One World, One Health」の概念に基づき、生態系の健
One World, One Health康に着目して、人の健康は全ての生き物や環境の健全性「に よ っ て 支 え て い る の だ と い う こ と を、 改 め て 認 識 し、今後の生き方（ライフスタイル）を模索する。

《主催》日本野生動物医学会《司会／座長》「保全医学と生態系の健康」

村田 浩一氏（日本大学生物資源科学部 教授／よこはま

動物園ズーラシア 園長／日本野生動物医学会 会長）《演者》

予防と治療」「霊長類の自己治療行動 —ハフマン・マイケル氏（京都大学 霊長類研究所 准教授）

津田 良夫氏（国立感染症研究所 昆虫医科学研究室 室長）「蚊が運ぶ病気と生態系の構造」「ダニが語る生物多様性～寄生生物の進化的重要単位の意義～」

五箇 公一氏（独立行政法人 国立環境研究所）

Workshop V
ワークショップ Ⅴ“One World, One Health”
Based on the concept ‘One World, One Health’, we will focus on the health of the ecosystem, reconfirm that ourhealth is supported by the health of all living creatures and the environment of this planet, and identify the ideal‘lifestyle’ for the future.
Organizer: Japanese Society of Zoo and Wildlife Medicine
MC / Chairperson:“Conservation Medicine and Ecological Health”
Koichi MURATA, PhD, Professor, College of Bioresource Sciences, Nihon University,
Director, Zoorasia Yokohama Zoological Gardens
President, Japanese Society of Zoo and Wildlife Medicine
Speakers:“Self-Medication in Primates- Prevention and Cure”
Michael A. HUFFMAN, PhD, Associate Professor, Primate Research Institute, Kyoto University“Structure of Animal Communities and Transmission Dynamics of Mosquito Borne Diseases”
Yoshio TSUDA, Chief, Laboratory of Taxonomy and Ecology, Department of Medical Entomology,
National Institute of Infectious Diseases (NIID)“Mites Talk about Biodiversity – Ecological Significance of Evolutionarily Significant Units in Parasites.”
Koichi GOKA, PhD, Invasive Alien Species Research Team, National Institute for Environmental Studies

2nd Live Love Animals International Conference on Animal Care in Kobe 2012

1

《主催者および座長メッセージ

ORGANIZER & CHAIR MESSAGE》

保全医学と生態系の健康
Conservation Medicine and Ecological Health日本大学 生物資源科学部 教授／よこはま動物園ズーラシア 園長／
日本野生動物医学会 会長・村田 浩一

Koichi MURATA, PhD, Professor, College of Bioresource Sciences, Nihon University,
Director, Zoorasia Yokohama Zoological Gardens
President, Japanese Society of Zoo and Wildlife Medicine

多くの人々は、保全医学（Conservation Medicine）とのために必須となる生物多様性（Biodiversity）の保全いう言葉を初めて耳にするかもしれない。それも当然のである。本学問領域は、健康や医療に関係する学問領域

ことで、本学問領域が産声を上げたのは 1990 年代後半を連携させ、生態学的健康（Ecological Health もしくはであり、初の教科書とも言える会議報告書（“Conservation

Ecohealth）を維持するための学際的で実践的な研究分野

Medicine: Ecological Health in Practice”） が 出 版 さ れと言える。

た の は 2000 年 代 に 入 っ て か ら で あ る（Alonso et al.,

保全医学における感染症対策は、病原体と宿主を取り2002）。しかし、本書の出版が大きな契機となり、保全

巻く有機的および無機的環境の相互関係を理解し、そ医学に関する研究が先進諸国で急速に展開されている。

れらの微妙なバランスで成り立っている生態系を考慮

保全医学は、「ヒトの健康、動物の健康および生態系して図られる。とくに新興感染症（Emerging Infectiousの健康に関わる研究分野を統合する学問領域」と定義さDiseases: EID）については、その原因が野生動物の生息れている（Tabor, 2002）。また、保全医学が目指してい域への人間の侵入であり、そのことから生物多様性のるのは、人間や家畜などの動物を縦割り的に区別した健維持が根源的な発生予防につながることを強く認識し康概念ではなく、それらの相互関係の中で維持される単ている。

一かつ横断的な健康、すなわち “One Health” であり、そMany of you may never have heard the term “Conservation
Medicine.” That is only natural because this field of study
was only born in the late 1990's and the first conference
report, which is referred to as the textbook for this new
discipline ("Conservation Medicine: Ecological Healthin Practice") was only published in this decade (Alonso
et al. 2002). However, inspired by the publication of the
textbook, studies related to Conservation Medicine havebeen evolving rapidly in developed countries.
Conservation Medicine is defined as “a discipline that unites
the fields of human health, animal health and ecosystem
health” (Tabor, 2002). Conservation Medicine is not basedon a health concept that posits human and animal in verticaldivisions. It is aimed at horizontal health that can besustained in interrelationship between humans, animals andthe ecosystem, that is to say, “One Health” and conserving
Biodiversity that is indispensable. This new field of study
can be considered as very pragmatic and interdisciplinary in
the way that it links related health and medical study fields
and helps sustain the Ecological or Eco-Health.

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りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

In Conservation Medicine, countermeasures to control
infectious diseases are designed based on an understandingof organic and inorganic host-pathogen interactions and theecosystem built on their subtle balance.
Emerging Infectious Diseases (EID) are, in particular,caused by human intrusion into the habitats of wild animals
and all the more, for this very reason, conservation of
Biodiversity is strongly recognized as fundamental to theprevention of those diseases.

霊長類の自己治療行動—予防と治療
Self-Medication in Primates- Prevention and Cure
京都大学霊長類研究所 准教授・ハフマン A. マイケル

Michael A. Huffman, PhD, Associate Professor
Primate Research Institute, Kyoto University

チンパンジーを初めとする野生霊長類は日常、栄養価

影響や、感染した際の宿主への反応は、長い進化の過程に富んだ果実や葉、若い芽などを食べるが、それ以外に、で培われてきた産物であることは間違いない。アフリカ

特殊な二次代謝産物を含む多くの植物の部位を食べる。

の大型類人猿についての最近の研究は、偶然ではなく、栄養的には乏しいと考えられるこれらの種あるいは部位薬効を期待してある種の植物を積極的に摂取しているこの非栄養的採食意義に、ここ数年、興味がもたれ、そのとが示唆されている。一方、マハレ山塊国立公園周辺で一つとして薬理的効果が指摘されている。更に、非栄養は、ヒトとチンパンジーでよく似た病徴を示す疾病に対的なある種の植物を食べると、寄生虫感染症の制御や、し、同じ植物を選択することが知られている。この事実

その二次的病徴である腹痛の治癒などに有効であるとすから、両者が系統的にもっとも近縁であるため、又は人る仮説が、アフリカの大型類人猿（チンパンジーとゴリラ）間が伝統的に動物の行動を観察することによって、新し研究により実証されてきている。

い「薬」を得ってきたという２つの説明ができる。

すなわち、東アフリカのチンパンジーにおいて、強烈アフリカの大型類人猿やその他の野生霊長類の自己な苦味をもつ髄部液を摂取し、又は葉をそのまま呑み込治療研究には、ヒト、家畜、飼育動物などの寄生虫感

むといった行動が生態学的・寄生虫学的解析から寄生虫染症を効果的に治療することに対する天然物の有効利

感染症の軽減に役立っていることが知られている。寄生用や新しい治療方法の提供についての期待を抱かせる虫は多くの病気を誘発し、個体それ自身の行動や、繁殖ものである。

能力にも影響を及ぼす。したがって、これらの悪影響を取り除くことは重要である。寄生虫感染症が宿主へ与える

Chimpanzees and other primates eat a variety of nutritious
items including fruits, leaves, young buds on a daily basis.
Besides these items, a number of plant parts containing
peculiar secondary plant compounds are occasionallyeaten. In the recent years, an interest has been shownin understanding the significance of ingesting thesenutritionally deplete plant items. One explanation is thatthese items are used for their pharmacologically active
properties. Strong evidence in support of this hypothesis hascome from research on African great apes (chimpanzees andgorillas) demonstrating anti-parasitic properties and or relief
from parasite related gastro-intestinal upset.
From ecological and parasitological analysis of the behaviorof chimpanzees in East Africa it has been shown that theingestion of extremely bitter juices from the pith of plants
or the swallowing of the rough leaves of other species
plays an important role in the suppression of parasite
infections. Parasites are responsible for a variety of
diseases that directly affect the behavior and reproductive
capacity of animals. Therefore, it is extremely importantthat animals should be able to eliminate parasites. It isevident that the effects caused by parasites on the host, andthe hosts’ responses to infection are the results of a longevolutionary process. Research has also shown that African
great apes do not accidentally ingest these items, but seek
these plants out for the curative properties. Interestingly,
humans and chimpanzees living in and around the Mahale
Mountains National Park of Tanzania select many of thesame medicinal plants for use when suffering from similarailments. From this and other evidence, two explanations
can be given. Firstly, they show similar behaviors because
they are phylogenetically very close and secondly, humans
have traditionally observed the habits of wild animals to
obtain valuable new medicines for their own use.
There is hope that the study of self-medicative behaviors in
the African great apes and other primates in the wild will
provide new methods of healing and new medicinal plants
effective in the treatment of the parasite disease in humans,
livestock and other domestic animals.

2nd Live Love Animals International Conference on Animal Care in Kobe 2012

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蚊が運ぶ病気と生態系の構造
Structure of Animal Communities and Transmission Dynamics of Mosquito Borne
Diseases
国立感染症研究所 昆虫医科学部第一室 室長・津田 良夫

Yoshio TSUDA, Chief, Laboratory of Taxonomy and Ecology, Department of Medical
Entomology, National Institute of Infectious Diseases (NIID)

蚊は生態系の分解者として、また天敵生物の食物源と密度、寿命など）。これらの性質は環境条件に影響される

して生態系を支えているが、他の昆虫にはないユニーク

ため、蚊の病気伝播力も時間的に変動する。蚊がうつすな役割を演じている。蚊は吸血習性を持つことで有名で病気の流行が、特に媒介蚊の吸血パターンに大きく依存ある。わが国には 100 種あまりの蚊が生息しているが、しているという研究例が、いくつか報告されている。

このうち 60 種ほどの蚊が人を吸血する性質を持ってい蚊の吸血パターンと病気流行の関係を考えるとき、蚊ると言われる。人を刺さない蚊の中には、大型の哺乳類が病原体の宿主になる動物から吸血することと、宿主でを好んで吸う種類、野鳥を好んで吸う種類、カエルをはない動物から吸血することを区別することが重要であ吸う種類や、魚を吸う種類なども報告されている。蚊がる。動物群集に病原体の宿主動物が多数含まれるとき、持つユニークな役割は、この吸血習性に関係している。

蚊と宿主動物の接触は頻繁になり、病原体の受け渡しが動物の病気の中には蚊によって伝播されるものがある。

容易で病気の流行も盛んになる。逆に宿主動物が少ない

これは、病気に罹った動物の血を吸った蚊が、病原体を動物群集では、蚊が宿主でない動物を吸血することが頻血液とともに体内に取り込み、別の健康な動物を吸血す繁になり、病原体の受け渡しの機会が減って病気の流行るときにその病原体を注入することによって起こる。

が抑えられる可能性がある。このような考えから、生物蚊が病気をうつす力は個体群の形質のひとつで、いく多様性と病気流行の関係に関する研究も進められている。

つかの生物学的、生態学的性質によって決定されている（例えば、病原体との親和性、吸血源動物嗜好性、成虫

Mosquito larvae work as scavengers and decompose
organic matters in aquatic ecosystems. They are importantfood resources supporting predator populations in aquaticcommunities together with other aquatic insects, such as
Chironomids, midges, etc. The adult mosquitoes also
provide a food source for wild birds, bats, spiders, and ants,
among others. Therefore, mosquitoes are an importantmember of aquatic ecosystems and help maintain the
structure and species diversity of animal communities.
Mosquitoes are well known for their blood feeding habits
and have unique roles within animal communities. Morethan 100 mosquito species live in Japan and about 60of them bite human beings. There are mosquitoes that
prefer to feed on wild birds, or on larger mammals, or
frogs, even fishes. It is through their blood feeding habitsthat some mosquito species transmit infectious disease tohumans as well as wild animals. Females that have fed
on infected animals ingest the pathogen with the blood
meal, and transmit it to uninfected animals. The capacityof mosquitoes to transmit pathogens is determined byseveral biological and ecological characters, such as vector
competence, host preference, biting density, feeding pattern,

4

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012and longevity. The transmission dynamics of the pathogens
in animal communities depends largely on the feeding
pattern of vector mosquitoes in the communities.
It is important to distinguish the amplifying- and the
diluting-vector-animal contacts in order to predict the
epidemic of mosquito borne diseases in animal communities.
When mosquito borne pathogens are introduced into
communities composed of many pathogen hosting animals,
vector mosquitoes have a high chance of taking blood meals
from host-animals and thus, the amplifying-vector-animal
contacts are frequent. Conversely, in animal communities
where host animals are rare, a large proportion of vector
mosquitoes feed on non pathogen hosting animals, thediluting-vector-animal contacts occurs frequently and thus,
the pathogen transmission rate is low. Therefore, we can
expect some relationships between community structure
and transmission dynamics of mosquito borne diseases
within animal communities. Theoretical as well as empiricalecological studies have been conducted to demonstrate therelationships between species diversity and transmission ofvector borne diseases.

ダニが語る生物多様性～寄生生物の進化的重要単位の意義～
Mites Talk about Biodiversity - Ecological Significance of Evolutionarily
Significant Units in Parasites.
独立行政法人 国立環境研究所 侵入生物研究チーム・五箇 公一

Koichi GOKA, PhD, Invasive Alien Species Research TeamNational Institute for Environmental Studies

生物多様性の保全が唱われて久しいが、生物多様性ををかけて、人間への宿主転換を図った結果と考えられる。

語る上で対象となる生物は、目で見て分かる、美しい、

寄生生物の多様性および宿主との共進化の歴史を知るこ

かわいらしい、あるいは格好がいい動物や植物が主流をとは、寄生生物との共生関係を維持する上でも重要な知占める。しかし、目に見えない、（一般には）美しくない、見となる。

微小な生物達も立派な生物多様性の構成員であり、重要

ダニは Macro-Parasite（目で見える寄生生物）群の中な生態系機能を担っている。特に、寄生生物は宿主生物で代表的な種群であり、多くの人は不快なイメージしかとの間に軍拡競争的共進化をもたらし、進化や種分化の抱かない生物であるが、その種数は分かっているだけで強力な駆動力として、生物多様性の創成において重要な

約 5 万種、未記載種を含めると 100 万種を超えるともい役割を果たしている。しかし、現在の人間活動による生

われ、その生活史も生息場所も多岐に渡る。自由生活者、物の生息地の破壊や生物の人為的移送は、宿主−寄生生

寄生者、捕食者など、彼らもまた生態系システムの中で物間における共進化の歴史を崩壊させ、寄生生物の感染

重要な役割を果たしており、立派な生物多様性の要因で爆発というかたちで生態系や人間社会に脅威をもたらしある。本講演では、ダニ学者でもある講演者自身のこれている。

までの研究成果を交えながら、寄生性ダニと宿主生物の近年、問題とされる新興感染症や再興感染症も、それらの病原体生物の住処である野生生物を、人間がハビタッ

間に繰り広げられる共進化の世界を紹介し、ミクロな生物多様性の重要性について考察をしたい。

トごと減少させたことにより、病原体微生物が生き残り

Biodiversity conservation has recently become a boom
field within environmental science. When we talk aboutbiodiversity people usually only focus on the visible,
beautiful, pretty or stylish animals and plants. But obviously
the less beautiful microorganisms also have membershipwithin biodiversity and play important roles in ecologicalsystems. Notably, parasitic organisms have served as
powerful causative agents behind evolution and wildlife
speciation through a co-evolution arms race between
parasites and host species. However, habitat destruction
and biological invasion by large-scale modern day humanactivity has caused the historical co-evolution of hostand parasite to collapse resulting in parasite pandemics.
Furthermore, some of the recent emerging and reemerging
disease problems are considered to have resulted from hostswitching by infectious viruses. These viruses once only
co-habited, in symbiosis, with certain specific wildlife
hosts but they have since lost their usual habitat due tohuman activity. Maintenance of the symbiotic relationshipbetween human and parasites must be an important process

for understanding the biodiversity of parasites and coevolutionary history between hosts and parasites.
The Acarian is a representative species group within macroparasites (visible parasites). While people almost always
have an unpleasant image of this species group, the varieties
already recorded within the group approximate to a totalof 50,000, and the actual total number, including nonrecorded species, may exceed 1,000,000. Furthermore thelife history and habitats of all these species ranges widelyover free living, parasite, predator and so on. So, we cansay that acarians are really important within biodiversity. In
this workshop I will introduce, as an acarologist, the worldof co-evolution produced by parasitic mites and their hostspecies, and discuss about the significance of miniatureorganism biodiversity.

2nd Live Love Animals International Conference on Animal Care in Kobe 20125

WS5-Record

WS5- 記録集

6

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

《主催者および座長メッセージ

ORGANIZER & CHAIR MESSAGE》

保全医学と生態系の健康
Conservation Medicine and Ecological Health日本大学 生物資源科学部 教授／よこはま動物園ズーラシア 園長／
日本野生動物医学会 会長・村田 浩一

Koichi MURATA, PhD, Professor, College of Bioresource Sciences, Nihon University,
Director, Zoorasia Yokohama Zoological Gardens
President, Japanese Society of Zoo and Wildlife Medicine
Hello everyone. I am Koichi Murata, President of thehealth. It is an interdisciplinary approach that reaches

Japanese Society of Zoo and Wildlife Medicine, and I

into a variety of research fields including political andwill be acting as the coordinator of today’s symposium.

social issues. It involves NPOs and ordinary citizens
rather than scholars, per se.

Let me begin by saying a big “thank you” to all of you
for coming. It is wonderful to see so many people here

The core aim and target of conservation medicine is

despite it being a cold Sunday morning.

the protection and preservation of biodiversity because
maintaining biodiversity is extremely important. I’

First of all, I would like to speak to you about them sure you have all had many opportunities to hearpurpose and intent of this symposium project. The

the word “biodiversity”. The mass media takes up

theme of the present symposium is “One World, One

the subject frequently and in 2010 an international

Health.” In other words, conservation medicine is an

conference called the ‘COP 10 (The 10th Conference of

academic and research discipline aimed at the concept

the Parties to the Convention on Biological Diversity)’that the entire earth has its own health.

was held at Nagoya. But what exactly is biodiversity?
And why is it so important? When we ask these

Now, what does conservation medicine actually consist

questions again, we see that there are some areas thatof? In all probability, most of you here are hearing theremain unclear.

term “conservation medicine” for the first time. Thatis reasonable and totally understandable because theAs this figure indicates, the global environment isdiscipline of conservation medicine was not pioneered

facing many threats at present. The red marks show

here in Japan but in North America, where it was firstthe causes of this critical situation. Among the criticalestablished just 15 years ago in 1997.

factors harming the Earth that we hear about often are
climate change (or global warming), the eutrophication

This slide shows how conservation medicine is aimed atof lakes, and the problem of acid rain. But in fact itachieving human health, animal health and ecosystemis the disappearance of biodiversity itself which ishealth in a comprehensive manner that addresses theconsidered to be the single biggest risk to the Earthrelationship between all three. Put simply, the concept

at present. The entire global ecosystem itself may beof health does not exist individually and separately

endangered if that risk continues to increase. Actually,in people, animals or ecologically, but stems frombiodiversity is considered to have a greater effect on

their mutual relationships. This is a quite radical andthe global environment than is usually stated in theessential definition of health.

mass media.

Conservation medicine, which focuses on addressing

So what is the significance or meaning of protecting

these issues, is an idea that at heart pursues ecologicalbiodiversity? Up until now, various researchers and2nd Live Love Animals International Conference on Animal Care in Kobe 20127

academics have tried to explain why it is so important.

species coexist. A specialized book has been written

A great many theories have been postulated and, amongon the subject, as is shown on the slide. In illustrating

them, the idea put forward by Stanford University

the dilution effect, Keesing took up the subject of

researcher Dr. Gretchen C. Daily of “ecosystem

Lyme disease, an infectious disease transmitted byservices” is considered particularly important. The

arthropods. Lyme disease is a zoonosis, meaning that it

idea behind ecosystem services is that protecting andis a disease transmitted between animals and humans.

preserving biodiversity can yield benefits for people.

It is actually a bacterial infection commonly spread

Accordingly, we must preserve biodiversity sustainably

by ticks. The disease-causing agents are bacteria

so that people can continue to enjoy the benefits ofbelonging to the genus Borrelia. Essentially, thebiodiversity. Personally I don’t like this idea very muchdisease is maintained through a relationship linking

because it is rather anthropocentric but, as a theory,the disease-causing bacteria, ticks and wild animals.

it has the merit of being very easy to understand andFrom time to time, people also become infected. The

is useful for providing a rationale for why biodiversity

disease causes a distinctive circular skin rash (known asshould be preserved.

erythema migrans), as well as flu-like symptoms suchas fever. Lyme disease is not life threatening although,These ecosystem services can be grouped into several

if treatment is delayed, symptoms can become severe.

categories. For example, there are so-called “cultural

However it is not something we need to fear very much.

services,” so-called “conservation services,” andwhat can be termed “supply” services. Ecosystems

These days however, the incidence of people infected

are considered to provide various services that are

by Lyme disease is spreading worldwide. In particular,

beneficial to people, and these services are related

many cases of infections are reported among urban

to each other. Among them are so-called “regulating

dwellers who go camping or pursue other outdoor

services”. These include such things as flood regulation,

activities in the countryside.

weather regulation, and disease regulation. Or in otherwords, by conserving biodiversity we can enjoy the

In a short while I would like to talk in a little more

benefit of controlling diseases. So from this point ofdetail about the connection between Lyme disease andview, biodiversity is very important.

the preservation of biodiversity. But before that, I will
try to give a simple description of the life cycle of ticks.

Now I would like to speak a little more on the subject

Near the end of this symposium, I believe Dr. Goka ofof disease regulation, which is one of the points we will

the National Institute for Environmental Studies will

be discussing during this symposium. In the context ofbe talking about ticks. But in simple terms, ticks growdisease regulation there is a phenomenon called thethrough the larval and nymph stages by sucking the‘dilution effect’. What this means is that biodiversity

blood of many kinds of vertebrate animals, and then,has the effect of diluting the incidence of disease.

when they reach the adult stage they lay eggs. That’sFirst proposed by the ecological researchers Ostfeld

their life cycle in a nutshell.

and Keesing, this is now a fairly well understood andaccepted theory that mainly deals with the relationshipTo sustain their life, ticks require nutrition in the form

between the amount of biodiversity and the prevalenceof blood from mammals or birds. However, they don’of vector-borne diseases carried by arthropods such ast draw this blood from pre-selected hosts, but rather,ticks and mosquitoes.

they encounter a host animal at random and then begin
sucking its blood. They may end up drinking the blood

I would like at this point to explain the dilution effectof an animal whose blood is unpalatable to them and if

in some detail. The main idea is that certain kinds ofthe blood is unpalatable they may die, (or at least theirdiseases are kept under control where there is sufficient

growth may be retarded).

biodiversity, such as in environments where many8

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

In the case of Lyme disease, it turns out that ticks

recently begun to spread in the human world, and in

harboring the bacteria that cause Lyme disease

most cases emerging infectious diseases are zoonoses.

are particularly fond of the blood of mice. It is

A zoonosis occurs when a disease-causing agent thatwell understood that if they get the opportunity tois present in one or more species of animals newly

drink mouse blood, they grow very well and tend to

crosses over to infect and cause disease in humans. As

proliferate. This is a key point. For instance, let’s takethis map shows, most zoonoses originate in tropicala look at an environment model. There are lots ofregions such as Africa, South America and Southeast

animals here. This environment has lots of different

Asia.

kinds of animals that ticks feed on, and within it there
are some mice. But there are also animals not favoredThe reason is that originally in such areas, wildby the ticks that transmit Lyme disease, such as birds

animals, pathogens and vectors had been living quietly

and skunks. For some reason the blood of skunks

together in a delicate balance, but that balance became

appears to be particularly unpalatable. Ticks feed on

destroyed because of developments such as agriculture.

the blood of individual animals at random so in thisThe collapse of the relationships between wild animals,

environment their chances of encountering a mousepathogens and vectors allows new infections to spreadare extremely low. As a result, their rates of growth andto the people and livestock that colonized the areas.

proliferation are not very high. But on the other hand,This map suggests that perhaps airplanes and ships

within a different environment where biodiversity is

carry diseases that occur in such places to industrialized

extremely low, (such as, for example, an environment incountries such as the nations of North America, Europe

which most animals are mice, with only the occasional

and Japan where they can spread further.

raccoon - a foreign exotic species), then most ticks willencounter mice, their favorite food source, and so their

On the other hand, there are some areas that are

rates of growth and proliferation will be high.

known as biodiversity hotspots. This slide shows the
distribution of rare animals, endangered species andKeesing and his fellow researchers conducted field

species indigenous to only a small area. Actually, manystudies to investigate how Lyme disease is actuallyrare species of wildlife are found where biodiversity

propagated in a species-rich environment. In this figure,is abundant and the environment is rich. The places

the horizontal axis shows the species diversity andmarked in red on the map are such hotspots and they

the ratio of ticks infected with Lyme disease is plotted

actually overlap quite well with the places I showedalong the vertical access. The environment on the leftearlier where new infectious diseases emerge.

is extremely simple with impoverished biodiversity
and with hardly any mammals apart from mice. WhenAs you are such an intelligent audience, I am sure you

ticks obtained from this environment were examined, ahave understood what I’ve said up to now. Although thelarge number of Borrelia bacteria, the pathogen causing

wild animals and pathogens living in these biodiversity

Lyme disease, were found on the ticks’ bodies. But

hotspots affect each other and the balance between

when the same kind of survey was carried out on ticks

them is delicate, under natural conditions things tendfrom within a biodiversity-rich environment, only a very

to work out somehow and diseases do not spread very

few were found to be carrying Borrelia.

much. But when people go into such places and exert
an influence on the environment or damage it with

Naturally, there are counterarguments. But on the otherdevelopment, this balance can collapse. And when thehand, there are reports that a similar dilution effect canbalance collapses, the pathogens can exert an influence

be observed in the case of West Nile virus and otheron livestock or people. In other words, we can say thatviral diseases such as the Sin Nombre virus. I’m sureby damaging biodiversity, people unleash a process ofyou have all heard of the term “emerging infectious

destruction that comes back to people again.

diseases.” These are infectious diseases that have

2nd Live Love Animals International Conference on Animal Care in Kobe 20129

I’ve been taking about ecosystem services so far, but

researching tick damage to agriculture. Ticks are also

more fundamentally, unless people establish a bettervery important organisms in the environment, andrelationship with pathogens, vectors and wild animals,

probably the soil cannot be kept in a healthy condition

in my opinion we will not be able to maintain the earth’

without their help. This means that environmentss ecological health. This is one of the major reasons

without ticks are environments where people cannot

why we planned this symposium at this time.

live either. I would like everyone to realize this, and thatis why I have invited Dr. Goka to speak to us.

So, in order to spread understanding of this purpose
more widely, I have requested three lecturers to giveNow, I’d like to tell you about to the relationships I havetalks on the subject.

with these three lecturers.

The first lecturer is Prof. Michael Huffman, an associate

As for Prof. Huffman, although I have known his

professor at the Primate Research Institute, Kyoto

name for a long time, as I mentioned I first became

University. Prof. Huffman has studied self-medicationacquainted with him in a research context at anby primates, and specifically by the great apes. He

international conference held several years ago on

has observed that apes control their own bodies,

the non-human primate malaria parasite Plasmodium.

which means they can maintain their own health, heal

At that time, Prof. Huffman was also working as athemselves when they become ill, and even prevent

coordinator of the International Primatological Society

illnesses from arising in the first place. From before,(IPS). In spite of his busy schedule, he participated in

I have read Prof. Huffman’s papers and specialized

the primate malaria conference, where he delivered

books with interest. I’ve invited him to talk to us today

a lecture. Perhaps because he was tired after that, I

because I thought it would be a good opportunity forremember he slept deeply during the conference.

us to learn about the intelligence of apes and about
their lifestyles, which are adapted successfully to the

I met Prof. Tsuda for the first time five or six years ago.

environment.

Although my specialty was avian malaria, I was almost
totally ignorant about mosquitoes. I wanted to develop

Our second lecturer today is Prof. Yoshio Tsuda,

avian malaria research in some way by obtaining Prof.

a researcher at the National Institute of Infectious

Tsuda’s cooperation, so I have accompanied him on

Diseases. Prof. Tsuda is proceeding with his research

fieldwork across Japan and carried out research withfrom a stance of looking at disease from the perspective

him as his co-researcher. Even today I receive guidanceof mosquito biology rather than that of the relationshipfrom him about mosquito biology, behavior andbetween mosquitoes and infectious disease. Whenclassification.

you think of mosquitoes, you may only be thinking
about how to squash them, but I think that if there isI have also been acquainted with Dr. Goka’s name foran environment in which mosquitoes can’t live, thenmany years. Perhaps you too are aware of his activities

perhaps it is an environment where people can’t live

through the mass media including TV. Althougheither. In this sense, I would like us all to learn how

he is extremely busy with his research, he actively

skillfully mosquitoes are engaged in their environment

participates in drinking sessions outside of researchand how important an element of the environment they

hours and he has developed a habit of taking photosare.

with his students. These are posted on Facebook. I
introduced one of these photos earlier showing him and

Dr. Koichi Goka, who is also a researcher at the National

me together. At this symposium too, he has been taking

Institute of Infectious Diseases, will give today’s lastphotos with many people, and these will also be posted

lecture. Dr. Goka is now working mainly on the control

on Facebook.

of invasive alien species. However, originally he was10

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

Now it is time to hear the lectures from these threeacademics, which is the original purpose of this
symposium. First, Prof. Michael Huffman, please start
your talk now. I invite you all to enjoy his lecture.

【Slide 4】【Slide 1】【Slide 5】【Slide 2】【Slide 6】【Slide 3】【Slide 7】

2nd Live Love Animals International Conference on Animal Care in Kobe 2012

11

12

【Slide 8】【Slide 12】【Slide 9】【Slide 13】【Slide 10】【Slide 14】【Slide 11】【Slide 15】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 16】【Slide 20】【Slide 17】【Slide 18】【Slide 19】

2nd Live Love Animals International Conference on Animal Care in Kobe 201213

霊長類の自己治療行動—予防と治療
Self-Medication in Primates- Prevention and Cure
京都大学霊長類研究所 准教授・ハフマン A. マイケル

Michael A. Huffman, PhD, Associate Professor
Primate Research Institute, Kyoto University
Good morning everybody. First of all, I would like tothat have a lot of nutritional value, such as the leaves,

express my thanks to all the people who have been

are also the parts that get eaten by animals. Plants are

involved in planning and hosting this highly significant

considered to employ two strategies in order to defendinternational conference, beginning with Prof. Murata.

themselves against being eaten. Their first defense

Yesterday, I heard a lot of talks, and although theystrategy is to produce various chemical substances.

addressed fields somewhat different to my own, I still

Due to the presence of toxic secondary metabolites,

found them very interesting and informative. I enjoyedimportant parts of many plants are rendered distastefulthem a great deal.

to animals. Many of these substances are bitter to thetaste. For instance, if a predator overeats a certain kind

I would like to talk to you now about my own research.

of leaf and the animal develops a disorder (such as bad

My talk will overlap to some extent with what Prof.

digestion, etc.) it will, as a result, tend to avoid feeding

Murata was talking about earlier so let me introduce

on the species of plant in question. The second strategy

that part from now.

is a physical defense. Some plants grow large burs or
thorns, while others have almost invisible small, hard

Today I am going to talk on the subject of “Self-

projections that are closely packed on the surface ofMedication in Primates - Prevention and Cure”. To

their leaves. These small projections, which make thebegin with, there is one point on which I must insist.

rough textured surface of the leaves, are made of a

Many people may think that primates are capable

glassy substance called silica which is very difficult toof self-medication because they are clever. But I

digest. So if an animal eats such leaves, it will develop

personally don’t think this reasoning is correct. As

indigestion.

Prof. Murata stated earlier, we humans too are animals.
We shouldn’t forget that just like us, plants and other

This is a photograph of the surface of such a leaf taken

animals are living things, and that we all live together

though an electron microscope. It gives a good idea ofin one world. With regard to self-medication, I don’how many tiny burs cover the leaf surface.

t believe that primates lead a particularly special kindof existence. On the contrary, I believe that all living

In short, third parties have taken over these twothings must perform self-medication in some way or

methods of defense, which originally evolved in orderanother. Because unless organisms - whether they be

to protect plants, for use in protecting their own bodies.

primates, birds, fish, or even insects - have some means

There are reports that many kinds of animals use theseof maintaining their own health when facing disease or

two plant defense methods as “medicines”. Insects arestress, then they would not be able to continue to exist

considered to have been the first animals to begin self-

on Earth.

medication as an evolutionary process. Around the time
the first flowers and fruit began to grow, there was also

14

Probably, the first living things to begin practicing self-

an explosive increase in the number of insect species.

medication were the plants, because predators eat

In the course of that process, insects began using theplants if they can’t protect themselves. Plants rely onplants for purposes other than nutrition. Plants were

their leaves to collect energy yet the parts of plants

also co-evolving with insects, and relationships of deep

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

mutual dependence developed between the two.

I’d like to introduce you to how chimpanzees maintaintheir own health using the two kinds of plant defense

This figure illustrates such close relationships between

systems I mentioned earlier, as well as to various otherspecific plants and insects. Some species of plants andkinds of behavior they engage in to maintain health.

insects have co-evolved into relationships of mutual

Roughly speaking, these behaviors can be considereddependence such that neither would be able to continue

as operating on three levels.

existing without the other. Ecosystems in which a single
species of plant and a single species of insect function

Level 1 is behavior aimed at avoiding becoming

as a single unit have formed.

infected with disease-causing agents and at reducing
contact with such agents.

Within these relationships, insects play a role inmaking plant reproduction possible by carrying pollen.

Two examples of this behavior are shown in these

Of course, from the insects’ standpoint, they are using

photographs. The one on the left shows olive baboons

the plants as a source of nutrition. And they also usethat live in the savanna on the Serengeti Plain.

the plants as “natural medical foods”, which means
they literally ingest medicinal plants. While on the

There are four individuals and at dawn they go out

one hand the insects help the plants, after ingesting

foraging. Overnight, they stay in different trees,

the nutrition of the plant, they also use them tomoving from one to another every few days. At times

stimulate various functions by accumulating the plants’

when food is plentiful they may remain on the same

secondary metabolites within their own bodies. Thesetree for a number of consecutive days. When they dosecondary metabolites serve a variety of functions.

this, a parasitic infection begins to break out from theFor example, insects use them to stimulate various

excrement they leave beneath the tree. Sometimes

interactions between individuals of the same species,

it takes a few days for the infection to begin, but if

such as their function as precursors in the formation of

the baboons climb the same tree everyday or carry

pheromones. These help the sexes come together forout activities on the ground beneath the tree, themating. Some insects also use secondary metabolites

probability that they will contract the infection becomesas social communication tools or for defense againstvery high. It is said that the baboons change the placenatural enemies. They make themselves unpalatable

where they stay overnight periodically in order toto predators by accumulating large amounts of theseminimize that risk.

substances in their bodies. So if a predator puts an
insect (such as a butterfly, which has adopted the

The other example I want to show you is the method

defense strategy) into its mouth, the presence of

illustrated in the photograph on the right. Thesethe substance will cause the predator to spit out themonkeys are hamadryas baboons that live on theinsect. In that way, the insect can avoid being eaten.

Arabian Peninsula. Their habitat is a desert area that

In addition, some insects use secondary metabolites

doesn’t have an abundant supply of water all year

for their anti-parasitic effects. Poisonous substancesround. When water levels become very low, all thecreated in plants and ingested by the insect cananimals in the area gather close to the limited water

function to destroy parasitic infections.

sources. Due to the small volume of the water, thetemperature of the water rises, creating a perfect

From insects to primates, many animals have beenenvironment for disease-causing agents (carried by theobserved to practice self-medication. Animals try tovarious animals in the area) to propagate. By drinking

protect themselves and maintain their health on several

this water, animals have a very high probability oflevels when they come into contact with diseases. Now

coming into contact with a wide range of pathogens.

I am going to change the subject to the self-medicative

These baboons do a very clever thing in order to avoid

behavior of primates, and in particular, of chimpanzees.

the problem. In this photograph, you can see green

2nd Live Love Animals International Conference on Animal Care in Kobe 201215

water flowing slowly at the bottom of the picture. The

people in Africa use many other plant parts such as

baboons are digging a hole in the sand at a place someleaves and leafy stems, trunks, seeds, etc., as medicinal

distance from this stream. The groundwater emerges atplants.

the place where the baboons dig their hole. By making
something like a well they are able to obtain cleaner

Now, I will show the situation with another primate

water.

species, the gorillas. In the same way as I did withchimpanzees, I surveyed how much overlap there was

Through these two examples, we can ascertain thatbetween the plant parts that gorillas eat and the plantsmonkeys know some ways of avoiding being infectedthat local people use for medicines, with reference toby disease and of reducing the risk of coming intoa list compiled of all the foods known to be eaten bycontact with pathogens.

the three sub-species of gorillas. Surprisingly, I foundthat the plan parts taken by both gorillas and humans

At level 2, animals eat foods that are nutritious andcontain substances that have a variety of effects. For

produce medicinal effects. In terms of the way humans

example, some of them contain factors that inhibit thelook at the world, these foods fall into what we call thegrowth of cancers, promote cardiac function, work as‘supplements’ and ‘spices’ categories.

stimulants, boost the immune response, etc., in addition
to working as antiseptic, anti-parasitic and antiviral

As you can see from this photograph, chimpanzees

agents. Unfortunately, it has not yet been observed how

follow a largely frugivourous diet and they can quickly

much, in what way, or in what situations gorillas use

gain energy this way. The sugars contained in fruits canthese plant parts.

be used as an immediate energy source. Many fruits
are also rich in protein and provide the animals with

The next level up is Level 3. At this level, primatesnecessary fiber and minerals too.

are using medicinal plants precisely as humans use
medicines. This is self-medicative behavior in which

On the other hand, chimpanzees also eat plants

primates are observed to use medicinal plants whenthat contain various other ingredients in addition tothey are sick or when disease symptoms appear. In

nutrients at certain times of the year. These plants

cases where large amounts of the plants are poisonous,

are classified as medicinal foods. Some plants containthey use limited amounts and employ special methods

substances that have bactericidal effects or whichto treat disease. Even if their health condition

inhibit parasitic infections.

deteriorates, they only use limited small amounts ofthese plants.

For example, for many years I have been conducting
research on chimpanzees in the Mahale Mountains

Now, let me explain how this works in the case of

National Park in Western Tanzania. In that park, I have

chimpanzees. They have two ways of self-medicating

focused on a group called the M Group and researchedthat I would like to introduce.

how much of these medicinal foods are included in thefood they actually eat. In the course of this research,

In the photograph on the left side of the slide, you

I have found that approx. 22% of the 172 kinds of

can see a chimpanzee named Linda, who is about tofood they usually eat coincide with natural medicines

put a leaf into her mouth. The plant is of the genus

that humans use to ward off parasitic infections. More

Aspilia, which has leaves with a roughly textured

generally, it has been established that throughout Africa

surface similar to the one I showed you in the electron

both chimpanzees and humans use the same parts of

microscope photograph earlier.

the same plant species for easing specific symptoms

16of specific diseases such as parasitic infections or

Chimpanzees put the leaves into their mouth one bygastrointestinal diseases. Interestingly, apart from fruit,

one, rolling each leaf around in their mouth and then

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

swallowing it without chewing it. Sometimes they may

the chimpanzee intestinal wall and produce nodules.

swallow up to a hundred leaves in this way at a single

After an incubation period of about one month,sitting. As I mentioned earlier, such leaves are difficult

the negative effects of the infection appear in theto digest. Chimpanzees eat things that are hard to digest

chimpanzees. If the degree of infection (the number

in order to promote the body’s rejection responses.

of adult worms infecting the host) becomes very highWhen the leaves pass through the digestive system,

this leads to symptoms such as intestinal inflammation,

they act as a de-worming agent, helping to remove thediarrhea, stomach pain, etc. If the infection isparasitic nematode worms that infest the chimpanzees’

particularly heavy, it may even kill the host chimpanzee.

intestines. This self-medication method involves a

In the period from the beginning to the middle of thephysical effect, and the chimpanzees’ are engaging inrainy season, infected chimpanzees frequently engage

what is known as “leaf swallowing behavior”.

in both bitter pith juice ingestion behavior and leaf
swallowing behavior.

Another method is to use Vernonia amygdalina, a plantin the family Asteraceae. The chimpanzees chew on the

Sick individuals carry out these two act ivit ies

bitter pith of the plant aggressively and suck out its

frequently and interchangably. Though as I mentioned

juice. This is known as “bitter pith chewing behavior”.

above, because Veronia is toxic, they do not practiceThis pith juice doesn’t contain anything of nutritional

this behavior as much as leaf swallowing. Now, I willvalue, but it is effective for treating oesophagostomiasis,

introduce the behavior in more detail.

an illness resulting from a parasitic nodular worm
infection. This infection is quite a serious disease, butThis photograph shows a chimpanzee putting a leaf

based on my own observations, by drinking the bitter

into its mouth, rolling it around and trying to swallow it

juice of the pith of this plant, visually confirmablein a gulp.

symptoms such as fatigue, decreased appetite andabnormally colored urine disappeared within 24 hours,

I once rolled up such a leaf and attempted to swallow

and the parasites’ egg laying activities also ceased.

it in the same way as the chimpanzees do, but it was

I have reported this observational data in scientificextremely difficult. The burs grow downward, so thejournals.

leaves tend to stick in the throat and will not travel
down smoothly. It was a thoroughly unpleasantIn the Mahale Mountains National Park, there are clear

experience for me. However, chimpanzees casuallydifferences in how the nodular worm infection rates

swallow up to a hundred of these leaves on occasion.

wax and wane between the rainy and dry seasons.
Within the approximately six months when the region

The chimpanzee in this photograph is again Linda.

receives heavy rain, these parasites actively and

She is about to swallow the leaf she is holding in her

repeatedly infect chimpanzees.

hand. The other photograph shows a leaf on which
you can see an adult modular worm of the species

This figure shows the life cycle of the nodular worms.

Oesophagostomum stephanostomum, which is about

When the chimpanzees excrete the eggs of these

3cm in length. Fighting infestations by this parasite isworms, they remain in the soil or on the surface of

one of the aims of this particular form of chimpanzee

low plant leaves until they reach the L3 stage. At

self-medication.

this stage they become larvae capable of re-infecting
chimpanzees. About the time when the rains start, theOn average, two leaves is effective in expelling one

environment becomes favorable for the development

worm. Sometimes, 20 to 30 adult worms are forced outof the eggs and young larvae excreted in chimpanzee

from a single ‘dose’ of 40~60 leaves. The de-worming

feces. When chimpanzees unknowingly take in theeffect is not due to the plant’s secondary metabolites

infectious L3 stage larvae, these parasites burrow into

but the result of transient diarrhea simply increasing

2nd Live Love Animals International Conference on Animal Care in Kobe 201217

movements of the intestines, which rapidly expel theIt has been demonstrated to lower malarial fever,leaves and worms with them. Even if the chimpanzees

blood cholesterol and blood sugar levels, and is very

ingest the leaves every day, it doesn’t seem to cause

effective against parasitic infections. People are widelythem any problems. During the rainy season, there

reported to use it for their own livestock. However,is a high possibility that individual chimpanzees will

although this plant has been studied for a century,

be infected by parasitic worms many times, but thisthe fact that primates use it as a medicine for treating

method seems to be sufficient for controlling theparasitic infections was not discovered until 1987. It

number of worms. Looking at the infection rates data,

was in fact myself who made the first observation andthe treatment seems to have this effect.

reported about this behavior. Interestingly, I foundthat both humans and chimpanzees exhibit the same

Chimpanzees engage in this behavior frequently at thesymptoms after ingesting Vernonia amygdalina. The

beginning of the rainy season when each individual’

plant is very bitter. When people use it, they first beat its modular worm infection burden increases. Not every

and then soak it in water until the water becomes deep

individual chimpanzee becomes infected, and thisbrown, which doesn’t take very long. Then they drink

behavior is not observed everyday in the rainy season.

the water down all at once. This is said to result in an

But in the dry season it is hardly observed at all.

improvement in their condition within 24 hours.

However, from about one month into the rainy season,a marked increase is observed in bitter pith chewing

In the case of chimpanzees also, within about 24 hours

behavior.

of drinking the bitter juice from the pith of the plant,
their body condition shows clear signs of improvement.

As research into the African great apes - chimpanzees,

By observing their behavior we can clearly see

bonobos and gorillas - has progressed over the past

improvements in their appetite and physical strength.

20 years, this leaf swallowing behavior has been

The fact that humans and chimpanzees have thisobserved at 16 research sites, not only at Mahale.

response in common is very interesting.

The same behavior has also been noted at many sites
being used to counter infection by the nodular worm

People have been researching Vernonia amygdalina as a

Oesophagostomum stephanostomum. Yet anothernatural compound for over a hundred years. A long list

target of the same behavior is the tapeworm Bertiellaof compounds have been extracted from the plant, withstuderi. Leaf swallowing behavior has a similar de-many kinds of sesquiterpene lactones among them.

worming effect on both infections. The adult stage

Every report without exception mentions the powerfulworms and the tapeworm proglottids are excreted

activity and poisonous ingredients of the plant.

together with the leaves. In the case of the nodular
worm, the number of adult-stage worms is clearly

However, until 1987, nobody had paid attention to the

reduced, so there seems to be a definite effect. As forplant pith, the part that is used by chimpanzees, so thethe tapeworm nodule excretion effect, there has notchemical composition of the pith was unknown. To

been much discussion on the subject. Up to now, it

remedy this situation, I carried out joint research withhas been established that chimpanzees engage in leaf

Prof. Koshimizu and Prof. Ohigashi of the Faculty ofswallowing behavior while making use of the leaves ofAgriculture at Kyoto University regarding the chemical

about 40 different species of plants. All of these species

analysis of Vernonia amygdalina and its bioactivity. One

have similarly rough textured leaves.

of the results of the research was that we discovered
13 new chemical compounds. These were identified to

Next, let’s take a closer look at the chimpanzees’ bitterbe steroid glucosides and were named Vernonioside A1,

pith juice ingestion behavior. The plant they use at

2, 3, 4, B1, 2, 3, etc.

Mahale is Vernonia amygdalina. This plant is very wellknown in both folk medicine and in pharmacognosy.

18

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

In summary, chimpanzees engage in leaf swallowing

and bitter pith juice ingestion behaviors as self-

noticed a weak porcupine digging up and eating the

medication during the rainy season when infection

root of a plant his tribe called mulengelele which herates of the no dular worm Oesophagostomum

recognized as being highly poisonous. Babu Kalunde

stephanostomum and the tapeworm Bertiella studeri

knew there must be a reason behind the behavior so he

are high. Other medicinal plants are also usedbrought a few roots back to his village and used themintensively throughout the rainy season when parasite

to treat some seriously ill patients. Mohamedi and otherinfection rates peak. The chimpanzees appear to use

healers still use this root today to treat infections forthese plants from time to time up until the end of thewhich western doctors would use antibiotics.

rainy season.
The next speaker, Prof. Tsuda, will be talking about
In the dry season, leaf swallowing and bitter pithmalaria, so I’m going to end my talk by giving a brief

juice ingestion behavior are rarely observed. And theintroduction to primate malaria. There is no doubt thatchimpanzees reduce their intake of natural medicinal

malaria has had a huge effect on primates as well as on

foods too. When the season changes, the animals

humans. It is an established fact that all four malariachange their food menu and employ more direct

species infecting humans are derived from strains thattreatment methods.

infect non-human primates. Recently, in Southeast
Asia, the simian malaria parasite Plasmodium knowelsi

Lastly, I would like to talk about ethnopharmacognosy,(which usually only infects macaques) has begun

which is another of my research themes. In thisinfecting humans too. Since this is an infectious diseaseconnection I would like to introduce you to Mohamedithat the local monkeys have been living with for a long

Seifu Kalunde, with whom I cooperate on chimpanzee

time, it does not represent a major problem for the

research in Tanzania. Mohamedi is very knowledgeablemonkeys. But as an emerging disease in humans, it

about medicinal plants and he works actively as acauses serious symptoms in people who contract it.

traditional healer treating the diseases that affect the
local people. He was born and raised in the forests ofAt present, there are no effective medicines for treating

the Mahale Mountains, and has a wealth of knowledge

the disease but in the course of recent research it

about local medicinal plants that has been handed

has been found that chimpanzees are also infected

down for generations in his family. I’ve walked aroundby malaria. As part of our 1990s research into thethe forest together with Mohamedi for almost 20 years

ingredients within the medicinal plant Vernonia

and he has taught me a great deal about chimpanzees

amygdalina - as used by chimpanzees - we haveand plants. For example, he has told me that among

discovered that chemical compounds have a strong

his own relatives there are people who tell how theyanti-malarial action. More recently, another chemical

obtained many new medicines by observing how sickcompound has been reported which also has anti-

animals act. Even while we were working together, hemalarial parasitic action. It was isolated from a species

discovered a new antidiarrhetic medication. Havingof plant called Trichilia rubescens and it is a plantseen a sick chimpanzee with diarrhea practicing self-that chimpanzees in Uganda use. So there is great

medication he correctly surmised that the plant being

anticipation that this discovery can be turned into aused might be effective for people too. So he tried it out

new medicine for people.

on himself and found that it did work well. It is widelyused nowadays.

Several years ago I checked out the latest reports about
Vernonia amygdalina (using Google) and found that theI have another interesting story to relate, this time

University of Missouri had obtained a patent to use aabout Babu Kalunde, Mohamedi’s grandfather, whosubstance obtained from this plant as a medicine for

was a traditional healer. He discovered a new drug justtreating breast cancer. Animals and humans have been

by watching the strange behavior of a porcupine. He

living together for a long time in one world but since

2nd Live Love Animals International Conference on Animal Care in Kobe 201219

we humans have come to live in modern societies wehave gradually lost touch with nature. As a result wehave started to lose the natural knowledge that we had
previously gathered. I believe there is a link between
preserving the natural environment and biodiversity
and protecting our own health. We need to reconsider
the importance of the global environment and our
position in nature. In closing I would like to thank youvery much for listening.

20

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

レベル 1

感染を避けることや病原体との接触を低減する。
level 1
optimal avoidance or reduction of the possibility for disease transmission,
such as the avoidance of feces contaminated food, water or substrates

Michael A. Huffman
Primate Research InstituteKyoto University, JAPAN【Slide 1】

Anubis baboons in the Serengeti, Tanzania

Hamadryas baboons in Taif, Saudi Arabia【Slide 5】�������
Plant self-defense mechanisms��������������������������
�������

level 2the dietary selection of items with a preventative or health maintenanceaffect, such as items eaten routinely in small amounts or on a limited basis�����������
Chemical feeding
deterrent���������
physical feeding deterrent�【Slide 2】

chimpanzees in the Mahale Mountains, Tanzania【Slide 6】��������������������	

Potential anti-parasitic properties in the dietof Mahale chimpanzees������������������	��������������������
����������� !
22% used by humans for treatment ofparasite infection or stomach upset.�

����	

pharmacophagy

fruit 5%!
seeds 5%!
bark 15%!

������������!
Plant food spp. ��������

leaves & stems 75% !

������������!
Parts used in traditional medicine �【Slide 3】【Slide 7】������������������������
����	

Oesophagostomiasis, chimpanzee foraging and self-medicative behavior

栄誉補給以外を目的とした、特殊な	成分を含む植物の摂取と体内蓄積	

The non-nutritional ingestion of plants containing
particular secondary compounds that areabsorbed and stored in the body.

性フェロモンの先駆物質	

sexual pheromone precursor

社会的伝達	

social communication

抗寄生虫作用	����

prepatent period
ca. 1 monthanti-parasitic action

天敵防衛	

predator defense【Slide 4】【Slide 8】

2nd Live Love Animals International Conference on Animal Care in Kobe 201221

������������������������

������������	

Oesophagostomiasis, chimpanzee foraging and self-medicative behavior

MEDICINAL FOODS�Rough, whole leaf swallowing

MEDICINE�

【Slide 9】【Slide 13】�����������������������	���������������������!

Pharmacological properties in the gorilla diet

The effect of leaf swallowing on parasite infections����������	����������	���������
��������É	

Recognized pharmacologicalproperties: stimulant, cardiotonic,
hallucinogenic, immuno-stimulant,
tumor growth inhibitor, bactericide,fungicide, anti-parasitic, antiviralÉ
Analysis based on published feeding lists of all long-term
gorilla study field sites in Africa and pharmacologicalliterature search. N = 118 spp. 59 plant Families
Cousins & Huffman 2002 African Study Monographs

1.早朝や空腹時に葉を呑み込むと、腸のぜん動運動が活発になり、成虫体が駆虫される。

	 	 Swallowed on an empty stomach, intestinal activity
increases and worms are expelled.

��呑み込む葉２枚あたり成虫一匹が排泄される。

Average of 1 worm expelled / 2 leaves	 (mean 19.8, range 1 Ð 55 leaves per bout)

�����
���
Oesophagostomum and whole leaf�

【Slide 10】����

病気やその症状を治療するため、生理活性のある植物部位の少量を限定した回数で利用する。栄養価値が低い。

level 3
ingestion of a substance for the curative treatment of a disease or the symptoms
thereof: use of toxic or otherwise biologically active items at low frequency or in small
amounts, having little or no nutritional value

�� 雨期に葉呑み込み行動を度々行うことによって、!
腸結節内の寄生虫感染を抑制する効果が期待できる。!
Frequently performed during the rainy season, leaf
swallowing effectively suppresses level of
Oesophagostomum infection.	
 Huffman et al., 1996; 1997; Huffman & Caton, 2001 !

【Slide 14】�����������������������������
Sites where whole leaf swallowing is seen in the African Great Apes

17�Over 40 plant species known to be swallowed and all are rough & hispid!

【Slide 11】���������������������������

【Slide 15】��������������

Oesophagostomiasis- infection intensity and rainfall  

Huffman et al. 2009

【Slide 12】22

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 16】���������������	New compounds isolated from Vernonia amygdalina�
vernonioside: !
������������!
Newly discovered class ofcompounds!

STEROID GLUCOSIDES!
vernonioside!

�������

�������

Human Malaria Ape

Macaque Malaria

Plasmodium falciparum <------------(�������gorilla origin)

P. reichenowi, P. gaboni

P. vivax<------------- P. simium(��������� Indian - Asian primate origin)
P. ovale<------------- P. ovale variant type(���������chimpanzees origin)
SESQUITERPENE LACOTONES!
vernodaline!����hyrdroxyvernolide
vernolide!

��vernolopin!
vernodalol! �vernomenin !!

sesquiterpene lactones: !
����������������
�������!
Widely reported in Vernonia�ssp. !

【Slide 17】����������������������

P. malariae<------------(����� Macaque origin)

P. knowlesi

P. knowlesi����������������������������������

【Slide 21】

����?�

Anti-malarial properties of Vernonia

Human see, human do?

【Slide 18】【Slide 22】�������������

タンザニアの伝統医が野生動物の行動観察から新薬の発見をする。

Anti-malarial properties of Trichilia

Traditional healers in Tanzania acquire new medicines fromthe observation of wild animals
Babu Kalunde and the!
crested porcupine & elephant!
Mohamedi Seifu
Kalunde!
and the chimpanzee!

Joha Kasante !
and the snake!
ÔmulengeleÕ Aeschynomene nyassana!

【Slide 19】ÔmhefuÕ Trema orientalis!

【Slide 23】

サルマラリア ヒトマラリア【Slide 20】【Slide 24】

2nd Live Love Animals International Conference on Animal Care in Kobe 201223

������������
�����������
In 2004, a patent was registered in
the US by researchers at JacksonState University, Missouri for thephytochemotherapeutic applicationsof Vernonia amygdalina. Plant
extracts demonstrated inhibitive
activity against growth of neoplastic
cells, including those of human breast
cancer.

【Slide 25】

24

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

蚊が運ぶ病気と生態系の構造
Structure of Animal Communities and Transmission Dynamics of Mosquito Borne
Diseases
国立感染症研究所 昆虫医科学部第一室 室長・津田 良夫

Yoshio TSUDA, Chief, Laboratory of Taxonomy and Ecology, Department of Medical
Entomology, National Institute of Infectious Diseases (NIID)

Hello, I am Yoshio Tsuda of the National Institute ofmosquitoes. But let’s take a closer look. This is a copy

Infectious Diseases.

of a page from a textbook about mosquitoes, and it
shows a mosquito larva, which is commonly known as

As Prof. Murata mentioned during his introduction,a wriggler. This schematic diagram shows an image

I am first and foremost engaged in research onof a rice paddy. Perhaps most of you have not had

mosquitoes that transmit diseases to humans. These

this experience, but if you go to a rice paddy not longdays however, just like Prof. Huffman who is working

after the rice seedlings have been planted and lookon simian malaria, and Prof. Murata who is working

closely, you will see that there are a lot of wrigglers inon avian malaria, I have also been working on animal

the water. There are lots of rice paddies, particularly

malaria and particularly on the vectors that spreadin Southeast and East Asia including Japan. And thesemalaria.

places where wet-paddy rice cultivation is carried out
are among the most important sources of wrigglers andI expect most of you have an image of mosquitoes

mosquitoes.

as disagreeable insects that suck blood andspread diseases. But today, let’s try to improve ourAt the same time, there are many different organisms

understanding a little more about mosquitoes and thealso living in rice paddies. In particular, during themechanisms by which they spread diseases, including

Japanese rainy season in June, when wrigglers are

the fact that not all species of mosquitoes actuallycommon, the fry of fish such as killifish, crucian carp

spread diseases. And on that basis, let’s explore how

and loach are emerging from their eggs. These young

mosquitoes spread infectious diseases in animal

fish rely on wrigglers as a major part of their foodcommunities including to humans. To begin with,intake. Water fleas also feed on the newly hatched

I would like to talk more about what Prof. Murata

mosquito larvae and other insects also use them asmentioned in his introductory talk because, althougha food source. The number of wrigglers that hatch

mosquitoes do carry diseases, this need not be such

each year is enormous, and they can be considered anan enormous problem. We should also be thinking

important food resource for many other creatures.

about what the ecosystems that include mosquitoes canachieve.

While we are focused on the image of the adultmosquitoes that come around to suck our blood,

In terms of content, I will be talking about the dilution

these creatures are in fact eaten by a host of naturaleffect that Prof. Murata introduced at the start.

predators such as birds, bats, frogs, spiders anddragonflies that prey on insects. So they are an

Among the questions I am often asked about

extremely important food source for natural predators.

mosquitoes are “what goo d do mosquitoes do,

Additionally, the wrigglers feed on the straw from theand wouldn’t it be better all round if they didn’t

previous year’s rice crop found in the waters of rice

exist?” Certainly, we tend to see only the bad side of

paddies. In so doing they help break this material down.

2nd Live Love Animals International Conference on Animal Care in Kobe 201225

Given this other role as scavengers they are a vitalthem are still in use but in the old days water from allcomponent of the ecosystem and their absence wouldof these reservoirs was used to provide irrigation water

cause problems.

for rice growing. These days a different water supply
system is used so most of the irrigation ponds are no

Of course, mosquitoes do not only live in rice paddies

longer used. For the most part nobody takes care of theand, worldwide, there are about 3,000 known species.

unused ponds so they have become places where the

In Japan alone, about 112 species exist in the wild.

wrigglers, the mosquito larvae, hatch and grow. This is

These various species of mosquito have different

a photo showing one of these ponds. The water here isbreeding habits and their wrigglers hatch in different

an ideal breeding ground for wrigglers and so I selectplaces. I’d like to talk about that next.

places like this for catching mosquitoes.

Mosquitoes live in a wide range of habitats, but for

The surveys are carried out in this kind of hilly area

today’s talk I will show you some data from the rice

and also along riverbeds in locations where there are a

paddies of Izumo in Shimane Prefecture. I’m sure

few trees growing up from the riverbed.

everybody here today has heard of Izumo, which isaround here on the map. Here is Lake Shinji, and here

Within the rice paddy areas, capturing mosquitoes

is the rice paddy zone where the data was gathered.

inside the paddies themselves is difficult. So, because
in most rice-growing communities there is a Shinto

The reason why this particular area was chosen for ashrine surrounded by thick growing vegetation, I try tosurvey is that it is famous for the enormous number of

capture mosquitoes there using traps.

migratory waterfowl that visit, as you can see from this26

photograph taken in October of the survey year. These

Here in Izumo, there is another interesting survey spot

birds overwinter in Izumo but there are other species

known as the “Sagi Yama” which translates as “heronof birds that are summer visitors. Because this small

mountain” in English. In summer, it attracts a greatarea attracts so many migratory birds, if individual

many herons, but various other kinds of birds also

birds carrying infectious diseases arrive, it is easy

congregate there and build their nests, so there are afor the infections to spread. For instance, a mosquito

lot of nests concentrated in the same location. Suchbiting an infected bird and sucking its blood also takes

places are commonly called “sagi yama” in Japan, so

in disease-causing agents, or pathogens, present inwhen I was informed that there was a heron mountainthe bird’s blood. Later, this same mosquito may go on

in Izumo, I decided to collect mosquitoes there. Today,

to bite another bird or even a human being, thereby

looking hard at my own slides, I’ve noticed that

infecting them with the pathogen too. My main work

although the subject of today’s talk is “mosquitoes”,

involves investigating these kinds of infection routes

there is not a single mosquito image among them.

and the amount of risk they entail. I survey mosquitoes

Although I said I was going to talk about mosquitoes

in various places where migratory birds congregate,

this talk is actually less concerned with the mosquitoes

and Izumo is one of these places.

themselves.

This figure is small so it may be difficult to make out. It

This is the mosquito species Culex tritaeniorhynchus

is a relief map, and just here, where you can see a grid

which is a vector in transmitting Japanese encephalitis.

pattern, is the rice paddy zone. And naturally, because

Japanese encephalitis has been the biggest single

rice paddies need irrigation, there is a river. Here you

infectious disease problem in Japan. These days there

can see the characteristics of Izumo. This is the hilly

are almost no patients with the disease, but there is stillarea behind the rice paddies, and you may be able toa problem in that a number of people do become sicksee some small ponds dotted about, which are marked

every year who appear to be infected with it on firstin blue. These are irrigation ponds. Even today some ofglance. These mosquitoes were captured in the vicinity

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

of a pond. You can see that there are mosquitoes ofis why I was able to take a photograph of it. Here anddifferent colors, which means that they belong tothere in the heron mountain there are fallen trees, anddifferent species. So from this you can see that there

lots of mosquitoes rest on the tree branches.

are various species present. About one quarter of theindividuals collected were of C. tritaeniorhynchus. At

This species of mosquito was captured from a heron

the shrine however, the mosquitoes collected were ofmountain but I am not going to talk about this

only three colors so the total number of species wasparticular species today. In total I have captured about

very small. Again, C. tritaeniorhynchus accounted for

16 species of mosquito. Now I would like you to take aabout one quarter of the individuals. In riverbed areas

look at this red area. This is a mosquito that has sucked

we come across individuals of a few other species, butblood. It has a partially full belly but, as I’m sure youin these places too C. tritaeniorhynchus is extremely

know, mosquitoes can keep sucking blood until theircommon. This also shows that we capture different

belly becomes really huge. That one there is a full-fed

kinds of mosquitoes in different places.

mosquito. Those with only partially full bellies have
only sucked a little blood. Perhaps the host bird moved

Perhaps, what we can catch depends on what kinds ofand caused them to stop while they were feeding. Thismosquitoes live in what kinds of places. But, more than

one has a belly half full with blood while the otherthat, because movement and behavior varies between

half has already been digested. When the blood has

different species of mosquito, each species tends to live

been half digested, the mosquito produces eggs whilein the places it finds convenient and easy to live.

continuing to digest the remaining blood. In this case,the eggs are filling up about half of the belly space.

To find out what a heron mountain is like, let us take

The condition of this next one is that all the blood has

a look at the data obtained from the heron mountainbeen digested and the belly is bulging with eggs. Thisin Izumo. This particular heron mountain is not such a

one has a flat belly because it has not yet sucked any

big one. When I talked to some locals at the start of theblood at all. We catch different mosquitoes exhibiting asurvey they told me that it was certainly big in the oldvariety of physiological conditions.

days. When I went to the site, the first thing I noticed
was a strong smell. There were lots of bird droppings

My main subject today is the analysis of the bloodlying around and the smell was overpowering. It wasthat these mosquitoes hold. After bringing back thealso very noisy. These birds tend to gather in places

mosquitoes, I ask someone to assist me with the things

where it is difficult for people to walk. While the

I can’t do myself such as removing the animal blood

number of birds at this site was not particularly large itfrom the mosquitoes and extracting DNA from thewas a proper heron mountain in which night herons, as

blood. By obtaining the DNA base sequence from thewell as little herons and cattle egrets, had all built theirblood and checking this against similar base sequences,

nests en masse. Beneath this heron mountain, among

we are able to identify the species of animal from which

the vegetation and the whitish bird droppings, if you

an individual mosquito has sucked blood.

dip into the soil where you can see these little channels,
you can capture the mosquitoes that suck the blood ofHere, from the data obtained in Izumo you can see avarious animals.

lineup of the animal species we found to have been
the sources of the blood taken from the mosquitoes

Here is a different heron mountain that I visited inanalyzed. Here are the species of mosquitoes. Here,

Tokushima Prefecture during the following year. This issurrounded by a thin green line are the birds whicha huge heron mountain that is literally covered in nests.

include great egrets, cattle egrets and intermediate

The birds make their nest at heights from between two

egrets. These mosquitoes were taken from a heron

meters to five or six meters. This nest is positioned

mountain so there were a lot of heron and egret

approximately two meters above the ground, whichsamples but we also found some sparrow blood. Here

2nd Live Love Animals International Conference on Animal Care in Kobe 201227

we have some mammal blood samples including bloodfrom raccoon dogs and Japanese sika deer, which

Despite all this variety, basically all the different

doubtless live in the area, as well as from mice, etc.

mosquito species have a lot in common. First of all,

Then there were frogs, such as tree frogs. And here at

if we consider how their so-called blood sucking

the bottom we have grass lizards.

patterns are decided we find that these patterns are
determined by genetic factors. It turns out that house

As you can see, mosquitoes suck the blood of manymosquitoes have the strongest disposition to suck thekinds of animals ranging from birds to reptiles. Here,blood of birds while striped mosquitoes have a strong

I have also split the mosquitoes into several groups.

disposition to suck the blood of mammals. In this sense,

The red group is the group that feeds on frogs. This

their behavior is genetically determined.

kind of mosquito is the most familiar one to most of
us here today. It’s the kind that buzzes in your ear

However, that isn’t the end of the story. For example,

during the night and wakes you up with an itchy

on a heron mountain, where there are lots of herons

mosquito bite. The mosquitoes that have this red partand egrets, it is clear that the mosquitoes will tend tohere mostly feed on birds. This group has a strong

suck the blood of these birds. Where there are herons,

preference for bird blood. The next group is known as

the mosquitoes nearby will try to drink their blood

the striped mosquitoes. In Japan, when we go out inand where there are no herons, the local mosquitoes

the summertime and sit on a shady bench in the park,

will try to drink the blood of other animals. If there are

we are likely to be bitten by a mosquito in no time.

no birds, they will feed on mammals such as raccoon

The mosquitoes lying in wait for us are the striped

dogs or on other animals, depending on which species

mosquitoes. As a group, they limit their blood-sucking

are present and in what ratio to each other. Also,

activities to mammals in almost all cases. This next

some mosquito species prefer to feed at night and

one is of the species Uranotaenia novobscura, known

others prefer to feed during the daytime. Generally, in

in Japan as “chibi ka” meaning “small mosquito”. And

my understanding, the overall balance of biological,

indeed they are about twice as small as most otherbehavioral and genetic factors determines the blood-mosquitoes. They are particularly fond of feeding on

sucking pattern. In particular, whether or not it isfrogs. The reason I was able to capture quite a lot ofeasy to suck the blood of a particular kind of host is

this particular mosquito species at this heron mountain

determined by ecological factors. For instance, it iswas, as you might expect, because they came there toeasier to suck the blood of animals that do not movefeed on the frogs. This next type is vary rare, but therearound at night.

are also mosquitoes that suck the blood of snakes,
lizards, etc.

Looked at in this way, the heron mountain results I
outlined earlier can be much better understood. This

Many mosquitoes of the genus Culex, known as houseslide is very difficult to understand, but let’s take amosquitoes, are extremely fond of birds and also feed

quick look at it. Up to now I’ve been talking about

partially on humans and other mammals. Moreover,mosquitoes, but now I’d like to talk a little about thethere are species that feed almost exclusively on

diseases that are transmitted by mosquitoes. And then,mammals, and, similar to Uranotaenia novobscura,

to finish up, I will talk about how mosquitoes spreadthere are species that like feeding on frogs, althoughthese diseases among groups of animals.

they also drink the blood of mammals occasionally.

28

And then, there are more adventurous eaters that like

Mosquitoes act as vectors in transmitting a variety of

to feast on the blood of reptiles and amphibians. So

pathogens. Among the diseases spread by mosquitoes

all in all, there are different mosquitoes that follow athat infect humans are malaria, dengue fever andwide range of blood sucking patterns depending on theJapanese encephalit is. As for animal diseases,

species or group to which they belong.

mosquitoes carry avian malaria, simian malaria,

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

canine filariasis, etc. The mosquitoes’ capacity tountil they eventually burst out in the form of worm-

spread infectious diseases is determined by a number

like vermicules. In this form, the sporozolites enter theof properties. The first of these is their affinity withmosquitoes’ salivary glands. Then, when an infected

the pathogen in question, although not all species ofmosquito sucks the blood of another animal, themosquitoes can transmit disease. For instance, Culex

sporozolites are transferred inside the animal along

tritaeniorhynchus is the most proficient mosquito atwith the saliva. This is how malaria is spread.

transmitting Japanese encephalitis. This is because
the Japanese encephalitis virus does not propagate in

As is written here, when a mosquito sucks the blood

the bodies of other mosquito species. So the capacityof an infected animal, it takes about 12 days for theto spread infection is partially dependant on the

sporozolites to enter the salivary glands. So until

compatibility between the host mosquito and thethis amount of time has passed, the mosquito cannot

pathogen it carries.

propagate malaria. In this respect, the lifespan of themosquito is very important.

And then, in the first place, there is the question ofwhat kinds of animals a given species of mosquito

Next, I would like to talk about how mosquitoes spread

prefers to feed on. Another important property is themalaria among groups of animals, and my talk will

lifespan of individuals of a given species. And lastly,

cover basically the same subject as the dilution effectthere is the question of how many intervals of thethat Prof. Murata explained at the beginning.

species are produced. Ultimately, the capacity of agroup of mosquitoes to spread disease depends on the

For infectious diseases, groups of animals usually

cumulative effect all of these properties.

include those who become hosts for the pathogens
and those that do not become hosts. Or in other words

Today, I am particularly interested in two things,

those that do not become infected with the disease innamely, ‘affinity for pathogens’ and ‘blood-sucking

question. Mosquitoes pick up pathogens from infected

preference’. These two things determine thehost animals and transmit them to other animals whencombination of vectors - the mosquitoes that carry

they bite with the result that the disease is spread or

infections - and the animals that become the hosts for“amplified”. This is known as the ‘amplifier concept’. In

the particular pathogens carried. So this is the mostshort, a relationship exists between the mosquitoes andinteresting part for me.

their hosts moderated by the activity of blood sucking.

This slide may also be a little difficult to understand.

As for animals that do not become hosts, for instance,

The uppermost part of the slide shows a mosquito’s

if a mosquito carrying avian malaria bites an animal

body cut in half longitudinally. Here is the head, thisthat cannot be infected with this pathogen, the diseaseis the thorax, or chest, and here is the abdomen. The

will not be spread and so this will not aid the pathogen’

wings would be about here and the legs would be here,s propagation. The more often this happens, the more

but these have been removed.

the transmission of the disease will be diluted.

First, if we talk about malaria, for instance, whether it

Ultimately, this balance determines whether or not

is simian malaria or human malaria or whatever, whenan epidemic will occur. If the mosquitoes come intoa mosquito ingests the blood of an animal infected withcontact with large numbers of animals that can serve

malaria, the blood goes into a part of their abdomen

as hosts, the amplification effect causes an epidemic toknown as the midgut. After that, the malaria pathogens

spread. On the other hand, if the dilution effect is larger,

in the blood form lump-like swellings called oocysts

then the scale of epidemic will be limited. Unlike ticks,

on the outside of the midgut. The pathogens develop

mosquitoes are good at choosing their hosts, and so theinto a form known as sporozolites inside the oocysts

mosquito blood-sucking pattern is very important for

2nd Live Love Animals International Conference on Animal Care in Kobe 201229

determining the balance of whether or not an epidemic

totally unrelated to monkeys. So this contact between

will continue to spread.

mosquitoes and monkeys was an example of a full
dilution effect.

Now, I would like to share with you some data takenfrom an article on simian malaria that was writtenWith regard to simian malaria, we know the following

over 50 years ago. As Prof. Huffman explained earlier,things. We conduct research into avian malaria,

simian malaria has recently become a major problem inand when avian malaria comes up as a subject ofSouth East Asia, and half a century ago similar research

conversation, we can’t avoid the feeling that this disease

was carried out on this disease. Here in a forest, on

is happening in places where people have totallythe branches of larger trees, platforms were set up in

different lifestyles to Japan, such as South East Asia andvarious locations with cages on them with monkeys

Africa. But even so, when I was actually researchingplaced inside. The mosquitoes that came to suck theiravian malaria, I found very similar stories. I would likeblood were then captured. This research was conducted

to talk a little about this to close my talk.

in 2007, but exactly the same kind of research was
carried out 50 years ago. In some cases, humans sat inThis is a park in Tokyo where I conduct surveys. It isthe cages to attract mosquitoes.

a rather large park. There are lots of trees growing,and I am always capturing mosquitoes in this area.

I really like this data. These mosquito species were

In places where this sort of vegetation grows I cancaptured in a coastal mangrove forest. Using the same

capture mosquitoes by sweeping a net about. The placemethod the researchers captured mosquitoes frommay be in urban Tokyo but I am still able to find 11

the lowland swamp behind the mangrove forest, andspecies of mosquito here. This is a red house mosquito

from the hill country behind the swamp. Naturally,(Culex pipiens pallens) and this part surrounded in red

the mosquito species they found in these differingis the blood sucking part. My analysis was centered onplaces were different. The problem was that there wereindividual red house mosquitoes that had sucked blood.

spherical oocysts on the outside of the mosquito midgut
and there were sporozolites in their salivary glands.

My analysis found that between 3% and 5% of theThis was what the data indicated.

mosquitoes that had not sucked blood were carriersof avian malaria. In the case of mosquitoes that had

We know that this part marked in red refers to simian

sucked blood, an analysis of the abdomen revealed

malaria parasites. As the data shows, it means thatthat 18.6% were carrying avian malaria, while about

the species of mosquitoes that were captured coming

3% seemed to be carrying it in their chest or salivary

to bite the monkeys were carrying simian malaria.

glands. So out of every 100 of these mosquitoes, we

As I explained earlier, there is a connection between

can be sure that several are carriers of avian malaria.

this and the “amplification” of malaria. What the30

green part shows is that, as the researchers worked

This is a survey of the animals on which the mosquitoes

hard to establish, these chevrotains, or mouse deer,

I captured had been feeding. Those surrounded by the

become infected with this type of malaria. I don’t really

dotted lines are all birds. There was only one humanunderstand this blue part very well. But at the time,

blood sample, meaning that out of the 220 mosquitoes

and even now, we are unable to classify all the things

surveyed, only one had bitten a human. The abovethat emerge from the bodies of mosquitoes merely by

three species, namely jungle crow, sparrow, and great

their shape. Even so, from the shape of this one, I cantit, accounted for 83.4% of the samples obtained.

tell that it is certainly not simian malaria. And looking

This part in red shows the numbers of avian malaria

at this one, I would guess it to be avian malaria. This

samples obtained. The ratios were 29%, 21% and 40%,means that, although these mosquitoes came to feed

respectively. So in all probability, these three species

on monkeys, the malaria parasites they carried wereof birds can be considered as host species for avian

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012malaria in Tokyo. I think that under this situation, thefact that so many mosquitoes feed on these host birds

Moreover, in the survey area there were other animals

creates a great many contact points for amplifying thebesides birds and other mosquitoes than the species

spread of avian malaria and gives little opportunity forsurveyed. We had to limit the species of mosquitoes indilution effects to operate.

the survey, and so we chose those species that fed mostoften on birds. These included the red house mosquito

Actually, the species of mosquitoes that feed on birds

that I have been discussing. On this occasion we alsochange according to the season. For instance, thesurveyed a member of the striped mosquito family,

numbers of mosquitoes that feed on crows are low in

but we found that these mostly sucked the blood of

May but increase gradually through June, July andmammals. Although on this occasion we targeted avian

August. And in line with this increase in numbers, themalaria, if we understand the conditions under whichratio of mosquitoes carrying avian malaria parasites

avian malaria is sustained in more detail, we will have aalso changes.

better idea about how this disease, which is transmitted
to wild animals by mosquitoes, is able to exist.

This chart shows data on various species of birds. We
looked at three species - crows, sparrows and greattits. The vertical axis shows the risk of avian malaria
infection for each species. For the sparrows, marked
with a white circle, the risk of becoming infected withavian malaria from a mosquito bite is high at the start
but becomes lower in the summertime. The great titstend to be bitten little by little throughout the period
but there is no particular time when lots of greattits are being bitten. So the risk of this species being
infected with avian malaria, while present, is very
low. In the case of the crows, which have the biggest
problem, as the summer progresses through June,
July and August, the mosquitoes come to feed almost
exclusively on crows. Therefore the risk of these birds
contracting avian malaria is very high. In the course of
our research, we found out that another such high risk
period occurs around October.
Put more simply, when we examined the red housemosquitoes captured at the park, we found evidenceof blood from avian malaria host bird species such as
crows, sparrows and great tits, and also of non-hostbird species. In this case, a single mediator species andseveral host species are involved. When mosquitoes
feed more on non-host species, we can expect thedilution effect to be favored, but when they feed moreon host species we can expect to see the amplification
effect happening. In this way, the overall propagation
ratio of pathogens is influenced by how many host andnon-host animals are available to the mosquitoes.

2nd Live Love Animals International Conference on Animal Care in Kobe 2012

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【Slide 1】【Slide 5】【Slide 2】【Slide 6】【Slide 3】【Slide 7】【Slide 4】【Slide 8】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 9】【Slide 13】【Slide 10】【Slide 14】【Slide 11】【Slide 15】【Slide 12】【Slide 16】

2nd Live Love Animals International Conference on Animal Care in Kobe 2012

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【Slide 17】【Slide 21】【Slide 18】【Slide 22】【Slide 19】【Slide 23】【Slide 20】【Slide 24】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 25】【Slide 26】【Slide 27】【Slide 28】

2nd Live Love Animals International Conference on Animal Care in Kobe 201235

ダニが語る生物多様性～寄生生物の進化的重要単位の意義～
Mites Talk about Biodiversity - Ecological Significance of Evolutionarily
Significant Units in Parasites.
独立行政法人 国立環境研究所 侵入生物研究チーム・五箇 公一

Koichi GOKA, PhD, Invasive Alien Species Research TeamNational Institute for Environmental Studies

Hello everybody. I am Koichi Goka of the National

As I mentioned just now, parasites played a major roleInstitute for Environmental Studies.

in the evolution of sex according to an idea known as“the Red Queen’ hypothesis”. One of many current ideas

First of all, I must apologize in advance to those ofconcerning evolution, the hypothesis takes its nameyou listening in English because I was late presenting

from the character in Lewis Carroll’s second “Alice”

my slides and the script of my speech is too long. This

book, Through the Looking-Glass, and What Alice Found

means I will have to speak so fast that the simultaneous

There. In the story, the Red Queen says, "It takes all theinterpreters may not be able keep up. So please readrunning you can do, to keep in the same place." Heremy English subtitles where they appear.

the Red Queen is used as a metaphor for the idea thatspecies, individuals and genes have to keep evolving if

Also, as I have a great many slides please regard mythey are to survive. In order for multicellular species

presentation as if it was an animation.

to keep warding off continual attacks by viruses, thespecies needs to be equipped with sufficient variation

At the request of Prof. Murata I am going to talk aboutat the genetic level. Clearly, there is a difference in themites and ticks which are my specialty subject. In

tempo at which evolution can take place in viruses andparticular, I intend to focus on biodiversity as seen

in multicellular organisms consisting of an enormous

through the study of mites. At the same time, I’d likenumber of cells. So if multicellular organisms were toto explain in an autobiographical manner about why I

counter the attacks of viruses by means of ordinary

turned towards the study of mites and why I love them.

mutation alone, they would never be able to win
the evolutionary battle. Instead, they have evolved

In today’s workshop we have been hearing about

as a result of gene exchanges and the creation ofvarious kinds of parasites, including mites. Parasites are

new genotypes through sexual reproduction. This

organisms that have existed almost since the beginning

hypothesis is one of several that attempts to accountof life on Earth. Ever since that time they have evolved

for the evolution of sexual reproduction.

together with the rest of the biosphere. Parasites
attach themselves to other living things in order toParasites have various ways of making a living. Forlive and, as you are probably aware, there is a theory

example, some kinds of organisms parasitize higherthat they played a role in the development of sexual

order organisms, while others practice kleptoparasitism.

reproduction. Many organisms have male and female

This is a photog raph of a Great Reed Warbler

individuals and reproduction between two sexes is the(Acrocephalus arundinaceus) feeding a Common

most common way in which reproduction takes place.

Cuckoo (Cuculus canorus) chick in an example of what
is known as “brood parasitism”. When we consider that36

Many kinds of living creatures, from primitiveparasitism itself is always associated with the evolution

organisms such as insects and plants to human beings,of organisms, and that some parasitic species exist

exist as male or female, as this slide illustrates.

inside almost all species of living things, parasites can

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

therefore be said to play a major role in promoting

However, even though mites have very simple bodies,

biodiversity.

these animals are distributed everywhere on Earth.
Also, the life histories and food sources of different

When we think about it, we human beings are living as

species of mites are amazingly varied, and the total

the biggest parasitic organisms on the Earth, and ournumber of mite species is enormous. There are aroundstyle of parasitism creates numerous problems. But at

50,000 known species recorded at present, and it

the same time, parasitic organisms have very important

has been estimated that there may be up to a million

functions within the ecosystem. As two other lecturers

species of mites all told.

noted earlier, in a sense parasites play very importantroles, and while they are universally disliked, we also

Mite habits also vary widely. For example, somehave to recognize that their roles make them very

species even live in the ocean. In this respect, mites

precious organisms.

have gone farther than insects as no insects live in thesea. Mites can inhabit both salt water and freshwater

From this point on I am going to talk about mites.

environments where they engage in eating plants
and in sucking the blood of animals. Also, there are

My specialty is acarology (the study of mites andpredatory mites that eat other mites and there areticks), and although I am involved in a variety of work

scavenger mites. There are many varieties of mites inconcerning the preservation of biodiversity, the things

the soil which break down organic matter and convert

I actually like most are mites. Actually, there is an

it to inorganic matter which helps create a rich soil. In

organization called the Acarological Society of Japan.

these and other ways, mites are organisms that carry

And although the study of acarology is not very wellout a wide range of functions and help to support

known, there is also an International Congress of

biodiversity.

Acarology, which is held every four years. Two years
ago, I attended the International Congress of Acarology

Hearing such a story, you might very well be thinking

held in Brazil where, for an entire week I took part inthat however important mites may be as an element

happy and harmonious conversations with acarologists

in the web of life, as a human being you don’t likefrom around the world about mites and nothing but

them personally. You may wish also that mites weremites.

organisms that did not concern human life at all.
However, mites of the species Demodex folliculorum

Now, what kind of creatures are mites? Since many ofare in all probability living happily on your face. As ayou here today are specialists perhaps I don’t need tomatter of fact, almost 80% of Japanese people are hosts

explain, but many members of the general public areto this species. Of course, newborn babies don’t haveconfused that mites are insects. In fact, mites are notthese mites to begin with but when a mother rubs her

insects. The mite body is very simple. It consists of only

cheek against her baby’s face, the mites are transferred.

one section to which the limbs and mouth are directly

In this way, every human family has its own mites that

attached.

are passed down the generations. So please bear inmind that mites are an excellent part of biodiversity as

The insect body is separated into three sections,a whole.

the head, thorax and abdomen, with six legs andup to four wings attached to the thorax. That’s the

Now I will proceed with my own story. I will explain

insect archetype. So insects have a far more complex

about why I started to research the subject of mites instructure than mites do. Like spiders, mites have eightthe first place. When I was a student in the Department

legs. But the spider body is divided into two sections,of Agriculture at Kyoto University, I chose spider

cephalothorax and abdomen, so spiders also have amites as my research subject. These are a family of

more complex structure than mites do.

herbivorous mites that parasitize plant leaves. From the

2nd Live Love Animals International Conference on Animal Care in Kobe 201237

human standpoint spider mites are a terrible problem

available, the more mating the male will perform. Givenbecause they get onto various plants and suck thethe opportunity, a male will keep mating whenever andjuices from the leaves. They eventually kill the plants

wherever it can until the point where it almost dies ofand cause major problems as a worldwide agricultural

exhaustion. I totally got into mites as living organisms

pest.

that embody the male’s fate as it is. I earned a master’s degree and a PhD by studying mites and after that

Regarding their living environment spider mites begin

went to work for a pesticides manufacture where I waslife as eggs and go through several stages before

involved in developing miticides.

reaching the adult stage. They exist as males andfemales and reproduce sexually. Mating between males

At that time too, in the battle between mites andand females is effective only one time. When a female

miticides, we found that no matter how many types

engages in mating, her semen tank becomes full withof miticide we produced, they would soon lose their

the result that subsequent mating is ineffective. So

effectiveness. We investigated many things related

for males, the obtaining of virgin females is a very

to spider mites including their DNA and came to theimportant breeding strategy. In view of this, the kindconclusion that spider mites encompass a huge rangeof behavior spider mites have evolved includes pre-of diversity and that they maintain their resistance bymating guard behavior. The male climbs onto a female

continuously evolving. From this, I realized more clearly

pupa before the adult stage and guards it. Then, as the

how important biodiversity is. In any case, the miticides

female starts to cast off the chrysalis, the male helps

we developed didn’t sell well, and the company where I

out, and then performs mating immediately. This is thewas working declined. So I left that company and joined

spider mite’s reproductive strategy.

the research institute where I am employed now taking
up work on the preservation of biodiversity.

Given this state of affairs, virgin females are a very
precious asset for the males. If another male comes

My initial research work at the institute was on thealong, the result is a fight. Two males will enter into

subject of alien species control, and I am still mainly

a violent combat that involves fencing using theirinvolved in this work. The first alien species I worked

stylet-like mouthparts. (These mouthparts are usually

on was the Buff-tailed Bumblebee (Bonbus terrestris),

employed to suck the juices out of plants). Often thewhich was imported to Japan from Europe.

fight continues until one kills the other and while they
are engaged in this battle, a third male may come along

This species of bee has been bred commercially for use

and mate with the virgin female. This kind of thingin pollinating tomatoes and other crops in greenhouses.

occurs quite often.

A species native to Europe, the Buff-tailed Bumblebee
has been imported to Japan in large numbers. As you

38

In my student days, there was a laboratory class during

can see, the beehives are installed in greenhouses inwhich we could observe these things taking place

this way, and the bees fly around carrying pollen andthrough a microscope. I first got into mite researchcarrying out the pollination tasks that previously had

when I saw these things. I was very impressed that mite

to be performed by the farmers themselves, while

ecology was so graphically revealing of the meaning ofsignificantly improving the tomatoes’ productivity inreproduction.

the process.

There was another experiment in which we observed

However, some of these bees of European origin

what happens when one male is placed alone in a placeescaped from the greenhouses and began to live in thewhere there are many virgin females. The point of thiswild as an alien species, which had a very bad effect

was to test the male mites’ reproductive capabilities.

on the native Japanese Bumblebee (Bombus hypocrita

Results showed that the more that virgin females are

sapporoensis). Because of this, use of the Buff-tailed

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

Bumblebee is now strictly regulated by the Ministry

analysis is that it allows us to guess at once theof the Environment to ensure that individuals of thiseffective evolutionary times of organisms such as

species do not escape from greenhouses.

different mites and bees, which may be very different
morphologically and taxonomically, because they have

While I was carrying out this ecological risk evaluationsome similar genes. This method is beneficial in that

I thought that, in importing the beehives from Europe,

we can get to know the effective evolutionary times

they must have also brought in some strange parasites.

of species by studying the genes that control identical

So I looked for parasitic mites and detected thecharacters in different species and calibration can bepresence of an endoparasitic mite species called theperformed by means of the molecular clock method.

Tracheal Mite (Locustacarus buchneri) on the bodies ofUsing this method, I located the region governingthese bees. Then I surveyed how widely these mites had

the assembly of the enzyme cytochrome c oxidase

been introduced into Japan.

in the mitochondrial DNA of both mites and bees. By
searching and analyzing the genes in this region I was

However, I discovered that the Japanese Bumblebee

able to construct an evolutionary tree for each species.

also carries this same endoparasitic mite. As a resultof analyzing the mites’ DNA, I ascertained that theIn this way, I was able to show that the evolutionary

Japanese and European forms have different DNA,trees of both species were almost exactly the same

which means that these mites also exhibit local

shape. You can see that, in the case of the bees, there

endemism.

is a clear separation and differentiation between thebees of Eurasia and Asia on the one hand and those

While conducting this research, I have paid particularof America on the other. The evolutionary tree of theattention to parasite co-evolution. Originally parasites

mites has an awkward shape as you can see. In short,and their hosts evolve in a kill-or-be-killed relationship,

the shapes of the trees of the two species do not

but when they continue in this over a long period, they

match. What this means is that we can surmise thateventually become tired out. Then they move to the next

the bees and the mites did not evolve in the same way.

step, which is a symbiotic relationship. For example,

In particular, we know that, compared with the Asianthe power of viruses becomes attenuated because theirand Eurasian bees which have undergone a great deal

hosts are able to use their immune systems to controlof genetic differentiation, the mites that parasitize

the viruses to a certain extent. Accordingly, symbiotic

these bees exhibit only a very slight degree of genetic

relationships represent the evolutionary end point ofdifferentiation.

the battle between parasites and hosts.
On the other hand, you can see that in America, theWhat this means is that, in order to prevent pandemics

mites are parasitic on only one species of bee thatand limit the disease damage that may be caused by

has no mitochondrial DNA variation, but the mites

various parasites in future, it is important to know

themselves display very active genetic differentiation.

the preexisting evolutionary histories of hosts andparasites. In other words, it is important to know

From the standpoint of diversity, in the case of Asia andwhere the original parasite evolved and where it lives.

Eurasia, the basic diversity index of the host bees is

So in the case of the Tracheal Mite, I tried to find out

0.04 while that of the parasitic mites is an order below

about its origin and how it has evolved up to now bythat at only 0.005. On the other hand, in the case ofgathering bumblebees and the mites that parasitize

America, the basic diversity index of the host bees isthem from all over the world.

zero while that of the parasitic mites is 0.05, which is
the reverse of the Asian and Eurasian situation. What

I checked the DNA of each of the types of organism I

this means is that these mites and bees have undergone

found. A convenient point about molecular phylogenetic

different evolutionary processes and their origins are

2nd Live Love Animals International Conference on Animal Care in Kobe 201239

also different.

When we examine this in more detail, we find that it isdifferentiated into the ‘big blue’ family in the northern

Basically, a lot of evolutionary research has been carriedpart and the ‘big red’ family in the southern part of its

out on the bees. They are considered to have originatedrange, and at the root of this tree is the ancestor of allin the central region of Asia and then rapidly expanded.

the subspecies of Giant Stag Beetle that exist today. In

As for the mites, from their present mitochondrial

fact, the point of differentiation occurred 5.2 million

DNA tree, they are considered to have originated inyears ago. Even species of such small insects achieve

America and, after spreading across that continent, they

genetic differentiation over time by spreading out theirswitched their hosts to bees and travelled to Eurasia.

ranges, and in the case of the Giant Stag Beetle thishas created subspecies with a history spanning more

In America this mite is parasitic on locusts so we canthan 5 million years. We call such a population an

suppose that in some way it must have switched hosts

evolutionarily significant unit (ESU). In the near future,

to bees and then newly evolved into its present form of

we will no longer be able to classify organisms merely

Locustacarus buchneri.

as species, but we must also handle them as units inwhich we consider the evolutionary history of each

When a parasite switches hosts we often focus on the

genotype and its weight.

point that introduced alien species usually have a bad
influence on native species. But actually, when alienThis next story concerns conservation. Again, I am

species enter Japan, Japanese parasites also transfer togoing to turn my attention to mites. This time, I would

these alien species and begin evolving into new forms,

like to talk about mites that parasitize beetles. There isand Japanese parasites are also capable of generatinga genus of mites called Coleopterophagus that live bypandemics on occasion.

attaching themselves thickly to the backs of beetles. I’
m sure that people who keep beetles have seen theseAn example of this is a Japanese mite that has

mites. Many beetle lovers hate them and brush them

explosively parasitized alien bees despite the fact that

off the backs of their pet beetles with considerable

this mite does not parasitize native bees very much. So

enthusiasm. Because so many of these mites attachparasites can utilize different strategies for living and,themselves to the back of a single beetle, the beetle

in many instances, they can more easily parasitize hosts

looks poorly, which is why the common Japanese namethat they have not co-evolved with.

of this mite is the ‘kuwagatanakase’, which literallytranslated into English means “beetle’s bane”.

After mites and bees, I turned next to stag beetles.
Individuals of alien species in this family are imported

However, these mites are merely scavengers. They areinto Japan in large numbers for commercial purposes,

cleaners that eat the fungus that grows on the stag

and their introduction has created problems. In Japan

beetle’s back or any waste matter that gets attached.

alone, there are many species of stag beetles, andSo actually, these are very good mites as far as thethroughout Asia the amount of speciation is greater still.

beetles are concerned. For this reason, I would advise

The beetles shown here are all of different subspecies

people who keep these beetles not to remove theof a species called the Giant Stag Beetle (Dorcus

mites. Moreover, the kuwagatanakase can only live ontitanus), which is distributed in Japan and across Asia.

the backs of stag beetles. They would die even if they

In order to know how much genetic diversity thiswere placed on some other insect or given double thespecies possesses, I made an evolutionary tree using

amount of waste to eat. For this reason, it is considered

mitochondrial DNA. As a result, I discovered that thisthat the stag beetles and the mites that live on theirsingle species encompassed a huge amount of genetic

backs have co-evolved.

diversity. This one species exhibits clear differentiationin each region and each island throughout its range.

40

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

This is a close up of one of these mites. The photo will

appeal strongly to mite lovers, but if you hate mites you

have an opportunity to talk about mites, I purposefully

probably won’t be able to stand it.

put in a slide like this in an effort to educate people as
to the splendor and beauty of mites. However, theseI love mites more than beetles, so I want to know about

efforts often come to grief as the bigger I make thethe evolution of mites. Actually, these kuwagatanakase

slides, the more people say they feel sick. When I drewmites are not only found on Japanese stag beetles.

this image, I thought it was well done, so I sent it to

They also live on stag beetles all over Asia. I performed

the publisher of an international acarology journal

a search of the beetles’ DNA and, along the way, I

in the United States and they used it on one of theiralso took a great deal of interest in the sort of trivia

cover pages. The publisher was very impressed withthat only an acarologist would care about. I refer tothe image and assumed I was an artist. He invited methings such as the amount of genetic diversity within

as an artist to attend the journal’s 60th anniversary

the genus Coleopterophagus, the evolutionary history

party and requested that I bring the original image

between the beetles and the mites, and place fromwith me. I felt frustrated that I wasn’t recognized as an

where the kuwagatanakase mites originally came. In

acarologist, so I told the publisher, “I am not an artist,

order to find out as much as I could I collected stag

I’m an acarologist!” and sent them one of my papers.

beetles from all over Asia and the mites attached to

They replied, “Never mind your paper! Just send yourtheir backs as well. Using the information in their DNA

picture.” Since the party was being held in Ohio andI built up an evolutionary tree. This is a mitochondrial

it was too much bother for me to travel there, in theevolutionary tree of the stag beetle species living in

end I sent the picture after all. This made the publisher

Asia including the Giant Stag Beetle. Since the tree is sovery happy, and they turned it into a memorial postage

large, you can’t read the writing on this slide, but pleasestamp. So if you are in the United States, please look

don’t worry about that.

out for a memorial postage stamp with a mite pattern
and buy it.

In order to complete this evolutionary tree, I had to readapproximately 2,000 bases. From this evolutionary tree,

Another thing, when the COP 10 conference on

we can see that the host species has a huge amountbiodiversity was held the year before last, the Emperorof genetic diversity. And here is the evolutionary tree

and Empress visited our research institute and I wasof the mites that live on these beetles. Somewhat

one of the people guiding them around. At that time, I

surprisingly, this species’ genetic differentiation has

put a lot of pictures on the wall. The Empress showedalso progressed to a great extent. Moreover, if we try tointerest and asked me what they were. I’m sure thatlink up the relationship between the host and parasite,

up until then she hadn’t seen any big pictures of mites.

we can obtain a one-to-one relationship like this.

From that point, I became a bit hyperactive. I stopped
talking about the institute and about biodiversity

This means that the mites have not simply been drifting

and instead I talked about mites for ten minutes. The

in their evolution and their mode of living. They have

Emperor and Empress seemed very impressed and theywalked and lived together with their beetle hosts along

took one of the pictures back to the Imperial Palace

an evolutionary history that stretches back for overwith them. This became a historical monument as

12 million years. The fact that different populations of

the first picture of a mite to be taken into an Imperial

these two species have been evolving together for such

residence.

long time also indicates that these small mites also exist
as evolutionarily significant units.

Recently I appeared on TV, where I had photos ofmyself taken with many entertainers. Among them,This is a computer graphic image of a Tracheal Mite.

Shokotan (Shoko Nakagawa) took the most interest in

I do computer graphics as a hobby and I’m proud tomites. I told her a lot about how mites couple, and she

say that this image is one of my own efforts. When I

responded that she would like to see mites coupling. So

2nd Live Love Animals International Conference on Animal Care in Kobe 201241

I devoted all my time over Golden Week to completingthe species level. What has caused this? I thought it

a computer graphic image of two mites coupling. Thiswas curious that such extensive genetic exchange wasis that picture. The larger mite is the female, and thetaking place in such a limited region as Japan. So I

other one, which is holding up its bottom, is the male.

studied those individuals for which differentiation was

They take a very unusual sexual position. I gave thisparticularly pronounced, and ascertained that they

picture to Shokotan and she was very happy with it.

were all parasitic on carnations.

Moreover, when former Environment Minister Ryu
Matsumoto visited our institute, I also presented the

As these mites are specifically parasitizing carnations,same image to him, explaining, “This is a picture of two

it would be quite reasonable if they were geneticallymites coupling.” He casually brought it back with him,

homogeneous. So why was there this much genetic

but he actually had it put up on the wall of his office.

variation among them? I studied this question andSince he later resigned in controversial circumstances,

found out that most carnations are not grown in Japan

this is now a sad memory for me.

but are cultivated abroad and imported and sold as cut
flowers. These carnations are grown in many countries,

I’ve wandered off the subject, but to come back to point

and Two-spotted Spider Mites live in all of these

I wanted to make, even mites exhibit endemism andcountries. That’s the reason why there is now so muchdiversity. These days, however, with problems suchgenetic diversification among the Two-spotted Spider

as globalization and the introduction of alien species,

Mites that live in Japan.

the endemism and diversity of mites is in a criticalsituation.

In fact, I interviewed carnation farmers asking themwhere they purchased their carnations, and found that

This is a spider mite. These mites are agricultural pests.

they imported them from many countries as shown

I myself researched this both in my student days andhere. Moreover, almost all the mites that exhibit genetic

when I was working for the pesticide manufacturer.

differentiation are of foreign origin. Clearly these mites

Spider mites also exhibit endemism and diversity, andwere brought into Japan from overseas.

this is also in a critical situation. As an example, thisTwo-spotted Spider Mite (Tetranychus urticae) is one

An even more troublesome thing is that because theseof the many spider mite species and it is a serious

mites are pests, their drug sensitivities differ from those

agricultural pest on a worldwide scale. This speciesof ordinary spider mites. When exposed to miticide,comes in two color varieties—a red variety and a green

since the green type mites are very similar genetically,variety. This is a rare intra-species variation, which isthey all die straight away, and most of the red typeconsidered to be part of an on-going process of genetic

monophyletic mites, which are the main variety in

speciation. Accordingly, I have taken an interest in thisJapan, also die.

process and tried to study the degree of differentiationof the intra-species variation. And to do this I have

However, such miticides are totally ineffective against

collected red and green mites from all over Japan andthe spider mites that have been imported from abroad

Europe and analyzed their DNA.

because these mites had sufficient genetic resistanceto the miticide from the beginning. When this much

As a result, I was able to construct this evolutionary

genetic variation is so widely distributed within atree, and from it I found that the green mites became

group, there must be some mites that have resistance,

differentiated from the red mites, perhaps throughand these survive and breed.

pigment decolorization. Here, I would like to draw

42

your attention to the fact that the red mites’ genetic

Since these mites are pests, they should have beendifferentiation is unusually active even within Japan.

prevented from entering the country by means of plantIndeed, this differentiation has progressed almost toquarantine in the first place. So I investigated why so

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

many things (that should have been incinerated) wereto the black list system is that the release ratio ofallowed to come into Japan. Now, the World Tradeagricultural pests has become higher. Since only thoseOrganization is aiming for global free trade and a part

species deemed to present a risk are listed, almostof that effort is the Trans-Pacific Partnership (TPP). This

all agricultural and forestry pests can now be freelyorganization, which promotes free trade, is promoting

imported.

agricultural pests as well.
The TPP, which has become a major subject of talk,Originally, the Two-spotted Spider Mite was on thepresents us with the same situation. One government

list of species for which importation into Japan was

minister has described the TPP as the ‘third opening

prohibited. However, in 2004, they were found onof the country’. Whenever the country is opened theapples imported from the United States and the apples

number of alien species increases. So if we think about

were incinerated. This provoked an angry response

protecting biodiversity in a true sense, in future, wefrom the US side, which sued Japan through the WTO.

should pay a lot of attention to this TPP argument fromThe US argument was that since the Two-spotted Spider

the ecological science and animal hygiene standpoints.

Mite already existed in Japan it was unreasonable toquarantine imports from the US on the grounds thatAs a case example, I’d like to talk about a dangerous

they harbored the mites. Japan lost this case and as amite that is brought into Japan together with imported

result, was forced to abolish the quarantine measuresliving organisms. Up to now I have been talking about

for the Two-spotted Spider Mite, allowing this species

rather mild things unrelated to human health. But

to be imported freely into the country.

what I’m going to talk about now are ixodid - hardbodied ticks - which feed on the blood of animals andThis is a very inconsistent approach. As I explained

spread various diseases. The most dangerous ones canearlier, perhaps these mites do look the same buttransmit zoonoses to humans.

they have very different genes and their sensitivity to
drugs also varies widely. Now they are freely imported.

In the current situation, there is concern that with the

And although most of us are unaware of the fact, thelarge numbers of reptiles being imported into Japanliberalization of agricultural pest species has been

and with almost all of them taken from the wild, many

proceeding apace.

kinds of ixodid ticks are being brought in with them.
What is even more troubling is that legal protections

The Plant Protection Act was finally revised in thesuch as guarantees on the safety of imported animals

spring of last year. Under the revised law, Japan has

mandated under the Infectious Disease Law by the

moved from a ‘white list’ system to a ‘black list’ system.

Ministry of Health, Labour and Welfare and animal

Under the white list system, the importation of all pests

quarantine provisions are limited to warm-bloodedthat damage plants was banned in principle. Only thoseanimals. Reptiles and amphibians can be brought into

species of insects, etc., that were on the white list (suchJapan without any guarantees at all. I was concerned

as stag beetles and unicorn beetles) were considered

about this so I began a project to study the mattersafe to import. The white list was a very strict

jointly with Prof. Kawabata of the National Institute ofregulation. By contrast, the black list system operates

Infectious Diseases. In the course of this research, as I

on the principle that all species can be imported unlesshad expected, we found ticks of the genus Amblyomma

they have been examined and specifically placed on

on turtles and many kinds of mites attached to reptiles

the black list. So only those species considered toimported into Japan.

constitute a risk are prohibited from being brought into
the country. Any species not on the black list can be

Moreover, the number of countries from where

freely imported. This is the same system as specified

these living things are imported is surprisingly large,

by the Alien Species Act. A consequence of the change

including such widely separated places as Sri Lanka,

2nd Live Love Animals International Conference on Animal Care in Kobe 201243

Tanzania, and Suriname. I wasn’t even sure of precisely

Parasites and their hosts establish peaceful andwhere some of the countries of origin were so, due

stable relations after a long period of co-evolution.

to this research, I also had an opportunity to study

Biodiversity is a cradle in which these organisms cangeography. What especially worried me was that thegrow and develop together, but it can also serve as amites themselves might be carrying some dangerous

cradle for pathogens. When human beings destroy thispathogens so I asked the NIID to do some testing. The

biodiversity there follows a collapse of evolutionary

results came back positive. We discovered the presence

history and co-evolution, and in its place, pandemicsof the bacterial genus Borrelia which can infect humans

occur. Examples of this process at work include SARS

with many diseases. I studied the genetic differentiationand HIV/AIDS. They have their respective origins inof this genus and produced an evolutionary tree. I

horseshoe bats in China and in chimpanzees in thenoticed that the genus includes a species that is the

Cameroon, and were living quietly with their hosts. The

agent for Lyme disease and a species that causes tick-reason why they turned into emerging diseases is thatborne relapsing fever. This information was so complete

humans destroyed the habitats of the hosts, allowingthat I was able to make use of it in conjunction withthe viruses to cross the species barrier. Now the viruses

the evolutionary tree. The new Borrelia bacteria weare desperately evolving in order to survive in theirdiscovered were not members of either of the above

new hosts, human beings, of which there are about 7

species. They are a totally new type. This is a very

billion individuals at present. They have already arrived

dangerous situation because nothing is clear includingin the urban jungle.

the pathogenicity and, even more troublingly, no risk
evaluation has been made of these bacteria because it

The important thing here is that, in line with thehas not been possible to grow them in isolation up to

evolutionary rule that has always been followed until

now. In view of this I have to say that, under the current

now, hosts that are infected either die or else they

free trade situation, people who want to keep reptiles

survive. Those that survive are more likely to passas pets need to seriously consider the potential risks

on their genes to the next generation. In this way,

they are taking.

succeeding generations have better resistance to theeffects of the virus and the two species gradually enter

For my own research I previously chose only visible

into a symbiotic relationship. Today, however, welarge alien species. But now I am paying attention toattempt to contain dangerous viruses by any means

invisible alien species as well. What set me off in thisavailable including the use of antiviral drugs anddirection was a disease called chytridiomycosis, another pharmaceuticals. The result is that the viruses

infectious disease of amphibians that is often fatal.

continue to evolve rapidly in response to the drugs

Perhaps you have heard of it. Chytridiomycosis is anthey are exposed to. This becomes a non-stop fightemerging disease that has spread worldwide and wiped

between humans and viruses. Only humans break thisout entire species of frogs in some places. It landed

evolutionary rule. When we consider the evolutionary

in Japan several years ago and caused considerable

history of viruses there is a high possibility that humans

uproar. I dislike frogs but I worked on this theme out ofwill lose this fight one day.

necessity, and I was shocked by my results. I don’t havetime to go into the details now, but I’d like to tell you

So, if we want to stop this fight, it is important for

about it when I get an opportunity.

humans to keep at a distance from biodiversity fromnow on. The idea of “natural symbiosis” or “living in

As Prof. Nakamura said at the beginning, the reason

harmony with nature” is often talked about. But thiswhy such emerging diseases that are close to being

does not mean it is OK for owners to kiss their pets or

zoonoses are being encountered more often now issomething like that. Humans have evolved as naked

because biodiversity is being gradually destroyed.

apes who can survive in the concrete jungle so when wetalk about ‘natural symbiosis’ it is important to apply

44

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

some kind of zoning between the wild world and thehuman world and to properly separate their functions.
In that sense, protecting biodiversity has anotherimportant meaning. It can serve as a means ofpreventing the expansion of emerging infectious
diseases. Biodiversity does not exist only to be
applied to beautiful living things. Even parasites areencompassed within biodiversity. So please extend yoursupport to the mites and ticks too.
【Slide 1】

That completes my talk. Thank you very much forlistening.

【Slide 2】【Slide 3】【Slide 4】

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【Slide 5】【Slide 9】【Slide 6】【Slide 10】【Slide 7】【Slide 11】【Slide 8】【Slide 12】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 13】【Slide 17】【Slide 14】【Slide 18】【Slide 15】【Slide 19】【Slide 16】【Slide 20】

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【Slide 21】【Slide 25】【Slide 22】【Slide 26】【Slide 23】【Slide 27】【Slide 24】【Slide 28】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 29】【Slide 33】【Slide 30】【Slide 34】【Slide 31】【Slide 35】【Slide 32】【Slide 36】

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【Slide 37】【Slide 41】【Slide 38】【Slide 42】【Slide 39】【Slide 43】【Slide 40】【Slide 44】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

【Slide 45】【Slide 49】【Slide 46】【Slide 50】【Slide 47】【Slide 51】【Slide 48】【Slide 52】

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【スライド 53】

【スライド 57】

【スライド 54】

【スライド 58】

【スライド 55】

【スライド 59】

【スライド 56】

【スライド 60】

りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012