Within recent years, the Palaearctic tortoise fauna has undergone a radical change. If you’re interested in the recognition and discovery of new species, in controversy and argument about the status of species, in neat evolutionary stuff such as resource polymorphism and resource-mediated dwarfism, and, least of all, in tortoises, then you should find this a fascinating area. I shall point out to start with that I’m referring specifically to the testudinid tortoises of the genus Testudo, an Old World taxon most closely related to the Asian tortoises (Indotestudo) and the Pancake tortoise Malacochersus tornieri and united with them in the recently-named clade Testudona (Parham et al. 2006a) [T. marginata shown here, from wikipedia].
Mostly inhabiting wooded hillsides, clearings and groves, and scrubland, little known is that some Palaearctic tortoise species are superb diggers, well able to excavate tunnels several metres long. Thanks to the pet trade, I suppose most people imagine that the staple diet for tortoises consists of tomatoes, cucumber slices and lettuce leaves. In fact wild tortoises have a surprisingly diverse diet; snails have proved quite important to some species, and they will also eat faeces and gnaw at bones and carrion. They may not drink, they indulge in vigorous combat during the breeding season, and they make loud vocalisations when they copulate.
Within recent decades just five Testudo species have been recognised (e.g., Ernst & Barbour 1989), and this conservative count will be referred to from hereon as the ‘conventional’ taxonomy. But, as usual, things aren’t so simple anymore. A huge number of new species and newly elevated former subspecies have recently been proposed, meaning that there are now as many as 27 proposed species within the genus Testudo. As is also usual (harking back to comments I made at Tet Zoo ver 1 about the lack of good literature on the extant herpetofauna), this major taxonomic reshuffling has gone unreported in the popular and semi-technical literature, and has been avoided by field guides, so the only way to chase up any of this stuff is to track down the primary literature.
The splitting up of Testudo
The five ‘conventionally’ recognised Testudo tortoises are; the Spur-thighed tortoise T. graeca Linnaeus, 1758, a species that sports a large conical tubercle on the posterior surface of its thigh; Hermann’s tortoise T. hermanni Gmelin, 1789, equipped with a large horny scale at the tail-tip; the Central Asian tortoise T. horsfieldi Gray, 1844 (or T. horsfieldii), a broad-shelled tortoise with just four claws on each forefoot [captive individual shown here]; the Egyptian tortoise T. kleinmanni Lortet, 1883; and the Marginated tortoise T. marginata Schoepff, 1792: a particularly large species with a strongly flared posterior margin to the carapace [see photo below].
However, two of these have now been removed from Testudo. The four-clawed Central Asian tortoise (or Horsfield’s tortoise) is now regarded by many experts as being distinct enough for its own ‘genus’, Agrionemys Khozatsky & Mlynarski, 1966 (the idea that this taxon represented a distinct genus was resurrected in 1957 and initially the name Testudinella Gray, 1870 was used. This turned out to be unavailable due to preoccupation). It has also been proposed that Hermann’s tortoise is distinct enough from Testudo to warrant generic separation, and fossils allied to this species – like ‘Testudo‘ turgaica from Kazakhstan and ‘Testudo‘ promarginata from Germany and France – show that its lineage has been distinct since the middle (and possibly Early) Miocene. Accordingly, Lapparent de Broin et al. (2006a) coined Eurotestudo for Hermann’s tortoise and the rest of its lineage (see also Lapparent de Broin et al. 2006b, c). However, Fritz & Bininda-Emonds (2007) failed to find support for this and (based on a five-gene data set, as opposed to mtDNA alone) found Hermann’s tortoise to form a clade with the Central Asian tortoise. Anyway, Eurotestudo turns out to be a junior synonym of both Chersine Merrem, 1820 and Medaestia Wussow, 1916, contrary to what Lapparent de Broin et al. (2006a) stated. If any name is used for the Hermann’s + Central Asian clade, it should be Chersine.
Hermann’s tortoise has conventionally been thought to consist of two taxa: T. h. hermanni in the western part of its range, and T. h. boettgeri in the Balkans. T. h. boettgeri is far less heavily marked than T. h. hermanni, and on the basis of this difference and others, it has been raised to full species status (as T. boettgeri) by some authors. Furthermore, T. boettgeri has itself been argued to include another overlooked taxon: T. hercegovinesis of the central Dalmatian region (Croatia). If Lapparent de Broin et al. (2006a, b, c) are right in separating Hermann’s tortoise from Testudo and regarding it as part of a distinct genus (and they may not be), then it follows that T. boettgeri, and presumably T. hercegovinesis, are members of that same genus [image below, from wikipedia, shows the amazing flaring carapace edge of T. marginata, at left, with a Sardinian tortoise T. marginata sarda at right. The taxonomic status of the Sardinian tortoises is uncertain; they may be recent introductions].
Incidentally, another two extant taxa have recently been argued to warrant separate species status, but this time relative to the Central Asian tortoise A. horsfieldi: A. kazachstanica Chkhikvadze, 1988 and A. rustomovi Chkhikvadze et al., 1990.
The north African tortoise explosion
Under the ‘conventional taxonomy’, all north African tortoises are regarded as belonging to the same species, Testudo graeca. However, Highfield (1990) argued that these tortoises exhibit a significant amount of morphological diversity: the many north African populations thought to belong to T. graeca could, according to Highfield, be shown to differ markedly from the tortoises properly associated with this name (the type specimen came from ‘Santa Cruz in West Barbary’; a location close to Oran, Algeria). They should, therefore, really be recognised as additional distinct species (or so it has been argued).
One tortoise from Algeria was argued by Highfield (1990) to be radically different from the others, and in fact so different that it required the creation of a new genus: Furculachelys nabeulensis, the Tunisian spur-thighed tortoise. The holotype is a partially decomposed, damaged specimen but live animals from the same region were argued to belong to the same taxon. What makes this small tortoise particularly unusual is that its suprapygal (the bone located dorsal to the pygal: the pygal is the midline bone that forms the posterior carapacial border just above the tail) is forked, hence the generic name (it means ‘forked tortoise’). Living Tunisian spur-thighed tortoises are reported to be yellowish with black blotches on some of their scutes and, as indicated by the common name, large spikes are usually present on the hindlimbs [image below shows Tunisian spur-thigh, from wikipedia].
One of the most remarkable claims made about Palaearctic tortoise taxonomy is that Timothy the tortoise, kept by the English naturalist Gilbert White, represented a distinct species of which ‘he’ was the first known representative (Timothy was actually female). White obtained Timothy following the death of his aunt in 1780, and prior to this the tortoise had been purchased by White’s uncle from a sailor in 1740. White thought that Timothy might have come from the USA (his aunt also kept box turtles), and identified ‘him’ as a specimen of T. graeca. Timothy’s shell was preserved following her death in 1794, and seems to correspond in its size and coloration with that of some Algerian tortoises described in 1945. Highfield & Martin (1989a) wrote how Timothy and these other individuals represented a distinct species: with a carapace about 25 cm long, they were big compared to T. graeca, and they were distincely patterned too, with a ray-like pattern radiating from their yellowish-greenish vertebral and costal scutes. Bennett, the editor of the 1836 edition of White’s book The Natural History and Antiquities of Selborne (1789), added a footnote in which he also argued that Timothy was distinct from T. graeca. As a result he proposed that it was a new species, T. whitei.
Van der Kuyl et al. (2005) were able to test the proposed affinities of individuals referred to T. whitei. Alas, they found that these tortoises fell within T. graeca, and specifically within T. g. graeca. They found T. graeca to consist of two complexes: a T. g. graeca clade, and a T. g. ibera clade. T. g. ibera , sometimes called the Eurasian tortoise (it occurs in Turkey, Greece, Macedonia, Bulgaria and Romania), has been suggested to be worthy of species status on several occasions. Indeed, this was supported by van der Kuyl et al. (2005) who inferred that T. ibera and T. graeca had diverged during the Early or Middle Pleistocene.
New tortoises of Europe and the Middle East
Bour (1995) named T. weissingeri for a population of dull-coloured, dwarf tortoises from the Peloponnese. These animals had conventionally been regarded as a population of Marginated tortoise T. marginata. Several authors later proposed that the supposedly distinct characters of T. weissingeri result from adaptation to a nutrient-poor, arid environment, and subsequent genetic work failed to find any indication that the Pelopennese dwarfs represented a distinct population relative to T. marginata (Fritz et al. 2005).
Of the many tortoise taxa conventionally regarded as part of T. graeca, Highfield & Martin (1989b) regarded T. zarudnyi (Nikolski, 1896) of the Iranian central plateau* as a distinct species. A rare, arid-land tortoise with an elongate carapace and flared, serrated marginal scutes, its diagnostic features include eyes which are unusually elongate and almond-shaped rather than rounded, dorsoventrally flattened forelimbs, and with one of the five hand claws noticeably smaller than the others. Almond-shaped eyes are also present in T. ibera and this species and T. zarudnyi are similar in several respects, the ‘conventional’ opinion being that they grade into one another. Highfield & Martin (1989b) thought that T. zarudnyi and T. ibera were close relatives, and that they are both close to the Marginated tortoise T. marginata.
* Although there is one record from Ashgabad, Turkmenistan.
In a taxonomic revision of the variation present within Middle Eastern tortoises, Perälä (2002) split Middle Eastern populations previously lumped together as T. graeca into eight separate species, and also named a new species from Turkey (T. perses).
Of the five ‘conventionally recognised’ Testudo species, the most poorly known is the Egyptian tortoise T. kleinmanni Lortet, 1883 [shown here, from wikipedia]. It is small, with females reaching just 13 cm in carapace length. In 1963 a specimen was collected from the Negev Desert in Israel (this was supposed to be the first record of this species from the country, but the occurrence of supposed T. kleinmanni individuals from the region had actually been written about during the 1880s). Perälä (2001) argued that the Negev animal was only superficially similar to T. kleinmanni, and could in fact be readily distinguished from it: with its particularly wide mid-body region, narrow vertebral scutes, and other distinctive features it was deserving of recognition as a new species, and was named T. werneri (after herpetologist Y. L. Werner).
And I think we should stop there, though of course there are multiple other resurrected or ‘newly promoted’ species that I could discuss as well. Does this amazing proliferation of new species names really reflect actual, genuine discovery? Does it mean that the ‘conventional’ taxonomy is woefully inadequate and way too conservative? Or does it show that some workers are taking a particularly relaxed view as to what a ‘species’ is? Are they being misled by intraspecific variation? While this taxonomic inflation is generally in keeping with current trends (see Laissez-faire lumping under fire again on ver 1), many of the newly proposed – or newly resurrected – species have proved controversial. One of the main problems seems to be that all of the ‘new’ species have been differentiated on morphological grounds (often on shell characters, but also on body size, scale size and distribution, and overall body colour), and there is a widespread suspicion among testudine workers that these are relatively ‘plastic’ features, prone to substantial variation and easily modified according to an individual’s life history. Indeed exactly the same problem has afflicted research on the giant island endemic tortoises of the Indian Ocean (for more on this, see the ver 1 article here).
With so many ‘new’ species now awaiting detailed evaluation (and with many of the claims being very recent), it is taking a while for the right sort of work to be done. However, to date, the results indicate that ‘premature taxonomic inflation’ (Parham et al. 2006b) has occurred. Genetic studies suggest that the ‘conventional’ taxonomy is better supported, and that strikingly little genetic variation exists between some of the putative new species (Fritz et al. 2005, 2006, van der Kuyl et al. 2005, Parham et al. 2006a, b). Given the high conservation priorities of Palaearctic tortoises, it can be argued that unfamiliar species names can obscure important evolutionary lineages [the image below, showing Galapagos giant tortoises, is irrelevant but I thought it looked pretty weird].
As Fritz et al. (2005) noted, most of the newly described or revived Testudo species have been published in ‘grey literature’. Indeed, many of the relevant papers have appeared in privately published books and booklets that aren’t widely available, or in obscure, hard-to-get journals. Examples of the latter include Emys, Dumerilia, Herpetozoa, Chelonii and Manouria. I know that describing these journals as ‘obscure’ and ‘hard-to-get’ is unjust given that they are required and regular reading for specialist testudine researchers, but for the rest of us… well, how many academic libraries do you know of that stock back-issues of Manouria?
And, if you’re wondering, Manouria is a generic name for an Asian tortoise.
Those who keep track of such things may be interested to know that this article has been alluded to since June 2007 at least. Another one to tick off the list.
Refs – –
Bour, R. 1995. Une nouvelle espèce de tortue terrestre dans le Péloponnèse (Grèce). Dumerilia 2, 23-54.
Ernst, C. H. & Barbour, R. W. 1989. Turtles of the World . Smithsonian Institution Press, Washington, D. C. & London.
Fritz, U., Auer, M., Bertolero, A., Cheylan, M., Fattizzo, T., Hundsdörfer, A. K., MartÃn Sampayo, M., Pretus, J. L., ?iroký, P. & Wink, M. 2006. A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zoologica Scripta, 35, 531-543.
– . & Bininda-Emonds, O. R. P. 2007. When genes meet nomenclature: tortoise phylogeny and the shifting generic concepts of Testudo and Geochelone. Zoology 110, 298-307.
– ., ?iroký, P., Kami, H. & Wink, M. 2005. Environmentally caused dwarfism or a valid species – is Testudo weissingeri Bour, 1996 a distinct evolutionary lineage? New evidence from mitochondrial and nuclear genomic markers. Molecular Phylogenetics and Evolution 37, 389-401.
Highfield, A. C. 1990. Tortoises of north Africa: taxonomy, nomenclature, phylogeny and evolution with notes on field studies in Tunisia. Journal of Chelonian Herpetology 1, 1-56.
– . & Martin, J. 1989a. New light on an old tortoise – Gilbert White’s Selborne tortoise re-discovered. Journal of Chelonian Herpetology 1 (1), 13-22.
– . & Martin, J. 1989b. A revision of the testudines of north Africa, Asia and Europe – Genus: Testudo. Journal of Chelonian Herpetology 1 (1), 1-12.
Lapparent de Broin, F, de, Bour, R., Parham, J. F. & Perälä, J. 2006a. Eurotestudo, a new genus for the species Testudo hermanni Gmelin, 1789 (Chelonii, Testudinidae). C. R. Palevol 5, 803-811.
– ., Bour, R., & Perälä, J. 2006b. Morphological definition of Eurotestudo (Testudinidae, Chelonii): first part. Annales de Paléontologie 92, 255-304.
– ., Bour, R., & Perälä, J. 2006c. Morphological definition of Eurotestudo (Testudinidae, Chelonii): second part. Annales de Paléontologie 92, 325-357.
Perälä, J. 2001. A new species of Testudo (Testudines: Testudinidae) from the Middle East, with implications for conservation. Journal of Herpetology 35, 567-582.
– . 2002. Morphological variation among Middle Eastern Testudo graeca L., 1758 (sensu lato) with a focus on taxonomy. Chelonii 3, 78-108.
Parham, J. F., Macey, J. R., Papenfuss, T. J., Feldman, C. R., Türkozan, O., Polymeni, R. & Boore, J. 2006a. The phylogeny of Mediterranean tortoises and their close relatives based on complete mitochondrial genome sequences from museum specimens. Molecular Phylogenetics and Evolution 38, 50-64.
– ., Türkozan, O., Stuart, B. L., Arakelyan. M., Shafei, S., Macey, J. R., Werner, Y. L. & Papenfuss, T. J. 2006b. Genetic evidence for premature taxonomic inflation in Middle Eastern tortoises. Proceedings of the California Academy of Science 57, 955-964.
van der Kuyl, A. C., Ballasina, D. L. P. & Zorgdrager, F. 2005. Mitochondrial haplotype diversity in the tortoise species Testudo graeca from north Africa and the Middle East. BMC Evolutionary Biology 2005, 5:29 doi:10.1186.1471-2148-5-29