What Is A Subspecies?

Editor’s Note – This essay was subsequently published as: Dillon, R.T., Jr. (2019c) What is a subspecies?  Pp 77 - 82 in The Freshwater Gastropods of North America Volume 3, Essays on the Prosobranchs.  FWGNA Press, Charleston.

Subspecies are populations of the same species in different geographic locations, with one or more distinguishing traits.  This is the modern textbook definition [1], due primarily to the 1942 work of Ernst Mayr [2].  The concept is so simple and basic to the training that most of us probably received as undergraduates that it is difficult to imagine how anybody could become confused about it.  But they do.

No, not any of you reading this essay!  I’m sure you all get it.  But (hard though it may be to believe) there are some evolutionary biologists active in our field today who imagine that Mayr’s definition of the noun “subspecies” says more than it does.  So indulge me while I make three (obvious) points. 

Point number 1 is that no definition of the word “subspecies,” ancient or modern, has ever specified anything about heritability.  Yes certainly, the morphological differences that distinguish subspecies A and B might indeed have a genetic basis.  In fact, subspecies are sometimes referred to as “insipient species.”  But even if the “one or more distinguishing traits” are entirely ecophenotypic in their origin, arising as plastic responses to differences in environment A and environment B, the validity of the subspecific status of populations A and B would not be compromised.

Point number 2 follows from point number 1.  If the trait(s) by which a subspecies is distinguished need have no heritable basis, then populations united under the same subspecific trinomen need share no evolutionary history.  Similar ecophenotypic responses can be elicited multiple times independently.

And point number 3 is that the modern definition of the subspecies also says nothing about the existence of morphological intermediates.  Yes, it is certainly possible that subspecies A and B might be universally distinguishable.  But typically just the opposite is the case.  To quote a recent review [3], “Intergradation at the boundary between two geographic replacement forms is the touchstone of trinominalism.”  So if, for example, a third population C exists, in an intermediate region or an intermediate environment between population A and population B, the demonstration of a perfectly intermediate C phenotype would not compromise the subspecific status of A and B.  Subspecies only need be distinguishable somewhere, not everywhere.

So to take a real example.  Many rivers of the Piedmont and upper Coastal Plain from Virginia to Georgia are inhabited by populations of (typical) Pleurocera catenaria, bearing shells with prominent costae, dissected by spiral cords.  These populations reach maximum abundance in rocky shoals in medium to large rivers.   Smaller and sandier tributaries, entering the larger rivers farther east in the coastal plain, are sometimes inhabited by populations with much plainer shells, lacking spiral cords and often demonstrating reduced costation as well.  Goodrich [4] referred these populations to a subspecies, Pleurocera ("Goniobasis") catenaria dislocata.

I strongly suspect that the shell differences between dislocata populations and typical catenaria populations have little heritable basis [5].  And in fact, a population genetic survey I published in 2002 [6] suggested that the dislocata phenotype seemed to have evolved multiple times independently.  The matrix below shows that the genetic identify between a Savannah dislocata population (“Srp”) and a Savannah catenaria population (“McC”) was 0.86, and that between a Broad/Santee dislocata (“Sant”) and Broad/Santee catenaria (“Cola”) was 0.89, but that the genetic identity between the two dislocata populations was only 0.81.

And although dislocata populations are distinctive in South Carolina, they intergrade with typical catenaria throughout the Tar River drainage of North Carolina.  The figure at the top of this essay shows three shells from Red Bud Creek in Nash County, a dislocata individual on the left without spiral cords, a typical catenaria on the right with strong cords, and an intermediate individual in the middle.

But none of these considerations – the questionable heritability of the distinguishing traits, their multiple independent origins, or the existence of intermediate forms – compromises the validity of Goodrich’s subspecific designation Pleurocera catenaria dislocata.

Many of my colleagues tell me that they “don’t like subspecies.”  And without question, the description of subspecies has fallen out of favor in modern evolutionary biology.  It is an old-school concept, dependent on the taxonomist’s subjective understanding of the adjective, “distinguishing.”  And modern classifications are supposed to reflect the evolutionary history of the populations being classified.  It seems misleading to lump a subset of Pleurocera catenaria populations under the subspecific trinomen “dislocata” that have, for reasons we admittedly do not understand, come to look similar independently.

On the other hand, some of us (on rare occasions, perhaps) find the composition of freshwater gastropod communities provides helpful information about the environment from which they were sampled [7].  So if populations of Pleurocera catenaria dislocata are indeed associated with shallower, sandier creeks than typical P. catenaria catenaria, the trinomial distinction would seem to serve a valuable function.

Moreover, the Linnean system of nomenclature was instituted neither to recapitulate the evolutionary history of the organisms being classified, nor to facilitate ecological generalizations.  Carl von Linne conceived his system of taxonomy for information retrieval, like a Dewey-decimal filing system for critters [8].  And very simply, a trinomial carries more information than a binomial.

So in the final analysis, I find the ecological and “information retrieval” arguments for subspecies more compelling than the evolutionary arguments against them.  There does exist a small (but not negligible) scientific literature associated with the pleurocerid nomen “dislocata,” which would be lost (or become much more difficult to Google, anyway) if that nomen were to disappear today.

And even more the shame for such better-known pleurocerid nomina as acuta, pyrenellum, and unciale/uncialis from the American interior.  The populations described by these names are indeed geographically separate (usually) and morphologically distinctive (usually) to the point that they have been recognized as valid species until quite recently [9].  Why not save the nomina as subspecies?   As long as we are clear that there may be no heritable basis for the distinction between Pleurocera canaliculata acuta and Pleurocera canaliculata canaliculata, and that the acuta phenotype seems to have arisen many times independently, and that intermediate populations exist between the typical, robust canaliculata form and the more slender acuta form [10], it seems to me that the information indexed to the name “acuta” is worth saving.

So at present, the FWGNA project recognizes four sets of subspecies, all in the family Pleuroceridae:  the catenaria/dislocata pair, the clavaeformis/unciale pair, the floridensis/timida pair [11], and the canaliculata/pyrenellum/acuta triplet.  Although none of these subspecific distinctions likely has any evolutionary basis, all these nomina most certainly do serve important indexing functions, and hence warrant preservation.

But everything I have written in my essay this month is predicated upon a firm understanding of the word “subspecies,” as defined in the first sentence of this essay.  What mischief might be visited upon evolutionary science by our colleagues should any of them become confused?  Tune in next month!

Notes

[1] Quoted verbatim from the glossary of Price, P. W. (1996) Biological Evolution. Saunders College Publishing.

[2] Mayr, E. (1942) Systematics and the Origin of Species. Harvard University Press, Cambridge, MA.

[3]  Mallet, J. (2007) Subspecies, semispecies, superspecies.  In Encyclopedia of Biodiversity [pdf]

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

[5] Urabe, M. (2000) Phenotypic modulation by the substratum of shell sculpture in Semisulcospira reiniana (Prosobranchia: Pleuroceridae). J. Moll. Stud. 66: 53-59.  See:

• Semisulcospira Research: A Message from The East.  [6Jan08]

[6] Dillon, R.T. & 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]

[7] See “Models of Species Distribution” (pp 391 – 407) in my book, The Ecology of Freshwater Mollusks (Cambridge University Press, 2000). [html]

[8] The information-retrieval function of zoological nomenclature is not incompatible with its scientific function, but not compatible, either.  See:

• When Worlds Collide: Lumpers and splitters.  [4Sept12]

[9] Dillon, R. T., Jr. (2011)  Robust shell phenotype is a local response to stream size in the genus Pleurocera.  Malacologia 53: 265-277.  [pdf]  See:

• Mobile Basin III: Pleurocera puzzles [12Oct09]
• Goodbye Goniobasis, Farewell Elimia [23Mar11]

[10] Dillon, R.T.,Jr., S. J. Jacquemin & M. Pyron (2013)  Cryptic phenotypic plasticity in populations of the freshwater prosobranch snail, Pleurocera canaliculata.  Hydrobiologia 709: 117-127 [html] [pdf]  See: 

• Pleurocera acuta is Pleurocera canaliculata [3June13]
• Pleurocera canaliculata and the Process of Scientific Discovery [18June13]

[11] Although web pages are not (at present) available for the typical Pleurocera floridensis floridensis.  Coming one day, I promise.

Why is Rarity?

We should begin this essay by reminding our readership of the very precise (and perhaps rather peculiar) definition of the adjective “rare” adopted by the FWGNA project, as developed in our essay of last month [1].  We have defined a species as “rare” if the number of samples in which it has been recorded ranks it in the lowest 25% of all species in the fauna under study.  We call this “incidence rarity,” to distinguish it from “abundance rarity,” which is the other way in which rareness is commonly defined [2].

We should also remind our readership that in the present discussion of rarity we have been led by a prominent authority of the subject, Prof. Kevin J. Gaston.  And point out that immediately after Prof. Gaston concluded sections 1.1 and 1.2 of his 1994 book [4] on the definition of rarity, he set his pen to several sections on scale-dependence, and the methods by which a biota might be circumscribed for study.  Because the first explanation for the phenomenon of rarity that occurred to Prof. Gaston was, in his own words, that:

“at local and regional scales, many (species) are not permanent members of the assemblage, do not breed, or do not have self-sustaining populations in the area of interest.  Such species have been variously termed accidentals, casuals, immigrants, incidentals, strays, tourists, transients and vagrants; I shall refer to them as vagrants.”

Prof. Gaston then went on to describe what he termed “the problem of vagrancy.”  Vagrants are typically over-represented in the fraction of the biota that workers in the field identify as “rare.”  Most of the bird species regarded as rare in Britain are vagrants, for example.  But such vagrants are (quite often) not rare elsewhere.  They are what Gaston calls (later, in Chapter 2) “pseudo-rare.”

The data we have gathered for our “Synthesis” of freshwater gastropod incidence in the Atlantic drainages of nine US states [5] do indeed demonstrate a phenomenon rather closely analogous to Gaston’s “problem of vagrancy.”  Our database contains only 4 records of Pleurocera floridensis, for example, ranking P. floridensis well down in the bottom quartile of the 67 freshwater gastropods listed in Table 1 [6].  But there is strong (albeit indirect) evidence suggesting that P. floridensis populations are not rare elsewhere.  The distribution map of S. M. Chambers at left [7] shows almost 100 populations of P. floridensis (as black circles) in the springs and rivers of western Georgia and Florida.

Pleurocera floridensis is not a “vagrant” as Gaston has defined that term, however.  Populations of pleurocerid gastropods do not blow in and out of our study area like birds [8].  And there is no reason to think that the 4 populations of P. floridensis we have documented (shown as green circles above) are not permanent or “self-sustaining.”  Rather, the reason that that P. floridensis appears rare in Table 1 but almost certainly is not actually rare is that our study area (green) has (by chance) only touched the northern edge of the P. floridensis range.  Pleurocera floridensis is not (literally) a “vagrant,” it is “peripheral.”

Here is the definition of the word “peripheral” we have adopted for use in the FWGNA project [9].  A species will be described as peripheral if it demonstrates less than median incidence within our area of study, but greater than median incidence outside our area of study.

So our fauna of 67 freshwater gastropod species includes 34 demonstrating incidences below the median of 23 records in our database.  To determine which of these 34 are peripheral in our study area will admittedly require some speculation on our part, because no data are available from outside our study area comparable in quality to those available inside.  But based on our reading of the literature [10] it would appear that exactly half – 17 – are peripheral.  Although Table 1 shows that these 17 species demonstrate below-median incidence in our study area, the published literature contains evidence suggesting that they may demonstrate above-median incidence elsewhere.

That subset of 7 peripheral species appearing in the bottom quartile of Table 1 are, to borrow Gaston’s term, “pseudo-rare.” And here is another remarkable insight brought to us by the good Professor Gaston.  There must also exist a condition he calls “non-apparent rarity,” which is the situation where species are indeed rare, but their rareness is not revealed in the data available.  Non-apparent rarity is the opposite of pseudo-rarity.  And:

“under some definitions of rarity one state cannot occur independently of the other.  For example, under a proportion of species definition, the misclassification of a species as rare when it is not must necessarily entail the misclassification of a species as not being rare when in fact it is.”

To summarize.  All 10 of the species marked in Table 1 as I-1 and I-2 (simply, without a suffix of “p”) are most certainly rare.  The 7 species marked I-1p and I-2p are pseudo-rare.  Then moving up Table 1, the 7 species marked I-3* demonstrate non-apparent rarity, deserving to have been ranked in the bottom quartile, but displaced by the 7 peripheral species occupying their spots.

I hate to draw a line here, but (once again) I sense I may be nearing the maximum length this peculiar format can comfortably contain.

I will close by noting, however, that we have barely “touched the periphery” of the question we have undertaken to address, the “why” of rarity.  The second explanation that occurred to Prof. Gaston, actually better described as a class of explanations, would be sampling error.  Species may appear rare because they are small or cryptic, clumped or aggregated, undersampled by the gear, and so forth.  The related sins of "conservation-biased oversampling" [11] and trash-snail undersampling occurred to me as I read this section of Gaston's book.

Professor Gaston does not begin to explore the causation of bona fide rarity until Chapter 6, which he divides into two subsections:  “environmental factors” and “colonization ability.”  And it is not until page 126 (in 163 pages of text) that it occurs to Prof. Gaston that human activities might have some effect on rarity, or that rarity might be anything other than a perfectly ordinary phenomenon of nature.

Yes, rare species are more likely to become extinct than common species.  And it is toward the subject of conservation that Prof. Gaston ultimately turns, in his Chapter 7.  But as he does so, this is his observation:  “Considerations of rarity lead almost ineluctably to the topic of conservation.  Indeed, it seems a popular belief that the two issues are inseparable.  Previous chapters should have established beyond any doubt that this is not so.”  Amen.

Notes

[1] What is Rarity?  [9Dec13]

[2] Actually there is a third way in which rarity can be understood – high habitat specificity.  This sets up a 2x2x2 classification by geographic range, local population size, and habitat specificity, with eight cells in the box.  Only species in one of these cells (demonstrating a wide range, large population sizes and low habitat specificity) will be considered common by everybody.  The other seven cells contain species that are rare, in some sense [3].  See Rabinowitz, A. B. (1981) Seven forms of rarity.  Pp 205 – 217 in “The Biological Aspects of Rare Plant Conservation” (Ed. H. Synge) Wiley, NY.

[3] Honestly, it is very easy to explain why species are rare.  The more difficult question would be “Why is anything common?”

[4] Gaston, K. J. (1994) Rarity.  Chapman & Hall Population and Community Biology Series 13. 205 pp.

[5] See the FWGNA Synthesis page for additional details.

[6] FWGNA Synthesis Table 1.  The 67 freshwater gastropod species inhabiting US Atlantic drainages, ranked by total incidence. [pdf]

[7] Chambers, S. M. (1990)  The genus Elimia (Goniobasis) in Florida (Prosobranchia: Pleuroceridae)  Walkerana 4: 237 - 270.

[8] Which is not to imply that aerial dispersal of freshwater gastropods is unimportant!  See [17Nov05]

[9] From late 2013 until mid-2015, I preferred the adjective "marginal" to describe populations demonstrating less than median incidence within the study area, but greater than median incidence outside it.  I ultimately changed from "marginal" to peripheral as a concession to previously-established usage in the ecological community.

[10] The most important references here were:

Jokinen, E. H. 1992.  The Freshwater Snails (Mollusca: Gastropoda) of New York State.  Albany: New York State Museum.  112 pp. 

Thompson, F. G. 1999.  An identification manual for the freshwater snails of Florida.  Walkerana 10 (23): 1 – 96.

[11] Toward the Scientific Ranking of Conservation Status - Part III [19Mar12]

What is Rarity?

Editor's Note - While the text of the post below remains relevant, in November 2015 the FWGNA database was expanded to include 6.5% additional records and 2 new species.  See the current FWGNA Synthesis page for our most recent analysis.

In recent weeks I have received some very generous compliments regarding the brand new “Synthesis” of freshwater gastropod abundance posted on the FWGNA site.  Essentially what my colleagues and I have done is delete the old “Recommendations” pages that used to be available separately from the FWGGA, FWGSC, FWGNC and FWGVA sites and replaced that little corner of cyberspace with a combined analysis of the “distribution of commonness and rarity” across all 67 species of freshwater gastropods (11,471 records) inhabiting the Atlantic drainages of the United States, from Georgia to the New York line [1].

My initial motivation was simply to expand (and formalize) the analysis I first proposed on this blog in January 2012 [2], adding data from five Mid-Atlantic states to data already in hand for the four states further south.  I confess that I was a bit disappointed, however, when the enlarged dataset did not fit a lognormal model this second time around, because I had already written a nice discussion section explaining why it should, and exploring all manner of elaborate implications about broad-scale ecological relationships in this diverse assemblage of freshwater gastropods over evolutionary time.  But I was teetering on the ragged edge of rejecting the lognormal in January 2012, with my Shapiro-Wilk W barely nonsignficant at p < 0.065, and an additional 2,597 records (and 10 species) pushed me off to p < 0.032.  So the new FWGNA “Synthesis” is entirely nonparametric.  Such is science.

During the literature review for this most recent analysis I came across a little jewel of a book which I think deserves a wider audience: “Rarity” by a (then) Fellow at the British Museum, Kevin J. Gaston [3]. The first chapter of Gaston’s book offers an especially insightful dissection of the meaning of the adjective, “rare,” beginning with all the dictionary definitions and proceeding through (what seems to be, almost!) every imaginable scientific usage in modern history.

The author takes as a given that the adjective “rare” must be a comparative term.  Things can only be rare relative to other things, which are called common.   At first blush, it might seem odd that Gaston does not explicitly consider such “absolute rarity” measures as seem to be popular in state natural heritage agencies here in the USA.  For example, North Carolina botanists define “significantly rare” as “generally with 1 – 100 populations in the state,” apparently unscaled by anything [4].  But the (unstated) implications of such an approach must be that plants with greater than 100 populations are insignificantly rare in North Carolina, and that the significants are rare relative to the insignficants.  If my wife passes me a trapezoidally-shaped bowl with 100 red candies in it, I would not consider red candy to be rare.  But if the bowl contained 100 red candies and 1000 browns, I might.

Now if there are more than two colors of candy in the bowl, say 100 red, 500 green, and 1000 brown, an additional complication may arise.  Perhaps the rareness of red remains unchanged, as 100/1000 or 100/1100?  Or perhaps red is now even more rare, as 100/1600?  Or perhaps rareness is best expressed as 1/3, unweighted by frequency?  The most interesting analysis in Gaston’s Chapter 1 is his demonstration that the most robust definition of a rare species is “the x% with the lowest abundances or smallest range sizes in the assemblage.”  Gaston would prefer the rank statistic for his bowl of candy, the rareness of red being 1/3.

Back in my essay of January 2012, I expressed a concern that most of the literature (with which I was familiar at the time) focused on the rarity of individuals within communities.  So if F. C. Baker’s samples of Oneida Lake contained 32 species, with Planorbula armigera ("jenksii") the least abundant (just N=1 individual), everybody will concur that Planorbula is rare in Oneida Lake [5].  But FWGNA data are incidences across a wide geographic area, not individuals within a single community.  So if the fauna of US Atlantic drainages from Georgia through Pennsylvania comprises 67 species, and Aplexa hypnorum is found in the lowest number of sample sites (just N=1 pond), is Aplexa rare in the same sense that Planorbula is rare?

Yes, Gaston reassures us that any technique we might apply to analyze the abundance-rarity of snail individuals within a single lake will generalize to the incidence-rarity of snail populations across nine states.  Note that his definition of rarity above makes no distinction between “lowest abundances or smallest range sizes.”  The ecological causes for these two types of rarity most certainly do differ, but the analytical consequences are the same.

Ultimately, although some statistics to measure rarity are more robust than others, the dividing line between rare and common must need be a subjective decision.  So what is a reasonable value for “x” in Gaston’s definition three paragraphs above?  Gaston’s remarkably insightful first chapter also includes a Table 1.4 reviewing 20 studies (mostly of plants and birds) in which the authors have both defined the word “rare” and provided data sufficient to calculate rarity, in its “proportion of species” sense [6].  And Gaston’s judgment suggested to him that a fair consensus might be 25%.

So ultimately, Gaston settled on what he called “the quartile definition,” defining rare species as the 25% with the lowest abundance or lowest incidence.  And this is the definition we have adopted for the FWGNA project as well, expanding Gaston’s concepts across the entire nine-state study area to elaborate a five-tiered system.  We elect to set aside the rarest 5% of the freshwater gastropod species in a special incidence category I-5, leaving the next 20% as I-4, and successive (increasingly widespread) quartiles I-3, I-2, and I-1.

So now that we have defined rarity, what are its causes?  That might be suitable grist for a future post.  But in closing I probably ought to re-emphasize the main point of the present essay, which at one time I should have imagined might be obvious to all my colleagues in this field, but which (I now have some reason to fear) may be lost on some.

Among the more colorful comments I received regarding my post of 9Sept13 [7] was the following: 

“You also go on about how this or that COMMON species of snail has been negligently overlooked in the list for Delaware or New Jersey.  Planorbella campanulata, Physella gyrina, P. acuta, P. heterostropha – who gives a S**T.   It’s f***ing Delaware and New Jersey and it’s not the FOCUS OF THE PAPER – which if you need reminding is about conservation of rare species.”

A species can be rare only by comparison with other species.  Unless we know what is common, we cannot recognize what is rare.  The comment above reminds me of the frat brother who said he’d rather have two slices of pizza than half a pizza, because he “didn't give a S**T about denominators.”

Notes

[1] The 2013 data and analysis are available for download here - [PDF]

[2] Toward the Scientific Ranking of Consevation Status – Part II.  [9Jan12]

[3] Gaston, K. J. (1994)  Rarity.  Chapman & Hall Population and Community Biology Series 13.  205 pp.  Prof. Gaston is currently at the University of Exeter.

[4] Two big reports, the North Carolina “Rare Plants List,” and the “Rare Animals List,” are downloadable here:

• NCDNER Natural Heritage Program Publications

Despite being entitled “Natural Heritage Program List of Rare Plant Species of North Carolina 2012” and “Natural Heritage Program List of Rare Animal Species of North Carolina 2012,” neither of these reports has much to do with rarity.  Both seem to be focused almost entirely upon such unscientific categories as “endangered,” “threatened,” “imperiled,” “vulnerable,” and “secure.”  A definition for “significantly rare” is, however, to be found at the bottom of page 6 in the plants list.

[5] Dillon, R. T. (1981)  Patterns in the morphology and distribution of gastropods in Oneida Lake, New York, detected using compuer-generated null hypothses.  American Naturalist 118: 83-101.  [PDF]

[6]  None of Gaston’s 20 examples included any references to the voluminous gray literature generated by natural heritage agencies here in the USA - state, federal, or NGO.  I cannot pretend to more than passing familiarity with any of it, myself.  But in the few cases of which I am aware, such as the NC “Rare Plants List” cited above, rarity definitions are incomplete.  Gaston might have summed up the “significantly rare” species of plants in North Carolina for his numerator, but we are not given the total species count for our denominator.

[7] Plagiarism, Paul Johnson, and The American Fisheries Society.  [9Sept13]

Potamopyrgus in US Atlantic Drainages

Editor’s Note – This essay was subsequently published as: Dillon, R.T., Jr. (2019d)  Potamopyrgus in US Atlantic drainages.  Pp 41 - 45 in The Freshwater Gastropods of North America Volume 4, essays on Ecology and Biogeography.  FWGNA Press, Charleston.

Hidden deep inside last month’s big release of the new “Freshwater Gastropods of Mid-Atlantic States” web resource was at least one item of unwelcome news.  A population of  the New Zealand Mud Snail, Potamopyrgus antipodarum, has been discovered in Spring Creek, a small tributary of the Susquehanna River in Centre County, PA.  This is the first record of Potamopyrgus from a US Atlantic drainage.

The circumstances surrounding the discovery are interesting, possibly even edifying.  The Pennsylvania Department of Environmental Protection has long maintained a water quality monitoring site #WQN415 on Spring Creek at the County 3001 bridge, at which they collect regular macrobenthic samples.  And I paid a call on the PADEP lab in Harrisburg this past spring, as an important stop on my regional tour of similar facilities around the East, reviewing the freshwater gastropod components of (what typically turn out to be) large collections of vials stuffed with large collections of mostly bugs.  And I actually held a vial of macrobenthos collected on 7Oct10 from WQN415 in my hand this past March 20, and saw (what I remember as) a very large number of very minute hydrobiids washing around at the bottom.  And misidentified them as Fontigens.

I wrote “F. nickliniana teensy and weird” on line #415 of the spreadsheet I carried that day on my clipboard.  In retrospect, I’m surprised that I remember anything at all about any particular vial among the thousands I have examined over the last 18 months.  But I don’t think any of those (hundreds?) of tiny little gastropods contained in vial #415 was much over 1 mm standard shell length.  I don’t remember any individuals that looked like legitimate adults.  But surely a sample containing hundreds of individuals couldn't be comprised entirely of juveniles, could it?  In retrospect, my eyes were not prepared to see what they were looking at.

So six months later, our good friend Steve Means of the PADEP sent me an email inquiry with “New Zealand Mud Snail in Spring Creek, Centre County” on the subject line.  And the jpegs attached to his email (one of which is inserted above) clearly depicted adult Potamopyrgus antipodarum in the 4-5 mm range, collected this most recent summer at WQN415.  Oops!  A bit red-faced, I added P. antipodarum as species #41 to the Mid-Atlantic photo gallery, and composed species page #87 for the FWGNA site [1].

Potamopyrgus is a notorious invader, making its first North American appearance in Idaho’s Snake River back in 1987.  Populations spread to Montana in 1995, Oregon and California in 1997, and as far as Arizona in 2002 [2]. Most of the western populations seem to be associated with trout fishing, and it has been speculated that their spread has been facilitated either by untidy anglers, or by gut passage in the fish themselves.

Meanwhile back East, populations of Potamopyrgus were first reported in Lake Ontario in 1991, Lake Superior in 2001, and Lake Erie in 2005 [3].  The eastern populations seem more associated with commercial shipping, the implication being that they might represent a separate introduction via bilge water.  And recent research has indeed confirmed that the eastern and western populations represent genetically distinct clones [4].

The Spring Creek population obviously inhabits an eastern longitude, but is quite intimately associated with trout fishing.  PADEP water quality monitoring station WQN415 is located approximately 1-2 km downstream from the Bellefonte State Fish Hatchery, on a stretch of river marked “Fisherman’s Paradise” in my topographic map book [5].  I understand from Steve that the hatchery does not import trout into its facility, from the West or anywhere else, and that recent benthic surveys show lower densities of Potamopyrgus at the hatchery, increasing downstream toward WQN415.  This strongly suggests that the source of the introduction has not been the fish, but the fishermen.

Might some transcontinental angler have carried a sticky creel or muddy set of boots all the way from Montana to Pennsylvania?  Or is the Spring Creek population a fresh introduction of the eastern clone, which has heretofore seemed primarily associated with commercial shipping [6]?  I understand that our colleagues Ed Levri of Penn State Altoona and Mark Dybdahl of Washington State University are working on this question as we speak.

Meanwhile, the Pennsylvania Fish and Boat Commission has issued the press release available from the link below:

• PFBC Issues Alert to Contain Invasive Species in Centre County [pdf]

Further spread throughout the Susquehanna drainage would seem inevitable, however, especially to nearby tributaries popular with the anglers.  Reference to the PFBC website [7] reveals a smorgasbord of Class – A streams in central Pennsylvania, including Logan Branch a few km to the east of Spring Creek and Buffalo Run a few km to the west.  Logan Branch even hosts a state trout hatchery.  Were I a researcher in the central Pennsylvania area interested in freshwater community ecology or energy flow, I’d begin planning my baseline studies in Logan Branch right now.


Notes

[1] For a broad review of the general biology, life history, ecology and systematics of the New Zealand Mud Snail, see the FWGNA species page...

• Potamopyrgus antipodarum

[2]  ...or the USGS Nonindigenous species database:

• Potamopyrgus antipodarum

[3]  See “Invaders Great and Small”  [19Sept08]

[4]  From the Aquatic Nuisance Species Taskforce:

• National Management and Control Plan for the New Zealand Mudsnail [pdf]

[5] The image of the “Fishermans Paradise” sign comes from the PFBC website:

• Bellefonte Hatchery

[6]  Although populations of the Great Lakes clone typically seem to reach maximum abundances at depths of 4 meters and below, recent surveys have uncovered populations in two small streams in western New York state, draining into Lake Ontario perhaps 300 km north of Spring Creek.  See Levri, Colledge, Bilka & Smith (2012) The distribution of the invasive New Zealand mud snail in streams in the Lake Ontario and Lake Erie watersheds.  BioInvasions Records 1: 215-219.

[7] Here’s a very nice interactive map from the PFBC:

• Trout Fishing Waters of Pennsylvania

Freshwater Gastropods of Mid-Atlantic States

We are pleased to announce that a new web-based resource, the Freshwater Gastropods of Mid-Atlantic States by R. T. Dillon, M. A. Ashton, and T. P. Smith, is now available from the FWGNAwebsite.  Hit the big FWGNA logo at right, and click the Mid-Atlantic region for a tour!

This is the sixth region to be added to the FWGNA site since its debut in 2003, extending our coverage from Georgia to the New York line, raising the total species reviewed from 79 to 87.

The new Mid-Atlantic site covers Delaware, Maryland, New Jersey, eastern Pennsylvania and the West Virginia panhandle.  Our database of 2,893 freshwater gastropod records was developed from the collections of the US National Museum, the Academy of Natural Sciences of Drexel University, the Carnegie Museum of Natural History, and the Delaware Museum of Natural History, the macrobenthic surveys of the Maryland DNR (Annapolis), the Pennsylvania DEP (Harrisburg), and the Delaware DNREC (Dover), and our own original fieldwork.  The new website features a dichotomous key and a photo gallery for all 41 species recovered from the five-state area, as well as range maps and notes regarding their ecology, life history, taxonomy and systematics.

Also new for 2013 is a page entitled “Synthesis,” which can be visited directly here:

• http://www.fwgna.org/fwgnasynthesis.html

In this analysis we combine our 2,893 Mid-Atlantic records with 8,568 data from Virginia, North Carolina, South Carolina and Georgia to generate a distribution of commonness and rarity over the entire 67-species Atlantic drainage freshwater gastropod fauna.   We suggest a new (nonparametric) system of “incidence ranks” as a supplement to, if not necessarily a replacement for, the subjective system of “conservation status ranks” currently in vogue with natural resource agencies [1].

All reference to conservation as a motivation or intent has now been removed from the FWGNA website, insofar as possible.  Henceforth the Freshwater Gastropods of North America project will restrict itself to science.

Notes

[1]  This is an expansion and refinement of the approach I first suggested for the 57 species of freshwater gastropods in:

• Toward the Scientific Ranking of Conservation Status - Part II [9Jan12]

Plagiarism, Paul Johnson, and The American Fisheries Society

Editor's Notes.  About halfway through this essay I am going to assume that you have previously read last month’s post, regarding Delaware and the nonprofit organization NatureServe.  If you have not already done so, please take a minute to back up to [19Aug13], and then read forward.

This essay was subsequently published as: Dillon, R.T., Jr. (2019d) Plagiarism, Paul Johnson, and The American Fisheries Society.  Pp 243 - 249 in The Freshwater Gastropods of North America Volume 4, Essays on Ecology and Biogeography.  FWGNA Press, Charleston.

My first impression of Dr. Paul D. Johnson was that of a “hard-charger.”  It was November of 1998, and I had been invited to Chattanooga to join a committee primarily composed of natural resource managers, fresh from organizing two successful meetings on unionid mussel conservation in the Midwest, interested in expanding their portfolio to include freshwater gastropods and going national.  That weekend we drafted a constitution for The Freshwater Mollusk Conservation Society and made plans for a first general meeting, to be hosted by Dr. Johnson in Chattanooga four months later.  I was pleased to accept the chairmanship of the FMCS Gastropod Committee that Saturday afternoon in November.  And I was honored to nominate Dr. Johnson to the office of President-elect of the entire society in March, from which he ascended to the presidency in 2000.

Even as early as 1998, Dr. Johnson was advocating a “national strategy” for the conservation of freshwater gastropods, to be modeled after a mussel strategy then nearing completion by the group.  This project would involve the development of a list of North American freshwater gastropods prioritized for conservation purposes.  And of course, Dr. Johnson envisioned that such a list would arise from a collaborative effort, presumably coordinated by the FMCS Gastropod Committee. 

Although I was not opposed to the idea (15 years ago), it was my strong opinion that our committee’s first order of business ought to be a comprehensive survey of the continental freshwater gastropod fauna, only after which conservation priorities might be assigned.  I have also developed moral scruples regarding the admixture of science, politics, and public policy, which have deepened in recent years, but no point in going down that road here [1].

In any case, I declined to become involved with Dr. Johnson’s “national strategy,” passing the chairmanship of the FMCS Gastropod Committee to him in 2002.   The effort seems to have subsequently shifted home, from the FMCS to the American Fisheries Society Endangered Species Committee, which has in recent years become a center for such work on the aquatic biota in general.  I have remained on the sidelines, hoping for the best while fearing the worst.  And in June, alas, my worst fears were realized.

In June Dr. Johnson and 13 of our friends and colleagues published a feature article in Fisheries, the peer-reviewed journal of the American Fisheries Society.  It is entitled, “Conservation status of freshwater gastropods of Canada and the United States” [2].

Although the paper extends to 36 journal pages, details regarding the development of the data upon which the Johnson/AFS recommendations of “conservation status” were based are extremely vague.  Here is the single relevant sentence from the methods section, quoted in its entirety:  “Species occurrences within provincial and state boundaries were generated using primary literature, including provincial and state checklists where available, as well as personal communications with professional who are knowledgeable about certain groups or regions.”

Now I have some very, very bad news to report.  If you open a new window in your browser today (9Sept13), go to the USGS website hosting the Johnson/AFS database, and execute a map query for Delaware, you will find almost exactly the same list of 8 species you received from your identical query of the NatureServe Explorer database last month.

This is a peculiar list.  Missing from it are the four most common gastropod species actually inhabiting the freshwaters of Delaware: Physa acuta (aka P. heterostropha), Menetus dilatatus, Ferrissia fragilis, and Lymnaea (Pseudosuccinea) columella.  All four of these species are very nearly cosmopolitan in their distribution throughout eastern North America, and simple reference to the collections of either the DMNH or the ANSP would have returned numerous Delaware records for most of them.

The Johnson/AFS report also includes one species that our extensive field surveys of Delaware and attendant reviews of systematic collections have failed to uncover, Physa gyrina.  Populations of Physa gyrina do inhabit Ridley Creek in Delaware County, southeastern Pennsylvania, so on first reading it certainly seems possible that the Johnson/AFS record might be bona fide.  Or might this record represent a misidentification of Physa acuta?  The DMNH collection does hold a single undated lot of P. acuta (locality just “Wilmington”) misidentified as P. gyrina.

On 3Aug13 I sent an email inquiry to Dr. Johnson, asking if he could provide a reference to the primary literature or any other source available to him supporting his report of P. gyrina in Delaware, with 12 of his coauthors on the CC line.  Dr. Johnson has not favored me with the courtesy of a reply [3].

The match between the Johnson/AFS database and the NatureServe database is simply too close to be coincidental.  But at no point in his paper does Dr. Johnson acknowledge NatureServe as the origin of his primary data – not in methods, results, or acknowledgments.  The NatureServe organization is mentioned only on pages 250, 252 and 263 with regard to its system of conservation ranking, and cited only with respect to conservation ranking in the reference section.  The Johnson paper does not include a citation to the NatureServe Explorer as explicitly required by NatureServe for the fair use of its data.

The match is not perfect.  The exotic Bellamya (“Cipangopaludina”) chinensis was deleted from the Johnson/AFS Delaware list, and Helisoma (Planorbella) trivolvis added, indeed #11 on the confirmed list soon to appear on the FWGNA website.  The generic nomina of Physa gyrina and Fossaria obrussa have been emended to Physella and Galba.

But the evidence of plagiarism is pervasive.  My thirty years of experience grading the genetics lab reports of lazy college sophomores have (alas!) given me way too much practice identifying the phenomenon [4].  I have footnoted analyses of the situations in West Virginia [5] and New Jersey [6] below.  If these examples do not constitute sufficient evidence to convince my readership that the extensive data table reproduced in the appendix of the paper by Johnson and his colleagues did not originate from the NatureServe Explorer, tell me how many more such examples are necessary, and I will supply them.

Dr. Paul D. Johnson and his 13 colleagues stole a crappy, spurious dataset off the internet, tweaked it to the point they thought nobody would catch them, put their names on it, and transferred it into the peer-reviewed literature without attribution.  Shame on everybody involved: Arthur E. Bogan, Kenneth M. Brown, Noel M. Burkhead, James R. Cordeiro, Jeffrey T. Garner, Paul D. Hartfield, Dwayne A. W. Lepitzki, Gerry L. Mackie, Eva Pip, Thomas A. Tarpley, Jeremy S. Tiemann, Nathan V. Whelan and Ellen E. Strong.  Your mothers taught you all better.

And both the American Fisheries Society and the USGS Southeast Ecological Science Center are now accessories to egregious plagiarism.  The Johnson paper must be retracted, with apologies to NatureServe and to the scientific community at large.

Because the damage extends beyond that done to the professional reputations of Paul Johnson and his 13 collaborators.  The greatest damage is that done to science.  For what was merely the conventional ignorance of the worldwide web has now been transformed, by its publication in what appears to be a reputable journal, into ignorance of a high and aggravated nature, disgorged by 14 professionals whose credentials would lead one to expect some minimum level of scientific rigor, wrongly.  And perhaps a bit of integrity, for a change.

Postscript – On the date this essay was posted I mailed a formal letter to Dr. John Boreman, the President of the AFS, accusing Dr. Johnson and his 13 coauthors of plagiarism.  Dr. Boreman then tasked Mr. Jeff Schaeffer, the chief science editor of Fisheries, to conduct an individual review.  And 11 days later, I received a letter from Mr. Schaeffer finding that my “letter of complaint and supporting information from the blog do not meet” the standard of plagiarism.  I do not know what testimony the 14 authors of the Johnson paper might have offered on their own behalf.  I myself was not interviewed.

Notes

[1]  The language, culture, and values of science are not incompatible with those of law, politics and public policy, but they are not compatible either.  And over the years it has become clearer to me that much damage is done by workers with either worldview when we try to force a fit with the other, directly analogous to the damage done when a false compatibility is forced between public policy and religion, or science and religion, for that matter.  See any of my essays labeled “Worldview Collision” at right for more.

[2] Johnson, P. D., A. E. Bogan, K. M. Brown, N. M. Burkhead, J. R. Cordeiro, J. T. Garner, P. D. Hartfield, D. A. W. Lepitzki, G. L. Mackie, E. Pip, T. A. Tarpley, J. S. Tiemann, N. V. Whelan & E. E. Strong (2013)  Conservation status of freshwater gastropods of Canada and the United States.  Fisheries 38: 247 – 282.

[3] The complete correspondence record is as follows.  On 2July13 I sent an email to Dr. Johnson inquiring if he might be willing to share his database of occurrences with me, and asking for additional detail on the method by which these data were converted to conservation status recommendations.  Twelve (of his 13) coauthors were on the CC line.  (I have been unable to find an email address for Tarpley.)  I received no reply from any of the 13 recipients.  On 3Aug13 I sent a second email to Dr. Johnson, again with 12 coauthors on the CC line, simply requesting information regarding the occurrence of Physa gyrina in Delaware.  I received one fragmentary reply from Mr. Jay Cordeiro, who abruptly broke off our correspondence when I asked for clarification.  And I have heard nothing since.

[4] The sad science of plagiarism detection focuses on the “shared bonehead error,” or SBE.  If student #2 copies the errorless lab report of student #1, he will not be caught.  If student #2 copies a lab report, finds errors and fixes them, he will not be caught.  In fact, if student #2 copies a lab report containing reasonable errors, for example “three squared equals six,” he will not be caught.  The key to detecting plagiarism is the situation where student #2 copies a bonehead error, for example “three squared equals seven.”  Such “shared bonehead errors” are like fingerprints.

[5] NatureServe’s West Virginia list includes 28 species.  To this list Johnson/AFS added nine nomina – five valid species and four junior synonyms.  But there are two SBE omissions on both lists: Lyogyrus granum and Physa (“Physella”) gyrina.  This despite the fact that reference to the ANSP collection online would return 1 West Virginia lot of the former and 6 lots of the latter.

[6] NatureServe’s New Jersey list includes 22 species, three of which are exotic or introduced, reducing the list to just 19.  To these 19 Johnson/AFS added ten nomina – nine of which are specifically valid.  But again there is one SBE omission [7] on both lists: Helisoma (Planorbella) campanulatum, of which the ANSP collection online holds 15 New Jersey lots.

[7] There is also at least one glaring “shared reasonable error” on the two New Jersey lists.  Neither includes Ferrissia fragilis, which is #8 most common of the 30 species (no not 22, no not 28) soon to be documented on our Freshwater Gastropods of the Mid-Atlantic website.  This omission does not qualify as a “shared bonehead error,” however, because no national collection (to my knowledge) actually holds a single New Jersey record of F. fragilis.  The ANSP does hold 8 lots of F. fragilis from New Jersey, but five are curated as “Ferrissia sp.” in their online database, and three are misidentified as Ferrissia rivularis.  Thus the absence of F. fragilis from the New Jersey tabulation of Johnson/AFS does not constitute evidence of plagiarism.  It is a glaring example of that simple, conventional ignorance which we all ought to be working to fix, together.

Delaware, and what we think we know, that we do not

Editor’s Note. This essay was subsequently published as: Dillon, R.T., Jr. (2019d) Delaware, And What We Think We Know, That We Do Not.  Pp 235 - 241 in The Freshwater Gastropods of North America Volume 4, Essays on Ecology and Biogeography.  FWGNA Press, Charleston.

Delaware, our first state, is surprisingly diverse.  Its Piedmont north is primarily industrial and urban, but there are some lovely (and surprisingly rich) rocky streams tumbling across the low fall line.  Large, prosperous farms dominate the sandy coastal plain of the south, where I was personally startled to find blackwater swamps, dominated by bald cypress.  And with the Delaware Museum of Natural History in Wilmington, the Academy of Natural Sciences 20 miles north in Philadelphia and the National Museum of Natural History 70 miles east in Washington, the state of Delaware is cradled in the greatest concentration of malacological talent in the USA, if not the world.

Should we be surprised to learn that Delaware has never seen a survey of its freshwater gastropod fauna?  Or that the systematic collections of the DMNH, the ANSP and the USNM hold but 151 lots of freshwater gastropods collected in The First State combined, under 31 nomina, 11 of which are misidentifications or junior synonyms?  It seems likely to me that this situation arises from some sort of “neglected backyard effect,” our North American imaginations so transfixed by the Brazilian Amazon and the Black Smokers of the Abyss that we tend to overlook the little creeks running through our own city parks back home.

I am now pleased to report that a remedy is at hand.  In coming months the FWGNA project will roll out a new website entitled, “The Freshwater Gastropods of the Mid-Atlantic States” which will include surveys of Delaware, Maryland, New Jersey, eastern Pennsylvania, and the West Virginia panhandle.  Our extensive original collections, sampled from approximately 144 sites spread down the 100 mile length and across the 30 mile breadth of The First State, will confirm that a fairly reliable estimate for the number of gastropod species inhabiting the freshwaters of Delaware is indeed 20, as might have been predicted from the meager museum records available.

We will be sharing much more detail about the freshwater gastropods of all the Mid-Atlantic states in the coming months.  My focus for the remainder of this essay is not on what we now know, but on what we thought we knew, that we did not.

I am not a fan of the nonprofit environmental group called, “NatureServe,” or its online database “Explorer.”  But if you were to open a new window in your web browser today (19Aug13), go to www.natureserve.org, hit that “Explorer” button on the right panel, and execute a query for freshwater snails AND Delaware, the search engine will return a list of just eight species.

This is a peculiar list.  Missing from it are the four most common gastropod species actually inhabiting the freshwaters of Delaware: Physa acuta (aka P. heterostropha), Menetus dilatatus, Ferrissia fragilis, and Lymnaea (Pseudosuccinea)columella.  All four of these species are very nearly cosmopolitan in their distribution throughout eastern North America, and simple reference to the collections of either the DMNH or the ANSP would have returned numerous Delaware records for most of them.

The NatureServe report will also include one species that our extensive field surveys of Delaware and attendant reviews of systematic collections have failed to uncover, Physa gyrina.  Populations of Physa gyrina do inhabit Ridley Creek in Delaware County, southeastern Pennsylvania, so on first reading it certainly seems possible that the NatureServe record might be bona fide.  Or might this record represent a misidentification of Physa acuta?  The DMNH collection does hold a single undated lot of P. acuta (locality just “Wilmington”) misidentified as P. gyrina.

On 28July13 I sent an email inquiry to Dr. Bruce Young, Director of “Species Science” for NatureServe, asking if he could provide a reference supporting his report of P. gyrina in Delaware.  Dr. Young replied the next day, apologizing that “for common species we do not tie specific records to individual references or museum collections.”  Ms. Margaret Ormes of NatureServe followed up with “I just looked at our database and my best guess is that it was added (as Physella gyrina) based on Burch (1989).” [1]

I do appreciate the courtesy of the NatureServe staff, but the facts are very plain and very ugly.  The mission of NatureServe is advocacy, not science, and Physa gyrina is a trash snail, and they do not care whether arbitrarily-chosen trash snails actually inhabit arbitrarily-chosen states.  The NatureServe Explorer database is a smokescreen and a ruse, designed to lend false scientific credibility to a political agenda.

Science is the construction of testable models about the natural world.  Such models need not necessarily be accurate, nor even based on reliable data.  I am not fussing here about the discrepancy between the NatureServe estimate of 8 freshwater gastropod species in Delaware, and the FWGNA estimate of 20.  Nor am I fussing about the basis of the NatureServe estimate, which is spurious.

Science will fix these things, eventually.  There are scientists who will drive 16,139 miles in a 1992 Nissan pickup, camp in the rain, and eat Dinty Moore beef stew for a week to not find Physa gyrina in Delaware.  There are scientists who will dump three years of unsorted DNREC-DWR macrobenthic samples into little Petrie dishes and squint through microscopes for hours to not find Physa gyrina in Delaware.  There are scientists who will sleep five nights on an air mattress in Alexandria to ride the orange line downtown to pull every drawer of physids out of the US National Museum to not find Physa gyrina in Delaware.  Science ultimately fixes carelessness, sloppiness, and neglect.

No, the worst thing about the Explorer database is not that it is wrong, but that it reinforces conventional ignorance, and in so doing works against the cause we all seek to advance.  Fresh young students, casting about for research ideas, will tend to assume that the freshwater gastropod fauna of North America is in some sense “known,” and divert their energies elsewhere.  A proposal to the NSF Biotic Surveys and Inventories Program will be reviewed more favorably if it is directed toward the Ubangi River than to the Nanticoke, even though the freshwater gastropod fauna of the Ubangi is better documented [2].  Reinforcement of conventional ignorance is not the main problem I have with the NatureServe organization [3], but it is certainly in the top ten.

How big is your budget, Dr. Young, and how large is your staff?  The FWGNA project has now surveyed all or part of ten states.  This we have done with no more than $5K in grant support total, over 15 years.  Those 16,139 miles we drove in 2012-13 were unreimbursed.  We have paid $49/night out of our own pockets to sleep on air mattresses in Alexandria.  We bought our own Dinty Moore.

I will end this essay, however, on a note of hope.  Despite the layers of pseudoscientific hoo-hah in which NatureServe cloaks its Explorer website, it remains just a website, run by a political advocacy group.  And (how many times must we warn our students?) the internet is a wild and woolly marketplace of information, both the good and the bad, and the buyer must beware.  Each report returned by the NatureServe Explorer comes with the following disclaimer: “All documents provided by this server are provided “as is” without warranty as to the currentness, completeness, or accuracy of any specific data.”  In the final analysis, the Explorer database is not peer-reviewed science, and it does not pretend to be.

Thank heaven no legitimate researcher would ever confuse spurious data made available from the website of an advocacy group with reliable science.  Thank heaven.

Notes

[1] Yes, it does seem plausible to me that the initial state-by-state freshwater gastropod distributions uploaded to the NatureServe Explorer may have been the work of some intern hired to extrapolate the broad ranges found in J. B. Burch’s North American Freshwater Snails.  Burch lists 15 subspecies of P. gyrina, the ranges of at least two of which certainly include Delaware.  The range of Physella gyrina aurea is given as “New Jersey to Kansas, south to Arkansas and Florida,” and that of Physella gyrina cylindrica is given as “Ontario and New York south to Virginia.”  Then did our young intern simply miss Delaware when extrapolating “New England to Ohio, Tennessee and the Virginias” for P. heterostropha?  And did that intern miss Delaware when extrapolating “Eastern United States, from Maine west to Iowa, south to Texas and Florida” for Menetus (Micromenetus) dilatatus?  And so forth?  The entire enterprise is a house of cards.

[2] Brown, D. S. (1994)  Freshwater Snails of Africa and their Medical Importance (Second Edition).  Taylor & Francis, London.  608 pp.

[3] My main problem with NatureServe is the pseudoscientific method by which they gin up “conservation status ranks.”  See:

• Toward the Scientific Ranking of Conservation Status [12Dec11]