Looking Good, Part I — Pectinate Claws (Avian Edition)

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Pectinate claw of the Great Egret (Casmerodius albus egretta) amongst the downy plumes.  Image credit: Yale Peabody Museum / Curious Sengi.

Astute birdwatchers might have noticed that some bird species have comb-like serrations running along one edge of a toe claw.  This feature, termed the pectinate claw, has long been assumed to be used just like combs we use for our own hair — to keep clean and look good.

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The Magnificent Frigatebird (Fregata magnificens), called the “Frigate Pelican” by Audubon, swoops down from the skies in this print from the masterwork “Birds of America.”  Image credit: John J. Audubon’s Birds of America at Audubon.org.

Upon seeing the Magnificent Frigatebird (Fregata magnificens), John James Audubon (1785 – 1851) remarked:

I have frequently observed the Frigate Bird scratch its head with its feet while on the wing; and this happening one day, when the bird fell through the air, as it is accustomed to do at such times, until it came within shot, I killed it when almost over my head, and immediately picked it up.  I had been for years anxious to know what might be the use of the pectinated claws of birds; and on examining both its feet with a glass, I found the racks [sic] crammed with insects, such as occur on the bird’s head, and especially around the ears. . . . I now therefore feel convinced, that, however useful this instrument may be on other occasions, it is certainly employed in cleansing parts of the skin of birds which cannot be reached by the bill (Audubon 1835).

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Pectinate claws emerge as a flange of the keratinous sheath.  They occur on the middle toe of each foot (Clayton et al. 2010; Bush et al. 2012).  Great Blue Heron (Ardea herodias).  Image credit: Yale Peabody Museum / Curious Sengi.

The function seems as self-evident to Audubon as it is to us — the pectinate claw combs out all those nasty ectoparasites (i.e., external parasites), especially the feather lice that eat precious down feathers.  Most birds have a little overhang at the tip of the beak for picking out and shearing apart lice, but a special foot comb would be ideal for reaching the head and neck areas inaccessible to the beak during preening (Clayton et al. 2010; Bush et al. 2012).  However, this tidy hypothesis quickly runs into some problems.

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The serrations of the pectinate claw can occur in a variety of shapes (Clayton et al. 2010), including the more curved, spatulate forms seen here in the Great Egret (Casmerodius albus egretta).  Image credit: Yale Peabody Museum / Curious Sengi.

The first is that pectinate claws occur only sporadically throughout the avian phylogenetic tree.  A review of 118 bird families found that only 17 possessed pectinate claws.  This was a diverse assemblage that included herons, nightjars, owls, frigatebirds, terns, grebes, and cormorants.  Curiously, only one family of passerines, the dippers (Clincidae), were observed to have pectinate claws; passerines  constitute the bulk of species diversity amongst birds.  Even so, within each family, only a handful of species might have this feature.  And within certain species, the appearance of the pectinate claw was variable among individuals (Clayton et al. 2010).

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The removal of ectoparasites is most widely believed to be the function of pectinate claws, but alternative hypotheses include roles in feeding, removing powder down, or straightening rictal bristles of the face (Clayton et al. 2010).  Detail of Montane Nightjar (Caprimulgus poliocephalus).  Image credit: Yale Peabody Museum / Curious Sengi.

So if the pectinate claw served such a vital function as stripping the feathers of harmful parasites, we should expect to find them consistently across a wide swath of bird diversity.  Instead, the pectinate claw seems to have evolved independently numerous times at very spotty intervals.

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The pectinate claw of the Barn Owl (Tyto alba insularis) becomes fully formed at about two years of age (Bush et al. 2012).  Image credit: Yale Peabody Museum / Curious Sengi.

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This captive barn owl demonstrates how handy it is to use your feet to groom your face!  Image credit: YouTube.

Another source of doubt cast upon the role of pectinate claws in removing ectoparasites comes from a study of Barn Owls (Tyto alba pratincola).  While owls with the most number of teeth on their pectinate claws were categorically the least likely to have lice infestations, there was no correlation between the number of lice and the number of teeth on the claw (Bush et al. 2012).  Foot claws are undoubtedly a critical tool in keeping a bird groomed, but given the rather ambiguous conclusions reached by researchers involved in these correlative studies, without experimental manipulation — e.g., filing off the teeth of the pectinate claw and comparing parasite loads between individuals  — there is little convincing evidence that pectinate claws function specifically to comb out ectoparasites (Clayton et al. 2010; Bush et al. 2012).

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Detail from Audubon’s color plate of the “Frigate Pelican”, which highlights his efforts to understand why frigatebirds have both pectinate claws and rudimentary partially-webbed feet.  How to explain this amalgamation of what he perceived as characteristically terrestrial and aquatic features?  Image credit: John J. Audubon’s Birds of America at Audubon.org.

As a coda, there is a fascinating tangent related to Audubon’s particular interest in the feet of the Magnificent Frigatebird.  His attention was drawn to the presence of the pectinate claw, a trait he considered characteristic of terrestrial upland birds, and the partially webbed feet characteristic of an aquatic animal.  According to Weissman (1998), Audubon was able to reconcile the presence of both features by seeing frigatebirds as a transitional form between land and seabirds.  While that relationship does not hold in light of modern analysis of anatomical and genetic characters, it is worth taking note that Audubon, like some of his contemporaries, was beginning to think in quasi-evolutionary terms well before Darwin.

References

Audubon, John James.  1835.  Ornithological biography, or an account of the habits of the birds of the United States of America.”  Vol. 3.  Edinburgh:  Adam & Charles Black.

Bush, Sarah E. et al. 2012.  “Influence of Bill and Foot Morphology on the Ectoparasites of Barn Owls.”  The Journal of Parasitology 98 (2):  256 – 261.

Clayton, Dale H. et al. “How Birds Combat Ectoparasites.”  The Open Ornithology Journal 3:  41 – 71.

Weissmann, Gerald.  1998.  Darwin’s Audubon:  Science and the Liberal Imagination.  Cambridge, MA:  Perseus Publishing.

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Mantles Most Splendid: Tridacna spp.

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Giant clams (Tridacna spp.) on display at the California Academy of Sciences in San Francisco.  There are more or less seven species of giant clams inhabiting the shallow tropical reefs of the Indo-Pacific (Klumpp, Bayne, & Hawkins 1991).  Image credit: California Academy of Sciences / Curious Sengi.

The elegant shapes and colorful patterns of shells often define the identity of the molluscs we encounter and gleefully collect.  But what we hold in our hands is a largely inert structure of calcium carbonate, devoid of its occupant, its essence incomplete.  What is missing are the squishy bits — the animal itself.  The soft tissues of clams and snails can be breathtaking in their colors and patterns.  One of the better known examples of this are the giant clams, Tridacna spp.

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Discarded shells of the largest clam in the world, Tridacna gigas.  Image credit: David Hall via Arkive.

Residing the shallow sunlit seas of the tropical Indo-Pacific, tridacnids are the largest clams in the world, with one individual measuring 1.4 m (4.6 ft) in length and 263 kg (863 lbs) in weight (Beckvar 1981).  While the shells have been collected as curios for their child-bathtub-sized novelty and undulating, fluted edges, there is little else that stands out about these shells.  What is mind-blowing about tridacnids are the vivid colors and patterns of iridescent blue, green, black, yellow, brown and violet of the exposed living tissue, the mantle.

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Tridacnid spotted off Thailand.  Image credit: Walkabout Alex.

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Get close to a world of color and fascination!  Detail of siphon and feathery gills.  Image credit: Fatherree via Reefs.com.

What makes these fleshy frills so psychedelic is a complex interplay between the tridacnid clam and its unicellular dinoflagellate symbionts called zooxanthellae.  The zooxanthellae primarily reside in the upper layers of tissue of the enlarged mantle and siphon, where they are exposed to sunlight and photosynthesize.  The simple sugars that are the result of photosynthesis — glucose and glycerol — are released into the bloodstream, thus providing a source of energy for the tridacnid (Goreau, Goreau, & Yonge 1973; Morton 1978; Fitt & Trench 1981; Wilkins 1986; Buck, Rosenthal, & Saint-Paul 2002).  Generally, clams are filter feeders, drawing in water and sorting out all the plankton and organic particulates for digestion.  While giant clams retain a fully functional and efficient filter feeding apparatus, the clear, nutrient-sparse waters of the tropics has likely driven the evolution of symbiotic relationships that provide alternate energy sources.  Adult tridacnids can probably sustain themselves on photosynthates alone and it is hypothesized that this influx is behind the spectacular growth rate of approximately 100 mm (4 in) per year observed in the species Tridacna gigas (Bonham 1965; Klumpp, Bayne, & Hawkins 1991).

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Zooxanthellae live as free cells into a branched tubular system running under the surface of the mantle and siphon tissue (Buck, Rosenthal, & Saint-Paul 2002).  Giant clams acquire symbiotic zooxanthellae through the environment; at around 20 to 25 days old, after the floating larvae settles into a more benthic post-metamorphic state, the clam ingests motile zooxanthellae.  How the symbionts are transferred from the stomach into the visceral and mantle tissues is unknown.  Growth accelerates after acquisition of symbionts (Jameson 1976; Fitt & Trench 1981).  Interestingly, free-living zooxanthellae will keep all products of photosynthesis inside their cell, but the presence of host tissues causes photosynthates like glucose and glycerol to be secreted, suggesting some kind of chemical regulation by the host (Muscatine 1967).  The purple spots are reflective iridophores.  Image credit: Science Photo Library via Getty Images.

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What does the nuclear tests off Bikini Atoll have to do with giant clams?   Bonham (1965) was able to calculate growth rates of T. gigas from Bikini Atoll by correlating dates of atomic tests and the deposition of radioactive strontium-90 in the growing shell.  Measuring from one radioactive growth line to the next, one specimen measured 10 cm long during the 1956 atomic tests and then 24 cm during the 1958 tests, indicating a growth rate greater than any other bivalve.  Image credit: Getty Images via The Independent.

So here is our first color component:  zooxanthellae use green chlorophyll and a red carotenoid called peridinin as photosynthetic pigments, rendering the single-celled organisms a brown or reddish-brown color (Fatherree 2007).

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T. squamosa.  Image credit: Wikimedia Commons.

The host clam itself generates accessory pigments — greens, browns, and yellows — that extend the range of usable wavelengths of light available for the symbiont’s photosynthesis (Fatherree 2007).  In addition, specialized cells (iridocytes) form clusters in the mantle called iridophores that act both as reflectors to redirect light into deeper tissue and as a sunscreen to prevent the zooxanthellae from getting fried from intense sun exposure.  Each iridocyte contains a stack of crystalline reflective platelets that scatter light, which makes pigments appear more vivid, creates those eye-popping electric blue-green colors, and makes the mantle shimmer with iridescence (Goreau, Goreau, & Yonge 1973; Griffths, Winsor, & Luong-Van 1992; Fatherree 2007; Todd, Lee, & Chou 2009).

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Iridescent sheen on the blue lip of this tridacnid.  Possible hybrid between T. noae and T. maxima.  Image credit: Jake Adams via Reef Builders.

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Blue-rimmed T. derasa.  Image credit: Ora Farm.

Photosynthetic pigments of zooxanthellae, accessory pigments and iridophores of the host tridacnid clam completes the palette of colors.  But how are these colors arranged into striped, spotted, and mottled patterns?  While variation in color is caused by localization of zooxanthellae (Todd, Lee, & Chou 2009), the pattern-generating mechanism remains unknown.  Despite some broad parameters of patterning seen between species, the role of genes remain ambiguous.  Offspring are observed to have a tremendous variety of colors and patterns different from their parents, suggesting a weak genetic link (Fatherree 2007).

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Bed of giant clams at low tide on Orpheus Island.  Image credit: goestaf via Panoramio.

Much of the tridacnid’s anatomy and behavior is focused on fostering the intimate relationship with their zooxanthellae symbionts.  The super-sized mantle and siphon blossom from the shell during the day and orient themselves to the light like flowers tracking the sun (Morton 1978; Wilkins 1986). This makes the exposed fleshy parts vulnerable to predation, especially from roaming fish looking for a quick bite.  Tridacnids do have several hundred well-developed pinhole eyes along the mantle and siphon that can detect shadows and moving objects, triggering immediate retraction and closing of the shell (Wilkins 1986; Land 2003; Todd, Lee, & Chou 2009).

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Giant clam researcher, Dr. Rick Braley, demonstrates a defensive response in T. gigas — squirting powerful jets of water upon tactile stimulus (Wilkins 986).  Image credit: Aquasearch.

However, responding to each threat by clamming up is hardly beneficial to the zooxanthellae that need to be exposed for hours a day for photosynthesis.  Todd, Lee, and Chou (2009) hypothesized that the colors and patterns of the mantle are actually cryptic, breaking up the outline of the animal and camouflaging it against the cluttered background of the reef.  High levels of morphological variation, i.e., polymorphism, is common in organisms inhabiting complex and unpredictable environments.  Analysis of RGB color values of mantles and background reef substrate indicate some color matching camouflage against fish predators with trichromatic color vision.  That a given set of parents spawns wildly polymorphic offspring might be a bet-hedging strategy that potentially some of the dispersing larvae will match their given substrate.  This also allows for colonization of a large range instead of being limited to one type of microhabitat for which they are a perfect background match.

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A study of color and pattern polymorphism in T. crocea by Todd, Lee, and Chou (2009) identified eight general color morphs in this species.  Larger individuals tended more towards greens and browns, while smaller individuals were vivid blue.  The researchers hypothesized a tradeoff:  that the blue structural color caused by iridophores act as a sunscreen that might be more vital to smaller clams than larger ones.  Image credit:  Todd, Lee, & Chou 2009.

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T. gigas and diver.  Image credit: Rick Hankinson via Wikimedia Commons.

Though the flamboyant mantles of tridacnids may serve to hide the clams from predators, they have captured the attention of human collectors.  Giant clams have long been an easily-accessible and prized food source for native Pacific Islanders.  With the opening up of global markets, tridacnid meat and shells have come into high demand, quickly exhausting local stocks (Jameson 1976; Benzie & Williams 1995; Foyle et al. 1997).  Overfishing has stimulated successful efforts at industrial-scale aqua- and mariculture (Klumpp, Bayne, & Hawkins 1991).  However, the heavy investment necessary to build large nursery facilities and the seven year growing time to bring species like Tridacna gigas to meat harvesting size was not within reach of many communities throughout the Indo-Pacific.  Instead, villagers have turned their attention to smaller species like T. crocea, T. maxima, and T. squamosa for the saltwater aquarium trade.  It only takes five to seven months for those species to reach a size suitable for shipping, making this an economical feasible option (Foyle et al. 1997).  The ability to breed tridacnids in captivity also creates opportunities to reseed depleted reefs (Beckvar 1981).

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T. maxima farmed for the aquarium trade.  More intense blue and green colors seem characteristic of smaller clams (Todd, Lee, & Chou 2009).  Image credit: PacificEastAquaculture via ReefEdition.

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Solomon Island local, Erik Koti, cleaning T. maxima and T. derasa in a family-run enterprise to raise giant clams for the aquarium trade.  Koti was trained by WorldFish Center and WWF in sustainable aquaculture methods.  Image credit: Jürgen Freund.

The success of raising tridacnids in captivity may have saved them from overfishing, but there is a new threat, one that impacts all marine creatures with photosynthetic zooxanthellae.  The symbiont in giant clams is a dinoflagellate named Symbiodinium microadriaticum, and this same species is supposedly found in all reef-building corals, many sea anemones, gorgonians (sea fans), and the Upside-Down Jellyfish, Cassiopeia (Fitt & Trench 1981).  With warming of ocean surface waters, symbiotic zooxanthellae are expelled, leaving their hosts bleached white.  One experiment recreated the conditions for an observed bleaching event on the Great Barrier Reef of Australia and determined that increased light intensity and water temperature were the main factors resulting in loss of zooxanthellae.  It is unclear whether the zooxanthellae are leaving or if they are being ejected by their hosts (Buck, Rosenthal, & Saint-Paul 2002).  In some cases, bleaching is a temporary loss of color that can last well over a year.  But in more severe cases, the damage is permanent — the spaces that once held zooxanthellae degenerate and the giant clam is left to struggle on its own, undoubtedly with poor outcomes (Norton et al. 1995).

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Localized bleaching in an animal for sale in the aquarium trade.  Stress from transport can cause loss of zooxanthellae.  Image credit: Fatherree via Reefs.com.

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Bleached and dead giant clam on Australia’s Great Barrier Reef.  Tridacnids derive the majority of their energy from their symbionts.  Rising water temperatures cause zooxanthellae to leave their hosts.  Image credit: Jake Adams via Reef Builders.

Incidence of coral reef bleaching is becoming more frequent and widespread.  This is not necessarily always fatal, but it does require immediate response to global climate change.

A clam is more than just its empty shell, to be discarded or set upon a shelf.  By delving into something as superficial as color and pattern, we have uncovered something about the essence of the tridacnid giant clam — the symbiotic relationship with zooxanthellae that is a vital focus of its form and function.

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Baby giant clams. Go, babies, go!  Image credit: Neo Mei Lin via Psychedelic Nature.

References

Beckvar, N.  1981. “Cultivation, Spawning, & Growth of the Giant Clams Tridacna gigas, T. derasa, & T. squamosa in Palau, Caroline Islands.”  Aquaculture 24:  21 – 30.

Bonham, Kelshaw.  1965.  “Growth Rate of Giant Clam Tridacna gigas at Bikini Atoll as Revealed by Radioautography.”  Science 149 (3681):  300 – 302.

Buck, Bela Hieronymous, Harald Rosenthal, & Ulrich Saint-Pail.  2002. “Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriactum and Tridacna gigas.”  Aquatic Living Resources 15:  107 – 117.

Fatherree, James W.  2007.  “Why Do Tridacnids Look the Way They Look?”  Tropical Fish Magazine April 2007.  Accessed 17 September 2016.

Fitt, William K. & Robert K. Trench.  1981.  “Spawning, Development, & Acquisition of Zooxanthellae by Tridacna squamosa (Mollusca, Bivalvia).”  Biological Bulletin 161:  213 – 235.

Foyle, Timothy P., J.D. Bell, M. Gervis, & I. Lane.  1997.  “Survial and growth of juvenile fluted giant clams, Tridacna squamosa, in large-scale grow-out trials in the Solomon Islands.”  Aquaculture 148:  85 – 104.

Goreau, T.F., N.I. Goreau, & C.M. Yonge.  1973.  “On the utilization of photosynthetic products from zooxanthellae and of a dissolved amino acid in Tridacna maxima f. elongate (Mollusca:  Bivalvia).”  Journal of Zoology 169:  417 – 454.

Griffiths, D.J., H. Winsor, & T. Luong-Van.  1992.  “Iridophores in the Mantle of Giant Clams.”  Australian Journal of Zoology 40 (3):  319 – 326.

Jameson, Stephen C.  1976.  “Early Life History of the Giant Clams Tridacna crocea Lamarck, Tridacna maxima (Röding), and Hippopus hippopus (Linnaeus).”  Pacific Science 30 (3):  219 – 233.

Klumpp, D.W., B.L. Bayne, & A.J.S. Hawkins.  1991.  “Nutrition of the giant clam Tridacna gigas (L.). I.  Contribution of filter feeding and photosynthates to respiration and growth.”  Journal of Experimental Marine Biology and Ecology 155 (1):  105 – 122.

Land, Michael F.  2003.  “The spatial resolution of the pinhole eyes of giant clams (Tridacna maxima).”  Proceedings of the Royal Society B 270:  185 – 188.

Morton, Brian.  1978.  “The diurnal rhythm and the processes of feeding and digestion in Tridacna crocea (Bivalvia:  Tridacnidae).”  Journal of Zoology 185:  371 – 387.

Muscatine, Leonard.  1967.  “Glycerol Excretion by Symbiotic Algae from Corals and Tridacna and Its Control by the Host.”  Science 156 (3774):  516 – 519.

Norton, J.H., H.C. Prior, V. Baillie, & D. Yellowless.  1995.  “Atrophy of the Zooxanthellal Tubular System in Bleached Giant Clams Tridacna gigasJournal of Invertebrate Pathology 66:  307 – 310.

Todd, P.A., J.H. Lee, & L.M. Chou.  2009.  “Polymorphism & crypsis in the boring giant clam (Tridacna crocea):  potential strategies against visual predators.”  Hydrobiologia 635:  37 – 43.

Wilkens, Lon A.  1986.  “Visual system of the giant clam Tridacna:  Behavioral adaptations.”  Biological Bulletin 170 (3):  393 – 408.

Joseph Leidy and The Little Turtles

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Image source: Wikimedia Commons.

To celebrate the beginning of a new school year, I wanted to share some fond memories students had of the great scientist and teacher, Joseph Leidy (1823 – 1891), who also celebrated a birthday a few days ago on September 9th.  It is difficult to describe Leidy in such a short space.  Among many other things, he was America’s first vertebrate paleontologist and early explorer of the West for fossils of large extinct animals, parasitologist who discovered the source of trichinosis in undercooked pork, accomplished microscopist who was among the first to apply medical forensic evidence in a murder trial, scientific artist, and an all around nice guy (Warren 1998).  Leidy is largely lost to us today because he was a true and gracious gentleman, a misfortune in a world where scandalous personalities have an infinitely longer shelf life.

But Leidy had a lasting impact on those who met him.  Paleontologist William Berryman Scott (1858 – 1947) recalled the frantic, anxious days of being a young scientist:

We were constantly running to Philadelphia and the Academy to see Leidy’s types to compare our material with that which he had described and named, and to ask his advice and help.  And, though we were mere tyros, beginners, utterly insignificant, he was invariably kind and considerate and thoughtful, and as lavish in the gift of his time, as though he had nothing else to do. . . . He had that sweetness and gentleness of personality that are so attractive when united with greatness.  I have known a few great men in my life, and without exception they have been men of extraordinary simplicity, without any airs, or graces (William Berryman Scott 1923; quoted in Warren 1998).

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Young Leidy brooding next to a Hadrosaurus leg bone.  Image credit: Mike Hardcastle at Cosmic Polymath.

Perhaps one of them most enduring stories about Leidy’s personality comes from his days teaching at a small liberal arts college in the suburbs of Philadelphia:

I heard no long ago, a story about one of our own naturalists, Dr. Joseph Leidy.  The little incident took place during the time he was actively connected with Swarthmore College.  Wishing to make some study or observations with regard to turtles, he obtained some of them from a pond near the college, saying, as he took them up, ‘I’ll bring you back again, little turtles.’

When he reached his home in the city, he found word awaiting him which necessitated an almost immediate trip abroad; but, however pressing his business was, it did not cause him to forget his promise to the little turtles.  The next day was Sunday, and, having no other time to fulfill his promise, he determined to do it then.  And now another obstacle arose.  There was no train which he could conveniently take.  But true to that old adage, ‘Where there’s a will, there’s a way,’ the doctor walked out to the college, a distance of about ten miles and restored the turtles to their home.  From this little act alone we see how great must be the kind-heartedness of the man and his faithfulness to his word (The Swarthmore Phoenix, 1 December 1888).

This anecdote has been told and retold with occasional embellishment, but the essence is always the same.  Here is a human being who exercised his curiosity about Nature, but understood the responsibility to prevent unnecessary harm.  He felt such empathy and respect for Nature, that even a seemingly silly promise to some lowly reptiles was to be faithfully honored.  And if Leidy was willing to walk out ten miles just to return some turtles into a pond, how far would he go to help a student, friend, or colleague?  Whether we are the students or the teachers (or both), let us always remember what it is like to be the little turtles and how far fulfilling a promise can go.

What stories do you have about your favorite teachers?

Tortoises, terrapins, and turtles London, Paris, and Frankfort :H. Sotheran, J. Baer & co.,1872. http://www.biodiversitylibrary.org/item/21827

Thanks, Dr. Leidy!  We don’t know exactly what kind of animal Leidy returned to the waters of Crum Creek that borders the Swarthmore College campus, by Emys geographica is a North American native with some geographical distribution in Pennsylvania.  Image credit:  Tortoises, terrapins, and turtles.  1872.  London, Paris, and Frankfort:H. Sotheran, J. Baer & Co. via Biodiversity Heritage Library on Flickr.

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For a number of years, students at Swarthmore College renamed their scientific society in honor of the beloved late Professor Leidy.  Image credit:  Swarthmore College, Halcyon 1897.

References

The Swarthmore Phoenix.  “A Reminiscence of Dr. Leidy.”  The Swarthmore Phoenix [Swarthmore, PA].  1 December 1888:  76.

Warren, Leonard.  1998.  Joseph Leidy:  The Last Man Who Knew Everything.  New Haven, CT:  Yale University Press.

Snips and Snails and Coelacanth Tails

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Fossil and model reconstruction of the Late Triassic coelacanth, Diplurus newarki, commonly found in New Jersey and Pennsylvania.  The model was designed by vertebrate paleontologist Bobb Schaeffer.  Image credit: Yale Peabody Museum / Curious Sengi.

From fossil to the end of a fisherman’s line, the scientific discovery of a living coelacanth in December 1938 is a favorite story of resurrection, determination of a young curator — Marjorie Courtenay-Latimer (1907 – 2004) — at the East London Museum in South Africa, international political intrigue, and intense excitement over what this living (and largely unchanged) representative of an ancient lineage could reveal about the origins of tetrapods like us.

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A living coelacanth, Latimeria chalumnae, generally indifferent to paparazzi and awed divers.  Image credit: Projet Gombessa via X-Ray Mag.

Courtenay-Latimer famously describes her initial encounter with a coelacanth that was hauled into a local fish market:

I picked away at the layers of slime to reveal the most beautiful fish I had ever seen.  It was five foot long, a pale mauvy blue with faint flecks of whitish spots; it had an iridescent silver-blue-green sheen all over.  It was covered in hard scales, and it had four limb-like fins and a strange puppy dog tail.  (Quoted from Amemiya, Dorrington, & Meyer 2014.)

Courtenay-Latimer sketch

Marjorie Courtenay-Latimer included this sketch in a letter sent to J.L.B. Smith, requesting his help in identifying an unusual fish brought in as by-catch on a local fishing vessel.  Note that Courtenay-Latimer drew the tail (labeled “caudal fin” here) twice to bring attention to that distinctive feature.  Image credit: African Coelacanth Ecosystem Programme (ACEP)/ South African Institute for Aquatic Biodiversity (SAIAB) via Twitter.

Uncertain what to make of this strange fish, Courtenay-Latimer writes to a scientific colleague and accomplished amateur ichthyologist, J.L.B. Smith (1897 – 1968).  Her sketch of the mystery animal sealed the deal — Smith identified it as a coelacanth, a fish believed to have been extinct since the Late Cretaceous, about 70 million years ago (Amemiya et al. 2013).  Key features to this thrilling recognition was the presence of muscular limb-like fins and the unusual “puppy dog tail” (Hissmann & Fricke 1996).

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Courtenay-Latimer and the fish that shook the world.  Confounded by the Christmas holidays and locals reluctant to have anything to do with this quickly decomposing, oily fish, this young curator managed to convince a taxidermist to salvage the skin.  Courtenay-Latimer remained an active and beloved part of the coelacanth research community until her death at age 97.  Image credit: Wikipedia.

The paired lobe fins were of great interest.  There were four of them, each one filled with muscle and bone and attached to the central, axial skeleton by a rudimentary limb girdle.  Smith made early speculations on the pattern of movement of these lobe fins (Fricke & Hissmann 1992).  It was hypothesized that the fin strokes would be homologous to how animals walk on land and that the coelacanth was pushing itself along the ocean floor with its limb-like fins (Fricke et al. 1987; Fricke & Hissmann 1992; Forey 1998).

Observations of live animals in their deep water habitats showed that coelacanths do not trot around the sea bottom at all, but instead favor life as drifters in the current or generally remaining in the same place, only making the occasional fast start to change direction or lunge towards a tasty item (Fricke et al. 1987; Uyeno 1991; Forey 1998).  While the lobe fins do move alternatively like legs, these are probably acting more as stabilizers.  Most of the slow, forward movement is propelled by the second dorsal and first anal fins sculling in unison (Fricke et al. 1987; Uyeno 1991; Fricke & Hissmann 1992).  This is very unlike many fish familiar to us that rely on their tails or the side-to-side lateral flexures of the body to generate forward thrust (Hissmann & Fricke 1996).

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The coelacanth propels itself forward using its second dorsal and first anal fins, as marked by the arrows.  These two fins beat in unison.  This mode of swimming is very similar to that found in [the completely unrelated] Ocean Sunfish (Mola mola).  The paired pectoral and pelvic fins serve more to stabilize the animal.  Image credit: YouTube.

But what about that weird tail with the little tuft at the end?  The presence of this odd mini-tail, giving the caudal fin an overall tri-lobed appearance, is utterly unique to coelacanths.  Variously termed the supplementary lobe, accessory lobe, terminal lobe, caudal tuft, etc., here we will call it the epicaudal lobe.  It appears as a distinct lobe with a plume of fin rays and occupies a place between the upper and lower halves of an otherwise nearly symmetrical tail (Hissmann & Fricke 1996; Forey 1998) and apparently “varies greatly in size among different individuals (Uyeno 1991).”  The epicaudal lobe is capable of moving independently of the rest of the tail, with a range of flexure up to 90° perpendicular to the main body axis (Fricke et al. 1987; Fricke & Hissmann 1992; Hissmann & Fricke 1996).

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Detail of the epicaudal lobe of the coelacanth Latimeria menadoensis from Indonesia.  Image credit: Seapics.com.

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Skeleton of a modern coelacanth on display at the Naturhistorisches Museum in Vienna, Austria.  Both the sensory lateral line and the notochord extend to the end of the epicaudal lobe.  The notochord is a flexible dorsal rod that acts as a developmental and evolutionary precursor to the vertebral column; this structure is retained in adult coelacanths.  Image credit: Fuck Yeah Coelacanths! on Tumblr.

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An especially long epicaudal lobe preserved in the Late Triassic Diplurus sp.  Image credit: Yale Peabody Museum / Curious Sengi.

In 1948, paleontologist Bobb Schaeffer (1913 – 2004) remarked that:  “It is difficult to visualize a separate and distinct function for the supplementary caudal [i.e., epicaudal] in spite of its morphological discreteness.”  And so it seems to stand.  Thorough analysis of video footage by Hans Fricke and Karen Hissmann demonstrate that the epicaudal is not coordinated with the movement of any other fins.  Neither does it move continuously.  It just seems to carry on in its own idiosyncratic way.  At best, it movements of the epicaudal appear to be correlated to making tight turns around obstacles or rotating in place, including maneuvers to position the coelacanth into the infamous “headstand” posture that baffled researchers for years.  So the epicaudal could act as a sort of small rudder involved in fine-scale adjustments.  However, given the relatively minuscule surface area presented by the epicaudal, it seems unlikely that it generates enough thrust force to contribute to locomotion (Fricke & Hissmann 1992; Hissmann & Fricke 1996).

Fricke & Hissmann obstacle turning

The coelacanth only employs its broad tail for fast starts and forward acceleration, which is usually not the preferred pace of life for this relaxed drifter.  In this figure, a coelacanth maneuvering around an obstacle was observed flexing the epicaudal lobe towards the obstacle, perhaps acting as a fine-tuned rudder.  But, for the most part, the epicaudal lobe seems to have a mind of its own.  Image credit:  Fricke & Hissmann 1992.

Fricke & Hissmann headstand

Movements of the epicaudal lobe have also been correlated to bringing the coelacanth into the bizarre headstand position.  Researchers now believe the headstand is meant to bring electrosensory receptors on the face closer to the substrate, where tasty prey items may be located.  Both this figure and the preceding one are tracings from video footage of live animals.  Image credit: Fricke & Hissmann 1992.

There was one more observation about the epicaudal lobe in living coelacanths.  The epicaudal had a tendency to be held at this 90º bent position while the fish was stationary.  This lead Hissmann and Fricke to hypothesize a sensory function for the epicaudal.  The pressure-sensitive lateral line of fish usually runs the length of the body and terminates at the base of the tail, right before the fin rays.  In coelacanths, the well-developed lateral line extends to the very tip of the tail through the epicaudal.  By kinking the epicaudal lobe perpendicular to the main axis of the body, it would be possible to pick up sensory cues about water movement not just hitting the sides of the body, but also in the fore and aft direction.  Having spatial awareness of movement in relationship to water currents would appear to be especially adaptive for keeping the coelacanths positioned in the narrow little caves they favor as resting spots (Hissmann & Fricke 1996).

Schaeffer coelacanth outlines

Body outlines of coelacanths from the Carboniferous period to the Late Cretaceous to the present day.  Very little has changed over 300 million years.  Or has it?  Image credit: Schaeffer 1948.

Here’s a final curiosity from the fossil record.  The coelacanth lineage is famous for having a generally unchanged body plan since its origins 300 million years ago, which led scientists to view them as slow evolving and essentially morphologically static (Forey 1998; Amemiya et al. 2013).  And the strange little epicaudal lobe was there from the beginning.  We do not know what function the epicaudal served over millions of years, but it quite certain that ancient coelacanths were not all just huddling in deep water caves.  An exceptional example is the Early Triassic coelacanth from British Columbia, Canada:  Rebellatrix divaricerca.  Unlike the long line of coelacanths before and after it, R. divaricerca was slender and had a deeply forked tail, indicative of fast swimming in open water.  Even so, a very distinct epicaudal was still present (Wendruff & Wilson 2012).

Wendruff & Wilson Rebellatrix paratype fin

Fossil of the paratype for Rebellatrix divaricerca, an Early Triassic coelacanth with a highly unusual forked tail.  The boxed area marked “D” shows the epicaudal lobe.  Image credit: Wendruff & Wilson 2012.

Wendruff & Wilson Rebellatrix reconstruction

Reconstruction of the fast, sleek Rebellatrix divaricerca.  Image credit: Wendruff & Wilson 2012.

Ultimately, the function of the epicaudal lobe remains unknown.  Perhaps this is unsurprising.  Between 1938 and 2014, less than 300 coelacanths have been captured and studied.  Observing the animals in their natural environment usually necessitates the use of submersibles or remotely-operated vehicles (ROVs), though there is one population in Sodwana Bay, South Africa that lives within reach of SCUBA divers (Amemiya, Dorrington, & Meyer 2014).

What is particularly alarming is that the species of coelacanth discovered by Marjorie Courtenay-Latimer, named Latimeria chalumnae in her honor, is now listed as being Critically Endangered (Musick 2000).  A second species, L. menadoensis, also serendipitously discovered in a fish market in Indonesia in 1997, is even less understood and listed as Vulnerable (Erdmann 2008; Amemiya, Dorrington, & Meyer 2014).  The mystery of the coelacanth’s “puppy dog tail” endures, along with other fundamental questions about breeding biology, behavior, and ecology.  There is so much left to learn.  Coelacanths are also amongst our closest living fishy relatives.  Let’s allow curiosity and kinship to keep this 300 million year old lineage going strong!

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How can you not love this wonderful face?  Image credit: Laurent Ballesta via National Geographic.

References

Amemiya, Chris T., R. Dorrington, & A. Meyer.  2014.  “The Coelacanth and Its Genome.”  Journal of Experimental Zoology (Mol. Dev. Evol.) 322 (6):  317 – 321.

Amemiya, Chris T. et al.  2013.  “The African coelacanth genome provides insights into tetrapod evolution.”  Nature 496:  311 – 316.

Erdmann, M.  2008.  “Latimeria menadoensis.”  The IUCN Red List of Threatened Species 2008.  Accessed 4 September 2016.

Forey, Peter.  1998.  History of the Coelacanth Fishes.  Londong:  Chapman & Hall.

Fricke, Hans & Karen Hissmann.  1992.  “Locomotion, fin coordination and body form of the living coelacanth Latimeria chalumnae.”  Environmental Biology of Fishes 34:  329 – 356.

Fricke, Hans, O. Reinicke, H. Hofer, & W. Nachtigall.  1987.  “Locomotion of the coelacanth Latimeria chalumnae in its natural environment.”  Nature 329:  331 – 333.

Hissmann, Karen & Hans Fricke.  1996.  “Movements of the Epicaudal Fin in Coelacanths.”  Copeia 1996 (3):  606 – 615.

Musick, J.A.  2000.  “Latimeria chalumnae.”  The IUCN Red List of Threatened Species 2000.  Accessed 4 September 2016.

Schaeffer, Bobb.  1948.  “A Study of Diplurus longicaudatus with Notes on the Body Form and Locomotion of the Coelacanthini.”  American Museum Novitates 1378:  1 – 32.

Uyeno, Teruya.  1991.  “Observations on locomotion and feeding of released coelacanths, Latimeria chalumnae.”  Environmental Biology of Fishes 32:  267- 273.

Wendruff, Andrew J. & Mark V.H. Wilson.  2012.  “A Fork-Tailed Coelacanth, Rebellatrix divaricerca, gen. et sp. nov. (Actinistia, Rebellatricidae, fam. nov.) from the Lower Triassic of Western Canada.”  Journal of Vertebrate Paleontology 32 (3): 499 – 511.