Libmonster ID: BY-1582

by Viktor GLUPOV, Dr. Sc. (Biol.), head of the Institute of Animal Taxonomy and Ecology, Siberian Branch of the Russian Academy of Sciences, head of the Laboratory of Insect Pathology; Vadim KRYUKOV, Cand. Sc. (Biol.), Vyacheslav MARTEMYANOV, Cand. Sc. (Biol.), and Natalya YURLOVA, Cand. Sc. (Biol.), scientists of this laboratory

Parasites are inseparable components of natural ecosystems essential to their functioning. They are playing the key role not only in the dynamics of host populations and communities, but also in the structure of alimentary chains; they are also making an important contribution to the biomass and energy. Their presence has been detected at various levels of hierarchy: from protozoans, viruses, bacteria, and fungi up to multicellular plants and animals. Understanding how this complex system works so as to act upon it is an important scientific problem.

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Trematodes make an important contribution to the biomass of water ecosystems. The cercaria biomass is comparable to the host Lymnaea stagnalis biomass (A). The biomass of the two prevalent trematode species (Echinoparyphium aconiatum and Plagiorchis elegans) is 50.8 and 58.3 percent of the host mollusk biomass, respectively (B).


Many living organisms, often invisible, surround us. Even the human body is a comfortable home for parasitic "residents" seen only under a microscope. This coexistence is called symbiosis (literally--"living together"). Most often it is associated with interrelationships implying mutual profit (importantly, in biological literature it is called mutualism--a word derived from the adjective "mutual"). In reality it may be different, for the coexistence profit vectors can be of different direction. In some cases it can be cooperation, sometimes very close. For example, the human digestive system just cannot work without enteric flora microorganisms. On the other hand, unwanted guests can infest the human body (or any other object of living nature) and use it not just as a habitat, but cause significant negative effects. These organisms are called parasites. Initially this definition carried a negative shade (Greek "parasites"--hanger-on, boarder); but actually its interpretation is not so simple: we are now starting to realize the multifarious role of these wonderful beings in the biosphere of our planet.

Valentin Dogel (elected corresponding member of the Academy of Sciences of the USSR in 1939), Russian zoologist and the founder of the ecological parasitology science, offered an accurate definition of this phenomenon. "Parasites are organisms using other living organisms as a habitat and a source of food, with the hosts partially or completely responsible for regulation of the parasites' relationships with the environment". A parasite in fact has two habitats: first--the host body, and second--the environment, with which it communicates through the host, and perhaps a third--if it is a super-parasite.

The great diversity of parasites is amazing; they are present in virtually all taxonomic groups of organisms of the Earth. Some are obligates--they cannot do without the host throughout their entire life span, while others, the facultatives, survive for some time (at certain developmental stages) outside the host. The mutual host/ parasite relationships differ greatly. Here we are going to discuss only some key aspects of the phenomenon restricting the range of hosts. These are invertebrates, namely, mollusks and their macroparasites--flat sucker worms (trematodes) as well as insects, with bacteria, fungi, viruses, and parasitoids (intermediate stage between parasites and predators) living in them.


The majority of the known trematodes have a trixenic (with three categories of hosts) life cycle and develop with the obligatory participation of mollusks. Gastropo-

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Trematodes as common components of natural ecosystems-incorporate into the alimentary chains of different trophic levels. Cercaria developing in mollusks become a fodder for water invertebrates and fishes.

da serve as the main hosts for miracidia's* larvae, from which a tremendous number of parthenogenetic** generations are formed in a mollusk's liver or reproductive organs; this progeny--sporocysts*** and redias****--reproduce themselves and give birth to free larvae, the cercaria. Cercaria, released into water from the first intermediate host, have to find their second host. For many trematodes these are mollusks, for others water invertebrates and fishes. The terminal hosts are vertebrates (often water and marsh birds) infested via the alimentary tract by eating the second intermediate host together with the larvae living in it.

Here we should like to touch upon some ecological aspects. The traditionally negative attitude to parasites has started to change during recent decades due to new research results, for example, data on the role of parasites in trophic relations in natural ecosystems, specifically, in water. Many-year studies in the fresh water (estuary) ecosystem of the Chany lake in the Novosibirsk region have shown that more than 100 trematode species, found here in terminal hosts (water and water-and-marsh birds) developed with the participation of 23 mollusk species. The mollusks participate in the transfer (transmission) of "migrants" to second intermediate hosts--water invertebrates and fishes, with which the

* Miracidium, the first larval stage of the individual development of parasitic trematodes (flat sucker worms).--Ed.

** Parthenogenesis (virginal reproduction, a form of sex reproduction of organisms, with the female sex cells developing without fertilization.--Ed.

*** Sporocyst, the first parasitic (parthenogenetic) generation with a miracidium as its larval stage.--Ed.

**** Redia, the next parasitic (second parthenogenetic) generation. Develops in a sporocyst's body cavity.--Ed.

parasites are eventually transmitted to terminal hosts via the trophic network (chain).

All trematodes form a group of highly specific parasites with respect to their first intermediate hosts. In order to get from their first to second hosts, transmissive trematode larvae are released into open water, where they serve as food for many water invertebrates and fishes. The littoral zone of the lake contains 10-30 g per m3 (100-180 g in some years, in dry weight) of Lymnaea stagnalis, a highly prevalent mollusk. The parasitic larvae released into water make up almost half of the invaded host biomass. We have found that the individual dry weight of free transmissive larvae (cercaria) is extremely low, varying from 0.002 to 0.0003 mg for different trematode species. However, due to their tremendous number, their summary biomass reaches values comparable to the host biomass. For example, the summary production of biomass of cercaria of two highly prevalent trematode species (Echinoparyphium aconiatum, Plagiorchis Sp.) during transmission reaches in some years 50-56.5 percent of the infested host (Lymnaea stagnalis) biomass.

Cercaria, in turn, released into water, become food for many other invertebrates and fishes in subsequent components of the trophic chain, while those which fail to get into the needed host or uneaten are drawn into other trophic chains.

Importantly, in order to realize their vital cycle, the parasites use strategies enabling them to act upon the host, modify its morphology, its normal biochemical status, immune system, and even genetics. Causing castration in mollusks, parasitic trematodes infest tissues of

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the digestive gland or gonads (organs producing sex cells), actually replacing them. Suppressing the reproductive potential of the host population, they ensure their own development and reproduction in the mol-lusk's body. The energy that would otherwise be spent for the host's reproduction is therefore spent for the parasite. It has been found that only 2-4 percent of infested mollusks participate in reproduction, and strange as it may seem, in some cases their individual fertility is higher than that of non-infested ones.

The parasite can change the host's behavior and hence, its food preferences, its ability to escape from predators, attitude to light, etc. Mollusks infested by trematodes are no longer able to hide by digging into silt under unfavor-

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able conditions and become easy prey for birds, the final hosts. Thus, the parasites have a better chance to get into their final hosts and complete their life cycle.

On the other hand, we have found that trematodes can induce morphologic changes in the mollusk, manifested, among other things, in a thickening of its shell that makes it better protected from mechanical injury and death; the parasite is therefore better protected as well, and the time of the infested matter released into the environment is thus prolonged. Naturally, the more specialized is the parasite, the more fine is the synchronization of its vital cycles and those of its host. That is, by changing certain physiological biochemical processes in the host the parasite makes the host show the ways of a predator, thus making it an easy prey. All these qualities are essential to the parasite for completing its vital cycle.


The host's ration, in turn, may act on the parasite. This is particularly demonstrative in such specific

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organisms as viruses and phytophage insects. We speak about a triatroph plant-host-parasite system in such cases. Everything in this system is so tightly interconnected that even a slight influence on one component ushers in changes in the triad's functioning. For example, even a slight damage inflicted by insects to a fodder plant causes significant changes in the chemical composition of its leaves. Partly this is explained by saliva effects on plant tissues as well as by direct defoliation of the fodder plant. Moreover, the components accumulating in the leaves consumed by insects stimulate an immune response in the phytophage. We have demonstrated this phenomenon on the gypsy moth worm--a highly prevalent forest pest in Eurasia and North America. Importantly, a higher immune status has been recorded only in insect females. Hence, their chance to survive in case of infestation by parasites, such as, for example, baculovirus or parasitic entomophages, is higher. And since this chance is better in females, the probability of reproductive efficiency is higher for the entire population of the host.

Environmental conditions are likewise important for the triatroph system. For example, cool weather in spring can lead to a significant delay of the hatching of gypsy moth worms. As a result, these insects, usually starting their growth on young newly opened leaves, have to consume more mature leaves instead. And this is possible with digestive enzymes of a different composition. In addition, the composition of first and second metabolites in mature leaves differs from that in the new leaves.

We have found that the eating of older leaves causes a reduction of some physiological parameters in the gypsy moth, which is eventually associated with a significant drop of activities of the insect's immune system components. So, we observe a situation similar to the herpesvirus in humans: present in the healthy body, it does not manifest itself, but it does as soon as immunity goes down. The same is observed in the gypsy moth. If its immunity is down, seemingly normal insects carrying the baculovirus* start falling ill. The only difference from the herpesvirus is that the baculo-viral infection is fatal for insects. Hence consumption of "bad" leaves leads to the death of more than half of the insects infected with the virus.

This phenomenon can be responsible for the drastic reduction of the gypsy moth population under conditions of the extracontinental climate when cold spring days are quite common. On the other hand, this phenomenon can be also responsible for a sharp increase in the gypsy moth population in favorable hot years. The animals not only feel well in warm weather, but they are better prepared to resist parasites anyplace. This inevitably tells on the population's reproduction coefficient. The summer of 2012 was not an exception: an early rather warm spring and hot summer in the Novosibirsk region have led to a sharp increase in the gypsy moth population. And the parasites are unable yet to control this population explosion.

* Baculovirus, a family of viruses causing diseases of various arthropod species, mainly lepidopterus; harmless for humans and warm-blooded animals.--Ed.

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A host's immune system is modified by environmental factors and by a parasite; this inhibits its activity or activates certain components, as its goal is to avoid the effects of this system. Parasites resort to different strategies, including molecular mimicry, when they form on their surface structures which cannot be recognized by a host's defense mechanism. In some cases the parasites create phantoms chased by the immune system, which in some cases fails to direct its activity towards the parasite proper. This can be due to hypersecretion of some compounds released into the host body. Rather often a parasite directly suppresses the host's immune system or part of it, which can be really harmful. The other part, not inhibited, prevents infestation of the host by other parasites. For example, a parasitoid at the first stages of its growth behaves like a parasite. Its female lays an egg on the surface of the Galleria mel-lonella moth worm and injects venom into the host. This "preventive" injection leads to partial suppression of its immune system which, however, is still capable of performing part of its functions, preventing the development of microorganisms, bacteria in the first place.

Paralyzed by a parasitoid, worms can serve as favorable substrates for entomopathogenic fungi, i.e. pathogenic with respect to insects. We have shown that the sensitivity of such worms to fungi increases thousand fold. Hence, feeding on the surface of or inside the victim, parasitoid larvae release fungistatic substances preventing the development of fungal pathogens. And only after the parasitoid is through with its growth, will the insect be completely colonized by the fungus.

In nature various insect species have many contacts with parasitic organisms. If a parasite is very active and not highly specialized, it kills its host but dies as well. That is why insect deaths are not a frequent event in nature.

The host survives--recovers--if the parasite is moderately or slightly virulent or the dose of its spores is low. Their intercourse in this case will tell on the physiological status of the host--its immune system can be activated, and in future the survivors will be better resistant to infections. However, a pre-invasion of the host can also stimulate its resistance to certain parasites and sensitivity to others. For example, the sublethal bacteriosis of worms can bring down their sensitivity to a subsequent bacterial infection and, simultaneously, build up their higher sensitivity to pathogenic fungi.

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Use of entomopathogenic fungi isolated in the steppe is most promising in the continental climate, due to their resistance to high temperatures and UV irradiation.


Entomopathogenic fungi are per se very interesting organisms widely used by plants for protection. Several thousand fungal species, parasitizing on insects are known. The strategies of their relationships with the hosts vary greatly: from facultative to obligate parasitism, from a very wide specialization to a very narrow one when the host is just one species or even at a definite stage of species ontogenesis. The strategy of the majority of these pathogens (for example, entomofluoric or many cup fungi) is aimed at killing the host and completely fill its body with their own thread-like formations, the hyphas. Only then will the fungus produce a daughter generation of spores on the dead insect and thus continue its cycle. They are closer to parasitoids than to parasites in this respect. However, there are also entomopara-sitic fungi, virtually never killing the host and completely depending on its life. This group includes Ascomycota, Laboulbeniales, represented by more than 1,500 highly specialized species. They are obligate parasites on an insect's outer skeleton. Interestingly, they are not only genus-, or species-specific, but even gender-specific as far as the host is concerned; moreover, they adhere only to a definite site of the outer skeleton.

Generally, we can speak about the alternation of the two trends in the evolution of parasitism in fungi: despecial-ization and specialization. The former consists in the loss of the gender stage (teleomorphs), the shortening of the life cycle, and clonal isolation. This has led to the extension of geographic and ecological areas and hence, to a wider range of hosts--that is, to biological progress. This process has been unfolding in different phylogenetic branches and has engendered a miscellaneous group, the anamorphic fungi. However, the fungi of this group are also characterized by progressive specialization in restricting the range of hosts or, most often, by adaptation to their habitat. For example, the species close to anamorphic entomopathogenic fungi can be confined to different plant associations or natural climatic zones. We have shown that the fungi adapted to the continental and arid climate, specifically, found in mixed grass and desert steppes, are most virulent for insects inhabiting open cenoses (locust, Colorado potato beetle).

Interestingly, the so-called toxigenic fungal strains are found in populations of some of the above species. They are characterized by a high level of production of toxins rapidly suppressing the cell immunity of a host; the host dies as a result, and so does the fungus. Why such behavior of these "kamikadze" strains? It is not clear yet; presumably, it is associated with the saprotro-phic* phase of their development. It is very difficult to find toxigenic strains in nature; specialists all over the world are hunting for them: it would be great luck to make a drug on the basis of a fungus, which is rather easily produced under artificial conditions, works rapidly and effectively, and is readily eliminated. On the other hand, less toxic cultures forming numerous "daughter infections" on dead hosts, are better for creating long-term foci of infection.

* Saprotrophs consume organic substances of dead bodies.--Ed.

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The cost of resistance to parasites is high, and the host that escapes often sacrifices its reproductive efficiency. Here's an example. In collaboration with our colleagues from the University of Swansea (U.K.) we have studied great bee moth populations having a different resistance to pathogens. The Siberian strain of insects--melanists (called so because they accumulate in their cuticle melanin, a black or brown pigment making them much darker than other insects of the same species)--are resistant to entomopathogenic fungi. In the European strain albino forms, highly sensitive to the fungus, predominate. Melanists have a very thick cuticle and readily produce enzymes responsible for melanism and antioxidant production. On the other hand, all these "expenditures" for defense mechanisms can lead to the insect's body weight loss and lower fertility.

The prospects of using our data on controlling insect populations, obtained also in collaboration with scientists from the All-Russia Institute of Plant Protection (St. Petersburg), are really great. Their efficiency will be higher if we use biopreparations attuned to the vital strategies of parasites and their hosts. Importantly, their effects on ecosystems will be minimized. The new bio-insecticides will be absolutely safe for humans and other mammals. Man is also a mammalian.


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