Snow monkeys fish in the winter (non-human primates that reside in the coldest habitat)

Main points:

• Generally speaking, monkeys reside in warmer climates on Earth while the Japanese macaques inhabit the coldest places in the world for a non-human primate. The high-altitude area of Kamikochi and Shiga Kogen in Nagano Prefecture can get as low as -20 degrees Celsius in the middle of winter.
• The presence of a Japanese macaque population in a habitat depends on whether or not it can survive the harshest winter season, and the population size is determined by the food resource availability during this critical time.
• A metagenomic analysis ^*1 was conducted to comprehensively examine the DNA of 38 fecal samples of Japanese monkeys in the upper highlands (fecal samples collected to avoid duplication of fecal samples of the same individual) over the three winter seasons of 2017-2019. As a result, the DNA of freshwater fish such as brown trout and aquatic insects was detected in the fecal samples, definitively showing that survival depends on organisms living in rivers as a nutrient source in the midwinter.
• Snow monkeys have not previously been documented to prey on fish that live in rivers, and the fact that aquatic insects are used as food is also directly evidenced by genomic analysis of feces. In addition, research related to the identification of aquatic insect species that are consumed has not been previously achieved.

   

  Background:

  Shinshu University Department of Science

  Professor Koji Tojo’s Lab has conducted fieldwork research in the Kamikochi Azusa River area for 20 years. He had previously observed circumstantial evidence of macaque groups gathering aquatic insects by the river in the middle of winter. (Video)

  With this background, Professor Alexander Milner of the University of Birmingham in the UK, who was a recipient of the JSPS Invitation Program for Overseas Researchers, came to Shinshu University for one year to conduct joint research in the field of ecology of mountain streams in Kamikochi. During this period, Prof. Milner also served as a special-appointment Professor at the Institute of Mountain Science, Shinshu University. In addition, Dr. Catherine Docherty, who obtained her Ph.D working in Greenland from Prof. Milner's laboratory, also joined the faculty at Shinshu University for two years as a specially-appointed Assistant Professor of the Institute of Mountain Science.

  Dr. Masaki Takenaka, who was a graduate student at Shinshu University at the time (and is now a specially appointed Assistant Professor at the University of Tsukuba), and others joined the research team to conduct collaborative research in Kamikochi. The group began a DNA metabarcoding analysis from fecal samples of Japanese macaques to elucidate their feeding habits in the severe winter months.

  A total of 38 fecal samples were collected during the three winter seasons of 2017 to 2019 by changing the sampling location and date to avoid duplicate analysis of fecal samples from the same individual and on the same day. The metagenomic analysis method using a next-generation sequencer^*2 was applied to a total of 38 feces samples collected at different sampling locations and on different sampling dates. Cawthron Institute of New Zealand was in charge of the metagenomic analysis using the next-generation sequencer, and Shinshu University and the University of Tsukuba were in charge of the analysis of DNA barcode regions in aquatic organisms inhabiting the Kamikochi region.

   

  Results and Discussion:

  DNA fragments of fish, aquatic insects, crustaceans, and mollusks were detected in all 38 fecal samples. Some of the DNA fragments were from animals considered to be of terrestrial origin (terrestrial shellfish and soil insects), but most of the DNA fragments were from aquatic animals that live in freshwater. DNA of arthropods (aquatic insects and aquatic crustaceans) was detected in about half of the feces samples (18/38 samples) (pond snails, garganeys, and chironomids). DNA of salmonids was detected in less than 20% of the fecal samples (7/38 samples), and DNA of freshwater mollusks (2 species) was detected in about 1/4 of the fecal samples (6/38 samples) (Fig. 3).

  In other words, it was scientifically proven that the behavior of Japanese macaques in Kamikochi, which had previously been circumstantially observed as displaying fishing, was actually feeding on aquatic insects and aquatic molluscs living in rivers. The nutritional value of these insects is extremely high compared to that of grass and tree bark, and the fact that aquatic insect DNA was consistently detected in samples from multiple individuals and multiple collection dates over multiple winter seasons is considered to be a characteristic of a stable diet of aquatic insects and mollusks by Japanese macaques in winter.

  Prof. Milner states, “Japanese macaques have a wider winter home range when food resources are scarce, but Kamikochi lies in a deep valley where they cannot cross the mountains. Population density is exceptionally high and macaques must overwinter in an extremely harsh environment. These larger populations create additional stress for surviving winter, but an abundance of groundwater upwellings and hot spring inputs from active volcanoes ensures many streams flow without ice cover allowing easy access to the monkeys. With high numbers of freshwater animals in its rivers and streams, the Kamikochi area may be the only environment in Japan where the topographical, geological, and meteorological conditions allow Japanese macaques to supplement their winter diet in this way.”

  The detection of salmonid DNA in multiple fecal samples from multiple collection dates during the winter of 2018 and 2019 was an unexpected result for the research team, but it is highly likely that the fish are consistently used as a food resource, rather than accidentally feeding on dead fish. It is highly likely that they are consistently using the fish as a food resource. However, this is the first case in the world where Japanese macaques have been documented to feed on fish under natural conditions.

  Although many groups of Japanese macaques are known in other regions, their behavior of feeding on aquatic insects and fishes may be a unique feature of Kamikochi and the surrounding areas. During the winter in Kamikochi, the water level of the Azusa River falls and the flow rate of surface water is greatly reduced. Many of the small streams that flow into the Azusa River originate from springs, and they flow gently through the relatively flat basin. The water temperature in the streams with a high proportion of spring water is stable at about 5-6℃ in winter and all year round. The topography and hydrological environment of the Kamikochi area, with its abundance of springs, is thought to be closely related to the unique behavior, foraging behavior, and ecology of these Japanese macaques. The macaques feed on aquatic insects in the river because the insects are at the larval stage during the winter and not as adults.

   

  Implications and Future Plans:

  The results of this study provide insight into the unique wintering strategy of the Japanese macaque population in the Kamikochi region, which lives in one of the harshest environments in the world (Fig. 4). The dependence on riverine aquatic organisms as a food resource is a unique trait that has not been considered in the behavior and ecology of monkeys in general. Furthermore, the results of fish predation were surprising. Orangutans have been reported to capture and prey on freshwater fish, but this is the first time that this behavior has been observed in monkeys. However, how do Japanese macaques capture salmonids? This has yet to be observed and is a subject of study in the future.

  Prof. Tojo states, “In the book Zoku: Kari no Kataribe by Yoshio Matsuyama published in 1977 there are observations made by the people of Ina Valley where a groups of monkeys carry stones to divert the flow of the river in order to catch aquatic insects and fish. Our study began with the desire to research these stories scientifically.”

   

  Glossary:

  ^*1 Metagenomic Analysis

  The term "meta" in metagenomic analysis was coined by combining "meta-" meaning "transcendence" and "genome". In this study, metagenomic analysis refers to the exhaustive analysis of genomic DNA from food resources contained in the feces of Japanese macaques by extracting, purifying, and directly sequencing the DNA. The term "comprehensive" here refers to the extraction of multiple animal-derived DNAs in the feces sample in a mixed state and the decoding of the obtained sequence fragment data. This is an attempt to identify the DNA of food resources contained in the feces samples (DNA barcoding) by referring to the sequence data registered in GenBank and the genetic information of aquatic insects inhabiting rivers collected in the upper highlands against the sequence data obtained in this way.

  ^*2 Next-generation sequencers

  Next-generation sequencing (NGS) is a technology that enables the simultaneous sequencing of thousands to millions of DNA molecules, including sequences derived from multiple species and individuals, and the equipment that makes such analysis possible is called a next-generation sequencer.

   

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  Title of paper and Authors:

  Title: Winter diet of Japanese macaques from Chubu Sangaku National Park, Japan incorporates freshwater biota

  Author : Alexander M. MILNER, Susanna A. WOOD, Catherine DOCHERTY, Laura BIESSY, Masaki TAKENAKA, Koji TOJO

  Journal : Scientific Reports

  URL: https:// www.nature.com/articles/s41598-021-01972-2

  DOI: 10.1038/s41598-021-01972-2

   

  Alexander M. Milner (Shinshu University, University of Birmingham) First Author.

  Susanna A. Wood (Cawthron Institute)

  Catherine Docherty (Shinshu University, University of Birmingham)

  Laura Biessy (Cawthron Institute)

  Masaki Takenaka (Tsukuba University)

  Koji Tojo (Shinshu University)

  For more information please contact the corresponding author:

  Professor Koji Tojo, Shinshu University

  E-mail：ktojo@shinshu-u.ac.jp