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Leaping the hedges with a butterfly amoeba

At the Milwaukee Public Museum with the butterflies.

I recently went to the Milwaukee Public Museum with my family.  This destination was carefully chosen because they have a butterfly exhibit, and my 5-year old daughter has developed a butterfly obsession.  In my experience, obsession of this sort is a good thing; in fact, it is the kind of thing that got me into science in the first place.  After I proudly watched her carefully hold and observe the different species of butterflies, and even have a few pleasant conversations with them, I wandered the exhibit and observed the diversity of colors and shapes myself.  There were some really spectacular species.

A butterfly amoeba

Perhaps because I recently had reason to open up Joseph Leidy’s incredibly beautiful 1879 foundational work describing North American testate amoebae (a group of amoebae that construct and live inside tests, or shells), my mind drifted to a statement Leidy made comparing a particular species of testate amoeba to a butterfly.  Apparently the simple beauty and elegance of this particular testate amoeba caused him to radically change his research focus.  He became obsessive about testate amoebae, or rhizopods as he called them. As with his previous research activities (e.g., paleontology, parisitology), his contributions to this new research area were enormous.

The testate amoeba in question was Hyalosphenia papilio.  In Leidy’s words:

“No other lobose rhizopod has more impressed me with its beauty than this one.  From its delicacy and transparency, its bright colors and form, as it moves among the leaves of sphagnum, desmids, and diatoms, I have associated it with the idea of a butterfly hovering among flowers.

A portion of a plate from Joseph Leidy’s 1879 monograph showing some of his drawings of Hyalosphenia papilio….the butterfly amoeba.

Leidy notes that he first observed the species thirty years prior to the publication of his seminal work, and seeing the species brought him fond memories of his explorations in the New Jersey pine barrens:

“Upward of thirty years ago, while examining the structure of sphagnum, my attention was distracted by the movements of a singular animal, whose character and affinities I did not then recognize.”

“This interesting Rhizopod, together with a profusion of other remarkable microscopic forms of both animal and vegetal life, of which many are novel and yet undescribed, recalls pleasing recollections of excursions into the sphagnous bogs, cedar swamps, and pine barrens in the southern region of New Jersey.

His fondness for the species is particularly evident in the next quote.  I can’t help to laugh a bit at the image of  him breaking out the microscope at a holiday dinner party, in order to display his “pets” to his friends.  Perhaps I should try this the next time I host a lab get together!

“I have collected it from early spring to late autumn, and have retained it alive in sphagnum, in a glass case, through the winter.  During the Christmas holidays, I have repeatedly exhibited it, in the living condition, to the admiration of friends.

A portion of a plate from Leidy’s 1865 Cretaceous Reptiles of the United States, showing some vertebrae from Hadrosaurus. (Image source)

What I find most interesting about this, is that Leidy was 50 years old when he decided to pursue this new line research.  He apparently dropped all of his other research endeavors, and focused solely on investigating these simple organisms for four or five years.  This shift in research focus was made by an already famous man who described the first complete dinosaur fossil, as well as many other North American fossils, and was widely recognized as the leading expert in parasitology.

A drawing of Trichina spiralis (now Trichinella spiralis), the  nematode parasite responsible for the disease trichinosis, done in 1887 by Joseph Leidy. Leidy first discovered that trichinosis was caused by a parasite that survived in undercooked meat (Chapman, 1891).  Image source: Collection 532. Joseph Leidy Teaching Diagrams. Academy of Natural Sciences of Philadelphia.

His obituary in the Proceedings of the National Academy of Arts and Sciences suggests that he left his paleontological research because of the extreme rivalries and unfriendly arguments that were shaping the field at the time – rather than get involved in these controversies Leidy may have just moved on.  He certainly would not be the only scientist to do such a thing.  However, according to his own words, it was the beauty of Hyalosphenia papilio that led him to study testate amoebae:

 “September 9th, 1873, the fiftieth anniversary of my birth, a friend, Clarence S. Bement, presented me with a Hartnack microscope, which, from its convenient size and form, I kept on my study table.  From time to time I was led to make observations on Fresh-water Rhizopods detected in sediments collected in the vicinity of Philadelphia.  A year later, in examining water squeezed from sphagnum obtained at Absecom, I observed many individuals of the same singular animal above indicated, but now, understanding its nature, I described it as Difflugia (Hyalosphenia) papilio.  It was the rediscovery of this beautiful form which impelled me to pursue the investigations which constitute the material of the present work.”

Published in 1897, his “Freshwater Rhizopods of North America” is a stunning combination of science and art, and still the most exhaustive description of North American testate amoebae.  For an interesting read on Leidy and the culture of science in mid-1800s North America, pick up a copy of Leonard Warren’s “Joseph Leidy: The last man who knew everything.”  For more on Leidy and a wonderful online version of the drawings included in the 1879 masterpiece, go here and here.

Joseph Leidy with his microscope circa 1870.

Leaping the hedges

The idea of following one’s interests, wherever they take you, is very attractive to me.  Of course, the culture of science has changed dramatically since the 1800s and scientists are generally narrower in focus and constrained by institutional expectations of tenure and promotion.  However, Leidy’s path of scientific exploration still seems a natural one, and I suspect that if more scientists followed his model instead of obsessively chasing promotion or the next big grant, we would collectively learn more about the natural world.

When I interviewed for a faculty position one of the questions that I was asked was to describe my 5-year research plan.  I was prepared for such a question, as it seemed like the sort of thing that I would be asked.  In fact, I carefully designed my research talk (candidates in academia usually “interview” for several days, typically giving one or two public lectures) to incorporate aspects of my long-term research plan.  Seven years later, perhaps not surprisingly, the most interesting science that I have done had little to do with my “plan.”  The projects that have excited me the most have been the things that I or my students have stumbled upon…things that I never could have planned.

I sincerely doubt that Joesph Leidy had a plan.  Sometimes something as simple as a beautiful amoeba, or a colorful butterfly, or perhaps an amoeba reminiscent of a butterfly…. can lead a scientist to wonderful new places.  Hopefully they will lead a certain 5-year old girl to some interesting places too.  The trick is identifying and following your passions (and obsessions), and knowing when it is time to move on to something new.  Leidy knew both…and he said so in the concluding statements of his great work:

“”I may perhaps continue in the same field of research and give to the reader further results, but I cannot promise to do so; for though the subject has proved to me an unceasing source of pleasure, I see before me so many wonderful things in other fields that a strong impulse disposes me to leap the hedges to examine them.””

-rkb

Addendum:

After posting I ran into this great piece.  A nice example of testate amoebae as inspiration for art.

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Save the amoeba?

Should microbial biodiversity (i.e., microscopic organisms like bacteria, archea, protists, and some fungi) be more directly considered in conservation efforts?  Certainly the importance of microscopic organisms in the earth system cannot be overstated, as they play vital roles in global element cycles – fixing atmospheric nitrogen and making it available to plants, returning nitrogen back to the atmosphere, playing important roles in food webs, and facilitating the decomposition of organic matter.  Furthermore, microorganisms are likely to become a critical source for new pharmaceuticals in the future (Chivian & Bernstein, 2008).  However, only rarely have microorganisms been included in biodiversity surveys, and although the International Union for Conservation of Nature (IUCN) recently added four critically endangered protists to the Red List (here, here, here, and here), a public outcry for their protection appears unlikely any time soon.

A plate from Joseph Leidy’s 1879 monograph on testate amoebae (1-8: Nebela ansata, 9-14: Nebela hippocrepis). Testate amoebae are a group of protists that produce morphologically distinct shells.

Of course the lack of emphasis on microorganisms in conservation biology is not particularly surprising, given that 1) we know relatively little about microbial diversity, 2) microbes are perhaps slightly less cute and charismatic than many other organism groups (although they are certainly cuter than some species), and 3) it has been widely assumed that microbial species have cosmopolitan distributions.  In other words, they are found everywhere.  More specifically, a microbial species occurs anywhere that suitable habitat exists for that particular species.  In 1934, Baas Becking simply stated this hypothesis as: “everything is everywhere, but the environment selects” (de Wit and Bouvier 2006).  What is implied by this hypothesis is that dispersal does not limit the distribution of microbes, and endemism (i.e., being confined to a particular region) should be rare.  Of course, if everything is everywhere, then we don’t need to worry much about any particular microbial species, because extinction is extremely unlikely unless the destruction of all suitable habitats occurs…across the entire planet.  Let’s hope that remains unlikely for some time.

However, research now clearly indicates that microbial biogeography is more nuanced and complex than implied by the “everything is everywhere” hypothesis. Many examples of limited geographic ranges have emerged over the past couple decades.  Some particularly striking examples are within the testate amoebae, a group of shell-producing protists that have been relatively well studied, at least in comparison to many other microbial groups.  For example, Apodera vas and species of the genus Certesella are restricted to the southern hemisphere and tropics, although suitable habitats for these species exist in Eurasia and North America (Smith and Wilkinson 2007).  The patterns suggest that these species had their origins on the continent of Gondwana sometime after it separated from Laurasia about 200-180 million years ago, and thus their current distribution may be a reflection of this geological and evolutionary history (Smith and Wilkinson 2007).  Apparently these species have been unable to disperse to North America or Eurasia.

A paleogeographic reconstruction of the Earth in the late Triassic, shortly before the separation of Gondwana (southern continents) from Laurasia (northern continents). The present distribution of Apodera vas and species of the genus Certesella is nearly restricted to the land that was once part of Gondwana, suggesting that they evolved on this landmass (Smith & Wilkinson 2007). (Image from wikipedia.org).

A potentially more restricted distribution pattern is that of Nebela ansata, an unusual (and dare I say, “charismatic”) species of testate amoebae known only from a few locations in eastern North America.  In 1874, Joseph Leidy first encountered this species from collections he made in the New Jersey Pine Barrens (Leidy 1879).  Since his initial descriptions, the species has only been recorded in the literature three times, always in temperate eastern North America, and always living in wetlands on moist Sphagnum moss. The species has gone unrecorded in the literature since the early 1950s, despite the intensive sampling of wetland testate amoeba communities (Heger et al. 2011).

The search for a forgotten microbe

Nebela ansata from Webb’s Mill Bog in the New Jersey Pine Barrens.  The horn-like lateral extensions are characteristic for the species. (Photo: Thierry Heger)

The New Jersey Pine Barrens are only a few hours from Lehigh University, so a few years ago we set out to see if we could find Leidy’s elusive and long-forgotten microbe.  His original samples were from cedar swamps near the town of Absecom (now spelled Absecon), and we used that as a guide when selecting potential wetlands for our sampling effort.  He also mentioned that Nebela ansata was commonly found in association with Nebela carinata, a more widely distributed species.  The ecology of Nebela carinata has been well characterized, and it prefers very wet Sphagnum moss and is often abundant where the water table is only a few centimeters below the moss surface.  We used this knowledge to target likely habitats within each of the wetlands that we sampled.  Maura Sullivan (Lehigh University, PhD student) and I sampled for two full days, returned the samples to the lab for examination, and managed to find the species!

Interesting, at about the same time as our rediscovery of Nebela ansata in the New Jersey Pine Barrens, the species was also discovered in Nova Scotia by Barry Warner and Taro Asada (University of Waterloo).  A collaborative effort soon took shape, with the goal of pulling together all the known information on the distribution, ecology, and phylogeny of the species.  Led by Thierry Heger, then a PhD student (Swiss Federal Research Institute WSL & The University of Geneva), an exhaustive literature and museum survey was undertaken and used in tandem with analyses of the samples from Nova Scotia and Pine Barrens to provide insight into the biogeography and ecology of Nebela ansata.  Together, the the results provide a compelling case of a microorganism with a very limited distribution range – apparently limited to temperate, eastern North America – representing a very clear exception to the ‘everything is everywhere’ hypothesis (Heger et al. 2011).

Webb’s Mill wetland in the New Jersey Pine Barrens, where individuals of the rare testate amoeba species, Nebela ansata, were found.

How many other microorganisms also have geographically restricted distributions?  What are the primary causes of these restricted distributions?  How many endemic species remain undescribed? What role do these relatively rare microorganisms play in ecosystems? How many microbial species are vulnerable to habitat destruction or other global changes?  Much work remains to be done in biodiversity research.

-rkb-

Literature cited

Chivian, E. & A. Bernstein, eds. 2008. Sustaining Life. How Human Health Depends on Biodiversity. Oxford University Press.

de Wit. R. & T. Bouvier. 2006. ‘Everything is everywhere, but the environment selects’; what did Baas Becking and Beijerinck really say? Environmental Microbiology 8: 755-758.

Heger, T.J, R.K. Booth, M.E. Sullivan, D.M. Wilkinson, B.G. Warner, T. Asada, Y. Mazei, R. Meisterfeld, & E.A.D. Mitchell. 2011. Rediscovery of Nebela ansata (Amoebozoa: Arcellinida) in eastern North America: biogeographical implications. Journal of Biogeography 38: 1897-1906.

Leidy, J. 1879. Fresh-water rhizopods of North America. Report of the United States Geological Survey of the Territories, 12, 1–324.

Smith, H.G. & D.M. Wilkinson. 2007. Not all free-living microorganisms have cosmopolitan distributions – the case of Nebela (Apodera) vas Certes (Protozoa: Amoebozoa: Arcellinida). Journal of Biogeography, 34: 1822–1831.

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