Elsevier

Quaternary International

Volume 563, 20 October 2020, Pages 38-50
Quaternary International

Linear enamel hypoplasia in large-bodied mammals of Pleistocene northern Vietnam, with a special focus on Pongo

https://doi.org/10.1016/j.quaint.2020.07.013Get rights and content

Abstract

The Coc Muoi fauna provides a good example of the type of tropical mammalian communities that existed in northern Vietnam during the late Middle Pleistocene. The first results of the analysis of hypoplasia indicated that rhinoceroses and wild cattle were exposed to multiple physiological and psychological stress events specific to age [Bacon et al., 2018. A rhinocerotid-dominated megafauna at the MIS 6-5 transition: The late Middle Pleistocene Coc Muoi assemblage, Lang Son province, Vietnam. Quat. Sci. Rev. 186, 123–141].

In this paper, we aim to supplement the study of hypoplasia in the orangutans (Pongo) from Coc Muoi and, more widely, from different Pleistocene faunas. To address this issue, we conducted a macroscopic analysis of linear enamel hypoplasia [LEH] on Pongo from three collections: Coc Muoi (148–117 ka), Duoi U'Oi (70–60 ka), and Tham Khuyen (>475 ka).

Such comparative analysis based on isolated teeth is constrained by numerous biases including: the small datasets; the differential representation of tooth types; the difficulty in distinguishing first from second molars; the small number of individuals [MNI]; the differential representation of males versus females. The data analysis has been divided into two parts: (1) an analysis of the frequency and expression of LEH on incisors, premolars, and molars (three sites), and (2) an analysis of the frequency and expression of LEH on a set of canines (Tham Khuyen). We used a reference sample composed of 17 adult and 10 immature Pongo individuals to determine the age range of fossil Pongo individuals, at the time of the defects.

Results show that hypoplasia was a common phenomenon in Pleistocene Pongo: two individuals at Coc Muoi; 2 out of 3 individuals at Duoi U’Oi; and 4 out of 6 individuals at Tham Khuyen. They experienced multiple stresses between ~2 and 5 years of age, a period of great vulnerability for immature individuals. The occurrence of accentuated lines of hypoplasia on canine crowns of Tham Khuyen suggests a greater intensity of the stressor, in a time range consistent with the long dietary and behavioral transition of the weaning. In terms of paleoecology, Pleistocene orangutans from the Asian mainland could survive in different environmental conditions than those they occupy today. Various sources (archaeozoology, geological context, and ecology of wild populations), suggest that they might have been larger apes than extant orangutans, living in limestone forests on hills and tower karsts.

Introduction

The Coc Muoi fauna documents a terrestrial ecosystem supporting megaherbivores in northern Vietnam, during the late Middle Pleistocene. The mammal assemblage has been constrained by age estimates obtained from the dating of fossiliferous breccia deposition in the cave site (Optically stimulated luminescence [OSL] and post-IR IR-stimulated luminescence [pIR-IRSL]), which produce an age range within a 1 σ confidence interval of 148 - 117 ka (Bacon et al., 2018a). The faunal analysis of the assemblage revealed the exceptional predominance of rhinoceroses (especially Rhinoceros sondaicus) amongst other large-bodied mammals (tapirs, wild cattle, elephants and stegodons). At that time, Indochinese mammalian guilds were also shaped by the presence of various herbivores and omnivores (muntjacs, sambar deer, medium-sized cervids, medium-sized bovids, porcupines, wild pigs, pandas, bears, macaques, and orangutans), and carnivores (tigers, leopards, and dholes), as the composition of the Coc Muoi fauna shows. In the first analysis of the fauna (Bacon et al., 2018a), we conducted a study of the prevalence of linear enamel hypoplasia [LEH] on the teeth of rhinocerotids (R. sondaicus, R. cf. unicornis, Dicerorhinus sumatrensis), bovids (Bos cf. sauveli), and tapirids (Tapirus indicus, Megatapirus augustus), to assess their health status during the first years of growth, in comparison with the prevalence estimated on the same taxa from some other Late Pleistocene Indochinese faunas (Tam Hang and Nam Lot in Laos; and Duoi U'Oi in Vietnam).

Dental enamel hypoplasias are deficiencies in enamel thickness resulting from physiological perturbations (stress) during the secretory phase of amelogenesis (Goodman and Rose, 1990: p.59). It is a common phenomenon in natural populations of large mammals. Large-bodied mammals are characterized by slow life-histories and a sensitivity to environmental stressors and, in these animals, hypoplasia is mostly caused by undernutrition and disease. Hypoplasia is particularly exacerbated when physiological stresses occur during key-events of development and growth (Hillson and Bond, 1997; Hillson, 2005; Dobney and Ervynck, 1998, 2000; Dirks et al., 2002, 2010; Niven et al., 2004; Franz-Odendaal, 2004; Skinner et al., 2012; Skinner and Skinner, 2017). In relation to large ungulates (rhinocerotids and bovids) of the Indochinese fossil sites, the results showed that hypoplasia is associated with physiological stresses specific to perinatal events, weaning, abandonment of calf and sexual maturity. In tapirids, no hypoplastic defects were observed (Bacon et al., 2018a). The prevalence and expression of hypoplasia remain however widely underexplored in fossil mammals from the region.

Like these large-bodied ungulates, orangutans (Pongo) have a particularly long period of immaturity in conjunction with long periods of crown formation (Guatelli-Steinberg, 2001). They are, together with gorillas, the most dimorphic apes in terms of body mass, with the mean weight of males (~78 kg) more than twice that of females (~35 kg) (Smith and Jungers, 1997). In the wild, infants remain dependent on their mothers for at least 6 years, and they reach sexual maturity between 11 and 15 years of age. Pongo species are distinguished particularly by a gradual weaning process and the late full independence of juveniles, which make them vulnerable throughout their period of development (Galdikas and Wood, 1990; Delgado and van Schaik, 2000; Jablonski et al., 2000; Knott, 2001; Wich et al., 2004, 2009; van Noordwijk and van Schaik, 2005).

Studies show that, among wild populations of great apes, there is a great interspecific variability, but it should be noted that the analyses are based on different sample sizes, and different methods of recording LEH-affected individuals (Guatelli-Steinberg et al., 2012, Table 1). Orangutans (Pongo abelii and P. pygmaeus) have the highest prevalence of hypoplasia, with ~79–100% of individuals (Guatelli-Steinberg, 2000; Hannibal and Guatelli-Steinberg, 2005; Guatelli-Steinberg et al., 2012). Proportions vary significantly between Gorilla species, with ~5.3–11% (G. beringei), ~39–95% (G. gorilla), ~75% (G. grauei), and between Pan species but to a lesser extent, with ~69.7–95.7% (P. troglodytes) and ~95.7–98% (P. paniscus) (Skinner, 1986a; Eckhardt, 1992; Stottlemire, 1998; Guatelli-Steinberg, 2000; Hürner and Vercauteren, 2003; Hannibal and Guatelli-Steinberg, 2005; Guatelli-Steinberg et al., 2012). All three taxa show the repetitive occurrence of LEH marks on incisors and canines, suggesting repeated stress events, but they differ in the mean number of recorded episodes, with ranges from 4.5 to 7.4 in Pongo, 3.1–4.7 in Pan, and 0.1–5.4 in Gorilla (Guatelli-Steinberg et al., 2012). An array of factors have been explored to attempt to explain the significance of these differences between great apes: biological factors such as enamel formation time, the level of abrasion of the surface of dental crowns, the angles between striae of Retzius and the enamel surface (Hannibal and Guatelli-Steinberg, 2005; Guatelli-Steinberg et al., 2012), or ecological factors related to the environmental context such as habitat, climate and seasonality, or again related to food availability, particularly the abundance of fruit (versus leaves) in ape diets. Overall, studies indicate that linear enamel hypoplasia is most likely influenced by a complex combination of factors (Dean, 2010), and that there is evidently a great variability in the way individuals feel stress.

In relation to wild populations of orangutans, it has been proposed that marked repetitive sequences of linear hypoplasia might be explained by a significant stressor, with an average periodicity of six months (or a multiple of six months), lasting 6–8 weeks. The nature of this stressor, however, remains unknown, although it has been suggested that seasonal changes are deeply involved (Skinner, 2000; Skinner and Hopwood, 2004; Skinner and Skinner, 2017). Temperature and humidity greatly influence the degree of virulence of parasites responsible for diseases and malnutrition in immature individuals, but some other factors may be important: the density of animals, which increases infection rates (Foitová et al., 2009), genetics (Goodman and Rose, 1990; Miles and Grigson, 2003), and annual or supra-annual variation in fruit cycling (Knott, 1998).

In this paper, we present the results of a macroscopic analysis of enamel hypoplastic defects in three fossil collections of Pongo teeth: the late Middle Pleistocene Coc Muoi Pongo cf. devosi (148–117 ka; Bacon et al., 2018a); the Late Pleistocene Duoi U'Oi P. pygmaeus (70–60 ka; Bacon et al., 2008, 2015, 2018b). The Middle Pleistocene Tham Khuyen series of isolated teeth have been allocated to various species, P. pygmaeus (Cuong, 1985), P. pygmaeus and P. hooijeri (Schwartz et al., 1995), or P. weidenreichi (Harrison et al., 2014), the age of which is however not precisely known (>475 ka; Ciochon et al., 1996). Despite multiple biases due to the nature of the fossil collections, our analysis seeks to test whether the Pleistocene Pongo experienced a level of developmental stress comparable to that of infants and juveniles (weaned immature individuals) from extant orangutan populations. Finally, the analysis of hypoplasia in the Coc Muoi large-bodied mammals, allows us to highlight the health status and level of stress of components of a late Middle Pleistocene fauna in a tropical ecosystem.

Section snippets

Dating and faunal context

Both faunal assemblages, almost essentially composed of isolated teeth of medium- to large-sized mammals, were recovered from karstic breccias in cave sites in northern Vietnam (Fig. 1SI). Their analysis revealed that they share comparable taphonomic pathways, due to the action of biotic (bone accumulator, either rodents or carnivores) and abiotic (water flows) agents, through processes of deposition (Bacon et al., 2015, 2018a).

Duoi U'Oi yielded 871 teeth (NISP), representing a fully modern

Material

We used a sample of seventeen adult individuals (twelve males, four females, and one of unknown sex), to assess the prevalence of hypoplasia and its range of expression on the permanent teeth of recent orangutans. Ten additional immature individuals (four males, one female, and five of unknown sex) with full deciduous dentition and erupted M1/m1 were also selected to evaluate the prevalence of defects on deciduous teeth and the first permanent molars. Within this overall sample, sixteen adult

LEH prevalence on Pongo milk teeth

The observation on recent immature individuals (N = 10) having complete deciduous dentition and permanent M1/m1, shows the low prevalence of hypoplasia on milk teeth. Only one (out of 10 individuals) has affected milk dentition. In this individual, one LEH defect is located on the basal third of M1/m1, and another one is visible as a thin depression of enamel on the mid-portion of deciduous canines (in a second individual, one defect is also located on the basal third of M1/m1, and there is no

Hypoplasia and life history

As shown in several publications (Guatelli-Steinberg, 2000; Skinner and Hopwood, 2004; Hannibal and Guatelli-Steinberg, 2005; Guatelli-Steinberg et al., 2012), LEH is a common phenomenon in extant Pongo species (94.1% of individuals in our reference sample, 100% when excluding the zoo-born individual). Although based on small datasets, results on incisors, premolars, and molars show that LEH frequencies have different distributions in each period of development: rare episodes from birth to ~3

Conclusion

In this study, we explored the prevalence and expression (furrow vs line of pits) of linear enamel hypoplasia (LEH) in Pongo from the Middle Pleistocene (Tham Khuyen, Coc Muoi) and the Late Pleistocene (Duoi U'Oi) karstic sites in northern Vietnam.

The results show that the LEH analysis based on isolated teeth is constrained by numerous biases including: the number of teeth; the differential representation of tooth types; the difficulty in distinguishing first from second molars; the small

Declaration of competing interest

I, Anne-Marie Bacon, declares no conflict of interest.

Acknowledgments

We thank all members of the Institute of Archaeology in Hanoi, and particularly Ass. Prof. Nguyen Giang Hai, Director of the Institute, for the agreement to study the Duoi U'Oi and Tham Khuyen collections. We thank also Nong Duc Kien, present Director of the Lang Son Museum, and Nguyen Gia Quyen and the other members of the Lang Son museum, regarding the study of the Coc Muoi collection.

Our thanks also go to Christine Lefèvre, Joséphine Lesur and Aurélie Verguin of the Laboratoire Mammifères et

References (90)

  • N.G. Jablonski et al.

    The influence of life history and diet on the distribution of catarrhine primates during the Pleistocene in eastern Asia

    J. Hum. Evol.

    (2000)
  • D. Li et al.

    The stable isotope record in cervid tooth enamel from Tantang cave, Guangxi: implications for the Quaternary East Asian monsoon

    Quat. Int.

    (2017)
  • L.B. Niven et al.

    An inter-site comparison of enamel hypoplasia in bison: implications for paleoecology and modeling Late Plains Archaic subsistence

    J. Archaeol. Sci.

    (2004)
  • D.J. Reid et al.

    A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes

    J. Hum. Evol.

    (1998)
  • T.M. Smith

    Dental development in living and fossil orangutans

    J. Hum. Evol.

    (2016)
  • R.J. Smith et al.

    Body mass in comparative primatology

    J. Hum. Evol.

    (1997)
  • P. Tafforeau et al.

    Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: potential implications for palaeoenvironmental isotopic studies

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2007)
  • D.M. Waddle et al.

    Sexing isolated hominoid canines with special reference to the Middle Miocene specimens from Paṣalar, Turkey

    J. Hum. Evol.

    (1995)
  • R.L. Anemone et al.

    Dental development of known-age chimpanzees, Pan troglodytes (Primates, Pongidae)

    Am. J. Phys. Anthropol.

    (1991)
  • A.D. Beynon et al.

    Histological study on the chronology of the developing dentition in gorilla and orangutan

    Am. J. Phys. Anthropol.

    (1991)
  • D. Brandon-Jones et al.

    Asian primate classification

    Int. J. Primatol.

    (2004)
  • R.L. Ciochon et al.

    Dated co-occurrence of Homo erectus and gigantopithecus from Tham khuyen cave, Vietnam

    Proc. Natl. Acad. Sci. U.S.A.

    (1996)
  • Nguyen Lan Cuong

    Fossile Menschenfunde aus Nordvietnam

  • M.C. Dean

    Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past

    Phil. Trans. Royal Soc. B.

    (2010)
  • M.C. Dean et al.

    Tooth crown heights, tooth wear, sexual dimorphism and jaw growth in hominoids

    Z. Morphol. Anthropol.

    (1991)
  • M.C. Dean et al.

    Developing pongid dentition and its use for ageing individual crania in comparative cross-sectional growth studies

    Folia Primatol.

    (1981)
  • M.C. Dean et al.

    A longitudinal study of tooth growth in a single individual based on long- and short-period incremental markings in dentine and enamel

    Int. J. Osteoarchaeol.

    (1993)
  • R.A. Delgado et al.

    The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands

    Evol. Anthropol.

    (2000)
  • W. Dirks et al.

    Out of the mouths of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia

    Am. J. Phys. Anthropol.

    (2002)
  • W. Dirks et al.

    The relationships of accentuated lines in enamel to weaning stress in juvenile baboons (Papio hamadryas anubis)

    Folia Primatol.

    (2010)
  • K. Dobney et al.

    A protocol for recording linear enamel hypoplasia on archaeological pig teeth

    Int. J. Osteoarchaeol.

    (1998)
  • R.B. Eckhardt

    The relative body weights of Bornean and Sumatran orangutans

    Am. J. Phys. Anthropol.

    (1975)
  • R.B. Eckhardt

    Tooth crown development: non-human primate perspectives on the interpretation of linear enamel hypoplasia frequencies in present and past hominid populations

  • I. Foitová et al.

    Parasites and their impacts on orangutan health

  • C.M. Francis

    A Field Guide to the Mammals of South-East Asia

    (2008)
  • T. Franz-Odendaal

    Enamel hypoplasia provides insights into the early systemic stress in wild and captive giraffes (Giraffa cameloparalis)

    J. Zool. London

    (2004)
  • T.A. Franz-Odendaal et al.

    Insights from stable light isotopes on enamel defects and weaning in Pliocene herbivores

    J. Bio. Sci.

    (2003)
  • B.M.F. Galdikas et al.

    Birth spacing pattern in human and apes

    Am. J. Phys. Anthropol.

    (1990)
  • J. Goddard

    Age criteria and vital statistics of a black rhinoceros population

    East Afr. Wildl. J.

    (1970)
  • A.H. Goodman et al.

    Factors affecting the distribution of enamel hypoplasias within the human permanent dentition

    Am. J. Phys. Anthropol.

    (1985)
  • A.H. Goodman et al.

    Assessment of systemic physiological perturbations from dental enamel hypoplasias and associated histological structures

    Yearbk. Phys. Anthropol.

    (1990)
  • D. Guatelli-Steinberg

    Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri)

    Am. J. Phys. Anthropol.

    (2000)
  • D. Guatelli-Steinberg

    What can developmental defects of enamel reveal about physiological stress in nonhuman primates?

    Evol. Anthropol.

    (2001)
  • D. Guatelli-Steinberg et al.

    Linear enamel hypoplasia as an indicator of physiological stress in great apes: reviewing the evidence in light of enamel growth variation

    Am. J. Phys. Anthropol.

    (2012)
  • D.L. Hannibal et al.

    Linear Enamel hypoplasia in the great apes: analysis by genus and locality

    Am. J. Phys. Anthropol.

    (2005)
  • View full text