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Endoparasites 318 PATHOLOGY C. Endoparasites OLIVER KRONE good parasite does not harm its host in a way that it Leibniz-Institute for Zoo and Wildlife Research (IZW) weakens or kills the host, because this also would affect Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany the parasite itself. And indeed, long-term, well-adapted parasites often are less pathogenic to their traditional hosts, whereas evolutionarily young parasites can harm their hosts severely. That said, the host–parasite rela- tionship is a dynamic evolutionary system that may be INTRODUCTION compared to an arms race, in which both sides alter their behavior in response to the other in a way that sustains Endoparasites are organisms that, in their developmen- the interaction (Van Valen 1973). Dobson et al. (1992) tal or adult stages, live in animals called hosts. Endopar- described parasitic worms as natural enemies causing a asites, which include single-celled protozoa, worms permanent drain of energy in their hosts that affects the (helminths), and arthropods, invade nearly all organs of behavior and reproductive success of them. Depending animals. Protozoans are found in digestive and respira- on age, immune status, and infection pressure, parasites tory systems, muscles, blood, and feces of their hosts. can invade their hosts to different degrees, and probably Several endoparasitic worms feed on the ingesta in the are a strong selective force on their hosts. intestine of the definitive (final) host or are attached to Parasitism as a way of life developed independent- the mucosal layer within the intestine or the trachea ly in different taxa. Endoparasites are believed to have where they suck blood or epithelial cells. Other worms evolved several million years ago. The oldest parasitic are found in specific organs or only parts of organs. roundworms (nematodes) were found in beetles embed- Some worms migrate through different internal organs ded in amber from the Eocene (Conway Morris 1981). during their stages of development. Parasitic arthro- Compared with their hosts, parasites are relatively sim- pods, including ticks, mites, flies, mallophages, and ple organisms, many of which have “degenerated” dur- fleas, often are found on the skin or feathers of their ing evolution, although parasites have the advantage hosts. Only a few arthropods enter the internal organs of that processes such as digestion or locomotion are pro- the hosts. Endoparasitic arthropods include mites living vided by the host. Tapeworms living in a nutritionally in layers of the skin or subcutaneously, and the larval rich environment — the intestine of their hosts — have stages of flies (maggots) that burrow through internal reduced their digestive system and are able to reabsorb organs. their food through their cuticula. Parasites also have It is not the aim of this chapter to describe all developed new abilities in response to their parasitic endoparasites and their ways of life but rather to pro- lifestyles (e.g., host-finding mechanisms, resistance vide information on several relevant examples. against the host’s immune and digestive system, and The traditional doctrine in parasitology states that a new organs such as sensoric receptors). As a result of PATHOLOGY 319 such adaptations, the genome of parasites can be bigger harm the health of the host. Continued parasitic infec- than those of the free-living parasite relatives and, in tion can weaken the host’s immune system, thereby some cases, bigger than those of the hosts they occupy enabling additional parasites to enter the host. In such (Poulin 1998). instances the parasitic infection is considered a factori- As an adaptation to their way of life endoparasites al disease. often develop complex life cycles, including stages of sexual and asexual reproduction. Sexual multiplication normally occurs in the definitive host they forage in. ENDOPARASITES OF BIRDS OF PREY The developing stages of endoparasites leave the host actively or passively to move to the next suitable envi- Endoparasites are frequently detected in raptors. ronment. The life cycle of a parasite can be direct or Indeed, in some populations of birds of prey, 90% of all indirect (i.e., via intermediate hosts). Complex life individuals have helminths (e.g., Krone 2000, San- cycles often contain more than one intermediate host martin et al. 2004). required by the parasite to reach the definitive host. Endoparasites found in birds of prey include proto- Sexual reproduction generally occurs in the definitive zoans, roundworms (nematodes), spiny-headed worms host and asexual reproduction occurs in intermediate (acanthocephala), flukes (digenetic trematodes), tape- hosts. On the way to the next host many developmental worms (cestodes), and tongue worms (pentastomida). stages may be lost. To increase the likelihood of host I provide a broad introduction here. A more exten- infection, parasite fecundity often has increased during sive review of endoparasites found in birds of prey is in its evolution. As a result, some roundworms can pro- Lacina and Bird (2000). A more general overview of duce about 200,000, and some tapeworms up to helminths in birds is in Rausch (1983). For information 720,000 eggs per day (Crompton and Joyner 1980). on the biology and treatment of parasites in raptors see Parasites have developed a diversity of strategies to Krone and Cooper (2002). reach their definitive host. They often try to produce as many eggs as possible of which only a few develop to Protozoa mature parasites. Sometimes intermediate hosts are manipulated by their parasites to become an easier vic- Unicellular parasites usually are very small and only tim to a predator. Several species of flukes that para- visible by a microscope (Fig. 1). Among the eight class- sitize piscivorous birds migrate into the eyes of the last es of protozoa, two are of major interest in raptor para- intermediate host (fish) reducing their ability to see sitology. (Odening 1969). Protozoa of the genus Sarcocystis use Trichomonas. One of the oldest recognized and raptors as definitive hosts and mice or birds as interme- most significant diseases in raptors, “frounce” or “crop diate hosts where they form cysts in the muscles. Infect- canker,” is caused by Trichomonas gallinae, a single- ed mice changed their behavior and are twice as likely celled organism that belongs to the class to be eaten by Common Kestrels (Falco tinnunculus) as Zoomastigophorea. These spindle- to pear-shaped small are non-infected mice (Hoogenboom and Dijkstra flagellated protozoans reproduce by simple division. 1987). Behavioral changes due to parasitic infections in Direct transmission via the feeding of nestlings with definitive hosts (birds of prey) also have been crop-milk occurs in Columbiformes. The parasite lives described. Experimentally infected American Kestrels on and in the mucosal layers of the oropharynx, oesoph- (F. sparverius) exhibited decreased flight activity dur- agus, and crop. Infection in raptors occurs via the inges- ing their reproduction and a prolonged courtship behav- tion of contaminated prey. Pigeons and doves are the ior compared to control birds (Saumier et al. 1991). main reservoirs of Trichomonas, but other birds, includ- Whether an infection with parasites induces clinical ing Passeriformes, also can be infected. Deep, yellow, signs depends on the status of the immune system, hor- crumbly, caseous lesions often are found in advanced mone status, and infection pressure. An infection with a infections in the upper digestive tract. These abscesses few ascarids, for example, may cause some irritation in can grow up to the size of ping-pong balls and, depend- the intestinal mucosa but may not necessarily affect the ing on where they are, can mechanically block the pas- condition of the host. A heavy infection can block the sage of food or respiration. Raptors feeding on birds are lumen partially or completely, resulting in a perforation more likely to be infected. Nestlings of urban goshawks or rupture. The metabolic products of worms also can often carry the agent at high prevalence in their pharynx 320 PATHOLOGY Figure 1. All protozoan parasites in line one are photographed at 1000x magnification (scale 50µm). The helminth eggs in lines two to four are photographed at 400x and 630x magnification (scale 50µm). (1) Sarcocystis sp., (2) Caryospora sp., (3) Haemopro- teus sp., (4) Leucocytozoon sp., (5) Trypanosoma avium, (6) Capillaria tenuissima, (7) Eucoleus dispar, (8) Syngamus trachea, (9) Hov- orkonema variegatum, (10) Porrocaecum sp., (11) Microtetrameres cloacitectus, (12) Synhimantus laticeps, (13) Physaloptera alata, (14) Serratospiculum tendo, (15) Metorchis sp., (16) Nematostrigea serpens, (17) Strigea falconispalumbi, (18) Neodiplostomum attenuatum, (19) Cladotaenia globifera, (20) Centrorhynchus sp. PATHOLOGY 321 without showing clinical symptoms. Sick birds may are vectors. In the avian host, the parasites reproduce develop stomatitis (i.e., inflammation of the mucous asexually in specific tissues. Only in the last stage do membrane of the mouth) and have difficulty in swal- the parasites appear in the blood while waiting for a lowing food items. Birds often dehydrate and starve. blood-feeding insect to infect. Plasmodium is more Secondary bacterial infections can complicate and pathogenic than Leucocytozoon and Haemoproteus. speed up the disease process. Plasmodium, in particular, causes problems in translo- Trypanosoma. Flagellated blood parasites of the cated birds from areas where birds are
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