Dr. Rob Dillon, Coordinator

Tuesday, March 14, 2017

Fred Thompson, Elizabeth Mihalcik, and the Pleurocerids of Georgia

Science is a human enterprise, alas.  Last month [1] we reviewed the fitful progress of research into the systematic relationships of the Florida Pleuroceridae through the 1970s and 1980s, as a function of the personalities of two scientists, the late Dr. Fred G. Thompson and Dr. Steven M. Chambers.  In 1990 Steve Chambers published a malacological masterpiece, “The genus Elimia (= Goniobasis) in Florida and adjoining drainage basins [2],” correcting Clench & Turner’s 1956 seven-species model down to four.  He then shifted his professional interests out of the field.  Thompson, failing to cite the Chambers 1990 paper or indeed (almost) any of Chambers’ impressive body of research, published an update of his “Freshwater Snails of Florida” in 1999.  He was going in the opposite direction.

Thompson’s Second Edition [3] began with the Clench & Turner seven-species model but added an undescribed “spring Elimia” from Holmes Creek and three new species that “may occur in Florida” (Elimia taitiana, Choctawhatchee Elimia and Escambia Elimia), bringing his grand total up to 11 and foreshadowing things to come.  Simultaneously, Thompson was working with a committee of the AFS to publish a second edition of the Turgeon et al. “Common and Scientific Names of Mollusks,” which appeared in 1998 [4].  The Turgeon work was destined, in a perverse way, to become the Bible of American malacology.  Thus less than ten years after the publication of Steve Chambers’ landmark paper, the Clench & Turner model became gospel, and Chambers’ work forgotten.

Meanwhile, a new graduate student arrived at the University of Florida named Elizabeth L. Mihalcik.  She entered the laboratory of the noted herpetologist F. Wayne King, and was “introduced into the world of invertebrates through her mentor and friend, Dr. Fred G. Thompson.”  In 1996 she was awarded an EPA STAR graduate fellowship for her proposal entitled, “Analyzing morphological forms within southeastern river system species complexes.”
The Mihalcik [6] study area, showing P. floridensis
Elizabeth Mihalcik’s proposal originally focused on estimating gene frequencies at polymorphic enzyme-encoding loci in populations of what her mentor and friend referred to as “the Elimia curvicostata complex” of Central Georgia and the Florida drainages of Alabama.  And in fact, I did host Elizabeth at my lab in Charleston for several days in the late 1990s, and showed her everything I knew about allozyme electrophoresis.  But if she ever ran an allozyme gel independently, I never saw the data.

Elizabeth’s (1998) dissertation [5] focused primarily on shell morphometrics: 6 measures, 4 counts, spire angle and 8 ratios of the above in various combinations, blessedly naive of any inkling that any shell character might demonstrate any interpopulation variance for any reason whatsoever.  But the winds of change were blowing across systematic biology.  Her dissertation also included a little bit of mtDNA sequence data.

The first fully automated sequencing DNA machine had come onto the market in 1987, even as Kerry Mullis’ patent for PCR amplification was approved.  The Folmer et al primers to amplify the mitochondrial CO1 gene were published in 1994, and by the late-1990s what had been a trickle of DNA sequence data became a torrent.  Surely such data must be useful for systematic biology, if we could just settle on an algorithm to build our gene trees, yes?  The “phylogenetic species concept,” originally proposed by Cracraft in 1983, came into vogue.

So by the time Elizabeth published her dissertation with Fred Thompson in 2002 [6], her analysis was almost entirely based on mitochondrial CO1 sequence data.  She sequenced 25 individual snails from 24 Pleurocera populations scattered across Florida, Georgia and Alabama, with one individual P. catenaria from South Carolina thrown in to boot.  Her results (below) returned four clusters of roughly 5 - 7 individuals each, corresponding remarkably well to the four species that Steve Chambers documented in 1990.

Mihalcik and Thompson also discovered at least three apparent cases of mitochondrial superheterogeneity (mtSH above).  I have very nearly beat this subject to death on the FWGNA blog, but see note [7] below if you need your memory refreshed.  MtSH may indeed have some utility in identifying genuine biological species, but only if the phenomenon is recognized, which Mihalcik and Thompson did not [8].  So setting aside their sequence data for those three individual snails, the remaining snails demonstrate four clusters neatly corresponding to the species Chambers called floridensis, curvicostata, dickinsoni, and “boykiniana*.”

Alas, Mihalcik and Thompson saw substantially more than four species in their gene tree.  They interpreted their 25 mtDNA sequences as evidence of 15 species and subspecies of Pleurocera in Central Georgia and the Florida drainages of Alabama, as follows.  Starting with baseline curvicostata, a catenaria reference from South Carolina and two flava references from Alabama, M&T resurrected four old Isaac Lea names from synonymy: induta, mutabilis, viennaensis, and ucheensis.  They raised Goodrich’s subspecies timida to the full species level, and described two new subspecies underneath it: exul and nymphaea.  And they freshly described five new species: exusta, glarea, annae, buffyae, and darwini, the last three of which Elizabeth named for her dogs. 

When one steps back to consider that the authors did not even consider six of the seven Clench & Turner species as members of the “Elimia curvicostata complex” (albanyensis, athearni, clenchi, dickinsoni, floridensis and vanhyningiana), the Mihalcik and Thompson hypothesis constitutes a staggering multiplication of pleurocerid nomina [9] for the region.

I myself was not idly sitting by in Charleston, however.  Through most of the 1980s I confess that I became distracted by hard clam aquaculture, and by the 1990s Amy Wethington and I were beginning to work on Physa.  But I never forgot my first love, which was the pleurocerid snails.  And in 2002, just a few months prior to the work of Mihalcik & Thompson, an undergraduate student and I published “A survey of genetic variation at allozyme loci among Goniobasis populations inhabiting Atlantic drainages of the Carolinas” [10].

We estimated gene frequencies at 8 polymorphic loci in 12 populations, picking up in NW North Carolina where my dissertation left off and extending through South Carolina to touch eastern Georgia – 4 populations of P. proxima and 8 populations of P. catenaria, including the type locality 50 km W of Charleston.  Our most interesting result touched a very familiar theme on this blog [11], ecophenotypic plasticity in pleurocerid shell morphology.  Populations of P. catenaria bearing typical shells in the Piedmont of the Carolinas tended to lose their spiral cords and costae as they ranged into the coastal plain, independently developing the shell form associated with the subspecific nomen “dislocata[12].

In 2004 Thompson published a third edition of his “Freshwater Snails of Florida,” this update strictly online [13].  From seven species of pleurocerid snails in 1984 and eleven in 1999, Thompson’s fresh online edition now recognized 12 species in Florida alone, the “Choctawhatchee Elimia” formally identified as buffyae, the “Escambia Elimia” now annae, and a new “Rasp Elimia” waiting in the wings, not as yet described.  None of Steve Chambers’ papers whatsoever were cited in Thompson’s 2004 online version.  Even the passing mention of Chamber’s 1980 paper had now disappeared.

So ten years ago, this was the situation:  Two morphologically variable species, P. proxima and P. catenaria, were understood to range from southern Virginia through North Carolina and South Carolina to the Georgia border.  At the Georgia border P. catenaria disappeared, to be replaced by over 20 rare and endemic pleurocerid species, each occupying single subdrainages, or in some cases single springs.  Does that model seem biologically plausible to you?
P. ucheensis is dislocata, the remainder are P. catenaria
In 2011 John Robinson and I extended our allozyme survey across Georgia, linking at long last my intensive dissertation work in Virginia with my buddy Steve Chambers’ extensive dissertation work in Florida [14].  John and I sampled 14 populations, including populations identified by Mihalcik & Thompson as viennaensis, darwini, mutabilis, induta and timida nymphea, reaching down to the boykiniana and floridensis populations of Chambers.  We estimated genetic divergence at 11 polymorphic allozyme encoding loci, calibrating our observed values with three populations of P. proxima, the conspecific status of which is unchallenged.

We did not include any bona fide curvicostata or dickinsoni in our survey, because those two taxa seemed unambiguous to us.  But the bottom line was that all the Georgia populations we sampled were either floridensis (including induta and timida) or catenaria (including albanyensis, boykiniana, darwini, mutabiliis, and viennaensis).  There are exactly four species of pleurocerid snails in Central Georgia, Florida, and the Florida drainages of Alabama as hypothesized by Chambers: curvicostata, dickinsoni, floridensis and (*a minor correction) catenaria, all boasting extensive ranges.  And the most widespread of those species, Pleurocera catenaria (Say 1822) extends through five states, from Virginia through the Carolinas and Georgia to mimic P. floridensis at Ichetucknee Springs, bringing the discovery Steve Chambers first reported in 1978 [15] into a properly regional context.

I didn’t expect Dr. Thompson to embrace the four-species model in 2011 any more than he did in 1990.  His species concept was rooted in nineteenth-century typology, no different from such giants of American malacology as Henry Pilsbry and F. C. Baker.  Indeed, distinction of species by shell costations or spiral chords is not conceptually different from distinction by individual nucleotide substitutions, as do many of our colleagues in the present day.  But I confess, when I saw the species list published by P. D. Johnson and colleagues in 2013 [16], including as it did albanyensis, annae, athearni, boykiniana, buffyae, clenchi, darwini, exusta, glarea, inclinans, induta, mutabilis, taitiana, timida, ucheensis, vanhyningiana, and viennaensis, I was just a little bit disappointed.


[1] Fred Thompson, Steve Chambers, and the pleurocerids of Florida [15Feb17]

[2] Chambers, S. M. (1990) The genus Elimia (= Goniobasis) in Florida and adjoining drainage basins (Prosobranchia: Pleuroceridae)  Walkerana 4: 237 – 270.

[3] Thompson, F. G. (2000)  An identification manual for the freshwater snails of Florida.  Walkerana 10(23): 1 -96.

[4] Turgeon, D.D., J.F. Quinn, A.E. Bogan, E.V. Coan, F.G. Hochberg, W.G. Lyons, P.M. Mikkelson, R.J. Neves, C.F.E. Roper, G. Rosenberg, B. Roth, A. Scheltema, F.G. Thompson, M. Vecchione, and G.D. Williams (1998) Common and scientific names of aquatic invertebrates from the United States and Canada: Mollusks (second edition), American Fisheries Society Special Publication 26, Bethesda, Maryland, 526 pp.

[5] Mihalcik, E. L. (1998)  Elimia curvicostata species-complex within the river drainages of the southeastern United States: Morphology, DNA, and biogeography.  Ph.D. dissertation, University of Florida, 209 pp.

[6] Mihalcik, E. L. & F. G. Thompson (2002)  A taxonomic revision of the freshwater snails referred to as Elimia curvicostata, and related species.

[7] Pleurocerid populations (and a variety of other gastropod populations as well) often demonstrate “mitochondrial superheterogeneity,” where two or more members demonstrate 10% sequence divergence or greater for any single-copy mtDNA gene, not sex-linked.  For more see:
  • Mitochondrial superheterogeneity: What we know [15Mar16]
  • Mitochondrial superheterogeneity: What it means [6Apr16]
  • Mitochondrial superheterogeneity and speciation [3May16]
Mihalcik and Thompson only sampled single individuals from almost all [8] of their populations, so (strictly speaking) mtSH cannot be recognized.  But based on my personal experience with many datasets of this sort, the cases labelled flava-1, annae, and boykiniana all look like mtSH to me.

[8] The only population from which M&T sampled more than one individual was their reference “flava” from Alabama, the two individuals sequenced from which apparently demonstrating more than 20% sequence divergence.  They might have been the first researchers ever to discover mtSH in the Pleuroceridae, had their eyes been open.  Dillon & Frankis didn’t formally document the phenomenon until 2004 [PDF].

[9] Here’s something even more remarkable, if you stop to consider it.  The 15 populations M&T identified as being members of the “Elimia curvicostata complex” (explicitly excluding floridensis, dickinsoni, or boykiniana) apparently represented all four of the Chambers species (curvicostata, floridensis, dickinsoni, and boykiniana) about equally.   Shows you the value of shell morphology, doesn’t it? 

[10] Dillon, R. T. and A. J. Reed (2002)  A survey of genetic variation at allozyme loci among Goniobasis populations inhabiting Atlantic drainages of the Carolinas.  Malacologia 44: 23-31. [PDF]

[11]  Much more on cryptic phenotypic plasticity in pleurocerid shell morphology:
  • Goodbye Goniobasis, Farewell Elimia [23Mar11]
  • Pleurocera acuta is Pleurocera canaliculata [3June13]
  • Elimia livescens and Lithasia obovata are Pleurocera semicarinata [11July14]
[12] More about the pleurocerid subspecific nomen “dislocata” and its treatment by Turgeon [4] can be found at:
  • What subspecies are not [5Mar14]
[13] Thompson, F. G. (2004) on-line edition: An identification manual for the freshwater snails of Florida. Florida Museum of Natural History, Gainesville, FL [html].

[14] Dillon, R. T. and J. D. Robinson (2011)  The opposite of speciation: Population genetics of  Pleurocera (Gastropoda: Pleuroceridae) in central Georgia.  American Malacological Bulletin 29: 159-168.  [PDF]

[15] Chambers, S. M. (1978) An electrophoretically detected sibling species of “Goniobasis floridensis” (Mesogastropoda; Pleuroceridae).  Malacologia 17: 157 – 162.

[16] Johnson, P. D. et al. (2013) Conservation status of freshwater gastropods of Canada and the United States.  Fisheries 38: 247 – 282.  See:
  • Plagiarism, Paul Johnson, and the American Fisheries Society [9Sept13]

Wednesday, February 15, 2017

Fred Thompson, Steve Chambers, and the pleurocerids of Florida

Word has reached us of the death of Dr. Fred G. Thompson, who passed away December 27, 2016 at his home in Ocala [1].  Dr. Thompson was Curator of Malacology at the Florida Museum of Natural History in Gainesville for 40 years.  He was 82.

Dr. Thompson’s body of published work must run into the hundreds of titles – focusing primarily on the North American Hydrobiidae, but extending to include the Pleuroceridae and a broad range of terrestrial gastropod taxa as well, especially of Mexico and Latin America.  I understand that his complete necrology will soon be published in The Tentacle.

I had no personal relationship with the late Dr. Thompson.  I did attend his talks at the AMU (later the American Malacological Society) over a period of some thirty years, although I don’t recall his attending any of mine.  He did not respond to my letters or emails.  During my visit to the Florida Museum in July of 2006 he did not emerge from his office.

We did, of course, have many mutual colleagues.  The American community of freshwater gastropod workers is not a large one.  All I know about the personality and character of Dr. Thompson I have gathered from friends.  Good friends, like Steve Chambers.

Steve Chambers was an important influence on my young career.  He first met Dr Thompson on a field trip as a graduate student at the University of Florida in 1976, and became interested in the genetic relationships among Florida pleurocerid populations known at that time as Goniobasis, now Pleurocera.  Steve’s major adviser, Dr. Thomas Emmel, ran a big laboratory specializing in the promising new technique of allozyme electrophoresis.  Steve thought that the estimation of genetic divergence among populations of pleurocerid snails as a function of gene frequencies at multiple allozyme-encoding loci might elucidate evolutionary principles of great generality and importance [2].
The Clench & Turner model, as figured by Chambers [7]
The pleurocerid fauna of Florida is no less enigmatic than that of most other regions of the American southeast. Goodrich [3] recognized three species: catenaria (2 subspecies), clenchi and curvicostata, with boykiniana (3 subspecies) in nearby South Georgia.  Clench & Turner [4] took a big swing at this system, substituting floridensis for catenaria cancellata, raising catenaria vanhyningiana to the full species level, bringing one of the boykiniana subspecies down into Florida (albanyensis) and raising it to the full species level as well.  They also described two new species (athearni and dickinsoni) which, together with clenchi and curvicostata yielded seven species of Goniobasis in Florida.

It was the seven-species Clench & Turner model that Fred Thompson preferred for the Pleuroceridae of Florida, and the seven-species model is what Steve Chambers brought into his study design.  His (1977) dissertation [5] was an impressive effort to replicate the extremely influential Drosophila research that F. J. Ayala [6] had published in 1974.  Steve showed that, just as in Drosophila, populations of Goniobasis at increasing degrees of taxonomic divergence demonstrated increasing levels of genetic divergence at allozyme loci.  The paper based on his dissertation research was published in 1980 [7].

Perhaps unsurprisingly, however, Steve’s genetic data did not jive especially well with the Clench & Turner seven-species model.  Allozyme divergence suggested that vanhyningiana and clenchi be synonymized under floridensis and that albanyensis, athearni and the REF population (more about which anon) “are in the range of conspecifics,” although Chambers called for further study on that question.  Note that by the time he had published his dissertation in 1980 he had already synonymized clenchi (marked “F” in the figure above) under floridensis.

Meanwhile, on a small farm in Kansas, a boy was growing up [8].  Well, actually, he entered the graduate program at the University of Pennsylvania in the fall of 1977, on a scientific journey remarkably similar to that of Steve Chambers, just a couple steps behind.  My adviser was also running a big lab specializing in the promising new technique of allozyme electrophoresis, and I too was interested in the genetic relationships among populations of Goniobasis, mine in the southern Appalachians.  And it turned out that my adviser, Dr. George Davis, was also the Editor of the journal to which Steve Chambers sent his first two papers, the 1980 work based on his dissertation and an earlier one on that “REF” population I mentioned above.

Steve had discovered his REF population quite by accident.  He had gone to sample Ichetucknee Springs (the source of North Florida’s Ichetucknee River) expecting to find a typical population of Goniobasis floridensis, and that’s what he thought he had, until he got back to the laboratory.  But his gels showed two reproductively isolated populations, one of which matched floridensis genetically and the other of which was much more similar to his sample populations of Goniobasis athearni and G. albanyensis.  He published “An electrophoretically detected sibling species of Goniobasis floridensis” in Malacologia in 1978 [9].

Both Steve’s 1978 and 1980 papers were highly influential in my budding career.  I struck up a correspondence with him and he was happy to share techniques, recipes, and tips.  Imagine my surprise (and dismay) when my adviser showed me a manuscript he had received attacking Steve Chamber’s work gratuitously and viciously.

Fred Thompson had submitted a Letter to the Editor for publication in Malacologia.  The journal very rarely published letters in those days.  In fact, no letters whatsoever had been published in the previous ten years.  But Dr. Thompson was livid about research that had taken place at his own home institution, research that very carefully and thoroughly documented a model of evolutionary relationships among the Florida Goniobasis he did not share.

That letter was ultimately published in 1982, along with Steve’s reply [10], over the protestations of a farm boy from Kansas [8].  It included such whoppers as “Because the Ichetucknee population of athearni is distantly related genetically to floridensis, they cannot be sibling species.”  But the amount of genetic divergence has nothing to do with sibling species.  Ernst Mayr coined that term in 1963, and he defined it as “morphologically similar or identical populations which are reproductively isolated,” and genetic divergence does not enter into it [11].  In fact, whether the observed amount of genetic divergence might correlate with the taxonomic divergence suggested by systematic biologists was the very hypothesis that Steve was trying to test.

Well, by 1982 Steve had been gone from Gainesville for five years.  He told me later that he had been a finalist for the opening at the University of Michigan Museum of Zoology left vacant when Henry van der Schalie retired, but that Dr. Thompson had written an unsolicited letter to his colleagues in Ann Arbor, scuttling Steve’s chances for that job.

But Steve was able to land a job with the FWS Office of Endangered Species in Washington, which turned out to be a plum.  From Washington he was able to publish two high-visibility works on chromosomal evolution in gastropods [12].  He also became interested in the land snail fauna of the Galapagos, describing two new species of bulimulids in 1986 [13].  And with Christine Schonewald-Cox and other colleagues he edited a very influential book on the budding discipline of conservation genetics [14].

Meanwhile up north, the farm boy from Kansas [8] accepted an AAAS congressional fellowship and moved to Washington for the 1981-82 academic year, still right on the heels of his buddy Steve.  And we struck up a personal friendship that year which I wish had lasted longer.  Toward the end of my brief sojourn in Washington Steve remarked to me, and I’m paraphrasing here, “In the entire wide community of systematic biology, malacologists have the reputation of being the most petty and venal.”  He was broadening his professional horizons, trying to shift away.

And meanwhile down south, Dr. Thompson published the first (1984) edition of his “Freshwater Snails of Florida” [15].  Perhaps unsurprisingly he clung to the Clench & Turner seven-species model, citing the work of Chambers only once, superficially: “Recent studies on isoenzymes show that, in Elimia, shell characters are conservative indicators of genetic divergence (Chambers 1980, Dillon & Davis 1980).”  Regarding Dr. Thompson’s choice of genus, see note [16] below.
From Chambers [17]
After ten years in Washington, Steve was transferred to the regional office in Albuquerque, where he became involved with federal efforts to protect endangered elements of the charismatic megafauna such as the Red Wolf.  But he had one more snail paper in the pipeline, his 1990 masterpiece “The genus Elimia in Florida and adjoining drainage basins” [17].  Here Steve combined his modern understanding of allozyme, chromosomal, and morphological divergence in an enigmatic and misunderstood freshwater gastropod fauna together with a scholar’s appreciation for the old literature and the old museum collections into a symphony of Malacological virtuosity.  He convincingly demonstrated that there are four species of Goniobasis in Florida and South Georgiaboykiniana (including athearni, albanyensis, and REF), curvicostata, dickinsoni, and floridensis (including vanhyningiana and clenchi), and the matter would seem to be settled.

But way back on page 261 of Chambers’ 1990 work we read: 
“R. T. Dillon has sent me shells of Elimia catenaria Say from South Carolina and suggested that my E. boykiniana may be a synonym of E. catenaria.  Although there is considerable merit in this suggestion, I decline to combine these Georgia and South Carolina populations with E. boykiniana at this time because they occur in major drainages for which genetic data are not available.”
Yes, after single years in Washington and at Rutgers, that farm boy from Kansas [8] had arrived in Charleston, SC, and begun work to tie his 1982 dissertation research in VA/NC together with the remarkable body of knowledge Steve Chambers had developed in FL/Ga.  Could direct conflict with Dr. Fred Thompson be avoided?  Tune in next time.


[1] Fred Gilbert Thompson (November 13, 1934 – December 27, 2016).  The Shell-O-Gram 58(1): 4-5.

[2] I did too, once.  When I was young.

[3] Goodrich, C. (1942) The Pleuroceridae of the Atlantic Coastal Plain.  Occas. Papers Mus. Zool. Univ. Mich. 456:1 – 6.

[4] Clench, W. J. & R. D. Turner (1956) Freshwater mollusks of Alabama, Georgia and Florida from the Escambia to the Suwannee River.  Bull. Florida State Museum 1:1 – 239.

[5] Chambers, S. M. (1977) Genetic divergence during speciation in freshwater snails of the genus Goniobasis.  Ph.D. dissertation, University of Florida, Gainesville. 59 pp.

[6] Ayala, F. J., M. L. Tracey, D. Hedgecock & R. C. Richmond (1974) Genetic differentiation during the speciation process in Drosophila.  Evolution 28: 576-592.

[7] Chambers, S. M. (1980) Genetic divergence between populations of Goniobasis (Pleuroceridae) occupying different drainage systems.  Malacologia 20: 63 – 81.

[8] Virginia, actually.  And he wasn’t born on a farm, and he never grew up, if you ask his wife.  For more, see…
  • The Clean Water Act at 40 [7Jan13]
[9] Chambers, S. M. (1978) An electrophoretically detected sibling species of “Goniobasis floridensis” (Mesogastropoda; Pleuroceridae).  Malacologia 17: 157 – 162.

[10] Thompson, F. G. (1982) On sibling species and genetic diversity in Florida Goniobasis.  Malacologia 23: 81 – 82.  
       Chambers, S. M. (1982) Sibling species and genetic diversity in Florida Goniobasis: A reply.  Malacologia 23: 83 – 86.

[11] Mayr, E. (1963) Animal Species and Evolution.  Belknap Press, 797 pp.  The definition of sibling species is found on page 34. 

[12] Chambers, S. M. (1982) Chromosomal evidence for parallel evolution of shell sculpture pattern in Goniobasis.  Evolution 36: 113 – 120.  
        Chambers, S. M. (1987) Rates of evolutionary change in chromosome numbers in snails and vertebrates.  Evolution 41: 166 – 175.

[13] Chambers, S. M. (1986) Two new bulimulid land snail species from Isla Santa Cruz, Galapagos Islands.  Veliger 28: 287 – 293. 

[14]   C. Schonewald-Cox, S. Chambers, B. MacBryde, and L. Thomas (1983) Genetics and Conservation: A Reference for Managing Wild Animal and Plant Populations.  Benjamin Cummings, Menlo Park.  722 pp.

[15] Thompson, F.G., 1984. The freshwater snails of Florida: A manual for identification. University of Florida Press, Gainesville, FL. 1-94.

[16] I suppose I should also mention that, separately but essentially simultaneously, J. B. Burch was working on his North American Freshwater Snails.  The Burch & Tottenham “Species List, Ranges and Illustrations” was published in 1980, with the full EPA Manual following in 1982 and the stand-alone separate work republished in 1989.  This work proposed a hybrid between the Goodrich and Clench & Turner classifications of the Florida and South Georgia pleurocerid fauna, which did not evolve through its extended publication history: athearni, clenchi, curvicostata, dickinsoni, induta, and boykiniana with three subspecies.  The recognition of a separate floridensis, while keeping vanhyningiana as a subspecies of catenaria, yielded a list of ten species and subspecies for the region, which Burch renamed to “Elimia.”

[17] Chambers, S. M. (1990) The genus Elimia (= Goniobasis) in Florida and adjoining drainage basins (Prosobranchia: Pleuroceridae)  Walkerana 4: 237 – 270.

Wednesday, January 11, 2017

A Previously Unrecognized Symbiosis?

Last month’s post on the aerial dispersal of freshwater gastropods [1] turned out to be one of my more popular in recent memory.  Thank you all for your kind emails.  Winning the award for most charming was our colleague Lusha Tronstad of the Wyoming Natural Diversity Database, who sent me the photos below:

And here is the story, verbatim as I received it from Lusha: 
“My son, Everett Tronstad (he just turned 6) caught this beetle (likely Dytiscus gigantus) in our barnyard this past summer.  We live northwest of Laramie, Wyoming in the foothills of the Snowy Mountains.    My son spends hours every day collecting invertebrates, both aquatic and terrestrial.  He caught this beetle on our car who probably thought the shiny paint was water.  Everett picked it up and we immediately saw the limpets attached.  We had just enough time to snap two photos before the beetle took off.  We watched the beetle fly off into the distance and we marveled at how invertebrates can hitchhike on other critters.  The date was 30 July 2016.”
I also received a cordial email from Chris Davis of the Pymatuning Lab up in Linesville, PA.  He called my attention to a note published by Andrea Walther and a host of colleagues in 2008 [2], with the striking figure reproduced below.

Andrea and her colleagues collected nine water bugs from a pond at the University of Michigan’s Edwin S. George Reserve, two of which bore five limpets each.  Note that the bugs were swimming at the time of their collection.  Andrea wrote, “Given the positioning of the L. fuscus on the dorsal surfaces of the B. flumineum, it is uncertain if the insects were able to lift their hemelytra to take flight.”

So those of you in my email address book [3] may remember the challenge I issued when I announced last month’s post, back on 15Dec16:  “Quick, quick!  How many reports of freshwater limpets on flying water bugs would you expect to find in the published literature?”  The answer I was looking for was 12, the ten listed by W. J. Rees [4] plus the two I found published between 1965 and 1991.  So here are two more [5], making 14.  At some point, a stack of related observations becomes a phenomenon, don’t you agree?

And here’s another remarkable observation, which I’m not sure has at yet been remarked.  There were three Ferrissia on Everett’s dytiscid beetle.  And there were five Laevapex on the back of each of Andrea’s belostomatid bugs.  On surface areas no more than 4 square cm??  I feel sure the densities of limpets on the insects must be orders-of-magnitude greater than their densities in the general environment.  The limpets are almost certainly aggregated on the bugs, don’t you think?

I have developed an hypothesis to account for the phenomenon of high limpet densities on large aquatic beetles and bugs.  This hypothesis depends on one obvious assumption, one commonplace observation, and one trivial fact, with a couple paragraphs of gratuitous speculation plated on the bottom.

The obvious assumption is that large aquatic beetles and bugs must remain motionless for extended periods of time, in contact with limpet habitat.  I have very little first-hand knowledge upon which to draw here, but my (admittedly superficial) google searches have returned the impression that both the dytiscid beetles and belostomatid bugs demonstrate a wide variety of life habits, but that the big species, in any case, often seem to hunt by stealth.  There are a couple YouTube videos [6] showing periods of both active swimming and quiescent waiting.  Belostomatids seem to rest anywhere, in contact with the bottom or the surface, although dytiscids seem to rest primarily at the surface.  Possibly under lily pads?  Lily pads seem to be prime limpet habitat.

My commonplace observation is that freshwater limpets tend to aggregate on smooth surfaces.  Anybody who has ever hunted for them knows that limpets are more common on smooth rocks than on rough rocks, and less common on the parts of waterlogged woody debris covered with bark than on the parts that have lost it.  When I arrive at a collecting site, one of the first items on my agenda is to wade under the bridge and look for beer bottles.  Limpets reach maximum abundance in old bottles, hard plastics, and smooth litter discarded by fishermen and motorists.  In fact, I have developed the abbreviation “bbl” for my field notes, which means “beer-bottle limpets.”  This means that limpets (of whatever species) were so uncommon as to be found only on smooth litter.

I feel sure this is an adaptation for defense.  Limpets are better able to make a seal with the lips of their shells, and indeed better able to create suction with their foot, on a smooth surface than a rough surface.  It is very nearly impossible to remove a limpet from a beer bottle.  They may slide around on the surface of the bottle, but they do not come off.  For this reason, I keep a scalpel in the pocket of my collecting vest (sheathed in an open plastic sample vial).  The only way to remove a limpet from a really smooth surface without damaging it is to insert a scalpel blade and lift.

My obvious assumption that big aquatic beetles and bugs must hold still, plus my commonplace observation that freshwater limpets tend to aggregate on smooth surfaces, plus the trivial fact that the backs of big beetles and bugs are smooth, can yield a symbiotic association between freshwater limpets and large aquatic insects.  I feel pretty sure that the relationship is positive for the limpets, at least initially, since smooth surfaces yield better protection from predators.  I imagine the relationship is slightly negative for the insects, since the limpets must add a bit of weight, and a bit of drag.  More negative for the bug if attached limpets interfere with its ability to fly, as Andrea suggests.

What might the unusually high densities of limpets we sometimes observe on the backs of aquatic insects eat?  It would be lots of fun to imagine that the limpets are commensal with the bugs – sharing or somehow benefiting from the meat diets of their hosts.  Dytiscid beetles seem to be such sloppy eaters [7] that one might hypothesize increased concentrations of bacteria and fungi on their bodies.  The excellent studies of Calow [8] from the mid-1970s, however, convince me that European Ancylus populations graze rather exclusively on periphytic algae, especially diatoms.  I just cannot find any warrant to imagine that limpets straying onto the backs of carnivorous insects might reasonably switch to anything else.

Which means that the limpets rapidly become hungry.  My gratuitous speculation is that they graze every last diatom cell off the backs of their hosts in a matter of hours, and subsequently ride around in sullen misery, regretting their decision to hitchhike, looking for any opportunity to get off.  Which brings us back to the phenomenon that brought us here, which, I seem to recall, was not symbiosis, but rather transport.

So after this brief but (I hope you’ll agree) interesting digression, next month we’ll return to the theme I introduced last month, which was the aerial dispersal, broadly, of freshwater gastropods, generally.


[1] Freshwater Gastropods Take To The Air, 1991 [15Dec16]

[2] Walther , A. C.,  M. F. Benard, L. P. Boris , N. Enstice , A. Tindauer-Thompson & J. Wan (2008) Attachment of the Freshwater Limpet Laevapex fuscus to the Hemelytra of the Water Bug Belostoma flumineum.  Journal of Freshwater Ecology, 23:2, 337-339, DOI: 10.1080/02705060.2008.9664207.

[3] If you’d like to receive regular alerts from the FWGNA, email me at DillonR@fwgna.org

[4] W. J. Rees (1965) The aerial dispersal of Mollusca.  Proc. Malac. Soc. Lond. 36: 269-282.

[5] Okay, fine, for you sticklers out there!  I understand that the first 13 were records of aquatic Coleopteran beetles, not technically Hemipteran “bugs.”  And I aso realize that the fourteenth wasn’t literally a “flying water bug,” because Andrea collected her Belostoma as they were swimming in the pond.  So technically, the answer to my query of 15Dec16 might still be zero.  I’ll bet you all really irritated your tenth-grade Biology teachers, didn’t you?

[6] Here’s a montage of videos of large belostomatid bugs hunting.  The first one shows a bug holding very still on a bottom of smooth stones (interestingly) waiting for its prey to swim by.  There’s also some footage of another belostomatid hunting from the surface, and then a sequence suggesting ambush from submerged vegetation:
As a bonus, around minute 2:30 there’s a sequence showing a belostomatid capturing and eating a big individual Melanoides.  The bug apparently lunges right by a fat, juicy Helisoma to snatch the bony Melanoides.  I can’t imagine why.

[7] Here’s a YouTube video of a Dytisid making very sloppy work of a minnow:
But we should probably also note simultaneously that belostomatids seem to be very neat eaters, inserting their proboscis and sucking their prey clean from the inside.

[8] Calow, P. (1973) The food of Ancylus fluviatilis Müll., a littoral stone-dwelling, herbivore. Oecologia (Berl.) 13, 113–133.  Calow, P. (1975) The feeding strategies of two freshwater gastropods, Ancylus fluviatilis Müll. and Planorbis contortus Linn. (Pulmonata), in terms of ingestion rates and absorption efficiencies.  Oecologia 20: 33-49.

Thursday, December 15, 2016

Freshwater gastropods take to the air, 1991

Thirty years ago, when I signed my contract with Cambridge University Press to deliver the book that ultimately became The Ecology of Freshwater Molluscs [1] I had a larger project in mind.  The original title of the book was to have been, The Evolutionary Ecology of Freshwater Mollusca, and I planned to cover population genetics all the way up to speciation, as well as life history, competition, predation, communities, and the more traditionally ecological topics.  That was too much.

But before I realized that I had bitten off more than I could chew, I spent the summer of 1991 working on a chapter about freshwater mollusk gene flow.  It included subsections on straight-ahead crawling, drift, and “phoresy” under which I lumped all the cases where mollusks are carried passively by anything, including fish carrying the glochidia of freshwater mussels.  I even covered human-mediated invasions in that chapter, or at least tried.  Way, way too much!

I never submitted my gene flow chapter for publication.  But I rediscovered a hard copy again as I was moving out of my old office this past August, together with a bunch of raw data and tables and figures, and analyses on tractor-feed printer paper, and it re-awakened a dormant interest [2], and gave it a fresh slant.  How much has science advanced in 25 years?  The quick answer is that in some areas, progress has been Yuuuuge!  But in other areas, not so much. 

So for the next couple months we’ll focus on dispersal in freshwater gastropods.  Any study of which, in 1991 or in the present day, might well begin with the charming 1965 “presidential address” offered by W. J. Rees, “The aerial dispersal of Mollusca” [3].  Rees accumulated dozens of published references, notes, stories and anecdotes about both bivalves and gastropods, both terrestrial and aquatic, both pinched onto the feet and riding upon the shoulders of birds, bugs and bats, and even occasionally sucked up in cyclones and spat out on the bowlers of unsuspecting Englishmen. 

Rees collected 10 reports of freshwater limpets on aquatic insects, and I found two additional cases published between 1965 and 1991 – van Regteren Altena (1968) reporting 6 ancylids on the elytra of an aquatic beetle in Surinam, and Rosewater (1970) reporting 2 Laevapex taken from the elytra of a dytiscid beetle captured in a Florida light trap [4].  Does that total surprise you as much as it surprises me?  Even I, who have devoted my entire professional life to malacology, think of freshwater limpets as among the most obscure of all God’s creatures.  They’re just tiny little brown bumps, for Heaven sake!  Would you have guessed 12 published reports of freshwater limpets on flying water bugs?  That’s probably more than the total number of papers published on all other aspects of ancylid biology in North America combined.

The overland dispersal of non-limpet families of freshwater gastropods seems to be significantly less common.  Rees conveyed the report of a single Australian worker, who on different occasions found 6 species of snails on the feet of ducks.  I caught one more – the report of Roscoe (1955) of juvenile Physa, Lymnaea, and Helisoma on the feathers of a white ibis collected in Utah [5].

The review of Rees was followed by a couple really cute experimental papers published between 1965 and 1991 – those of Boag [6] on floating feathers and Malone [7] on severed killdeer feet.

Malone simply shot a killdeer, mounted its legs on a pair of props, and moved them through shallow water where the birds had been observed feeding.  He inspected the legs frequently, never allowing them to remain stationary for more than three minutes.  Two resident snails, Lymnaea humilis (“obrussa”) and Promenetus exacuous [8] often attached passively, drawn by the surface film or dislodged from vegetation as the feet moved through.  Although adult Lymnaea clung no more than five minutes if the feet moved, Promenetus and juvenile Lymnaea remained attached indefinitely.  All snails fell off when re-immersed in water.  Malone reported that L. humilis could survive 2 – 14 hours out of water, and Promenetus 5 – 14 hours, although admittedly not in conditions designed to duplicate flight.

Malone also reported that mature Lymnaea attached to the feathers of a (presumably footless) killdeer body left floating in shallow water for only three minutes.  Continuing along these lines, Boag [6] reared populations of Lymnaea stagnalis, L. elodes, and Helisoma trivolvis from eggs to age three months, periodically floating a feather in each culture pail.  Feathers with adhering snails were removed and placed in an air jet simulating flight speed for up to 15 minutes.  He record the sizes of the snails attached, their detachment rates, and their subsequent viability.  All of the (many) hundred snails found attached to feathers were in the 1 – 3 mm size range.  Although Boag did not monitor the size distributions of the base populations, it seems certain that the volunteer aviators tended to be significantly smaller, especially as the months of his experiment advanced.  The figure below shows his results combined over the duration of the experiment for the population with the largest data set, L. elodes.

Although riding on a feather must at best be only a rough approximation of riding on a bird, it is safe to conclude that either experience is quite rigorous.  Factoring both attachment and survivorship together, Boag’s data show that 56% of the L. elodes would arrive viable after 1 minute of flight, 17% after 5 minutes, 16% after 10 minutes, and only 4% after 15 minutes.  Figures were comparable for L. stagnalis and suggested an even lower probability of successful colonization for H. trivolvis.
Juvenile L. elodes on feathers exposed to simulated flight [6]
Three points emerge from the consideration of Malone’s data together with those of Boag.  First, it is clear that the attachment of snails to birds is the easy part, although perhaps only the smallest are likely to hold on.  And survivorship of these (typically small) individuals riding on birds is probably nowhere near the hours suggested by Malone, but more like minutes.  But finally, since the absolute frequency at which snails become attached to birds may be surprisingly high, even a 4% survival rate may be sufficient to render aerial dispersal a significant factor in initial colonization and subsequent gene flow among populations of freshwater snails.

In 1991 I also reviewed a second set of experiments published by Malone [9] assessing the likelihood of freshwater gastropod dispersal via gut transport.  It’s not great.  Malone fed caged ducks large volumes of aquatic vegetation, to which were attached the adults, juveniles, and egg masses of Physa and Helisoma.  Although he did not offer an estimate of the number of individual snails ingested, one can indirectly infer that this was surely in the thousands.  While no adults or juveniles were identified in the feces, Malone recovered 9 viable Physa embryos.  He also tried feeding about 500 – 1000 Physa egg masses and 200 – 400 Helisoma egg masses to killdeer, collecting feces in aerated water.  A total of 17 viable embryos were recovered.

Almost all of the material above was extracted from my 1991 chapter on dispersal.  So what progress have we made in studies on the aerial dispersal of freshwater gastropods since?  A fair amount, actually.  Tune in next month!


[1] Dillon, R. T. Jr.  (2000) The Ecology of Freshwater Molluscs.  Cambridge University Press. 509 pp.

[2] This is the second essay I have posted on the subject of aerial dispersal in freshwater gastropods, the first coming way back in November of 2005.  I also invoked a gene flow mechanism I termed the “sticky bird express” just this past April.  See:
  • Aerial Dispersal of Freshwater Gastropods [17Nov05]
  • Mitochondrial Superheterogeneity: What it means. [6Apr16]
[3] W. J. Rees (1965) The aerial dispersal of Mollusca.  Proc. Malac. Soc. Lond. 36: 269-282.

[4] van Regteren Altena, C. O.  (1968)  Transport of Ancylidae (Gastropoda) by a water beetle in Surinam.  Basteria 32:1.  Rosewater, J. (1970) Another record of insect dispersal of an ancylid snail.  Nautilus 83: 144-145.

[5] Roscoe , E. J. (1955)  Aquatic snails found attached to feathers of white-faced glossy ibis.  Wilson Bulletin 67: 66.

[6] Boag, D. A. (1986) Dispersal in pond snails: Potential role of waterfowl. Can. J. Zool. 64: 904-909.

[7] Malone, C. R. (1965) Killdeer (Charadrius vociferus) as a means of dispersal for aquatic gastropods. Ecology 46: 551-552.

[8] I’m a bit skeptical of this identification.  Perhaps Promenetus is significantly more common in NW Montana, where Malone conducted his research, than anyplace I have any personal observations.  But my guess would be Gyraulus parvus, not P. exacuous.

[9] Malone C.R. (1965) Dispersal of aquatic gastropods via the intestinal tract of water birds. Nautilus, 78: 135–139.

Monday, November 14, 2016

One Goodrich Missed: The skinny simplex of Maryville is Pleurocera gabbiana

Editor’s Note.  This is the third installment in a three-part series on the discovery of a cryptic pleurocerid species in East Tennessee.  You might want to back up and read my essays of 13Sept16 and 14Oct16 if you haven’t already.  A more technical version of the present essay was published in the FMCS Newsletter Ellipsaria 18(3): 10 – 12 [pdf] if you’re looking for something citable.

Longtime readers may remember the 2007 essay I wrote on Calvin Goodrich [1], who monographed the North American pleurocerids in a series of spare papers published by the University of Michigan 1939 – 1944.  Goodrich synonymized scores of specific pleurocerid nomina without rationale, and simply neglected to mention many more.  And by the end of his six-year effort, what had been a jungle of 1,000 species of North American pleurocerids [2] had been bush-hogged down to a merely untidy 150.  While admitting that Goodrich’s scholarship might not have been the most intellectually satisfying, here’s what I wrote in 2007: 
 “And Goodrich's review has proven to be of great use to malacologists working in American freshwaters today.  My 25 years of research on the population genetics of pleurocerids in the South suggests to me that the total number of biological species in this country will prove to be far less than 500, and indeed less than 100. I haven't found a biological species that Calvin Goodrich missed.”
 So back in September I reported the discovery of two species of Pleurocera cryptic under the common and widely-distributed P. simplex in East Tennessee, “fats” and “skinnies.”  And in October, I matched the fat simplex to the type population in Saltville, Virginia.  Now what are those “skinnies?”

My first thought was to refer back to Goodrich’s (1940) paper covering that part of the world [3], to see if one of the names Goodrich synonymized under P. simplex might be resurrected.  There were only five such names: warderiana, subsolida, densa, vanuxemii, and prestoniana [4].

Goodrich’s papers were unfigured, alas, and so my next move was to pull my trusty copy of Tryon (1873) off the shelves and try to picture-match [5].  If some of the shells of those putative simplex-synonyms figured in Tryon had been skinny, and if their original authors had been so kind as to suggest a type locality, I suppose I would have been strongly tempted to visit that locality and fetch a batch home for genetic work.  But none of the figures in Tryon corresponding to any of the names in Goodrich looked skinny in the least.

Figure 1.   Holotype of Goniobasis gabbiana (center) is compared to exemplars from S1 of Indian Creek (left) and S5 topotypic P. simplex (right).  The scale bar in mm.  A = Apex height, B = Body whorl height.

So I put the question aside for a while, and diverted my attention to other questions.  The thought of describing a new species did cross my mind. But good grief, number 1,001?  Does North America need another nominal species of pleurocerid?

In 2012 the focus of the FWGNA project shifted from East Tennessee to the Middle Atlantic States, and I started paying calls to all the national collections in the big cities of the east.  So it must have been the third or fourth day of my visit to the National Museum of Natural History on Constitution Avenue, and I got getting tired of logging drawers full of Physa.  And I thought I might just have a peek at the type collection, probably more out of intellectual curiosity than anything else.  Isaac Lea described over 400 species of pleurocerids [6] between 1831 and 1869, and (I suppose) a large fraction of his types are housed at the USNM, pretty much all together in a set of locked cabinets off to the side.  And by chance, my eyes happened to fall on USNM 118991, the lectotype of Goniobasis gabbiana.

Isaac Lea first published a brief Latinate description of Goniobasis gabbiana in his (1862) description of the new genus Goniobasis, followed by a more complete (English) description and figure in 1863 [7]. His locality data were uselessly vague: “Tennessee Prof. G. Troost; Alabama Prof. Tuomey.” The species nomen was passed along as valid by Tryon (1873) but was essentially forgotten by Goodrich, who listed it as a “species in doubt” in his 1930 Alabama paper [8] but neglected it entirely in his 1940 review of the Pleuroceridae of the Ohio River drainage system [3], which covered East Tennessee. Thus, although still valid, Goniobasis (or “Elimia”) gabbiana was not included in the more recent reviews of Burch (1989) and Turgeon et al. (1998).  In addition to the lectotype, the USNM holds just two lots labeled Goniobasis gabbiana, both from the nineteenth- century malacologist A. G. Wetherby, neither matching the type. To my knowledge, no pleurocerid lots are held under the nomen gabbiana in any other North American collection.

Figure 2.  The Goniobasis gabbiana collection at the USNM.

In Figure 3, the holotype of P. gabbiana is plotted by its apex height (A) and body whorl height (B) on that graph of Saltville fats and Indian Creek skinnies I developed last month [9]. The match in relative shell dimensions between USNM 118991 and Pleurocera population S1 of Indian Creek would appear nearly perfect. The evidence thus suggests that Pleurocera population S1 at Indian Creek and (by inference) skinny population S6s at Pistol Creek may be identified as Pleurocera gabbiana (Lea 1862), a nomen here revived after 150 years of obscurity.

The fat simplex /skinny simplex situation contrasts rather strikingly with most of my previous experience working with the systematics of the North American Pleuroceridae [10].  Typically intraspecific shell variation is so extreme that nineteenth-century taxonomists have recognized multiple nominal species, and even multiple genera, within single conspecific populations. Here’s the opposite situation, where interspecific shell variation is so slight that twentieth-century taxonomists have not distinguished any differences.

Figure 3. Shell apex (A) as a function of body whorl (B) in P. simplex topotypic population S5 and in population S1 from Indian Ck.  Exemplar shells are noted with arrows, cross marks the lectotype of Goniobasis gabbiana.

Our subsequent field surveys have uncovered 58 additional populations apparently referable to P. gabbiana -- often mixed with typical P. simplex -- locally abundant in small streams of the Tennessee River drainage from the vicinity of St. Paul, Virginia, southwest perhaps 100 km to Madisonville, Tennessee [11]. As we mount expeditions to catalog the rich biodiversity perhaps lying undiscovered in the most remote corners of the earth, we might profitably pause to examine the less exotic but equally remarkable biodiversity we have too often overlooked in our own backyards.


[1]  The Legacy of Calvin Goodrich  [23Jan07]

[2] Graf, D. L. (2001)  The cleansing of the Augean Stables, or a lexicon of the nominal species of the Pleuroceridae of recent North America, North of Mexico.  Walkerana 12: 1 – 124.

[3] Goodrich, C. 1940. The Pleuroceridae of the Ohio River system. Occasional Papers of the Museum of Zoology, University of Michigan 417:1-21.

[4] John Robinson and I added a sixth synonym in 2007, aterina (Lea 1863).  See:
  • Dillon, R. T., Jr. and J. D. Robinson. 2007. The Goniobasis ("Elimia") of southwest Virginia, I. Population genetic survey.  Report to the Virginia  Division  of  Game  and  Inland  Fisheries.  25 pp. [pdf]
[5] Tryon, G. W., Jr. 1873. Land and Freshwater Shells of North America. Part IV, Strepomatidae.  Smithsonian Miscellaneous Collections 253, 435 pp. Washington, D.C

[6] By my actual count, paging through Graf [2], Isaac Lea described 438 species of North American pleurocerids.  Not counting all the spelling errors and similar screw-ups by subsequent authors.

[7] Lea, I. (1862) Description of a new genus (Goniobasis) of the family Melanidae and eighty-two new species. Proceedings of the Academy of Natural Sciences, Philadelphia 14:262-272.  Lea, I. (1863) New Melanidae of the United States. Journal of the Academy of Natural Sciences, Philadelphia 5:217-356.

[8] Goodrich, C. 1930. Goniobases of the vicinity of Muscle Shoals. Occasional Papers of the Museum of Zoology, University of Michigan 209:1-25.

[9] The Fat Simplex of Maryville Matches Type [14Oct16]

[10] Papers documenting the situation where high levels of shell phenotypic variation have fooled previous authors into recognizing multiple species of pleurocerids where only one exists: Dillon, R. T., Jr. and J. D. Robinson (2011)  The opposite of speciation: Population genetics of Pleurocera (Gastropoda: Pleuroceridae) in central Georgia. American Malacological Bulletin 29:159- 168 [pdf].  Dillon, R. T., Jr.  2011.  Robust shell phenotype is a local response to stream size in the genus Pleurocera (Rafinesque 1818). Malacologia 53: 265-277 [pdf].  Dillon, R. T., Jr., S. J. Jacquemin and M. Pyron.  2013.   Cryptic phenotypic plasticity in populations of   the freshwater prosobranch snail, Pleurocera canaliculata.  Hydrobiologia 709:117-127 [pdf].  Dillon, R. T., Jr. 2014. Cryptic phenotypic plasticity in populations of the North American freshwater gastropod, Pleurocera semicarinata. Zoological Studies 53:31 [pdf].

[11] A detailed map comparing the distributions of P. simplex and P. gabbiana in East Tennessee and SW Virginia is downloadable from the FWGNA site.  [pdf map]

Friday, October 14, 2016

The Fat simplex of Maryville matches type

Editor’s Note.  This is the second installment of a three-part series on the discovery of a cryptic pleurocerid species in East Tennessee.  You might want to back up and read my essay of 13Sept16 if you haven’t already.  The present essay was published in the FMCS Newsletter Ellipsaria 18(2): 16 - 18 [pdf] if you’re looking for something citable.

So when last we left our intrepid malacologist, puzzling at his lab bench in the summer of 2008, he had come around to the realization that the population of Pleurocera simplex inhabiting Pistol Creek at the Courthouse Park in Maryville, Tennessee, was actually two reproductively isolated populations, fats (S6f) and skinnies (S6s).  Which population might be the bona fide P. simplex of Thomas Say (1825)?  And what might be the identity of the other?

I actually started out with a pretty good hunch.  In 2007 John Robinson and I ran allozyme gels on five populations of P. simplex from up in Virginia, including a nice sample from Say’s type locality in Saltville [1].  The Saltville population (S5) was fixed for the Oldh100 allele that turned out to be diagnostic for the Maryville S6f fats.  And interestingly enough, the simplex population John and I sampled from Indian Creek at Kesterson Mill way down at the southwest tip of Virginia (S1) was nearly fixed for that Oldh104 allele diagnostic for the Maryville S6s skinnies.  I hadn’t noticed any shell morphological differences between the Saltville simplex and the Kesterson Mill population at the time, however.

So in August of 2008 [2] I drove up to Virginia for additional samples from Saltville and from Kesterson Mill, which I returned to Charleston to run alongside a fresh batch of Maryville samples, to make sure all the bands matched up. Sure enough, the Maryville S6f fats were indeed genetically similar to P. simplex collected from its type locality at Saltville S5, not just at the Oldh locus but over all ten of the allozyme loci I have found informative for studies of this sort.  And the Maryville S6s skinnies were similar to Kesterson Mill S1.

Figure 1.  See footnote [3] for methodological details.

I also took the calipers to a bunch of the shells from Saltville and Kesterson Mill.  And sure enough, exactly the same pattern reappeared that we first noticed at Maryville.  Dividing the total shell length into body whorl height (B) and apex height (everything else, A), the (N = 37) shells I sampled from Kesterson Mill showed a significantly greater ratio of A to B than the (N = 40) shells from Saltville.  Figure 2 shows that the simple regression of apex height on body whorl height for the Saltville type population S5 was A = 0.157B + 2.46 (r = 0.36), very significantly different (ANCOVA t = -9.52, p < 0.0001) from the regression for the Kesterson Mill population S1, A = 0.556B - 0.09 (r = 0.84).  Saltville snails are fat, and Kesterson Mill snails are skinny.

Figure 2.

I have picked two shells directly off the regression lines to illustrate the difference between the two species.  So since the Maryville S6f fats match that lower-sloping S5 sample of N = 40 from Saltville both genetically and morphologically, and since Saltville is the type locality of Pleurocera simplex (Say 1825), clearly the Maryville S6f fats must be the bona fide simplex [4].

Then what might be the identity of the Maryville S6s skinnies, matching the higher-sloping S1 population from Kesterson Mill both genetically and morphologically? Tune in next time!


[1] Dillon, R. T., Jr. and J. D. Robinson. 2007. The Goniobasis ("Elimia") of southwest Virginia,  I. Population genetic survey.   Report to the Virginia Division of Game and Inland Fisheries.  25 pp. [pdf]

[2]  Yes, this was the same trip I featured last month, in which I resampled Maryville.  I’ve been sandbagging my story a little bit, to make it unfold in a more linear fashion.  To tell you the truth, I got the “hunch” mentioned in this month’s essay pretty much immediately upon reading my first Maryville simplex gel, and last month’s story unfolded pretty much simultaneously with this month’s story.

[3] Subsamples of 14 individuals from population S5 and 41 from population S1 were analyzed electrophoretically together with the 20f + 51s individuals from Pistol Creek I featured in last month’s blog post.  These data were combined with the data sets of N = 34 from population S5 and N = 37 from population S1 previously published by Dillon & Robinson (2007), and with the N = 17f + 13s data I had previously accumulated from Maryville. Then BIOSYS version 1.7 (Swofford & Selander, 1981) was used to calculate matrices of Nei's (1978) unbiased genetic identity (below the diagonal in Fig 1) and Cavalli-Sforza and Edwards (1967) chord distances between all pairs of control populations S1 and S5 and the two cryptic S6 populations co-occurring in Maryville. Chord distances were used as the basis for the neighbor-joining tree shown above the diagonal in Figure 1, as calculated using PHYLIP v3.65 program NEIGHBOR (Felsenstein, 2004).

[4]  Ultimately I only used that sample of 20 + 17 = 37 fats as my S6 Maryville control in Dillon 2011.  The existence of a second Pleurocera population at Maryville cryptic under simplex was not mentioned in my 2011 paper at all:
  • Dillon, R. T., Jr.  2011. Robust shell phenotype is a local response to stream size in the genus Pleurocera (Rafinesque 1818).   Malacologia 53:265-277. [pdf]