uneven jaws in the literature... aside from a weird proposal involving Skimmers. The Theatrical Tanystropheus mentioned a couple ("digging for small, sand-dwelling organisms or as a bat with which to stun fish") which are plausible, but I don't know where they are from or what lines of reasoning are behind them. There are extant species with a superficially similar condition - billfishes - and it could be relevant to review what they do with their bills.

Atlantic White Marlin (Tetrapturus albidus) from Wikipedia Commons.

Swordfish (Xiphiidae) and Marlins/Sailfishes/Spearfishes (Istiophoridae) are living sister taxa¹ in the clade Xiphioidea; while traditionally included in Scombroidei, billfishes are presently regarded as phylogenetically distinct (Orrell et al. 2006) and possibly close relatives of jacks and... flatfishes (Little et al. 2010). Fish phylogenetics is scary business, and I suspect billfish relations will undergo further revisions as the monstrosity known as "Perciformes" is reasoned into pieces. Anyways, while xiphiids² and istiophorids look superficially similar, they actually have rather distinctive morphology. Swordfish have a bill which is flat in cross-section, toothless, blunt-tipped, and with central chambers (compared to rounded, denticulated, pointed, and chamber-less for istiophorids), a weak mandible much shorter than the rostrum, no scales, and no pelvic fins (Collette et al. 2006; Fierstine 2006; Fierstine and Voight 1996 citing Nakamura 1983). Strangely, most extinct billfishes have jaws of equal length, and if the proposed (Istiophoridae + Hemingwayidae) and (Xiphias + Xiphiorhynchus) clades (Fierstine 2006) are correct (see note 1), this would mean the unequal jaws of extant billfishes evolved twice. 

¹ A detailed cladistic analysis with the fossil members of the group has yet to be undertaken (Fierstine 2006).
² As for what the deal with them and ziphiids is, I have no idea.

Swordfish (Xiphias gladius) from Wikipedia Commons.

One infamous use of the billfish bill is impaling unexpected objects. One Blue Marlin was found with rostrum fragments from two other, different billfish species (Fierstine 1997). Other unfortunates include large fish, whales, bales of rubber, boats, ships, deep-diving vessels, people, and turtles (Frazier et al. 1994 - citing various). The billfish-on-billfish impaling has been interpreted as defense against predators (Fierstine 1997) and in the case of the turtles, it was hypothesized that the billfish accidentally impaled them when aiming for fish aggregated nearby (Frazier et al. 1994). Istiophorids can survive with a foreshortened rostrum (Fierstine 2006) so apparently these accidents are survivable. But this raises another question - do they need an elongated rostrum at all?

One study of 227 Blue Marlins (Makaira nigricans) stomach contents found that 38% of prey items showed evidence of damage from the bill, 11% of which were speared and 81% of which were slashed, and the rest of which were in multiple pieces (Shimose et al. 2007). Bizarrely, another study with 226 Blue Marlins found no evidence of prey being struck or speared (Vaske et al. 2011). Vaske et al. (2011) offered no explanation for this anomaly, and I can't see an obvious one either. Both populations (from Japan and Brazil, respectively) even primarily preyed on Skipjack Tuna (Katsuwonus pelamis), which were normally killed with the bill in the former population. I'm stumped.

Fierstine (2006) hypothesized that unequal jaw length in billfishes may have evolved to avoid suffocation when impaling large objects (predator or prey) and to avoid damage to the mandible. I don't buy the mandibular reasoning since extant billfishes get by just fine with them naturally foreshortened. The available evidence suggests impaling is a rather rare event and thus unlikely to be the main factor in the evolution of the characteristic billfish bill. An alternate hypothesis could be that the mandible was shortened so the rostrum could be "weaponized" (sword-like flattening in xiphiids and denticles in istiophorids³) to slash at prey. However, the population which apparently doesn't use bills to feed and healthy individuals with damaged rostra are problematic for both of these hypotheses. Perhaps future studies will show that the bill is generally important for feeding in the group and that the counterexamples are just freaks, but either way, it seems premature to make any conclusions about why billfish have their striking morphology.


³ The ichthyosaur Eurhinosaurus has teeth on the upper jaw which could be a similar instance of "weaponization". 

I really have no idea how eurhinodelphids fit into this framework since Fierstine's hypothetical suffocation would not be an issue (if they could impale at all) and the rostrum does not seem particularly dangerous (no teeth, denticles, or flattening). I wonder if this morphology evolved for different reasons, or if it evolved for reasons that have yet to be hypothesized.

References:

Collette, B. B., McDowell, J. R., and Graves, J. E. (2006). Phylogeny of Recent Billfishes. Bulletin of Marine Science 79(3), 455-468. Available.

Fierstine, H. L. (2006). Fossil history of Billfishes (Xiphioidea). Bulletin of Marine Science 79(3), 433-453. Available.

Fierstine, H. L. (1997). An Atlantic Blue Marlin (Makaira nigricans), impaled by two species of billfishes (Teleostei: Istiophoridae). Bulletin of Marine Science 61(2), 495-499. Available.

Fierstine, H. L., and Voight, N. L. (1996). Use of Rostral Characters for Identifying Adult Billfishes (Teleostei: Perciformes: Istiophoridae and Xiphiidae). Copeia 1996(1), 148-161. Available.

Frazier, J. G., Fierstine, H. L., Beavers, S. C., Achaval, F., Suganuma, H., Pitman, R. L., Yamaguchi, Y., and Prigioni, C. M. (1994). Impalement of marine turtles (Reptilia, Chelonia: Cheloniidae and Dermochelyidae) by billfishes (Osteichthyes, Perciformes: Istiophoridae and Xiphiidae). Fisheries Science 39(1), 85-96. Available.

Little, A. G., Lougheed, S. C., and Moyes, C. D. (2010). Evolutionary affinity of billfishes (Xiphiidae and Istiophoridae) and flatfishes (Plueronectiformes): Independent and trans-subordinal origins of endothermy in teleost fishes. Molecular Phylogenetics and Evolution 56(3), 897-904. doi:10.1016/j.ympev.2010.04.022

Nakamura, I. (1983). Systematics of billfishes (Xip­hiidae and Istiophoridae). Publications of the Seto Marine Biological Laboratory 28, 255-396.

Orrell, T. M., Collette B. B., and Johnson, G. J. (2006). Molecular data supports separate scombroid and xiphioid clades. Bulletin of Marine Science 79(3), 505-519. Available.

Shimose, T., Yokawa, K., Saito, H., and Tachihara, K. (2007). Evidence for use of the bill by blue marlin, Makaira nigricans, during feeding. Ichthyological Research 54(4), 420-422. DOI: 10.1007/s10228-007-0419-x

Vaske, T., Travassos, P. E., Pinheiro, P. B., Hazin, F. H. V., Tolotti, M. T., and Barbosa, T. M. (2011). Diet of the Blue Marlin (Makaira nigricans, Lacepède 1802) (Perciformes: Istiophoridae) of the southwestern equatorial Atlantic Ocean. Brazilian Journal of Aquatic Science and Technology 15(1), 65-70. Available.

Picture of the Indiscriminate Interval #000008 - Eurhinodelphis longirostris

Eurhinodelphis longirostris at the American Museum of Natural History.

The most striking trait of Eurhinodelphidae is a toothless extension of the rostrum beyond the mandible (Lambert 2005), superficially similar to the bills of Billfish and Swordfish. Oddly, this morphology was speculative for a period of time (Kellogg 1925) although it has apparently been confirmed in several species as of Lambert (2005). Unfortunately, information on eurhinodelphids is scant and/or difficult to access and, among numerous other basics of their biology, I really don't know what the function of the extended rostrum would be. The only suggestion I could find is from one professor Abel who speculated that the cetaceans "swam on the surface of the sea, where they captured food - probably fishes - in much the same manner as does the skimmer (Rhynchops) [sic] among birds" (Anonymous 1909). Somehow, I find this even less plausible than azhdarchids-as-skimmers. On a curious note, there is a cetacean with the reverse of eurhinodelphid morphology (mandible extending past rostrum) unofficially known as the... skimmer porpoise.

Phylogenetically, eurhinodelphids have bounced around from being considered stem-ziphiids, the sister group to Delphinida, and the sister group to Squalodontidae + Squalodelphidae (Geisler et al. 2011 - citing various); within Geisler et al. (2011), they were placed outside crown-Odontoceti¹ in an unconstrained analysis and as the sister group of platanistoids in a constrained analysis. The authors regarded the latter position as more probable and placed eurhinodelphids within the new group Synrhina, which includes most odontocetes except for Sperm Whales and assorted extinct taxa. Whatever their placement, eurhinodelphids are certainly close relatives of living toothed whales, despite that whole extinct thing.

¹ It actually states they "did not fall inside crown Cetacea", but this is a typo. Otherwise, they'd be Miocene Archaeocetes. 

Eurhinodelphis longirostris seems to have an unusually long neck for a cetacean. The cervical vertebrae are not fused (Kellogg 1925), however this is a surprisingly common trait shared with river dolphins, monodontids, rorquals, and gray whales (Tinker 1988). The neck of E. longirostris appears to be proportionally longer than those of the baleen whales and Narwhal and is probably comparable to those of the Beluga and Dorudon. River dolphin skeletons are hard to find, but it seems likely they have similarly proportioned necks. It seems that Eurhinodelphis wasn't a total freak, well, except for the snout.

The Theatrical Tanystropheus covered Eurhinodelphis as well, and it doesn't even overlap that much!

References:

Anonymous. (1909). Notes. Nature 2088 (82), 16. Available.

Geisler, J. H., McGowen, M. R., Yang, G., Gatesy, J. (2011). A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea. BMC Evolutionary Biology 11 (112). Available.

Kellogg, R. (1925). On the occurrence of fossil porpoises of the genus Eurhinodelphis in North America. Proceedings of the U. S. National Museum 66(26), 1-40. Available.

Lambert, O. (2005). Les dauphins longirostres et les baleines à bec du Néogène de la région d’Anvers: systématique, phylogénie, paléo-écologie et paléo-biogéographie. Doctoral Thesis. Partially Available.

Tinker, S. W. (1988). Whales of the World. E. J. Brill Publishing Company: New York. Partially Available.

Picture of the Indiscriminate Interval #000007 - Narwhal

Monodon monoceros at the American Museum of Natural History.

Narwhals are a bit strange even by cetacean standards. I'll let the title of this Tet Zoo article speak for itself: "A 3-m tooth that can bend 30 cm in any direction and is hypersentitive to salinity, temperature and pressure... and the sonic lance hypothesis".

They get weirder. Without the tooth (or sometimes, teeth) it is difficult to picture how this flat-skulled cetacean could be the same as a bulbous-headed Narwhal. As brought up in my Dorudon post, there are colossal amounts of soft tissue involved.

Another soft-tissue feature not hinted at by the skeleton are unusually shaped flukes... in males. Fontanella et al. (2010) suggest that the concave leading edge and lack of sweepback of the flukes increases lift and thrust to compensate for the drag caused by the tusk in males. The implications of the occasional tusked female narwhal were not discussed by the authors.

One female Narwhal was estimated to be 114.8 (± 10.2) years old (Garde et al. 2007) which, if correct, would make Narwhals the third oldest known mammals after humans (122 years) and Bowhead Whales (211 years?). Garde et al. (2007) used a sample of 75 individuals (15 juvenile) from a heavily hunted population, and subsequently speculated that Narwhals in other populations could potentially reach "considerably higher" ages. As for methodology, Garde et al. (2007) used aspartic acid racemization rate in the eye; this method was also used to calculate the extreme age estimate for Bowheads (George et al. 1999), and ages of over a hundred years have subsequently been supported by bomb lance fragments (George and Bockstoce 2008) and ovarian corpora counts (George et al. 2011). So it looks probable that aspartic acid racemization does not provide grossly inaccurate estimates of old age - why would Narwhals live to be centenarians? Garde et al. (2007) note that Narwhals and Bowheads are both year-round Arctic residents and speculate that their extreme longevity is an adaptation to drastic changes is climate. While an interesting idea, there does not seem to be much data available on cetacean longevity (Table 2 in Garde et al. 2007 has only 12 out of ~80 species) and Narwhals are apparently not far older than other cetaceans (for instance, Orcas apparently live to be 90). It could be possible that further investigation into cetacean longevity will reveal that lifespans of over a hundred years are perfectly normal.

References:

Fontanella, J. E., Fish, F. E., Rybczynski, N., Nweeia, M. T., & Ketten, D. R. (2010). Three-dimensional geometry of the narwhal (Monodon monoceros) flukes in relation to hydrodynamics. Marine Mammal Science 27(4), 889-898. Available.

Garde, E., Heide-Jørgensen, M. P., Hansen, S. H., Nachman, G., and Forchhammer, M. C. (2007). Age-specific growth and remarkable longevity in Narwhals (Monodon monoceros) from West Greenland as estimated by Aspartic Acid Racemization. Journal of Mammalogy 88(1), 49-58. Available.

George, J. C., Follmann, E., Zeh, J., Sousa, M., Tarpley, R., Suydam, R. Horstmann-Dehn, L. (2011). A new way to estimate the age of bowhead whales (Balaena mysticetus) using ovarian corpora counts. Canadian Journal of Zoology 89(9), 840-852. doi: 10.1139/z11-057

George, J. C., and Bocktoce, J. R. (2008). Two historical weapon fragments as an aid to estimating the longevity and movements of bowhead whales. Polar Biology 31(6), 751-754. Available.

George, J. C., Bada, J., Zeh, J., Scott, L., Brown, S. E., O'Hara, T., & Suydam, R. (1999). Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Canadian Journal of Zoology 77, 571-578.

The Giant Turtle Therizinosaurus

Therizinosaurus, you look... unwell. Reconstruction by K. K. Fierova, from Maleyev (1954).

I am quite fond of old, weird reconstructions, and the initial classification of Therizinosaurus cheloniformis as a "turtle-like reptile"¹ resulted in the magnificent specimen above. So how could the veritable Jabberwocky we're all familiar with be misinterpreted to such a colossal degree?

¹ This odd phrasing is mirrored in the scientific name ("saurus" = lizard, "cheloniformis" = turtle-like). Malayev (1954) linked Therizinosaurus with members of Protostegidae and thus (probably) didn't intend to suggest another clade of reptiles which converged on turtles. Bizarrely, Rozhdestvensky (1974) claimed Malayev/Maleev classified Therizinosaurus as a "turtle-like pangolin"! Rozhdestvensky (1977) does not reiterate that statement, and further notes that another worker (Sukhanov) classified Therizinosaurus as a turtle; I unfortunately cannot find that source ("The subclass Testudinata" in Osnovy Paleontologii).

Therizinosaurus in its non-turtle form. From Wikipedia Commons.

Malayev (1954) described Therizinosaurus from scrappy remains: a metacarpal fragment, 3 manual unguals, and rib fragments (Zanno 2010). One of the ribs was an estimated 1.5 meters long when complete and was used to calculate a maximum body width of 3.25 meters (10'8") and body length of 4.5 m (14'9") (Malayev 1954); this is of course quite a bit larger than even the largest known Stupendemys geographicus. The rib was noted to lack costal elements, which is curious since turtle skeletons generally look like this:

 

Common Snapping Turtle (Chelydra serpentina) skeleton. Note the plastron is missing. From Wikipedia Commons.

Surprisingly, this is not necessarily a critical flaw, as (all?) turtles have distinct ribs during development before the carapace is fully formed (Wyneken 2001, fig. 90; Sánchez-Villagra 2009, figs. 3, 4). Malayev (1954) did not mention this nor the obvious possibility of a multi-ton hatchling. Instead, the "form of the ribs" was compared to Archelon and Protostega:

Archelon skeleton. From Wikipedia Commons.

The similarity is very general and Malayev (1954) does not list any specific shared characteristics. Due to the lack of costal elements, Malayev (1954) speculated that Therizinosaurus was in a distinct clade and in life had "barely developed or almost completely absent bony armor". It is incredibly strange that the Leatherback Seaturtle (Dermochelys coriacea) was not mentioned, as it entirely lacks costal elements and instead has thousands of dermal ossicles (Cebra-Thomas et al. 2005). The skeleton (sans ossicles) looks like an attempt by turtles to become "normal" tetrapods again.. until you notice the pectoral girdle within the ribcage:

From Wikipedia Commons

The rib material used to describe Therizinosaurus cheloniformis is apparently not from a therizinosaur at all, but a sauropodomorph (Zanno 2010 citing Rozhdestvensky 1970). Isn't it a major problem that the holotype is a chimera? Whatever the case, Therizinosaurus cheloniformis has been re-described a few more times and other rib material has been referred to the species (Zanno 2010). However, all of the diagnostic traits (and most of the material) are from the forelimbs (Zanno 2010).

From Wikipedia Commons.

Malayev (1954) interpreted the metacarpal and phalanges to be "powerful swimming organs" and suggested the huge claws were used for "cutting aquatic vegetation or for another functions, constrained by movement and acquiring food". The longest phalanyx was 60-65 cm long, not including the keratin covering (Malayev 1954), which suggests that the claws were ridiculously huge in life, even for a turtle-like reptile with a 4.5 meter body. I have observed turtles using their claws to climb and tear apart food (maybe what Malayev had in mind...), but clearly claws this disproportionate were doing something special. Something like this:

I like to think that Therizinosaurus, despite not being turtle-shaped anymore, waved its giant claws seductively in the faces of prospective mates.

References:

Cebra-Thomas, J., Tan, F., Sistla, S., Estes, E., Bender, G., Kim, C., Riccio, P., and Gilbert S. F. (2005). How the Turtle Forms its Shell: A Paracrine Hypothesis of Carapace Formation. Journal of Experimental Zoology 304B, 558-569. Available.

Maleyev, E. A. (1954). A new turtle-like reptile from Mongolia. Priroda 3, 106-108. Available.

Rozhdestvensky, A. K. (1977). The study of Dinosaurs in Asia. Journal of the Palaeontological Society of India 20, 102-119. Available.

Rozhdestvensky, A. K. (1974). History of the dinosaur fauna of Asia and other continents and questions concerning paleogeography. Transactions of the Joint Soviet–Mongolia Paleontological Expedition 1, 107–131. Available.

Rozhdestvensky, A. K. (1970). On the gigantic claws of mysterious Mesozoic reptiles. Palaeontological Journal 1, 131-141.

Sánchez-Villagra, M. R., Müller, H., Sheil, C. A., Scheyer, T. M., Nagashima, H., and Kuratani, S. (2009).  Skeletal Development in the Chinese Soft-Shelled Turtle Pelodiscus sinensis (Testudines: Trionychidae). Journal of Morphology 270, 1381-1399. Available.

Wyneken, J. (2001). The Anatomy of Sea Turtles. U.S. Dept Commerce NOAA Tech Mem NMFS SEFSC-470. Available.

Zanno, L. E. (2010). A taxonomic and phylogenetic re-evaluation of Therizinosauria (Dinosauria: Maniraptora). Journal of Systematic Palaeontology 8(4), 503-543. Draft Available.

A Giant Snapper At Last!

A common cliché in fringe anecdotes is that when eyewitnesses see something beyond belief, the camera has the lens cap on/no film/failed to work/been misplaced. Logically this should be taken as a strike against veracity... but I began to wonder otherwise when it happened to me. 

Of course, I've documented a big snapping turtle before, but my subsequent failures were astounding. I saw the turtles on multiple occasions this year (alluded to here), sometimes up close (touching, in fact) and once in triplicate. On all of these occasions I didn't bring my camera because I was commuting via bike, or the turtles fled before I could get their photographs. After a couple dozen failures, I gave up. Impulsively I decided on 8 November 2011 to take a trip searching for any reptiles or amphibians still active in the abnormally warm weather (about 70° F, 21° C) and saw this (plus a frog):

Blobturtle! I saw the turtle fairly clearly, but evidently my camera didn't. Rather than leave and be disappointed for a few months and then fail to see the turtles ever again, I realized I had no other option but to go in after it. Not only was the water very cold (it had snowed earlier in the year), it was murky and muddy and possibly had other snapping turtles I couldn't see. Gradually and with little subtlety, I made my way over to the turtle which had of course noticed me, but did not attempt to escape.

Remembering previous encounters and advice on pick-pocketing from Fagin, I approached the turtle from the rear, knowing it would eventually rotate around to defend itself. I also kept in mind how to fight the Cyberdemon from Doom - it's not just the shooting, it's the circle-strafing. With the cold water being slightly less of a hindrance for me, I managed to avoid something getting amputated. 

Getting closer, I confirmed my suspicions that, yes, this turtle is really really big.

The closest thing I could get to a measurement.

Eventually the turtle kicked up large amounts of silt and released gas (from... somewhere) and became impossible to see. I "ran" off, knowing that my luck in succeeding with this ill-conceived shenanigan was running out.

I know I'm never going to get an accurate length or weight measurement from this turtle... not without one or both of us getting hurt. Even if this specimen was a record (and there's no guarantee), it would not be worth risking the life of an old reptile to revise the SCLmax of 49.4 cm for Chelydra serpentina. From now on I'm leaving these turtles alone, my curiosity is satiated, and bothering them further will have no benefits. I'll have to live with the wonder that despite inhabiting a polluted body of water and having human hunt them and compete for their resources, things like this still exist.

Picture of the Indiscriminate Interval #000006b - Morone saxatilis

I can assure you this Nightmare Mode identification challenge is solvable. Okay, so maybe fish crania are rarely figured in the literature and this particular example was damaged before I could photograph it, but all the pieces are there, I swear!

Location is a major clue. The specimen was found far into Narragansett Bay in an area with a salinity of 30.0 ppt (Hicks 1959), which is right at the brackish-saline transition. Considering that this delicate structure was recovered intact, it seems probable that the fish died in the immediate vicinity. I think it's safe to conclude that the owner of the cranium was tolerant of marine and brackish conditions, which reduces the number of candidates considerably.

Then there's size. After having recently skeletonized a fish and being surprised at the comparatively puny cranium, I was startled to see a cranium around 6" (15 cm) long, when complete. Since it does not appear that any large local fish have a head less than 1/3 of the total length (yes, even American Angler and Oyster Toadfish) and since cranium ≠ head, I set a very conservative lower bounds of 50 cm (20"). This is still a massive body size and coupled with the presumed habitats, a very manageable number of candidates emerges. 

The Atlantic Sturgeon (Acipenser oxyrinchus) is anadromous and very large, however, the cranium is radically different. I cannot resist mentioning the bizarre proboscis-mouth. Atlantic Cod (Gadus morhua) are certainly large enough, however the cranium is not a match, despite being much more similar than that of the sturgeon. I have observed a large dead Tautog (Tautoga onitis) in almost the same locale, but cannot find the neurocranium illustrated anywhere. Before trying to acquire a dead Tautog and testing that hypothesis, I wondered if there was a better candidate I overlooked. I recalled seeing Striped Bass (Morone saxatilis) being caught nearby and photographs of local specimens which demonstrated that they reached colossal sizes fairly regularly. By sheer dumb luck, I stumbled across Jordan (1905) which had the cranium figured:

The supraoccipital (sagittal crest-like structure) and end of the snout strongly resembled the illustration below before being damaged.

Note that the mystery specimen still has an attached vertebrae. It seems somewhat wider than the Striped Bass cranium, but this could be due to damage, variation, or the illustration being inaccurate. 

The mystery specimen lacks the paired foramina (?) on the midline about  3/4 of the way up. Considering that the crania appear to be otherwise identical, maybe it was just weird shading or these fish are variable.

One odd difference aside, this is certainly the owner's species (being held):

From Wikipedia Commons.

The Striped Bass has some other relatives in the 'family' Moronidae and while a couple species in my area attain record lengths approaching 50 cm TL (Morone americana, M. chrysops), such sizes are apparently freakish and I doubt the crania would be large enough anyways.

My hat is off to anyone seriously working with fish skeletons. After my little tastes, I am completely and utterly traumatized. 

References:

Hicks, S. D. (1959). The Physical Oceanography of Narragansett Bay. Limnology and Oceanography 4(3), 316-327. Available.

Jordan, D. S. (1905). A Guide to the Study of Fishes. Volume 1. Henry Holt and Company: New York. Available.