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Notes on the Biology of Plagiorchis Noblei Park, 1936 (Trematoda: Plagiorchiidae)

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Notes on the Biology of Plagiorchis Noblei Park, 1936 (Trematoda: Plagiorchiidae) 44 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY Notes on the Biology of Plagiorchis noblei Park, 1936 (Trematoda: Plagiorchiidae) HARVEY D. BLANKESPOOR1 Department of Zoology, Iowa State University, Ames, Iowa 50010 and Iowa Lakeside Laboratory, Milford, Iowa 51351 ABSTRACT: Several aspeets of the parasite-host relationships of larval and adult Plagiorchis noblei were investigated. In the laboratory, eggs and metacercariae were infective for a longer time than had previously been reported. Cercariae of P. noblei from naturally infected lymnaeid snails showed marked nocturnal periodicity. Examination of more than 4,000 naturally occurring adult Lymnaca stagnaUs and Stagnicola reflexa revealed that the highest prevalence of infection with this plagi- orchiid trematode occurred from August to early October. Prevalence of adult worms in red-winged and yellow-headed blackbirds collected in the same area peaked in late June to early August. Digenetic trematodes of the genus Plagior- nated eggs incubated at room temperature in chis Liihe, .1899, are intestinal parasites found filtered lake water. Snails were reared and in nearly every class of vertebrates, but partic- maintained in aquaria on a diet of lettuce, fish ularly in birds and mammals. Most known life pellets and oyster shells. histories of Plagiorchis involve lymnaeid snails Cercariae of P. noblei, showing nocturnal and aquatic insects as first and second inter- periodicity, were obtained by first placing in- mediate hosts, respectively. Knowledge of life fected snails under fluorescent light for 24 cycles of members of this genus was summa- hours and then in total darkness for an addi- rized by Buttner and Vacher (1960). tional hour. Various species of aquatic insect Plagiorchis noblei was described by Park larvae were exposed to these cercariae. Mos- (1936) from a collection of 20 specimens re- quitoes and certain chironomids were reared covered from the small intestines of red-winged from eggs; other species were collected from blackbirds, Agelaius phoeniceus. Of the more tertiary ponds at the Ames Sewage Plant than 45 species included in the genus Plagior- (Ames, Iowa). Because these ponds contained chis at that time, P. noblei most closely resem- no lymnaeid snails, naturally occurring infec- bled P. maculosus (Rudolphi, 1802) Braun, tions of Plagiorchis were not present. Dragon- 1902, from mice. Certain aspects of the life fly naiads, individually isolated in finger bowls history of Plagiorchis noblei have been studied to prevent cannibalism, were fed small aquatic by Williams (1964a, b), Daniell (1964) and arthropods obtained from the same ponds. Daniell and Ulmer (1964). These studies, Birds used in this study were either reared however, have been published only in the form from eggs under helminth-free conditions of brief abstracts. Additional life cycle data (house sparrows) or were purchased as newly resulting from experimental studies on host- hatched young from suppliers (domestic parasite relationships of P. noblei are presented chicks). Newly hatched birds were placed in in this study. artificial nests and transferred to a simple incu- bator constructed of wire mesh, wood and a Materials and Methods heating pad. Adults were maintained on a Eggs of Plagiorchis noblei were recovered mixture of coarse game-scratch and 26% grain from naturally infected red-winged blackbirds balancer (nonantibiotic). Occasionally, insect (Agelaius phoeniceus). Gravid worms were larvae (Tenebrio molitor and Musca domestica) placed in petri dishes containing boiled lake were used to supplement this diet. water and teased apart to obtain the eggs. Laboratory-reared Stagnicola reflexa and Lym- Summary of Life Cycle naea stagnaUs were exposed to fully embryo- The life cycle of Plagiorchis noblei involves at least two species of snails, Stagnicola reflexa 1 Present address: Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109. and Lymnaea stagnaUs. Following ingestion of Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 44, NUMBER 1, JANUARY 1977 45 TIME (HOURS) Figure 1. Cercarial emergence of P. noblei from three naturally infected lymnaeid snails at hourly intervals during a continuous 48 hours of natural light and darkness. embryonated eggs, miracidia hatch, penetrate when experimentally fed to yellow-headed the gastropod's digestive tract, then elongate to blackbirds (Daniell, 1964). form mother sporocysts on the outer surface Definitive hosts acquire P. noblei by inges- of the intestine. Daniell (1964) observed fully tion of infected second intermediate hosts. developed miracidia within the eggs two days Experimental hosts include domestic chicks after they were expelled from adult flukes. (Gallus gallus), yellow-headed blackbirds (Xan- Daughter sporocysts produced by mother thocephalus xanthocephalus) and red-winged sporocysts migrate to the hepatopancreas of the blackbirds (Agelaius phoeniceus) (Daniell, snail and produce large numbers of xiphidio- 1964). Blankespoor (1974) found that at least cercariae approximately 40 days after the egg 17 species of birds and mammals are capable was ingested. Daniell (1964) and Williams of harboring experimental infections of this (1964b) observed nocturnal periodicity of cer- species. cariae shed from Stagnicola rejlexa. Cercariae penetrate and encyst in a variety of aquatic Experimental Results second intermediate hosts including odonates, Egg dipterans, caddisflies, mayflies and amphipocls Data from this study indicate that labora- (Daniell, 1964; Williams, 1964a). tory-reared S. reflexa became infected when According to Daniell and Ulmer (1964), exposed to eggs of P. noblei 84 hours following metacercariae of P. noblei are infective seven extrusion from adult worms. Furthermore, ex- days or less after cercarial penetration into perimental infections could still be established immature insects (damselfly and dragonfly in snails 43 days after eggs had been main- naiads and midge larvae). Williams (1964a), tained in the laboratory at room temperature. working with the same trematode species, found metacercariae to be infective four to six Cercaria days after cercarial penetration of a mosquito, DIEL PERIODICITY: The following investiga- Aedes aegypti. Metacercariae encysted in tion was undertaken to obtain more precise dragonfly naiads for 36 days were still infective information on cercarial emergence of P. noblei Copyright © 2011, The Helminthological Society of Washington 46 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY 400- LIGHT DARKNESS £ 300- S. REFLEXA oc L. STAGNALIS u L. STAGNALIS ec in U f g 200- O KXH TIME (HOURS) Figure 2. Cercarial emergence of P. noblei from three naturally infected lymnaeid snails during alter- native three-hour periods of light and darkness. during alternating periods of light and dark- experiment were again individually isolated in ness. Two days before hourly counts of finger bowls and then subjected to alternating cercarial emergence began, three naturally in- three-hour periods of light and darkness. How- fected lymnaeid snails were individually iso- ever, during this experiment, a constant lated in finger bowls containing lake water temperature of 19-20 C was maintained. and were then maintained under natural con- Cercariae emerged from these snails almost ditions of light and darkness. At hourly in- entirely during periods of darkness (Fig. 2). tervals for two consecutive days, each snail SEASONAL PERIODICITY: During the summer was transferred to another bowl containing and fall of 1969 (June-October), 4,361 snails, fresh water at the same temperature. Cer- representing two lymnaeid species (S. reflexa cariae that had emerged during the previous and L. stagnalis) were collected in nature, in- hour were then fixed in 5% formalin and sub- dividually isolated in the laboratory, and ex- sequently counted. amined for natural infections of P. noblei. As shown in Figure 1, cercariae of P. noblei Twenty-two of 2,691 (0.82%) S. reflexa and exhibit pronounced nocturnal periodicity, but 19 of 1,676 (1.13%) L. stagnalis harbored the time of maximum emergence appears to natural infections of P. noblei. Natural infec- vary with individual gastropod hosts. Of a tions from both species of snails over the entire total of 15,218 cercariae from these snails, period averaged 0.94% (41 of 4,361). Per- 10,957 (72%) were shed between 8:30 PM centages of infection are based, however, on and 5:30 AM. In these experiments, water tem- numbers of snails actually shedding cercariae peratures varied in accordance with ambient and do not take into account all those with temperatures. To determine if declining tem- prepatent infections. Figure 3 summarizes peratures at night relate to nocturnal period- monthly percentages of naturally infected icity, another set of experiments was under- snails. Infections remained below one per cent taken. The three snails used in the above until August and September. Rate of natural Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 44, NUMBER 1, JANUARY 1977 47 JUNE JULY AUG SEPT OCT TIME (MONTHS) Figure 3. Percentage of naturally infected Stagnicola reflexa and Lymnaea stagnalis shedding cercariae of P. noblei. infection in S. reflexa reached a peak of 1.14% nearly 10 days, whereas those maintained at (6 of 525) in August, whereas 4.33% (16 of temperatures of 16 and 30 C survived for 370) of L. stagnalis harbored infections of P. only 90 and 18 hours, respectively. Cercariae noblei in September. Infections of P.
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