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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りぶ・らぶ・あにまるず 神戸アニマルケア国際会議 2012

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