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Parasitology

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A new point of view in parasitology: what can we learn from the host-parasite model?


‘‘If one judges the adapted forms of the parasites according to the amounts of retrogressed information, one finds a loss of information that coincides with and completely confirms the low estimation we have of them and how we feel about them.’’ Konrad Lorenz, Nobel Laureate 1973

Abstract

Parasitism is a kind of symbiosis which involves two organisms, one of them is the parasite which lives on or in the body of the other organism, the host. Dealing with parasites and their hosts from an ecological perspective we must consider the ecology of the host/hosts in a parasite life cycle, as well as the host as a habitat for the parasite. Here we present a review of the current knowledge of the interaction between Phalacrocorax (the host) Contracaecum (the parasite) and other organisms involved in a single lifecycle. We will use this information as an example of this entire bioecological context that is parasitology. As a conclusion we can say that the presence of certain parasites in their hosts is related with some characteristics of the host, such as the composition of host diet, geographic distribution, characteristics of the environment and the specificity between parasites and hosts. Because of this, we can say that parasitology should be an integral component of any programs for biodiversity assessment on local, regional, or global scales. We believe that parasitology can really break down the boundaries between classical zoological sciences as an integrator discipline, which contributes to combine knowledge of many other biological fields.

Introduction

Parasitology is the science that deals with several different symbiotic relationships. To define parasitism we can say that is a kind of symbiosis that involves two organisms, one of them is the parasite which lives on or in the body of the other organism, the host. Those parasites which live on the host are called “exoparasites” and those which live inside the host are called “endoparasites”. In general, exoparasites tend to belong to the phylum Arthropoda such as some kinds of flies (Insecta: Diptera), mites (Acari), fleas (Insecta: Siphonaptera) and lice (Insecta: Phthiraptera). Endoparasites, sometimes called helminthes, belong to the phyla Platyhelminthes (Cestoda and Trematoda); Acanthocephala and Nematoda. And we cannot forget the unicellular parasites that belong to different Phyla. Most of them have sanitary importance. In addition, parasites are not only common in humans, they are present in all plant and animal groups. In fact various estimates suggest that at least 50 % of plants and animals are parasitic at some stage during their life cycle (and we are including here viruses, bacteria and fungi). As we can imagine parasitology is an unpleasant discipline for the majority of people. “Parasites are creepy” people usually think about them, but the truth is that parasites can show us a variety of characters of their host, and can tell us about evolutionary novelty and speciation which involves both organisms at the same time (Vickerman, 2009). So this article is for those people who wonder why those “aberrant animals” exist in the world. We will see the relationships between birds (as model host), their parasites (in our case nematodes) and the ecological relationship between them. We will take the example of cormorants (genus Phalacrocorax) as the definite host. The most common parasites that can frequently appear in aquatic birds and fish are nematodes. Nematodes are one of the most diverse phyla in the world. More than 28,000 different species have been distinguished; but only 16,000 are parasitic. Nematodes have successfully adapted to nearly every ecosystem from marine to fresh water, to soils, and from the polar regions to the tropics. From all nematodes, those of the family Anisakidae have a worldwide distribution and their lifecycle generally includes aquatic invertebrates and fish as intermediate hosts and birds and mammals as definitive hosts (Anderson, 2000). On the other hand the larvae of these worms can cause anisakiasis when ingested by humans who consume uncooked fish, but these worms do not reproduce except in marine mammals or seabirds. So this nematode family has a health importance and veterinary importance too because the parasites can affect fishery industries. Belonging to the family Anisakidae are the species of Contracaecum Railliet and Henry, 1912. The definitive hosts are piscivorous birds and mammals, e.g., cormorants, pelicans, and seals, associated with freshwater and marine systems (Anderson, 2000). Contracaecum species are commonly found parasitizing cormorants on the southwestern Atlantic coast (Garbin et al., 2008). With all this background we will present a review of the current knowledge of the interaction between Phalacrocorax, Contracaecum and other organisms involved in this entire bioecological context.

Ecology and the host parasite- relationship

When we deal with parasites and their hosts from an ecological perspective we must consider the ecology of the host/hosts in a parasite life cycle, as well as the host as a habitat for the parasite. Many of the biotic and abiotic fluctuations affecting the ecology of the host will also affect the parasite. Moreover the parasite must deal with a host that is capable of responding physiologically and immunologically against the parasite. So this interaction between the parasite and the host is as ecological as those involving the host´s relationships with its own environment. That is why when we study parasites, we must know very well the environment in which it develops, and this is the host. The parasites As we have already said, nematodes in the genus Contracaecum exists as adult parasites in the upper digestive tract of vertebrates, including piscivorous fishes, birds and mammals. The larval stages are commonly found in the mesenteries and internal organs of a variety of marine and freshwater fishes (Huizinga, 1966). The morphology of some species in the genus Contracaecum are very similar; in consequence, sometimes they become very difficult to identify. Because of the morphological similarity between species at the infective larvae stage (L3), their identification has usually not been possible. That is why molecular studies are very common these days and have become a powerful tool to differentiate species when morphology does not allow doing it. For example, combining different genetic–molecular and morphological evidence, it was possible to discover and describe new taxa of Contracaecum as parasites of aquatic birds, i.e.: Contracaecum bioccai (Mattiucci, et al., 2008) from Pelecanus occidentalis (L.) in Colombia and Contracaecum pyripapillatum (Shamsi et al., 2008) from Pelecanus conspicillatus (Temminck) in Australia. Contracaecum gibsoni (Mattiucci et al., 2010) and Contracaecum overstreeti (Mattiucciet al., 2010) infected Pelecanus crispus (L.) in Greece (see Mattiucci et al., 2010), (Garbin et al., 2011). There are some qualitative and quantitative characters about the morphology of these parasites which help specialists to identify the different species. These characters concern the caudal zone (it is called “caudal papillae”) and the proportion of the length of spicules on the body length (for example: “length of the spicules over 44% of the body length” indicates that the species is C. travassosi) (Labriola & Suriano, 1996). When the definite host eats the intermediate host with parasites inside (in larvae stage), nematodes become adults and infest their host and begin feeding on their fluids.

The intermediate hosts

As we have said, the intermediate hosts of Contracaecum parasites could be aquatic invertebrates and fish. For example Engraulis anchoita (known as “anchoíta” in Argentina) is one of the most abundant fish species in the Argentine Sea. They constitute an important food base for other species, for example fishes (like Merluccius hubbsi and Scomber japonicus), squids, marine birds and mammals because of their high availability. So they become potential intermediate hosts for parasites. At present, three species are known of anisakids founded in Engraulis anchoita, they are: Anisakis simplex, Terranova sp. and Contracaecum sp. (Timi et al., 2001). We have given the example of Engraulis anchoita because it is a common fish that people consume in Argentina and so we have to pay attention to its potential as a transmitter of Anisakiasis. This can happen when the larvae are eaten alive by the consumer (in this case by humans) because the food is eaten raw or lightly cooked. Anisakiasis can cause ulcers and gastroenteritis. When parasites are consumed by a host that is not the definitive one, it is called paratenic host. Those parasites will not continue their development until they enter their final host. In the case that we have mentioned humans assume the role of paratenic host. Another species of Contracaecum has a partial development in copepods (Arthropoda: Crustacea) followed by later development in fish until it reaches the final host (e.g Phalacrocorax spp.).

The definite host

The bird family Phalacrocoracidae is represented by some 40 species of cormorants and shags. Cormorants (23 species) are aquatic birds at the top of food webs in marine or estuarine ecosystems. All of them are fish-eaters. They dive from the surface, and under water they propel themselves with their feet. Some cormorant species have been found to dive to depths of as much as 45 metres. These birds have a wide distribution along Argentina and other countries of South America; the neotropical cormorant, Phalacrocorax brasilianus (Gmelin, 1789), occurs from Tierra del Fuego, Patagonia, Argentina to coastal Texas, USA, the northernmost extreme of its known geographical distribution (Amato et al., 2006). They can be seen in both marine environments and continental freshwaters environments. Several studies have been done on these birds in different continents, and most show an effort to give these species the status of pest or plague. Some investigations have shown that these birds cause considerable economic losses for different reasons: on commercial fisheries, because they compete for commercial fish and on the aquaculture of commercial fish, such as catfish, atlantic and pacific salmon, rainbow trout, crabs, prawn, shrimps, ornamental fish and mussels, because cormorants feed on ponds where resources are concentrated. Other studies, however, indicate that cormorants do not generate economic losses and contribute to the ecosystem in different ways, because they: perform fish density-dependent regulation allowing fish diversity; are part of bird biodiversity; extract sick organisms from farms, since these are easier to capture; and indicate quality of the water. Maybe the greatest influence of cormorants on wetlands is on nutrient production, because of guano excretion. Cormorants are ideal species to study material flow from aquatic ecosystems to terrestrial ecosystems, via stable isotope analysis of their diets. Also, due to their high mobility, these birds transport eggs of invertebrates, snails, seeds, vegetable material and algae stuck to their feet, feathers or in their digestive tract (Gil de Weir et al., 2003) As we have seen, some parasites of this species use fishes as part of its lifecycle. These fish are eaten by cormorants, the definitive host of these parasites. The presence of Contracaecum nematodes in cormorants is well known. They are common parasites of the gut and proventriculus of these birds, often causing pathological lesions in their hosts. At the same time Cormorant chicks (Phalacrocorax spp.) may be seriously affected by diseases of parasitic origin, mainly due to the habit of food regurgitation from parents to their chicks. Contracaecum species parasitizing cormorants on the southwestern Atlantic coast include C. travassosi Gutiérrez, 1943, which was described from Phalacrocorax atriceps (= P. albiventer) Lesson (Pelecaniformes: Phalacrocoracidae) from Península Valdés, Argentinean seacoast, and C. caballeroi Bravo Hollis, 1939 in P. brasilianus (= P. olivaceus) from the Uruguayan coast (Gutiérrez, 1943; Lent and Freitas, 1948). Later, were found Contracaecum sp. in regurgitated pellets of P. atriceps (= P. albiventer) from Punta León, Chubut Province, Argentina (Garbin et al., 2008). We can say that these birds can contribute to the success of the lifecycle of Contracaecum nematodes, and can be harmful in the case in which humans engage in this lifecycle as paratenic hosts. But at present we need more studies to confirm this idea. Some species of this genus as Contracaecum osculatum, which has been reported from many region of the world to be one of the most common parasites of pinnipeds (Mammalia: Carnivora), and it has been considered to have a worldwide distribution. So we can find these parasites in marine mammals too.

Conclusions

By the beginning of the twentieth century, most of the major discoveries concerning the nature and life cycles of parasites had been made and tropical medicine was beginning to establish itself as a discipline but parasitology still lacked any real cohesion or focus. This focus arrived in 1908 when George Nuttall founded a new journal, Parasitology, as a supplement to the Journal of Hygiene in order to respond to the increasing numbers of papers on protozoological, helminthological and entomological topics that were being submitted for publication to that journal. This brought these three subjects together under one heading and that established the discipline of parasitology (Cox, 2009). About this discipline Keith Vickerman said: “I have always been of the opinion that parasites can provide novel systems for molecular biologists to work on and I have been personally gratified to see the immigration into parasitology of distinguished biochemists, molecular biologists and geneticists. Interest in trypanosomes and parasitology generally snowballed in the last 20 years of the century, as did many of its branches. But what does the future hold for parasitology?” (Vickerman, 2009). In my opinion parasitology can really break down the boundaries between classical zoological sciences as an integrator discipline. This may happen because parasitology contributes to ecology, systematics, evolution, biogeography and ethology. The presence of certain parasites in their hosts is related with some characteristics of their hosts, such as the composition of diet, geographic distribution, characteristics of the environment and the specificity between parasites and hosts. Because of this, we can say that parasitology should be an integral component of any program for biodiversity assessment on local, regional, or global scales (Brooks & Hoberg, 2000). The history of parasitology is fascinating, filled with mysteries solved and new ones created by their resolution. This is the nature of science itself: by answering old questions, always new ones will be discovered.

References

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