Cold Discomfort: A Model to Explain Repetitive Linear Enamel Hypoplasia Among Pan troglodytes and Pan paniscus

Skinner, Mark

doi:10.1007/s10764-021-00206-6

Cited by 8 publications

(18 citation statements)

References 124 publications

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“…Ecological factors such as precipitation, rain, and fruiting patterns significantly influence the health and wellness of wild primates (Skinner, 2021; Skinner & Skinner, 2017). In this study, we examine whether orangutan canines exhibit cyclically occurring markers of physiological stress and, if so, whether any difference in pattern is identifiable between Bornean and Sumatran orangutans.…”

Section: Introductionmentioning

confidence: 99%

“…“Physiological stress” is a non‐specific and ambiguous term often used in anthropological studies (Temple & Goodman, 2014). In the case of developmental defects of enamel, physiological stress events may refer to insults such as illnesses, infections, cold discomfort, maternal separation, and psychological stress, among others (Dirks et al, 2010; 2002; Goodman & Rose, 1990; Guatelli‐Steinberg, 2001; Guatelli‐Steinberg & Benderlioglu, 2006; Guatelli‐Steinberg et al, 2012; Lemmers et al, 2021; Skinner, 2021; Skinner et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…It has been suggested that the seemingly regular timing and frequency of dental defects in nonhuman primates may represent cycles of increased physiological susceptibility related to local environmental factors (Chollet & Teaford, 2010; Hannibal & Guatelli‐Steinberg, 2005; Skinner et al, 2014; Skinner & Hopwood, 2004; Skinner & Pruetz, 2012). Studies have attempted to link developmental defects with environmental and ecological phenomena that occur with a seasonal regularity (e.g., monthly, semi‐annual, annual, or supra‐annual cycles) such as rainy, dry, and cold seasons as well as seasonal food resource depletion (Chollet & Teaford, 2010; Dirks et al, 2002; 2010; Macho et al, 1996; Skinner, 1986, 2014, 2021; Skinner et al, 1995; Skinner & Hopwood, 2004; Smith & Boesch, 2015). Previous studies of Pongo have indicated that Pongo pygmaeus and P. abelii may exhibit different cycle periodicities due to environmental differences between Borneo and Sumatra (Skinner, 2014; Skinner & Hopwood, 2004; Skinner & Skinner, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…LEH were added until there was only one perikyma between the last LEH and the cervix. Thus, inSkinner's (2021) Figure6, all 1000 generated teeth have 1 perikyma between at least one pair of defects. Again, Skinner found that the number of perikymata between LEH differed significantly from randomly generated LEH.Here, a randomly generated sample of the number of perikymata between defects was based on the number of individuals and number of defects per tooth for a particular sex and species.…”

mentioning

confidence: 95%

“…In the present study, the word "cycle" refers to a regular pattern of defect occurrence within an individual; a cycle's "periodicity" refers to cycle duration. Skinner and colleagues (Skinner, 2014(Skinner, , 2021Skinner & Hopwood, 2004) have counted perikymata between sets of adjacent LEH, averaging the time between all defect pairs from multiple individuals. In doing so, they found clusters of six, 12, and 18 months between defects.…”

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confidence: 99%

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Some orangutans acquire enamel defects at regular intervals, but not according to seasonal cycles

O'Hara

McGraw

Guatelli‐Steinberg

2023

American Journal of Biological Anthropology

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Objectives Developmental defects of tooth enamel are associated with systemic physiological stress and have been linked to seasonal environmental factors such as rainfall, temperature, and fruit availability. Here, we evaluate whether linear enamel hypoplasia and accentuated perikymata occur with any cyclicity on lower canines and then whether cycles differ between Bornean and Sumatran orangutans. Materials and Methods Epoxy casts of lower canines from Pongo abelii (n = 14) and P. pygmaeus (n = 33) were evaluated for perikymata and dental enamel defects. Individual developmental sequences (IDSs) were generated for each canine, tracking the position of each defect in the context of continuous perikymata (time). Autocorrelation, a form of time‐series statistical analysis was run for each canine to identify whether any cyclicity of defect expression was discernable. Results Autocorrelation revealed cycles of defect expression within canines, but no common cycle periodicities were identified between individuals of the same species or across species. P. pygmaeus averaged more linear enamel hypoplasia per year than P. abelli, but no other comparisons (number of defects, number of perikymata between defects, and autocorrelation analysis) revealed differences between the species. Discussion Although no common patterns of defect expression were identified within or between P. abelli and P. pygmaeus, the potential for autocorrelation analysis is promising for primatological and paleoanthropological studies of seasonal phenomena.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 95%

mentioning

confidence: 99%

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Some orangutans acquire enamel defects at regular intervals, but not according to seasonal cycles

O'Hara

McGraw

Guatelli‐Steinberg

2023

American Journal of Biological Anthropology

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Revisiting Linear Enamel Hypoplasia in Cayo Santiago Rhesus Macaques (Macaca mulatta): How a Stress Marker Relates to Environment and Maternal Lineage in a Rare Rhesus Colony With Known Life History

Guatelli‐Steinberg,

Watson,

Samuel

et al. 2024

American J Primatol

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Linear enamel hypoplasias (LEHs) are development defects appearing as lines or grooves on enamel surfaces. Forming when physiological stressors disrupt developing teeth, LEHs provide retrospective insight into stress experienced in early development. Here, LEHs in Cayo Santiago rhesus macaques (Macaca mulatta) were observed with respect to decade of birth, whether an individual was transferred from the free‐ranging colony to the captive facility during probable crown formation periods, and matriline of birth. It was hypothesized that later decades would exhibit higher prevalence than earlier decades as climatic conditions in Puerto Rico worsened over time. Transfer was expected to affect LEH formation because the process of transfer, and subsequent restriction to captivity, is thought to be stressful. Matriline membership was hypothesized to relate to LEH formation because there is some evidence of a genetic influence on susceptibility to form LEH and because offspring of matrilines of different dominance ranks are known to experience different levels of aggression. Lower third premolars with minimal enamel surface wear were scored for LEH using a digital microscope, while a follow‐up analysis of the two matrilines with the most extreme differences in LEH frequency was conducted using enamel surface profiles. Results were: (1) individuals born during the 1990s had significantly greater LEH prevalence than those born in the 1960s, (2) transferred individuals exhibited weak evidence of greater LEH prevalence than nontransferred comparison groups, and (3) matrilines did not differ in LEH expression in the initial or follow‐up analysis. Although sample sizes were small for some comparisons, these results suggest that not all decades saw an equal prevalence of LEH, that there might be a small effect of transfer from free‐ranging to captive conditions on LEH prevalence that is difficult to detect, and that the matriline into which an individual is born is not related to LEH expression.

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Potential of Japanese Macaques for Understanding Etiology and Seasonality of Repetitive Linear Enamel Hypoplasia in Nonhuman Primates

Skinner,

Asami,

Skinner

et al. 2024

American J Primatol

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Japanese macaques are ideal to advance understanding of a wide‐spread pattern of recurrent developmental distress in great apes, preserved as repetitive linear enamel hypoplasia (rLEH). Not only are they numerous, unendangered, and well‐studied, but they are distributed from warm‐temperate evergreen habitats in southern Japan to cool‐temperate habitats in the north, where they are adapted behaviorally and phenotypically to winter cold and seasonal undernutrition. We provide a pilot study to determine if enamel hypoplasia exists in Japanese macaques from the north and, if temporal patterns of enamel hypoplasia are consistent with seasonal cold, undernutrition and/or exposure to secondary plant compounds. High‐resolution casts of canine teeth from 15 males obtained from Shimokita Peninsula (latitude 41.3° N) between 2012 and 2014, whose skeletons are curated at the Center for the Evolutionary Origins of Human Behavior, Kyoto University, were imaged by confocal and scanning electron microscopy. Perikymata, the surface expression of regularly deposited imbricational layers of enamel, provide an estimate of time between and within hypoplastic enamel defects. Based on histological sections from five individuals, we determined Retzius periodicity to be 7 days. Evidence for recurrence, duration, and severity of 68 LEH defects was collected from perikymata counts as well as measurements of LEH angle of onset, depth and width. Male canine teeth show four to five recurrent, evenly‐spaced enamel defects per crown with a median of 54.8 (range 18–74) perikymata between defects; lasting on average 8.7 (range 1–20) perikymata. These translate into repetitive developmental distress averaging every 1.05 years, lasting 8.7 weeks, less than local winter foraging conditions (100 days). We conclude that linear enamel hypoplasia recurs circ‐annually among high‐latitude male monkeys from Japan. The triad of cold, hunger and anti‐feedants can be differentiated in future study through recourse to provisioned and un‐provisioned populations throughout the Japanese archipelago.

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Cold Discomfort: A Model to Explain Repetitive Linear Enamel Hypoplasia Among Pan troglodytes and Pan paniscus

Cited by 8 publications

References 124 publications

Some orangutans acquire enamel defects at regular intervals, but not according to seasonal cycles

Some orangutans acquire enamel defects at regular intervals, but not according to seasonal cycles

Revisiting Linear Enamel Hypoplasia in Cayo Santiago Rhesus Macaques (Macaca mulatta): How a Stress Marker Relates to Environment and Maternal Lineage in a Rare Rhesus Colony With Known Life History

Potential of Japanese Macaques for Understanding Etiology and Seasonality of Repetitive Linear Enamel Hypoplasia in Nonhuman Primates

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