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

Abstract

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.