Wednesday, November 11, 2015

Untangling the Viny Viornas: A Case of How We've Underestimated Biodiversity in Architecturally Complex Genera (Part 2 of 2)

In the first part of this series, I laid the groundwork for how architecturally complex plant groups can be difficult to study. Perhaps no group better exemplifies this than the viny viornas or leatherflowers of the genus ClematisLeatherflowers are herbaceous vines that grow up to about 9 ft in length. They generally trail over surrounding vegetation or climb shrubs. Their architectural complexity stems from various floral and vegetative characteristics. Clematis is represented by more than 400 species globally. Since the 1940s between 8 and 12 species have been recognized in the eastern U.S. by taxonomists. Ralph Erickson in his treatment of the viornas recognized 12 species, whereas W. Michael Dennis recognized 8 species in his PhD dissertation which focused on the biosystematics of the group.

I first became interested in Clematis in 2003 during the first year of my PhD program at the University of Tennessee. Even though I lived in Knoxville, I regularly traveled back to central Tennessee to collect specimens. One late spring day I traveled from Knoxville to collect plants in the Nashville area along the Cumberland River. During this collection trip I happened to collect Clematis viorna from moist forested slopes in Jackson Co., TN in the upper Cumberland River Valley. The flowers were bright, cherry red on the outside with a cream interior and most parts of the plant were relatively smooth. The sepals were weakly corrugated along the back. The flower stalks (peduncles) were longer and the bract leaves were larger. The leaves of these plants were biternately compound. Later that same trip, and about 75 miles to the west, I collected another Clematis that also keyed to C. viorna, but was clearly very different when examined side by side. These plants from dry rocky wooded slopes adjacent to limestone cliffs in Cheatham Co., Tennessee had pale-lavender flowers fading to cream sepal tips, sepals grooved on the back, a different leaf dissection, and were soft-hairy on leaves, stems, and flowers. I thought to myself, how can these two collections represent the same species? Examine Fig. 1 and ask yourself the same question!

Fig. 1. The red star indicates the location of specimens of C. viorna collected in Jackson Co., TN (plants in upper right with bright reddish flowers. The blue star indicates the location of specimens of C. viorna collected in Cheatham Co., TN (plants in upper left). Both were collected along the Cumberland River and both key to C. viorna in most keys. The bold green line represents an important geographic break within eastern North America. Many primarily Appalachian species do not occur west of this line and many "western" species rarely occur east of this line. 

So after careful observation in the field and much thought on the subject, I did what any taxonomic botanist would do. I went back to the University of Tennessee Herbarium to examine specimens and to dig into the taxonomic literature to see what previous Clematis experts (Ralph Erickson, Mike Dennis, and Jim Pringle) had to say about variation in Clematis viorna

Features that seemed so clearly distinct in the field such as flower color, grooving of the sepals, leaf dissection, pubescence, and position of the leafy bracts on the flower stalks, all seemed to "break down" upon initial inspection of  all of the C. viorna specimens at UT (see Figs 2-3). Flower color and sepal grooves were impossible to tell because of discoloration of the flower and distortion (through flattening and shrinking) of the sepals upon drying. Leaf dissection was challenging because some collectors collected only the distal-most stem section whereas others collected from mid-stem sections, or in other cases leaves were so poorly pressed that they were sometimes folded and their original dissection pattern was impossible to discern. Thus, leaf pubescence and bract position were the only really "useful" features that could be used when examining most herbarium specimens.  

Fig. 2. This specimen illustrates some of the difficulties of working with Clematis in the herbarium. This specimen is poorly pressed with overlapping leaves and stems and folded leaflets. Compare this specimen with Figure 3 below.
Fig. 3. This is the same species as shown in Fig. 2 but note that the critical features needed for identification are shown, including the dissection pattern of the leaves and the general features of the flowers, their peduncles, and bracts. Collectors of Clematis are encouraged to press specimens with such characters in mind.

Some general patterns seemed to hold when I examined leaf pubescence in Clematis viorna. Most specimens could be separated into a relatively smooth "Appalachian" type and a pubescent "Interior" type. The "Appalachian" type seemed restricted to the Appalachian Mountains, Piedmont, and Atlantic Coastal Plain from northern Georgia and east Tennessee north into southeastern Ohio and Virginia. The "Interior" type seemed to be the main type west of the Appalachian Plateaus (Cumberland and Allegheny) west to the Ozarks and ranging north-south from southern Indiana to central Alabama.   

What was troubling to me was how could these plants be so distinct in the field and then seem to break down in the herbarium? Using hairiness as one criterion to sort specimens, I was intrigued by populations within the Appalachian zone that were quite hairy like "Interior" populations. These isolated "Interior" populations stranded in Appalachia popped up in interesting places like in east Tennessee and southwestern Virginia in the Ridge and Valley Province, near Shenandoah National Park in Virginia's Blue Ridge Mountains, and in the Ocoee River Gorge of  Tennessee's southern Blue Ridge. I only had one or two specimens of each of these outlier "Interior-like" plants to examine so I chalked them up as aberrant individuals and was left scratching my noggin.

Not wanting to get entangled in a leatherflower thicket, I decided to put the problem aside for another day given that I had an actual PhD dissertation to finish -- oh yeah that. Years went by and I had the occasion to study additional specimens from time to time, once during a Christmas break trip to the Missouri Botanical Garden in St. Louis, another when I pulled an all-nighter at the University of Alabama Herbarium on my way to Panama City with the family, and many other trips to eastern U.S. herbaria, including small ones like Stephen F. Austin State University in Texas and the famed Gray Herbarium at Harvard.

During my time in grad school, I added my own contributions to other aspects of Clematis taxonomy by describing a new species from the Carrizo Sands of east Texas, which I named Clematis carrizoensis in 2006. My friend and colleague, Chris Fleming and I also discovered Clematis morefieldii, a federally endangered species, new to Tennessee. 

Fast-forward a few years to 2009 and I again stumbled into the Clematis problem. My good friend and colleague Theo Witsell, botanist for the Arkansas Natural Heritage Program in Little Rock (who I affectionately refer to as my "red-headed brother from another mother from across the Big River"), sent me some specimens to examine (which I still have on loan!). In that batch were specimens of an unusual Clematis from the Arkansas River Valley and adjacent Ouachita Mountains. These specimens resembled those of the "Appalachian" type described earlier in having biternately dissected leaves, long peduncles, and in being relatively smooth. However, they possessed a suite of additional characters which readily distinguished them, including narrowly cylindric flowers, flowers that were light pinkish-purple fading to cream tips, and peduncle bracts that were generally lobed or divided into three leaflets (ternate). My botanical buddy and botanist extraordinaire, Aaron Floden, and I decided to take a trip out to visit the Arkansas populations with Theo and our feelings that it was a distinct undescribed species were strengthened. In the herbarium these Arkansas plants had been identified one of two ways. Some botanists identified them as Clematis viorna -- the name I considered to be the "Appalachian" type with cherry-red flowers. Others called these plants Clematis reticulata, even though they scarcely had reticulate leaves.

For the first time it occurred to me that part of the problem with studying Clematis is that most people had previously relied on herbarium specimens. This makes sense given that a researcher can borrow thousands of specimens from dozens of herbaria and within a few weeks can study a large percentage of specimens ever collected for a particular species. These specimens span nearly two centuries and represent the individual collections of dozens of collectors from potentially hundreds of counties and dozens of states. It would be impractical, likely impossible, for a single researcher to try and see most of these populations live in the field. Just think of how costly such a trip would be with all the expenses of fuel, food, hotel or camping fees, automobile repairs, etc. The ideal taxonomic study should involve extensive herbarium study and ample amount of fieldwork. Usually study of herbarium specimens reveals variation and a researcher can then navigate to those populations to study them live, make photographs, collect tissue samples, and collect material for common garden studies.

Through my experience with examining thousands of herbarium specimens and observing populations from across the Southeast I realized there had to be more to the story given all of the variation in morphology. I decided to dig deeper for clues and again I turned my attention back to herbarium specimens to see what could be leading folks (including me!) astray. Specifically, I wanted to search for specimens that troubled previous botanists. While examining specimens from the University of Arkansas Herbarium with Theo we found what I had been looking for, only it opened the door to a whole new way of thinking. What if taxonomists have been greatly underestimating the number of Southeastern species of Clematis? 

The specimen that led me to ask this question is shown in Figs. 4-5. When this specimen was first collected in 1955 its collector did not identify it to species. Eleven years later, E.B. Smith annotated the specimen as Clematis versicolor. Ten years after that, W. Michael Dennis determined the specimen to be C. reticulata. In 1988, Smith returned with a second annotation and considered the specimen to be C. reticulata introgressed with C. viornaWhy did this specimen receive so many conflicting annotations? What led these experts to label this specimen with three different species names?

Fig. 4. Specimen of Clematis sp. nov. (Ouachita Leatherflower) from the University of Arkansas Herbarium, illustrating the hallmark of undescribed species represented in herbaria.
Fig. 5. Note the lack of lack of a consensus among
experts as reflected by the conflicting annotations
for this specimen.

I said to Theo, "what if there are several undescribed and narrowly endemic species of Clematis from different regions across the Southeast that have clouded our thinking?" Perhaps all along I and other botanists have had trouble with Clematis because we were discounting the potential that much of what we have been looking at in herbaria could be undescribed.  Have we been trying to  "pigeonhole"  undescribed species into known species?

Specimens such as this one tell a story. They can be indicators of undescribed species. They bear conflicting annotations which point to a lack of consensus among original collectors and regional or taxonomic experts. I have seen such specimens in other taxonomic groups and they have frequently been annotated as possible hybrids, just as this specimen was labeled as C. reticulata "contaminated with" C. viorna

According to my own research, this specimen represents an undescribed species. So why did it take until now to realize its distinctiveness? Furthermore, why were past botanists so quick to invoke the hybrid scenario first? Why not simply put a note stating that the specimen does not fit well within either C. reticulata or C. viorna? Or, why not annotate it in any number of other ways, such as calling it Clematis aff. reticulata or Clematis cf. reticulata. It seems that in some groups some botanists are all too quick to jump to the conclusion that an unusual plant is a hybrid, but I rarely see folks going to the other extreme and questioning from the start as to whether a specimen could represent a new species.

I'm not advocating that we should immediately assume that a plant that doesn't seem to fit a known species be considered an undescribed species at the onset. After all, it is a fairly rare event to encounter a new species. Just in the same manner as doctors are trained to first consider that a patient's ailments are due to some common cause, they must also be willing to consider that although against the odds a person could have some very rare condition. I have seen numerous cases where perfectly distinct species were initially regarded as mere aberrations, possible hybrids, or lumped away and considered to represent variation within a morphologically plastic species. This may have been done out of convenience for it often takes a lot of work to determine whether something is indeed a new species or not--as it should. 

It isn't clear why previous taxonomists didn't notice this new species but I suspect that there are probably three main reasons: 

  1. in the late 20th century I think that many botanists were reluctant to believe that some areas of the South could still harbor undescribed species, especially narrowly endemic taxa; 
  2. the fact that our collective knowledge of Southeastern phytogeographic patterns was still in a relatively elementary state in the 1970s-80s due to inadequate collecting in some areas and lack of published studies of biogeographic patterns of Southeastern plants, and 
  3. the fact that Clematis is an architecturally complicated genus that presents numerous difficulties to herbarium study.

First, I would contend that in some cases botanists think that everything has been discovered already or they are reluctant to believe that an unusual population could represent an undescribed species. For a great discussion on this topic see Barbara Ertter's publication Floristic surprises in North America north of Mexico. 

In the 1970s-80s, the Ouachita Mountains had not yet become known as a center of vascular plant endemism. However, since the 1970s numerous narrowly restricted species have been discovered in this ecoregion, including Amorpha ouachitensis (1975), Cardamine angustata var. ouachitana (1982), Carex ouachitana (1987), Polymnia cossatotensis (1989), Hydrophyllum brownei (1991), Sabatia arkansana (2005); several additional species remain undescribed (Theo Witsell, pers. comm.). The fact that this region is a burgeoning hotspot suggests that we should actively seek out potentially undescribed species from the Ouachitas that may be "hiding out" in herbaria. A 2010 publication by D.P. Webber and numerous coauthors titled "Herbaria are a major frontier for species discovery.", published in the Proceedings of the National Academy of Sciences, suggests that many undescribed species are hiding out in herbaria awaiting our discovery.  

Second, prior to the 2000s we did not have a very good handle on phytogeographic patterns of the Southeastern flora. Thanks to major botanical collectors such as Robert Kral, R. Dale Thomas, Delzie Demaree, Roland Harper, and E.J. Palmer, hundreds of thousands of plant specimens have been collected from all over the Southeast. Prior to the 1960s taxonomists had only a few specimens from each state to examine and there were significant gaps with many areas under-collected. This made it difficult to identify geographic distribution patterns, especially those involving narrowly endemic species. Fortunately as species distribution maps were published online (e.g. BONAP) our understanding of plant distribution patterns has advanced greatly. It is now much more widely accepted that we CAN and DO have species that are found in only one or two counties, but I think most taxonomists in the Southeast prior to the 1970-80s considered this unlikely, thus many restricted endemics were considered to be aberrant individuals or hybrids rather than distinct species. Of course there are exceptions. Botanists like J.K. Small recognized many narrowly restricted species. His work with the numerous endemics of Florida probably influenced his tendency to do so. Reed Rollins of Harvard University also is well-known for his work on the narrowly endemic species of Leavenworthia and Lesquerella, which harbor numerous narrowly restricted species including a couple that are single-county endemics. 

Detailed distribution maps like the one in Fig. 6 for Clematis reticulata available from BONAP were not available until recently. Such maps were compiled from specimen data available in dozens of herbaria. When Ralph Erickson was constructing his distribution map of C. reticulata in the 1940s many counties highlighted in the BONAP map below had no collections of C. reticulataWithout the intense collection of specimens during the latter half of the 20th century the many gaps in the range of the species that Erickson encountered would not have been filled. For example, look at the large gap in the range of C. reticulata that separates populations on the east and west sides of the Mississippi River. Phytogeographers now have enough data from many dozens of species (e.g. longleaf pine) that show that this is a very common gap. However, in the early 20th century the paucity of plant collections from many parts of the South made such patterns difficult to interpret whether a species was truly absent from a region or just under-collected. Such inadequate maps made it difficult to determine phytogeographic patterns. In another case, note the two central Texas counties that contain C. reticulata but that are separated from the other east Texas populations. Is this a real gap or would additional fieldwork likely fill this void?

Fig. 6. Distribution of Clematis reticulata according to BONAP (2015).

The lack of accurate distribution maps meant that we did not have a good concept of phytogeography until relatively recently. Robert Kral's two volume publication A Report on Some Rare, Threatened, or Endangered Forest-Related Vascular Plants of the South greatly advanced our knowledge of plant distribution patterns, especially of rare species. By the turn of the 21st century several published atlases of plant distribution patterns had been published. Various publications have focused on distribution patterns of Southeastern plants (phytogeographic patterns), including Bruce Sorrie and Alan Weakley's paper "Coastal Plain vascular plant endemics: phytogeographic patterns" and Doug Zollner et al.'s (2005) paper entitled "Endemic vascular plants of the Interior Highlands, USA."  

I believe that the third major reason for the underestimation of diversity in Clematis is due to their architectural complexity. They aren't like dandelions or other small plants where you can put the whole plant on a single herbarium sheet. Most are long vines, but specimens usually consist of a 10-16 inch section of the vine, and often the distal-most portion of the stem. As a result many potentially important characters are often not collected or documented such as mid-stem leaf dissection. Other features are quickly obliterated by pressing and drying, such as flower color and shape. Below, I discuss some of the characteristics of Clematis and the challenges they present to taxonomists.

The nature of the inflorescence in Clematis has been recognized as taxonomically important but still much confusion exists (Fig. 7). For example, Clematis morefieldii has axillary flowers that usually hang down below the leaves on very short pedicels and that are subtended by small hairy bracts. In contrast, C. viorna  has ascending peduncles that are usually quite long and subtended by two foliaceous and generally smooth bracts. Some botanists have been reluctant to accept C. morefieldii as a distinct species, presumably in part because of the numerous "intermediate" forms that exist between it and C. viorna. For example, populations currently considered to be C. viorna from west-central Alabama and eastern Mississippi and other populations in northern Arkansas are very much like C. morefieldii in their short peduncles. Peduncle length and bract size do vary, particularly with respect to developmental stage. Some species, like C. viorna, tend to have shorter peduncles with smaller bracts earlier in the season at the tip of the stem. Those developing later and farther down on the stem tend to have longer peduncles and larger bracts. With continued development, additional flowers and bracts may develop. Even with this variation on a single plant, the flowers and inflorescences of each entity seems to be constrained  within a certain range.

Fig. 7. Plate showing inflorescence structures of various Clematis. The image at the far left is of Clematis morefieldii. The image at far right is of typical C. viorna. The four center images are various populations currently identified as C. viorna. Note differences in peduncle length, peduncle orientation (ascending vs. descending), bract size, and bract position.

The flowers of Clematis resemble small bells (Fig. 8). Unfortunately, floral characters do not preserve well on herbarium specimens. As a result, important features such as flower shape have largely been ignored by taxonomists. Some species (e.g. C. glaucophylla) have narrowly urn-shaped flowers whereas others are broadly egg-shaped in outline (e.g. C. morefieldii). In some species, the tips of the sepals recurve prominently (e.g. C. viorna) but in other species the tips remain straight and do not recurve (e.g. C. glaucophylla). Another feature that seems to be useful for discriminating taxa is whether or not the backs of the sepals are ridged or smooth. Clematis viorna and C. carrizoensis are examples of species with smooth unfurrowed sepal backs whereas C. reticulata and C. flaccida are prominently grooved. Finally, some species, like C. crispa and C. pitcheri, have sepals with thin, wavy (crispate) margins whereas others lack such a dilated margin.

Fig. 8. This plate shows how fresh flowers can yield potentially taxonomically significant characters that are obliterated during pressing and drying. The column to the far left represents Clematis morefieldii which prior to 1987 was considered part of C. viorna. The three remaining columns are all from populations currently identified as C. viorna. Note the major differences in flower shape, degree of sepal reflexion, sepal tip length, flower color, degree of sepal corrugation, and sepal width.

The general color of Clematis flowers is very important taxonomically (Fig. 9). Some species such as C. texensis, C. carrizoensis, C. versicolor, and C. glaucophylla can only be reliably distinguished by flower color.  Flower color varies with time of flowering and ecological conditions. Plants in full sun typically have lighter colored flowers than those in shade. Distribution of color is also important. Some species have sepal backs that are monochromatic or have one color from base to apex. This is the case in C. texensis, which is scarlet throughout. Other species like Clematis versicolor are bicolored, with darker coloration near the base and becoming lighter toward the tip.  The coloration of the inside of the flower can also be important taxonomically. Some species, such as C. vinacea have sepals with the same color on both the outside and inside surfaces. Others, like C. viorna are dark outside and cream-colored inside.  Most species have a fairly wide range of color variation even within a population or on a single plant, as illustrated in different flower colors on a single vine in a population of C. subreticulata from Mt. Cheaha, Alabama. In spite of the variability of flower color within a species, each species generally has its own particular color range. 
Fig. 9. This figure shows the difference between two plants that were formerly both treated as a single species, Clematis viorna. The two images on the left represent typical C. viorna. Notice the distinct cherry-red exterior and creamy-yellow interior. The two photos on the right represent the recently described C. vinacea. Note this species has flowers with the same color on the exterior as the interior. Also note the difference in sepal pubescence.

Typically, herbarium specimens of Clematis only include the terminal section of the vine, usually the last 8-15 inches or so. Unfortunately, such specimens rarely show mid- and lower stem leaves, which often are larger and more dissected. Most of the viornas have leaves that are compound. The leaflets are not always attached in a single plane to the main rachis, rather they often attach at an angle and are held in a different plane than the axis. Pressing specimens obscures this aspect of leaf morphology. The degree and type of leaf dissection is also important taxonomically (Fig. 10), though such characters have been used rarely to separate species. Some species typically have mid- and upper stem leaves that are pinnately compound and the leaflets often lack lobes (e.g. C. morefieldii) wheras other species are often biternately compound throughout (C. viorna). Careful observation of the variation in leaf dissection should be made on a single plant and across the population.

Fig. 10. Both of these leaves are from plants that would key to Clematis viorna in nearly all plant identification manuals. The specimen on the right represents true C. viorna from the Appalachian region whereas the photo on the left is from an undescribed species in the Arkansas Ozarks.

Past taxonomists have used degree of leaf vein reticulation to distinguish some species of Clematis. This refers to whether or not the veins are raised above the surface of the leaf blade forming a net-like reticulum as opposed to the veins being flush with the leaf surface or embedded in the leaf tissue. Herbarium specimens rarely capture the full range of venation for a population. Plants growing in shade tend to have less reticulate veins and the leaves are often thin or flaccid whereas plants in full sun can have strongly reticulate-veined and thicker leaves. For example, vegetative or fruiting specimens of Clematis versicolor in deep shade are nearly impossible to separate from specimens of C. glaucophylla, whereas sun plants are easy to distinguish based on leaf thickness and venation

Degree of leaf vein reticulation has been the primary character for separating Clematis viorna from C. reticulata (Fig. 11). The former is considered to have veins that are not raised above the surface of the leaf or with only the primary and secondary veins slightly raised whereas C. reticulata usually has primary, secondary, tertiary, and quaternary veins raised above the surface of the blade, forming a net-like reticulum. Like the C. versicolor-C. glaucophylla example above, shade vs. sun leaves complicates interpretation of this character. It is possible that degree of reticulation is due to clinal variation. Populations of C. reticulata in Florida, for example, have very thick and strongly reticulated leaves but as you go northward through Alabama populations of what have been called C. reticulata become thin-leaved and less strongly reticulate. 

Fig. 11. Graphic showing the range of leaf vein reticulation from non-reticulate leaves at the far left to strongly reticulate leaves at the far right.

Restoring Order to the Viornas

My recent research suggests there may be as many as 9-12 previously undescribed species of leather flowers in the Southeast (Figs. 12-13). All of these are being "carved out" of either Clematis viorna or C. reticulata, both previously considered widespread and variable species. Two species have already been separated in recent years, including Clematis morefieldii and C. vinacea, both split out of C. viorna from the Southern Appalachians.

Fig. 12. Overview of the Clematis viorna complex. Typical C. viorna is represented by the red circles with yellow border in the Appalachian region. The stars represent species already described (C. morefieldii = yellow star; C. vinacea = red stars). All other entities shown on this map represent putatively undescribed species.

Fig. 13. Overview of the Clematis reticulata complex. Typical C. reticulata is represented by the pink circles with black border in the southeastern U.S. Coastal Plain. Orange circles in Alabama and adjacent states represents the previously described Clematis subreticulata, a species that probably needs to be resurrected. All other entities represent undescribed species.

Nearly all of the new species to be recognized are diagnosed by a syndrome of morphological features but no single species can be separated by any one feature. The various taxonomically important features in Clematis such as leaf dissection, inflorescence type, flower color, bract size and placement, sepal grooving, pubescence, etc., all are recombined in various ways such that oftentimes each major ecoregion has its own distinctive Clematis.

In the third part to this series I will provide photographs and tentative range maps of all of the members of the C. viorna and C. reticulata groups to help guide botanists in the eastern U.S. in interpreting variation of the eastern North American leatherflowers.

Saturday, May 9, 2015

Is over-reliance of using herbarium specimens for taxonomic studies leading us to underestimate Southeastern plant diversity? Part 1 of 2.

Most of our current knowledge of Southeastern plant biodiversity comes from botanists who have worked on bits and pieces over the past 250 years. Prior to the early to mid-1800s most of the botanists dealing with the Southeastern flora, even the American flora for that matter, were Europeans who had never or only rarely set foot on American soil. Afterward, in the late 19th and up through the mid-20th centuries the majority of botanists working on the eastern U.S. flora were affiliated with "Northern" academic institutions like Columbia, Harvard, and Cornell universities. With a few notable exceptions, most of these botanists rarely traveled to the Southeast. This meant that they rarely got into the field to observe firsthand the South's exceptional biodiversity. Instead, botanists like Asa Gray, Merritt Fernald, and Arthur Cronquist mostly relied on dried, pressed herbarium specimens sent to them for study by Southern botanists who lacked the prestige and reputation of their Northern counterparts. In many cases, these Northern botanists would look at specimens sent to them that resembled species common in the Northern states and they would often identify the Southern example as being the same as the northern species - lumping them together.

One notable exception to the Northern lumping botanists was John Kunkell Small of Columbia University, who was affiliated with the New York Botanical Garden. Small studied the Southeastern flora extensively, especially that of Florida and adjacent states. Many of his Northern counterparts felt he was too "splitty" in his classification of Southern plants. After he published his Flora of the Southeastern U.S in 1933 it was only a matter of time before Northern botanists began to lump his Southern species into Northern ones, usually doing so at whim and without the backing of scientific evidence. Many of Small's species that he recognized in 1933, which were subsequently disregarded by many later botanists, are now being upheld by science as good species and are being resurrected.

The study of plant species, their characteristics, and how they are classified is known as plant taxonomy. It is usually cost prohibitive for botanists to drive around the country to study hundreds of populations of a particular group of plants just to determine whether the group is just one widespread species with lots of variation or whether the group consists of multiple similar but distinct species. Imagine with today's gas prices how much it would cost to study a species that has a range that covers most of the eastern U.S.! 

Approximate geographic distribution of Wild Ginger (Asarum 
canadense). The red, yellow, and blue polygons represent morpho-
logical extremes that some botanists have recognized as distinct 
species or varieties. The most recent consensus is that they
represent a single highly variable species whose morphological 
variability lacks geographic correlation. Most studies of wild ginger 
variation have relied heavily on examination of herbarium 
specimens and little on examination of living populations. 
Attempting to study live populations across such a vast range is 
difficult due to high travel costs. Map from Estes (unpubl. data).
So, since we can't afford to cover so much ground, like our botanical forefathers before us, we must rely heavily on the study of pressed, dried, plant specimens stored in museums called herbaria. To thoroughly understand the taxonomy of a particular group of plants may require examining thousands of specimens collected by dozens of botanists over hundreds of years and stored in many different herbaria. From the study of these specimens, we usually can identify a specimen to a given species. We can even use the specimens to ask questions about whether something that has always been called one species should be divided into two or more species. The scientific method can then be employed to answer these questions.

Botanists must be careful however not to rely too much on the study of herbarium specimens alone. For one, we are often only examining a part of a much larger plant that can't be pressed on a piece of herbarium paper that is typically 18 x 11.5 " long. For example, with trees we tend to press a section of a twig but we can't press the entire tree. Consequently there are features we miss. Other features like floral scent, bark texture, and colors may not preserve on herbarium specimens and they often aren't recorded by the botanists who collected them. Fortunately, herbarium specimens seem to allow most trees, shrubs, small herbs, ferns, grasses, sedges, and rushes to be studied and differentiated rather easily.

Some plant groups present great challenges to botanists who rely solely or primarily on herbarium specimens to interpret patterns of variation and species boundaries. For example, palm trees are difficult to study because their leaves and other parts are enormous and impossible to fit on a single herbarium specimen. 

Other plant groups are what I call "architecturally complex." These are groups that have complicated flower shapes or leaves whose potentially important taxonomic characters become destroyed upon pressing. For example, think about the complexity of most orchid flowers and imagine smashing that flower and drying it for days and then trying to compare the fine details of the smashed flower of your specimen to hundreds of other smashed flowers from other orchid collections. Preserving the flowers in some sort of liquid preservative would prevent destroying taxonomically important features but this is rarely done. 

Herbarium specimens of wild ginger showing variation in flower size and shape when pressed and dried. These flowers are  highly three-dimensional and their original dimensions, orientation, color, and scent are lost when pressed and dried. 

Blackberries are another architecturally complex group. They are difficult to study since no one likes to collect them because of their prickles and because they are hard to press. Typically one must cut a whole blackberry bush into numerous sections, pressing each section carefully. The stems may have certain growth patterns that can't be observed on a herbarium specimen, like whether they grow appressed to the ground or form an arching shrub. in order to really have a specimen worth studying later, nearly complete specimens are needed. Such complete collections typically don't exist in most herbaria. 

In the Southeastern flora there are many groups which are architecturally complex, including wild gingers (Asarum), jack-in-the-pulpit (Arisaema), various orchids, blackberries, pitcher plants (Sarracenia), and leather flowers (Clematis). This architectural complexity has made these groups difficult to study using herbarium specimens. Once their parts become smashed and dried the various species often look alike and differences that seem to exist when viewing living plants side-by-side in the field or garden seem to break down in the herbarium. This has led many botanists to do a lot of "lumping" in some of these groups. 

Wild ginger (Asarum canadense)  has been classically treated as a single widespread and variable species by most botanists. These two flowers were photographed in Maryland where two strikingly different morphological "forms" co-occurred in the same forest. Plants with flowers like those on the left have been treated as Asarum reflexum while those on the right are best treated as typical Asarum canadense. At this site the plants generally occupied different microhabitats with one occurring on a floodplain terrace and the other on adjacent toe slopes.

Photographs showing "architecturally complex" flowers of wild gingers. Recent research by Estes (unpubl. data) suggests that what we currently call one species (Asarum canadense) is best considered three distinct species, A. canadense, A. reflexum, and A. acuminatum. Reliance on herbarium specimens by many has led to lumping these three as one species in the past. Their distinctiveness is getting clearer but only after logging several thousand miles across eastern North America to study and examine living populations. Estes still needs to examine populations in portions of the Midwest and Great Lakes states to finish the study. 

Recently, evidence has been mounting that suggests relying too much on herbarium specimens for interpreting the taxonomy of architecturally complex plant groups may lead to a serious underestimation of biodiversity. As such we may be failing to protect critically endangered species that we don't realize exist. 

In the second part of this series, I will discuss how we have seriously underestimated biodiversity in the viny leather flowers of the southeastern U.S. and in doing so have overlooked nearly a dozen undescribed species.

Monday, January 5, 2015

Biodiversity Hotspots Hold the Key to New Species Discovery in the Southeast

New species are still being discovered with regularity. Nearly every week there are posts of newly discovered species on Facebook's Novataxa page of some recently found frog from the Congo or new plant from the Peruvian Amazon. The majority of new species are being discovered in remote tropical areas - places like Borneo, Laos, Brazil, and Madagascar -  that are still relatively understudied and have a considerable amount of unexplored territory. Most of these are from regions called global biodiversity hotspots. Worldwide, there are 35 global biodiversity hotspots recognized by Conservation International. Examples include the Atlantic forests of Brazil, the Caucasus Mountains of Eurasia, and the pine-oak woodlands of Mexico. For a region to be a hotspot it must meet strict criteria aside from just having a high number of species. First, It must contain at least 1,500 endemic plant species (endemic species are species restricted to an area that occur nowhere else). Secondly, at least 70% of the region must have suffered from habitat loss or significant degradation such that less than 30% of its original vegetation remains. These threatened hotspots support more than half of all known plant species and more than 40% of mammal, bird, reptile, and amphibian species, despite just making up 2.3% of the Earth's land surface (Conservation International 2015).

Fig. 1. Map of Global Biodiversity Hotspots

Smaller biodiversity hotspots can also occur on a regional scale. For example in the mountains of southwestern China - which is itself a global biodiversity hotspot - there are specific mountains or watersheds that harbor their own sets of narrow endemics that can be thought of as local or regional hotspots. 

A new paper by Reed Noss and colleagues, entitled How global biodiversity hotspots may go unrecognized: lessons from the North American Coastal Plain, published in 2014 proposes that the southeastern US, specifically the Coastal Plain province, which comprises approximately half of the area known to many as "The South," should be considered the 36th global biodiversity hotspot since it meets the criteria set by Conservation International. Within this newly proposed global biodiversity hotspot, there are also regional hotspots that were identified in 2001 by former University of Tennessee researchers, James Estill and Mitch Cruzan. Their study identified several "centers of endemism" within the South - particular regions that are biodiversity hotspots but on a small regional scale. Examples include the Appalachicola region of the Florida Panhandle, the Southern Appalachian Mountains, and the Central Basin of Tennessee. 

Their maps provide coarse resolution of hotspots and are a good start, but recent data suggests that there are small hotspots even within some of the ones Estill and Cruzan found. For example, the Southern Appalachians contains numerous hotspots of endemism, each likely to harbor undescribed species as well. There a few areas not identified as hotspots by Estill and Cruzan that may in fact be unidentified hotspots that need additional study. Such areas include the upper Cumberland River Valley of Tennessee and Kentucky and the Boston Mountains of Arkansas. 

Estill and Cruzan's (2001) map of southeastern U.S. "centers of endemism."
These can be thought of as biodiversity hotspots within the larger southeastern
U.S. global biodiversity hotspot proposed by Noss et al. (2014).

Given the Southeast's status as a global biodiversity hotspot, It should be no surprise that the region is still yielding many new species of plants and animals despite 350 years of intensive exploration and scientific study. Recent remarkable U.S. examples of new animals include the discovery of four new bass species from Alabama, a new turtle species in Mississippi, and a new giant crayfish in south-central Tennessee. Data compiled independently by Alan Weakley (Univ. of North Carolina, Chapel Hill) and myself reveals that there have been more than approximately 250 plant species described from the Southeast since 1970 and the rate of discovery continues to remain steady at an average of five per year. There may be a few hundred species left to describe from the Southeast.

Vascular plant species described in the southeastern U.S. between 1970-2010.

Now, perhaps more than ever, it is imperative that we find, describe, and study new species because what little remains of our natural habitat in the South is now faced with nearly constant threats stemming from increased population growth. The continued degradation of our Southern landscape has been especially obvious to members of the conservation communities who are now in their 80s and 90s. Dr. Robert Kral, retired Vanderbilt University botanist, relayed the erosion of our biodiversity to me in this way: "Dwayne, 18 out of every 20 sites I've visited over my career that were high quality sites are now gone or degraded beyond repair." Numerous factors are responsible for the degradation of our natural habitats including urban sprawl, habitat fragmentation, wetland destruction, conversion of woodlands to pine plantations, increased herbicide usage, fire suppression, and competition from invasive species. Coastal areas are also under threat from sea level rise due to global warming. The sad reality is that if we don't act fast many species will likely become extinct before we can ever describe them. Given these threats and the potentially great number of species left to find and describe, is there any way to expedite the discovery of the South's undescribed species?

The Race to Discover the South's Remaining Undesribed Species

I believe there is a way to speed up and focus our efforts to identify new species. First, we need to understand the likely characteristics of those species that are still out there. You might think of this as a sort of forensic profile. Here's a list of things to consider:

  1. A significant number of new species, perhaps 50-70%, are very rare and known only from a few populations - thus the reason they've escaped detection.
  2. A high percentage, perhaps 20-40%, are actually quite widespread and have escaped detection because they are cryptic or belong to groups that are taxonomically  or architecturally complex.
  3. Probably at least 75-90% of all species to be described from the Southeast have already been "found" by past botanists and collections likely exist in herbaria, but their distinctiveness has yet to be realized.
  4. Probably only a very small number of species to be discovered have never been collected previously by botanists.
  5. probably less than 25% are species that are immediately recognizable as new species - that is they are so distinct as to be easily separable at a glance. 
  6. The remaining 75% will likely require detailed scientific research involving statistical analyses of morphological variation and examination of DNA sequence data.
  7. More than 90% will have geographic ranges that are restricted to or centered on known biodiversity hotspots.

Since we know that biodiversity hotspots are the areas most likely to contain narrowly endemic species these are the same areas where we should focus our efforts to locate undescribed species. For example, an analysis of the new species described in the past 40 years reveals distinct patterns. Certain areas have routinely yielded new species. For example, there have recently been a number of new species described from the Cumberland Plateau of Alabama and Tennessee in the past few decades (e.g. Blephilia subnudaClematis morefieldiiPenstemon kraliiPolymnia johnbeckiiSolidago arenicola, and Stenanthium diffusum). Other regions that have consistently yielded new species include the West Gulf Coastal Plain of eastern Texas and western Louisiana, the southern Ridge and Valley of Alabama and Georgia, the Florida Panhandle, and the Blue Ridge Mountains. What is clear from these data is that some places just aren't as likely to harbor undescribed species, such as areas along the Mississippi River in eastern Arkansas or western Tennessee.

While it is true that many of the remaining species to be discovered are in remote areas, many, if not most of those left to find in the Southeast literally may be in our backyards, along our favorite hiking trails, or along the side of the busy roads we travel everyday. A 2000 publication by Barbara Ertter (Univ. of California, Berkeley) titled Floristic surprises in North America north of Mexico, described countless examples of new species that were discovered right under our noses. Recent examples of newly discovered species in Southern "backyards" include the endangered John Beck's Leafcup (Polymnia johnbeckii) and the Smoky Mountain Sedge (Carex fumosimontana). The leafcup was discovered in 2008 along the side of Interstate 24 just a few miles west of Chattanooga, Tennessee in the southern Cumberland Plateau ecoregion - an area identified on Estill and Cruzan's map as a hotspot. This new species has escaped detection by countless botanists and millions of passersby over several decades in spite of growing abundantly along rocky ledges within 30 feet of and in plain site of the interstate. The Smoky Mountain Sedge was discovered in another hotspot, the Southern Appalachians. It was found on eastern North America's second highest mountain, Clingman's Dome, in Great Smoky Mountains National Park and was the dominant ground cover beneath the  observatory tower, at what may very well be the single most heavily visited landmark in the US National Park system.

Polymnia johnbeckii (John Beck's Leafcup), a new species discovered D. Estes in 2008
known from two localities just west of Chattanooga, TN and nowhere else.

It is imperative that we continue to conduct, support, and fund inventories of our biodiversity. We also should not take it for granted that just because botanists have studied an area or a group of plants in the past that there's nothing left to do or discover. 

Unfortunately funding for describing species is almost non-existent. It is generally beyond the purview of large granting agencies such as the National Science Foundation. Federal and state agencies charged with environmental protection are also generally reluctant or unable to fund the description of undescribed species since they don't yet officially have a name. This is unfortunate given that most undescribed species that remain are likely the rarest of the rare and many would qualify as candidates for federal listing or at least being tracked as rare species at the state or provincial level. A related factor is lack of time. Many of the people who describe new species are affiliated with academic institutions and between balancing their responsibilities for teaching, advising, committee assignments and research, the meticulous work required to research and describe new species must be moved to the back burner. It often takes 2-5 years of research to do the work necessary to describe a species and prove its distinctiveness. When we couple this with how few researchers there are in the Southeast who are actively working on describing species, it is evident that it could take decades to describe all that are presently known. Many species don't have that kind of time and will face serious depletions in populations sizes, numbers of populations, and perhaps even extinction before we can get to them. 

To highlight just how large the problem is with the new species backlog, consider the figure below that shows numerous undescribed species and some recently described species found within the past few years.

Forty undescribed or recently described species from the Southeast. Twenty-five of the species photographed in this plate are putatively undescribed.