Keywords: pollution, eutrophication, parasites, infectious diseases, fish, sticklebacks, Baltic Sea.
Humans strongly influence the environment and most people are aware of the dramatic impacts of pollutants or climate change on wildlife. However, it has recently become obvious that our impact on nature can also influence parasites thereby affecting wildlife and human health. My research fits in this framework.
In details, I investigate the impact of eutrophication, a particular type of water pollution, on parasitism of Baltic populations of the threespine stickleback (Gasterosteus aculeatus). My research relies on the use of multidisciplinary approaches linking mechanisms (e.g. immunity) and processes (e.g. food-web) shaping epidemics in these populations of fish.
We monitor epidemics in stickleback populations from several locations in Southern Finland that are characterized by different levels of eutrophication. Fish are caught at three times during the breeding season: in May when they arrive at the breeding grounds, in June at the height of the breeding season and in July when the breeding season ends. A number of environmental data (chlorophyll a concentration, salinity, pH, surface temperature) are collected as well.This allows us to (1) determine correlations between eutrophication and health of fish populations in the Baltic Sea and (2) experimentally investigate the underlying mechanisms explaining the observed patterns.
Where to look for parasites?
The
threespine stickleback (Gasterosteus aculeatus) has become an established model in the study of
host-parasite interactions.This fish preys on a wide range of aquatic
invertebrates and is preyed by several vertebrates (fish, birds, sea mammals
and even humans!). Because
of this position in the food-web, stickleback carry several kinds of parasites
that use them to grow and/or reproduce. Here, I give an overview of the
diversity of the parasites infecting Baltic sticklebacks and describe their
amazing life-style.
Ecto-parasites
Ciliates
Trichodina sp. (skin,
fins, gills, nostrils - Size: >0.5mm) source for picture: http://www.passionbassin.org/
Trichodina parasites
belong to the family of Urceolarridaen (Order: Peritrichidia). These protozoans
mainly feed on bacteria and are considered as ecto-commensals. However they
also scrap and eat epithelial cells on their hosts causing irritation. The
gills are especially vulnerable and irritations can trigger breathing problems
and unbalance ionic regulation. This is especially true when they are quite
abundant on infected hosts. Such a problem is often encountered when organic
materials are abundant and fish experience stressful conditions as in fish
farms. Trichodina can multiply fast on their host as reproduction in
ciliates can be both asexual and sexual. During sexual reproduction, there is
no fusion of independent gametes but two entire individuals come together
temporally and exchange mononuclei (conjugation).
Monogenans
Gyrodactylus sp. (skin, fins
and gills - Size: 0.5mm) source for picture:
http://www.koiandponds.com
These hermaphroditic flukes attach
to the host by a modification of the posterior end, the opisthaptor, which
normally possesses hooks and effectively holds the parasite to the skin of the
fish. Zygotes exhibit serial polyembryony: in its developing uterus a second
embryo is already developping (so a bit like a Matryoshka doll). Soon after birth,
the parasites start giving birth to the embryo, and then can mate
and produce additional offspring. Consequently populations can build up quickly
on the host. Transmission requires direct or close contact. Therefore
controlling the spread of the parasite can be very problematic at fish farms.
Copepods
Most
copepods are free-living but
many are parasitic. Caligidae are probably the most renowned
representatives as they occasionally cause fish kills at fish farms.
Thersitina gasterostei (skin, fins, inner side of the
operculum and gills - Adult size: 0.5 to 1mm)
Dispersion occurs during a brief
planktonic larval stage. After mating, females seek for stickleback during the
summer on which they will remained attached to. Infections can involve several
hundreds of Thersitina and thus can especially damage the gills of the host.
Caligus lacustris (skin and
fins - Adult size: >5mm)
These
lice feed on fish blood. Females can grow to 8mm long and carry egg
bags that can reach up to 2.5 times their size. These generalists anchor
to the skin and fins of the host and can transmit a number of
pathogens.
Branchiurids
Branchiurids, so-called "carp
lice" or "fish lice", are crustaceans that temporally parasitize fishes. They superficially resemble copepods, but differ from the latter in
the possession of compound eyes. They are found
on both fresh and salt water fishes.
Argulus foliaceus (skin, fins,
gills - Adult size: 5mm)
This generalist typically uses two strategies to reach a fish: during the day, they "sit and wait" for a fish to pass by, while during the night, they actively search for the host. Once
a fish is approaching, the parasite leaves the substrate to attache
itself to the host with its
modified first pair of antennae. Then, the modified mouth
parts pierce the skin of the fish and the parasite starts feeding on the
blood
while simultaneously releasing anti-coagulant substances. The wounds are
often infected by opportunistic bacteria and fungi which can weaken
fish (to death). Argulus parasites can stay several weeks on the same
host and mate on them.
Reproduction in Finland seems to
occur only during the warmest months i.e. May to August during which females
lay their eggs on hard substrates in shallow waters (<1m). During their
lifetime (sometimes >2 years), females produce 5 to 10 clutches containing
up to 150 eggs. Freshly-hatched metanauplii larvae carry limited sets of
resources and hence seek for hosts to infect. Nevertheless, the high motility
of fish makes host encountering unpredictable. Research conducted on related
species indicates that females could show adaptive bet-hedging strategies when laying
eggs in order to counteract this hazard and maximize their fitness. Maturity is
reached at the tenth developmental stage (4-5mm length, i.e. 40 days after
hatching at 15°C, the full adult size is reached at 80 days).
Endo-parasites
In
Southern
Finland, stickleback can serve either as definitive hosts (the fish is
used for sexual reproduction) or as secondary intermediate hosts (the
fish is used for growth or for transmission) of several endo-parasites. A
number of these parasites are able to manipulate the behaviour of their
intermediate host to increase their chances to get to the next host in
their life-cycle. This is especially true for parasites that use the
food web to transmit to the predator of their intermediate host (i.e.
trophic transmission). Accordingly, endo-parasites can be quite
sensitive to environmental changes
and their presence can indicate the well-functionning of ecosystems.
Digenean Trematodes (Eye Flukes)
Typically, eye flukes require three
hosts to complete their life cycles: a mollusc, a fish and a bird. Eggs are
released with the faeces of the definitive host into the water. From the
egg hatches a free-living miracidia larvae infective to a mollusc.
Inside the first intermediate host the parasite will encyst as sporocyst that
will produce asexually hundreds of cercariae. Free-living cercariae seek
for the second intermediate host (fish, amphibians) in which they will develop
as metacercariae and induce severe pathologies (blindness, malformations)
in order to make their host more susceptible to predation by birds where they
establish in the gut.
Life cycle
of Diplostomum spathaceum
Diplostomum spp. (in the
lens, in the vitreous body and in the retina - Size: >0.5mm)
From Lymnaea snails, sporocysts
release cercariae in seek for fish to infect. The production of cercariae is
highly dependent towards temperature so that transmission downstream hosts is
only possible between May to August in Southern Finland, most of infections
occuring during the late summer. Once in the lens of the fish, metacercariae
causes blindness due to the metabolic wastes.
Apatemon sp. (vitreous
body - Size: >1mm)
As
for Diplostomum spp., asexual production of cercarial stages takes
place in lymnaeid snails. They later encyst in the eyes of fish and are
transmitted by predation of infected fish to bird final hosts.
Cestodes
Cestodes need to infect a variety of
intermediate hosts in which they pass through specific developmental stages
before the adult establish in the digestive tract of vertebrates. In Southern
Finland, Baltic populations of threespine stickleback can serve as intermediate
or definitive hosts for a number of cestodes. Some tapeworms are said
autogenic when they spend their entire life-cycle in aquatic environments (e.g.
Triaenophorus crassus) or allogenic when the life cycle involves
terrestrial and aquatic stages (e.g. Schistocephalus solidus).
Schistocephalus solidus (body cavity
- Size: >5cm)
S. solidus
has established as model system for studying complex life-cycle
parasites because all stages of the parasite can be easily reared and
manipulated in the laboratory. Non-invasive tracking of the course of
infection in
the first host and the availability of the complete genome sequence of
the secondary intermediate host (i.e. the threespine sitckleback)
further provide good opportunities to study host-parasite interactions
at
a very fine scale. Finally being a simultaneous hermaphrodite able to
reproduce
by selfing and crossing, this cestode has also become a model system in
the
study of sexual selection and life-history theory.
Life cycle
of Schistocephalus solidus
To
complete its life cycle, this
tapeworm depends on three hosts: a cyclopoid copepod, a threespine
stickleback
and a warm blooded vertebrate. After hatching, free-swimming coracidia
larvae are eaten by cyclopoid copepods in which they develop as
procercoid. Once infective for the next host, the parasite manipulates
the behaviour
of the copepod to enhance transmission to the downstream host, the
threespine
stickleback. Most of the growth of the parasite occurs in the fish host
and
plerocercoid larvae often reache sizes comparable to the size of its
fish
host. Indeed, the bigger the parasite is the best are its chances to
establish
in the final host. As a consequence, this parasite imposes a strong
selection
pressure on host populations. Transmission to stickleback seem to occur
during
the late summer when young sticklebacks are feeding on small preys such
as copepods.
However, the growth of the parasite does not start immediately. Indeed
it has
been shown that host size was a constrain for the development of
plerocercoids. Therefore established parasites have to wait until the
host is big enough to start growing massively. Transmission to the
definitive
host enhanced by lowering the response to predation risk of infected
stickleback. Hence the parasite overwinters in the fish in high
latitudes
and is transmitted during the summer. Eggs are then released with the
bird
faeces into the water.
Microsporidians
Glugea anomala
(can be everywhere - Variable size)
Microsporidians are intra-cellular
parasites directly transmitted via the emission of spores. Highly contagious
spores enter the host and prenetrate the epithelium. Via the blood
stream, the parasite make its way to the skin, muscle or other tissues. In host
cells the parasite undergoes asexual division and starts producing spores.
Infected cells are filled with spores causing strong hypertrophy (infected
cells become round white cysts/xenoma). Spores are released into the water from
lesions on the body surface. Host death is triggered by the degeneration of
infected cells.
Keywords: parasites, life-cycle, life-history, threespine
stickleback, Gasterosteus aculeatus
Nota bene: All pictures, drawings and figures for which source is not cited are the property of Alexandre Budria.
Humans strongly influence the environment and most people are aware of the dramatic impacts of pollutants or climate change on wildlife. However, it has recently become obvious that our impact on nature can also influence parasites thereby affecting wildlife and human health. My research fits in this framework.
In details, I investigate the impact of eutrophication, a particular type of water pollution, on parasitism of Baltic populations of the threespine stickleback (Gasterosteus aculeatus). My research relies on the use of multidisciplinary approaches linking mechanisms (e.g. immunity) and processes (e.g. food-web) shaping epidemics in these populations of fish.
We monitor epidemics in stickleback populations from several locations in Southern Finland that are characterized by different levels of eutrophication. Fish are caught at three times during the breeding season: in May when they arrive at the breeding grounds, in June at the height of the breeding season and in July when the breeding season ends. A number of environmental data (chlorophyll a concentration, salinity, pH, surface temperature) are collected as well.This allows us to (1) determine correlations between eutrophication and health of fish populations in the Baltic Sea and (2) experimentally investigate the underlying mechanisms explaining the observed patterns.
Where to look for parasites?
The threespine stickleback (Gasterosteus aculeatus) has become an established model in the study of host-parasite interactions.This fish preys on a wide range of aquatic invertebrates and is preyed by several vertebrates (fish, birds, sea mammals and even humans!). Because of this position in the food-web, stickleback carry several kinds of parasites that use them to grow and/or reproduce. Here, I give an overview of the diversity of the parasites infecting Baltic sticklebacks and describe their amazing life-style.
Ecto-parasites
Ciliates
Trichodina parasites
belong to the family of Urceolarridaen (Order: Peritrichidia). These protozoans
mainly feed on bacteria and are considered as ecto-commensals. However they
also scrap and eat epithelial cells on their hosts causing irritation. The
gills are especially vulnerable and irritations can trigger breathing problems
and unbalance ionic regulation. This is especially true when they are quite
abundant on infected hosts. Such a problem is often encountered when organic
materials are abundant and fish experience stressful conditions as in fish
farms. Trichodina can multiply fast on their host as reproduction in
ciliates can be both asexual and sexual. During sexual reproduction, there is
no fusion of independent gametes but two entire individuals come together
temporally and exchange mononuclei (conjugation).
Monogenans
These hermaphroditic flukes attach
to the host by a modification of the posterior end, the opisthaptor, which
normally possesses hooks and effectively holds the parasite to the skin of the
fish. Zygotes exhibit serial polyembryony: in its developing uterus a second
embryo is already developping (so a bit like a Matryoshka doll). Soon after birth,
the parasites start giving birth to the embryo, and then can mate
and produce additional offspring. Consequently populations can build up quickly
on the host. Transmission requires direct or close contact. Therefore
controlling the spread of the parasite can be very problematic at fish farms.
Copepods
Most
copepods are free-living but
many are parasitic. Caligidae are probably the most renowned
representatives as they occasionally cause fish kills at fish farms.
Dispersion occurs during a brief
planktonic larval stage. After mating, females seek for stickleback during the
summer on which they will remained attached to. Infections can involve several
hundreds of Thersitina and thus can especially damage the gills of the host.
These
lice feed on fish blood. Females can grow to 8mm long and carry egg
bags that can reach up to 2.5 times their size. These generalists anchor
to the skin and fins of the host and can transmit a number of
pathogens.
Branchiurids
Branchiurids, so-called "carp
lice" or "fish lice", are crustaceans that temporally parasitize fishes. They superficially resemble copepods, but differ from the latter in
the possession of compound eyes. They are found
on both fresh and salt water fishes.
This generalist typically uses two strategies to reach a fish: during the day, they "sit and wait" for a fish to pass by, while during the night, they actively search for the host. Once
a fish is approaching, the parasite leaves the substrate to attache
itself to the host with its
modified first pair of antennae. Then, the modified mouth
parts pierce the skin of the fish and the parasite starts feeding on the
blood
while simultaneously releasing anti-coagulant substances. The wounds are
often infected by opportunistic bacteria and fungi which can weaken
fish (to death). Argulus parasites can stay several weeks on the same
host and mate on them.
Reproduction in Finland seems to
occur only during the warmest months i.e. May to August during which females
lay their eggs on hard substrates in shallow waters (<1m). During their
lifetime (sometimes >2 years), females produce 5 to 10 clutches containing
up to 150 eggs. Freshly-hatched metanauplii larvae carry limited sets of
resources and hence seek for hosts to infect. Nevertheless, the high motility
of fish makes host encountering unpredictable. Research conducted on related
species indicates that females could show adaptive bet-hedging strategies when laying
eggs in order to counteract this hazard and maximize their fitness. Maturity is
reached at the tenth developmental stage (4-5mm length, i.e. 40 days after
hatching at 15°C, the full adult size is reached at 80 days).
Endo-parasites
In Southern Finland, stickleback can serve either as definitive hosts (the fish is used for sexual reproduction) or as secondary intermediate hosts (the fish is used for growth or for transmission) of several endo-parasites. A number of these parasites are able to manipulate the behaviour of their intermediate host to increase their chances to get to the next host in their life-cycle. This is especially true for parasites that use the food web to transmit to the predator of their intermediate host (i.e. trophic transmission). Accordingly, endo-parasites can be quite sensitive to environmental changes and their presence can indicate the well-functionning of ecosystems.
Digenean Trematodes (Eye Flukes)
Typically, eye flukes require three
hosts to complete their life cycles: a mollusc, a fish and a bird. Eggs are
released with the faeces of the definitive host into the water. From the
egg hatches a free-living miracidia larvae infective to a mollusc.
Inside the first intermediate host the parasite will encyst as sporocyst that
will produce asexually hundreds of cercariae. Free-living cercariae seek
for the second intermediate host (fish, amphibians) in which they will develop
as metacercariae and induce severe pathologies (blindness, malformations)
in order to make their host more susceptible to predation by birds where they
establish in the gut.
Life cycle
of Diplostomum spathaceum
From Lymnaea snails, sporocysts
release cercariae in seek for fish to infect. The production of cercariae is
highly dependent towards temperature so that transmission downstream hosts is
only possible between May to August in Southern Finland, most of infections
occuring during the late summer. Once in the lens of the fish, metacercariae
causes blindness due to the metabolic wastes.
As for Diplostomum spp., asexual production of cercarial stages takes place in lymnaeid snails. They later encyst in the eyes of fish and are transmitted by predation of infected fish to bird final hosts.
Cestodes
Cestodes need to infect a variety of
intermediate hosts in which they pass through specific developmental stages
before the adult establish in the digestive tract of vertebrates. In Southern
Finland, Baltic populations of threespine stickleback can serve as intermediate
or definitive hosts for a number of cestodes. Some tapeworms are said
autogenic when they spend their entire life-cycle in aquatic environments (e.g.
Triaenophorus crassus) or allogenic when the life cycle involves
terrestrial and aquatic stages (e.g. Schistocephalus solidus).
S. solidus
has established as model system for studying complex life-cycle
parasites because all stages of the parasite can be easily reared and
manipulated in the laboratory. Non-invasive tracking of the course of
infection in
the first host and the availability of the complete genome sequence of
the secondary intermediate host (i.e. the threespine sitckleback)
further provide good opportunities to study host-parasite interactions
at
a very fine scale. Finally being a simultaneous hermaphrodite able to
reproduce
by selfing and crossing, this cestode has also become a model system in
the
study of sexual selection and life-history theory.
Life cycle
of Schistocephalus solidus
To
complete its life cycle, this
tapeworm depends on three hosts: a cyclopoid copepod, a threespine
stickleback
and a warm blooded vertebrate. After hatching, free-swimming coracidia
larvae are eaten by cyclopoid copepods in which they develop as
procercoid. Once infective for the next host, the parasite manipulates
the behaviour
of the copepod to enhance transmission to the downstream host, the
threespine
stickleback. Most of the growth of the parasite occurs in the fish host
and
plerocercoid larvae often reache sizes comparable to the size of its
fish
host. Indeed, the bigger the parasite is the best are its chances to
establish
in the final host. As a consequence, this parasite imposes a strong
selection
pressure on host populations. Transmission to stickleback seem to occur
during
the late summer when young sticklebacks are feeding on small preys such
as copepods.
However, the growth of the parasite does not start immediately. Indeed
it has
been shown that host size was a constrain for the development of
plerocercoids. Therefore established parasites have to wait until the
host is big enough to start growing massively. Transmission to the
definitive
host enhanced by lowering the response to predation risk of infected
stickleback. Hence the parasite overwinters in the fish in high
latitudes
and is transmitted during the summer. Eggs are then released with the
bird
faeces into the water.
Microsporidians
Microsporidians are intra-cellular
parasites directly transmitted via the emission of spores. Highly contagious
spores enter the host and prenetrate the epithelium. Via the blood
stream, the parasite make its way to the skin, muscle or other tissues. In host
cells the parasite undergoes asexual division and starts producing spores.
Infected cells are filled with spores causing strong hypertrophy (infected
cells become round white cysts/xenoma). Spores are released into the water from
lesions on the body surface. Host death is triggered by the degeneration of
infected cells.
Keywords: parasites, life-cycle, life-history, threespine
stickleback, Gasterosteus aculeatus
Nota bene: All pictures, drawings and figures for which source is not cited are the property of Alexandre Budria.
