TREMATODES OF WILD BIRDS

Trematodes are flat, leaflike parasitic helminthes that Platyhelminthesa diverse are classified in the phylum

group of free-living and parasiticworms that also includes the

cestodes . Current taxonomy places trematodes into two classesthe monogenetic trematodes that are primarily ectoparasites of fish and possess a posterior attachment organ or haptor armed with hooks and the digenetic trematodes that are common endoparasites of a variety of vertebrate hosts and have muscular oral and or ventral suckers. The digenetic trematodes have life cycles with both sexual and asexual phases of

reproductionthe former in their vertebrate definitive hosts and the latter in molluscan intermediate hosts. !ith the exception of the schistosomes, trematodes are hermaphroditic and generally have one or two large, sometimes branched, testes, a comparatively small ovary, an often long and looping uterus, and a single common genital pore. They typically have a bifurcated intestine and blind ceca that exit the body through an anus or via an excretory vesicle. "nlike nematodes, and similar to both cestodes and acanthocephalans, the tegument
lacks a cuticle.

HOST RANGE AND DISTRIBUTION The geographical distribution of tre atodes is influenced b! en"iron ental conditions that affect the distribution of their inter ediate hosts# These conditions include biotic "ariables such as "egetation co"er and abiotic "ariables of the lentic en"iron ent such as si$e% a"erage depth% salinit!% and characteristics of the sedi ents# &or e'a ple% a tre atode that uses a particular species of ollus( as an inter ediate host a!

onl! occur )here that

ollus( is found# The hosts of

Uvulifer ambloplitis% a parasite of (ingfishers *Megaceryle spp#+% include snails% fish% and birds# The distribution

of this tre atode is a co bination of the ranges of all three hosts# Nonetheless% the distribution of a 2 particular tre atode can span large areas% particularl! if definiti"e and inter ediate host species li"e in a broad range of habitats or if the definiti"e host
"ast regions#.
Some species of trematodes occur with great frequency in a large variety of avian hosts, others seem to be rarer, even specific for one or more hosts. Monostomes such as Notocotylus attenuatus and Catatropis verrucosa occur in a large variety of hosts. Holostomes such as Strigea spp. are common parasites of birds of prey, ducks, and gulls. Prosthogonimus ovatus likewise occurs in numerous birds, more than half of which are passerines of wading birds. The species P. cuneatus shows an even greater preference for passerines. At the other extreme, the two most common echinostomesEchinostoma revolutum and Hypoderaeum conoideumare almost entirely confined to ducks and their close relatives Dicrocoeliidae infect the liver (Table 12.2). A number of trematodes develop in very specific and unusual sites. Both Lyperosomum longicauda, a common fluke of Carrion Crows (Corvus corone) in Europe, and Athesmia heterolecithodes from the Ruffed Grouse (Bonasa umbellus) develop specifically in the liver. Clinostomum complanatum is found in the buccal cavity and the upper ends of the esophagus and trachea. Renicola pinguis (Troglotrematidae) and Eucotyle nephritica (Eucotylidae) inhabit the kidney. Some birds are exceptional in harboring two or more species of trematodes that belong to the same genus. The Black Scoter has been reported to be parasitized by 7 species of Gymnophallus (Microphallidae) (Dawes 1946). Skrjabin (1926) described an example of a bird parasitized by 17 species of helminths. The larval stages of trematodes are influenced by density-independent factors such as temperature and moisture. Their populations may fluctuate dramatically over time as a result of environmental changes, possibly leading to local extinctions (Bush et al. 2001). Trematodes that use hosts that are also strongly influenced by density-independent factors and parasites living at the edges of their geographic ranges may also be strongly influenced by density-independent factors (Bush et al. 2001). In contrast, density-dependent effects primarily occur within vertebrate and intermediate hosts and can reduce trematode survival or fecundity and ultimately regulate parasite abundance. Two of the factors most likely to be important in exerting density-dependent effects are host immune responses and competitive interactions either within or between trematode species. Both these factors may lead to host mortality as trematode density increases, with ultimate effects on overall abundance of the parasites

igrates o"er

Summary of host range and distribution information for Sphaeridiotrema globulus (family Psilostomatidae), Cyathocotyle bushiensis (family Cyathocotylidae), and Leyogonimus polyoon (family Lecithodendriidae). in harboring two or more species of trematodes that

Typical life cycle of a digenetic trematode. Eggs are released by adult worms and pass with feces of their avian hosts either into water or onto land. When eggs reach freshwater, a ciliated free-swimming miracidium is released which penetrates a snail, loses its cilia, and develops into a sporocyst. Sporocycsts reproduce asexually to form either more sporocysts or a number of rediae. Rediae reproduce asexually to form more rediae or tailed forms called cercariae. The cercariae emerge from the snail and penetrate a second intermediate host (either a mollusk, amphibian, or fish), the final host, or encyst on vegetation where they transform into metacercariae. Adult worms develop from metacercariae when they are ingested by a suitable definitive host

Typical life cycle of a digenetic trematode.

CLINICAL SIGNS Clinical signs of trematode infections vary and depend on the number of parasites, species of trematode involved, and the organs and organ systems affected. Signs seen in gastrointestinal infections includewatery blood-stained diarrhea and pericloacal feathers stained with blood (Roscoe and Huffman 1982), weakness (i.e., wing droop) (Huffman and Roscoe 1989), leg weakness (van Haitsma 1931), inability to fly (Kocan and Kocan 1972), unsteady gait, disorientation, and a weak raspy call (Huffman and Roscoe 1989). Emaciation (Poonswad et al. 1992) and diarrhea (Dedrick 1965; Patnaik et al. 1970; Graczyk and Schiff 1993) also occur in wild birds. A high intensity of infection with Paratanaisia bragai in the kidney can cause apathy, loss of weight, diarrhea, and death in pigeons (Portugal et al. 1972; Arnizaut et al. 1992). Cloacal discharges have been reported in waterfowl infected with gastrointestinal trematodes (Annereaux 1940; Biester and Schwarte 1959). Increases in cloacal temperature have also been noted (Gagnon et al. 1993). Anemia can be pronounced in infected birds (Kocan and Kocan 1972; Huffman and Roscoe 1989; Luppi et al. 2007). Increases in hemoglobin and packed cell volume have been reported (Gagnon et al. 1993). Mallards (Anas platyrhynchos) experimentally infected with S. globulus develop increased prothrombin time. Excysted metacercariae were shown to produce beta hemolysis on blood agar (Tabery et al. 1988). Approximately 25 proteins have been isolated from the excretory/secretory products of S. globulus (Babu 2000). These have an effect on the coagulation factors Xa and IIa (Isopi 2000)causing a 54% inhibition of factor Xa and a 17% inhibition of IIa. How the excretory/secretor

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