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Life history aspects of Phalloceros anisophallosLucinda, 2008 (Osteichthyes, Poeciliidae) fromCórrego Andorinha, Ilha Grande (RJ, Brazil)Pedro H. Almeida-Silvaab & Rosana Mazzoniaa Ecology Department, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazilb Instituto Federal do Rio de Janeiro, Volta Redonda, BrazilPublished online: 18 Sep 2014.

To cite this article: Pedro H. Almeida-Silva & Rosana Mazzoni (2014): Life history aspects of Phalloceros anisophallosLucinda, 2008 (Osteichthyes, Poeciliidae) from Córrego Andorinha, Ilha Grande (RJ, Brazil), Studies on Neotropical Fauna andEnvironment, DOI: 10.1080/01650521.2014.957968

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ORIGINAL ARTICLE

Life history aspects of Phalloceros anisophallos Lucinda, 2008 (Osteichthyes, Poeciliidae) fromCórrego Andorinha, Ilha Grande (RJ, Brazil)

Pedro H. Almeida-Silvaa,b* & Rosana Mazzonia

aEcology Department, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil; bInstituto Federal do Rio de Janeiro,Volta Redonda, Brazil

(Received 17 September 2013; accepted 21 August 2014)

Life history traits of Phalloceros anisophallos from Córrego Andorinha, Ilha Grande (RJ, Brazil) were examinedand the following parameters were evaluated: superfetation, matrotrophy, brood size, reproductive season, length–weight relationship, female weight and brood size relationship. Males were smaller and less abundant thanfemales. According to the temporal variation of the gonadosomatic index, reproduction occurred throughoutthe year, with a reduction around April. We did not register superfetation among reproductive females, but therewas significant increase of dry weight of developing embryos, indicating substantial matrotrophy. Such acombination of reproductive features seems to be rare in the family Poeciliidae but common in the genusPhalloceros. More studies on the other species of the genus are necessary to confirm this pattern.

Aspectos da história de vida de Phalloceros anisophallos do Córrego Andorinha, na Ilha Grande (RJ, Brasil)foram estudados, tendo sido avaliados os seguintes parâmetros: superfetação, matrotrofia, tamanho da ninhada,estação reprodutiva, relação peso-comprimento e relação entre peso das fêmeas e tamanho da ninhada. Osmachos foram menores e menos abundantes do que as fêmeas. De acordo com a variação temporal do ÍndiceGonadossomático, a reprodução ocorreu ao longo de todo ano, mas foi reduzida em abril. Não registramossuperfetação entre as fêmeas reprodutivas, mas registramos aumento significativo do peso seco dos embriões aolongo do desenvolvimento, indicando matrotrofia substancial. Tal combinação de características reprodutivasparece ser rara na família Poeciliidae, mas comum no gênero Phalloceros. Mais estudos sobre as demais espéciesdo gênero são necessários para confirmar esse padrão.

Keywords: Brazil; matrotrophy; superfetation; sexual dimorphism; continuous reproduction; coastal streams

Introduction

Most Actinopterygii and Teleostei are oviparous;however, among the 200 known species ofPoeciliidae (subfamily Poeciliinae; Parenti 1981) onlyTomeurus gracilis Eigenmann, 1909 is not live-bearing(Rosen & Bailey 1963; Lucinda & Reis 2005; Hrbeket al. 2007). Species of Poeciliidae have several adap-tations related to reproduction, mainly internal ferti-lization and different degrees of viviparity associatedwith matrotrophy and superfetation (Thibault &Schultz 1978).

Superfetation is the presence of multiple broodsof young at different developmental stages in asingle female (Turner 1947; Arias & Reznick2000). This phenomenon is widespread within thefamily Poeciliidae and has been observed in otherTeleostei families such as the Clinidae andZenarchopteridae (Pollux et al. 2009). In lecithotro-phy, eggs already contain all the necessary nutrientsbefore fertilization (Reznick et al. 1992). Thisimplies that all the nutrients come from the yolk,

and only some inorganic ions and dissolved gasesare exchanged between maternal circulation and theembryo (Pough et al. 1993). On the other hand, inmatrotrophy, the supply of nutrients to embryos ismaintained even after fertilization (Reznick et al.1992), thus during embryo development. Someauthors consider only matrotrophy as a real caseof viviparity, and interpret lecithotrophy as ovovi-viparity (Scrimshaw 1945; Pough et al. 1993). Thereis a close association between superfetation andmatrotrophy, which suggests that the origin of oneof these traits may facilitate the evolution of theother (Pollux et al. 2009), but Thibault and Schultz(1978) had already shown that these traits are notalways combined, as in Poeciliopsis monacha Miller,1960 which has superfetation but lacksmatrotrophy.

According to Marsh-Matthews (2011), in manyspecies thought to be strictly lecithotrophic, there issupply of organic nutrients from the mother, butembryo mass decreases significantly during gestation,

*Corresponding author. Email: pedro.silva@ifrj.edu.br

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at a rate similar to that of an embryo developingoutside the mother in oviparous fishes. This condi-tion, which may be called incipient matrotrophy,was suggested to be the plesiomorphic condition forlive-bearing poeciliids, rather than pure lecithotrophy(Marsh-Matthews 2011). Other species typically havesmall eggs with minimal yolk stores and embryo massincreases dramatically during gestation (Marsh-Matthews 2011). This condition can be called sub-stantial matrotrophy.

In this study, we evaluate several life historyaspects of Phalloceros anisophallos Lucinda, 2008from Córrego Andorinha, Ilha Grande (RJ, Brazil).The study of P. anisophallos may be interesting sinceArias & Reznick (2000) found variation in the degreeof matrotrophy across populations of Phalloceroscaudimaculatus (Hensel 1868) and now this specieshas been divided into 21 new species (Lucinda 2008)including P. anisophallos. It is therefore interesting todescribe the reproductive strategy, especially matro-trophic patterns, in this newly described species,occurring in a region where reproductive studies forPhalloceros are absent.

Materials and methods

Study site

Córrego Andorinha (23°11′11.7″ S, 44°12′02.0″ W) is athird order stream draining the east side of IlhaGrande, in Rio de Janeiro, Brazil. It is approximately10 km long and flows into Dois Rios inlet (Rezende &Mazzoni 2006) next to the Centro de EstudosAmbientais e Desenvolvimento Sustentável (CEADS-SR2-UERJ – Center for Environmental Studies andSustainable Development). Regional climate is tropi-cal, hot and wet, with a mean annual temperature closeto 23°C. Relatively intense rainfall occurs through theyear, but a lower mean precipitation is recordedbetween June and August (83.6–92.8 mm month–1)whereas a higher average rainfall is recorded betweenDecember and March (258.8–278.8 mm month–1)(Silva-Filho et al. 2006). The study area comprisedtwo sites along the longitudinal section of CórregoAndorinha named A and B which differed mainly byaltitude (50–150 m asl) and vegetation cover (Rezende& Mazzoni 2006). At both study sites, inclination,water velocity and substrata were basically the same,with mesohabitats dominated by rapids, interspersedby pools, with rocky and sandy-silty bottom.

Fish sampling and laboratory methods

We examined 380 specimens of P. anisophallos col-lected in 12 bimonthly samples taken from October

2001 to August 2003. Fishes were collected by trawlsand sieves (meshes 0.5 and 0.3 cm, respectively) andkept on ice for transport. Sampled fishes were eutha-nized by an immersion in MS222 solution. Voucherspecimens of P. anisophallos were placed in theichthyological collection of Universidade doTocantins (UNT 6772 – paratype specimen) and inMuseu Nacional do Rio de Janeiro (MNRJ 28725).

Standard length (SL, cm) and total weight (Wt, g)were registered for each specimen. Individuals withidentifiable gonopodium or ovaries were classified asmales or females, respectively. We dissected the fishfor the identification of ovaries and we macroscopi-cally identified the gonads. Individuals without recog-nizable ovaries or gonopodium were not sexed andtherefore were classified as juveniles. Gonadalmaturation stage was not evaluated.

Developing ovaries were removed, weighed (Gw,g), fixed in formalin 5% and preserved in alcohol 70%.For the samples obtained since August 2002, gonadscontaining embryos were analyzed under a stereomi-croscope and embryos were classified into five stagesaccording to eye development: 1: non-eyed, 2: early-eyed, 3: mid-eyed, 4: late-eyed and 5: very late-eyed(Reznick & Endler 1982). Some gonads were fixed inLillie Formalin (Vazzoler 1996) for histological ana-lysis and confirmation of macroscopic distinctionbetween the stage 1 (non-eyed) and the maturationstages prior to fertilization. For gonads that were notintended for histological analysis, the embryos werecounted and approximately 30 embryos of each stagewere measured (diameter in mm) to provide size infor-mation of pre-classified embryos (Table 1).

Brood size was estimated as the number ofembryos in the same stage of development containedin the abdominal cavity. Brood size and femaleweight relationship were analyzed for each samplingmonth. Reproductive season was determined by thetemporal variation of the gonadosomatic index (GSI= Gw/Wt × 100) of females sampled between October

Table 1. Increase of mean diameter (± SD, range) withadvancing stage of embryos of Phalloceros anisophallosfrom Córrego Andorinha, Ilha Grande (RJ, Brazil). n = 30for each sample.

Embryo diameter

Mean ± SD RangeEmbryonic stage (mm) (mm)

1. Non-eyed 1.39 ± 0.23 1.00–1.752. Early eyed 1.59 ± 0.18 1.30–2.003. Middle-eyed 1.99 ± 0.15 1.60–2.304. Late-eyed 2.24 ± 0.16 1.90–2.455. Very late-eyed 2.56 ± 0.26 2.20–2.90

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2001 and August 2003. Variations in GSI valuesreflect changes in the size of ovaries, and are higherduring the breeding season and lower during the restseason (Vazzoler 1996). Temporal variation of therelative brood size (RBS, number of embryos in thesame stage/female Wt) and the proportion of differentembryonic stages per month from August 2002 toAugust 2003 were performed as complementaryanalysis for the determination of the reproductiveseason.

To evaluate the degree of matrotrophy, we com-pared the dry weight of embryos at each developmen-tal stage (Arias & Reznick 2000). The embryos wereobtained from females collected in October 2002,April 2003 and June 2004. Embryos from each samplewere grouped according to developmental stage andkept in an oven at 55°C for 24 hours. Since embryoshad been stored in ethanol, whereby lipids areremoved, the weight determined is the lean dry weight(sensu Arias & Reznick 2000). Results are expressedas the mean embryo dry weight (mg) for each stageand sample. Linear regression analysis of embryoweight–stage of development was performed basedon the subset of litters that were early-eyed or moreadvanced in development (stages 2–5) as in Arias &Reznick (2000) to allow comparison with their results.

Statistical analysis

Frequency distribution of lengths was analyzed formales, females and juveniles, and the differencesbetween mean lengths of these three groups weretested with a Student’s t-test. Frequency distributionof lengths was also analyzed for sites A and B and themean lengths of each group were compared throughStudent’s t-test. Sex ratio was assessed for the wholepopulation and for each study site. Variations of theexpected 1:1 sex ratio were tested by χ2 test. Length(ln SL)–weight (ln Wt) relationship was determinedfor juvenile, male and female specimens and between-groups differences of b values (regression slope) wastested with the t-test (Pauly 1993). All regressionswere tested for significance. All statistical analyseswere conducted using STATISTICA 7.1 software(StatSoft, Inc. 2005).

Results

Frequency distribution of lengths

Among the 380 sampled individuals of P. anisophal-los, 62 were considered juveniles, 84 were males and234 were females. Fish size varied from 1.1 to 4.1 cmand frequency distribution was very similar in the twostudy sites. Mean values of SL did not show

significant differences between sites for both juvenilesand males (tj = 0.27; p > 0.05/tm = 0.27; p > 0.05), butfemales were significantly bigger in site A (3.1 ± 0.4cm) than in site B (2.9 ± 0.4 cm; t = 4.72; p < 0.05).

Considering the frequency distribution of SL ofboth sites treated together (Figure 1), juveniles andmales varied from 1 to 3 cm. The length class withhighest occurrence of juveniles was 1.9–2.1 cm,whereas the highest occurrence of males was in the2.2–2.4 cm class (Figure 1). The mean SL of juvenilesand males were 2.06 ± 0.41 cm and 2.15 ± 0.33 cm,respectively without significant differences (t = 1.56,p > 0.05) between both groups. Females length variedfrom 1.6 to 4.2 cm and the class with highest occur-rence was that varying from 2.8 to 3.0 cm (Figure 1).Mean length of females was 2.99 ± 0.44 cm, beingsignificantly higher than the average length of juve-niles (t = 14.95, p < 0.05) and males (t = 15.74;p < 0.05).

Sex ratio

Females were more frequently captured than malesat both study sites (χ2A = 66.8; p < 0.05/χ2B = 11.5;p < 0.05), but the imbalance was more marked at siteA where we registered a females:males ratio of 7.3:1against 1.8:1 at site B. Sex ratio for the whole popula-tion was 2.8:1, differing significantly from expectedratio of 1:1 (χ2 = 70.8; p < 0.05).

SL–Wt relationship

There were high correlations between SL and Wt forboth sexes and juveniles (Figure 2). The equationsthat explained the relationships were: (a) juveniles:ln Wt = 2.96 ln SL – 3.80/R2 = 0.97/t = 44.38,p < 0.001; (b) males: ln Wt = 2.59 ln SL – 3.57/R2

Figure 1. Frequency distribution of lengths for Phallocerosanisophallos from Córrego Andorinha, Ilha Grande (RJ,Brazil).

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= 0.88/t = 22.85, p < 0.001; (c) females: ln Wt = 2.93ln SL - 3.67/R2 = 0.93/t = 54.65, p < 0.001. The slopesof these three equations did not differ between juvenilesand adults (both males and females – tjuveniles/males =1.42, p > 0.05/tjuveniles/females = 0.24, p > 0.05), butdiffered significantly between males and females(tmales/females = 2.95, p < 0.05).

Reproduction

Data concerning diameter of embryos for eachdevelopmental stage are presented in Table 1. Broodsize ranged from two to 27 embryos for females of 2.0cm (coinciding with the smallest female containingembryos) and 3.8 cm respectively. Brood size andfemale weight relationship was positive and statisti-cally significant (p < 0.01) for each sampling month(Figure 3). There were no batches at different stagesof embryonic development simultaneously. Weobserved only oocytes together with embryo stage 5.

Temporal variation of GSI was similar for the twostudy years, with means varying from 3.7 to 9.7. Thelowest values were registered in April and the highestoccurred from August to December in both years(Figure 4). The distribution of the RBS followed asimilar pattern as the GSI, ranging from 11.4 to 17.7embryos per gram (female Wt), with the lowest meanoccurring in April and the highest mean in October

(Figure 4). The occurrence of different stages ofembryonic development showed no relation with sea-sonality, and stage 5 also occurred throughout thewhole study period (Figure 5). Mean dry weight ofembryos in stage 5 was about 2.8 times the dry weightof embryos in stage 1 (Figure 6), confirming the pre-sence of substantial matrotrophy. There was weightloss from first to second stage and the rate with whichembryo weight increased thereafter varied.Parameters of the regression are provided in the equa-tion: embryo weight (mg) = 0.1867 stage2-5 – 0.1424/R2 = 0.8615/t = 7.89/p < 0.001.

Discussion

Frequency distribution of lengths and sex ratio

Frequency distributions of P. anisophallos lengthsfrom both sites were very similar, indicating that thepatterns observed are consistent. The initial lengthclasses showed very low abundances; this was prob-ably due to mesh size allowing small fish to slipthrough so that they were underrepresented in oursample. However, this bias starts to decrease in class1.6–1.8 cm, since P. anisophallos has body depthbetween 25.8% (females) and 33.5% (males) of SL(Lucinda 2008). Males were smaller and less abun-dant than females and these are very common pat-terns in Phalloceros (Aranha & Caramaschi 1999;Arias & Reznick 2000; Wolff et al. 2007) and otherPoeciliidae species (Andrade et al. 2008; Zúñiga-Vegaet al. 2012). This pattern could be explained byfemales having more post-maturation growth andlonger post-maturation lifespans, as registered forPoecilia reticulata Peters, 1859 (Reznick et al. 1996).

Bizassa & Pilastro (1997) have also shown that forPoeciliidae adopting a tactic of mating without femaleconsent, a smaller size of males may increase theirreproductive success. This tactic of mating was sug-gested for many Poeciliidae species (Farr 1975) andmay be occurring within the studied population.

Arias & Reznick (2000) addressed four popula-tions of Phalloceros and found spatial differences inthe size structure and the size at first maturity. AfterLucinda (2008) and based on the sampling sites andvoucher individuals, we assumed that these popula-tions may refer to three new species: Phalloceros har-pagos Lucinda 2008 (Paraguay location), Phallocerostupinamba Lucinda 2008 (Rio Silva and Rio Purubalocations), and Phalloceros spiloura Lucinda 2008(Arroyo Afluente location). Our study showed similarresults for the beginning of reproduction of femalesfrom Paraguay and Arroyo Afluente populations, butdiffered from Rio Silva and Rio Puruba populations(both P. tupinamba) in which females reached

Figure 2. Relationship between standard length and totalweight of juveniles (n = 55), males (n = 74) and females(n = 232) of Phalloceros anisophallos from CórregoAndorinha, Ilha Grande (RJ, Brazil).

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maturity at higher lengths (2.5–2.7 cm). The meanlength of females of P. anisophallos of the presentstudy was similar to Rio Puruba population and wasnot very different from the other Phalloceros popula-tions if the standard deviation is considered. We didnot observe the bimodal or polymodal size distribu-tion of males registered by Arias and Reznick (2000).

The mean length and range of P. anisophallos maleswere higher than those reported for the Paraguaypopulation (mean SL: 1.7 cm, range: 1.4–2.2 cm)but similar to those in other populations (Arias &Reznick 2000).

Similar results for size structure were reported forP. caudimaculatus (probably P. harpagos, Lucinda

Figure 3. Relationship between female total weight and brood size for each sampling event of Phalloceros anisophallos fromCórrego Andorinha, Ilha Grande (RJ, Brazil).

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2008) from Rio Ubatiba (Aranha & Caramaschi1999), Guarapava (Iguaçu basin) (Wolff et al. 2007)and Parque Florestal do Itapetinga (Machado et al.2002). Although there are some differences betweenour study and the studies cited above, some patternsare also verified and these differences can be attribu-ted to environmental factors but also to interspecificvariation.

Reproductive season

Edwards et al. (2006) argued that the use of GSI asthe only reproductive measure in the study of vivi-parous species may lead to inconclusive results as itdoes not take into account factors such as stage ofembryonic development and degree of matrotrophy.

In the present study, we found seasonal variation inGSI, but embryos in various stages of developmentwere found throughout the study period, suggestingthat mating and gestation of P. anisophallosoccurred throughout the annual cycle. The greatsimilarity between the analysis of temporal varia-tion of GSI and the RBS suggests that GSI reflectedmainly a seasonal variation in fecundity, which waslower around April, shortly after the rainiest periodof the year (December–March).

Machado et al. (2002), studying P. harpagos,found a well-defined reproductive season, with a per-iodic interruption of embryo production from April toJune. However, according to Tedesco et al. (2008),life history strategies are closely related to climate andto seasonal gradients in hydrological conditions.Continuous reproduction has been widely demon-strated in the tropical ichthyologic literature (Lamas& Godinho 1996; Mazzoni & Petito 1999; Alkins-Koo 2000; Mazzoni & Iglesias-Rios 2002), includingfor Poeciliidae species (Turner 1938; Morris & Ryan1992; Winemiller 1993), and Phalloceros populations(Aranha & Caramaschi 1999; Wolff et al. 2007). Thisfeature was also cited as a component of the oppor-tunistic reproductive strategy (Winemiller 1989) andmay be related, at least in part, to favorable environ-mental conditions for birth and growth of juvenilesthroughout the year, as well as to instable conditionsof water dynamics of small tropical streams (Garutti1988; Menezes & Caramaschi 1994; Mazzoni &Iglesias-Rios 2002). Thus, continuous reproductionincreases the survival chances of newly recruited juve-niles as it provides constant reproductive investmentduring the year rather than concentrate it in oneperiod, which may, due to hydrological instability,not be favorable for the development of juveniles.

Figure 4. Temporal analysis of gonadosomatic index (GSI)and relative brood size of Phalloceros anisophallos fromCórrego Andorinha, Ilha Grande (RJ, Brazil) between2001 and 2003. The vertical bars associated with the meanvalues correspond to their standard deviations (SD). Thenumbers at the tops of vertical bars are numbers of femalesanalyzed.

Figure 5. Temporal analysis of proportion of females con-taining the different embryonic stages for Phalloceros aniso-phallos from Córrego Andorinha, Ilha Grande (RJ, Brazil)between 2002 and 2003. The numbers at the tops of columnsare numbers of females analyzed.

Figure 6. Mean dry weights of embryos of Phallocerosanisophallos from Córrego Andorinha, Ilha Grande (RJ,Brazil), in the five embryonic developmental stages.Number of females analyzed = 52. Number of embryosweighed = 535.

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Superfetation and degree of matrotrophy

Our study did not provide clues for superfetation inP. anisophallos, as only mature oocytes occurredtogether with embryos in stage 5. In agreementwith our findings, superfetation was not observedin any other study for the genus Phalloceros(Machado et al. 2002), even in laboratory experi-ments (Arias & Reznick 2000).

The increase in diameter (1.8 times) and dryweight (2.8 times) of embryos strongly suggests thepresence of substantial matrotrophy in P. anisophal-los. Matrotrophy has been claimed to be suitable forspecies adapted to environments with constant foodsupply, because food shortages could impair theembryos’ development (Trexler & DeAngelis 2003;Lima 2005; Pollux & Reznick 2011).

Arias and Reznick (2000) also found substantialmatrotrophy for Phalloceros populations and ourresults are within the range of their results. Theyalso observed an initial weight loss from non-eyed tothe early-eyed stage in one population, suggesting anonset of matrotrophy between embryonic stages 2 and3. Placentotrophic species like Poeciliopsis turneriMiller, 1975 and Poeciliopsis prolifica Miller, 1960showed the greatest gain in mass after the yolk hadbeen consumed and the placenta was well developed(Thibault & Schultz 1978) and this could also be thecase with P. anisophallos.

Although Marsh-Matthews et al. (2005) andRiesch et al. (2010), analyzing radiolabeled nutrienttransfer between mother and embryos in Poeciliidaespecies, concluded that incipient matrotrophy couldbe widespread, occurrence of substantial matrotrophyis still considered strongly related to the occurrence ofsuperfetation (Pollux et al. 2009; Pires et al. 2010).However, our results suggest that in P. anisophallos,substantial matrotrophy occurs whereas superfetationdoes not. This reproductive strategy was alreadyreported for other species of Phalloceros and wasconsidered as a novel variation for the theme of live-bearing by Arias and Reznick (2000). In a recentreview of Poeciliidae evolution, Pollux et al. (2009)presented another two species with this strategy(Girardinus denticulatus Garman, 1895 andScolichthys greenwayi Rosen, 1967). Studies on theother species of Phalloceros, described recently byLucinda (2008), are necessary to verify if substantialmatrotrophy without superfetation is a general pat-tern within this genus.

Phylogeny of the Poeciliidae is still unclear, parti-cularly regarding the tribal definitions and the ances-try of live-bearing and superfetation (Lucinda & Reis2005; Hrbek et al. 2007). Pires et al. (2011) conductedan evolutionary study relating life-history traits to

matrotrophy evolution in the genus Poeciliopsis andemphasized the importance of similar studies in otherclades. Within the genus Phalloceros important varia-tion of reproductive strategies is found and morestudies for other species and environments could elu-cidate the role of matrotrophy and superfetation onreproductive success and phylogenetic relationshipsbetween the species of Poeciliidae.

AcknowledgmentsWe are grateful to all members of the Laboratório de Ecologia dePeixes (UERJ) for fieldwork, to CEADS/SR2/UERJ for the logisticinfrastructure provided for this work, to INEA for the samplinglicense (Proc. 029/2010) and to Eugenia Zandonà for suggestions onthe first version of the manuscript. This work is part of the ScientificInitiation work of PHAS (FAPERJ – E-26/152.201/2002) and hadfinancial support from FAPERJ (APQ1 – E/26 – 170.555/2000) andpersonal grant to RM (CNPq – 302.628/2002-9).

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