Wednesday, May 1, 2013

Brains: The Conundrum of the Agglutinated Foraminifera

Some have brains, and some haven’t, he says, and there it is.
~ A. A. Milne quoting Winnie-the-Pooh, in the Introduction to Winnie-the-Pooh (1926, reprinted September, 1961, p. x)

Does Pooh have brains?  Ah, that’s a delightful question underlying the Pooh stories.  Pooh variously describes himself as either a “Bear of Very Little Brain” or a “Bear of No Brain at All.”  Christopher Robin follows suit, though, at one point, his perception of the bear is completely overthrown.  Upon hearing Pooh’s inspired suggestion that they might sail on the flood waters in an open umbrella to rescue Piglet, Christopher Robin “could only look at him with mouth open and eyes staring, wondering if this was really the Bear of Very Little Brain whom he had known and loved so long.”  (p. 144)  The umbrella “boat” is christened by Christopher Robin as The Brain of Pooh.

At one time, a kind of minute marine protozoa, the agglutinated foraminifera, prompted a similar question regarding its “intelligence.”  Though the assumptions, understanding, and terminology have changed over time, these single-called organisms still pose a related conundrum for those who would study them.

Foraminifera, often called forams, are single-celled marine organisms known from the Early Cambrian to the present.  They occupy a test (shell) often less than a millimeter in diameter.  Foraminifera tests come in an wonderful variety of shapes featuring one or more distinct chambers.  Benthic forams live in the sediment on the bottom of bodies of water while planktonic forams are free floating in the upper reaches of the water column.  To capture food, these microorganisms extend cytoplasm in the form of pseudopodia (think amoeba) into the surrounding environment.  Benthic forams also use pseudopodia to anchor themselves and to move along the bottom.  And, though most tests are built up from secreted calcite, a group of benthic forams use pseudopodia to construct their tests from material found in the environment.  These are the agglutinated foraminifera.

Savor that . . . single-celled organisms that build their own “houses.”  I remarked previously on this but only in passing.  I certainly did not give this phenomenon its due.

This assembly of the test is generally not some random process.  Different agglutinated species are known to be very precise in the shapes, sizes, and mineralogy of the material they select and use to construct their tests, though they are sometimes opportunistic, using what's available.  They may also carefully gather objects lost from organisms such as smaller forams’ tests, sponge spicules (structural spines), and coccoliths (the plates that encase coccolithophores).  Further, agglutinated foraminifer assemble the material carefully, orienting some items uniformly, as they affix them to an organic template.  Depending upon the foram, different cements are used.

Pictured below is a nice, relatively large fossil test from (what I believe to be) a species of Textularia, an agglutinated foraminifera.  I found this at the northern end of the Calvert Cliffs which places it in the lower to middle portion of the Miocene Epoch (maybe 18 to 16 million years ago).

Creation of its own test is, by all measures, a marvelous feat for a single cell with no nervous system and . . . no brain.

Well, therein lies this tale.  As he pondered intelligence among animals, British naturalist William Benjamin Carpenter (1813-1885) puzzled over the agglutinated foraminifera (he knew them as “Arenaceous Foraminifera”).  In his article titled On The Hereditary Transmission of Acquired Psychical Habits, which appeared in the Contemporary Review for April, 1873, Carpenter noted that for most species the question of “what part of its life-work is Instinctive and what is Rational” could be easily answered, but not for a handful of special cases.
The Deep-Sea researches on which I have been recently engaged, have not “exercised” my mind on any topic so much as on the following:– Certain minute particles of living jelly, having no visible differentiation of organs, possessing neither mouth, stomach, nor members, save such as they extemporize, and living (as it would seem) by simple absorption through the “animated spider’s web” into which they can extend themselves, build up “test” or casings, of the most regular geometrical symmetry of form, and of the most artificial construction.  (p. 784)
Carpenter described the way three different foraminifera species interact with the resources available in their environment to create their own tests.  He observed that, if a human mason, working from an undifferentiated mass of stones of various shapes and sizes, were to fashion a smooth “dome,” using the least amount of cement, “we should give him credit for great intelligence and skill.  Yet this is exactly what these little ‘jelly-specks’ do on a very minute scale . . . .”

Was this construction a deliberate, intentional action by the organisms or something mechanical?  Carpenter had no answer for this question, but, he knew it was imperative to attack that “easiest” of answers for these special cases, that is, laying it all on God (“the Creative Mind”), saying “God hath made them so.”  To invoke God, he argued, would not only strip these organisms of any inherent power of their own, but, to be consistent, this “First Cause” would have to be applied to all organisms, spelling the end of Science.  His is a masterful and powerful argument for the separation of science and religion:
There is, as it seems to me, no half-way house.  Either we must have immediate recourse to the First Cause in every instance, in which case we rest in it; or else we must seek to connect every phenomenon with its Physical Cause, so as to frame a scientific conception of the Order of Nature.  (p. 786)
He chose the latter.

At least one of Carpenter’s readers wrote to thank him for this essay; the account of the agglutinated foraminifera had clearly caught this reader’s attention.  In a letter of April 21, 1873, from Down House, Charles Darwin penned the following:
I read two days ago your article in the last Contemporary, and I must take the pleasure of expressing my extreme interest and admiration of it.  This will cause you no trouble, as this most obviously requires no answer.  The case of the 3 species of Protozoon (I forget the names) which apparently select differently sized grains of sand, &c. is almost the [most?] wonderful fact I ever heard of.  One cannot believe that they have mental power enough to do so, and how any structure or kind of viscidity can lead to this result passes all understanding.
(This text appears in Three Unpublished Letters of Charles Darwin, an article written by G.D. Hale Carpenter, and published in Nature, March 7, 1936.)

“Passes all understanding” is certainly hyperbole, not some form of verbally throwing in the towel.  How the agglutinated foraminifera does what it does is exactly the kind of question I think Darwin would have wrestled with, along with its corollary, how did this come to be.

And fashioning an answer to just that first question for these foraminifera has continued to bother naturalists.  Forty years after Carpenter’s article appeared, that renowned amateur naturalist and foraminifera authority Edward Heron-Allen  (1861 – 1943) joined the fray.  In 1913, he and Arthur Earland (1866 – 1958) (both men appear in a previous post) co-authored a paper on agglutinated foraminifera in which they described how Psammosphaera parva fashions its test by cementing grains of sand around a solitary sponge spicule:
We cannot but arrive at the conclusions that the presence of the central spindle in var. parva is not fortuitous, but that the animal deliberately chooses the spindle as a main constituent of its “house” . . . .  (Journal of the Royal Microscopical Society, 1913, p. 18.)
(As quoted in by Michael A. Kaminski in his article Edward Heron-Allen and His Theory of “Purpose and Intelligence” in the Foraminifera, which appeared in “Edward Heron-Allen FRS:  Scientist” Proceedings of the 4th Heron-Allen Symposium, 2004, 2005, p. 16.  I have been guided by Kaminski’s essay in exploring Heron-Allen’s various statements on this topic, as well as the critiques leveled against his position cited below.)

Reproduced below is one of the plates showing agglutinated foraminifera that appeared in the Heron-Allen/Earland piece of 1913.  The first ten illustrations show the successive stages of growth and test construction for the species Saccammina sphaerica.

Over the next couple of years, Heron-Allen became more explicit in his assessment that the agglutinated (arenaceous) foraminifera were exhibiting what in humans would pass for signs of intelligence.  Indeed, he posited in 1915 that “every living organism living an independent existence of its own is endowed with the measure of intelligence requisite to its individual needs.”  Further, when it came to the Marsipella spiralis which builds its test by aligning sponge spicules along a left-handed spiral, Heron-Allen remarked that this microorganism had “made the same discovery as did the prehistoric genius who invented string.”  (On Beauty, Design and Purpose in the Foraminifera, Proceedings of the Royal Institution of Great Britain, Volume 95, 1915, as quoted in Kaminski.)

Heron-Allen was on a roll and, in a paper presented at a meeting of the Royal Microscopical Society in the latter half of 1915, asserted that every animal living an independent life is
capable of developing functions and behaviour (including the adaptation of extraneous matters to its use and protection), which in the Metazoa might be called, and would properly be so called, Phenomena of Purpose and Intelligence.
(A Short Statement Upon the Theory, and the Phenomena of Purpose and Intelligence Exhibit by the Protozoa, . . . , Journal of the Royal Microscopical Society, 1915, p. 556.)
His was a beleaguered position.  Several prominent voices responded negatively.  Biologist E. Ray Lankester (1847 – 1929) delivered devastating blows in a paper titled The Supposed Exhibition of Purpose and Intelligence by the Foraminifera (Journal of the Royal Microscopical Society, 1916, p. 133 et seq).  Lankester denounced any ascription of purpose and intelligence to the foraminifera as those terms were understood and defined.  Intelligence or “mental faculties” in humans, he noted, are “immensely complex” and the product of “an almost inconceivably complex structure – the brain . . . . ”  He argued that, if one considered, in succession, organisms with “less elaborate” brains and “less complex mental faculties” until reaching the foraminifera, one “cannot fail to dismiss the notion of attributing to it purpose and intelligence, or anything that can be seriously be called by those names.”

Naturalist J. Arthur Thomson (1861 – 1933) took Heron-Allen to task for confusing “intelligent purposefulness” with “organized purposiveness.”  The former was on display, he contended, when rooks dropped mussels on the rocks in order to break open the shells; the latter was seen when the starfish attacked the sea urchin by severing its pedicellaria (claw like structures on the sea urchin).  In so doing, the starfish was engaged, according to Thomson, in “prolonged activity directed towards a future result.”  That was organized purposiveness and that was what the foraminifera were exhibiting.  (Proceedings of the Royal Microscopical Society, June 16, 1916, p. 251.)

Heron-Allen (mostly) ceded the field, admitting that he’d inappropriately applied his terminology to foraminifera.  In its stead, he embraced the terms Thomson proposed, particularly purposiveness.  But, he added, though “I am not arguing for the possession of ‘high’ skeletal structure, or mental activities in the Protozoa – it is obvious that these must be as rudimentary as they are in any egg – but in that rudimentary condition it seems to me that they must be there, awaiting the stimulus that calls them into action.”  (Proceedings of the Royal Microscopical Society, June 16, 1916, p. 137 – 138.)

In the midst of the Heron-Allen kerfuffle, Lankester penned a brilliant passage that was as cutting as it was insightful,
To say that they [the actions of the agglutinated foraminifera] are due to Purpose which is not Purpose as the word is ordinarily understood, and to Intelligence which is not Intelligence in the usual acceptation of term, seems to me to tend to misconception and a mistaken notion that we know more about the activities of the Protozoa than we do.
(Journal of the Royal Microscopical Society, 1916, p. 135 – 136, emphasis added.)
All of these scientists were, he argued, debating in ignorance about the phenomenon in question.  They were getting ahead of themselves.

You would have thought we’d have caught up by now, nearly a century later.  But, even today, I don’t believe Lankester would be satisfied with how little of the phenomenon we understand.  Though we certainly don’t ascribe intelligence to this test construction, we still cannot explain how this single celled organism does what it does.

Two decades ago, Christoph Hemleben and Michael Kaminski, in their introduction to Paleoecology, Biostratigraphy, Paleoceanography and Taxonomy of Agglutinated Foraminifera (Proceedings of the NATO Advance Study Institute, edited by Christoph Hemleben et al., 1990), wrote:
There has been much speculation about the adaptive benefits of grain selection, but exactly 75 years after Heron-Allen’s presentation, the fundamental question of how certain foraminifers select grains of a particular composition remains unanswered.  (p. 5-6.)
This is not their assessment alone.  Others have more recently reached essentially the same conclusion, positing, for instance, that “the process of grain selection in agglutinated foraminifera remains poorly understood,” or “[h]ow a single celled organism distinguishes between single grains remains totally elusive,” or “the mechanisms by which this may be achieved are not yet known from either cultures or experiments.”  (These quotations are from:  Kathryn Allen, et al., Fractal Grain Distribution in Agglutinated Foraminifera, Paleobiology, Volume 24, Number 3, 1998, p. 349; Dominic Armitage, Poster, University College London, 2004 (?); and George William Tuckwell, et al., Simple Models of Agglutinated Foraminifera Test Construction, Journal of Eukaryotic Microbiology, Volume 46, No. 3, May-June, 1999.)

Yes, there are hypotheses about how the selection takes place that involve genetics, where the foraminifera embryo first comes to rest, as well as the interaction between the membrane of the cell’s pseudopodia and the surface of the material encountered.  (See, for example, Tuckwell, et al., and Armitage.)  Nevertheless, that underlying, first order question remains unanswered, a conundrum to be pondered amid one's amazement at what's accomplished by an organism with no brain.
“Is that the end of the story?” asked Christopher Robin.
“That’s the end of that one.  There are others.”
“About Pooh and Me?”
“And Piglet and Rabbit and all of you.  Don’t you remember?”
“I do remember, and then when I try to remember, I forget.”
“That day when Pooh and Piglet tried to catch the Heffalump—”
“They didn’t catch it, did they?”
“Pooh couldn’t, because he hasn’t any brain.  Did I catch it?”
“Well, that comes into the story.”
Christopher Robin nodded.
(Winnie-the-Pooh, p. 20.)

Additional Sources

For general information on foraminifera, I have relied most fully on the foraminifera chapter in Microfossils by Howard A. Armstrong and Martin D. Brasier (2nd edition, 2005).  Other useful, though dated, sources on foraminifera include Cecil G. Lalicker’s chapter on foraminifera in Invertebrate Fossils, edited by Raymond C. Moore, et al., 1952; and Alfred R. Loeblich, Jr., and Helen Tappan’s Part C:  Protista 2, Sarcodina, Chiefly “Thecamoebians” and Foraminiferida, one of the volumes in the Treatise on Invertebrate Paleontology, edited by Raymond C. Moore, 1964.

A very clear and succinct description of the composition of the different kinds of foraminifera tests is available from the Jason Education Project at Texas A&M.

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