Geophagy among nonhuman primates: A systematic review of current knowledge and suggestions for future directions

Abstract

ObjectivesGeophagy, the intentional consumption of earth, is widely practiced among humans and other mammals, but its causes are not well understood. Given the growing number of reports of geophagy among nonhuman primates (NHP), we sought to (1) advance and codify our understanding of the patterns and functional and evolutionary significance of geophagy among NHP and (2) provide a research agenda for a more unified approach to its study.MethodsWe systematically reviewed all available literature on NHP geophagy, extracted available data on taxa, geography, climate, diet, sex, age‐class, reproductive status, and the characteristics of the earth. We used these data to evaluate three major hypotheses about geophagy, that it is protective, provides mineral supplementation, and is nonadaptive.ResultsWe identified 287 accounts of geophagy among 136 species, adding 79 new primate species to the list of those considered in prior reviews. Nineteen percent of species were in the suborder Strepsirrhini, while 81% were in the suborder Haplorrhini. There were reports of geophagy from 9 of the 17 families and 39 of the 76 genera currently recognized by the International Union for Conservation of Nature.DiscussionThe limited evidence suggests that geophagy is adaptive, and provides protection and mineral supplementation. We specify the behavioral, dietary, and soil data required to more rigorously investigate these hypotheses across representative species of all taxonomic groups, geographical regions, and dietary classification. Given the plausibility of geophagy for maintaining the health of both wild and captive populations, we urge further study and conservation of geophagy sites.

Possible mineral contributions to the diet and health of wild chimpanzees in three East African forests

“…Some bird and mammalian species, including elephants, macaques, tamarins, gorillas, chimpanzees, and humans (Wilson ), consume soil of a variety of kinds, often in the form of clay. Geophagy is widespread and has been observed on all continents inhabited by humans and nonhuman primates (Pebsworth, Huffman, Lambert, & Young, ), with archeological evidence suggesting its practice to be as old as 2 million years (Clark, ). Though the most prominent causes of geophagy remain unclear (Pebsworth et al, ), the practice of geophagy increases micronutrient intake, which may have nutritional value, and other benefits such as the detoxification of harmful compounds such as alkaloids in the diet (Klaus, Klaus‐Hugi, & Schmid, ), protection against infection by parasites and pathogens (Knezevich ), and alleviation of gastro‐intestinal upsets (Mahaney, Hancock, Aufreiter, & Huffman, ; Young ).…”

“…Geophagy is widespread and has been observed on all continents inhabited by humans and nonhuman primates (Pebsworth, Huffman, Lambert, & Young, ), with archeological evidence suggesting its practice to be as old as 2 million years (Clark, ). Though the most prominent causes of geophagy remain unclear (Pebsworth et al, ), the practice of geophagy increases micronutrient intake, which may have nutritional value, and other benefits such as the detoxification of harmful compounds such as alkaloids in the diet (Klaus, Klaus‐Hugi, & Schmid, ), protection against infection by parasites and pathogens (Knezevich ), and alleviation of gastro‐intestinal upsets (Mahaney, Hancock, Aufreiter, & Huffman, ; Young ). As pointed out by Pebsworth et al (), in a review of the literature in this field, the total elemental composition of soil may not reflect the amount of minerals available for the consumer, and in vitro studies are needed to determine bioavailability of mineral elements eaten in the course of geophagy (Pebsworth et al, ; Seim et al, ; Wilson ).…”

“…Though the most prominent causes of geophagy remain unclear (Pebsworth et al, ), the practice of geophagy increases micronutrient intake, which may have nutritional value, and other benefits such as the detoxification of harmful compounds such as alkaloids in the diet (Klaus, Klaus‐Hugi, & Schmid, ), protection against infection by parasites and pathogens (Knezevich ), and alleviation of gastro‐intestinal upsets (Mahaney, Hancock, Aufreiter, & Huffman, ; Young ). As pointed out by Pebsworth et al (), in a review of the literature in this field, the total elemental composition of soil may not reflect the amount of minerals available for the consumer, and in vitro studies are needed to determine bioavailability of mineral elements eaten in the course of geophagy (Pebsworth et al, ; Seim et al, ; Wilson ). Probably no single characteristic of soils eaten by animals, including humans, can account for their consumption (Abrahams, ; Wilson, ; Young, Sherman, Lucks, & Pelto, ), with mineral supplementation, medical, and detoxification functions all playing a part (Aufreiter et al, ; Aufreiter, Hancock, Mahaney, Strambolic‐Robb, & Sanmagudas, ; Ketch, Malloch, Mahaney, & Huffman, ; Mahaney, ; Mahaney et al, ; Pebsworth et al, ; Vermeer & Ferrell, ; Wilson, ; Young ).…”

“…As pointed out by Pebsworth et al (), in a review of the literature in this field, the total elemental composition of soil may not reflect the amount of minerals available for the consumer, and in vitro studies are needed to determine bioavailability of mineral elements eaten in the course of geophagy (Pebsworth et al, ; Seim et al, ; Wilson ). Probably no single characteristic of soils eaten by animals, including humans, can account for their consumption (Abrahams, ; Wilson, ; Young, Sherman, Lucks, & Pelto, ), with mineral supplementation, medical, and detoxification functions all playing a part (Aufreiter et al, ; Aufreiter, Hancock, Mahaney, Strambolic‐Robb, & Sanmagudas, ; Ketch, Malloch, Mahaney, & Huffman, ; Mahaney, ; Mahaney et al, ; Pebsworth et al, ; Vermeer & Ferrell, ; Wilson, ; Young ). Furthermore, geophagy may not always be beneficial as soil may contain soil‐transmitted helminths, heavy metals, and increase the risk of predation (Link, de Luna, Arango, & Diaz, ; Matsubayashi et al, ., Pebsworth, Archer, Appleton, & Huffman, ).…”

Assessing the function of geophagy in a Malagasy rain forest lemur

“…Among wild primates, geophagy has been well‐studied in Neotropical primates (Ferrari, Veiga & Urbani, ; Izawa, ), Old World monkeys (Mahaney, Milner & Sanmugadas, ; Oates, ; Wakibara et al., ), and great apes (Mahaney, Hancock, Aufreiter & Huffman, ; Mahaney, Hancock, Aufreiter, Milner & Voros, ; Mahaney, Watts & Hancock, ), but remains poorly studied in Madagascar's lemurs (but see Ganzhorn, ; Norscia, Carrai, Ceccanti & Borgognini Tarli, ; Semel, ). A recent review on primate geophagy by Pebsworth, Huffman, Lambert and Young () found 44 studies describing lemur geophagy, of which only five directly analyzed consumed soils. While most researchers agree that geophagy is typically an adaptive behavior, causes for geophagy remain poorly understood (Krishnamani & Mahaney, ; Pebsworth et al., ).…”