UC Berkeley

Alcohol, specifically ethanol, is estimated to have been consumed by 46% of the world’s population above the age of 15 in 2019. Human societies have been intentionally brewing alcohol for consumption for at least 9,000 years, likely longer. Why are humans so attracted to ethanol consumption? Is it merely the result of a happy biochemical accident? Or could there be an evolutionary explanation? The "drunken monkey" hypothesis points out that the ancestors of humans were frugivorous for tens of millions of years and predicts that the fruits they ate underwent microbial fermentation resulting in the accumulation of ethanol. Olfaction of fruit ethanol by foraging animals may facilitate the localization of fruit crops and indicate the suitability of individual fruits for consumption. The ingestion of fruit ethanol may itself provide beneficial services such as appetite stimulation. Physiological tolerance of increasingly ethanolic fruits by primates and other animals may therefore have been adaptive over evolutionary time. The "drunken monkey" hypothesis thus receives its name from the prediction that an evolutionary bottleneck resulted in a period when intoxication was a dietary tradeoff for survival among our as yet ethanol-naive ancestors. Such a mismatch can be seen among the contemporary well-studied alcohol drinking habits of the vervet monkeys on the island of St. Kitt’s in the Caribbean, which are exposed to highly concentrated cocktails left by tourists, and which are frequently observed to be visibly intoxicated. Thus, the "drunken monkey" hypothesis suggests that the contemporary human propensity for alcohol is the result of our evolutionary heritage of chronic fruit consumption. This dissertation began with the aim of collecting basic empirical fruit alcohol data to test the "drunken monkey" hypothesis, by estimating whether the fruits consumed by wild chimpanzees today contain ethanol in sufficient concentrations to amount to a physiologically relevant dosage. I was then also able to collect direct physiological evidence in support of this hypothesis, by measuring a liver metabolite of ethanol (ethyl glucuronide) in the urine of chimpanzees. Chimpanzees were chosen as the study subject for the first two chapters because they, along with bonobos, are the closest living relatives to humans, and thus their ethanol-related physiology is the most likely to correspond to that of our ancestors who lived a similar forest-dwelling lifestyle. The third chapter consists largely of a broad multispecies survey of floral nectar ethanol in the university’s botanical garden. I used published studies to determine the pollinator associated with each species of flower in its native range. I then found studies the on the field metabolic rate of some of those pollinators, and estimated the ethanol dosage that they would consume on an average day of foraging. This third chapter is what broadens the scope of the dissertation beyond testing the "drunken monkey" hypothesis towards the search of a broader wild fermentation ecology. Chapter 1 shows that chimpanzee-consumed fruits at two field sites contained ~0.3% ethanol, and that the average daily rate of fruit consumption of wild chimpanzees equates to ~14 grams of pure ethanol, or the equivalent to 1–2 standard drinks per day by human standards. Three distinct methods of ethanol assay were used in this chapter, two that measured the concentration of ethanol in the headspace of fruit pulp, and one method that detected ethanol in centrifuged fruit juice by changing its color with chemical reagents. This chapter was published in the journal Science Advances. Chapter 2 shows that the majority of chimpanzees whose urine was sampled passed a concentration threshold of 500 ng/mL ethyl glucuronide, indicating a daily consumption of at least 1–2 standard drinks as evidenced by human studies. The method consists of applying a few drops of chimpanzee urine to a lateral flow dipstick immunoassay similar to a pregnancy test, offering a cheap field-portable method for estimating the relative exposure of wild animals to ethanol in lieu of a breathalyzer. This method is well suited for dietary studies because it reflects alcohol consumed over a period of 24–48 hours as the metabolite accumulates in the bladder. This chapter was published in the journal Biology Letters. Chapter 3 shows that ethanol can be found across many species of flowers and in a high percentage of samples. The ethanol concentrations appear low, on the order of 0.02%, but given the large daily volume of nectar that pollinators such as hummingbirds consume, as much as 192% of their body mass, this adds up to a physiological dosage equivalent to 1–2 standard drinks per day by human standards. The method used was an exceptionally sensitive enzyme-based assay kit. This chapter was published in the journal Royal Society Open Science. This dissertation offers an empirical foundation for the continuing study of wild fermentation ecology. There is no longer any ambiguity that fruit- and nectar-feeding animals are chronically exposed to low concentrations of ethanol. It remains to be shown whether or not seed dispersers and pollinators actively prefer ethanol or are simply unable to avoid it. Future studies should match fruit/nectar ethanol data with more direct observations of the microbial community and its effects on animal foraging decisions. While the microbial ecology of floral nectar has been relatively well documented, the microbial community ecology of fruit pulp remains virtually unstudied in the wild. The next logical step is to describe the microbial community assembly underpinning wild fruit and nectar fermentation, which is crucial for a complete understanding of the dietary ecology of fruit and nectar eaters, including that of our own species. The raw data for each chapter can be found in the supplementary materials of its respective open access publication.