studies on the helminth fauna of iowa ii. cestodes of...

OF WASHINGTON, VOLUME 43, NUMBER 2, JULY 1976 191

Literature Cited

Dickey, L. B. 1921. A new amphibian cestode.J. Parasit. 7: 129-136.

Douglas, L. T. 1958. The taxonomy of nema-totaeniid cestodes. J. Parasit. 44: 261-273.

Hsu, H. F. 1935. Contribution a 1'etude descestodes de Chine. Rev. Suisse Zool. 42;477-570.

James, H. A. 1969. Studies on the genusMesocestoides (Cestoda: Cyclophyllidea).Dissertation Abstracts 29: 3541-B.

Jewell, M. 1916. Cylindrotaenia americana nov.spec, from the cricket frog. J. Parasit. 2:181-192.

Lawler, H. 1939. A new cestode Cylindro-taenia quadrijugosa n. sp. from Rana pipiens,

with a key to the Nematotaeniidae. Trans.Amer. Micr. Soc. 58: 73-77.

Liihe, M. 1899. Zur Kenntnis einiger Distomen.Zool. Anz. 22: 524-539.

. 1910. Die Stisswasserfauna Deutsch-lands. In A. Brauer, Parasitische Plattwiirmer,II : Cestodes, Vol. 18. 153 p.

Wardle, R. A., and J. A. McLeod. 1952. TheZoology of Tapeworms. Univ. Minn. Press,Minneapolis. 780 p.

, , and S. Radinovsky. 1974.Advances in the Zoology of Tapeworms,1950-1970. Univ. Minn. Press, Minneapolis.274 p.

Yamaguti, S. 1959. Systema Helminthum Vol.II . The Cestodes of Vertebrates. IntersciencePub., Inc., New York. 860 p.

Studies on the Helminth Fauna of Iowa II.Cestodes of Amphibians

MARTI N J. ULMER AND HUGO A. JAMESIowa State University, Ames, Iowa 50010, and University of Bridgeport, Bridgeport, Connecticut

ABSTRACT: A survey of 706 amphibians representing 8 species, collected principally during the summersof 1953-74, reveals an incidence of 13.6% infection with cestodes, infected hosts having been collectedfrom 24 areas of northwest Iowa. Almost all infections represent new locality records. Hosts examinedinclude Ambystoma tigrinum (Green), Bufo americanus Holbrook, Bufo cognatns Say, Acris crepitansBaird, Hyla versicolor LeConte, Pseudacris triseriata (Wied), Rana catesbeiana Shaw, and Rana pipiensSchreber.

Three species of adult cestodes are represented in the collection, namely: Cylindrotaenia americanaJewell, 1916; Ophiotaenia saphena Osier, 1931; and Nematotaenoides ranae Ulmer and James, 1976, thelatter from Rana pipiens.

Two types of larval cestodes occur: tetrathyridia of Mesocestoides, and proteocephalan plerocercoids.Rana pipiens, the most abundant host in the region, harbors all five species of cestodes recovered. Each ofseven hosts (5 R. pipiens and 2 B. americanus) harbored more than one type of tapeworm infection.

This study, the second in a series of con-tinuing investigations on the helminth faunaof Iowa (Ulmer, 1970), is based on collectionsof amphibians from the northwest region ofthe state.

Seven hundred and six amphibians were ex-amined; 96 harbored cestodes. Infected hostswere collected from 24 localities (Map 1) rep-resenting four counties (Clay, Dickinson, PaloAlto, and Woodbury). Most specimens werecollected in the vicinity of the Iowa LakesideLaboratory on West Lake Okoboji, DickinsonCounty, during the summers of 1953-74. Dataon host species examined and number of thoseharboring cestodes appear in Table 1. Adult

and larval cestodes are indicated in Table 2.Names of hosts are in accordance with the list-ings by Conant (1958).

Representative slides of cestodes collectedduring the course of this investigation havebeen deposited in the helminthological collec-tion of Iowa State University at Ames.

Cestodes were fixed in AFA, 10% formalin orRistroph's fluid, and whole mounts werestained either in Mayer's paracarmine, Mayer'sHCl carmine, Delafield's or Harris' hema-toxylin. Fast green (0.1% in 95% ethanol)was frequently used as a counterstain forcarmine-stained preparations.

Copyright © 2011, The Helminthological Society of Washington

192 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY

Table 1. Amphibian hosts examined 1953-74.

Map 1

Lakes region of northwest Iowa (DickinsonCounty), indicating collecting sites of amphibians.

12. Methodist camp13. Jemmerson Slough14. Center Lake (North)15. Center Lake (South)16. Diamond Lake17. Kettleson Hogsback18. Marble Lake19. Hottes Lake20. Spirit Lake21. Prairie Lake

1. Milford Creek2. Little Sioux River3. Crossroads pond4. Garlach Slough5. Little Sioux River6. Fairy shrimp pond7. Kettlehole8. Lakeside Laboratory9. Manhattan Slough

10. Little Sioux River11. Triboji Slough

Three additional collecting areas, not shown onmap, include: Trumbull Lake (Clay County),Virgin Lake (Palo Alto County), and the BigSioux River near Stone Park (Woodbury County).

Drawings were made with the aid of a Leitzmicroprojector.

Many of the specimens obtained for thisstudy were provided by graduate students atIowa Lakeside Laboratory, to whom gratefulacknowledgment is made for their contribu-tions to the helminthological collection.

Hosts

Order CandataFamily Ambystomatidae

Ambystoma tigrinum (Green)(Tiger Salamander)

Order SalientiaFamily Bufonidae

Bufo americanus Holbrook(American Toad)

Bufo cognatus Say(Plains Toad)

Family HylidaeAcris crepitans Baird

(Cricket Frog)Hi/hi versicolor LeConte

(Common Tree Frog)Pseudacris triseriata (Wied)

(Western Chorus Frog)Family Ranidae

Rana catesbeiana Shaw(Bullfrog)

Rana pipiens Schreber(Leopard Frog)

Total

54

101

4

6.9

0

26 4 15.4

1 0 0

8 0 0

21 0 0

491 85* 7.3

706 96 13.6

* Includes 11 hosts whose cestode parasites were notavailable for study.

Support for this study was provided in partby grants from the Iowa State UniversityAlumni Research Foundation and by NationalScience Foundation grants G-9022, G-23597,GB-2384 and GB-5465X.

Table 2. Adult and larval cestodes recovered1953-74.

No. infected hosts

Cestodes recovered

Adult cestodesFamily Nematotaeniidae

Cylindrotaenia americanaNematotaerwides rutwe

Family ProteocephalidaeOphiotaenia saphena

Larval cestodesFamily Mesocestoididae

Mcsocestoides tetrathyridiaFamily Proteocephalidae

Proteocephalan plerocercoids

Total

26

4 10

.1 36

7 74



Adult CestodesOrder Cyclophyllidea

Family Nematotaeniidae

1. Cylindrotaenia americanaJewell, 1916 (Figs. 6-9)

HOSTS: Rana pipiens Schreber (leopardfrog), Bufo americanus Holbrook (Americantoad), Acris crepitans Baird (northern cricketfrog).

HABITAT : Intestine.This cylindroid species, originally described

by Jewell (1916) from the intestines of variousanurans including the southern cricket frog(Acris gryllus), is represented in our collectionby specimens from 4 Rana pipiens, 1 Bufoamericanus, and a single Acris crepitans takenin the Okoboji region of northwest Iowa. C.americana is easily recognizable from othergenera within the family Nematotaeniidae bythe presence of two parauterine organs persegment, and by the relatively few eggs withineach.

The formation of the parauterine organswithin a given proglottid was described in con-siderable detail by Jewell (1916) and involvesthe production of a pair of conspicuous trun-cated cones, one dorsal and one ventral, eachof which consists of two portions: a smaller,basal and a larger, bulbular, apical portion con-taining the oncospheres (Fig. 7).

The lif e cycle of C. americana, as reportedby Joyeux (1924), is said to be direct. Hisstudies, however, did not involve experimentalinfections. Because Douglas (1958) ques-tioned the validity of R. pipiens as a host forC. americana, it wil l be necessary that experi-mental studies be undertaken to determine itsrelationship to a closely related species, C.quadrijugosa described by Lawler (1939) fromthis species of anuran. Reference to Lawler'saccount, particularly with reference to theparauterine organ, indicates that specimens inour collection are C. americana,

2. Nematotaenoides ranaeUlmer and James, 1976(Figs. 16-18)

HOST: Rana pipiens Schreber (leopardfrog).

HABITAT : Intestine.

A single Rana pipiens, collected July 8, 1971at Kettleson Hogsback, near Marble Lake(Dickinson County), was infected with 'Nema-totaenoides ranae Ulmer and James 1976, 20specimens having been recovered from theintestine. Attempts to find additional speci-mens in frogs of the Okoboji region in subse-quent years have been unsuccessful. Charac-teristic of gravid proglottids in this species isthe presence of a single parauterine organ,certain developmental stages of which areshown in Figures 17—18. All other describedspecies of nematotaeniids in genera currentlyascribed to this family (i.e., Raerietta Hsu1935, Cylindrotaenia Jewell 1916, Distoich-ometra Dickey 1921, and Nematotaenia Liihe1899) are characterized by the presence of twoor more parauterine organs. A detailed mor-phological description of adult N. ranae waspresented by the authors (1976).

The creation of a new order, Nemato-taeniidea by Wardle, McLeod and Radinovsky(1974), appears unjustified in our opinion,and hence we prefer to retain the family Nema-totaeniidae in the order Cyclophyllidea.

Order ProteocephalaFamily Proteocephalidae LaRue, 1911

3. Ophiotaenia saphena Osier, 1931(Figs. 1-5, 10, 11)

HOSTS: Rana pipiens Schreber (leopardfrog), Bufo americanus Holbrook (Americantoad).

HABITAT : Intestine.This is the most commonly encountered

tapeworm of amphibians of northwest Iowa,almost all examples having been recoveredfrom leopard frogs (R. pipiens), and only oncein a toad (B. americanus). The species wasoriginally described by Osier (1931) fromspecimens found in Rana clamitans in Mich-igan. Thomas (1931, p. 191), referring toFormer's (1923) statement that only \% of177 R. pipiens in the Douglas Lake region ofMichigan harbored tapeworms, recorded thepresence of proteocephalan tapeworms in thisamphibian, but did not identify the speciesinvolved.

Ophiotaeniid cestodes follow a typicalproteocephalan lif e cycle, involving a pro-cercoid larva containing a cercomer and devel-



Figuresproglottid

1-5. Ophiotaenia saphena Osier, 1931 (all specimens from R. pipiens). 1,, 4. Gravid proglottid. 5. Spent proglottid. Note uterine clefts.

2. Scolex. 3. Mature



oping within the haemocoel of a copepod host.The lif e cycle of O. saphena was elucidatedby Thomas (1931, 1934a), and involves thecopepods Cyclops vulgaris var. brevispinosusand Mesocyclops obsoletus, in which matureprocercoids develop in 12-14 days followingingestion of eggs. Thomas observed that theyoungest adults recovered from the intestinesof Rana clamitans resembled in all respects butsize the well-developed procercoids found inthe copepod intermediate host, and suggestedthe possibility of direct infection by frogsthrough accidental ingestion of infectedCyclops. More recent studies on the lif e cyclesof proteocephalans, however (e.g., Fisher andFreeman, 1969), have shown that in a relatedspecies (P. ambloplites) in smallmouth bass,the parenteral plerocercoids are capable ofleaving the viscera and penetrating the gut ofthe same bass host, and that a well-developedend organ is involved in such penetration.Specimens recovered from R. pipiens and B.americanus in this study agree in all respectswith the species description provided by Osier(1931). Unidentified plerocercoid larvae withwell-developed apical organs are also found inthe same species of hosts harboring the adultworm, and occasionally larvae and adults ap-pear concurrently in a single host. Thomas(1931) referred to the hypertrophy of theapical or end organ in the plerocercoid stage,followed by its atrophy and vestigial conditionin adult worms.

Two instances of anomalies involving super-numerary genitalia were found in specimens ofO. saphena recovered in this survey. In one, asingle mature proglottid contained a double setof male and female terminal genitalia (Fig. 10)and in another, a gravid proglottid was pro-vided with a double ovary (Fig. 11).

This study constitutes the first report ofadult O. saphena from Rana pipiens, previousaccounts having indicated that R. clamitansand R. catesbeiana serve as definitive hosts forthis ophiotaeniid. Freze (1965) placed allophiotaeniid tapeworms from amphibians inthe genus Batrachotaenia Rudin 1917 andreferred to this species as B. saphena (Osier,1931). Although Freze cited R. pipiens as ahost, no references included in his monographlist this amphibian host as harboring adult O.sapliena. Apparently Freze misinterpreted

data presented by Thomas (1931) regardinghosts of this species.

Larval CestodesOrder Proteocephala

Family Proteocephalidae LaRue, 1911

4. Proteocephalan plerocercoids(Figs. 12-14)

HABITAT : Liver, mesenteries, coelomiccavity.

Encysted and non-encysted proteocephalanplerocercoids of varying size (0.3 to 30+ mm)were recovered from 36 Rana pipiens and asingle B. americanus on various occasionsbetween June and October. Larger plero-cercoids show evidence of immature proglottidsposteriorly. Al l plerocercoids recovered wereapparently of similar type, characterized bythe presence on the scolex of a well-developedapical organ. Several investigators, includingWood (1965) and Fisher and Freeman (1969)indicate this apical or end organ in proteo-cephalans to be an exocrine gland, used inlysing host tissue.

Although such plerocercoids have not beenidentified with certainty, they may representimmature stages of Ophiotaenia perspicua, acestode of garter snakes and water snakeswhose lif e cycle was determined by Thomas(1934b, 1941) andbyHerde (1938). Thomas(1941), however, distinguished plerocercoidsof O. perspicua from those of O. saphena bythe presence of minute scale-like spines in thetegument of the former species. Our specimensshow no evidence of such tegumental struc-tures.

Thomas (1941, p. 77) suggested that plero-cercoids of O. perspicua may require a sojournwithin the tissues of a second intermediatehost before becoming infective and establishingthemselves within the intestine. More recently,Mead and Olsen (1971) in a study of O.filaroides, whose adults parasitize salamanders,indicated that development to the mature adultwithin the definitive host is dependent uponthe degree of development of plerocercoidswhen ingested. If full y developed, they rap-idly attain a strobilate condition in the intes-tine; if , however, copepod intermediates areingested before the metacestode is well-devel-oped, plerocercoids undergo a tissue (par-



enteral) phase of varying length, ultimatelyreturning to the intestinal lumen by penetrationor by being ingested by another suitabledefinitive host by cannibalism. Such variationsin lif e cycles of ophiotaeniids apparently are ofrather common occurrence among those specieswhose development has been experimentallystudied. Fisher and Freeman (1969) describedthe penetration of such parenteral plerocercoidsof Proteocephalus ambloplitis (Leidy) into thegut lumen of smallmouth bass, reporting thephenomenon as a seasonal one. Prolongedsojourns of plerocercoids in definitive hosts mayalso provide an effective means for survival ofthe species over winter, as suggested by Meadand Olsen (1971) for O. filaroides.

The identification of proteocephalan plero-cercoids of amphibian hosts in our collectionis difficult , and experimental studies are neededto establish their precise taxonomic status.

Order CyclophyllideaFamily Mesocestoididae

5. Mesocestoides tetrathyridia (Fig. 15)HOSTS: Rana pipiem Schreber (leopard

frog), Bufo americanus (American toad).HABITAT : Mesenteries, connective tissues of

brachial region, embedded in mesonephros,liver, and muscular layers of intestinal wall.

Tetrathyridia of Mesocestoides were recov-ered from four B. americanus and 10 R. pipiens.Such larvae lie scattered in varying numbers,but occur most frequently embedded withinthe intestinal wall, in liver and mesonephrictissue, and are also associated with mesenteriesof the brachial region. Both single and multiplecysts were recovered, enclosed in thin cystwalls of host origin.

Specific identification of these larvae wasnot attempted, but unpublished studies byJames provide evidence that the genus ismonotypic, all described species probablybeing M. lineatus (Goeze, 1782). The first

report of North American amphibians harbor-ing tetrathyridia was that of James and Ulmer(1967) who reported their presence in north-west Iowa in the two host species indicatedabove.

Multiple InfectionsMultipl e infections by helminths within a

single amphibian host have been reported fre-quently and were observed often in this study.However, infections involving more than asingle species of cestode within an individualamphibian are relatively infrequent. Brandt(1936), for example, in a study of more than350 specimens of six species of salientians fromNorth Carolina, found only a single frog (R.catesbeiana) harboring two different speciesof cestodes.

During the course of the present investiga-tion, seven instances of multiple cestode infec-tions were encountered, five involving R.pipiens and two, B. americanus. Only one ofthese (a R. pipiens collected 8 July 1971)involved two species of adult cestodes (Ophio-taenia. saphena and Nematotaenoides ranae,Ulmer and James, 1976). Three instancesof concurrent infection involved Mesocestoidestetrathyridia and proteocephalan plerocercoids,two of such double infections having beenencountered in R. pipiens, one in B. americanus.Additionally, two examples of R. pipiens har-boring both Ophiotaenia saphena adults andunidentified proteocephalan plerocercoids,and a single occurrence of tetrathyridia andadult O. saphena in B. americanus were alsorecorded.

DiscussionCestodes of North American amphibians are

singularly few when compared with trematoclesreported from these vertebrates. Leidy (1851)was apparently the first North Americaninvestigator to have indicated the presenceof tapeworms when he reported "Taenia

Plate 2

Figures 6-9. Cylindrotaenia aniericana Jewell, 1916. 6. Scolex (Host: Acris crepitans). 7, 8. Developingparauterine organs (Host: Bufo americanus). 9. Terminal proglottid, showing dorsal and ventral para-uterine organs (Host: B. americanus).

Figures 10, 11. Ophiotaenia saphena, anomalies (from R. pipiens). 10. Mature proglottid with doubleset of male and female terminal genitalia. 11. Gravid proglottid with double ovary.



pulchella" from Bufo americanus, indicatingonly that his specimens consisted of "immatureforms of uncertain classification." In Yama-guti's (1959) Systema Helminthum, Vol. II(The Cestodes of Vertebrates) only eight pagesare devoted to cestodes of amphibians, farfewer than to cestodes of any other vertebrategroup.

Surveys of amphibian cestodes often referto the paucity of these helminths. Early work-ers (LaRue, 1909, 1911, 1914, 1914a; Dickey,1921; Woodland, 1925; and Hannum, 1925)for example, frequently noted this, as haveinvestigators in more recent years when exten-sive surveys have been undertaken. Thus,Ingles (1936) in a study of 264 Californiaamphibia reported cestodes as "very rare";Rankin (1945) reported a single infection ineach of two species of adult cestodes (Bothrio-cephalus rams Thomas, 1937 and Cylindro-taenia americana Jewell, 1916) and single in-fections of larval tapeworms in three hosts;Bouchard (1951) found but a single infectionof cestode (Cylindrotaenia americana) in 195amphibians collected in Maine; Odlaug (1954)in a survey of helminths of 14 species of Ohioamphibians recorded but a single cestode(Distoichometra bufonis Dickey, 1921). Leh-mann (1960) examined 178 California am-phibians and recorded only a single infectionof pseudophyllidean (Bothriocephalus rams)in a newt and Cylindrotaenia in 10 specimens ofsalamanders. Waitz (1961) recorded thepresence of only one undetermined species ofBaerietta in 10 specimens of salamanders(Plethodon) in a survey of 167 amphibiansfrom Idaho. In marked contrast to these find-ings, Brandt (1936), in an extensive surveyof 368 North Carolina amphibians, observedcestode infections ranging from 0-51% in sixspecies of hosts. He also reported that largerhosts harbored more adult cestodes than didyounger ones, and that larval cestodes werefar more abundant than adults in a given host.

Our results confirm his finding that larvalcestodes are considerably more abundant thanare adults in amphibian hosts (Table 2). Hisstudy is apparently the only one indicating ahigher percentage of cestode infections inamphibians than the 13.6% infection in 706hosts representing eight species of amphibiansreported here.

Literature CitedBouchard, J. L. 1951. The Platyhelminthes

parasitizing some northern Maine amphibia.Trans. Amer. Micr. Soc. 70: 245-250.

Brandt, B. B. 1936. Parasites of certain NorthCarolina Salientia. Ecol. Mon. 6: 490-532.

Conant, R. 1958. A field guide to reptiles andamphibians of the United States and Canada.Houghton Miffli n Co., Boston, 336 p.

Dickey, L. 1921. A new amphibian cestode. J.Parasit. 7: 129-136.

Douglas, L. T. 1958. The taxonomy of nema-totaeniid cestodes. J. Parasit. 44: 261-273.

Fisher, H., and R. S. Freeman. 1969. Penetra-tion of parenteral plerocercoids of Proteo-cephalus ambloplitis (Leidy) into the gut ofsmallmouth bass. J. Parasit. 55: 766-774.

Fortner, H. C. 1923. The distribution of frogparasites of the Douglas Lake region, Mich-igan. Trans. Amer. Micr. Soc. 42: 79-90.

Freze, V. I. 1965. Proteocephalata in fish,amphibians and reptiles. In Skrjabin andSpasskii, Essentials of Cestodology, Vol. 5.(English trans. 1969. Available from U. S.Dept. of Commerce.) 597 p.

Haniium, C. A. 1925. A new species of cestodeOphiotaenia magna n. sp., from the frog.Trans. Amer. Micr. Soc. 44: 148-155.

Herde, K. E. 1938. Early development ofOphiotaenia perspicua LaRue. Trans. Amer.Micr. Soc. 57: 282-291.

Ingles, L. G. 1936. Worm parasites of Cali-fornia Amphibia. Trans. Amer. Micr. Soc. 55:73-92.

James, H. A., and M. J. Ulmer. 1967. Newamphibian host records for Mesocestoides sp.(Cestoda: Cyclophyllidea). J. Parasit. 53: 59.

Plate 3

Figures 12-14. Proteocephalan plerocercoids from R. pipiens. 12. Young plerocercoid. 13. Anterior endof plerocercoid showing well-developed apical gland. 14. Large plerocercoid with apical gland.

Figure 15. Tetrathyridium of Mesocestoides, from R. pipiens.Figures 16-18. Nematotaenoides ranae, Ulmer and James 1976 from R. pipiens. 16. Scolex. 17. Develop-

ing parauterine organ. 18. Terminal proglottid showing single parauterine organ.



Jewell, M. E. 1916. Cylindrotaenia americananov. spec., from the cricket frog. J. Parasit.2: 181-192.

Joyeux, Ch. 1924. Recherches sur le cycleevolutif des Cylindrotaeni. Ann. Parasitol.Hum. Comp. 2: 74-81.

LaRue, G. R. 1909. On the morphology anddevelopment of a new cestode of the genusProteocephalus Weinland. Trans. Amer. Micr.Soc. 29: 17-48.

. 1911. A revision of the cestode familyProteocephalidae. Zool. Anz. 38: 473-482.

. 1914. A revision of the cestode familyProteocephalidae. 111. Biol. Mon. 1: 1-350.

1914a. A new cestode, Ophiotaeniacryptobranchi, nov. spec, from Cryptobranchusattegheniensi.i (Daudin). Report Mich. Acad.Sci. 16: 11-17.

Lawler, H. J. 1939. A new cestode, Cylindro-taenia. quadrijugosa n. sp. from Rana pipiens,with a key to Nematotaeniidae. Trans. Amer.Micr. Soc. 58: 73-77.

Lehmann, D. L. 1960. Some parasites ofcentral California amphibians. J. Parasit.46: 10.

Leidy, J. 1851. Helminthological contributions.No. 3. Proc. Acad. Nat. Sci. Philadelphia5: 239-244.

Mead, R. W., and O. W. Olsen. 1971. Thelif e cycle and development of Ophiotaeniafilaroides (LaRue, 1909) (Proteocephala:Proteocephalidae). J. Parasit. 57: 869-874.

Odlaug, T. O. 1954. Parasites of some Ohioamphibians. Ohio J. Sci. 54: 126-128.

Osier, C. P. 1931. A new cestode from Ranaclamitans Latr. J. Parasit. .1.7: 183-186.

Rankin, J. S., Jr. 1945. An ecological study ofhelminth parasites of amphibians and reptiles

of western Massachusetts and vicinity. J.Parasit. 31: 142-150.

Thomas, L. J. 1931. Notes on the lif e historyof Ophiotaenia saphena from Rana clamitansLatr. J. Parasit. 17: 187-195.

. 1934a. Further studies on the lif e cycleof a frog tapeworm Ophiotaenia saphenaOsier. J. Parasit. 20: 291-294.

. 1934b. Notes on the lif e cycle ofOphiotaenia perspicua, a cestode of snakes.Anat. Rec. 60: 79-80 (Suppl.).

1941. The lif e cycle of Ophiotaeniaperspicua LaRue, a cestode of snakes. Revistade Medicina Tropical y Parasitologia 7: 74-78.

Ulmer, M. J. 1970. Studies on the helminthfauna of Iowa. I. Trematodes of amphibians.Amer. Midi. Nat. 83: 38-64.

Ulmer, M. A. and H. A. James. 1976. Nema-totaenoides ranae gen. et sp. n. (Cyclo-phyllidea: Nematotaeniidae), from the leopardfrog (Rana pipiens) in Iowa. Proc. Helm. Soc.Wash. 43: 185-191.

Waitz, J. A. 1961. Parasites of Idaho am-phibians. T. Parasit. 47: 89.

Wardle, R. A., J. A. McLeod, and S. Rad-inovsky. 1974. Advances in the zoology oftapeworms. Univ. of Minnesota Press, Minne-apolis. 274 p.

Wood, D. E. 1965. Nature of the end organ inOphiotaenia filaroides (LaRue). J. Parasit.51: 541-544.

Woodland, W. N. F. 1925. On three newproteocephalids (Cestoda) and a revision ofthe genera of the family. Parasitol. 17: 370-394.

Yamaguti, S. 1959. Systema Helminthum, Vol.II . The Cestodes of Vertebrates. IntersciencePub., New York. 860 p.

Announcement

4th International Congress of ParasitologyWarsaw, Poland

August 19-26, 1978

For further information contact:

Prof. Dr. Bernard BezubikSecretary General of ICOPA IVDepartment of ParasitologyUniversity of Warszawa00-927 Warszawa, Poland


studies on the helminth fauna of iowa ii. cestodes of...

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