Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Hamann, Monika I.; Kehr, Arturo I.; González, Cynthya E.; Duré, Marta I.; Schaefer, Eduardo F. PARASITE AND REPRODUCTIVE FEATURES OF nasicus (Anura: ) FROM A SOUTH AMERICAN SUBTROPICAL AREA Interciencia, vol. 34, núm. 3, marzo, 2009, pp. 214-218 Asociación Interciencia Caracas, Venezuela

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative PARASITE AND REPRODUCTIVE FEATURES OF Scinax nasicus (Anura: Hylidae) FROM A SOUTH AMERICAN SUBTROPICAL AREA

Monika I. Hamann, Arturo I. Kehr, Cynthya E. González, Marta I. Duré and Eduardo F. Schaefer

SUMMARY

From February 2002 to December 2004, the helminth parasite est prevalence (41%). The definitive hosts of these larval trema- fauna and reproductive features of the Scinax nasicus were todes are probably snakes; S. nasicus acts as second intermedi- studied from Corrientes city, Province of Corrientes, Argenti- ate host, and become infected by direct penetration of cercariae. na. The parasite richness was 15 species of helminths (larval The number of mature ova per female ranged from 413 to 3922, and adult) including trematodes (73%), nematodes (20%) and and the mean mature ovum diameter was 0.76 ±0.17mm. This acanthocephalans (7%). Opisthogonimus sp. showed the high- species has a prolonged reproductive pattern.

PARÁSITOS DE Scinax nasicus (Anura: Hylidae) DE UN ÁREA SUBTROPICAL DE AMÉRICA DEL SUR Y SUS RASGOS REPRODUCTIVOS Monika I. Hamann, Arturo I. Kehr, Cynthya E. González, Marta I. Duré y Eduardo F. Schaefer RESUMEN

Desde febrero de 2002 a diciembre de 2004, se analizó la fau- Los hospedadores definitivos de esta metacercaria son probable- na de helmintos parásitos y las características reproductivas de mente las serpientes. Scinax nasicus, interviene como segundo Scinax nasicus en un área cercana a la ciudad de Corrientes, Ar- hospedador intermediario, infectándose por la penetración directa gentina. La fauna de parásitos helmintos estuvo conformada por de cercarias. El número de óvulos maduros por hembra (comple- 15 especies de helmintos (larvas y adultos) incluyendo trematodes mento ovárico) osciló entre 413-3922, mientras que el diámetro (73%), nematodes (20%) y acantocéfalos (7%). La especie Opis- medio de los óvulos fue de 0,76 ±0,17mm. Esta especie posee un thogonimus sp. presentó la mayor prevalencia (41%) de infección. patrón reproductivo prolongado.

Introduction Santa Cruz, Tarija), and south- occurs in , shrublands S. nasicus from north-western western Brazil to Rio Grande and , and is very Argentina have been analyzed The genus Scinax is dis- do Sul State, being found up well adapted to anthropogen- by Perotti (1995) and Prado tributed from eastern and to 1000masl (Lavilla et al., ic areas (Duré 1999, 2004, et al. (2005) from populations nouthern Mexico to Argen- 2000, Frost, 2007). Schaefer, 2007). living at least 800km away tina and Uruguay, as well as In the province of Cor- The presence of the nema- from the present work study in Trinidad and Tobago, and rientes, Argentina, S. nasi- tode genus Gyrinicola (Phar- area. However, integrated stud- St. Lucia (Frost, 2007). Sci- cus is very abundant, and yngodonidae) in tadpoles of ies are necessary for a better nax nasicus can be found in its conservation status is S. nasicus was recorded by understanding of the ecology Paraguay, Northern Argentina “not threatened” (equivalent González and Hamann (2005) of this species. Studies carried (provinces of Corrientes, Cór- to “Least Concern for Red for the Corrientes’ populations. out without basic information doba, Chaco, Formosa, Entre List Category”) according to The parasitic fauna of this on the natural history of this Ríos, Jujuy, Salta, Santa Fe, Lavilla et al. (2000). In con- frog, which consists mainly particular frog run the risk of Santiago del Estero, Tucumán, trast, Uruguayan populations of nematodes, has also been producing irrelevant results. In Misiones and Buenos Aires), are listed as “threatened” by studied to some extent by fact, conceptually-based ques- Uruguay (Artigas, Paysandú, Maneyro and Langone (2001). Baker and Vaucher (1984) in tions must be asked within Río Negro and Salto), eastern This species of Scinax lives in Paraguayan populations. Some the framework of the ecology Bolivia (Beni, Chuquisaca, sympatry with S. acuminatus, reproductive characteristics of of the individual species if

KEYWORDS / Argentina / Ecology / Helminths Parasites / Reproduction / Received: 10/06/2008. Modified: 03/03/2009. Accepted: 03/04/2009

Monika I. Hamann. Doctor in gaciones Científicas y Técnicas Cynthya E. González. Biologist, CONICET, Argentina. e-mail: Natural Sciences, Universidad (CONICET), C.C.291; (3400) Universidad Nacional del Nor- [email protected] Nacional de La Plata (UNLP), Corrientes, Argentina. e-mail: deste, Argentina. Researcher, Eduardo F. Schaefer. Doctor in Argentina. Researcher, Centro [email protected] CECOAL-CONICET, Argenti- Natural Sciences, UNLP, Ar- de Ecología Aplicada del Li- Arturo I. Kehr. Doctor in Natu- na. e-mail: cynthyaelizabethg@ gentina. Researcher, CECOAL- toral (CECOAL-CONICET), ral Sciences, UNLP, Argen- hotmail.com CONICET, Argentina. e-mail: Argentina. Address: Centro de tina. Researcher, CECOAL- Marta I. Duré. Doctor in Natu- [email protected] Ecología Aplicada del Litoral CONICET, Argentina. e-mail: ral Sciences, UNLP, Argen- (CECOAL), Consejo de Investi- [email protected] tina. Researcher, CECOAL-

214 0378-1844/09/03/214-05 $ 3.00/0 MAR 2009, VOL. 34 Nº 3 PARASITOS DE Scinax nasicus (Anura: Hylidae) DE UMA ÁREA SUBTROPICAL SUL AMERICANA E SEUS RASGOS REPRODUTIVOS Monika I. Hamann, Arturo I. Kehr, Cynthya E. González, Marta I. Duré e Eduardo F. Schaefer RESUMO

Desde fevereiro de 2002 a dezembro de 2004, se analisou a infecção. Os hospedadores definitivos desta metacercária são fauna de helmintos parasitos e as características reprodutivas provavelmente as serpentes. Scinax nasicus, intervem como se- de Scinax nasicus em uma área perto da cidade de Corrientes, gundo hospedador intermediario, infectando-se pela penetração Argentina. A fauna de parasitos helmintos esteve conformada direta de cercarias. O número de óvulos maduros por fêmea por 15 espécies de helmintos (larvas e adultos) incluindo trema- (complemento ovárico) oscilou entre 413-3922, enquanto que o todes (73%), nematodes (20%) e acantocéfalos (7%). A espécie diâmetro médio dos óvulos foi de 0,76 ±0,17mm. Esta espécie Opisthogonimus sp. apresentou a maior prevalência (41%) de possui um padrão reprodutivo prolongado.

they are to be examined and Parasite study non index (H’; Shannon and remove excess liquid, using interpreted correctly (Greene, Weaver 1949) using decimal an electronic balance to the 1986, Vitt et al., 2002). for the parasite study logarithms. The chi-square nearest 0.01g. Ova maturity The main goals of this (21 females and 28 males) test, with Yates correction was determined by the degree study of a northeastern Argen- were caught from March 2003 for continuity, was used for of pigmentation (Basso 1990, tinian population of S. nasicus to December 2004. Speci- comparing the sex ratio of Perotti 1994, 1997). Once the were 1) to determine the num- mens were transported to the frogs. A 2×2 contingency ovarian complement for each ber of helminth taxa infecting the laboratory, placed in a table was used for compar- female had been calculated, this frog under natural condi- chloroform (CHCL3) solution ing the infection between the 100 mature ova were separat- tions, and 2) to analyze the and their snout-vent length sexes. ed randomly and measured for reproductive characteristics (SVL) measured, and then obtaining the mean diameter (number and diameter of ma- weighed. At necropsy, hosts Reproductive study and the standard deviation. ture ova, reproductive effort). were sexed and the alimentary Reproductive effort (RE) was canal, lungs, liver and gall Frogs for the reproductive measured as the percentage Materials and Methods bladder, kidneys, body cav- study (13 gravid females and of ovary mass relative to net ity, musculature, integument 12 males) were caught from body mass (Prado et al., 2000, The study area was estab- and brain were examined February 2002 to April 2004. Prado and Hadad, 2005). lished within a maximum for parasites by dissection. The specimens were placed distance of approximately Helminths were observed in in chloroform (CHCL3) solu- Results 40km towards the east and vivo, counted and killed in hot tion, fixed in 10% formalin south of the city of Corri- distilled water and fixed in and deposited in the Centro Parasite study entes (27º30’S, 58º45’W) and 70% ethyl alcohol. Digeneans de Ecología Aplicada del Li- the Paraná River established and acanthocephalans were toral (CECOAL-CONICET) Out of a total of 48 individ- its western and northern stained with hydrochloric car- collection. The morphometric uals analyzed, 37 (76%) were limit. As in Schaefer et al. mine, cleared in creosota and variables considered for both found infected with helminths. (2006), adults of S. nasicus mounted in Canada balsam. sexes were body length (SV- There was no significant dif- 2 were hand-captured prefer- Nematodes were cleared in Lmm) and body mass (BMg). ference (χ -Yates correction entially between 19:00 and glycerin or lactofenol and ex- For females the net body for continuity= 0.19; df = 1; 24:00, using the sampling amined as temporary mounts. mass (total body mass - ovary P>0.05)in the number of in- technique defined as visual The systematic determination mass) was used. The repro- fected females (17) and males encounters survey (Crump of the helminths was carried ductive variables analyzed for (20). and Scott, 1994). The study out following the guidelines each individual were gonad The component community area is distinguished by its given by Yamaguti (1961, mass (GMg= ovary mass for consisted of 15 helminth taxa large diversity of , 1963, 1971, 1975), Anderson females and testes mass for (larvae and adults), including containing numerous tem- et al. (1974), Baker (1987), males), total mature ova count trematodes (73%), nematodes porary, semi-permanent and Anderson (2000), Gibson et number per female (ovarian (20%) and acanthocephalans permanent ponds, with her- al. (2002), and Jones et al. complement= OC), mature ova (7%). Helminth species di- baceous strata composed of (2005). The infection preva- diameter (ODmm), reproduc- versity (H’= 0.83) and even- gramineous species, cacti and lence, intensity and abundance tive effort (RE), mature ova ness (J’= 0.70) were high. At terrestrial bromeliads, where were calculated for helminth coloration and testes color- the infracommunity level the the is the dominant species according to Bush et ation and form. All variables mean helminth intensity was vegetation. In the present al. (1997). Species richness were registered on individuals 1.48 ±2.56 (maximum= 110) study, all the regulations and is the number of helminth fixed in formaldehyde (10%). worms per frog. Mean helm- ethical and legal consider- species, and mean helminth Body length and ova diam- inth species richness was 2.47 ations for the capture and species richness is the sum eter were determined to the ±1.31 (maximum= 6) species use of established by of helminth species, per in- nearest 0.1mm with a caliper. per infected frog. Multiple in- the Centro de Ecología Apli- dividual frog, divided by the Body, ovary and testes masses fections were common, with 1, cada del Litoral (CECOAL- total number of infected in- were measured in the labora- 2, 3, 4, 5 and 6 species simul- CONICET), Argentina, have dividuals. The diversity was tory after the individuals and taneously present in 9, 15, 6, been followed. calculated with the Shan- gonads were blotted dry to 4, 3, and 1 frogs, respectively.

MAR 2009, VOL. 34 Nº 3 215 Larval digeneans dominated human buildings. Tadpoles Discussion Muzzall et al., 2001; Bolek numerically and taxonomically were observed in different and Coggins, 2003; Hamann the helminth infracommunity, developmental stage and con- Parasite ecology et al., 2006a, b) suggest that with prevalence ranging from tinuously throughout most of numerous vacant niches ex- 41% for Opisthogonimus sp. the year in temporary, semi- Previous studies of amphib- ist within these hosts. The (located in body cavity, liver, permanent and permanent ian helminth infracommunities analysis presented here has muscle and pharyngeal zone) ponds. (McAlpine and Burt, 1998; shown that S. nasicus has ac- to a low of 2% for unknown echinostomatid species (lo- TABLE I cated in kidney) and Aphar- INFECTION PARAMETERS, STAGE AND MICROHABITAT OF HELMINTH SPECIES ingostrigea sp. (located in PARASITIZING Scinax nasicus FROM CORRIENTES, ARGENTINA body cavity). The cistacanth (Centrorhynchus sp.) found in Helminths # % Mean MI Stage Micro- the liver and in the mesentery abundance (range) in frog ** presented an infection preva- Trematoda lence >15%, whereas adult Bursotrema tetracotyloides 265 20 5.40 ±18.80 26.50 (1-110) Metacerc. K trematodes and nematodes CECOAL 03120202 located in the intestinal tract Unknown diplostomid species 21 8 0.42 ±1.62 5.25 (3-9) Mesocerc. K presented infection prevalences CECOAL 04121322 <15% (Table I). Travtrema aff. stenocotyle 190 30 3.87 ±15.09 12.66 (1-101) Metacerc. B-P-Mu CECOAL 04012008 Reproductive study Styphlodora sp. 23 16 0.46 ±1.67 2.87 (1-10) Metacerc. K-Mu-L CECOAL 04012003 Meristics and reproductive Lophosyciadiplostomun aff. nephrocystis 14 6 0.28 ±1.39 4.66 (1-9) Metacerc. K CECOAL 04050347 data of males and females are Apharingostrigea sp. 1 2 0.02 ±0.14 1 Metacerc. B summarized in Table II. For CECOAL 04121324 females, significant correla- Opisthogonimus sp. 226 41 4.61 ±13.26 11.30 (1-69) Metacerc. B-Mu-P-L tions were found between SVL CECOAL 04092904 and the variables OC (rs = Unknown echinostomatid species #1 78 24 1.59 ±4.28 6.50 (1-22) Metacerc. K-B-P 0.54, P=0.05, n=13), GM(ovary CECOAL 04012014 mass) (rs= 0.75, P=0.003, n=13), Unknown echinostomatid species #2 1 2 0.02 ±0.14 1 Metacerc. K RE (rs= 0.64, P=0.03, n=13), CECOAL 04121318 and OD (rs= 0.71, P=0.006, Catadiscus inopinatus 7 10 0.14 ±0.45 1.40 (1-2) Adult Li n=13). The BM(net body mass) of CECOAL 04121330 females was significantly cor- Glypthelmins sp. 2 2 0.04 ±0.28 2 Adult Si related with OC (rs = 0.85, CECOAL 04092904 P=0.0003, n=13), GM(ovary mass) Nematoda (rs= 0.89, P=0.0001, n=13), Oxyascaris caudacutus 1 2 0.02 ±0.14 1 Adult Si RE (rs= 0.76, P=0.003, n=13) CECOAL 03120202 and OD (rs = 0.57, P= 0.04, Cosmocerca parva 1 2 0.02 ±0.14 1 Adult Li n=13). CECOAL 04121316 No significant sexual di- Unknown rhabdochonid species 10 6 0.20 ±0.91 3.33 (1-5) Larvae S morphisms were observed for CECOAL 04101102 SVL (Mann-Whitney U-Test= Acanthocephala 0.30, P=0.57; n = 12, n = ♂ ♀ Centrorhynchus sp. 91 16 1.85 ±7.15 1.37 (1-44) Cystacanth. L-Me-S 13); and BM (Mann-Whitney CECOAL 04092904 U-Test= 0.15, P= 0.99, n = ♂ #: number of parasites, %: prevalence. 12, n♀= 13). ** Site of infection is K: kidneys, B: body cavity, P: pharyngeal zone, Si: small intestine, Li: large intestine, S: serous The coloration of each layer of the stomach, Mu: muscle, and Me: mesenteries. L: liver. ovum was 50% dark brown and 50% white, with the ani- TABLE II mal and vegetable poles well MEAN ±1 SD OF REPRODUCTIVE AND MORPHOLOGICAL VARIABLES FOR FEMALES differentiated. The color of AND MALES OF Scinax nasicus FROM CORRIENTES, ARGENTINA the oval shaped testes was white. For their reproduction, Variables Females Males the adults showed preference SVLmm 29.94 ±1.97 (27.20-33.30; 6.60%; 13) 30.07 ±1.44 (27.50-32.15; 4.78%; 12) for flooded vegetation near BM 2.59 ±0.70 (1.67-4.14; 26.00%; 13) 2.56 ±0.66 (1.54-3.84; 25.64%; 12) the shore or inside temporary, g OC 1628.54 ±1019.52 (413-3922;62.60%; 13) __ semi-permanent and perma- nent ponds, as well as for GMg (ovary/testes) 0.54 ±0.32 (0.11-1.13; 59.94%; 13) <0.01 (12) flooded high grass (normally RE% 19.47 ±9.25 (6.59-33.24; 47.49%; 13) ND no more than 2m in height). ODmm 0.76 ±0.17 (0.43-1.07; 22.15%; 1800mature ova) __ It is interesting to remark that SVL: body length, BM: net body mass for females, OC: total mature ova count number per female, GM: ovary or in the present study area, S. testes mass, RE: percentage of gonad mass relative to net body mass= GM/net body mass (specified only for females), nasicus is the most common OD: ova diameter. In parenthesis: minimum-maximum; mean variation coefficient (expressed as percentage); sample anuran species that inhabits size. ND: not determined.

216 MAR 2009, VOL. 34 Nº 3 quired a great richness (15 2002), may be regulating the male reproductive effort (18.00 Basso NG (1990) Estrategias ad- species) of helminths (larval stability of this host-parasite ±8.92%) that we observed aptativas en una comunidad subtropical de anuros. Cuad. and adult), with a maximum system. was lower than observed by Herpetol. Ser. Monog.1: 1-72. of six species per frog and Perotti (1994, 1995). These Bolek MG, Coggins JR (2003) high values of diversity and Reproductive ecology differences could be simply Helminth community structure evenness, but no core species due to peculiarities of two of sympatric eastern Ameri- (<50% of infections). Adult Reproductive activity (gravid populations that inhabit totally can toad, Bufo americanus, helminths were very low in females and calling males) different environments, the northern Leopard frog, Rana pipiens, and Blue-spotted sala- number in the digestive tracts, in S. nasicus occurs for most season in which samples were mander, Ambystoma laterale, but larval trematodes were the of the year except in June collected or even the great from southeastern Wisconsin. primary members of this am- and July, the winter months variability normally presented J. Parasitol. 89: 673-680. phibian’s helminth infracom- with the lowest temperatures, by S. nasicus. Males and fe- Bush AO, Lafferty KD, Lotz JM, munity. These results indicate thus establishing S. nasicus males did not present signifi- Shostak AW (1997) Parasitol- that S. nasicus is infected by as a prolonged breeder (Wells, cant differences for SVL and ogy meets ecology on its own direct penetration of cercariae 1977). Prado et al. (2005) how- BM. Females with higher SVL terms: Margolis et al. revisited. J. Parasitol. 83: 575-583. in the tadpole stage or when ever, suggest for populations of and net BM had significantly entering the water for a short higher values of GM , Crump ML, Scott NJJr (1994) Vi- this species in El Pantanal, ovary mass sual encounters surveys. In period to breed, and it acts Brazil, that S. nasicus has an OC, RE and OD, probably Heyer WR, Donnelly MA, as intermediate hosts of these explosive reproductive pattern. due to the presence of breed- McDiarmid RW, Hayek LC, parasites. Perotti´s (1995) observations in ing females of different ages Foster MS (Eds.) Measuring S. nasicus occupies an in- Salta, Argentina, on the other or that females that were able and Monitoring Biological Di- versity - Standard Methods termediate position in the hand, are consistent with the to feed better before the re- for . Smithsonian food web, being a prey only present study since this author productive season had better Institution Press. Washington for terrestrial animals. In this also classified the species as a conditions for increased egg DC, EEUU. pp. 84-91. respect, possibly the definitive prolonged breeder. production. These are only, Duellman WE, Trueb L (1986) hosts of these larval trema- For the reproductive mode, for the moment, hypotheses Biology of the Amphibians. todes are mammals (Burso- Perotti (1994) and Prado et al. that require further research McGraw Hill. New York, NY, trema tetracotyloides) and (2005) classified this species to be tested. USA. 670 pp. snakes (Travtrema aff. steno- as Mode 1 according to Du- Duré MI (1999) Interrelaciones en los nichos tróficos de dos cotyle and Styphlodora sp.). ellman and Trueb (1986), con- Acknowledgements especies sintópicas de la fa- On the other hand, host feed- sisting in eggs and exotrophic milia Hylidae (Anura) en un ing habitats were an impor- tadpoles in lentic water. We This research was partially área subtropical de Argentina. tant factor in determining the also use mode 6, proposed by supported by Consejo Nacio- Cuad. Herpetol. 13: 11-18. adult helminth faunal compo- Lavilla and Rougés (1992), nal de Investigaciones Cientí- Duré MI (2004) Estructura Trófica sition in S. nasicus. Thus, the which is more precise accord- ficas y Técnicas (CONICET), y Aspectos Ecológicos de los Argentina, through grants Gremios de una Comunidad lower prevalence of infection ing to our observations and de Anfibios de la Provincia de and poorer species richness implies eggs laid in a spheri- PIP 2945 and 2766 to M.I. Corrientes. Tesis. Universidad of adult digeneans suggest cal jellied mass that adheres Hamann and A.I. Kehr, re- Nacional de La Plata. Buenos that intermediate hosts of this to submerged objects. The spectively. The authors have Aires, Argentina. 210 pp. helminth may not be an im- embryonic and tadpole de- complied with all applica- Esch GW, Barger MA, Fellis KJ portant item in this amphib- velopment occur in the same ble institutional care (2002) The transmission of ian’s diet. The relative high water body in which the eggs guidelines, and all required digenetic trematodes: style, elegance, complexity. Integr. intensity of infection found for are laid. state and federal permits have Comp. Biol. 42: 304-312. cystascanth (Centrorhynchus Of 27 species (5 Bufonidae; been obtained. Frost D (2007) Species sp.) may be explained by the 1 Cycloramphidae; 6 Lepto- of the World: an Online Refer- predominant coleopterans in dactylidae; 4 Leiuperidae; 10 References ence. Version 5.0 American the alimentary items of S. na- Hylidae and 1 Microhylidae) Museum of Natural History, sicus (Duré, 1999, 2004). The studied in the area (Schaefer, Anderson RC (2000) Nematode New York, NY, USA. http:// life cycle of Centrorhynchus 2007) females of S. nasicus Parasites of Vertebrates: Their research.amnh.org/ herpetol- Development and Transmis- ogy/amphibia/index.php (Cons. sp. depends on terrestrial in- are those presenting bigger sion. 2nd ed. CABI. Walling- Febr. 2007). termediates (e.g., coleopter- values of reproductive effort ford, UK. 650 pp. Gibson DI, Jones A, Bray RA ans). 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