Notocotylus biomphalariae n. sp. (Digenea: Notocotylidae)from Biomphalaria peregrina (Gastropoda: Pulmonata) in Patagonia,Argentina

Veronica Flores* & Norma BrugniLaboratorio de Parasitologıa, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue,Quintral 1250, 8400, San Carlos de Bariloche, Rıo Negro, Argentina

Accepted for publication 3 January, 2005

Abstract

A new species of Notocotylus was found parasiting a freshwater pulmonate snail, Biomphalaria peregrina.Naturally infected snails were collected from two temporary ponds in the Nahuel Huapı National Park inPatagonia. The characteristics of the larval stages are presented. Experimental adults were recovered fromthe intestinal caeca of ducks and chicks. Adults of Notocotylus biomphalariae n. sp. exhibit an aspinosetegument, two lateral rows of 11 ventral glands and a median row of four, a uterus with 12–16 coils ofwhich 2–4 are previtelline, a metraterm equivalent in size to 65–68% of the cirrus-sac length, a previtellinefield which extends to the middle of the body, a lobed testis and a genital pore closely posterior to theintestinal bifurcation. The rediae have one to three cercariae. The cercariae, when shed, are trioculate andhave a long tail; they encyst in the environment and become infective 12 days after encystment.

Introduction

The life-cycle of species of Notocotylus Diesing,1839 includes snails as the first intermediate host,shed cercariae that encyst on vegetation and snailshells, and the definitive hosts are mainly birds andmammals. The snail Biomphalaria peregrinad’Orbigny has been recorded from Colombia,Ecuador, Bolivia, Chile, Brazil, Paraguay,UruguayandArgentina (Rumi, 1991). In Argentina, infectedB. peregrina north of 35� S have been found to beparasitised by a furcocercus cercaria, two xiphidi-ocercariae, two echinostome cercariae and twomonostome cercariae (Morris, 1976, 1978; Ostrow-ski deNunez, 1981;Ostrowski deNunez et al., 1990,1997). One of the monostome cercariae (Ostrowskide Nunez, 1976) is a larval stage of Hippocrepisfuelleborni Travassos & Vogelsang, 1930 but theother has an unknown life-cycle (Morris, 1978).

The purpose of the present paper is to describethe life-cycle of Notocotylus biomphalariae n. sp.,

which parasitises B. peregrina, including details ofits intra-molluscan, cercarial and metacercarialstages and a description of experimentally rearedadults.

Materials and methods

Two fish-less temporary ponds, one near NahuelHuapı Lake (41�03¢S, 71�23¢W), i.e. ‘FantasmaPond’, and the other near Mascardi Lake (41�17¢S,71�34¢W), were studied. They have a hydroperiod,which extends from autumn (April) to early sum-mer (December).

Naturally infected B. peregrina were collectedbetween the spring of 2002 and the summer of2003. The snails were captured at a depth of 20–50 cm. Each snail was placed in a glass with 30 mlof tap-water to observe cercarial shedding andmetacercarial encystment on the wall. One-day-oldGallus gallus domesticus and Anas sp. were fed withmetacercariae at different days post-encystment(Table 1). Metacercariae (N=25) were observed

*Author for correspondence: (E-mail: vflores@crub.uncoma.edu.ar)

Systematic Parasitology (2005) 61:207–214 � Springer 2005DOI 10.1007/s11230-005-3166-2

and measured live. Rediae (N=30) and cercariae(N = 20) were observed live, fixed in 4% hotformalin and measured. Adults (N=15) were fixedin 4% hot formalin, stained with Grenacher’scarmine-alum, cleared in creosote, mounted inCanada balsam and measured. All of the experi-mental adults obtained came from naturallyinfected B. peregrina collected at Fantasma Pond.Measurements of holotype and paratypes corre-sponding to worms of 21 days post-infection(d.p.i.) from Anas sp. are given in text, with rangeand mean in parentheses. Measurements of worms14 d.p.i. and 21 d.p.i. recovered from G. g.domesticus and those of 14 d.p.i. from Anas sp.are given in Table 2. All measurements are givenin micrometres. Drawings of the rediae, metac-ercariae and adults were made with the aid of adrawing apparatus and the cercariae were drawnfree-hand.

Additionally a specimen (in dorsal view) ofN. gibbus (Mehlis in Creplin, 1846) (MACN-Pa 42)from Fulica leucoptera (see Szidat & Szidat, 1961),deposited in the Coleccion Nacional de Parasitolo-gıa (MACN-Pa) in the Museo Argentino deCiencias Naturales Bernardino Rivadavia, wasstudied.

Notocotylus biomphalariae n. sp.

Type-host: Anas sp. (type-host) and Gallus gallusdomesticus (both experimental).Site: Distal portion of caeca.

Intermediate host: Biomphalaria peregrina (D’Or-bigny) (Mollusca).Site: Digestive gland along and around intestinalwall.Type-locality: Fantasma Pond (near Nahuel HuapıLake) (41�03¢ S, 71�23¢ W), Patagonia, Argentina.Prevalence in intermediate host: 0.7% (16/2,447).Other locality: Pond near Mascardi Lake (41�17¢S,71�34¢W), Patagonia, Argentina.Prevalence in intermediate host at other locality:7.6% (8/104).Type-material: Holotype No. 427 (1) and threeparatypes No. 427 (2–4), two slides of rediae No.427 (5–6) and one of cercariae No. 427 (7)deposited in the Coleccion Nacional de Parasit-ologıa (MACN-Pa) in the Museo Argentino deCiencias Naturales Bernardino Rivadavia, Bue-nos Aires, Argentina. Three paratypes No. 5401,one of rediae No. 5402 and one slide of cercariaeNo. 5403 in the Coleccion Helmintologica delMuseo de La Plata, Museo de La Plata, Argen-tina. Two paratypes Reg. No. 2005.2.8.4-5, oneslide with cercariae Reg. No. 2005.2.8.6 and oneslide with rediae Reg. No. 2005.2.8.7 depositedin the Collection of the Natural HistoryMuseum, London, UK. Six paratypes No. 194(1–6) and two slides of cercariae and three slidesof rediae No. 193 (1–5); all of the specimens of14 d.p.i. from Anas sp. No. 195 (1–15) and thoseof 14 d.p.i. – No. 159 (1–2) and 21 d.p.i. – No.160 (1–2) from G. gallus domesticus are depositedin the Coleccion Parasitologica del CentroRegional Universitario Bariloche, Universidad

Table 1. Protocol of infection for Notocotylus biomphalariae n. sp. indicating: locality, experimental hosts, age of metacercariae,number of cysts fed, days post-infection and number of specimens obtained.

Locality Experimental

host

Age of

encysted cercariae (days)

No. of

cysts fed

Days

post-infection

No. of

specimens recovered

Fantasma Pond Anas sp. 19–26 300 14 52

Anas sp. 35 200 14 1

Anas sp. 12 150 21 19

Anas sp. 18 150 14 0

G. gallus dom. 15 95 21 2

G. gallus dom. 15 55 14 2

G. gallus dom. 15 28 14 0

Pond near Mascardi Lake G. gallus dom. 3–5 90 14 0

G. gallus dom. 11 40 14 0

G. gallus dom. 7 125 21 0

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Nacional del Comahue, San Carlos de Bariloche,Argentina.

Description

Adult (Figures 1–3). Body, 1,573–2,059 · 801–1,030 (1,861.0 · 938.1), flat, oval with roundedposterior end, concave ventrally. Tegument aspi-nose. Ventral glands arranged as follows: 11glands in each lateral row and 4 glands in medialrow; first gland of medial row overlaps base ofcirrus-sac and last one overlaps ovary; first glandof lateral rows at level of first third of cirrus-sac

and last at post-testicular level. Oral sucker 122-144 · 134-161 (132.6 · 151.2), terminal. Pharynxabsent; oesophagus 7–48 (28.6); caeca lateral,extend posteriorly, bordering uterine coils, passbetween ovary and testes and reach to level ofexcretory pore.

Testes 250–336 · 163–221 (289.4 · 190.6) atposterior end of body, symmetrical with externalmargin lobed. External seminal vesicle forms coilprior to opening dorsally into cirrus-sac. Cirrus-sac 422–643 · 98–144 (510.7 · 113.9), represent-ing 23–32 (27.7)% of body length, elongate,contains cirrus, prostatic cells and internal coiledseminal vesicle. Cirrus with maximum length of

l

Table 2. Measurements of Notocotylus biomphalariae n. sp. obtained experimentally from Anas sp. and Gallus gallus domesticus atdifferent days post-infection and of N. gibbus.

Species Source N. biomphalariae n. sp. Present study N. gibbus

Szidat & Szidat, 1961

Host Anas sp. Gallus gallus domesticus Fulica leucoptera

No. of parasites measured 15 2 2 1

Days post-infection 14 14 21 Natural infection

Variables Min Max Mean Min Max Min Max

Body length 1,316 1,659 1,451 1,888 2,031 1,516 2,231 1,761

Body width 601 801 690.2 972 1,173 715 1,030 795

Oral sucker length 98 122 111.0 132 163 120 144 103

Oral sucker width 115 130 121.8 158 185 132 158 161

No. of ventral glands 11-4-11 11-4-11 11-4-11 –

Oesophagus length 36 84 56.5 31 31 36 48 29

Testes length 180 259 226.2 317 355 240 384 187

Testes width 125 182 145.8 211 221 161 230 127

Ovary length 115 182 144.8 127 132 151 202 122

Ovary width 94 163 138.2 158 178 127 178 132

Cirrus-sac length 365 461 423.0 528 557 461 595 509

Cirrus-sac width 84 115 93.1 137 149 103 144 98

Cirrus length 77 163 136.4 – – – – 132

Cirrus width 43 62 52.1 – – – – 38

Cirrus papillae height 2 4 3.1 – – – – –

Metraterm length 274 384 303.7 384 396 324 408 264

No. of uterine coils 12 15 13.4 13 13 15 15 13

No. of previtelline uterine coils 1 3 2 2 3 2 3 6

Vitelline field length 394 538 470.4 739 806 461 787 442

Anterior limit of vitelline fields 605 806 699.5 826 902 749 998 912

Egg length 22 26 23.5 24 24 24 24 24

Egg width 10 12 11.3 12 12 12 12 12

Metraterm/Cirrus-sac (%) 63 88 72.0 69 75 69 70 52

Cirrus-sac/Body length (%) 25 34 29.3 27 28 27 30 29

Ant. vitelline limit/Body length (%) 46 52 48.2 44 44 45 49 52

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Figrues 1–3. Notocotylus biomphalariae n. sp., experimental adult of 21 d.p.i. from Anas sp. 1. Ventral view, eggs in uterine coilsomitted. 2. Terminal genitalia. 3. Ventral view showing distribution of ventral glands. Scale-bars: 1,3, 500 lm; 2, 100 lm.

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355 and width of 96; extrusible portion coveredwith papillae 5–7 (5.3) high. Genital pore ventro-medial, closely posterior to level of intestinalbifurcation.

Ovary 137–192 · 134–252 (169.0 · 170.6), sit-uated between testes, lobed. Ratio between testic-ular and ovarian length 1:1.5–1.9 (1.7). Uterusintercaecal, arranged in 12–16 transverse coils,with 2–4 of these coils previtelline and 2 small coilslocated to left of cirrus-sac. Metraterm 288–420(335), representing 56–84 (69.7)% of cirrus-saclength, lies parallel to cirrus-sac on its left side,well differentiated, with thickened walls. Worms of21 d.p.i. have eggs densely arranged in all uterinecoils. Eggs in mounted specimens 22–26 · 10–14(24.3 · 12.0), with 1 filament at each pole. Vitel-larium composed of distinct irregular follicles;fields lateral, 538–749 (641.8) long, with somefollicles extending back lateral to testes; previtel-line region of body 720–960 (853.1); ratio betweenprevitelline region and body length 43–51 (45.9)%.Transverse vitelline ducts arise from posterior ends

of vitelline fields, unite at level of Mehlis’ gland toform oval vitelline reservoir.

Excretory pore sub-terminal.

Redia (Figure 4). Yellowish rediae occur in diges-tive gland along and around intestine wall ofmollusc, 643–1,248 · 173–307 (1,013.4 · 217.6).Muscular pharynx 58–86 · 58–96 (68.5 · 73.3);gut filled with brownish-black particles, 288-893(600.2) long, representing 33–75 (58.9)% of bodylength. Birth-pore not observed. Rediae containup to 3 advanced oculate cercariae and numerousgerm-balls at posterior end.

Cercaria (Figure 5). Cercariae within rediae, pig-mented only around eye-spots. Shed cercariae,brown pigmented and tri-oculate, 346–394 · 154–221 (369.1 · 191.0). Distance between median eye-spot and anterior extremity 39–53 (42.7), betweenanterior extremity and lateral eye-spots 48–62(55.0). Cystogenous cells numerous, throughoutentire body (not illustrated); adhesive pockets

Figures 4–6. Stages of Notocotylus biomphalariae n. sp. 4. Redia with immature cercariae. 5. Cercariae. 6. Metacercariae. Scale-bars: 100 lm.

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situated postero-laterally, not prominent. Tail -long, cylindrical, 634–797 · 58–77 (701.8 · 62.4),narrows distally. Ventral sucker absent; oralsucker 36–53 · 34–50 (41.6 · 41.3). Pharynxabsent; oesophagus tubular; intestinal bifurcationat level of lateral eye-spots; caeca extend toposterior extremity. Genital primordia formed by2 cell masses, 1 at end of first third of body andother anterior to excretory vesicle, connected bymedian string of cells. Excretory system with 2lateral branches, unite at level of median eye(monostomi type) and open posteriorly into excre-tory vesicle; branches filled with oblong granules(5–10 · 3–5 (6.6 · 4.1)) at level of eye-spots, withsmaller, spherical granules elsewhere. Caudalexcretory canal not seen in either live or in fixedcercariae.

Metacercaria (Figure 6). Hemispherical, darkbrown metacercarial cyst 146–158 (151.9) in diam-eter. Cyst-wall 10–17 (13.5), consists of 3 layers;outer layer irregular and granular; other 2 regularand laminated.

Remarks

Metacercariae of N. biomphalariae n. sp. wereinfective at least 12 days after encystment(Table 1). In Anas sp. and G. g. domesticus theadults grew until 21 d.p.i. reaching a similar size inboth hosts. Specimens obtained from Anas sp. at21 d.p.i. were nearly 25% larger than thoseobtained at 14 d.p.i. (Table 2).

Discussion

The taxonomy of the notocotylids is based on thenumber and arrangement of the ventral glands(Dubois, 1951). Species with up to 10 medialglands are: N. gibbus (Mehlis in Creplin, 1846)Kossack, 1911 from Fulica atra in Europe andGallinula chloropus and F. leucoptera from south-ern South America (Szidat & Szidat, 1961);N. pacifera (Noble, 1933) Harwood, 1939 fromF. americana and F. atra in North America andEurope (Szidat & Szidat, 1933; Harwood, 1939);N. porzanaeHarwood, 1939 from Porzana carolinain North America (Harwood, 1939); N. regisHarwood, 1939 from Rallus elegans in NorthAmerica and Europe (Harwood, 1939); N. skrja-

bini Ablasov, 1953 from Anas platyrhynchos andIxobrychos minutus in Asia (Yamaguti, 1971,1975); N. breviserialis (Stunkard, 1967) fromA. platyrhynchos, A. bahamensis, Amazonetta bra-siliensis and Gallus gallus in South America(Muniz-Pereira & Amato, 1995); N. schmidtiBrooks & Heard, 1977 from Rallus longirostris inNorth America (Brooks & Heard, 1977); andN. gallinulae El-Naffar & Khalifa, 1983 fromG. chloropus chloropus in Africa (El-Naffar &Khalifa, 1983). Following Odening (1966),N. gibbus, as described by Kossak (1911), isconsidered a species inquirenda. Odening statedthat it was impossible to find specimens with 6-8ventral glands in each row in the Palaeartic region.

N. biomphalariae n. sp. differs in the number ofmedial and lateral ventral glands (11-4-11) fromN. skrjabini (5-5-5), N. breviserialis (4-5-4) andN. schmidti (4-3-4). It also has a greater egg size (22–26 · 12–14 lm) thanN. skrjabini (21–24 · 13 lm),N. breviserialis (18–22 · 11–13 lm) andN. schmidti(20–23 · 11–14 lm). It also differs fromN. brevise-rialis and N. schmidti in the absence of tegumentalspines. The position of the genital pore is similar(posterior to intestinal bifurcation) to N. skrjabiniandN. schmidti, but it is closely posterior to the oralsucker inN. breviserialis (see Beverly-Burton, 1958;Brooks &Heard lll, 1977; Muniz-Pereira & Amato,1995; Yamaguti, 1971, 1975).

N. biomphalariae is similar in the number oflateral glands (10-11) to N. pacifera, N. regis,N. porzanae and N. gallinulae but differs in thesmaller (4) number of medial glands from N. regis(8-10), N. gallinulae (8), N. porzanae (6) andN. pacifera (4-5), and in the absence of tegumentalspines (Harwood, 1939; Larios, 1943; Lumsden &Zischke, 1963; El-Naffar & Khalifa, 1983),although Odening (1966) observed the presenceof small scales (‘‘kleine SchUppchen’’) in anexperimental immature specimen from N. pacifera.

N. biomphalariae differs in the relationshipbetween the length of the previtelline region andbody length (46%) fromN. regis (34%),N. porzanae(33%), N. gallinulae (54%) and N. pacifera (50–57%). The new species also differs in the number ofthe previtelline uterine coils (2–4) fromN. gallinulae(5–8), N. pacifera (5) and N. porzanae (0), and issimilar to N. regis (3–4). The relationship betweenmetraterm and cirrus-sac length inN. biomphalariae(70%) is similar to N. regis (68%), N. gallinulae(66%) and N. pacifera (70%), but differs from N.

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porzanae (90%). Furthermore, N. biomphalariaehas larger eggs (22-26 lm) than N. gallinulae(22 lm), N. pacifera (21 lm) and N. porzanae(20 lm), but similar to those of N. regis (24 lm)(Dubois, 1951; El-Naffar & Khalifa, 1983; Har-wood, 1939; Larios, 1943; Lumsden & Zischke,1963; Odening, 1966).

N. biomphalariae is similar to the examinedspecimen of N. gibbus, obtained by Szidat & Szidat(1961) from F. leucoptera on the Quequen River, inthe number of ventral glands (10-4-10), according tothe description given by the authors, and in egg-size(24 · 12 lm). However, this specimen differs in thenumber of previtelline uterine coils (6), in the greaterrelationship between the length of the previtellineregion and body length (52%), in the smallerrelationhisp between the lengths of the metratermand cirrus-sac (52%), in the ratio between testicularand ovarian length (1:2), and in the smooth marginof the testes. In view of these characteristics, weconsider the latter specimen as not belonging to thenew species. Odening (1966) stated for N. gibbusthree rows with 6-8 ventral glands, suggesting thatN. gibbus could be synonymous with N. pacifera.The specimen from F. leucoptera of Szidat & Szidat(1961) belongs neither to N. gibbus, in view ofthe number and distribution of the ventral glands(10-4-10), nor to N. pacifera, considering egg-sizeand the ratio between metraterm and cirrus-saclength.

The larval stages of N. biomphalariae differsfrom other Notocotylus species in using a differentsnail as its first intermediate host (Biomphalariaperegrina), e.g. N. pacifera utilises Physa fontinalisand N. regis parasitises Planorbis planorbis. Thenew species also differs in the size of the rediae(643–1,248 lm) from N. regis (1,468–1,918 lm)(Odening, 1966). The cercariae of N. biomphalariaediffers in body size (346–394 · 154–221 lm) fromN. regis (447–499 · 294–308 lm) and fromN. pacifera (240 · 118 lm) (Odening, 1966). Fur-thermore, the new cercaria does not exhibit ante-rior sensory structures, as in N. pacifera andN. regis (see Odening, 1966). The diameter of themetacercarial cyst (146–158 lm) of N. biomphala-riae differs from that of N. regis (191-206 lm) andN. pacifera (183–186 lm) (Odening, 1966). On theother hand, comparing the cercaria of N. biomp-halariae with that of other monostome cercariae inB. peregrina, it differs from the cercaria ofHippocrepis fuelleborni (233-250 · 116 lm) and

from the other monostome cercaria listed above(513 · 250 lm) in body size (Morris, 1978;Ostrowski de Nunez, 1976).

Notocotylus spp. with up to 10 median ventralglands utilise mainly birds of the families Rallidae(Gruiformes), Anatidae (Anseriformes) andArdeidae (Ardeiformes) as definitive hosts. InPatagonia, all of these families are present andcan be found inhabiting the localities studied(Canevari et al., 1991), so they represent possiblehosts for the new species.

Differences in the number and distribution ofventral glands, the ratio between the length of theprevitelline region and body length, the number ofthe previtelline uterine coils, the ratio betweenmetraterm and cirrus-sac length, egg-size, charac-teristics of the larval stages and the geographicaldistribution enable us to distinguish N. biomphala-riae as a new species. This constitutes the first recordof a digenean in B. peregrina from Patagonia.

Acknowledgements

We are grateful to F. Tricarico of the MuseoArgentino de Ciencias Naturales BernardinoRivadavia for lending the specimen of N. gibbus(MACN-Pa 42). Financial support was providedby the Universidad Nacional del Comahue B –115 and to CONICET PIP – 02752.

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