Claims of taurodontism in Homo floresiensis by Charles Oxnard, Peter Obendorf, Maciej Henneberg and Robert Eckhardt a result of incompetence and inexperience

Taurodont teeth
Taurodont molar teeth have a vertically enlarged pulp chamber, with apical displacement of the pulpal floor, no constriction at the level of the cement enamel junction, the point of trifurcation/bifurcation of the roots is moved apically, and there is greatly reduced vertical root length. This change in tooth shape is caused by a failure of Hertwig’s epithelial sheath diaphragm to invaginate at the proper level during the formation of the tooth (Jafarzadeh et al. 2008). Taurodont teeth are known to occur at high frequency in a range of x-linked syndromes (Gage 1978; Jaspers and Witkop 1980), Down’s Syndrome (Bell et al. 1989; Jaspers 1981), Klinefelter’s Syndrome (Gardner and Girgis 1978), and at a lower frequency in the human population more broadly. There is a recorded familial incidence (Goldstein and Gottlieb 1973), some modern human populations have a higher frequency of taurodont teeth than others (Constant and Grine 2001), third molar teeth are more commonly affected than the first and second molars, both deciduous and permanent teeth can have taurodont pulp chambers (Rao and Arathi 2006), and permanent premolars can also be taurodont (Llamas and Jimenez-Planas 1993).

Normal and taurodont molar tooth anatomy
Aboriginal mandibular molars molar teeth normal taurodont
Australian Aboriginal mandibular molar teeth from an archaeological site, all with normal root development for their tooth class. The molar on the right side is a third molar, with constricted roots. This tooth is not taurodont. As is common in third molars, the limited space for root development often results in constricted and shorter roots than is usual in the first two molars. Lateral x-rays of normal (A) and taurodont (B) mandibular molars. Note elongated pulp cavity and apical position of root bifurcation in B.

(Shaw 1928) was the first person to define different categories of taurodontism (cynodont, hypotaurodont, mesotaurodont, hypertaurodont) based on external morphological criteria linked to the apical displacement of the pulp chamber floor. More recent forms of classification have been designed to work with radiographs and use dimensions of the pulp chamber, root lengths, and external tooth dimensions, to develop a taurodont index (Blumberg et al. 1971). 

taurodont molar classification
taurodont molar classification
Measurements taken from lateral x-rays are sometimes used to classify taurodont molar teeth. However, the degree of pulp cavity enlargement, as well as the other characteristics of taurodont teeth, form a continuous distribution. The division between what is normal and what is classed as hypotaurodont, for instance, is a matter of interpretation.

Taurodont permanent and deciduous teeth arealso known to occur at a high frequency in Neandertal’s, for instance at Krapina (Kallay 2014), without any associated skeletal evidence of developmental syndromes. It would be extremely unlikely, if all Neandertal’s, throughout their geographic range and over 10’s thousands of years, all suffered from Down’s Syndrome or an x-linked chromosomal disorder. The probability of reaching adulthood, and reproducing, would have been extremely small, as most syndromes have dramatically reduced fertlity and life expectancy. The incidence of taurodontism in other hominin species has not been documented in any detail. However, some of the Homo erectus from Zhoukoudian had taurodont molars, while known middle Pleistocene Homo from China do not (Weidenreich 1937; Xing 2012; Xing et al. 2014). The etiology of taurodontism is therefore complex. In modern humans the highest frequencies are associated with a range of developmental disorders, but within each of these there is variation in the degree of expression. Taurodont molars were also present at very high frequencies in at least one extinct hominin species, without skeletal evidence of the syndromes known to be associated with these teeth amongst some living humans.

x-rays of taurodont Neandertal molar teeth from Krapina (Kallay 2014)
Krapina molars x-ray

Krapina mandible M molars

Krapina mandible M molars. Note apical position of root bifurcation in M1 and M2, with minimal constriction at the cemento-enamel junction. Roots of the M3 are compressed and the crown of the tooth was impacted on the M2 (position and angle of wear facets).

Claims of taurodontism in the teeth of LB1 and LB6 Homo floresiensis.

In 2008 Peter Obendorf, Charles Oxnard and Ben Kefford (Obendorf et al. 2008) argued that the Liang Bua Homo floresiensis skeletons were most likely the remains of modern humans with myxoedematous endemic (ME) cretinism. While the authors had not examined the original skeletons, and their research was at best speculative fiction (Brown 2012), they also make claims unrelated cretinism. One of these, is evidence of taurodontism in the LB1 and LB6 teeth which they imagine they can see in an x-ray in a TV documentary.

They state that they used “captured images from X-ray scans presented in'The mystery of the human hobbit' (BBC Horizon, 2005)” to interpret the distinctive crown and root anatomy of the permanent premolars in LB1 and LB6, and determine that they were really deciduous molars (for a rebuttal see Brown 2012). Obendorf et al. (2008) then argue (presumably based on the same x-rays shown on TV), that “significant taurodontism, that is the presence of a substantial neck due to an apical displacement of the bifurcation of the roots, is evident in these and other LB1 teeth. Taurodontism is more pronounced in Australo-Melanesian populations in both deciduous and permanent molars (Rao and Arathi 2006).”

BBC Horizon x-rays of Homo floresiensis
BBC horizon Homo floresiensis LB1 ct reconstruction BBC Horizon LB6 Homo floresiensis x-ray BBC Horizon LB6 Homo floresiensis x-ray root reconstruction
First captured screen image from BBC Horizon documentary. This is a 3D reconstruction of the lower face and teeth of LB1 Homo floresiensis, based on low resolution ct scans. The BBC artists have highlighted the position and rough dimensions of the teeth (first permanent premolar in blue). This is not, and was never intended to be, a precise representation of tooth crown shape and root lengths. It is a piece of artwork. You certainly could not determine if the first permanent premolar, was really a deciduous molar, or if the teeth were taurodont, from this image. Lateral radiograph of the LB6 Homo floresiensis mandible taken in 2005, after it had been badly damaged. Captured screen image from BBC Horizon documentary. As is usual with this type of radiograph, this is a 3D object compressed onto a flat surface. The teeth from the left and right sides of the arch overlap (shadows) and most details of crown, root and pulp cavity shape and size can not be seen. You certainly could not determine if the first permanent premolar, was really a deciduous molar, or if the teeth were taurodont, from this image. Final captured screen image from the BBC Horizon documentary. Only difference is that the BBC have highlighted what they interpret as the root form (paired roots) in one of the first premolars (micro ct's have subsequently demonstrated that while the first premolars have double roots, they are not of equal length, and are of different cross sectional shape).

Firstly, the x-rays do not show evidence of an apical displacement of the root bifurcations. There are three different “X-ray scans” shown in the BBC documentary. The first is a BBC graphic artists reconstruction of premolar root form in LB1. It is based on a very low resolution CT scan and there is no evidence of pulp cavity dimensions or any accurate details of tooth crown and root anatomy. The other x-rays are of the LB6 mandible taken after it was badly damaged at Gadja Mada University in 2004. Due to shadows of overlapping teeth, and the position of the mandible on the x-ray film, no information of pulp cavity and crown and root form is available. The x-ray was only adequate to show that the first premolar had two roots.

Secondly, Obendorf et al. (2008) cited reference does not discuss taurodontism in teeth from Australo-Melanesian populations as they claim. A complete fabrication. In their introduction, Rao and Arathi (2006:42) state that taurodontism “is commonly observed among the Eskimos and Natives of Australia and Central America.[8],[9],[10]” None of the three references they cite provide evidence of taurodontism in Australian Aborigines, or the Australo-Melanesians mentioned by Obendorf et al. (2008). Apart from the brief reference in their introduction there is no further mention of Aboriginal teeth, although they do provide high resolution x-rays of taurodontism in the deciduous and permanent teeth in two of two Indian patients.

8. Dervazeh AM. Prevalence of taurodontism in Jordanian Dental patients. Dento Maxillofac Radiol 1998;27:163-5. 
9. Goz PW, White SC. Oral Radiology (Principle and interpretation), 3rd edn. St.Louis, Missouri: C.V. Mosby Year Book Inc; 1994. 
10. Mac Donald-Jankowski DS, Li TT. Taurodontism in a young adult chinese population. Dento Maxillo Radiol 1993;22:140-4.         

Henneberg et al.  (2014) revisit the subject of taurodontism in H. floresiensis when they attempt to demonstrate that LB1 was a modern human with Down’s Syndrome. They write, “Others (68) (Obendorf et al. 2008) have proposed the presence in LB1 of significant taurodontism; that is, the presence of an enlarged tooth body due to an apical displacement of the root bifurcation, is evident in these and other LB1 teeth.The teeth referred to are identified by Brown and colleagues as first lower premolars (P3s), which Obendorfs group (68) hypothesize are retained first lower deciduous molars (dm1s). Though there is no compelling basis to accept the interpretation of LB1 lower premolars as retained deciduous molars, such an interpretation is a possibility. Irrespective of this interpretation, we regard the presence of some degree of taurodontism in LB1 as sustainable. Its presence is, however, uncertain due to the poor quality of evidence that continues to be provided by Peter Brown and his supporters.”

They have no evidence but think that it is “sustainable”. Weasel words from Maciej Henneberg and Robert Eckhardt where they are implying that taurodontism may be present, as it suits their claim of Down’s Syndrome, while stating that the evidence is uncertain (poor quality evidence provided by Peter Brown), enabling their suggested possibility of tarodontism to be denied if their statement is challenged. A small example of the smoke and mirrors found throughout Henneberg et al. 2014 (see also Maciej Henneberg’s earlier claim about evidence of modern dentistry in LB1 Homo floresiensis).

Henneberg et al. (2014) then discuss the evidence they have seen in relation to taurodontism in LB1 and LB6 Homo floresiensis, taurodontism generally, and taurodontism’s association with several syndromes. They then conclude, “Taurodontism has not been found in dentitions of normal Australomelanesians, despite thorough study of those dentitions nearly a century ago (83). Thus, any presence of taurodontism in LB1 in the small sample from Liang Bua comprising one maxillary and two mandibular dentitions is more likely to be attributable to disrupted development than nonpathological regional variation.”

Here, Henneberg et al. (2014) argue that as taurodontism has not been recorded in Australomelanesians, that any presence in LB1 and LB6 must therefore be the result of a developmental disorder rather than a regional population trait. However, the literature published prior to when the author’s PNAS article was submitted (November 2013) provides absolutely no support for this conclusion. Elvery et al. (1998) x-rayed the teeth of 38 adult adult skeletons excavated from the Broadbeach Aboriginal cemetery (Haglund 1976). Mesotaurodontism was present in over 10% of the molars, with high resolution x-rays published of some teeth (:216), see below.

Broadbech taurodont molars

Broadbeach mandibular teeth

Mandibular molars from Broadbeach 45 and 106. The first molars in both appear to have developed normally, without apical displacement of the root bifurcation. As the taurodont teeth ilustrated in Elvery et al. (1998) don't have identification numbers I don't know which individuals they were from, but the author's have only classified around 10% as being mesotaurodont. X-rays A & B from Elvery et al. (1998:216) illustrating Broadbesch mesotaurodont molars.

I examined all of the Broadbeach skeletons in 1980 (Brown 1989) and no one has ever suggested that skeletal morphology, skeletal and dental dimensions, oral health, mandibular morphology or age at death distribution of these skeletons was anything but normal for an Aboriginal population (Elvery et al. 1998; Freedman and Wood 1977; Haglund 1976; Haglund-Calley 1968a; Haglund-Calley 1968b; Murphy 1978; Smith et al. 1981; Wood 1968). A skeletally relatively large, robust and long-lived sample, not consistent with the characteristics of Down Syndrome or Klinefelter’s Syndrome. Taurodont molar teeth are also relatively common in Aboriginal skeletons from the north coast of NSW, like those from the Moonee Beach midden (see below). Unambiguous evidence that taurodontism was present in at least some normal Australomelanesians, at a relatively high frequency when compared with other human populations.

Aboriginal taurodont molar
Taurodont maxillary molar excavated from the Moonee Beach midden, northern NSW, in the 1970's.

A final comment on the poor scholarship in Henneberg et al. (2014). They state “we regard the presence of some degree of taurodontism in LB1 as sustainable. Its presence is, however, uncertain due to the poor quality of evidence that continues to be provided by Peter Brown and his supporters.”  They seem to have missed, at least for the purposes of their PNAS article, the high resolution micro CT scans of the LB1 molar teeth published by Jungers and Kaifu (2011), see below. Even if enlarged pulp cavities were present, it could have been a species characteristic, as in Neandertals, not evidence of a developmental syndrome.

LB1 Homo floresiensis molar micro ct As detailed in Jungers and Kaifu (2011) this micro ct slice was taken to demonstrate that, contrary to the claims of Henneberg, there as no evidence of modern dental intervention in the crown of LB1's mandibular left first molar. The plane of this ct (longitudinal mesiodistal through the cenrte of the M1) is at an angle to the centre's of the M2, and, to a greater extent, the M3 (see below). As the mandibular roots are oval-shaped in bucco-lingual cross section, the roots of the M2 appear thickened, as they are sectioned at a different angle to the M1. The M3 roots have a similar problem, but the ct section has only captured the edge of the mesial (anterior) root. The most accurate view of the relative proportions of the pulp cavity and position of root bifurcation is for the M1. This is clearly not a taurodont tooth. As discussed by Jungers and Kaifu (2011) there is some sediment in the pulp cavities of M1 and M2.
mand molar root alignment The modern human mandibular dental arch is "U-shaped" and the three molar teeth are not aligned in a straight line. A further complication is the helicoidal plane and Curve of Spee, that results in third molars being tilted lingually relative to the first two molars. A micro ct slice designed to run through the middle of the first molar, will usually only run through the buccal edge of the third molar. Depending upon the shape of the dental arch, and the alignment of the M1 and M2, sections through the M1 and M2 will also not be comparable.

Developmental disorders of the teeth. A slide share presentation.

http://www.slideshare.net/chelseaignacio/developmental-disturbances-of-the-teeth

 

Abnormalities of the pulp. A slide share presentation

http://www.slideshare.net/chelseaignacio/abnormalities-of-the-pulp

References

Bell J, Civil CR, Townsend GC, and Brown RH. 1989. The prevalence of taurodontism in Down's syndrome. Journal of Intellectual Disability Research 33(6):467-476.
Blumberg JE, Hylander WL, and Goepp RA. 1971. Taurodontism: a biometric study. American Journal of Physical Anthropology 34:243-255.
Brown P. 1989. Coobool Creek: A morphological and metrical analysis of the crania, mandibles and dentitions of a prehistoric Australian human population. Canberra: Department of Prehistory, Australian National University. 205 p.
Brown P. 2012. LB1 and LB6 Homo floresiensis are not modern human (Homo sapiens) cretins. J Hum Evol 62:201-224.
Constant DA, and Grine FE. 2001. A review of taurodontism with new data on indigenous southern African populations. Arch Oral Biol 46:1021-1029.
Elvery MW, Savage NW, and Wood WB. 1998. Radiographic Study of the Broadbeach Aboriginal Dentition. Am J Phys Anthropol 107:211-219.
Freedman L, and Wood WB. 1977. Metrical features of Australian Aboriginal crania and mandibles from Broadbeach, south-east Queensland. Arch Phys Anthropol Oceania 12:1-25.
Gage JP. 1978. Taurodontism and enamel hypomaturation associated with X-linked abnormalities. Clinical Genetics 14:159-164.
Gardner DG, and Girgis SS. 1978. Taurodontism, shovel-shaped incisors and the Klinefelter syndrome. Dental Journal 44:372-373.
Goldstein E, and Gottlieb MA. 1973. Taurodontism: familial tendencies demonstrated in eleven of fourteen case reports. Oral Surgery, Oral Medicine and Oral Pathology 36:131-144.
Haglund L. 1976. The Broadbeach Aboriginal burial ground. Brisbane: University of Queensland Press.
Haglund-Calley L. 1968a. The Aboriginal burial ground at Broadbeach, Queensland. Mankind 6:676-680.
Haglund-Calley L. 1968b. The relation between the Broadbeach burials and the cultures of eastern Australia [M.A.]: University of Queensland.
Henneberg M, Eckhardt RB, Chavanaves S, and Hsü KJ. 2014. Evolved developmental homeostasis disturbed in LB1 from Flores, Indonesia, denotes Down syndrome and not diagnostic traits of the invalid species Homo floresiensis. Proceedings of the National Academy of Sciences 111(33):11967-11972.
Jafarzadeh H, Azarpazhooh A, and Mayhall JT. 2008. Taurodontism: a review of the condition and endodontic treatment challenges. International Endodontic Journal 41:375-388.
Jaspers MT. 1981. Taurodontism in the down syndrome. Oral Surgery, Oral Medicine, Oral Pathology 51(6):632-636.
Jaspers MT, and Witkop CJ. 1980. Taurodontism, an isolated trait associated with sydndromes and x-chromosomal aneuploidy. American Journal of Human Genetics 32:396-413.
Jungers WL, and Kaifu Y. 2011. On Dental Wear, Dental Work, and Oral Health in the Type Specimen (LB1) of Homo floresiensis. American  Journal of Physical Anthropology 145:282-289.
Kallay J. 2014. A radiographic study of the Neanderthal teeth from Krapina. In: Brothwell DR, editor. Dental Anthropology: Volume V: Society for the study of human biology: Elsevier. p 75-86.
Llamas R, and Jimenez-Planas A. 1993. Taurodontism in premolars. Oral Surgery, Oral Medicine and Oral Pathology 75:501-505.
Murphy AMC. 1978. The Broadbeach and coastal Adelaide Aboriginal populations: a metrical analysis of the femora and tibiae [MSc Honours]: University of Queensland.
Obendorf PJ, Oxnard CE, and Kefford BJ. 2008. Are the small human-like fossils found on Flores human endemic cretins? Proceedings of the Royal Society of London B: Biological Sciences 275(1640):1287-1296.
Rao A, and Arathi R. 2006. Taurodontism of deciduous and permanent molars. Journal Indian Society of Pedodontics and  Preventive Dentistry 24(1):42-44.
Shaw JC. 1928. Taurodont teeth in South African races. J Anat 62:476-498.
Smith P, Brown T, and Wood WB. 1981. Tooth size and morphology in a recent Australian Aboriginal population from Broadbeach, south-east Queensland. Am J Phys Anthropol 55:423-432.
Weidenreich F. 1937. The dentition of Sinanthropus pekinensis: A comparative odontography of the hominid. Palaeont Sin New Series D No 1:1-180.
Wood WB. 1968. An Aboriginal burial ground at Broadbeach, Queensland: skeletal material. Mankind 6:681-686.
Xing S. 2012. Morphological variation of Zhoukoudian Homo erectus teeth. PhD thesis.Graduate School, Chinese Academy of Sciences.
Xing S, Martino ́n-Torres M, Bermu ́dez de Castro JM, Zhang Y, Fan X, Zheng L, Huang W, and Liu W. 2014. Middle Pleistocene Hominin Teeth from Longtan Cave, Hexian, China. PLOS ONE 9(12):1-38.