Parasitism (An Introduction to Parasitology)

Background

The parasitic way of life is one of the most common, if not the most common, way of life on Earth. It is likely that more than half of all species of organisms are parasites, many of them of very great economic and medical importance. Indeed, some of the most devastating diseases of man, such as malaria, are caused by parasites, and the economic loss caused by parasites of plants and livestock reaches billions of US$ every year. - Here we give a brief overview of the kinds of parasites, their adaptations, effects on hosts and economic/medical importance.

Definition

Different authors use different definitions for parasitism, reflecting their practical or research interests. Thus, a medical parasitologist will stress that a parasite causes certain diseases, and will exclude all those organisms from the definition which have no apparent effect on the host, a zoologist might be more interested in the physiological and morphological adaptations of a parasite to its host. We define parasitism in a very wide sense, i.e., as a close association between two organisms, in which one, the parasite, depends on the other, the host, deriving some benefit (usually food) from it without necessarily damaging it.

The domain of parasitology

Many groups of organisms that have a parasitic way of life, such as fungi, bacteria and viruses, are usually included in the domain of microbiology, whereas parasitology is restricted to protozoan and metazoan parasites.  (In France, fungi are often studied by parasitologists).

Associations related to parasitism

Some kinds of associations resemble parasitism in various aspects and cannot always be unambiguously distinguished from it, either because we know little about particular species, or because genuine intermediate forms exist. Such associations include commensalism, phoresis, mutualism, symbiosis (sensu strictu) and predation.

Phoresis (phoresy)

In phoresis, one organism uses another for transport and/or protection. Barnacles can again serve as an example: some species live attached to the surface of whales, by which they are carried around finding new sources of pelagic (plankton) food (other barnacles are genuine parasites, their tissues extending deep into the whale’s tissue absorbing food from it).

Mutualism

Symbiosis

Symbiosis (sensu stricto)  is an extreme form of mutualism, in which the  association is compulsory, i.e. both partners (symbionts) benefit and cannot live without each other,  such as fungi and algae in lichens. However, the term symbiosis (sensu lato) is also used in a wider sense, including all types of associations of organisms (parasitism, commensalism, phoresis, mutualism).

Predation

In predation, one, the predator (often larger than its prey) attacks, usually kills and eats another, the prey.

Change of kinds of associations

That a distinction between the various kinds of associations is sometimes difficult, is shown by the observation that the same organism may sometimes be a parasite, a commensal, mutualist or predator, depending on the circumstances.  Thus, the amoeba Entamoeba histolytica  may live as a harmless commensal feeding on bacteria in the intestine of man, or it may live as an often fatal parasite ingesting red blood cells. Some parasites may even improve the health and fitness of their hosts when infection intensities are low.

Kinds of parasites

Fleas, lice, isopods, monogenean flukes and copepods, among many others, are ectoparasites that live on the surface of hosts. Nematodes (roundworms), tapeworms (cestodes), flukes (trematodes) and protistans (unicellular organisms) of vertebrates are endoparasites found in the tissues of their hosts. Tapeworms and flukes are obligatory parasites which cannot survive without a host at least for part of their life cycle, whereas normally saprophagous maggots (feeding on decaying organic matter) are facultative parasites which infect living hosts only occasionally. A permanent parasite, such as most parasitic worms (helminths) is an organism that is parasitic on or in a host over long time spans, whereas a temporary parasite, such as mosquitoes or leeches, is parasitic only for short periods. Some organisms, e.g. gnathiid idopods, live a parasitic way of life only as larvae, they are so-called larval parasites (Figure 1). Most parasites are adult parasites, i.e., they are associated with a host during at least part of their mature phase. Mosquitoes are periodic parasites which visit  a host from time to time. When individuals of the same species parasitize individuals of the same species, they are referred to as intraspecific parasites. Examples are males of certain deepsea fish that are permanently attached to females of the species absorbing food from them. Hyperparasites (of the 1st, 2nd, etc. degrees) are parasites living on or in other parasites. For example, a certain monogenean is a hyperparasite of the first degree, infecting copepods which are themselves ectoparasitic on marine fishes. Latent parasites are parasites which do not have any obvious effects on the host. Kleptoparasites are animals which force others to regurgitate their food and then swallow it, such as frigate birds chasing other birds in flight. Cowbirds and about 50 species of cuckoos are brood parasites, i.e., they lay their eggs into the nests of other birds where they are incubated by these birds. Microparasites include protistans, bacteria, viruses and some worms (helminths), which reproduce in/on the host and induce immune responses in vertebrate hosts. Macroparasites include most helminths and arthropods; they do not reproduce on or in the host, inducing no or weak immune responses depending on infection intensities;  infections often last long (i.e., they are chronic) and usually are not fatal. Many species of hymenopterans are parasitoids which lay their eggs into insect hosts; although hosts may survive for some time, they are always killed by the growing parasitoid. – Among parasitic plants, we distinguish holo- and hemiparasites. The former are entirely dependent on their host, since they lack chlorophyll and cannot synthesize their own food, the latter are only partly dependent on their host, since they can use their own chlorophyll to synthesize some of the necessary organic matter (Figure 2).


Figure 1. A third stage female larva of Gnathia sp., a larval isopod parasite of marine fishes. Note the large thorax which fills with blood after a blood meal of the larva.
© Professor Alexandra Grutter, University of Queensland.






Figure 2. A hemiparasitic mistletoe on a gumtree (eucalypt) in NSW, Australia. Note the bulbous connection of the parasite to the host tree (arrow), consisting of the haustorium of the mistletoe and host tissue. The crosses indicate the outline of the mistletoe. In Australia, various bird species, particularly the Mistletoe Bird (Dicaeum hirundinaceum) and some honeyeaters are responsible for dispersal of the parasites' fruits. The association between birds and mistletoe can be considered a mutualistic one.

Adaptations to parasitism

Special adaptations, body size, sacculinization, dispersal

Each parasite species must have special adaptations that guarantee infection of a host and survival in it. For example, a malaria parasite of a bird cannot survive in humans, the human pinworm (roundworm, nematode) Enterobius vermicularis can survive only in humans.  In other words, each of these species possesses characteristics enabling it to complete its life cycle using these particular hosts.  Such characteristics (in very few cases analysed in some detail) determine not only the kinds of host(s) used, but also the degree of host specificity, i.e., how many host species a parasite can utilize.  - Parasites among the flowering plants possess haustoria, which form a close connection with the vascular system of host plants, either in the roots or shoots, extracting nutrients from it.

In addition to special adaptations, many parasites also share some features that can be considered as general adaptations to a parasitic way of life. Among these are the smaller body size of parasites relative to that of their host, only few parasites reaching a body volume or length exceeding that of the host (Figure 3). However, at the first glance perhaps surprising, many parasites are larger than their free-living relatives for two reasons: parasites usually have an almost unlimited food supply, and they must produce a large number of offspring in order to overcome the hazards of their life cycles which necessitates infecting a host: only few eggs or larvae manage to succeed: the larger the body, the larger the egg producing capacity!


Figure 3. The amphilinid tapeworm Austramphilina elongata in the body cavity of a turtle. The parasite is very large (several cm long), but still much smaller than its host. Its large body size (much larger than that of related free-living flatworms) enables it to produce large number of eggs, necessary to overcome the hazards of the life cycle.
© Klaus Rohde.

Many parasites have undergone a process referred to as sacculinization, i.e., a reduction in the complexity particularly of sensory organs and the nervous system, although some exceptions have been well studied (see the knol on sacculinization: ( http://knol.google.com/k/klaus-rohde/the-aspidogastrea-a-parasitological/xk923bc3gp4/15).

Like all animal species, parasites must be able to disperse, 1) because a population too restricted in its distribution may become extinct if conditions become unfavourable, 2) because dispersal reduces inbreeding and the loss of evolutionary adaptability, and 3) and (only with regard to parasites)  because dispersal may reduce the chances of hosts  becoming over-infected (???).  In parasites, dispersal is often largely or even entirely passive, i.e., due to the dispersal of the host, but many parasites have elaborate dispersal mechanisms, such as flotation organs of larval flukes (cercariae).

Mechanisms of infection

Particularly impressive and well studied in many species are mechanisms of infection. Hosts can become infected by inoculation (malaria), faecal contamination of wounds (Chagas disease transmitted by assassination bugs), retrofection (migration of larvae from the anus into the gut, human pinworm), ingestion of cysts (amoebic dysentery), ingestion of eggs (human roundworm Ascaris lumbricoides), ingestion of spores (protistan microsporans) (Figure 4), ingestion of transport hosts (roundworm Anisakis), ingestion of intermediate hosts (broad fish tapeworm Diphyllobothrium latum), inhalation (protistan Pneumocystis?), contact transfer (mange mite), kissing (flagellated protistan Trichomonas tenax), sexual intercourse (flagellated protistan Trichomonas vaginalis), penetration through the skin (hookworms), penetration into the nasal passage (protistan Naegleria fowleri), intrauterine infection (protistan malaria parasites and Toxoplasma).


Figure 4. Mature spore of Vairimorpha cheracis, a microsporidian parasite of the Australian yabby, Cherax destructor, transmission electron micrograph. Note the nucleus, posterior vacuole and sections through 11 coils of polar filament. A new host cell is infected by extrusion of the spore’s content into the cell through the everted filament. © Dr. Elizabeth Moodie.


Many species possess astonishing behavioural adaptations that guarantee entrance into a host. We mention some examples from the flukes (trematodes). The liver fluke of sheep, Dicrocoelium lanceolatum, uses land snails as the first and ants as the second intermediate hosts. Cercariae are produced in the snails where they cluster in slime balls; they are expelled by the snails and eaten by ants. The first cercariae (tailed larvae) that enter an ant migrate into the subesophageal ganglion, thereby inducing cramp-like behaviour of the ant which makes it cling to a plant where its chances to be eaten by sheep are enhanced. A larval stage (the sporocyst) of the trematode Leucochloridium  macrostomum possesses conspicuous outgrowths which can extend into the tentacles of its snail host. By pulsating rhythmically they mimic worms, the natural food of small birds. Birds, "believing" that they are eating worms, bite off the tentacles and become infected. Infection also makes the snails move to more exposed sites (Figure 5).


Figure 5. The sporocyst of the digenean trematode Leucochloridium. Part of the sporocyst, which is conspicuously coloured resembling a worm, can extend into the tentacle of a snail. It pulsates, thus attracting the attention of the final host, a worm-eating bird. The bird bites the tentacle off and becomes infected by the metacercariae located in the sporocyst.

Aggregation, hermaphroditism, parthenogenesis and asexual reproduction

Surveys of the distribution of parasites in host populations always find that not all host individuals are infected to the same degree. The majority of parasites is usually concentrated in a few of the hosts. This is meant when we say that distributions are aggregated.  There has been some debate, without much evidence, on whether aggregation has a biological function, such as facilitating the finding of mating partners, or limiting the damage done to the host population. Common among parasites are hermaphroditism, parthenogenesis and asexual reproduction. And these phenomena almost certainly have a biological function. Because in most species, only single or few parasites will manage to infect a host, it is important that populations can be built up from  these few individuals or even from a single individual. And parthenogenesis and sexual reproduction permit just that. In the first case, gametes (sex cells) develop without fertilization, in the second, somatic (body) cells can undergo development. An example of asexual reproduction is malaria parasites developing by schizogony in human red blood cells. An  example for parthenogenesis is (probably) trematode larvae developing in snails. Almost all trematodes, as well as the cestodes and monogeneans, are hermaphroditic, thereby doubling the  chance of meeting a mating partner. Furthermore, some species can at least sometimes self-fertilize.

Host specificity

Parasites are never found on all host species that could possibly be infected. In other words, all parasites show a certain degree of host specificity, although the degree of specificity varies. For example, the large human roundworm Ascaris lumbricoides occurs only in humans (although a closely related species, Ascaris suis, occurs in pigs and is sometimes considered to be the same species), whereas the protistan Toxoplasma gondii has been shown to occur in a wide range of mammals and birds. - The same refers to site specificity. All parasites prefer certain tissues or organs or even narrow niches within them to others, but site specificity varies. For example, larval flukes (metacercariae) of many species infect a variety of tissues of fishes, whereas adult schistosomes (blood flukes) are restricted to the blood vessels.

Simple and complex life cycles

We distinguish two main kinds of life cycles: many parasites (lice, flea, monogenean flukes, many roundworms, etc.) use a single host, i.e., they have a direct life cycle. Others use a final (= definitive) host, as well as one or several intermediate hosts, i.e., they have indirect life cycles (for example all digenean flukes = Trematoda). The sexually mature stage occurs in the final hosts, developing immature stages occur in the intermediate hosts. An example of a trematode with three intermediate hosts is the bird fluke Strigea falconispalumbi.  As in almost all digenean flukes, molluscs and usually snails serve as the first intermediate host, tadpoles/frogs in this species serve as second intermediate hosts, and amphibians, snakes, mammals and birds serve as third intermediate hosts. Predatory birds which feed on the third intermediate hosts are the final (=definitive) hosts. In certain parasite species, alternative life cycles are possible. For example, in the aspidogastrean fluke Aspidogaster conchicola, both a direct and an indirect life cycle are possible: adult worms in the mollusc produce eggs which are inhaled by other molluscs, but fish can also become infected by eating infected molluscs (Figure 6). In other aspidogastreans, and in the amphilinid tapeworm Austramphiina elongata, among many others, the life cycle is always indirect, involving an intermediate and final host. In the amphilinid tapeworm turtles serve as final hosts, eggs escape in an unknown way, larvae hatch in freshwater and penetrate into the intermediate host, a crayfish, which is eaten by a turtle (Figure 7).


Figure 6. Life cycle of Aspidogaster conchicola (Trematoda, Aspidogastrea). Note: the parasite can complete its life cycle in the mollusc, i.e., it has a direct life cycle involving only one host. Alternatively, it can use a fish as a final and a mollusc as an intermediate host, i.e., it has an indirect life  cycle. © Klaus Rohde

Figure 7. Life cycle of Austramphilina elongata (Cestoda, Amphilinidea). Note: the parasite has an indirect life cycle, always including an intermediate host, a crayfish, and a final host, a turtle. © Klaus Rohde

Virulence of parasites

Virulence of parasites can be defined as the degree of damage done by the parasite to the host. There are two opposing trends which determine the degree of virulence: 1) sometimes it may not be in the parasite's interest to severely damage or even kill its host, because this would also affect the fitness of the parasite; 2) on the other hand, parasite transmission to another host may be facilitated by such damage: a weak host may be easier prey for a predatory final host than a strong one. Therefore, evolution will lead to an increase or a decrease in virulence, depending on the circumstances.

Host-parasite interactions

Cleaning symbiosis

A considerable range of behavioural patterns leading to (or thought to lead to) the removal of parasites has been observed. They include preening and bathing of birds in dust and water, passive and active anting (where ants are allowed to passively crawl over the body, or where ants are actively squeezed over the plumage). Also, dolphins rubbing  against rocks, fish jumping out of the water, etc.) may have a cleaning function. Best known is cleaning symbiosis, in which one animal (the cleaner) cleans another (the host) from parasites and diseased (necrotic) tissues. For example, cleaning behaviour has been observed in birds which remove ectoparasites from cattle, hippopotamus and large marine fish floating on the ocean surface, in several species of shrimps, and in more than 100 species of fish. Hosts are freshwater and marine fishes, the Galapagos marine iguana, whales and dolphins, invertebrates, among others. Many cleaner fish  possess special morphological adaptations which enable them to pick up parasites, (a terminal mouth, fused anterior teeth, conspicuous colour patterns). The cleaner fish Labroides dimidiatus (Figures 8 and 9)  even performs a cleaning dance to attract host fish. "Invitation postures" of hosts signal to the cleaner that they are ready to be cleaned.


Figure 8. The cleaner wrasse Labroides dimidiatus cleaning a host, the marine fish Diagramma pictum. Note the conspicuous colour pattern of the cleaner fish and its terminal mouth.
© Professor Alexandra Grutter, University of Queensland.


Figure 9. The cleaner wrasse Labroides dimidiatus cleaning a host, the marine fish Diagramma pictum. Note the conspicuous colour pattern of the cleaner fish and its terminal mouth.
© Professor Alexandra Grutter, University of Queensland.

Immune- and tissue reactions, resistance

Hosts are protected against parasite infections by two kinds of mechanisms.

1) Humoural and tissue reactions of hosts use the host's ability to distinguish self (its own cells) from non-self (foreign cells and material). In vertebrates  three types of such reactions have been demonstrated: phagocytosis, inflammation and adaptive immunity. The first two are non-specific tissue reactions, the third is specific to a certain type of non-self material. Immune reactions involve parasite antigens which induce the formation of specific antibodies in the host. In microparasites  immune responses are more effective than in macroparasites.

2) Hosts show different degrees of “resistance” to infections which are not due to acquired immunity. For example, some sheep are more "resistant" to roundworms than others. In age resistance, older individuals are more resistant than young ones.

Effects on hosts

As pointed out earlier, some parasites may have little, others very strong and sometimes fatal effects on the hosts.  Malaria has very serious effects on humans, particularly children, often leading to death. The human pinworm Enterobius vermicularis, in contrast, often (but not always) rather has nuisance value. Monogenean flukes of fish usually have little effect, but some species lead to mass mortalities, particularly in aquaculture.

Species richness of parasites and distribution of parasites in the animal and plant kingdoms

 Arndt (1940) was the first who counted the number of parasites as a proportion of a total fauna.  He found 10,000 parasitic species out of a total of 40,000 species in Germany, but did not include insects parasitizing plants (“herbivores”). Price (1977) included such species but excluded temporary parasites (e.g., mosquitoes and leeches) in his survey of the British fauna. He estimated that more than half of all British species are parasitic.

Thirteen large taxa (phyla, subphyla or classes) consist entirely of parasites, and many other groups include a high proportion of parasitic species. Even among the vertebrates several species are parasitic. Among the 250,000 to 400,000 species of flowering plants (angiosperms) there are about 4,100 parasitic species included in 16-19 of the approximately 462 plant families. 

Economic and hygienic importance of parasites

Some of the most important tropical diseases are caused by parasites, such as bilharzia (caused by the bloodfluke Schistosoma), filariasis (nematodes), amoebic dysentery (the protozoan Entamoeba histolytica), and in particular malaria (four species of the protozoan Plasmodium). Hundreds of millions of people are infected with malaria, and more than a millions die every year, particularly children in sub-Saharan Africa. There is no effective vaccination, and resistance to the various anti-malaria drugs develops very fast.

The web pages of The World Health Organization, Division of Tropical Diseases, CTD, and of the Center for Disease Control (CDC) contain information about the current status of the important parasitic diseases, which is continually updated.

Reduced immune reactions due to AIDS, the development of  resistance to certain drugs used to treat parasite infections (malaria, for example) represent problems in the fight against parasitic disease. The prevalence of intestinal parasites world-wide is increasing, partly due to urbanization. Global warming will lead to a spread of parasitic infections into some countries.

Among parasites of livestock, Ostertagia ostertagi, one of the nematodes infecting cattle, alone is estimated to cause an annual loss of $600 million  to the cattle industry in the US. Drench resistance is also a serious problem.

Parasites are of very great importance in the aquaculture industry, where they have repeatedly led to mass mortalities.

Many parasites are among the most important pests of plants. Nematodes are of particular importance. The annual loss to crop production due to nematodes in the US was estimated to be US$8 billion (12%), and $78 billion globally.

On the other hand, parasites can also be used to control insect pests.

Related knols

Monogenea: http://knol.google.com/k/klaus-rohde/monogenea-ectoparasitic-flukes-flatworms/xk923bc3gp4/75
Trematoda: http://knol.google.com/k/klaus-rohde/flukes-trematodes-the-biology/xk923bc3gp4/76#
Gyrocotylidea: http://knol.google.com/k/klaus-rohde/the-gyrocotylidea-an-aberrant-group-of/xk923bc3gp4/79#
Aspidogastrea I. http://knol.google.com/k/klaus-rohde/the-aspidogastrea-a-parasitological/xk923bc3gp4/13#
Aspidogastrea II. http://knol.google.com/k/klaus-rohde/the-aspidogastrea-a-parasitological/xk923bc3gp4/15
Aspidogastrea III. http://knol.google.com/k/klaus-rohde/the-aspidogastrea-a-parasitological/xk923bc3gp4/16
Marine parasites. http://knol.google.com/k/klaus-rohde/meeresparasiten-wirtschaftliche-und/xk923bc3gp4/2
Amphilinidea: http://knol.google.com/k/klaus-rohde/the-amphilinidea-a-small-group-of/xk923bc3gp4/21#
Marine parasites of man: http://knol.google.com/k/klaus-rohde/marine-parasites-of-man-anisakis/xk923bc3gp4/59#edit

Acknowledgement

I wish to thank Professor Alexandra Grutter, University of Queensland, Brisbane, for the photos of Gnathia and the cleaner fish (Figures 1, 8 and 9), and Dr. Elizabeth Moodie, Townsville, for the transmission electron- micrograph of the microsporidian (Figure 4).

Further Reading

My review article in the Encyclopedia of Biodiversity, Academic Press 2001 (see below) contains a more detailed account of parasitism. Important textbooks dealing with various aspects of parasitology are listed below.


Bogitsh  B.J. & Cheng T.C. (1990). Human Parasitology. Saunders College Publishing, New York.

Kinne O. (1980 - 1985). Diseases of Marine Animals; Volume 1 - 4. John Wiley & Sons, Chichester, New York, Brisbane, Toronto, and Biologische Anstalt Helgoland, Hamburg.

Odening K. (1969). Entwicklungswege der Schmarotzerwürmer. Akademische Verlagsgesellschaft Geest & Portig K.G., Leipzig.

Press M.C. & Graves, J.D. Eds. (1995). Parasitic Plants.  Chapman & Hall, London.

Rohde K. (1993). Ecology of Marine Parasites 2nd Edition. CAB International, Oxford.

Rohde, K. (2001). Parasitism. Encyclopedia of Biodiversity. Academic Press.

Rohde, K. ed. (2005). Marine Parasitology. CSIRO Melbourne and CABI Wallingford, Oxon.

Schmidt G.D., Roberts L.S. & Janovy, J. (1995). Foundations of Parasitology 5th Edition. McGraw Hill, New York.

Urquhart, G.M. & Jennings, F.W. (1996). Veterinary Parasitology 2nd Edition. Iowa State University Press, Ames, Iowa.