Macroscopic and microscopic analyses of linear enamel hypoplasia in Plio-Pleistocene South African hominins with respect to aspects of enamel development and morphology

This study uses macroscopic and microscopic methods to analyze the expression of linear enamel hypoplasia (LEH) in Plio-Pleistocene South African hominins. LEH is a developmental defect of enamel that is used in many anthropological contexts as a physiological stress indicator. Previous research has not settled the question as to whether differences in LEH expression exist between Paranthropus and Australopithecus and if they exist, to what extent these differences might be explained simply by taxonomic differences in enamel development and morphology rather than by differential stress experience. In this study, the analysis of LEH is conducted with respect to differences between Paranthropus and Australopithecus in aspects of enamel development and morphology that are thought to influence LEH expression. Two factors impacting LEH expression are considered: the duration of enamel formation, and the spacing of perikymata. It is predicted that if the first factor strongly influences the expression of LEH, then there should be fewer defects per tooth in Paranthropus because of its abbreviated crown formation spans (and fast extension rates) relative to Australopithecus. It is also predicted that because Australopithecus has more densely packed perikymata in comparable regions of the crown than Paranthropus, this taxon should, on average, have narrower defects than Paranthropus. To address these questions, 200 Australopithecus and 137 Paranthropus teeth were examined for LEH, and the analysis of defect width with respect to perikymata spacing was conducted on tooth impressions examined under a scanning electron microscope using INCA (Oxford Instruments) measurement software. Data support the first prediction: Australopithecus does have significantly more defects per canine tooth than Paranthropus. Data do not support the second prediction in large part because several Australopithecus specimens have wide groove defects in which perikymata are not visible and enamel is irregular. Such wide grooves are not predicted by perikymata spacing such that alternative explanations, including taxonomic differences in ameloblast sensitivity and the duration/severity of disruptions to enamel growth, must be considered.     

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

Physiological stress, such as malnutrition or illness, can disrupt normal enamel growth, resulting in linear enamel hypoplasias (LEHs). Although ecological factors may contribute to LEH expression, other factors, such as surface abrasion and enamel growth variables, are also likely to be involved. Attention to these other factors is necessary before we can begin to understand what LEH might signify in terms of ecological sources of physiological stress in non-human primates. This study focuses on assessing the contribution of these other factors to variation in LEH expression within and across great ape taxa. Here, we present LEH data from unabraded crown regions in samples of seven great ape species. We analyze these data with respect to lateral enamel formation time and the angles that striae of Retzius make with the enamel surface, as these variables are expected to affect variation in LEH expression. We find that although the duration of enamel formation is associated with sex differences in LEH expression, it is not clearly related to taxonomic variation in LEH expression, and does not explain the low frequency of LEH in mountain gorillas found in this and a previous study. Our data on striae of Retzius angles suggest that these influence LEH expression along the tooth crown and may contribute to the consistently high frequencies of LEH seen in Pongo in this and previous studies. We suggest that future work aimed at understanding species variation in these angles is crucial to evaluating taxonomic patterns of LEH expression in great apes.     

Life history, enamel formation, and linear enamel hypoplasia in the Ceboidea

Linear enamel hypoplasia (LEH), a developmental defect of enamel, increases in frequency from prosimian to monkey to lesser ape to great ape grades (Guatelli-Steinberg 2000 Am. J. Phys. Anthropol. 112:395-410, [2001] Evol. Anthropol. 10:138-151; Newell 1998 Ph.D. dissertation, Temple University). This taxonomic pattern in the distribution of LEH is closely related to maturation length across the primate order (Newell 1998 Ph.D. dissertation, Temple University, 2000 Am. J. Phys. Anthropol. [Suppl.] 30:236). Longer maturation periods are associated with higher LEH frequencies; they appear to provide greater opportunity for defects to form. The present study explores the relationship between maturation length and LEH frequency within the Ceboidea. Because of its prolonged period of growth, Cebus is predicted to manifest LEH at a higher frequency than the more rapidly maturing ceboid genera. To test this hypothesis, two separate researchers (E.A.N. and D.G.-S.) examined LEH in nonoverlapping museum series of ceboids. The results support the hypothesis: in 13 genera (n = 1,276), E.A.N. found that LEH frequencies ranged from 0% in Callicebus, Cebuella, and Saimiri to 20% in Cebus. D.G.-S. found similar frequencies among five genera (n = 107), from 0% in Saimiri to 32% in Cebus. Thus, the broad pattern of LEH distribution evident across major taxonomic groups of primates is repeated within the Ceboidea. We also examined a related hypothesis linking the spacing of perikymata, which is influenced by enamel extension rates (Shellis 1998 J. Hum. Evol. 35:387-400), to LEH. The most likely areas of tooth crowns to exhibit LEH in human teeth are those in which perikymata are most closely spaced (Hillson and Bond 1997 Am. J. Phys. Anthropol. 104:89-103). We hypothesized that the longer-maturing Cebus, with its elevated LEH frequency, will also exhibit more closely spaced perikymata than other ceboids. Analysis of a small microscopic subsample (n = 8) lends limited support to this second hypothesis.     

Relationship of enamel hypoplasia to the pattern of tooth crown growth: A discussion

The defects of enamel hypoplasia can be related to the layered structure of enamel which represents the sequence of development in tooth crowns. From such studies, it is possible to see that furrow-type enamel defects (the most common form of hypoplasia seen with the naked eye) are just the most prominent expression of a continuum which extends ever smaller, down to a microscopic disturbance to a single layer in the crown formation sequence. Furthermore, the progressive decrease in spacing between development layers which occurs down the crown sides, from occlusal to cervical, affects both the prominence and apparent width of the defects. This makes it difficult to use measurements as a means of estimating the duration of the disturbance causing a particular defect. The difficulty is even greater for the less common pitted or exposed-plane-type defects, for which the apparent width bears very little relationship with the duration of the growth disturbance. The defects of enamel hypoplasia can therefore be understood clearly only when examined under the microscope in relation to the structures which mark the development sequence of the tooth crown. Am J Phys Anthropol 104:89–103, 1997. © 1997 Wiley-Liss, Inc.     

Preferential expression of linear enamel hypoplasia on the sectorial premolars of rhesus monkeys (Macaca mulatta)

Three hundred and sixty rhesus macaque specimens at the Caribbean Primate Research Center were examined for evidence of linear enamel hypoplasia (LEH). A previously unreported intertooth pattern in LEH was observed. Defects occur preferentially on the sectorial premolar of both males and females. Relative to other teeth, the sectorial premolar exhibits more prominent defects and is more likely to exhibit multiple defects. This pattern is unlike the human intertooth LEH pattern and unlike patterns previously reported for monkeys and apes. These observations are discussed in the context of factors thought to influence the intertooth distribution of LEH in humans and in nonhuman primates. The authors reject crown height, the timing of crown development, and the duration of crown formation as factors contributing to the observed pattern and favor an explanation involving enamel thickness, perikymata spacing, and/or prism orientation. Am J Phys Anthropol 107:179–186, 1998. © 1998 Wiley-Liss, Inc.     

Meaningful measures of enamel hypoplasia: Prevalence and comparative intensity of developmental stress

Objectives

Developmental stress causing enamel thinning is an important topic in primate biology. Because taxa differ in growth rates and enamel thickness, the goal is to provide a new method allowing direct comparison of prevalence and salience of enamel defects among samples.

Materials and Methods

Casts of ape teeth spanning the Late Pleistocene to Late Miocene from three site areas of increasing seasonality, equator (Sumatra) to 20° (Vietnam) and 25°N latitude (China), were examined for enamel defects among paleo-orangutans (n = 571, 222, respectively) and Lufengpithecus lufengensis (n = 198). Frequency of affected teeth and number of linear enamel hypoplasia were recorded. Defect dimensions were measured with a confocal microscope. Simple prevalence is compared to weighted prevalence (%), calculated by dividing “number of LEH from specific tooth groups” by “specific tooth sample size”; this quantity divided by “tooth-specific years of imbricational enamel formation.” Defect dimensions are reduced to a dimensionless index termed “enamel deficit ratio” through dividing “daily enamel deficit” by “daily secretion rate.”

Results

Weighted prevalence increases to the North, highlighting latitudinal similarities. In contrast, “enamel deficit ratio,” designed to express comparative severity of developmental stress among samples, was least in the high latitude sample and differed little between paleo-orangutan samples.

Discussion

The actual numbers generated are not as important as efficacy of the proposed methods for other taxa. Developmental stress appears least severe in the high latitude (Lufengpithecus) sample but affects a greater proportion, compared to paleo-orangutans. Regardless of findings, the proposed solutions to improve comparability of disparate samples, yield reasonable results.     

Dental microwear and stable isotopes inform the paleoecology of extinct hominins

Determining the diet of an extinct species is paramount in any attempt to reconstruct its paleoecology. Because the distribution and mechanical properties of food items may impact postcranial, cranial, mandibular, and dental morphologies related to their procurement, ingestion, and mastication, these anatomical attributes have been studied intensively. However, while mechanical environments influence skeletal and dental features, it is not clear to what extent they dictate particular morphologies. Although biomechanical explanations have been widely applied to extinct hominins in attempts to retrodict dietary proclivities, morphology may say as much about what they were capable of eating, and perhaps more about phylogenetic history, than about the nature of the diet. Anatomical attributes may establish boundary limits, but direct evidence left by the foods that were actually (rather than hypothetically) consumed is required to reconstruct diet. Dental microwear and the stable light isotope chemistry of tooth enamel provide such evidence, and are especially powerful when used in tandem. We review the foundations for microwear and biogeochemistry in diet reconstruction, and discuss this evidence for six early hominin species (Ardipithecus ramidus, Australopithecus anamensis, Au. afarensis, Au. africanus, Paranthropus robustus, and P. boisei). The dietary signals derived from microwear and isotope chemistry are sometimes at odds with inferences from biomechanical approaches, a potentially disquieting conundrum that is particularly evident for several species.     

Femoral lengths and stature in Plio-Pleistocene hominids

This study reports the femoral lengths of 31 Plio-Pleistocene hominids dated between 3.1 and 0.7 million years ago, and uses those lengths to estimate stature by way of the femur-stature ratio reported by Feldesman et al. (Am. J. Phys. Anthropol. 78:219-220, 1989). By this method the average female Australopithecus afarensis is 105 cm and the average male is 151 cm. The respective values are 115 and 138 cm for A. africanus. As defined by Howell (In VJ Maglio and HBS Cooke (eds): The Evolution of African Mammals. Cambridge: Harvard University Press, 1978) and Johanson et al. (Kirtlandia 28:1-14, 1978), Homo habilis is a sexually dimorphic species, with females standing 118 cm and males 157 cm. Such apparently strong dimorphism may be due to the possibility that there are actually two species of nonrobust hominids between 2 and 1.7 m.y.a. The estimate for the female Australopithecus boisei is 124 cm and for the male, 137 cm, but these estimates are especially difficult to be certain of because there are no femora that can be positively identified as male A. boisei. Australopithecus robustus is estimated to be 110 cm (female) and 132 cm (male). African Homo erectus stood 160 cm (female) and 180 cm (male). From these estimates several generalizations are apparent. First, there is apparently strong sexual dimorphism in stature in A. afarensis and H. habilis, but less in the other species. Second, the "robust" australopithecines were relatively small statured. Third, it is apparently not true that humans have been getting progressively taller throughout their evolutionary history. Some individuals were as tall as modern humans 3 m.y.a., by 2 m.y.a. one individual stood about 173 cm, and by 1.7 m.y.a. a stature of 180+ cm was not uncommon.     

Chimpanzee variation facilitates the interpretation of the incisive suture closure in South African Plio-Pleistocene hominids

For a better understanding of early hominid growth patterns, we need to compare skeletal maturation among humans and chimpanzees. This study provides new data on variation of the incisive suture closure in extant species to facilitate the understanding of growth patterns among South African Plio-Pleistocene hominids. The complete anterior closure of the incisive suture occurs early during human life, mostly before birth. In contrast, in chimpanzees a complete anterior closure occurs mostly after the eruption of either the first permanent molars (pygmy chimpanzees) or the third molars (common chimpanzees). The first aim of this study is to test whether the patterns of closure of both the anterior and palatal components of the incisive suture in chimpanzees accurately mirror their polytypism by investigating 720 museum specimens of known geographical origin. Then we use the data gleaned from the incisive suture closure in chimpanzees to determine whether there are different growth patterns among South African Plio-Pleistocene hominids and to interpret them. Results about the pattern of incisive suture closure are consistent with the differences among chimpanzees as revealed by molecular data. Thus, the variation in chimpanzee patterns of incisive suture closure facilitates the interpretation of morphology in South African fossil hominids. In Australopithecus (Paranthropus) robustus as compared to Australopithecus africanus, the complete anterior closure and, probably, the complete palatal closure of the incisive suture occurs during early life in the same way as they occur in humans. Moreover, the closure pattern observed on Stw 53, a supposed early Homo from Sterkfontein Member 5, is similar to that seen in A. africanus and in chimpanzees. Thus, with respect to the anterior component of the incisive suture, A. africanus and Stw 53 retain the primitive feature for which A. (P.) robustus and Homo share the derived character state. Finally, it is worth noting that the Taung child does not show the robust condition. Am J Phys Anthropol 105:121–135, 1998. © 1998 Wiley-Liss, Inc.     

Viewpoints: Diet and dietary adaptations in early hominins: The hard food perspective

Recent biomechanical analyses examining the feeding adaptations of early hominins have yielded results consistent with the hypothesis that hard foods exerted a selection pressure that influenced the evolution of australopith morphology. However, this hypothesis appears inconsistent with recent reconstructions of early hominin diet based on dental microwear and stable isotopes. Thus, it is likely that either the diets of some australopiths included a high proportion of foods these taxa were poorly adapted to consume (i.e., foods that they would not have processed efficiently), or that aspects of what we thought we knew about the functional morphology of teeth must be wrong. Evaluation of these possibilities requires a recognition that analyses based on microwear, isotopes, finite element modeling, and enamel chips and cracks each test different types of hypotheses and allow different types of inferences. Microwear and isotopic analyses are best suited to reconstructing broad dietary patterns, but are limited in their ability to falsify specific hypotheses about morphological adaptation. Conversely, finite element analysis is a tool for evaluating the mechanical basis of form‐function relationships, but says little about the frequency with which specific behaviors were performed or the particular types of food that were consumed. Enamel chip and crack analyses are means of both reconstructing diet and examining biomechanics. We suggest that current evidence is consistent with the hypothesis that certain derived australopith traits are adaptations for consuming hard foods, but that australopiths had generalized diets that could include high proportions of foods that were both compliant and tough. Am J Phys Anthropol 151:339–355, 2013.© 2013 Wiley Periodicals, Inc.     

On the eruption pattern of the permanent incisors and first permanent molars in Paranthropus

It has been claimed recently that Australopithecus exhibited a pattern of permanent tooth eruption like that of extant great apes, whereas a significantly different pattern was shared by Paranthropus and Homo (Dean, 1985). More particularly, each of the four Paranthropus specimens examined in that study was held to show advanced development and eruption of the permanent incisors relative to the first molar. It is demonstrated here that the eruption sequence that was posited for at least one of these four Paranthropus specimens (SK 61) is clearly erroneous, while the developmental/eruption sequences manifested by the other three specimens would appear to be more ambiguous than was claimed. Another juvenile specimen of Paranthropus (KNM-ER 1820) that was not included in Dean's study also does not necessarily support the eruption pattern that was said to characterize that taxon.     

Viewpoints: Feeding mechanics,diet, and dietary adaptations in early hominins

Inference of feeding adaptation in extinct species is challenging, and reconstructions of the paleobiology of our ancestors have utilized an array of analytical approaches. Comparative anatomy and finite element analysis assist in bracketing the range of capabilities in taxa, while microwear and isotopic analyses give glimpses of individual behavior in the past. These myriad approaches have limitations, but each contributes incrementally toward the recognition of adaptation in the hominin fossil record. Microwear and stable isotope analysis together suggest that australopiths are not united by a single, increasingly specialized dietary adaptation. Their traditional (i.e., morphological) characterization as “nutcrackers” may only apply to a single taxon, Paranthropus robustus. These inferences can be rejected if interpretation of microwear and isotopic data can be shown to be misguided or altogether erroneous. Alternatively, if these sources of inference are valid, it merely indicates that there are phylogenetic and developmental constraints on morphology. Inherently, finite element analysis is limited in its ability to identify adaptation in paleobiological contexts. Its application to the hominin fossil record to date demonstrates only that under similar loading conditions, the form of the stress field in the australopith facial skeleton differs from that in living primates. This observation, by itself, does not reveal feeding adaptation. Ontogenetic studies indicate that functional and evolutionary adaptation need not be conceptually isolated phenomena. Such a perspective helps to inject consideration of mechanobiological principles of bone formation into paleontological inferences. Finite element analysis must employ such principles to become an effective research tool in this context. Am J Phys Anthropol 151:356–371, 2013.© 2013 Wiley Periodicals, Inc.     

Fossil hominin ulnae and the forelimb of Paranthropus

The discovery of Pan in the Middle Pleistocene deposits of the Kapthurin Formation of the Tugen Hills (McBrearty and Jablonski: Nature 437 (2005) 105-108) inspires new interest in the search for other chimpanzee fossils in the East African Rift Valley. Craniodental evidence of an eastward excursion of chimpanzee populations in the Plio-Pleistocene goes undetected in other hominin sites, but one enigmatic postcranial fossil, the Olduvai Hominid 36 ulna, has many chimp-like features. Analyses by Aiello et al. (Aiello et al.: Am J Phys Anthropol 109 (1999) 89-110) reveal that it is similar to extant Pan in some respects, but it also has unique traits not seen in other hominoid species. They refer it to Paranthropus boisei. In this study, we reassess the affinities of OH 36 using a different data set that includes more recently discovered hominin fossils including those attributed to Paranthropus. Despite its superficial resemblance to modern Pan, our results agree with those of Aiello et al. (Aiello et al.: Am J Phys Anthropol 109 (1999) 89-110) that OH 36 is distinctly different from modern chimpanzees. By default, it is reasonable to assign this specimen to P. boisei, but it is not at all similar to other ulnae referred to this genus. Ulnae attributed to Paranthropus from South Africa, Kenya, and Ethiopia are morphologically more heterogeneous than those within species of large-bodied Hominoidea. Although there are many apparent shared derived traits justifying a monophyletic Paranthropus clade, most if not all of these traits are related to a single functional complex (hypermastication) that may have evolved in parallel and thereby constituting a paraphyletic group of species.     

Brief communication: linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta)

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.     

Enamel microstructure of the hominid KB 5223 from Kromdraai, South Africa

The Plio-Pleistocene site of Kromdraai, South Africa, is well known for the recovery of the holotype of Paranthropus robustus, one of nine individual hominids recovered from this site to date. Among the Kromdraai sample, the specimen KB 5223 comprises several isolated deciduous and permanent lower teeth assigned to Paranthropus, the only recognized genus at this site. However, a more recent analysis of this specimen suggested that it should be classified as Homo. The lower right first permanent molar of KB 5223 had been previously sectioned along the tips of the mesial cusps, exposing its enamel microstructure. Previous studies had indicated differences between Homo and Paranthropus at the microstructural level. A portable confocal scanning microscope was used to describe details of the enamel microstructure of the M1 and I1 of this specimen. Angles formed between the striae of Retzius and the enamel dentine junction (EDJ), daily secretion rates in cuspal enamel of the protoconid and metaconid and crown formation time of the RM1 are provided. The number of perikymata on the right I1 was counted. Results indicate that some features recorded in the KB 5223 molar differ from those of Paranthropus. However, the number of perikymata on the I1 is lower than values so far reported for early Homo but similar to Paranthropus. Crown formation time of KB 5223 M1 was markedly lower than mean values of M1 in H. sapiens, but similar to other early hominids. Daily secretion rates in the cuspal enamel of KB 5223 M1 were higher than in modern humans.