What is in a Name: Nomenclature and Taxonomy in Turtles
A Case study on the Relationship of Conservation Biology and Taxonomy
Figure 1 | The Southern Stream Turtle (Elseya (Hanwarachelys) rhodini) of southern New Guinea (Thomson et al., 2015)
- In this article I am bringing together two of the major areas of study in Biology, or Life Sciences. Those being Conservation Biology and Taxonomy. Conservation is totally reliant on the study of taxonomy as its source of basic information on species, species identification, delineation, boundaries (both geographical and biological) and their nomenclature. This relationship is by necessity one way. Taxonomy is by necessity a supplier of information to Conservation, but Conservation cannot drive taxonomy. Taxonomy is a complicated science that is poorly taught. Many misunderstand it. This paper is aimed at the vast majority of people, and biologists who are interested in biodiversity and saving it from what is likely the 6th great extinction. To save it you have to know what it is and taxonomy is the science that will tell you what it is you are saving.
- This lecture is based on a plenary lecture that myself Scott Thomson and Peter C. H. Pritchard gave at the Turtle Survival Alliance conference in 2018. It is relatively advanced taxonomy and conservation biology material. I would recommend reading the Introduction to Taxonomy page to ensure you have the concepts of biological classification understood for this. As a scientist I have been heavily involved in the last 15 years or so in a number of works that do this particularly in areas of development of policy for international and regional checklists, species identification guides etc. I am a taxonomist and a paleontologist, more or less the same thing but one works with living species and one works with fossils. Although I studied Ecology as an undergraduate at the University of Canberra I do not work as a conservation biologist. As a practicing taxonomist I have named 7 new species, one genus and one subgenus, all turtles, both living and fossil. Peter has also named several species. I have also published field keys, synonymy's and many nomenclatural acts as has Peter in his many books on turtles. In one way or another we have effected the scientific names of many turtle species. So taxonomy in the here and now is where I will start, then I am going to relate it to Conservation.
Concepts in Taxonomy
- Species boundaries are one of the most important parts of taxonomy that is used in conservation. This tells us if the species is a distinctive entity, how it differs from its relatives and where it is located.
- Nomenclature provides the name for the species, each rank of which is called a taxon. The binomen is actually made up of two separate taxon names, the genus and the species. Its importance to Conservation is it provides the name of the species. This name is often a requirement of legislative protection for a species.
- Taxon : any named unit in the classification system
- Type : name bearing specimen representing a taxon
- Nomen, Nomina : name of a taxon that is attached only to the type
- Combination : the genus + species binomial
- Nomenclatural Act : any code compliant statement that changes nomenclature
- Circumscription : nomenclatural act that applies a name to a specimen
Why is this Important Now?
In recent years there has been misunderstandings between the taxonomic and conservation communities, largely because taxonomy and nomenclature are not taught well, if at all, in many biology degrees around the world. When they are it is largely only some rudimentary classification and molecular phylogenetics. This is not true of all universities, but is unfortunately all too common. As such conservationists are calling for stability in the names, they do not want species to be split, lumped or placed into different genera. None of these actually refer to stability as it is defined in the ICZN Code. This led to the publishing of a now famous opinion piece by Stephen Garnett and Les Christidis in Nature entitled "Taxonomy anarchy hampers conservation." This paper was met with a large number of rebuttal papers, largely they were against the notions of intruding governance over taxonomy and controls on the methods of the science. In short their view was seen as anti-science. One of the papers was one I was lead author of (out of 184 authors) published in PLoS One which we entitled "Taxonomy based on science is necessary for global conservation." Garnet and Christidis argue for a Governing Body (possibly under the IUBS) to be formed to review and decide on the validity of taxonomic papers, and that this committee would decide on the species concept to be used in taxonomic research. Whereas Thomson et al. (and many other responses) argue that this approach is non scientific, stifles scientific advances and blurs the distinction between taxonomy and nomenclature. To address this fully we need to understand what taxonomy and nomenclature are and how they relate to conservation.
What is Taxonomy and Nomenclature
Figure 2 | The relationship between Taxonomy and its components and Nomenclature. Taxonomy is made up of Classifications and Taxa, taxa are defined by relationships. These are linked to names through the type specimen. The Type specimen carries the name and is the signifier of the name. The populations are signified by the type specimen. The only specimen of a species that hold the name is the type.
Taxonomy is a hard science (ie data driven) that determines the relationships between populations, if they represent species, genera etc. It determines how we use the names for taxa and this part is called validity under the ICZN code. Nomenclature is not a science, it is a regulated bookkeeping system of names that follows a set of rules. These rules govern how names are formed, how they are published and if they may be used. This is called availability. As shown in Figure 2. the holotype or other type specimen is the connection between the names and the populations using the names. The type specimen holds the name, the type identifies the name and only the type specimen can use the name. The population is given the name by the type when it is demonstrated that the type specimen is a member of that population. This is an important concept to understand as this is why when it is demonstrated that a holotype has been misidentified the name must be moved to a different taxon we have been used to applying it to. All biologists for 200 years have agreed to follow the rules of nomenclature so when mistakes are made in nomenclature it can have undesirable outcomes. Hence this is a field exacting care and diligence. The Science of Taxonomy uses multiple tools (Morphology, DNA sequencing, Morphometrics) to determine relationships, leading to circumscription of taxa. It is a base, data driven science and determines the combination of the names (ie: genus + species) and also the rank of the names within each defined taxon group, for genus group names is it a genus or a subgenus, for species group names is it a species or a subspecies. Nomenclature as a code driven system of producing and using names is entirely governed by the rules of nomenclature (ICZN for animals) The code refrains from infringing on taxonomic judgement which cannot be subjected to regulation or restraint. It cannot determine the inclusiveness or exclusiveness of any taxon, nor the rank to be accorded to any assemblage of animals. The rules are a set of tools that are designed to provide the maximum stability compatible with taxonomic freedom.
The Concept of Stability In Nomenclature
This is the confusing part for many people, what do we mean by stability in names. It does not mean stability of the combination because the combination is a taxonomic decision and the code precludes itself from ever infringing on taxonomic thought. It only refers to conserving current usage of mononomial’s (single parts of names). The Binomial combination does not have to be stable.
Example: Myuchelys vs. Wollombinia
- Myuchelys has usage over Wollumbinia and hence is the valid name unless a decision published as an opinion by the ICZN states otherwise. Myuchelys appears in over 10 Journals and 120 publications since 2009. The name Wollombinia only appears in 30 publications, of which 70% of them use it to synonymize it.
- Article 82.2 Conservation of Usage.
- Article 23.10. Erroneous reversal of precedence. If action taken under Article 23.9.2 is found later to have been taken in error in that conditions 18.104.22.168 and 22.214.171.124 were not met, the case is to be referred to the Commission. Prevailing usage must be maintained Article 82.2 until the Commission has made a ruling.
To put that more simply, some argue that the sinking of the name Wollombinia, 2 months after it was published as it was deemed an unavailable name due to invalid publication, was wrong. Since that time the name Myuchelys has come into usage. To fix this mistake, however, a case must be submitted to the ICZN and it must be determined by the ICZN how to proceed, until they make their decision prevailing usage, most common usage, must be maintained. This is to stop people just swapping names around continuously because they think differently to the last publication. It maintains stability and prevents confusion.
What is the Type Specimen
Figure 3 | Holotype of the Australian fossil turtle Rheodytes devisi Thomson 2000. This is the original specimen used to define the species, the name is attached to this specimen.
The type, usually holotype, is the original specimen used in the circumscription of the species. It is the specimen to which a name is attached. If there is only one it is called the holotype, in the past they used to use multiple types of equal value these are called syntypes. If necessary one syntype can be later declared the lectotype and becomes the name bearing type. Some authors also set paratypes, additional specimens used in the description, they may declare one of these an allotype which is the opposite sex of the holotype. Another that rarely comes up but does exist is an iconotype, this occurs when the only specimen was a photograph or drawing of the animal but the specimen did not exist. These are not set anymore but some historical species have them.
ICZN Code: Crucial Points
- ICZN Preample - "The objects of the Code are to promote stability and universality in the scientific names of animals. All its provisions and recommendations are subservient to those ends and none restricts the freedom of taxonomic thought or actions."
- ICZN 1st Guiding Principal: "The Code refrains from infringing upon taxonomic judgment, which must not be made subject to regulation or restraint"
What you must not do with Nomenclature
The job of the ICZN: If it is the ICZN Commission’s decision, they must make it.
- Example: McCord et al. 2007
- The authors attempted to set a Neotype for Chelodina oblonga to conserve the name for the Perth (Australia) form.
- Only the ICZN can replace an existing Holotype with a Neotype.
- Result: A new species, Chelodina oblonga McCord et al 2007, which was a Junior Objective Synonym of Chelodina colliei.
Make Nomenclatural Acts without Examining the types.
- Example: Wells and Wellington 1985*
- The authors set a lectotype for Emydura victoriae. The lectotype they set was a specimen of Emydura macquarii.
- Result: Emydura victoriae is a junior subjective synonym of Emydura macquarii and hence invalid name. (sensu Iverson et al, 2001)
- This issue was recently repaired by Kehlmaier et al. (2019) after some 25 years of confusion as it took considerable effort to obtain the necessary data to overturn the decision.
Mix Taxonomy and Nomenclature
- Example: The Case against Wells and Wellington 1985 to the ICZN explicitly cited the taxonomic confusion that their work created.
- Result: The ICZN refused to rule citing the situation was taxonomic and not nomenclatural, hence was outside their capacity to act.
Taxonomic and Nomenclatural Changes
- "…a taxonomic change,…should be refuted rather than ignored…" Pritchard (1996:37) is one of the major tenants in nomenclatural taxonomy. It basically means when a name is proposed, or changed, you must refute the research that produced the name or change, or you must accept it. This concept is relevant to both taxonomy and nomenclature, though is applied differently to each.
- If this is about Taxonomy, the refutation must be based in science. Eg genus combination changes, rank changes, validity.
- If this is about Nomenclature, the refutation must be code compliant. Eg. Synonymies, availability.
Now for some Taxonomy
Up to this point I have been largely discussing nomenclature, it is often misunderstood. Now we can discuss some taxonomy, issues in taxonomy, best practices etc. As I showed above this is what is on the other side of the type specimen from nomenclature. This area is science, it is about hypothesis testing, about relationships between populations and whether or not we name these populations. Are they species. Also about whether we can group some of these populations together into evidence based natural groups, called genera. This science must follow the current best practices of science which generally means the results are published in peer reviewed journal papers. In general it will have the following features:
- Must present a Phylogeny - what are called trees, a representation of the evolutionary tree of life are produced from data matrices which show evolutionary relationships and statistical support for them. Many software packages are available for this.
- The Total Evidence Approach is the combination and reconciliation of mtDNA, nuDNA and Morphology to produce the trees, it will also include morphometric analysis.
- It must also include the fossil record, 99% of all life that has ever lived is now extinct, it is negligent of all this data to ignore the fossil record.
Total Evidence Example
Figure 4 | Manning River Turtle from Australia. This species is separated from the genus Myuchelys by 103 Million Years.
- Genus Flaviemys Li et al. 2014. (Figure 4)
- Entire mtDNA genome + morphology have it paraphyletic with respect to Emydura. Is related to Rheodytes and Elusor. Some have the species as a member of Myuchelys.
- nuDNA has it as sister to Myuchelys.
- Fossil record dates Myuchelys (excluding Flaviemys) to 103 million years, older than all modern mammals or birds.
- So why is it in Myuchelys ??…..
You Cannot Ignore the Fossils
- According to Paleontological Data the Superfamily Chelydroidea (American Snapping Turtles) contains the Families: Chelydridae; Dermatemydidae; Kinosternidae; and Planetochelyidae.
- However, if only the Extant taxa are examined a different result occurs with the Family Chelydridae on its own and the Superfamily: Kinosternoidea containing the Families: Dermatemydidae and Kinosternidae.
What has happened here is that relationships between the fossils and the living species have effected the types of relationships between the species, this has caused a difference in the ways the tree lays out, the support for those trees is also effected. As the fossil turtle species outnumber the living ones by at least 4:1 whenever you add in the fossil taxa the tree changes significantly. Trees with the most data points always have more support. Hence, you cannot ignore the fossils.
In recent years this has become an issue and it can be a little confusing exactly what it means. In the past the publication of your research was a time consuming and expensive process. Difficult for people to do themselves. However, with the advent of desktop printers and modern computers it became possible for anyone to mass produce their work. This avoids peer review which means people can publish anything they want, but should we follow the recommendations of privately published works that have never been reviewed in any way prior to their release?
- It is the unjustified, by any acceptable evidence, nomenclatural rearrangement of taxa.
- It cannot be followed and permitted.
- It discredits all science, and all of us.
Genuine vandals have dragged others down with them by encouraging them to add their name to quick and easy publications. Nomenclatural Acts and Taxonomic re-arrangements must be published with the benefit of peer review. The best practice argument. This means for turtles, nomenclatural review and taxonomic review needs to be done by specialists in turtle taxonomy and nomenclature. Too many have taken short cuts, we now have little choice but to be severe on this.
Taxonomy, Nomenclature For Conservation
Conservation Biology is largely about protecting Biodiversity, habitats and the species within them. It is a complicated and broad science and is a mesh of Ecology and Management. With respect to how it utilizes taxonomy, taxonomy provides names for the various species practitioners are interested in. From this conservation assists in the establishment and implication of legislation for protecting species. In general this is referred to as "protected species lists' or "scheduled species lists" depending on the country it is different. This legislative action is attached to species names. Although it is largely unavoidable it is somewhat self destructive attaching the legislation to the name itself. This is because taxonomy is a science it is in a constant state of change, legislative acts do not cope well with a constantly changing taxonomy. A better option is to protect populations by recognizing and protecting populations defined in species definitions. The science will change, will update. A species will change genus, be renamed. But the wild population represented by all this remains the same. Protect the population as defined by the descriptions.
The number of species and genera , and the combinations between them. Will always change, as science will always change. There is no stability in this it cannot be expected. Stability as defined above only applies to the mononomial, any expectation that the combination (genus + species) will remain the same is unrealistic and fails to recognize that taxonomy is a science.
Conservation must not attempt to drive the science of taxonomy or we have a circular argument. When conservation comes up against industry for example, there will generally be at least a study such as an Environmental Impact Assessment to determine and then minimise the impacts. This can be contributed to by the industry, they will look at the species involved in the issue. The last thing that conservation wants is it to be demonstrated that the species was described and restricted to a small range so it could be used in this way, to stop a project. This will call into question the validity of the science and the motivations of the scientists involved. When I have described species I do not discuss the conservation issues for the species, they are described based only on the science.
- Taxonomic science must determine if a population represents a species and this must be based solely on the hard data.
- Conservation science must determine if that population needs help, what help it needs and this is based on the Ecology of the species.
- Taxonomy provides Conservation with a name for that population and its basic informational science such as distribution.
Real Examples of Nomenclatural Issues
Conservation of Usage: Podocnemis unifilis
Occasionally old names are found to be the actual valid name of a species, but we have been using a younger name. A strict following of the ICZN code would mean we change the name, however, this is not always desirable so there is a mechanism to keep using the current name. This is a real case of how this works. The two names in question are as follows, both refer to the same species:
- Emys cayennensis Schweigger, 1812:298. Type locality: ‘Cayenna’ [= Cayenne, French Guiana]. Lectotype: Bour (2006): MNHN 8359 (see also Pritchard & Trebbau, 1984)
- Podocnemis unifilis Troschel, 1848:647. Type locality, ‘Rupununi und Takutu’, Guyana. Syntypes: Museum für Naturkunde, Berlin ZMB 142
Part of the issue was that the name P. cayennensis was used for another species P. erythrocephala incorrectly for a considerable time. This error was first discovered by Mittermeier and Wilson (1974), then Pritchard and Trebbau (1984), followed by Bour (2006). Within the rules it does permit that taxonomists can just declare completely forgotten names as nomen oblitum or forgotten name, but in this case the name Emys cayennensis had been used so it was not possible. So a Case was taken to the International Commission on Zoological nomenclature for them to use their plenary powers to reverse the priority of the two names. We are always supposed to use the oldest available name for a species, this is called the Principal of Priority. In the case we had to do the following:
- Reverse Priority.
- Establishes the full synomymy
- Split the type series for P. unifilis.
- Demonstrate Usage statistics for the names.
One of things to establish in a request to the ICZN such as this is how much usage each name has had in its valid placement. That is how many publications have used each name to apply to what is commonly known as the Yellow-spotted River Turtle of South America. The Code explains it like this:
- Article 126.96.36.199. Article the junior synonym or homonym has been used for a particular taxon, as its presumed valid name, in at least 25 works, published by at least 10 authors in the immediately preceding 50 years.
It was found that Emys cayennensis Schweigger 1812: 298 (circa 5 publications) whereas Podocnemis unifilis Troschel in Schomburgk 1848: 647 (>200 publications). Note here I am using what is known as the original combination, this is about the species epithet only, the genus is irrelevant. Hence to make it clear which name we are talking about it is being used in the original genus it was described in with the author, year and page number. Nomenclature is a very exacting field. Once the case is submitted the current prevailing usage must be used for the species until the ICZN makes a decision, called an Opinion. As per Article 82.1. Maintenance of prevailing usage. When a case is under consideration by the Commission, prevailing usage of names is to be maintained until the ruling of the Commission is published.
Another issue was that the name Podocnemis unifilis was based on a type series (syntypes) rather than a single holotype. Both specimens had the same museum number. This is not desirable in modern nomenclatural and taxonomic work so we split the type series. One specimen kept the original number, ZMB 142, and became the lectotype or name bearing type specimen. The other received a new number ZMB 49415 and became the paralectotype for the species.
In 2019 the ICZN published its opinion on the case where they accepted the request and reversed the priority for the two species, permitting the continued usage of the well known name for the species, Podocnemis unifilis.
Replacement Type Terrapene putnami
Since holotypes and their equivalents are used to determine which population the name belongs to it is important that these types are in good condition. Sometimes the original material is just not good enough. This was true of the case of the fossil species Terrapene putnami. The holotype was a single bone from the plastron of the turtle. It is difficult for anyone, no matter how skilled, to utilise such scant material to determine relationships. However, no matter how poor, the type does exist and this means only the ICZN can replace the type with more usable material.
- Case 3628: Terrapene putnami Hay, 1906 (Testudines, EMYDIDAE): replacement of the holotype by designation of a neotype.
For this case the goal is to have a diagnosable type for the species which permits better placement of the species in phylogeny hence an improved understanding of relationships. Further it resticts the species boundary to a diagnosable entity. The authors have had to nominate a suitable specimen to replace the original type, it consists of an almost complete fossil, carapace, plastron, skull and limb bones. This particular case is still awaiting resolution from the ICZN. However, this is the correct way to deal with damaged type specimens.
- Garnett, S; Christidis, L. (2017). "Taxonomy anarchy hampers conservation". Nature 546 (7656): 25–27. doi:10.1038/546025a. ISSN 0028-0836. https://www.nature.com/news/taxonomy-anarchy-hampers-conservation-1.22064.
- Thomson, S; et al. (2018). "Taxonomy based on science is necessary for global conservation". PLoS One 16 (3): e2005075. doi:10.1371/journal.pbio.2005075. ISSN 0028-0836. https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.2005075.
- International Commission on Zoological Nomenclature (2012). "ICZN Code Online Preamble". ICZN. ICZN. Retrieved 2 November 2019.
- Iverson, J.B.; et al. (2001). "Validity of the taxonomic changes for turtles proposed by Wells and Wellington.". Journal of Herpetology 35: 365–368.
- Kehlmaier, C; et al. (2019). "Mitogenomics of historical type specimens of Australasian turtles: clarification of taxonomic confusion and old mitochondrial introgression.". Scientific Reports 9 (5841). doi:10.1038/s41598-019-42310-x.
- Wells, R.W.; Wellington, C.R. (1985). "A classification of the Amphibia and Reptilia of Australia.". Australian journal of herpetology (supplementary series) 1: 1-61. http://www.calodema.com/product_info.php?cPath=28&products_id=319.
- Pritchard, Peter C. H. (1996). "The Galápagos Tortoises: Nomenclatural and Survival Status.". Chelonian Research Monographs 1: 1-85. ISSN 0-9653540-0-8. http://www.chelonian.org/crm.
- Vogt, R.C.; Thomson, S.A., Rhodin, A.G.J.; Pritchard, P.C.H.; Mittermeier, R.A. & Baggi, N. (2012). "Podocnemis unifilis Troschel, 1848 (Reptilia,Testudines): proposed precedence over Emys cayennensis Schweigger, 1812.". Bulletin of Zoological Nomenclature 70 (1): 33-39. ISSN 0007-5167. https://www.iczn.org/submitting-to-the-bulletin-of-zoological-nomenclature.
- International Commission on Zoological Nomenclature (2019). "Opinion 2431 (Case 3587) – Podocnemis unifilis Troschel, 1848 (Reptilia, Testudines): precedence given over Emys cayennensis Schweigger, 1812". Bulletin of Zoological Nomenclature 76: 77-78. doi:10.21805/bzn.v76.a023. ISSN 2057-0570. https://www.iczn.org/submitting-to-the-bulletin-of-zoological-nomenclature.
- Ehret, D.J.; Bourque J.R. & Hulbert, R.C. Jr. (2013). "Case 3628: Terrapene putnami Hay, 1906 (Testudines, EMYDIDAE): replacement of the holotype by designation of a neotype.". Bulletin of Zoological Nomenclature 70 (3): 193-198.