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Parasite and reproductive features of Scinax nasicus (Anura: Hylidae) from a South American subtropical area/Parasitos de Scinax nasicus (Anura: Hylidae) de un area subtropical de Americana del sur y sus rasgos reprodutivos/Parasitos de Scinax nasicus (Anura: Hylidae) de uma area subtropical sul Americana e seus rasgos produtivos.

SUMMARY

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

RESUMEN

Desde febrero de 2002 a diciembre de 2004, se analizo la fauna de helmintos parasitos y las caracteristicas reproductivas de Scinax nasicus en un area cercana a la ciudad de Corrientes, Argentina. La fauna de parasitos helmintos estuvo conformada por 15 especies de helmintos (larvas y adultos) incluyendo trematodes (73%), nematodes (20%) y acantocefalos (7%). La especie Opisthogonimus sp. presento la mayor prevalencia (41%) de infeccion. Los hospedadores definitivos de esta metacercaria son probablemente las serpientes. Scinax nasicus, interviene como segundo hospedador intermediario, infectandose por la penetracion directa de cercarias. El numero de ovulos maduros por hembra (complemento ovarico) oscilo entre 413-3922, mientras que el diametro medio de los ovulos fue de 0,76 [+ o -] 0,17mm. Esta especie posee un patron reproductivo prolongado.

RESUMO

Desde fevereiro de 2002 a dezembro de 2004, se analisou a fauna de helmintos parasitos e as caracteristicas reprodutivas de Scinax nasicus em uma area perto da cidade de Corrientes, Argentina. A fauna de parasitos helmintos esteve conformada por 15 especies de helmintos (larvas e adultos) incluindo trematodes (73%), nematodes (20%) e acantocefalos (7%). A especie Opisthogonimus sp. apresentou a maior prevalencia (41%) de infeccao. Os hospedadores definitivos desta metacercaria sao provavelmente as serpentes. Scinax nasicus, intervem como segundo hospedador intermediario, infectando-se pela penetracao direta de cercarias. O numero de ovulos maduros por femea (complemento ovarico) oscilou entre 413-3922, enquanto que o diametro medio dos ovulos foi de 0,76 [+ ou -] 0,17mm. Esta especie possui um padrao reprodutivo prolongado.

KEYWORDS / Argentina / Ecology / Helminths Parasites / Reproduction /

Introduction

The genus Scinax is distributed from eastern and northern Mexico to Argentina and Uruguay, as well as in Trinidad and Tobago, and St. Lucia (Frost, 2007). Scinax nasicus can be found in Paraguay, Northern Argentina (provinces of Corrientes, Cordoba, Chaco, Formosa, Entre Rios, Jujuy, Salta, Santa Fe, Santiago del Estero, Tucuman, Misiones and Buenos Aires), Uruguay (Artigas, Paysandu, Rio Negro and Salto), eastern Bolivia (Beni, Chuquisaca, Santa Cruz, Tarija), and south-western Brazil to Rio Grande do Sul State, being found up to 1000masl (Lavilla et al., 2000, Frost, 2007).

In the province of Corrientes, Argentina, S. nasicus is very abundant, and its conservation status is "not threatened" (equivalent to "Least Concern for Red List Category") according to Lavilla et al. (2000). In contrast, Uruguayan populations are listed as "threatened" by Maneyro and Langone (2001). This species of Scinax lives in sympatry with S. acuminatus, occurs in forests, shrublands and grasslands, and is very well adapted to anthropogenic areas (Dure 1999, 2004, Schaefer, 2007).

The presence of the nematode genus Gyrinicola (Pharyngodonidae) in tadpoles of S. nasicus was recorded by Gonzalez and Hamann (2005) for the Corrientes' populations. The parasitic fauna of this frog, which consists mainly of nematodes, has also been studied to some extent by Baker and Vaucher (1984) in Paraguayan populations. Some reproductive characteristics of S. nasicus from north-western Argentina have been analyzed by Perotti (1995) and Prado et al. (2005) from populations living at least 800km away from the present work study area. However, integrated studies are necessary for a better understanding of the ecology of this species. Studies carried out without basic information on the natural history of this particular frog run the risk of producing irrelevant results. In fact, conceptually-based questions must be asked within the framework of the ecology of the individual species if they are to be examined and interpreted correctly (Greene, 1986, Vitt et al., 2002).

The main goals of this study of a northeastern Argentinian population of S. nasicus were 1) to determine the number of helminth taxa infecting this frog under natural conditions, and 2) to analyze the reproductive characteristics (number and diameter of mature ova, reproductive effort).

Materials anal Methods

The study area was established within a maximum distance of approximately 40km towards the east and south of the city of Corrientes (27[degrees]30'S, 58[degrees]45'W) and the Parana River established its western and northern limit. As in Schaefer et al. (2006), adults of S. nasicus were hand-captured preferentially between 19:00 and 24:00, using the sampling technique defined as visual encounters survey (Crump and Scott, 1994). The study area is distinguished by its large diversity of habitats, containing numerous temporary, semi-permanent and permanent ponds, with herbaceous strata composed of gramineous species, cacti and terrestrial bromeliads, where the forest is the dominant vegetation. In the present study, all the regulations and ethical and legal considerations for the capture and use of animals established by the Centro de Ecologia Aplicada del Litoral (CECOAL-CONICET), Argentina, have been followed.

Parasite study

Frogs for the parasite study (21 females and 28 males) were caught from March 2003 to December 2004. Specimens were transported to the laboratory, placed in a chloroform ([CHCL.sub.3]) solution and their snout-vent length (SVL) measured, and then weighed. At necropsy, hosts were sexed and the alimentary canal, lungs, liver and gall bladder, kidneys, body cavity, musculature, integument and brain were examined for parasites by dissection. Helminths were observed in vivo, counted and killed in hot distilled water and fixed in 70% ethyl alcohol. Digeneans and acanthocephalans were stained with hydrochloric carmine, cleared in creosota and mounted in Canada balsam. Nematodes were cleared in glycerin or lactofenol and examined as temporary mounts. The systematic determination of the helminths was carried out following the guidelines given by Yamaguti (1961, 1963, 1971, 1975), Anderson et al. (1974), Baker (1987), Anderson (2000), Gibson et al. (2002), and Jones et al. (2005). The infection prevalence, intensity and abundance were calculated for helminth species according to Bush et al. (1997). Species richness is the number of helminth species, and mean helminth species richness is the sum of helminth species, per individual frog, divided by the total number of infected individuals. The diversity was calculated with the Shannon index (H'; Shannon and Weaver 1949) using decimal logarithms. The chi-square test, with Yates correction for continuity, was used for comparing the sex ratio of the frogs. A 2x2 contingency table was used for comparing the infection between the sexes.

Reproductive study

Frogs for the reproductive study (13 gravid females and 12 males) were caught from February 2002 to April 2004. The specimens were placed in chloroform ([CHCL.sub.3]) solution, fixed in 10% formalin and deposited in the Centro de Ecologia Aplicada del Litoral (CECOAL-CONICET) collection. The morphometric variables considered for both sexes were body length ([SVL.sub.mm])and body mass ([BM.sub.g]). For females the net body mass (total body mass--ovary mass) was used. The reproductive variables analyzed for each individual were gonad mass ([GM.sub.g]= ovary mass for females and testes mass for males), total mature ova count number per female (ovarian complement= OC), mature ova diameter ([OD.sub.mm]) , reproductive effort (RE), mature ova coloration and testes coloration and form. Ali variables were registered on individuals fixed in formaldehyde (10%). Body length and ova diameter were determined to the nearest 0.1mm with a caliper. Body, ovary and testes masses were measured in the laboratory after the individuals and gonads were blotted dry to remove excess liquid, using an electronic balance to the nearest 0.01g. Ova maturity was determined by the degree of pigmentation (Basso 1990, Perotti 1994, 1997). Once the ovarian complement for each female had been calculated, 100 mature ova were separated randomly and measured for obtaining the mean diameter and the standard deviation. Reproductive effort (RE) was measured as the percentage of ovary mass relative to net body mass (Prado et al., 2000, Prado and Hadad, 2005).

Results

Parasite study

Out of a total of 48 individuals analyzed, 37 (76%) were found infected with helminths. There was no significant difference ([chi square]-Yates correction for continuity= 0.19; df = 1; P>0.05)in the number of infected females (17) and males (20).

The component community consisted of 15 helminth taxa (larvae and adults), including trematodes (73%), nematodes (20%) and acanthocephalans (7%). Helminth species diversity (H'= 0.83) and evenness (J'= 0.70) were high. At the infracommunity level the mean helminth intensity was 1.48 [+ or -] 2.56 (maximum= 110) worms per frog. Mean helminth species richness was 2.47 [+ or -] 1.31 (maximum= 6) species per infected frog. Multiple infections were common, with 1, 2, 3, 4, 5 and 6 species simultaneously present in 9, 15, 6, 4, 3, and 1 frogs, respectively.

Larval digeneans dominated numerically and taxonomically the helminth infracommunity, with prevalence ranging from 41% for Opisthogonimus sp. (located in body cavity, liver, muscle and pharyngeal zone) to a low of 2% for unknown echinostomatid species (located in kidney) and Apharingostrigea sp. (located in body cavity). The cistacanth (Centrorhynchus sp.) found in the liver and in the mesentery presented an infection prevalence >15%, whereas adult trematodes and nematodes located in the intestinal tract presented infection prevalences <15% (Table I).

Reproductive study

Meristics and reproductive data of males and females are summarized in Table II. For females, significant correlations were found between SVL and the variables OC ([r.sub.s]= 0.54, P=0.05, n=13), [GM.sub.(ovary mass)] ([r.sub.s] = 0.75, P=0.003, n=13), RE ([r.sub.s] = 0.64, P=0.03, n=13), and OD (rs= 0.71, P=0.006, n=13). The [BM.sub.(net body mass)] of females was significantly correlated with OC ([r.sub.s]= 0.85, P=0.0003, n=13), [GM.sub.(ovary mass)] ([r.sub.s]= 0.89, P=0.0001, n=13), RE ([r.sub.s]= 0.76, P=0.003, n=13) and OD ([r.sub.s] = 0.57, P=0.04, n=13).

No significant sexual dimorphisms were observed for SVL (Mann-Whitney U-Test= 0.30, P=0.57; n[male]= 12, n[female]= 13); and BM (Mann-Whitney U-Test= 0.15, P= 0.99, n[male]= 12, n[female]= 13).

The coloration of each ovum was 50% dark brown and 50% white, with the animal and vegetable poles well differentiated. The color of the oval shaped testes was white. For their reproduction, the adults showed preference for flooded vegetation near the shore or inside temporary, semi-permanent and permanent ponds, as well as for flooded high grass (normally no more than 2m in height). It is interesting to remark that in the present study area, S. nasicus is the most common anuran species that inhabits human buildings. Tadpoles were observed in different developmental stage and continuously throughout most of the year in temporary, semi-permanent and permanent ponds.

Discussion

Parasite ecology

Previous studies of amphibian helminth infracommunities (McAlpine and Burt, 1998; Muzzall et al., 2001; Bolek and Coggins, 2003; Hamann et al., 2006a, b) suggest that numerous vacant niches exist within these hosts. The analysis presented here has shown that S. nasicus has acquired a great richness (15 species) of helminths (larval and adult), with a maximum of six species per frog and high values of diversity and evenness, but no core species (<50% of infections). Adult helminths were very low in number in the digestive tracts, but larval trematodes were the primary members of this amphibian's helminth infracommunity. These results indicate that S. nasicus is infected by direct penetration of cercariae in the tadpole stage or when entering the water for a short period to breed, and it acts as intermediate hosts of these parasites.

S. nasicus occupies an intermediate position in the food web, being a prey only for terrestrial animals. In this respect, possibly the definitive hosts of these larval trematodes are mammals (Bursotrema tetracotyloides) and snakes (Travtrema aff. stenocotyle and Styphlodora sp.). On the other hand, host feeding habitats were an important factor in determining the adult helminth faunal composition in S. nasicus. Thus, the lower prevalence of infection and poorer species richness of adult digeneans suggest that intermediate hosts of this helminth may not be an important item in this amphibian's diet. The relative high intensity of infection found for cystascanth (Centrorhynchus sp.) may be explained by the predominant coleopterans in the alimentary items of S. nasicus (Dure, 1999, 2004). The life cycle of Centrorhynchus sp. depends on terrestrial intermediates (e.g., coleopterans). The results indicate the importance of local factors associated with aquatics and terrestrial habitat use by the host. Thus, the combination of these factors with the diet, body size, and reproductive behavior of the host (Hamann and Kehr, 1998, 1999a,b, Kehr et al., 2000, Hamann, 2004, 2006, Hamann et al., 2006a,b) and the behavioral ecology of intermediate hosts, in combination with transmission strategies of parasites (Esch et al., 2002), may be regulating the stability of this host-parasite system.

Reproductive ecology

Reproductive activity (gravid females and calling males) in S. nasicus occurs for most of the year except in June and July, the winter months with the lowest temperatures, thus establishing S. nasicus as a prolonged breeder (Wells, 1977). Prado et al. (2005) however, suggest for populations of this species in El Pantanal, Brazil, that S. nasicus has an explosive reproductive pattern. Perotti's (1995) observations in Salta, Argentina, on the other hand, are consistent with the present study since this author also classified the species as a prolonged breeder.

For the reproductive mode, Perotti (1994) and Prado et al. (2005) classified this species as Mode 1 according to Duellman and Trueb (1986), consisting in eggs and exotrophic tadpoles in lentic water. We also use mode 6, proposed by Lavilla and Rouges (1992), which is more precise according to our observations and implies eggs laid in a spherical jellied mass that adheres to submerged objects. The embryonic and tadpole development occur in the same water body in which the eggs are laid.

Of 27 species (5 Bufonidae; 1 Cycloramphidae; 6 Leptodactylidae; 4 Leiuperidae; 10 Hylidae and 1 Microhylidae) studied in the area (Schaefer, 2007) females of S. nasicus are those presenting bigger values of reproductive effort (18.00 [+ or -] 8.92%), being only overcome by females of Pseudopaludicola falcipes (22.83 [+ or -] 11.96%).

Comparing the present results with those obtained by Perotti (1994, 1995) for populations from Salta, in northwest Argentina, the values are similar regarding mean body length, mean body mass, mean ovarian complement and mean ova diameter. However, the mean ovary mass (0.48 [+ or -] 8.92g) and mean female reproductive effort (18.00 [+ or -] 8.92%) that we observed was lower than observed by Perotti (1994, 1995). These differences could be simply due to peculiarities of two populations that inhabit totally different environments, the season in which samples were collected or even the great variability normally presented by S. nasicus. Males and females did not present significant differences for SVL and BM. Females with higher SVL and net BM had significantly higher values of [GM.sub.ovary mass], OC, RE and OD, probably due to the presence of breeding females of different ages or that females that were able to feed better before the reproductive season had better conditions for increased egg production. These are only, for the moment, hypotheses that require further research to be tested.

ACKNOWLEDGEMENTS

This research was partially supported by Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET), Argentina, through grants PIP 2945 and 2766 to M.I. Hamann and A.I. Kehr, respectively. The authors have complied with all applicable institutional animal care guidelines, and all required state and federal permits have been obtained.

Received: 10/06/2008. Modified: 03/03/2009. Accepted: 03/04/2009

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Monika I. Hamann. Doctor in Natural Sciences, Universidad Nacional de La Plata (UNLP), Argentina. Researcher, Centro de Ecologia Aplicada del Litoral (CECOAL-CONICET), Argentina. Address: Centro de Ecologia Aplicada del Litoral (CECOAL), Consejo de Investigaciones Cientificas y Tecnicas (CONICET), C.C.291; (3400) Corrientes, Argentina. e-mail: monika_hamann@yahoo.com

Arturo L Kehr. Doctor in Natural Sciences, UNLP, Argentina. Researcher, CECOAL-CONICET, Argentina. e-mail: arturokehr@yahoo.com.ar

Cynthya E. Gonzalez. Biologist, Universidad Nacional del Nordeste, Argentina. Researcher, CECOAL-CONICET, Argentina. e-mail: cynthyaelizabethg@ hotmail.com

Marta I. Dure. Doctor in Natural Sciences, UNLP, Argentina. Researcher, CECOAL-CONICET, Argentina. e-mail: martadure@yahoo.com

Eduardo F. Schaefer. Doctor in Natural Sciences, UNLP, Argentina. Researcher, CECOAL-CONICET, Argentina. e-mail: eclschaefer247@yahoo.com.ar
TABLE I
INFECTION PARAMETERS, STAGE AND MICROHABITAT OF HELMINTH
SPECIES PARASITIZING Scinax nasicus FROM CORRIENTES, ARGENTINA

Helminths                        #     %           Mean
                                                 abundance
Trematoda
  Bursotrema tetracotyloides    265    20   5.40 [+ or -] 18.80
  CECOAL 03120202
  Unknown diplostomid species    21     8   0.42 [+ or -] 1.62
  CECOAL 04121322
  Travtrema aff. stenocotyle    190    30   3.87 [+ or -] 15.09
  CECOAL 04012008
  Styphlodora sp.                23    16   0.46 [+ or -] 1.67
  CECOAL 04012003
  Lophosyciadiplostomun          14     6   0.28 [+ or -] 1.39
  aff. nephrocystis
  CECOAL 04050347
  Apharingostrigea sp.            1     2   0.02 [+ or -] 0.14
  CECOAL 04121324
  Opisthogonimus sp.            226    41   4.61 [+ or -] 13.26
  CECOAL 04092904
  Unknown echinostomatid         78    24   1.59 [+ or -] 4.28
  species #1
  CECOAL 04012014
  Unknown echinostomatid          1     2   0.02 [+ or -] 0.14
  species #2
  CECOAL 04121318
  Catadiscus inopinatus           7    10   0.14 [+ or -] 0.45
  CECOAL 04121330
  Glypthelmins sp.                2     2   0.04 [+ or -] 0.28
  CECOAL 04092904
Nematoda
  Oxyascaris caudacutus           1     2   0.02 [+ or -] 0.14
  CECOAL 03120202
  Cosmocerca parva                1     2   0.02 [+ or -] 0.14
  CECOAL 04121316
  Unknown rhabdochonid           10     6   0.20 [+ or -] 0.91
  species
  CECOAL 04101102
Acanthocephala
  Centrorhynchus sp.             91    16   1.85 [+ or -] 7.15
  CECOAL 04092904

Helminths                            MI            Stage      Micro-
                                   (range)        in frog     habitat
                                                                 **

Trematoda
  Bursotrema tetracotyloides    26.50 (1-110)   Metacerc.     K
  CECOAL 03120202
  Unknown diplostomid species   5.25 (3-9)      Mesacerc.     K
  CECOAL 04121322
  Travtrema aff. stenocotyle    12.66 (1-101)   Metacerc.     B-P-Mu
  CECOAL 04012008
  Styphlodora sp.               2.87 (1-10)     Metacerc.     K-Mu-L
  CECOAL 04012003
  Lophosyciadiplostomun         4.66 (1-9)      Metacerc.     K
  aff. nephrocystis
  CECOAL 04050347
  Apharingostrigea sp.          1               Metacerc.     B
  CECOAL 04121324
  Opisthogonimus sp.            11.30 (1-69)    Metacerc.     B-Mu-P-L
  CECOAL 04092904
  Unknown echinostomatid        6.50 (1-22)     Metacerc.     K-B-P
  species #1
  CECOAL 04012014
  Unknown echinostomatid        1               Metacerc.     K
  species #2
  CECOAL 04121318
  Catadiscus inopinatus         1.40 (1-2)      Adult         Li
  CECOAL 04121330
  Glypthelmins sp.              2               Adult         Si
  CECOAL 04092904
Nematoda
  Oxyascaris caudacutus         1               Adult         Si
  CECOAL 03120202
  Cosmocerca parva              1               Adult         Li
  CECOAL 04121316
  Unknown rhabdochonid          3.33 (1-5)      Larvae        S
  species
  CECOAL 04101102
Acanthocephala
  Centrorhynchus sp.            1.37 (1-44)     Cystacanth.   L-Me-S
  CECOAL 04092904

#: number of parasites, %: prevalence.
** Site of infection is K: kidneys, B: body cavity, P: pharyngeal
zone, Si: small intestine, Li: large intestine, S: serous layer
of the stomach, Mu: muscle, and Me: mesenteries. L: liver.

TABLE II
MEAN [+ or -] 1 SD OF REPRODUCTIVE AND MORPHOLOGICAL VARIABLES FOR
FEMALES AND MALES OF Scinax nasicus FROM CORRIENTES, ARGENTINA

Variables                  Females                     Males

[SVL.sub.mm]         29.94 [+ or -] 1.97        30.07 [+ or -] 1.44
                   (27.20-33.30; 6.60%; 13)   (27.50-32.15; 4.78%; 12)

[BM.sub.g]            2.59 [+ or -] 0.70         2.56 [+ or -] 0.66
                   (1.67-4.14; 26.00%; 13)    (1.54-3.84; 25.64%; 12)

OC                 1628.54 [+ or -] 1019.52              --
                    (413-3922; 62.60%; 13)

[GM.sub.g             0.54 [+ or -] 0.32             <0.01 (12)
(ovary/testes)     (0.11-1.13; 59.94%; 13)

[RE.sub.%]           19.47 [+ or -] 9.25                 ND
                   (6.59-33.24; 47.49%; 13)

[OD.sub.mm]           0.76 [+ or -] 0.17                 --
                     (0.43-1.07; 22.15%;
                    [1800.sub.mature ova])

SVL: body length, BM: net body mass for females, OC: total mature
ova count number per female, GM: ovary or testes mass, RE:
percentage of gonad mass relative to net body mass= GM-net body
mass (specified only for females), OD: ova diameter. In
parenthesis: minimum-maximum; mean variation coefficient
(expressed as percentage); sample size. ND: not determined.
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Title Annotation:REPORTS/COMUNCACIONES/COMUNICACOES
Author:Hamann, Monika I.; Kehr, Arturo I.; Gonzalez, Cynthya E.; Dure, Marta I.; Schaefer, Eduardo F.
Publication:Interciencia
Date:Mar 1, 2009
Words:4447
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