Tiger Lilies Are What's Up

I hesitate to sing the praises of a flower that’s a non-native (to North America), but the spectacular Tiger Lily, Lilium lancifolium Thunb., has managed to steal the show this past week.  I usually have eyes only for those wildflowers, particularly the native ones, that grace the railroad bank and roadside a short walk from my summer cottage on the North Fork of Long Island.  Unfortunately, mowing crews came through several weeks ago and did a particularly thorough job.  Recovery has been slow with flowers from an alien, Chicory (Chicorium intybus), and a native, Daisy Fleabane (Erigeron annuus), among those only just now beginning to reappear.  As a result, the real action has shifted to a nearby yard where Tiger Lilies, imports from Japan and China, have been on display.

The vagaries of taxonomy and the characters who cast themselves as taxonomists tend to make taxonomic histories worth exploring.  So it is with the Lilium lancifolium.

Until recently, the accepted scientific name assigned to Tiger Lilies was Lilium tigrinum Ker Gawl., a name dating from 1809.  But, apparently, the plant described in 1794 by Swedish naturalist and Linnaean disciple Charles Peter Thunberg in the Transactions of the Linnean Society (Botanical Observations on the Flora Japonica) is now accepted as having been a Tiger Lily and so, Thunberg’s name for the flower has precedence over English botanist John Bellenden Ker’s 1809 effort.

The scientific name of the flower in question isn’t the only name marked by uncertainty.  Though I’ve chosen to call the botanist John Bellenden Ker, it’s not clear to me what name I should use for him.  More on the source of this confusion in a moment.

That I’m a bit puzzled by Thunberg’s description of Lilium lancifolium is not surprising.  It is, of course, written in Latin, and Google Translate did a very poor job, stymied by the abundant botanical terms.  Armed with Jason Hollinger’s Plant Latin Dictionary and my two years of high school Latin, I got enough out of the description to have a quibble with Thunberg's description and a wee doubt as to whether what he was describing is what I’m seeing.  He wrote that the corolla (the structure made up of the flower’s petals) is subcampanulatis which I translate as “nearly bell-shaped.”  To my mind there’s nothing sub about the campanulatis nature of the Tiger Lily corolla.  The flower hang down, fully bell-like.

Too bad there is no drawing of the specimen described in Thunberg’s article, as there is in the 1809 publication in which Bellenden Ker offered up his choice of name for the flower.

Bellenden Ker is the stuff of fiction (perhaps a romp by Henry Fielding or George MacDonald Fraser).  John Bellenden Ker (1765? – 1842) was born John Gawler.  He was forced to resign his military commission in 1793 because, according to the National Biographical Dictionary (Volume 31, 1892), he “displayed sympathy with the French revolution.”  In 1804, he changed his name to Ker Bellenden (Bellenden was his mother’s maiden name).  Curiously, he was apparently forthwith known as “Bellenden Ker.”  The name change was part of an effort by his second cousin William, seventh baron of Bellenden and fourth duke of Roxburgh, to ensure that his estate and titles went to John.  But, after William’s death, protracted litigation thwarted those intentions.  The National Biographical Dictionary noted, in its usual understated way, that, John Bellenden Ker “was long known as a wit and man of fashion in London.  Many stories were told of the charm of his conversation, and he was the hero of some ‘affairs of gallantry.’” (p. 52)

In botanical names attributable to him, his name is abbreviated “Ker Gawl.”  A beautiful illustration of what are clearly Tiger Lilies accompanies his 1809 article in Curtis’s Botanical Magazine.  (The publication from which I acquired this image is dated 1810, but, since it contains volumes 31 and 32 of Curtis’s Botanical Magazine, I assume the 1809 date widely cited is correct for the 31st volume.)

Now, Bellenden Ker knew about Thunberg’s work, but, apparently, concluded that his was a separate species.  He characterized as “erroneous” botanist Carl Ludwig Willdenow's attempt to label Lilium tigrinum a synonym for “Thunberg’s lancifolium.”  As for the specific plant depicted in the illustration, Bellenden Ker wrote, “Our drawing was made from a plant in Mr. Salisbury’s Botanic Garden, Sloane-Square.”  (I really like this kind of arcane and largely irrelevant detail.)

Here, then, are several photographs of the small nearby stand of Tiger Lilies that seduced me these past few days, at least until a full day of rain beat down many of the blossoms.  It wasn’t until later, after handling the flower, that I realized the anthers on the ends of the dangling stamens had covered my hands and pants with a sticky rust colored pollen.

As for the last photograph, it was taken because, not having ever really paid attention to these flowers, I had hoped that when I peered into a corolla I would spot the tell-tale green star outlined by the base of petals that marks the native Turk’s-Cap Lily (Lilium superbum L.).  But, it wasn’t there.  No need to comment on the common name of this particular lily, but the scientific name merits a couple of parting remarks.  First, the “L.” following the name is the abbreviation for Linnaeus who named it – a very fine pedigree.  Second, I stumbled over the species name until I realized that the accent is on the second syllable, not the first (try it) – superbum is Latin for “haughty” or “proud.”

The Turtle Essentials

Scene:  Beck Bennett is seated with a group of children.

Beck Bennett:  What’s something that’s slow you wished was fast?
Austin:  Turtle.
BB:  Really?  A turtle?
Austin:  Yeah.
Girl seated next to Austin raises her hand.
BB:  What about you?
Girl:  I’d rather be a slow turtle.
BB:  Wha . . . ummmmm.
Girl:  I know why.  Because when you’re slower you won’t have to get in the street as fast and get ran [sic] over.
BB:  But if you’re a slow turtle and you’re in the middle of the street, what happens?  Austin.
Austin closes his eyes and slaps his forehead with his hand.
BB:  Exactly.

I thoroughly enjoy ATT’s “It’s Not Complicated” series of ads, but this particular one makes me wince.

I wrote last year of an unexpected visit from an Eastern box turtle (Terrapene carolina) in the woods near my rundown summer cottage out on the far end of Long Island, New York, the so-called North Fork.  This visitor, I noted, was the first of its kind in several years.  This month, during my first bike ride of the year along the bay near my cottage, I came upon two turtles who had failed in their attempts to cross the road.  I hurried past.  The only positive interpretation of these ruined bodies that came to mind was that there are more turtles around than there have been.  Somehow I doubt it.

But, a day later, while standing at the kitchen sink washing dishes, I happened to look out the window.  There, near a back wheel of a potential agent of turtle death (i.e., my lawnmower which had refused all my entreaties to start) was a very alive, very remarkable (they all are) turtle who had paused in his journey across the yard.

I came out and knelt beside him, photographed him, moved around to get a better angle – all the while, he (perhaps she, I didn’t inspect the base of his tail closely) kept an eye on me, but made no effort to retreat into his shell.

As I watched him, I stumbled over the obvious, something I’d never considered before but which was always right there – turtles all have the same body plan whatever their ilk – terrestrial, freshwater, brackish water, or seawater.  These different groups of turtles, evolved to live in different environments, are all turtles.  Yes, there have been some changes, perhaps foremost, land turtles have legs with claws for walking, sea turtles have flippers for swimming.  But, regardless, every turtle taxon is recognizably turtle qua turtle.  I also realized that the turtle’s evolutionary journey between land and water was unlike the one traveled by whales because the latter’s move to the sea left no obviously whale analog lumbering along on land, nor did the whale return to the land to fashion that terrestrial analog.

So, what was the turtle’s experience?  Where did it originate?  In the water?  On the land?  What does the fossil record have to say about that?

I have learned that, in general, these are all open and debated questions.  We (the curious, the scientist) are in the midst of an argument, a scientific argument.  In the last few years, our knowledge of early turtles has grown, but without prompting a general consensus as to origins.  It is, from my uninformed vantage point, an inspiring state of affairs – one can watch science at work.

The discussion of origins partly involves finding the turtle’s nearest ancient relatives and seeing if they were land or water based.  There is no agreement on a single candidate for this sister-group.  The hunt for transitional fossils continues apace, whether those might be newly discovered or might be discerned among existing fossil groups.

Frankly, in my haphazard and only marginally informed reading of the scientific and popular literature on this subject, I am beginning to think that, at its heart, lies the fundamental question – what, in the first place, actually constitutes a turtle?  What’s essential for an entity to be considered a turtle?  The shell?  All of one, part of one?  The quest for the origin seems centered on deciding at what point an evolving reptile became a turtle (and did that occur on land or in the water?) and at what earlier point did the initial inklings of turtlehood (whatever those might be) emerge (again, terrestrial or aquatic?).

What follows are a few of what, for me, are the most startling aspects of where science appears to be on the turtle’s origin and where that occurred.  (I have not bothered attaching the titles of the resources I cite to links, partly because several lie behind paywalls.)  For a long time, the basis in the fossil record for analyzing turtle origins was primarily Proganochelys quenstedti, a fossil turtle dated from the Triassic.  (Robert R. Reisz and Jason J. Head place it at between 206 to 204 million years ago.  (Turtle Origins Out to Sea, Nature, November 27, 2008, p. 450.))  Proganochelys looked an awful lot like today’s snapping turtle, complete with shell and that was (perhaps still is) a problem.  To get a sense of the magnitude of this issue, consider what biologist James R. Spotila, wrote in 2004:

Proganochelys literally pops into the fossil record as a completely formed turtle.  Its immediate ancestors are unknown and there is no known transitional animal between other reptiles and turtles.  Given that early turtles lived in the water and their shells would have readily fossilized in the mud, it is puzzling that no fossils of turtle precursors exist.  (Sea Turtles:  A Complete Guide to Their Biology, Behavior, and Conservation, 2004, p. 57)

The crux of the matter apparently is largely the shell which in Proganochelys appears full blown.  The turtle shell is composed of three elements, a carapace (the part carried on the turtle’s back), a plastron which covers the underbelly, and a bridge which links those top and bottom plates.  Spotila decided a turtle with a shell really did happen upon the scene suddenly, in “one or two evolutionary leaps.”  (p. 58)

The “instantaneous” evolution solution to this problem in the fossil record seemed to me to be a bit like the “and then a miracle occurred” way of dealing with the issue.  Indeed, ecologist and MacArthur Fellow Carl Safina thought the magnitude of the required changes argued against a couple of “evolutionary leaps.”  In The Voyage of the Turtle:  In Pursuit of the Earth’s Last Dinosaur (2006, a somewhat hyped title), he wrote:

Achieving a shell like that [of the turtle] requires extensive bodily rerigging that doesn’t evolve overnight – moving the shoulder inside the ribs, for example, and devising a way to breathe through lungs locked within a pair of hard plates.  Such a radical makeover takes what turtles had:  time.  (p. 21)

The changes required in a reptilian body plan to evolve a turtle figure directly in the debate over the place of origin – water or land.  When they considered what modifications were needed to yield up a turtle, biologist Olivier Rieppel and paleontologist Robert R. Reisz (The Origin and Early Evolution of Turtles, Annual Review of Ecology and Systematics, Volume 30, 1999) concluded that an aquatic setting was the logical one.  “It would seem difficult to simultaneously derive the turtle mode of respiration and locomotion in a terrestrial environment that requires continuous body support.  By contrast, the aquatic environment provides buoyancy, which greatly facilitates both body support and locomotion.”  (p. 15)  The plastron also fit with a water origin because the necessity for protection of the underbelly would be greater for a swimmer than a four-legged walker.  Still, this is not a uniformly embraced position.  Biologist Michael S.Y. Lee (Correlated Progression and the Origin of Turtles, Nature, February 29, 1996) looking at possible sister-groups to the turtles found turtle-like morphologies in certain terrestrial pareiasaurs (herbivorous reptiles protected by scutes or bony plates) that suggested they were closely related to turtles.  Further, he explained how interactions among gradual changes in pareiasaur morphology (i.e., correlated progression) might tend “towards ‘turtle-ness’.”  In this scenario, terrestrial origin and measured alterations yield turtle.

The debate over origins shifted from Proganochelys to Odontochelys semistestacea in 2008.  Paleontologist Chun Li, et al. (Olivier Rieppel is one of the “et als”) described a fossil turtle from the Late Triassic, some 220 million years ago (An Ancestral Turtle From the Late Triassic of Southwestern China, Nature, November 27, 2008).  The striking aspect of Odontochelys is that it had a fully developed plastron but lacked a fully developed carapace.  Half a shell, and the bottom half at that.  This turtle was not only older but more primitive than Proganochelys, for instance, it had teeth.  To Li et al., these fossil remains, which were deposited in a marine environment, showed that turtles developed the plastron before the carapace and that they likely had an aquatic beginning.

Reisz and Head (Turtle Origins Out to Sea, cited above) dissented, and raised the issue of the direction in which this transitional fossil might have been headed evolutionarily.  They asked, could Odontochelys have been a stage in the process of modifying a complete turtle shell making it more suitable for an aquatic existence?  The carapace, they posited, wasn’t lacking but, rather, had been reduced.  This turtle could, therefore, have been part of a radiation from land to sea.  If Reisz and Head are correct, then possibly waiting in sedimentary rock somewhere are fossils of a still earlier land turtle with a complete shell.

I enjoy this process of proffering alternative interpretations of data.  There is a bite and cleverness in the exchange.  Who can make the most logical, most persuasive argument based on the data at hand?

Evolutionary biologist (and general provocateur) Richard Dawkins, in The Greatest Show on Earth:  The Evidence for Evolution (2009), considered the debate over Odontochelys and came down foursquare with the water origin camp.  That the plastron was fully developed made absolute sense for an aquatic origin – the plastron providing protection against predators swimming from below.  More significant to him was that, if Odontochelys were developing a complete shell, this meant that there were at least two evolutionary episodes of turtle movement from water to land.  Dawkins looked at Proganochelys (and Palaeochersis, another ancient turtle) which were on land 15 million years after Odontochelys with fully developed shells.  This, he surmised, meant that, in this 15 million year window, sea turtles with fully developed shells moved onto land, giving rise to Proganochelys and Palaeochersis.  “But, wait!  There’s more!”  Dawkins noted that these land turtles had gone extinct and were not the forbearers of Testudinidae, modern land dwelling turtles.  So, there was another, later, journey from sea to land, giving rise to Testudinidae.  And, he added, what of fresh water and brackish water dwelling turtles?  Way stations on a movement from sea to land?  Or, perhaps, separate movements?

Despite the breathlessness with which Dawkins described his conclusion about multiple loops between sea and land, I would note that the notion of multiple returns to land or sea by turtles apparently has been rather accepted stuff.  Carl Safina, considering the evolution of sea turtles, identified three movements from land to sea – one during the Jurassic and two during the Cretaceous.

And, so, the debate continues with analysis and reanalysis of data offering up different hypotheses of which groups are sister-groups to turtles and which earlier reptiles might exhibit those initial marks of “turtleness” (e.g., Tyler R. Lyson, et al., Transitional Fossils and the Origin of Turtles, Biology Letters, 2010).  Analysis of turtle genomes speaks to this debate, (e.g., Zhuo Wang, et al., The Draft Genomes of Soft-Shell Turtle and Green Sea Turtle Yield Insights Into the Development and Evolution of the Turtle-Specific Body Plan, Nature Genetics, June, 2013), but I struggle to understand its insights.

I am left with my questions unanswered, but they are now wonderfully enveloped in context.  And, of course, I remain convinced of how remarkable the turtle is.

As the turtle, who paused in my backyard, continued on his way with his awkward gait (see video below - I hope it works), I do have to think that an aquatic origin might be in the cards.  A cardinal's song signals the turtle's departure, as do, prophetically, the sounds of nearby construction.