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Diet of Enyalius bilineatus(Leiosauridae: Squamata) at a sitein southeastern Brazil: effects ofphylogeny and prey availabilityVitor Souza Borgesa, Renan Condé Piresa, Antônio Meira Linaresa &Paula Cabral Eterovicka

a Programa de Pós Graduação em Zoologia de Vertebrados,Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte,Minas Gerais, BrazilPublished online: 01 Oct 2013.

To cite this article: Vitor Souza Borges, Renan Condé Pires, Antônio Meira Linares & Paula CabralEterovick , Journal of Natural History (2013): Diet of Enyalius bilineatus (Leiosauridae: Squamata)at a site in southeastern Brazil: effects of phylogeny and prey availability, Journal of NaturalHistory, DOI: 10.1080/00222933.2013.802048

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Journal of Natural History, 2013http://dx.doi.org/10.1080/00222933.2013.802048

Diet of Enyalius bilineatus (Leiosauridae: Squamata) at a site insoutheastern Brazil: effects of phylogeny and prey availability

Vitor Souza Borges, Renan Condé Pires, Antônio Meira Linaresand Paula Cabral Eterovick*

Programa de Pós Graduação em Zoologia de Vertebrados, Pontifícia Universidade Católica deMinas Gerais, Belo Horizonte, Minas Gerais, Brazil

(Received 11 July 2012; final version received 15 April 2013)

We studied the diet of Enyalius bilineatus (Leiosauridae: Squamata) at the InhotimInstitute, southeastern Brazil, through induced regurgitation. We obtained 27 indi-viduals using pitfall traps with drift-fence, active search, opportunistic encountersand capture by persons not directly involved in the study. We quantified preyavailability at the site using pitfall traps and used electivity indices to identify pre-ferred prey items based on ingested and available prey. Preferred prey includedLepidoptera larvae considering number of prey ingested and Orthoptera consider-ing volume ingested. We obtained the available data on diet of Enyalius species fromthe literature and compared a phylogenetic distance matrix with a diet dissimilaritymatrix, showing that phylogenetically closer species tended to have less dissimilardiets. We used independent contrasts to show that environmental impact did notreduce Enyalius population trophic niches, excluding the effects of phylogeny onniche breadth. Species of Enyalius may adapt to some disturbance in their habitats.

Keywords: lizard; independent contrasts; niche conservatism; trophic niche; humanimpact

Introduction

One of the most important and dynamic components of lizards’ interactions withtheir environments is the manner in which they obtain food (Duffield & Bull 1998).Biological aspects are directly linked to lizards’ diet and their foraging strategies (Huey& Pianka 1981; Pough et al. 2008); however, some qualitative and quantitative varia-tions can be noted in the diet of some species (Duffield & Bull 1998; Van Sluys et al.2004). Variations that happen in individuals of the same species can be caused by fac-tors such as sex, age and morphological or physiological differences (Filho et al. 2003;De Souza & Cruz 2008), as well as food availability in their habitats (Menezes et al.2008).

On the other hand, in species that share ancestry it is common that some ecologicaltraits such as diet are preserved, a phenomenon called niche conservatism (Wiens &Graham 2005). Nevertheless, that does not occur in all species; sometimes species thathave a distant phylogenetic relationship have more ecological resemblance than siblingspecies (Losos et al. 2003). Niche conservatism can even contribute to speciation, mak-ing it harder for species to adapt to new ecological conditions in an initial splitting of

*Corresponding author. Email: pceterovick@gmail.com

© 2013 Taylor & Francis

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two allopatric lineages. These lineages end up becoming two different species with eco-logical resemblance because of their inability to occupy the new locations with differentconditions (Wiens 2004; Kozack & Wiens 2006). This happens when the fragmentationof ancestral geographic range (e.g. by climatic change) is faster than the capacity of theorganisms to adapt to new environmental conditions (Kozack & Wiens 2006). In thisscenario, environmental impacts could be highly detrimental if they alter the environ-ment’s ecological conditions further than the species’ capacity to adapt, dramaticallyreducing its realized niche (Berg & Ellers 2010).

There are 248 known species of lizard in Brazil (Bérnils & Costa 2012). TheLeiosauridae family is composed of 14 species in the country, nine of them in theEnyalius genus (Bérnils & Costa 2012). Some information about morphology and nat-ural history is available for some species from this genus: Enyalius catenatus Wied, 1821(Vanzolini 1972), Enyalius leechii Boulenger, 1885 (Vitt et al. 1996), Enyalius iheringiiBoulenger, 1885 (Sazima & Haddad 1992), Enyalius bilineatus Duméril and Bibron,1837 (Vanzolini 1972; Zamprogno et al. 2001), Enyalius brasilienses Lesson, 1828 (VanSluys et al. 2004) and Enyalius perditus Jackson, 1978 (De Sousa & Cruz 2008; Sturaro& Silva 2010). According to Jackson (1978), Enyalius bilineatus can be diagnosed byusually straight canthal ridge, subdigital lamellae not keeled, tail scales not arranged indorsal–ventral rows, tail longer than 2.4 times snout–vent length, presence of a row ofenlarged vertebral scales, enlarged ventralmost subocular scale, preocular with strongkeel on posterodorsal margin, enlarged supraocular and other head scales smooth,ventral scales strongly keeled. Maximum snout–vent length is 82 mm for males and92 mm for females. Its coloration pattern is very diverse and it occurs in southeast-ern Brazil, in the states of Minas Gerais, Rio de Janeiro and Espírito Santo, usuallyin riparian forests and “cerrado”, but close to forest enclaves. This lizard has diur-nal and arboreal habits and it can be found on trees and bushes most of the timemore than 2 m above the ground (Jackson 1978; G.R. Colli, personal communica-tion). However, there is evidence of ground foraging, based on a study conducted inthe state of Espírito Santo (Zamprogno et al. 2001) and another conducted at Inhotim,state of Minas Gerais, Brazil (Linares 2009).

We aimed to study the diet of E. bilineatus at the Environmental Preservation Areaof Inhotim, Brumadinho municipality, Minas Gerais state, and investigate whether theEnyalius genus exhibits niche conservatism, that is, whether the species diet has sig-nificant phylogenetic influence. We also tested whether the trophic niche of Enyaliusspecies is reduced in impacted compared with preserved landscapes, excluding theeffect of phylogeny.

Material and methods

Enyalius bilineatus dietWe conducted fieldwork from July 2008 to January 2009 at the EnvironmentalPreservation Area of Inhotim (20◦07′27′′ S, 44◦13′07′′ W, Datum WGS 84; 700–1300 maltitude), located in Brumadinho municipality, Minas Gerais state, southeasternBrazil. Inhotim encompasses 786.06 ha, 440.16 ha of which are preserved forest frag-ments and “cerrado” (on higher terrains). The area also has three springs, and somecreeks (Inhotim 2010). The region has an altitudinal subtropical climate with dry win-ters and rainy summers, annual precipitation varying between 1000 mm and 1500 mm.

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Annual average temperature is 18◦C, and annual average humidity is 80% (Antunes1986; IBRAM 2003).

Based on evidence of ground foraging for E. bilineatus (Zamprogno et al. 2001;Linares 2009) we used pitfall traps to capture individuals for stomach content extrac-tion. We used 100 pitfall traps disposed in 20 linear transects of five 60-l buckets spaced10 m from each other and connected with drift-fence. Drift-fences were made of resis-tant plastic or a net (at windy and sunny sites), their bases were buried about 15 cmbelow ground surface; they passed through the middle of the buckets and their topswere 80 cm above ground. Eight series of traps were located in anthropogenic envi-ronments (ornamental gardens) and 12 series in natural forest/“cerrado” fragments.Traps remained open only during sampling periods, resulting in a total of 84 days ofsampling effort (7 days per month) for each of the 100 traps. We inspected traps oncea day in the morning. Costa et al. (2008) compared diets of eight lizard species cap-tured with pitfall traps (inspected once a day) and other methods (by hand, noose orshotgun) and found no difference, showing that pitfall traps are a good way to capturelizards for diet studies. Mean total retention time of food in lizard guts was reported tobe at least 20.1–23.7 h for insect feeders based on available data (Hatch & Afik 1999).For this reason, we believe that eventual losses of prey through digestion while theE. bilineatus were in the buckets were small and would only happen if a lizard fell intoa bucket immediately after inspection and had a digestion time among the fastest forinsectivorous lizards.

We also conducted diurnal and nocturnal active searches in an attempt to captureindividuals that might not be using the ground to forage. Nocturnal searches lastedfrom just after sunset until approximately 01.00 h. Daily searches were made between15.00 h and 17.00 h. We also obtained some individuals from opportunistic encounters(Martins & Oliveira 1998), i.e. occasional sightings (by us or local staff) when we werenot conducting active searches.

We obtained E. bilineatus stomach contents using the regurgitation method (Legler& Sullivan 1979). We introduced a catheter into the lizard’s mouth and injected a smallvolume of water (at ambient temperature) until the lizard regurgitated. This method ishighly recommended for dietary studies because it does not require the studied spec-imens to be killed and it provides good results with very low risk of injury (Legler &Sullivan 1979). Stomach flushing was conducted as soon as we found the lizards (inthe traps or during visual searches). Lizards captured by persons not involved in thestudy were used when captured during our stay in the field, so stomach flushing wasconducted at most 1 hour after capture. The specimens we stomach-flushed regurgi-tated very easily and promptly, and we performed two or three stomach flushes untiljust water came out with no food remains. Usually all the stomach contents cameout promptly and we performed the additional flushes just to make sure that noth-ing remained in the stomach. After obtaining the stomach contents, we released thelizards at their capture sites. The lizards were marked for another study conductedat the same site (Linares 2009), and we did not consider recaptures to avoid pseudo-replication. We analysed stomach contents using a stereomicroscope and specializedliterature (Borror et al. 1989; Ruppert et al. 2004) to identify prey items to the orderlevel (family level for Hymenoptera). We measured prey total length and width to esti-mate prey volume using an ellipsoid formula [Volume = (π × prey’s length × prey’swidth2)/6] (Miranda & Andrade 2003). We assessed prey availability based on thearthropods captured in the same pitfall traps used to capture lizards. Although lizards

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could prey on captured arthropods while inside the buckets, the level of digestion of theprey items obtained from their stomachs indicated that this did not happen (we foundno prey that looked as if it had been recently eaten). Besides, we occasionally observedlizards standing next to potential prey and not eating inside the buckets, probablybecause trying to escape from the trap was a priority over eating once captured (a totalof about 1 hour of observations of 18 different lizards). Costa et al. (2008), comparinglizards of eight species captured by pitfall traps and other methods, failed to find morestomach contents in pitfall-trapped lizards (with one exception) compared with lizardscaptured by other methods. According to them, lizards that search their prey activelyare unlikely to feed when restricted to traps.

We calculated electivity indices (D), to evaluate prey preference by E. bilineatus,according to Jacobs (1974): D = (Rk – Pk)/[(Rk + Pk) – (2Rk Pk)]; where Rk = pro-portion of item “k” (or size class “k”) in the diet, Pk = proportion of item “k” (or sizeclass “k”) in the environment. D varies from + 1 (total selection or preference for item“k”/size class “k”) to – 1 (item “k”/size class “k” is present in the environment butnot in the diet). D equals 0 when item “k”/size class “k” is consumed in the same pro-portion that it occurs in the environment. We called this index Df when it was basedon the frequency of prey in the stomachs, and Do when it was based on the occurrenceof prey in the stomachs, that is the number of stomachs that contained each categoryof prey. We used this additional approach to study the diet of E. bilineatus because thehigh consumption of a type of prey by a single individual could interfere in the species’apparent preference result. In this case, the occurrence index would provide a differentresult and aid in data interpretation.

Niche conservatism in Enyalius speciesTo build a matrix of phylogenetic distances between species pairs, we used the softwareCOMPARE 4.6 (Martins 2004) to obtain phylogenetic distances between the speciesthat already had their diet studied (Enyalius bilineatus, Enyalius leechii, Enyalius perdi-tus, Enyalius brasiliensis and Enyalius iheringii, see Table 1). We used the cladogramtopology of Bertolotto (2006) of Enyalius species, based on the concatenated sequencesof three mitochondrial genes (ND4, cyt b, 16S) and one nuclear gene (c-mos) obtainedwith the method of maximum parsimony. We generated random phylogenetic distancesassuming Brownian movement, with character measures and variants equal to zeroaccording to the method of Felseinstein (1985), described originally to explain pheno-type evolution under the effect of genetic drift. We considered phylogenetic distance aszero for populations of the same species at different localities.

We built a Bray–Curtis matrix of diet dissimilarity for studied populations ofEnyalius species using our data and data available in the literature (number of preyconsumed per category), using the software SYSTAT 12 (SYSTAT 2007). We com-pared the phylogenetic distance matrix and the diet dissimilarity matrix with a Manteltest in the software PCORD (McCune & Mefford 1999) to check whether phylogenyhas a significant influence on the diet of Enyalius species. We applied a Monte Carlotest (5000 simulations) to obtain the level of significance (defined as p < 0.05).

We used the method of independent contrasts (Freeman & Herron 2001) to testwhether the Enyalius species/populations studied in areas under some level of impact(given by the presence of agricultural activities or urbanization; see Table 1) sufferedtrophic niche reduction when compared with species/populations of preserved areas,

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Table 1. Species of the genus Enyalius with available information on diet composition, includingnumber of individuals analysed with prey in their stomachs: (n), location, sampling methodemployed, schedule, assessment of prey availability, and references.

Species n Study site(biome)

Samplingmethod/schedule

Preyavailability

analysis

Source

Enyaliusleechi

Amazon Forest Dissection/1987;1984–1986; 1995

No Vitt et al.(1996)

Enyaliusbilineatus

48 Atlantic Forest Dissection/February1995 to March 1996

No Zamprognoet al. (2001)

Enyaliusbrasiliensis

15 Atlantic Forest Dissection/Scheduleunavailable

No Van Sluyset al. (2004)

Enyaliusbilineatus

89 Atlantic Forestand coffeeplantation

Dissection/December1997 to November2000, monthly

No Teixeira et al.(2005)

Enyaliusbrasiliensis

27 Atlantic Forestand coffeeplantation

Dissection/December1997 to November2000, monthly

No Teixeira et al.(2005)

Enyaliusperditus

55 Atlantic Forest Dissection/March1997 to March 1998,fortnightly

Yes De Souza andCruz (2008)

Enyaliusiheringii

23 Atlantic Forest Dissection/2001–2008 Yes Liou (2008)

Enyaliusperditus

66 Atlantic Forest Dissection/2002–2008 Yes Liou (2008)

Enyaliusbilineatus

21 Atlantic Forest/Cerrado

Regurgitation/July2008 to January 2009

Yes Present study

Enyaliusperditus

38 Atlantic Forest Dissection/August2005 to July 2006

Yes Sturaro andSilva (2010)

discounting the phylogeny effect. We classified these areas at the landscape level, con-sidering as altered those areas with human influence represented by agriculture orurbanization within the study site described in the respective studies. The descriptionswere qualitative, so we only considered landscapes as altered or preserved. Alteredlandscapes, though, could also have patches of natural vegetation, and lizards couldpotentially eat either within these patches or in the impacted areas. We calculated nichebreadth for each population using Hurlbert’s (1971) PIE (Probability of InterspecificEncounter) diversity index in the software ECOSIM (Gotelli & Entsminger 2001).Subsequently, we calculated independent contrasts for niche breadths for each clado-gram branch (cladogram extracted from Bertolotto 2006). We did the same for impactlevel, given as 0 (preserved habitats) or 1 (impacted habitats). The contrasts were thencompared using a Spearman correlation in the software BIOESTAT (Ayres et al. 2005).A negative correlation would indicate the association of narrower niches with the useof impacted landscapes. To avoid an additional variation source that could be addedbecause of substantial differences in prey availability between biomes, in this analysiswe only considered typical Atlantic Forest species, we excluded E. leechii for being theonly Amazonian species included in the previous analysis (see Table 1).

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Results

We captured 27 individuals of E. bilineatus, eight of which were females and 19 weremales. Of all lizards, 21 had stomach contents, the remaining lizards had empty stom-achs. Most individuals (n = 25) were captured in forest habitats and only two werecaptured in anthropogenic areas. Pitfall traps captured 18 individuals, four were cap-tured in opportunistic encounters, three by active search and two were located byInhotim staff. Among the nine lizards located visually, five were on the ground.

We identified seven invertebrate orders as prey in the lizards’ stomach contents andrecorded eight orders as available in the environment (Table 2). According to electivityindices (Df and Do) E. bilineatus showed a preference for Lepidoptera (larvae) andColeoptera. Araneae showed positive electivity only when occurrence was considered(Do, Table 2). Items avoided included Blattaria, Chilopoda, Hymenoptera (Formicidaeand Vespidae) and Opiliones (Table 2). When we considered prey volume, the impor-tance of Lepidoptera and Orthoptera was reinforced, although the most representativeitem regarding volume was Orthoptera (Table 2).

Phylogeny explained a significant amount of the Enyalius species diet composition(r = 0.748; p = 0.0002). When the effect of phylogeny was excluded, the existence ofhuman impact in the habitats of Enyalius populations did not seem to cause trophicniche contraction (rs = –0.301; p = 0.468; n = 8 pairs).

Table 2. Estimated availability of prey categories in the environment (number of individuals)at Environmental Preservation Area of Inhotim, Brumadinho, Minas Gerais, Brazil. Frequency(number of items in stomachs) and occurrence of prey in the stomach contents of E. bilineatus(number of stomachs containing the item) with their respective electivity values (Df and Do).Prey volume is also presented as raw data (mm3) and relative value (%).

Order/Family Availability Stomachcontent

Electivity(Df )

Stomachcontent

Electivity(Do)

Volume

Frequency Occurrence mm3 %

Araneae 100 5 −0.27 5 0.37 636.02 0.136Blattaria 45 0 −1.00 0 −1.00 − −Coleoptera 82 10 0.21 5 0.46 574.49 0.123Coleoptera

(larvae)0 1 − 1 − 53.88 0.011

Chilopoda 15 0 −1.00 0 −1.00 − −Hymenoptera

(Apoidea)0 2 − 2 − 42.96 0.009

Hymenoptera(Formicidae)

450 3 −0.91 3 −0.72 1.32 0.000

Hymenoptera(Vespidae)

17 0 −1.00 0 −1.00 − −

Isoptera 0 45 − 1 − 114.68 0.025Lepidoptera

(larvae)38 4 0.12 3 0.54 1117.34 0.239

Orthoptera 256 14 −0.26 6 −0.06 2139.90 0.457Opiliones 3 0 −1.00 0 −1.00 − −Total 1006 84 − − − 4680.59 1.000

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Discussion

Our findings on E. bilineatus diet differ from those previously reported for a locality inthe state of Espírito Santo, also in southeastern Brazil, which pointed to Orthopteraas the most frequent prey in this lizard’s diet (Zamprogno et al. 2001). Another studyof E. bilineatus diet also showed a different result, reporting ants as the most fre-quently consumed item, followed by Orthoptera and Blattaria (Teixeira et al. 2005).Diets of individuals usually reflect diets of a species in a particular habitat (Vitt &Caldwell 2009). This shows that there can be variations between different populations,which can be linked with prey availability in the environment. However, prey availabil-ity was not assessed in either of these studies so more data on prey availability andconsumption at different localities are needed to test this hypothesis for E. bilineatus.In our study, however, although Orthoptera was not a preferential prey based on itsfrequency or occurrence, this order represented an important proportion of the vol-ume of ingested prey because of its great size. Formicidae and Blattaria, on the otherhand, were avoided by E. bilineatus at our study site.

The large number of individuals captured with pitfall traps in our study confirmsthe use of the ground by E. bilineatus, as observed by Zamprogno et al. (2001) andLinares (2009); Teixeira et al. (2005) observed a large amount of terrestrial arthropodsconsumed by the species, also corroborating these results. According to Zamprognoet al. (2001), E. bilineatus exhibits sit-and-wait foraging behaviour, however, our resultsindicate that this species also has some characteristics of an active forager. Otherspecies of Enyalius have already been reported to forage actively. Vitt et al. (1996)observed E. leechi to eat a large amount of termites and caterpillars, which they asso-ciate with active foraging. Sturaro and Silva (2010) also considered E. perditus to forageactively based on the amount of sedentary prey in this species’ diet. The significantpresence of sedentary prey such as Lepidoptera and Coleoptera larvae in the stomachsof the individuals analysed characterizes an active foraging behaviour that is expectedin lizards with an elongated body and tail (Pough et al. 2008). According to Poughet al. (2008) E. bilineatus could be considered an errant forager, showing affinity forlarger and active prey such as beetles and locusts besides sedentary prey such as lar-vae. Isoptera represented 54% of all prey items; however, they were all found in a singlestomach. This result indicates an opportunistic component in the feeding strategy ofE. bilineatus: when in contact with a high availability of a specific prey the lizard maydirect its capture effort to it. The same opportunism was reported by Teixeira et al.(2005), who observed that a few individuals of E. bilineatus consumed a large amountof Isoptera.

A significant part of Enyalius species diet composition is explained by phylogeny,confirming that trophic niche conservatism occurs in the genus. According to Jackson(1978), the allopatric distribution of Enyalius species can be explained by the incapac-ity of niche partitioning among them because of their ecological resemblance. Thisscenario is in accordance with a possible influence of niche conservatism on speciationpatterns (Wiens 2004; Kozack & Wiens 2006) if Enyalius species have been maintainedin allopatry by the disjoint distribution of their preferred environments.

Our results indicate that Enyalius species are able to maintain their trophic nichebreadth in human-altered habitats close to their trophic niche breadth in preservedhabitats, indicating some resistance to habitat alteration, at least concerning the main-tenance of a diversified diet. Although this species was considered mainly restricted

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to forested habitats (Jackson 1978; Colli et al. 2002), some authors have found itassociated mainly with altered areas, such as coffee plantations, secondary forests,pastures and even urban areas (Teixeira et al. 2005; Costa et al. 2009), showing thetolerance of the species to open habitats, even benefiting from deforestation (Teixeiraet al. 2005). It is possible that the kinds of impacts occurring at the sites where Enyaliuspopulations had their diets assessed were not detrimental to arthropod diversity, somaintaining sufficient food availability to supply the lizards’ needs. An assessment ofpossible effects of human impact on diet composition and nutritional value would beinteresting, but it will only be possible when more data on food availability at Enyaliushabitats are provided concomitantly with diet studies.

Another possible explanation for the lack of niche reduction at altered habitatsmay be the ability of Enyalius species to choose proper foraging microhabitats. In ourstudy, for instance, just two out of 27 individuals were captured in anthropogenic areas,perhaps because of the lizards’ preference for forested sites. This result indicates thatthe level of urbanization found in Inhotim, where natural areas are preserved and inter-spersed with human structures (buildings, ornamental gardens), allows the existence ofspecies such as E. bilineatus that can maintain their lifestyle in these environments. Thepopulation of E. bilineatus in Inhotim would provide a good example of “reconcilia-tion ecology”, a concept proposed by Rosenzweig (2003). According to this concept,anthropogenic and natural microhabitats should be interleaved as a means to preservethe remaining biodiversity where humans are already established. Considering the highrate of human population growth and human use of space, it is necessary to provideconditions for wild species to use anthropogenic areas once the natural reserves are nolonger sufficient to preserve a significant proportion of biodiversity. The populationof E. bilineatus at Inhotim provides a good example of the benefits of reconciliationecology. This is promising if we take into account that E. bilineatus belongs to a genuswith niche conservatism, that is, little flexibility to adapt to new, altered food resources.

AcknowledgementsWe would like to thank M. Cozzuol, A.M. de Souza and two anonymous reviewers for sug-gestions on early versions of this manuscript, the staff of Inhotim for receiving us and beingvery helpful during project activities, and ICMBio (Instituto Chico Mendes de Conservaçãoda Biodiversidade) for research and collecting permits (13036–1 and 13036–3). A ResearchProductivity grant (301077/2010-0) was awarded to P.C. Eterovick, and student scholar-ships were awarded to V.S. Borges, R.C. Pires and A.M. Linares by Conselho Nacional deDesenvolvimento Científico e Tecnológico (CNPq).

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