RevBiotemas31-4-18

Conservation status of Astyanax biotae in Mato Grosso do Sul 51of Astyanax biotae reported in this paper come from according to law no 9.985 of 15/07/2000 (ICMBIO,different research projects and were captured in four 2009). The stream is on the northern boundary oflocalities (Figure 1 and Table 1), described below: the conservation unit and is about 3.8 km long. It presents calm and limpid waters, a sandy substratea) Égua Stream, municipality of Angélica, a first-order with deposits of plant litter and organic matter in stream, tributary of the Piravevê River, tributary the margins, as well as many macrophytes and of the Ivinhema River. The site is in the region of aquatic grasses, and is surrounded by typical vereda headwaters and still has fragments of riparian forest vegetation (palm swamp) represented by Mauritia depleted by the advance of pastures, on the edges of flexuosa Mart., or the buriti palm (Figure 2a). a dirt road. c) Marsh in the headwaters of São Bento Stream, ab) Headwaters of Rapadura Stream, a first-order stream small tributary of the Vacaria River, affluent of the tributary of Ribeirão Pombo, affluent of the Verde Ivinhema River (Figure 2b). The collection site is River. The collections were made during expeditions located along Highway BR-060, in the municipality for a biological inventory aimed at developing the of Dois Irmãos do Buriti, on the Serra de Maracaju, Management Plan of Parque Natural Municipal exactly in the watershed transition between the do Pombo (PNMP), Três Lagoas municipality, basins of the upper Paraná and upper ParaguayFIGURE 1: Astyanax biotae records in the upper Paraná River basin, Mato Grosso do Sul, Brazil. The dashed line represents the border between the upper Paraná River and upper Paraguay River basins. In blue, the Ivinhema River basin, and in green, the Verde River basin. The star represents the type locality of A. biotae; numbers represents the new records presented in this work: 1. Égua Stream; 2. Rapadura Stream; 3. São Bento Stream; 4. Lagoon at PEVRI. Revista Biotemas, 31 (4), dezembro de 2018

52 M. J. A. Vilela et al.TABLE 1: Records of Astyanax biotae collections in Mato Grosso do Sul State, upper Paraná River basin. In Number of individuals column, the numbers represent the total number of individuals in the lot and those analyzed herein, respectively. Local Date Lat S Long W Altitude Number of Voucher (m) individualsÉgua Stream 22.04.2005 22°10’30’’ 53°50’10” 335 DZSJRP 7510Rapadura Stream 01.03.2012 20°20’06” 52°35’30” 399 17/11 ZUFMS 5541São Bento Stream 30.08.2016 21°02’01” 55°18’16” 563 18/6 ZUFMS 04898Lagoon at PEVRI 28.05.2017 22°51’48” 53°38’32.8” 240 13/1 CPUEMS 0537 2/2 river basins. During the rainyUsneiavseornsidtahdise aEresataduCaloldeçeãoMdaetoPeGixreossdsoa UdnoiveSruslida(CdePUEsEtaMdSua),l daendMaCtooleção de pe becomes a large floodplain of about 60 ha. Grosso do Sul (CPUEMS), and Coleção de Peixes do Departamento RdeioZooDloegpiaarteamBeontâtonicdae, ZUonoilvoegrisaideadBeoEtâsntaicdau,aUl dneivSerãsoidPaaduelo “Júlio de Md) Lagoon in Parque Estadual das Várzeas do Ivinhema (PEVRI), a conservatiFoinlhuon”itSãloocJaotesdé dino RiEosPtaredtuoa,lSdPe (SDãZoSPJaRuPlo). “Júlio de Mesquita Filho” São the Ivinhema River basin. The collection site is José do Rio Preto, SP (DZSJRP). located in alunonwadrleaernadfolfuwvviáaartlez/lreasac,uorsectgrciiuFnopeInGiaeiUldnnRflouEbmeyn2ec:npePNciloaa(arnetttuu.iegareral.er,lvMiewuFnIGiocUfipRtahEle2d:cooPdalPlo.aeorRcPmtiatoaipblmoaovndbi;uoesbwr;iab.teoS.MfstMrteahoaaerfrmsschAh,oilsoonltennyctahtthtienhoeanPehxasehriaqtbeeduiaswoedotaNwafteeaAart.stsuetaryoraa.sflnSRMoaãxfauopbnSBaiiãocdeoitnupataerBoal. eSnttoreaSmtre, aimn th given to d vegetation Panicum prionitis Nees, Sagittaria monteviddreynsseiasson. Stream during the dry season. Cham. & Schtdl., Cyperus sp., Pfaffia iresionoides Sprengel, and Eichhornia spp.) (IMASUL, a2008). Data sampling and laboratory processing The specimens were collected with a dragging bnet and sieve, both with 2.5 mm mesh. Collectedspecimens (License SISBIO 15044-1) were fixed in10% formaldehyde and later transferred to 70% alcohol.Sampling occurred in shallow places, between 10 cmand 150 cm deep, and the specimens were identifiedbased on the original description (CASTRO; VARI,2004). Morphometric and meristic measurements wereperformed on 20 specimens according to Fink andWeitzman (1974), using a digital caliper with precisionof 0.1 mm, for comparisons with the descriptive data ofthe species. All proportions were estimated in relationto the standard length (SL), with the exception of eyediameter, interorbital width, snout length and maxillarylength, referred to as head length (HL). Voucher specimens were deposited in the followingichthyological collections: Coleção Zoológica daUniversidade Federal de Mato Grosso do Sul (ZUFMS),Revista Biotemas, 31 (4), dezembro de 2018 Analysis Based on the International Union for Conservation of Nature (IUCN) guidelines

Conservation status of Astyanax biotae in Mato Grosso do Sul 53 Analysis yellowish-brown color, mixed with silver-bluish tones on the flanks, overlapping the dark lateral stripe; anterior Based on the International Union for Conservation portion of the abdomen silverish; hyaline pectoral andof Nature (IUCN) guidelines, adopted by the Chico pelvic fins, slightly yellowish; dorsal and anal fins withMendes Institute for Biodiversity Conservation for the slight grayish-blue coloration and a dark marginal band;Brazilian Red List assessment of fish species (ICMBIO, and gray-blue caudal fin, more pronounced in the upper2013; IUCN, 2013; 2017), we listed the conservation and lower lobes, with dark median rays (Figure 3). Incategory of this species. fixed individuals, these nuances of color disappear, with the yellowish-brown tone prevailing in the body and theResults slightly bluish hyaline of the fins, as shown in Figure 3. The specimens from PEVRI showed a more pronounced Astyanax biotae is distinguished from congeners by reticulated pattern and the spot in the caudal pedunclethe presence of a vertically elongated humeral spot and was also more marked in relation to the other samples,a slightly dark strip in the medial portion of the flanks, which may be related to small differences in habitatmore visible from the dorsal fin to the caudal peduncle, conditions (e.g., water color, chemical parameters,where it forms a dark rounded spot. We observed that availability of light in the water column, etc.) or tonewly captured specimens show the following: upper phenotypical variations.medial portion of the body and head with a slightFIGURE 3: Astyanax biotae, ZUFMS-4898, 39.40 mm SL, from São Bento Stream, Mato Grosso do Sul State, Brazil: exemplar sample in vivo (top) and in 70% alcohol (bottom). Revista Biotemas, 31 (4), dezembro de 2018Morphometric and meristic data of the measured individuals are presented in Table 2.

54 M. J. A. Vilela et al. Morphometric and meristic data of the measured Standard length varied between 17.5 mm and 39.4individuals are presented in Table 2. The specimens mm, with an average of 30.31 mm, less than the averagepresent premaxillary teeth in two rows, four or five recorded (44.2 mm) for the paratypes. As observed byteeth on the inner premaxillary row and complete lateral Castro and Vari (2004) in individuals from streams ofline, conferring with the basic characteristics defined for the Paranapanema River basin, we also noticed a slightAstyanax Baird & Girard, 1854. increase in body height in larger individuals, althoughTABLE 2: Morphometric and meristic data of Astyanax biotae recorded in the upper Paraná River basin. N = number of examined specimens, SD = Standard Deviation. Morphometric data N Range (%) Mean (%) SDStandard length (mm) Percents of SLBody depthHead length 20 17.5-39.4 30.31 –Head depthPredorsal distance 20 33.2-42.3 37.67 2.32Prepelvic distancePelvic fin to anal fin distance 20 26.8-32.9 29.68 1.57Caudal peduncle depthDorsal fin base length 20 26.3-33.7 29.65 2.12Anal fin base lengthPectoral fin length 20 53.2-58.5 56.11 1.33Pelvic fin lengthDorsal fin length 20 45.7-53.8 48.45 1.93Anal fin lengthCaudal peduncle length 20 13.7-20.0 16.48 1.82Dorsal fin to adipose fin distanceOrbit to dorsal fin origin distance 20 11.3-13.9 12.62 0.74Dorsal fin to caudal peduncle distance 20 12.5-16.5 14.74 0.93Upper jaw lengthOrbital diameter 20 28.9-36.3 32.95 1.84Snout lengthInterorbital width 20 19.9-23.7 22.43 1.55Meristic dataDorsal fin rays 20 15.4-21.5 18.10 1.42Anal fin raysCaudal fin rays 19 26.4-31.3 29.91 1.40Pectoral fin raysPelvic fin rays 20 17.8-24.2 20.98 1.90Pored lateral line scales 20 9.7-13.1 11.53 0.94 20 34.8-39.2 37.10 1.27 20 38.2-44.3 40.59 1.27 20 46.7-53.8 49.16 1.70 Percents of HL 19 36.4-44.2 41.25 2.09 20 31.6-40.0 36.62 2.59 20 20.7-27.1 24.01 2.11 20 33.4-39.2 36.18 1.91 (N) Range Mode 20 ii,8-9 ii,9 20 iii,22-25 iii,24 20 i,8-10/8-10,i i,9/8,i 20 i,10-12 i,12 20 i,6-8 i,7 19 31-35 34Revista Biotemas, 31 (4), dezembro de 2018

Conservation status of Astyanax biotae in Mato Grosso do Sul 55Meristic data (N) Range ModeCircumpeduncular scales 20 12-15 14Scale rows above lateral line 20 6-7 6Scale rows below lateral line 20 4-6 5Scale sheath along anal-fin base 19 8-16 12Predorsal scales 20 9-13 11Maxillary teeth 19 0-1 1Premaxillary teeth – outer row 19 4-5 4Premaxillary teeth – inner row 19 4-5 5Dentary teeth 19 4-5 4more specimens are necessary to make a more complete Cerrado and forest areas include a large part of theanalysis about this morphological feature. Body height/ headwaters that supply the two large hydrographic basinsSL ratio in the smallest individual, 17.2 mm, was of the state, which still have considerable gaps in relation33.16%, while in the largest, 39.4 mm, it was 42.8%. to what is known about the ichthyofauna, especially small species, despite some progress made in recent In general, the morphometric data are similar to years. The records are recent, with the earliest dated tothose obtained by Castro and Vari (2004), as were the 2005, and coincide with the advance of inventories andobserved meristic data. However, scale sheath along collections in more isolated, previously not sampled,anal-fin base showed one of the largest amplitudes of sites. It is even possible that the actual distribution of thevariation, between 8 and 16, with a mode equal to 12 species is greater than the one known to date, considering(vs. 8-11, mode 9), and one specimen had four the numerous sample gaps that exist throughout the state.premaxillary teeth in the inner row (vs. five). Nevertheless, we believe that A. biotae is a species with a more restricted distribution to certain areas, essentiallyDiscussion because its presence has not been registered in other areas, even in densely sampled places. In addition, the According to Langeani et al. (2007), nine species reduced number of individuals in the catches so farof Astyanax occur in the upper Paraná River basin. suggest that populations are also small.Astyanax altiparanae (= A. lacustris), A. bockmanni, A.fasciatus, and A. paranae are the most widely distributed, The capture sites of the samples are somewhatin the basin, while A. schubarti, A. trierythropterus and similar, being lentic or semilentic water types,two new species not yet described show more restricted protected by aquatic macrophytes and linked to nearbydistributions, like A. biotae. For the latter species, records lotic drainages. Two occurrences were recordedof its occurrence at the time of the study were only from within protected areas. In PEVRI, occurrences weretwo small streams in the Ivinhema and Paranapanema characterized by ponds with good water quality andRiver basins (CASTRO; VARI, 2004; CETRA et al., other habitat attributes. This area has been protected2016; FROELICH et al., 2017), including the recent from anthropic actions since December 1999, whenpaper by Oliveira et al. (2018). the decree of expropriation was issued for the effective implementation of the unit (IMASUL, 2008). In PNMP, The samples recorded in the present study extend the captures occurred in pools formed by blockedthe distribution area in Mato Grosso do Sul State, adding culverts for a stream by an old road and reasonably well-records for the upper reaches of the Ivinhema River basin preserved habitat conditions. The other two occurrencesand in the Verde River basin. These heavily anthropized were recorded in stretches of semi-dammed streams Revista Biotemas, 31 (4), dezembro de 2018

56 M. J. A. Vilela et al.due to the presence of roads. One is a point of Égua between headwaters and is about 100 km from São BentoStream that is cut by an unpaved road and surrounded Stream, the westernmost point of the distribution of A.by pastures and crops. Another is São Bento Stream, biotae.that is a floodplain cut by a heavily used highwayand completely surrounded by monocultures, mainly In streams from the Paranapanema River basin,sugarcane and soybeans. In spite of wire fencing that Cetra et al. (2016) considered A. biotae a rare species,separates the wetland from cultivated areas, the site is with low occurrence frequency, abundance andeasily accessible, including by potential fishers, along biomass. Its conservation status, at the national level,the highway. These environments are similar to the type was considered Deficient Data (DD) (ICMBIO, 2016).locality, Água Mole Stream, which is also located in an However, Oliveira et al. (2018) suggest its classificationarea of agricultural activity with a corresponding loss of status as Least Concern (LC) at the national level,native forest. These types of habitats are quite common considering the absence of real threats within thein the landscape of Mato Grosso do Sul, especially from protected area (PEVRI).the central to the southern part of the state, but remainneglected in terms of ichthyofaunal surveys, although According to the methodology and guidelines of theimportant information about the biology of species IUCN, we classified A. biotae as Least Concern (LC) inwith restricted ranges can be obtained from them (e.g., Mato Grosso do Sul State. The species occurs in two sitesSEVERO-NETO; VOLCAN, 2018). of headwater areas surrounded by crops or pasture and, hence, is susceptible to various types of threats, including It is noteworthy that the Paranapanema River, loss/alteration of habitat, cattle trampling, siltation, groundthe basin of the type locality, flows into the Paraná leveling, deforestation and contamination by pesticidesRiver practically at the same latitudinal line as that of in areas in contact with monocultures. On the other hand,Ivinhema River floodplain, on the right bank. Thus, the registration of the species within two protected areasthe distance between the Paranapanema and Ivinhema offers this fish a relative degree of protection. In PEVRI,river systems is relatively small, which may explain the total area is large (more than 73,000.00 ha) and therethe natural occurrence of the species in the two areas. are no significant threat records so far. In PNMP, we alsoRapadura Stream, in turn, is located in an isolated and did not detect effective threats; however, we warn thatdifficult access point in the upper section of the Pombo the place of occurrence of A. biotae is at the border of theRiver, in the Verde River basin. Between the Verde and protected area and, to a certain extent, more exposed to theIvinhema river basins, there are two other important interferences of the surroundings. Thus, it is important todrainage systems, the Pardo and Taquaruçu rivers, where strengthen surveillance in that area, in order to guaranteeichthyofaunal surveys are practically non-existent. It greater protection to the creek and, consequently, to theis possible that A. biotae occurs at more points among species that inhabit it.the known ones, but, so far, the large sampling gaps donot allow us to establish a hypothesis that explains the This classification reinforces the nationaldistribution pattern of the species. Its presence in the classification suggested by Oliveira et al. (2018). Todrainage over the watershed between the Paraná and avoid re-evaluation of this status, it is necessary to protectParaguay river basins (São Bento Stream) also raises the headwater areas, which are continuously impacted bythe possibility of its occurrence In the headwaters human activities. No information is available on the sizeof upper Paraguay River streams due to the shared of populations/subpopulations and the number of adultichthyofauna between drainages. This possibility of individuals within them, but the data to date suggest thatshared ichthyofauna between basins is reinforced by the A. biotae is a rare and infrequent species. Thus, there isrecent record in the upper Paraná River basin of Astyanax a need for more studies about the natural history of thelineatus (FERREIRA et al., 2017), a species previously species and the subpopulations recorded to date. Further,only known from the upper Paraguay River basin, which ichthyofauna sampling in the region should increase inwas caught in an area under similar conditions of contact order to reduce the sample gaps that still exist in Mato Grosso do Sul drainages.Revista Biotemas, 31 (4), dezembro de 2018

Conservation status of Astyanax biotae in Mato Grosso do Sul 57Acknowledgements e considerações sobre as demais espécies do gênero na bacia. Comunicações do Museu de Ciências e Tecnologia da PUC, We are grateful to Mr. Klaus Duarte Barreto, Série Zoologia, Porto Alegre, v. 13, p. 65-88, 2000.Casa da Floresta Environmental Consultancy, whoorganized the on-site inventory in PNMP and obtained GÉRY, J. Characoid of the World. New Jersey: T. F. H. Publ.,the authorization for data collection. We would like to 1977. 672 p.thank Gabriel Guedes, Gabriel Nakamura, Josileide deCastro Santana, Maria Angélica Galli Dutra, Mariana ICMBIO. Sistema Nacional de Unidades de Conservação.Oliveira, Marina Souza, Thais Buzetti Barbosa and Série Legislação ICMBio, Vol. 1. 2009. Brasília: ICMBio/MMA.Túlio Arantes, trainee students from the Ichthyology Available from: <http://www.icmbio.gov.br/portal/images/stories/Laboratory at UFMS/Campus Três Lagoas, for their comunicacao/legislacaoambientalvolume1.pdf>. Access in: 12participation while making collections. We also want to November 2017.thank Dr. Yzel Suárez Rondon (UEMS-CPUEMS) andDr. Francisco Langeani (UNESP-DZSJRP) for providing ICMBIO. Aplicação de critérios e categorias da UICN nathe samples from fish collections. avaliação da fauna brasileira. Versão 2. 2013. Brasília: ICMBio/ MMA, Available from: <http://www.icmbio.gov.br/cepsul/images/References stories/especies_ameacadas/publicacoes/2013_apostila_aplicacao_ criterios_categorias_UICN_versao_2.0.pdf>. Access in: 12BERTACO, V. A. Astyanax douradilho, a new characid fish November 2017.from the rio Tramandaí system, southern Brazil (Characiformes:Characidae). Zootaxa, Auckland, v. 3794, n. 3, p. 492-500, 2014. ICMBIO. Avaliação do risco de extinção da fauna brasileira. 2016. Available from: <http://www.icmbio.gov.br/portal/CASTRO, R. M. C.; VARI, R. P. Astyanax biotae, a new species of faunabrasileira/avaliacao-do-risco-de-extincao>. Access in: 12stream fish from the Rio Paranapanema basin, upper Paraná system, December 2017.southeastern Brazil (Ostariophysi: Characiformes: Characidae).Proceedings of the Biological Society of Washington, Washington, IMASUL. Plano de Manejo do Parque Estadual das Várzeasv. 117, n. 3, p. 330-338, 2004. do Rio Ivinhema. Campo Grande: Instituto de Meio Ambiente do Mato Grosso do Sul, 2008. Available from: <http://www.servicos.CETRA, M.; MATTOX, G. M. T.; FERREIRA, F. C.; GUINATO, ms.gov.br/imasuldownloads/PlanosdeManejo/planomanejoPEVRI.R. B.; SILVA, F. V.; PEDROSA, M. Headwater stream fish fauna pdf>. Access in: 28 November 2017.from the Upper Paranapanema River basin. Biota Neotropica,Campinas, v. 16, n. 3, p. 1-6, 2016. LANGEANI, F.; CASTRO, R. M. C.; OYAKAWA, O. T.; SHIBATTA, O. A.; PAVANELLI, C. S.; CASATTI, L. DiversidadeESCHMEYER, W. N.; FONG, J. D. Catalog of fishes. 2018. da ictiofauna do Alto Rio Paraná: composição atual e perspectivasAvailable in: <http://researcharchive.calacademy.org/research/ futuras. Biota Neotropica, Campinas, v. 7, n. 3, p. 1-17, 2007.ichthyology/catalog/SpeciesByFamily.asp>. Access in: 5 January2018. LIMA, F. C. T.; MALABARBA, L. R.; BUCKUP, P. A.; SILVA, J. F. P.; VARI, R. P.; HAROLD, A.; BENINE, R.; OYAKAWA,FERREIRA, F. S.; VICENTIN, W.; SÚAREZ, Y. R. Astyanax O.; PAVANELLI, C. S.; MENEZES, N.; LUCENA, C.;lineatus (Perugia, 1891) (Characiformes: Characidae): first record MALABARBA, C. S. L. M.; LUCENA, Z. M.; REIS, R. E.;in the upper Paraná River basin, Mato Grosso do Sul, Brazil. LANGEANI, F.; CASSATI, L.; BERTACO, V. A.; MOREIRA, C.;Checklist, Rio Claro, v. 13, n. 2, p. 1-4, 2017. LUCINDA, P. H. F. Genera Incertae sedis in Characidae. In: REIS, R. E.; KULLANDER, S. O.; FERRARIS JR., C. J. (Ed.). CheckFINK, W. L.; WEITZMAN, S. H. The so-called cheirodontin list of the freshwater fishes of South and Central America. Portofishes of Central America with descriptions of two new species Alegre: EDIPUCRS, 2003. p. 106-169.(Pisces: Characidae). Smithsonian Contributions to Zoology,Washington, v. 172, p. 1-46, 1974. LUCENA, C. A. S.; SOARES, H. G. Review of species of the Astyanax bimaculatus “caudal peduncle spot” subgroup sensuFROEHLICH, O.; CAVALLARO, M.; SABINO, J.; SÚAREZ, Y. Garutti & Langeani (Characiformes, Characidae) from the RioR.; VILELA, M. J. A. Checklist da ictiofauna do estado de Mato La Plata and Rio São Francisco drainages and coastal systems ofGrosso do Sul, Brasil. Iheringia, Série Zoologia, Porto Alegre, v. southern Brazil and Uruguay. Zootaxa, Auckland, v. 4072, n. 1, p.107 (supl.), p. 1-14, 2017. 101-125, 2016.GARUTTI, V. Descrição de Astyanax argyrimarginatus sp. n. MENEZES, N. A.; WEITZMAN, S. H.; OYAKAWA, O. T.;(Characiformes, Characidae) procedente da bacia do rio Araguaia, LIMA, F. C. T.; CASTRO, R. M. C.; WEITZMAN, M. J. PeixesBrasil. Revista Brasileira de Biologia, São Carlos, v. 59, n. 4, p. de água doce da Mata Atlântica: lista preliminar e comentários581-591, 1999. sobre conservação de peixes de água doce neotropicais. São Paulo: Museu de Zoologia, Universidade de São Paulo, 2007. 407 p.GARUTTI, V.; BRITSKI, H. A. Descrição de uma espécie novade Astyanax (Teleostei: Characidae) da bacia do alto rio Paraná OLIVEIRA, C. A. M. Revisão taxonômica do complexo de espécies Astyanax scabripinnis sensu Bertaco & Lucena (2006) (Ostariophysi: Characiformes: Characidae). 2017. 339 f. Tese (Doutorado em Ecologia de Ambientes Aquáticos Continentais) – Universidade Estadual de Maringá, Maringá. 2017. OLIVEIRA, C. A. M.; OLIVEIRA, A. G.; PAVANELLI, C. S. Expanding the geographical distribution of Astyanax biotae Castro Revista Biotemas, 31 (4), dezembro de 2018

58 M. J. A. Vilela et al.& Vari, 2004 (Characiformes, Characidae), with comments on its SEVERO-NETO, F.; VOLCAN, M. V. Population dynamics ofconservation status. Check List, Rio Claro, v. 14, n. 2, p. 387-392, Melanorivulus rossoi, a restricted geographic distribution killifish2018. species. Environmental Biology of Fishes, New York, v. 101, p. 245-255, 2018.RIBEIRO, J. F.; WALTER, B. M. T. Fitofisionomias do biomaCerrado. In: SANO, S. M.; ALMEIDA, S. P. (Ed.). Cerrado: ZEE-MS – ZONEAMENTO ECOLÓGICO-ECONÔMICO DOambiente e flora. Planaltina: EMBRAPA – CPAC, 1998. ESTADO DE MATO GROSSO DO SUL. Anexo I da Lei no 3.839,p. 89-166. de 28/12/2009, 2009. Available from: <http://193.43.36.109/docs/ pdf/bra116233AnnexI.pdf>. Access in: 14 November 2017.Revista Biotemas, 31 (4), dezembro de 2018

Biotemas, 31 (4): 57-63, dezembro de 2018 http://dx.doi.org/10.5007/2175-7925.2018v31n4p5597ISSNe 2175-7925Nutritional potential of a novel sea asparagus, Salicornia neei Lag., for human and animal diets Kennia Brum Doncato 1* César Serra Bonifácio Costa 2 Universidade Federal do Rio Grande, Instituto de Oceanografia 1 Programa de Pós-Graduação em Aquicultura 2 Laboratório de Biotecnologia de Halófitas Avenida Itália, Km 8, CEP 96203-900, Rio Grande – RS, Brasil * Corresponding author [email protected] Submetido em 30/04/2018 Aceito para publicação em 26/10/2018 Resumo Potencial nutricional de uma nova variedade de aspargo marinho, Salicornia neei Lag., para dietas humana e animal. O perfil mineral e o valor nutricional para a alimentação humana e animal de uma nova variedade de aspargo marinho brasileiro, Salicornia neei Lag., foram caracterizados por espectrofotometria. As plantas da progênie F4 da variedade pura denominada BTH1, cultivada com efluente salino da carcinicultura, possuem alto conteúdo mineral, particularmente N, K, P, Ca, Fe e Mn. A ingestão diária de 20, 200 e 5 g de caules secos de BTH1-F4 pode ser inserida e suplementada nas dietas, respectivamente, do homem, ovelhas e peixes cultivados comercialmente. Palavras-chave: Alimento saudável; Agricultura salina; Nutrição mineral Abstract The mineral profile and nutritional value of a novel variety of the Brazilian sea asparagus, Salicornia neei Lag., was characterized for feeding humans and animals using spectrophotometry. Plants of the F4 progeny of the purebred variety named BTH1 cultivated with saline shrimp farm effluent have high mineral content, particularly N, K, P, Ca, Fe and Mn. Daily intakes of 20, 200 and 5 g of dried shoots of BTH1-F4 could be added to and supplement human, sheep and commercial fish diets, respectively. Key words: Health food; Mineral nutrition; Saline agricultureEste periódico está licenciado Revista Biotemas, 31 (4), dezembro de 2018conforme Creative CommonsAtribuição 4.0 Internacional.

60 K. B. Doncato e C. S. B. CostaIntroduction al., 2015) and animal diets (D’OCA et al., 2012; COSTA et al., 2014a; BERTIN et al., 2014), biofuel production Food production from saline agriculture is (D’OCA et al., 2012; COSTA et al., 2014a) and use bypracticed in coastal areas, arid regions and on solodic the pharmaceutical industry (EPAGRI, 2008; BERTINsoils and human induced salinized soils, through the et al., 2014). Additionally, according to Doncato andconscious use of natural resources and for economic Costa (2018), green salt (i.e., biosalt) of this species isbenefit. This cultivation system requires using plants richer in some minerals than other species within thewith morphological and/or physiological mechanisms same genus; moreover, the amount of sodium chloride inthat tolerate high salinity levels (i.e., halophytes). Due commercial salt is three times more than S. neei (DIAS,to their high salt tolerance, high nutritional value and 2015). All information cited above was obtained fromlong tradition of consumption by humans, the genera non-selected wild plants and, except for an in vitro studySalicornia and Sarcocornia (Amaranthaceae, subfamily on the bioaccessibility of minerals of wild shoots of seaSalicorniodeae) are among the most promising halophyte asparagus ingested by humans (BERTIN et al., 2016), nocrops. Species of these genera have been cultivated study has evaluated the daily intake of S. neei requiredwith saline water (VENTURA et al., 2011; VENTURA; for human and animal diets.SAGI, 2013; COSTA et al., 2014b; VENTURA et al.,2015) and saline effluent from shrimp farms (COSTA, Since 2010, the Laboratório de Biotecnologia de2006; GREIS, 2009; COSTA et al., 2014a; DONCATO; Halófitas (BTH) at the Federal University of Rio GrandeCOSTA, 2018). They have typical succulent young (FURG, Rio Grande – RS, Brazil) has carried out ashoots and are sold in the gourmet food market because breeding program of S. neei by identifying and crossingof their peculiar salty taste and health value. Common pure lineages of ecomorphotypes native to the Patosnames for the two genera include sea asparagus, Lagoon estuary (RS) (FREITAS; COSTA, 2014). Theglasswort, pickleweed, and marsh samphire. Piirainen F4 progeny of the breeding program generated a novelet al. (2017) showed that Sarcocornia is paraphyletic in variety named BTH1, which is characterized by a redrelation to Salicornia and proposed a new taxonomic shoot phenotype at maturity, prostrate growth form andclassification, merging Sarcocornia in three subgenera high reproductive investment. Recently, Steffen et al.under Salicornia. In the present study, we followed the (2015), in a molecular-phylogenetic analysis, pointednomenclature proposed by these authors. out that the prostrate growth form arose multiple times in Salicornia and Sarcocornia and might represent different A recent phylogenetic analysis using ETS stages of speciation. Plant field trials of this novel S. neeisequences confirmed the identity of Brazilian are needed to evaluate its nutritional quality under salineaccessions of sea asparagus as Salicornia neei Lag. irrigation. Thus, in order to characterize the mineral(COSTA et al., 2018). This species is widely distributed content and the nutritional potential of this novel varietyand occurs along the coasts of Brazil, Uruguay and for feeding humans and animals (i.e., sheep and fish),Argentina, as well as on the Pacific coast of Chile we analyzed shoot macrominerals and microminerals ofand Peru. Due to its reduced morphology and great a field crop irrigated with saline effluent from shrimpphenotypic plasticity, S. neei was previously described farming and assessed how well BTH1 met daily intakeas many taxa [synonym of Sarcocornia ambigua requirements of minerals stated by the Institute of(Michx.) M.A. Alonso & M.B. Crespo, Salicornia Medicine – IOM (U.S. National Academy of Medicine)gaudichaudiana Moq., Sarcocornia perennis (Miller) and the National Research Council (NRC).Scott or Sarcocornia fruticosa (L.) Scott] (ALONSO;CRESPO, 2008; STEFFEN et al., 2015; COSTA; Material and MethodsHERRERA, 2016). In the last decade, studies of S.neei have highlighted the high nutritional and chemical Seeds of the S. neei F4 progeny of the lineagequality of its seeds and shoots, as well as its potential for BTH1 (BTH1-F4) were obtained from germplasmhuman (COSTA, 2006; BERTIN et al., 2014; TIMM etRevista Biotemas, 31 (4), dezembro de 2018

Nutritional potential of sea asparagus diets 61at the Laboratório de Biotecnologia de Halófitas and was the main source of nutrients and water for the S.germinated following the protocol of Freitas and neei plants.Costa (2014). Seedlings were maintained for a totalof 25 weeks in an unheated greenhouse before being At the end of cultivation (June 2014), five plantstransplanted at the cultivation site. were randomly chosen and harvested just above ground level, bagged and transported to the laboratory. From February to June 2014, plants of BTH1-F4 Shoot samples were washed to remove soil, weighedwere grown in a plot located at the Marine Station of on a precision scale to determine the fresh weight,Aquaculture (EMA, FURG) in Rio Grande – RS, Brazil. oven dried at 60°C for 48 h and weighed again toA total of 20 plants were distributed in two adjacent determine the dry weight (DW). The macromineralsrows spaced 60 cm apart with 25 cm between each and microminerals were determined from the dryplant. The plants were irrigated by filling up drainage mass (n = 5) of BTH1-F4 shoots, according to Tedescoditches between the rows four times a day (25 L per et al. (1995), using spectrophotometry. The shootminute for 15 minutes) with saline effluent from a tank biomass chemical analyses were performed by theof Litopenaeus vannamei (stocked with 120 shrimp.m2) Departamento de Solos of Federal University of Pelotascultivated in a Biofloc Technology System (BFT). The (UFPel, RS, Brazil).measured water parameters during cultivation (mean ±standard error; n = 9) were the following: salinity 7.67 Results± 0.27 g.L-1 NaCl (≈ 11.40 dS.m-1), pH 8.42 ± 0.01,dissolved oxygen 8.05 ± 0.04 mg.L-1, nitrate 4.00 ± Shoots of S. neei had an average succulence of5.66 mg.L-1, total ammonia nitrogen 0.04 ± 0.03 mg.L-1 86.6% water. The mineral composition of dry shootsand phosphate 1.21 ± 0.04 mg.L-1.The soil of the plot of the novel S. neei is shown in Figure 1 and representswas Orthic Quartzarenic Neosol and the saline effluentFIGURE 1: Photograph of the novel Salicornia neei BTH1-F4 and average values (± standard-error) of macro- and microminerals in its shoot (DW: dry weight of shoot). The comparison of the mineral profile of S. neei BTHRe1v-isFta4Biwoteitmhast,h3e1 (d4a),ildyezemmibnreordael 2018requirement standards for humans (IOM, 2005) and farm animals, such as sheep (NRC, 1985)and fish (particularly carp and tilapia; NRC, 1993), highlights the high nutritional quality of

62 K. B. Doncato e C. S. B. Costaa great food source of minerals. Notably, this species subfamily Salicorniodeae (i.e., Salicornia bigelovii andaccumulated a considerable amount of minerals, Salicornia stricta) and vegetables, such as asparagusparticularly N, P, K, Ca, Fe and Mn. (Asparagus officinalis) and spinach (Spinacia oleracea) (N = 11.6-53.0 g.kg-1 DW; P = 1.6-7.8 g.kg-1 DW; The comparison of the mineral profile of S. neei K = 7.0-32.8 g.kg-1 DW and Ca = 2.1-12.5 g.kg-1 DW)BTH1-F4 with the daily mineral requirement standards (GORHAM; GORHAM, 1955; MAKUS, 1994; LU etfor humans (IOM, 2005) and farm animals, such as al., 2010; SHEIKHI; RONAGHI, 2012). In contrast, thesheep (NRC, 1985) and fish (particularly carp and tilapia; average Mg content in BTH1-F4 was near (6.9 g.kg-1NRC, 1993), highlights the high nutritional quality of DW) (MEDINA et al., 2008) or lower than wild S. neeithis plant obtained from relatively small recommended and other Salicorniodeae species (10.2-11.4 g.kg-1 DW)daily intakes (Table 1). (LU et al., 2010; BERTIN et al., 2014).Discussion The micromineral composition of BTH1-F4 shoots showed high levels of Fe and Mn (Figure 1). Except Most minerals that were quantified in the shoots for Fe content in spinach (Fe = 249.1 mg.kg-1 DW)of S. neei BTH1-F4 cultivated with saline effluent (SHEIKHI; RONAGHI, 2012), which was approximatelyirrigation showed higher concentrations than tissues 20% higher than that of BTH1-F4, the average contentsof wild plants of this species and common vegetables. of these minerals in the novel variety were higher thanBTH1-F4 showed higher concentrations of N, P, K and found in the Salicorniodeae species and vegetables citedCa than wild plants of S. neei (N = 15.4 g.kg-1 DW; above (Fe = 50.0-99.9 mg.kg-1 DW and Mn = 20.0-104.8P = 1.0 g.kg-1 DW; K = 9.7-15.8 g.kg-1 DW and Ca = mg.kg-1 DW) (GORHAM; GORHAM, 1955; MAKUS,2.4-4.6 g.kg-1 DW) (MEDINA et al., 2008; BERTIN 1994; LU et al., 2010; SHEIKHI; RONAGHI, 2012).et al., 2014), and ranked in the mid-upper range of The concentrations of Cu and Zn in BTH1-F4 shootsthese macrominerals compared to other species of the were lower than those cited for cultivated plants of S. bigelovii (Cu = 7.9 mg.kg-1 DW and Zn = 35.0 mg.kg-1TABLE 1: Daily mineral requirement standards and the percentage of these recommended intakes (PI; inside brackets) for an adult man, an adult sheep and a commercial-sized fish supplied by the consumption of dried shoots of S. neei BTH1-F4. The amounts of dry shoot biomass of S. neei considered for estimation of man, sheep and fish PIs were 20, 200 and 5 g, respectively, and their salt content should not adversely affect growth and feed efficiency of these organisms. Diet Macrominerals (g.kg-1) Microminerals (mg.kg-1) P K CaMan 1 N 0.70 4.70 1.20 Mg Fe Mn Cu ZnPI (%) 9.74* (9) (8) (14) 0.42Sheep 2 2.70 6.50 5.10 (33) 8.00 2.30 0.90 11.00PI (%) (4) (22) (60) (34) 1.50Fish 3,4 16.52* 0.17 0.18 0.21 (92) (48) (106) (7) (3)PI (%) (9) (55) (20) 0.02 (23) (208) 40.00 30.00 9.00 26.50 1.75* (97) (82) (7) (14) (6) 4.50 0.39 0.09 0.75 (22) (157) (18) (13)PI = Percentage of recommended mineral intake supplied. * A protein-to-nitrogen conversion factor of 5.75 for plant foodswas applied (ANVISA, 2003). 1 Daily mineral requirement standards for an adult man (over 51 years old) (IOM, 2005).2 Daily mineral requirement standards for an adult sheep (50 kg; consumption of 2% body weight of dry matter per day)(NRC, 1985; LEE, 2014). 3 Daily mineral requirement standards for a commercial-sized fish (1 kg; consumption of 3% bodyweight of dry matter per day) (NRC, 1993). 4 Combined values for carp and tilapia, except K (chinook salmon).Revista Biotemas, 31 (4), dezembro de 2018

Nutritional potential of sea asparagus diets 63DW) (LU et al., 2010), A. officinalis (Cu = 18.0 mg.kg-1 intake of 10 mg (WHO, 1996). Thus, S. neei BTH1-F4DW and Zn = 77.3 mg.kg-1 DW) (MAKUS, 1994) and S. had an average content several times lower than the limitoleracea (Cu = 9.9 mg.kg-1 DW and Zn = 108.6 mg.kg-1 for the Brazilian market of fruits, vegetables and oilseedsDW) (SHEIKHI; RONAGHI, 2012). in natura and in industry. The daily consumption of 20 g of dried shoots Since adult sheep could intake a large amount ofof the BTH1-F4 progeny would partially supply the salt enriched S. neei BTH1-F4 biomass, 200 g of driedrecommended daily intake of P (9%), K (8%), Ca BTH1-F4 shoots can meet approximately 60% of its K(14%), Mg (33%), Fe (48%) and Mn (100%) for an maintenance requirement, while 5 g of dried BTH1-F4adult man (over 51 years old) (IOM, 2005) (Table 1). shoots can meet half of K requirement for fish (Table 1).Moreover, this amount of shoot mass would not exceed Potassium is the third most abundant mineral in thethe recommended daily intake of salt for humans (less human body and often needs to be supplemented in somethan 2 g.day-1) (WHO, 2012), since Na content in S. ruminant diets (MCDOWELL, 2003; MASTERS et al.,neei shoots ranges between 87-139 g.kg-1 DW (BERTIN 2005). Regarding Ca, P is one of the largest mineralet al., 2014). Young sheep (≈ 35 kg) would be able to constituents of bones, and its deficiency in vertebrateconsume 74-90 g Na per day (MASTERS et al., 2005) animals and young people results in rickets and in adultsand these amounts do not adversely affect the growth causes osteomalacia (WHO, 1998; MCDOWELL, 2003).and feeding efficiency of salt tolerant varieties of carp For all organisms, P is used in the construction of geneticand tilapia (NRC, 1993). material (DNA and RNA) and in energy storage (ATP), and the daily consumption of dried S. neei BTH1-F4 The recommended daily Fe and Mn intakes for an shoots for a sheep (200 g DW) and a commercial-sized fishadult human are 8.0 mg and 2.3 mg (IOM, 2005), and (5 g DW) can meet 22% and 9% of their P requirement,half of Fe and the full amount of Mn can be reached respectively. In monogastric animals and humans, Mgby ingesting approximately 20 g DW of BTH1-F4 deficiencies are rare, but in ruminants this nutritionalshoots. Deficiency in iron is probably the most common deficiency is related to hypomagnesemia (MCDOWELL,nutritional deficiency disorder in humans, causing 2003). The high Ca and Mg content in S. neei BTH1-F4anemia (MCDOWELL, 2003; FAO; WHO, 2004). Mn means a daily consumption of 200 g of BTH1-F4 dryis an element that has low toxicity (oral ingestion) to matter would supply 34% of the Ca and 92% of the Mghumans (WHO, 1996), but its deficiency in domestic required for an adult sheep, as well as 20% and 200%animals causes reduced appetite and growth, impairs the for fish, respectively. Concerning microminerals, theseiron metabolism and alters brain function. Due to the Zn amounts of dried BTH1-F4 shoots would supply roughlylevels in BTH1-F4 tissues, high intakes of plant biomass the daily needs of Fe and Mn for an adult sheep and exceedwould be necessary to meet the daily requirements of the Mn requirement for a commercial-sized fish. Overall,humans (11 mg) (IOM, 2005), but its use as a supplement the novel S. neei BTH1-F4 has a rich mineral profile thatin animal feed is possible. Zn deficiency in humans and could have great potential for feeding both humans andanimals results in reduced appetite, lethargic growth, skin farm animals, particularly sheep.abnormalities and impaired reproduction (WHO, 1996;MCDOWELL, 2003; FAO; WHO, 2004). In humans, ReferencesCu is needed in very small amounts (daily intake of0.9 mg), according to IOM (2005), and its deficiency is ALONSO, M. A.; CRESPO, M. B. Taxonomic and nomenclaturalassociated with anemia and hematologic abnormalities notes on South American taxa of Sarcocornia (Chenopodiaceae).(WILLIAMS, 1983; WHO, 1996). Excess Cu is toxic Annales Botanici Fennici, Helsingin, v. 45, n. 4, p. 241-254,(WHO, 1996) and, according to the Brazilian Ministry 2008.of Health (BRASIL, 1998), the Cu concentration level ANVISA – AGÊNCIA NACIONAL DE VIGILÂNCIAin vegetables for sale corresponds to 10 mg.kg-1 FW; the SANITÁRIA. MINISTÉRIO DA SAÚDE. Resolução RDC n. 360,World Health Organization defines a maximum Cu daily de 23 de dezembro de 2003. Diário Oficial da União, n. 251, de 26 dez. 2003. Seção 1, p. 33. Revista Biotemas, 31 (4), dezembro de 2018

64 K. B. Doncato e C. S. B. CostaBERTIN, R. B.; GONZAGA, L. V.; BORGES, G. S. C.; FAO – FOOD AND AGRICULTURE ORGANIZATIONAZEVEDO, M. S.; MALTEZ, H. F.; HELLER, M.; MICKE, G. OF THE UNITED NATIONS; WHO – WORLD HEALTHA.; TAVARES, L. B. B.; FETT, R. Nutrient composition and, ORGANIZATION. Vitamin and mineral requirements inidentification/quantification of major phenolic compounds in human nutrition. Geneva: WHO, 2004. 341 p.Sarcocornia ambigua (Amaranthaceae) using HPLC–ESI-MS/MS.Food Research International, Amsterdam, v. 55, n. 1, p. 404-411, FREITAS, R. F.; COSTA, C. S. B. Germination responses to salt2014. stress of two intertidal populations of the perennial glasswort Sarcocornia ambigua. Aquatic Botany, Gainesville, v. 117, n. 1,BERTIN, R. L.; MALTEZ, H. F.; GOIS, J. S.; BORGES, D. L. p. 12-17, 2014.G.; BORGES, G. S. C.; GONZAGA, L. V.; FETT, R. Mineralcomposition and bioaccessibility in Sarcocornia ambigua using GREIS, G. Cultivo de Salicornia gaudichaudiana Moq. irrigadaICP-MS. Journal of Food Composition and Analysis, Grangues, com efluente de camarão no clima temperado na costa sulv. 47, n. 1, p. 45-51, 2016. do Brasil. 2009. 63 f. Dissertação (Mestrado em Oceanografia Biológica) – Universidade Federal do Rio Grande, Rio Grande.BRASIL – MINISTÉRIO DA SAÚDE. Portaria n. 685, de 27 de 2009.agosto de 1998. Aprova o Regulamento Técnico: “Princípios Geraispara o Estabelecimento de Níveis Máximos de Contaminantes GORHAM, A. V.; GORHAM, E. Iron, manganese, ash, andQuímicos em Alimentos” e seu Anexo: “Limites máximos de nitrogen in some plants from salt marsh and shingle habitats.tolerância para contaminantes inorgânicos”. Diário Oficial da Annals of Botany, Oxford, v. 19, n. 76, p. 571-577, 1955.República Federativa do Brasil, Brasília, 28 ago. 1998. Seção 1,p. 28-29. IOM – INSTITUTE OF MEDICINE. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol,COSTA, C. S. B. A Salicórnia: uma planta que pode ser utilizada no protein, and amino acids. Washington: The National Academiescultivo integrado com o camarão. Panorama da Aquicultura, Rio Press, 2005. 1358 p.de Janeiro, v. 98, n. 1, p. 28-33, 2006. LEE, I. C. Sheep nutrition and feeding. In: LEE, I. C. (Ed.). AnimalCOSTA, C. S. B.; BONILLA, O. H.; OLIVEIRA, R. D.; ALVES, nutrition handbook. Cap. 16. Auburn: Auburn University, 2014.P. R.; LOPES, E. F.; LUCAS, D. S. Influence of different saline p. 520-540.irrigation regimes on soil electrical conductivity and crop yieldof Sarcocornia ambigua in the semi-arid region of NE Brazil. In: LU, D.; ZHANG, M.; WANG, S.; CAI, J.; ZHOU, X.; ZHU, C.INOVAGRI INTERNATIONAL MEETING, II, 2014, Fortaleza. Nutritional characterization and changes in quality of SalicorniaAnnals… Fortaleza: INOVAGRI, 2014b. p. 3234-3243. bigelovii Torr. during storage. LWT – Food Science and Technology, Zurich, v. 43, n. 3, p. 519-524, 2010.COSTA, C. S. B.; HERRERA, O. B. Halophytic life in Braziliansalt flats: biodiversity, uses and threats. In: KHAN, M. A.; BOËR, MAKUS, D. J. Mineral nutrient composition of green and whiteB.; ȪZTURK, M.; CLÜSENER-GODT, M.; GUL, B.; BRECKLE, Asparagus spears. HortScience, Alexandria, v. 29, n. 12, p. 1468-S. W. (Ed.). Sabkha ecosystems volume V: the Americas. Cap. 2. 1469, 1994.Berlin: Springer, 2016. p. 11-27. MASTERS, D. G.; RINTOUL, A. J.; DYNES, R. A.; PEARCE, K.COSTA, C. S. B.; KADEREIT, G.; FREITAS, G. P. M. Molecular L.; NORMAN, H. C. Feed intake and production in sheep fed dietsmarkers indicate the phylogenetic identity of southern Brazilian high in sodium and potassium. Australian Journal of Agriculturalsea asparagus: first record of Salicornia neei Lag. in Brazil. Research, Melbourne, v. 56, n. 5, p. 427-434, 2005.Rodriguésia, Rio de Janeiro, 2018 (In press). MCDOWELL, L. R. Minerals in animal and human nutrition.COSTA, C. S. B.; VICENTI, J. R. M.; MORÓN-VILLARREYES, Amsterdam: Elsevier Science B.V., 2003. 660 p.J. A.; CALDAS, S.; CARDOSO, L. V.; FREITAS, R. F.; D’OCA,M. G. M. Extraction and characterization of lipids from Sarcocornia MEDINA, E.; FRANCISCO, A. M.; WINGFIELD, R.; CASAÑAS,ambigua meal: a halophyte biomass produced with shrimp farm O. L. Halofitismo en plantas de la costa caribe de Venezuela:effluent irrigation. Anais da Academia Brasileira de Ciências, halófitas y halotolerantes. Acta Botánica Venezuélica, Caracas, v.Rio de Janeiro, v. 86, n. 2, p. 935-943, 2014a. 31, n. 1, p. 49-80, 2008.DIAS, G. Sal verde é mais saudável. Agropecuária Catarinense, NRC – NATIONAL RESEARCH COUNCIL. NutrientFlorianópolis, v. 28, n. 1, p. 29-31, 2015. requirements of sheep. Washington: National Academy Press, 1985. 112 p.D’OCA, M. G. M.; MORÓN-VILLARREYES, J. A.; LEMÕES, J.S.; COSTA, C. S. B. Fatty acids composition in seeds of the South NRC – NATIONAL RESEARCH COUNCIL. NutrientAmerican glasswort Sarcocornia ambigua. Anais da Academia requirements of fish. Washington: National Academy Press, 1993.Brasileira de Ciências, Rio de Janeiro, v. 84, n. 3, p. 865-870, 128 p.2012. PIIRAINEN, M.; LIEBISCH, O.; KADEREIT, G. Phylogeny,DONCATO, K. B.; COSTA, C. S. B. Growth and mineral biogeography, systematics and taxonomy of Salicornioideaecomposition of two lineages of the sea asparagus Sarcocornia (Amaranthaceae/Chenopodiaceae) – A cosmopolitan, highlyambigua irrigated with shrimp farm saline effluent. Experimental specialized hygrohalophyte lineage dating back to the Oligocene.Agriculture, Cambridge, v. 54, n. 3, p. 399-416, 2018. Taxon, Vienna, v. 66, n. 1, p. 109-132, 2017.EPAGRI – EMPRESA DE PESQUISA AGROPECUÁRIA E SHEIKHI, J.; RONAGHI, A. Growth and macro and micronutrientsEXTENSÃO RURAL DE SANTA CATARINA. Panicêutico concentration in spinach (Spinacia oleracea L.) as influenced by– você sabe o que isto significa? Agropecuária Catarinense, salinity and nitrogen rates. International Research Journal ofFlorianópolis, v. 21, n. 2, p. 13, 2008. Applied and Basic Sciences, Tonekabon, v. 3, n. 4, p. 770-777, 2012.Revista Biotemas, 31 (4), dezembro de 2018

Nutritional potential of sea asparagus diets 65STEFFEN, S.; BALL, P.; MUCINA, L.; KADEREIT, G. Phylogeny, VENTURA, Y.; SAGI, M. Halophyte crop cultivation: the case ofbiogeography and ecological diversification of Sarcocornia Salicornia and Sarcocornia. Environmental and Experimental(Salicornioideae, Amaranthaceae). Annals of Botany, Oxford, v. Botany, Paris, v. 92, n. 1, p. 144-153, 2013.115, n. 3, p. 353-368, 2015. VENTURA, Y.; WUDDINEH, W. A.; MYRZABAYEVA, M.;TEDESCO, M. J.; GIANELLO, C.; BISSANI, C. A.; BOHNEN, H.; ALIKULOV, Z.; KHOZIN-GOLDBERG, I.; SHPIGEL, M.;VOLKWEISS, S. J. Análise de solo, plantas e outros materiais. SAMOCHA, T. M.; SAGI, M. Effect of seawater concentrationPorto Alegre: Departamento de Solos – Universidade Federal do on the productivity and nutritional value of annual Salicornia andRio Grande do Sul, 1995. 174 p. perennial Sarcocornia halophytes as leafy vegetable crops. Scientia Horticulturae, Amsterdam, v. 128, n. 3, p. 189-196, 2011.TIMM, T. G.; SILVA JÚNIOR, A. A.; BERTIN, R. L.; TAVARES,L. B. B. Processamento de conservas de Sarcocornia perennis. WHO – WORLD HEALTH ORGANIZATION. Trace elements inAgropecuária Catarinense, Florianópolis, v. 28, n. 1, p. 97-102, human nutrition and health. Geneva: WHO, 1996. 361 p.2015. WHO – WORLD HEALTH ORGANIZATION. Guideline: sodiumVENTURA, Y.; ESHEL, A.; PASTERNAK, D.; SAGI, M. The intake for adults and children. Geneva: WHO, 2012. 46 p.development of halophyte-based agriculture: past and present.Annals of Botany, Oxford, v. 115, n. 3, p. 529-540, 2015. WILLIAMS, D. M. Copper deficiency in humans. Seminars in Hematology, Philadelphia, v. 20, n. 2, p. 118-128, 1983. Revista Biotemas, 31 (4), dezembro de 2018



Biotemas, 31 (4): 65-69, dezembro de 2018 http://dx.doi.org/10.5007/2175-7925.2018v31n4p6675ISSNe 2175-7925 Comunicação BreveSais inorgânicos no controle em pós-colheita de Penicillium digitatum (Pers.) Sacc. em laranja Anderson Eduardo Brunetto * Keilor da Rosa Dorneles Cassio Muller Leandro José DallagnolUniversidade Federal de Pelotas, Faculdade de Agronomia Eliseu Maciel Trindade, CEP 96010-900, Pelotas – RS, Brasil * Autor para correspondência [email protected] Submetido em 26/07/2018 Aceito para publicação em 03/11/2018Resumo O objetivo da pesquisa foi avaliar o efeito da aplicação dos sais inorgânicos cloreto de potássio (KCl), hidróxido de potássio (KOH) e silicato de potássio (K2SiO3) sobre laranja no controle do bolor verde causado por Penicillium digitatum. O delineamento experimental utilizado foi inteiramente casualizado com cinco tratamentos e quatro repetições, cada uma composta por vinte frutos. Os frutos foram lavados e desinfestados, após 24 h foram feridos com uma agulha (2-3 mm de profundidade) e tratados com os sais inorgânicos ou água destilada (controle) e 2 h após, inoculados por meio da deposição de 15 μL da suspensão de esporos de P. digitatum. Às 96, 120 e 245 horas após a inoculação (hai) foram realizadas as avaliações de incidência do bolor verde, taxa da expansão da lesão, tamanho da lesão e da área esporulante. Às 245 hai, entre os sais, o KOH e o K2SiO3 foram os mais efetivos, afetando todas as variáveis avaliadas, reduzindo a incidência da doença em 80% e 36%, respectivamente, quando comparados à testemunha. Contudo, o tratamento com o KOH afetou a qualidade visual dos frutos, ocasionando enrugamento e desidratação da casca. Desse modo, conclui-se que, entre os sais inorgânicos testados, o K2SiO3 (50 g.L-1) apresentou redução no bolor verde sem comprometer a qualidade visual do fruto, podendo ser incluído como uma medida complementar no manejo da doença. Palavras-chave: Bolor verde; Citricultura; Controle de podridões; Minerais; SilícioAbstract Inorganic salts in the postharvest control of Penicillium digitatum (Pers.) Sacc. in orange. The objective of this research was to evaluate the effect of treating oranges with potassium chloride (KCl), potassium hydroxide (KOH) and potassium silicate (K2SiO3) for green mold caused by Penicillium digitatum. The experimental design was completely randomized with five treatments and four replications, each with twenty fruits. For the experiment, the fruits were washed and superficially disinfected. After 24 hours, the fruits were pierced with a needle (2-3 mm deep) and treated with inorganic salts or distilled water (control) and, 2 hours later, inoculated with 15 μL of P. digitatum spore suspension. Green mold incidence, rate ofEste periódico está licenciado Revista Biotemas, 31 (4), dezembro de 2018conforme Creative CommonsAtribuição 4.0 Internacional.

68 A. E. Brunetto et al. lesion expansion, lesion size and sporulation area were evaluated at 96, 120 and 245 hours after inoculation (hai). At 245 hai, the KOH and K2SiO3 (50 g.L-1) treatments were the most effective, affecting all evaluated variables and reducing the disease incidence by 80% and 36%, respectively, compared to the control. However, the KOH treatment caused wrinkling and dehydrated the peel, affecting the visual quality of the fruits. In conclusion, among the tested inorganic salts, the K2SiO3 treatment (50 g.L-1) reduced the green mold in the citrus without negatively effecting fruit appearance, which indicates that this treatment is an option as a complementary measure to manage the disease. Key words: Citriculture; Control of rot; Green mold; Minerals; SiliconIntrodução biótica quanto abiótica têm demonstrado resultados promissores no controle de doenças de pós-colheita Entre as doenças em pós-colheita dos citros, o (BENATO et al., 2018). Esses compostos têm apresen-bolor verde [Penicillium digitatum (Pers.) Sacc] é a tado ação no patógeno de maneira direta bem comomais importante, e se encontra presente em todos os indireta pela potencialização de mecanismos de defesapaíses produtores (GHOOSHKHANEH et al., 2018). do hospedeiro ao agente patogênico (SPADARO;O fungo P. digitatum causa podridão mole em frutos, DROBY, 2016).que se inicia por pequenas anasarcas na superfície dacasca que, rapidamente, progridem até tomarem todo Nesse contexto, o objetivo da pesquisa foi avaliaro fruto. O fungo desenvolve um micélio branco sobre o efeito da aplicação dos sais inorgânicos cloreto deo tecido afetado, que depois é revestido por uma densa potássio, hidróxido de potássio e silicato de potássiomassa de esporos de cor verde. Uma vez alterada sua sobre laranja no controle do bolor verde causado porconsistência, o fruto desprende um odor característico P. digitatum.e torna-se impróprio para o consumo. Em adição,P. digitatum produz várias toxinas, como a patulina, que Laranjas, cv. Valência, foram desinfestadascontamina sucos feitos de frutos parcialmente infectados superficialmente com hipoclorito de sódio (1%) por 120pelo patógeno, provocando vários distúrbios como segundos, em seguida lavadas por três vezes com águaagitação, ulceração, vômitos e inflamação intestinal em deionizada por 60 segundos e deixadas sob bancada aquem os consome (FISCHER et al., 2007). 25°C por 24 h. Em seguida, em cada fruto foi realizado um ferimento, na região equatorial (diâmetro de 0,5 Para o controle do bolor verde em citros são mm e profundidade de 2 a 3 mm), com auxílio de umarecomendadas práticas culturais visando à redução do agulha estéril, que foi marcado com um círculo cominóculo no campo, como eliminação de frutos infectados, uma caneta esferográfica. Posteriormente, foi realizadacuidados na colheita e no transporte para evitar a aplicação dos tratamentos: cloreto de potássio 15 g.L-1ferimentos e higienização constante dos equipamentos. (KCL, Vetec, Brasil), hidróxido de potássio 15 g.L-1Não obstante, o tratamento químico, com fungicidas do (KOH, Vetec, Brasil) e silicato de potássio nas dosesgrupo benzimidazol e imidazol em pré e/ou pós-colheita, 15 g.L-1 e 50 g.L-1 (K2SiO3, PQ Corporation), atravésé o método mais utilizado (GHOOSHKHANEH et al., da imersão dos frutos por dois minutos nas respectivas2018). soluções de cada composto. Como controle foram utilizados frutos tratados com água deionizada. Após Ademais, o mercado nacional e internacional de o tratamento, os frutos foram deixados para secar emfrutas tem buscado reduzir o uso de agrotóxicos em condições ambientais por 2 h. Em seguida, os frutospós-colheita e estimular a adequação dos produtores foram colocados em bandejas plásticas (8 cm de alturae comerciantes à produção integrada de frutas (PIF) x 31 cm de largura x 50 cm de comprimento) e foi(FISCHER et al., 2007). Diante disso, a comunidade realizada sua inoculação por meio da deposição decientífica tem buscado formas alternativas de controle 15 µL da suspensão de esporos (1x105 conídios. mL-1) dedessa doença, sendo que compostos tanto de origemRevista Biotemas, 31 (4), dezembro de 2018

Sais inorgânicos no controle em pós-colheita de P. digitatum em laranja 69P. digitatum. O fungo foi isolado de frutos sintomáticos experimento foi repetido duas vezes. Os dados foramcoletados em pomar comercial da região de Pelotas/RS submetidos à análise de variância (ANOVA) e as médiase cultivado em meio de cultura batata-dextrose-agar dos tratamentos comparadas pelo teste Tukey (p ≤ 0.05).(BDA) (Fluka, Sigma, USA) a 25 ± 1°C e fotoperíodode 12 h. Após inoculação, os frutos foram mantidos a Os sais inorgânicos reduziram a incidência do bolor24 ± 1ºC e umidade relativa 90 ± 5%. verde, exceto o cloreto de potássio a partir das 120 hai (Figura 1). A maior redução na incidência da doença, As variáveis avaliadas foram incidência do bolor de 100% às 96 hai até 80% às 245 hai, comparadaverde, taxa da expansão da lesão (r) e tamanho da lesão à testemunha, foi obtida com hidróxido de potássio(TFL) e da área esporulante (TLE).Aincidência da doença (Figura 1).foi avaliada às 96, 120 e 245 horas após a inoculação (hai)e expressa em porcentagem de frutos sintomáticos em Contudo, o tratamento com o hidróxido de potássiorelação ao número total de frutos do tratamento. A taxa de afetou a qualidade visual dos frutos, ocasionandoexpansão da lesão (r), indicada pelo coeficiente angular enrugamento, desidratação e branqueamento da casca.da regressão linear foi calculada a partir das mensurações Os tratamentos com silicato de potássio, especialmentediárias do tamanho da lesão, até as 245 hai, utilizando na dose de 50 g.L-1, reduziram a incidência da doençapaquímetro eletrônico digital (Stainless, Hardened, de 82% às 96 hai até 36% às 245hai.China). O tamanho final da lesão (TFL) foi medido às 245hai, em todas as laranjas que apresentavam os sintomas A taxa da expansão da lesão e o TFL somentede cada tratamento. O tamanho final da área esporulante foram reduzidos nos tratamentos com hidróxido de(TLE) foi obtida de forma semelhante ao TFL, porém potássio, em 46 e 44%, respectivamente, e o silicato deconsiderando somente a área com esporos do patógeno. potássio, na dose 50 g.L-1, em 29 e 26%, respectivamente, comparados ao controle (Tabela 1). A área com O delineamento experimental foi inteiramente esporulação do fungo somente foi reduzida, em 77%,casualizado com cinco tratamentos e quatro repetições, pelo tratamento com hidróxido de potássio, comparadasendo cada repetição composta por vinte frutos. O ao controle (Tabela 1).FIGURA 1: Incidência (%) de bolor verde em frutos de laranja da cultivar Valencia, tratados como cloreto de potássio (KCl, 15 g.L-1), hidróxido de potássio (KOH, 15 g.L-1) e silicato de potássio (K2SiO3, 15 g.L-1 e 50 g.L-1), às 96, 120 e 145 h após a inoculação. Médias seguidas pela mesma letra, em cada horário de avaliação, não diferem entre si pelo teste de Tukey (p ≤ 0,05). Água a ab100 KOH a bc c 80 a K2SiO3 (15 g. L-1) ab K2SiO3 (50 g. L-1)Incidência (%) KCl bc 60 b 40 c c d d 20 c 120 245 0d 96 Horas após a inoculação Revista Biotemas, 31 (4), dezembro de 2018

70 A. E. Brunetto et al. Os resultados apresentados neste estudo demonstram os patógenos, por meio da alteração do pH e/ou aumento do potencial osmótico na superfície do hospedeiro,que o tratamento em pós-colheita com sais inorgânicos, ambas condições prejudiciais às células fúngicas, o que podem levar ao seu colapso, comprometendo acloreto de potássio (KCl), hidróxido de potássio (KOH) adesão e a germinação de conídios e o desenvolvimento de hifas (DELIOPOULUS et al., 2010; JABNOUN-e silicato de potássio (K2SiO3), reduziram a severidade KHIAREDDINE et al., 2016). No caso do silicato dedo bolor verde causado por P. digitatum. Entre estes, potássio, além do provável efeito no pH e no potencial osmótico na superfície do hospedeiro, pode tambémo KOH seguido do K2SiO3 (50 g.L-1) foram os que ter a contribuição da barreira física formada pelaapresentaram as maiores reduções na incidência e no polimerização do sal acima da cutícula, conforme já reportado em outros patossistemas (RODRIGUES;progresso da doença. DATNOFF, 2015).TABELA 1: Taxa da expansão da lesão (r), tamanho final No entanto, os benefícios demonstrados pela da lesão (TFL) e da área esporulante (TLE) aplicação dos sais no controle da doença podem ser em frutos de laranja tratados com hidróxido mitigados devido ao comprometimento da aparência do de potássio, cloreto de potássio e silicato fruto, a qual está entre os atributos de qualidade mais de potássio e inoculados com Penicillium exigidos pelo consumidor. Dessa forma, a depreciação digitatum. da qualidade visual, causada pela mudança de coloração e pelo enrugamento da casca pela aplicação do KOH,Tratamentos r TFL TLE inviabiliza o uso desse composto, na dose testada, para (mm) (mm) o controle do bolor verde em citrus. Controle 0,44 a 46,47 a 42,16 a KOH 0,24 c 26,03 c 9,76 b Assim, conclui-se que, entre os sais inorgânicos 0,42 a 46,07 a 35,87 a testados, o silicato de potássio na dose de 50 g.L-1 K2SiO3 15 0,31 b 34,32 b 29,08 a apresentou redução no bolor verde sem comprometer a K2SiO3 50 0,37 ab 41,08 ab 37,80 a qualidade visual do fruto, podendo ser incluído como 17,25 34,03 uma medida complementar no manejo da doença. KCl 17 CV% ReferênciasTratamentos: controle (água destilada), hidróxido de potássio BENATO, E. A.; BELLETTI, T. C.; TERAO, D.; FRANCO, D. A.(KOH, 15 g.L-1), cloreto de potássio (KCl, 15 g. L-1) e silicato de S. Óleos essenciais e tratamento térmico no controle pós-colheitapotássio (K2SiO3, 15 g.L-1 e 50 g.L-1). Médias seguidas pela mesma de bolor verde em laranja. Summa phytopathol, Botucatu, v. 44,letra não diferem entre si pelo teste de Tukey (p ≤ 0,05). n. 1, p. 65-71, 2018 DELIOPOULUS, T.; KETTLEWELL, P. S.; HARE, M. C. Fungal O efeito adverso na infecção e colonização do disease suppression by inorganic salts: a review. Crop Protection,patógeno causado pela aplicação dos sais é constatado Guildford, v. 29, n. 10, p. 1059‑1075, 2010.através da redução da incidência e posteriormente FISCHER, I. H.; TOFFANO, L.; LOURENÇO, S. A.; AMORIM,pelo progresso de expansão da lesão causada pelo L. Caracterização dos danos pós-colheita em citros procedentes deP. digitatum, conforme indicado pela variável r, que foi “packinghouse”. Fitopatologia Brasileira, Brasília, v. 32, n. 4, p.menor nos frutos tratados com KOH e K2SiO3 (50 g.L-1). 304-310, 2007.A variável r se refere à velocidade de colonização GHOOSHKHANEH, N. G.; GOLZARIAN, M. R.;do patógeno no tecido do hospedeiro, influenciando MAMARABADI, M. Detection and classification of citrus greendiretamente no tamanho final da lesão e na severidade mold caused by Penicillium digitatum using multispectral imaging.final da doença (MENEGON et al., 2005). Por fim, o Journal of the Science of Food and Agriculture, London, v. 98 p.menor tamanho da área esporulante afeta o volume de 3542-3550, 2018.inóculo secundário, que pode ser disperso no ambiente,dando origem a novos ciclos da doença (FISCHER etal., 2007). Os resultados demonstram que a aplicação de saisinorgânicos em pós-colheita afetou o desenvolvimentodo bolor verde. Os sais inorgânicos podem atuar contraRevista Biotemas, 31 (4), dezembro de 2018

Sais inorgânicos no controle em pós-colheita de P. digitatum em laranja 71JABNOUN-KHIAREDDINE, H.; ABDALLAH, R.; EL- RODRIGUES, F. A.; DATNOFF, L. E. Silicon and plant diseases.MOHAMEDY, R.; ABDEL-KAREEM, F.; GUEDDES-CHAHED, Basel: Springer International Publishing, 2015. 148 p.M.; HAJLAOUI, A.; DAAMI-REMADI, M. Comparative efficacyof potassium salts against soil-borne and air-borne fungi and their SPADARO, D.; DROBY, S. Development of biocontrol productsability to suppress tomato wilt and fruit rots. Journal of Microbial for postharvest diseases of fruit: The importance of elucidating theand Biochemical Technology, Louisville, v. 8, n. 2, p. 45-55, 2016. mechanisms of action of yeast antagonists. Trends in Food Science & Technology, Cambridge, v. 47, p. 39-49, 2016.MENEGON, A. P.; FORCELINI, C. A.; FERNANDES, J. M. C.Expansão de lesão por manchas foliares em cevada e sua interaçãocom a aplicação foliar de fungicidas. Fitopatologia Brasileira,Brasília, v. 30, p. 134-138, 2005. Revista Biotemas, 31 (4), dezembro de 2018



Biotemas, 31 (4): 71-75, dezembro de 2018 http://dx.doi.org/10.5007/2175-7925.2018v31n4p7731ISSNe 2175-7925 Short Communication Record of Carineta Amyot and Audinet-Serville, 1843 (Hemiptera: Cicadidae: Cicadettinae: Carinetini) in Goiás State, Brazil Douglas Henrique Bottura Maccagnan * Alan Ricardo Souza Gomes Hiago Costa Dias Millena Oliveira Duarte Laboratório de Entomologia, Universidade Estadual de Goiás, Câmpus Iporá Avenida R2 Qd1, s/no, Bairro Novo Horizonte 2, CEP 76200-000, Iporá – GO, Brasil * Autor para correspondência [email protected] Submetido em 12/03/2018 Aceito para publicação em 10/09/2018Resumo Registro de Carineta Amyot e Audinet-Serville, 1843 (Hemiptera: Cicadidae: Cicadettinae: Carinetini) no Estado de Goiás, Brasil. Cigarras (Hemiptera: Cicadidae) são insetos caracterizados principalmente pelo som que emitem, o que torna sua presença evidente em áreas naturais e urbanas. Além disso, sabemos pouco sobre as espécies que ocorrem na região neotropical, inclusive no Brasil. Este é o primeiro relato de espécies de Carineta no estado de Goiás, Brasil. As coletas foram feitas com armadilhas luminosas em duas localidades próximas na área central do bioma Cerrado. Foram amostradas as espécies Carineta durantoni Boulard, 1986, C. gemella Boulard, 1986, C. rufescens (Fabricius, 1803) e C. spoliata (Walker, 1858). Imagens dessas espécies e sua distribuição atual são apresentadas aqui. Palavras-chave: Biogeografia; Cerrado; Cicadoidea; Distribuição; InsectaAbstract Cicadas (Hemiptera: Cicadidae) are insects characterized mainly by the sound they emit, which makes their presence evident in natural and urban areas. Beyond this, we know little about the species that occur in the neotropical region, including Brazil. This is the first report of species of Carineta in Goiás State, Brazil. The collections were made with light traps in two close localities in the core area of the Cerrado biome. We sampled the species Carineta durantoni Boulard, 1986, C. gemella Boulard, 1986, C. rufescens (Fabricius, 1803) and C. spoliata (Walker, 1858). Images of these species and their current distribution are presented here. Key words: Biogeography; Cerrado; Cicadoidea; Distribution; InsectaEste periódico está licenciado Revista Biotemas, 31 (4), dezembro de 2018conforme Creative CommonsAtribuição 4.0 Internacional.

74 D. H. B. Maccagnan et al. Cicadas are insects characterized mainly by the 6500K) in the neighboring municipalities of Dioramapresence of a sound-producing organ in the male. There (16°14’S, 51°16’W) from Septenber 2011 to Februaryare more than 3,000 species worldwide (SANBORN, 2014 and Israelândia (16º21’S, 51º00’W) from August2013), and Brazil is currently known to harbor 158 2016 to January 2018. The insects were collected underspecies distributed in 33 genera (SANBORN 2016a; a permit from Instituto Chico Mendes de Conservação2017a; RUSCHEL; CARVALHO, 2018). The Carinetini da Biodiversidade (ICMBio), license number 51649-1.are characterized as follows: the pronotum distinctly During the collection period, the light traps were setnarrowed anteriorly, never longer than the mesonotum, up for two consecutive nights, twice a month. Thesometimes much shorter; the lateral pronotal margins distance between the two sampling sites was about 30are oblique, not ampliate; the body being more or km. These municipalities are located in the core of theless robust, narrowed towards the head and apex of Cerrado biome (Brazilian savanna) and the climate isabdomen, which is sometimes very short; tegmina and characterized by a dry season from May to Septemberwings hyaline, the former being in a few cases semi- and a wet season from October to April (Köppen Awopaque, but usually clear, and frequently unspotted – tropical savanna climate) (ALVES, 2011).(DISTANT, 1905). Included in the Carinetini are eightgenera, of which seven are restricted to the neotropical The identification of the species was based on theregion (Ahomana Distant, 1905; Carineta Amyot & literature (BOULARD, 1986; MARTINELLI; ZUCCHI,Audinet-Serville, 1843, Guaranisaria Distant, 1905, 1989; 1997) and by comparison with previouslyHerrera Distant, 1905, Novemcella Goding, 1925, identified specimens. Some species of Carineta formParanistria Metcalf, 1952 and Toulgoetalna Boulard, groups that are very similar morphologically, making it1982) and the other (Karenia Distant, 1888) occurring necessary to analyze the male genitalia to confirm somein China and Thailand (SANBORN, 2013; 2014). identification (BOULARD, 1986; CHAMPANHET, 1999). When necessary, the male genitalia were cut off Carineta is the richest genus of cicadas in the and heated in a double-boiler in 5% KOH until clarified.neotropical region, and this genus of the Carinetini is Subsequently the genitalia were washed in distilled waterthe only one with representives in Brazil. In this genus, and placed in Eppendorf-type plastic tubes containing76 species have been recorded, distributed from Mexico 60% glycerin. The survey of occurrence sites wasto Central America and all South America (SANBORN, based on the catalogs of Metcalf (1963), Duffels and2013; 2017b). Carineta can be distinguished from the Van der Laan (1985), Sanborn (2013), Ruschel andother genera of the tribe by the following: the fore wing Carvalho (2018) and latest publications (BARRETO;much longer than the body and with greatest width PORFIRO, 2015; SANBORN, 2016b; 2017b). Theabout one-third the length; head (including eyes) more distribution map was made using the SimpleMappror less narrower than base of the mesonotum; front (SHORTHOUSE, 2010). Voucher material of the cicadasabout as long or a little longer than vertex; pronotum collected is deposited in the Entomological Collectionconsiderably shorter than mesonotum; and abdomen of the Universidade Estadual de Goiás – Câmpus Iporáabout as long as space between apex of head and base (CE-UEG).of cruciform elevation (DISTANT, 1906). Twenty-twospecies of Carineta are recorded for Brazil (RUSCHEL; Although there are many species of CarinetaCARVALHO, 2018). However, there is lack information distributed throughout a large area of Brazil, no speciesabout their general ecology, including distribution in the of this genus has been previously reported in Goiás. Incountry. Therefore, the aim of the present work was to our field work, we collected four species belonging torecord for the first time the occurrence of four species Carineta as follows:of Carineta in Goiás State, Brazil. ■ Carineta durantoni Boulard, 1986 (Figure 1A) The cicadas were collected by the use of four – We collected one male of C. durantoni in thelight traps with compact fluorescent lamps (4u, 46W, municipility of Israelândia on April 2017. The occurrence of this species has been recorded inRevista Biotemas, 31 (4), dezembro de 2018

Record of Carineta in Goiás State, Brazil 75French Guiana (BOULARD, 1986; SANBORN, ■ Carineta gemella Boulard, 1986 (Figure 1B) – In2013) and previously in Brazil only in Rondônia all, 90 male specimens and only one female of C.State (SANBORN, 2008) (Figure 2). gemella were collected. This species was abundantFIGURE 1: Carineta species collected in Goiás State, Brazil. A. Carineta durantoni Boulard, 1986 (CE-UEG no 00336). B. Carineta gemella Boulard, 1986 (CE-UEG no 00159). C. Carineta rufescens (Fabricius, 1803) (CE-UEG no 00331). D. Carineta spoliata (Walker, 1858) (CE-UEG no 00337). Scale 20 mm.FIGURE 2: Records of occurrence of Carineta durantoni, Carineta gemella, Carineta rufescens and Carineta spoliata. Marks in red represent occurrence in Brazilian states and in black other FIGURE 2: Records of occurrence of Carineta durantoni, Carineta gemella, Carineta rufescens and Carineta spoliata. Marks in red FIGURErceop2rue:sneRtnrteiocecosc.rudrrsenocfe ioncBcruazrirleianncsetatoefs aCndarininbelatcak dotuhrear ncotuonntir,iesC. arineta gemella, Carineta rufescens and Carineta spoliata. Marks in red represent occurrence in Brazilian states and in black other countries. Revista Biotemas, 31 (4), dezembro de 2018 In BIrnazBilr,azmilo, smtocsitccaidcaadsabsebleolnogngininggttoo tthhee ggeennuussCCarairnienteataarearceurcruenrrtleynktlnyowknnotwo noctcouroicncur inthe northern region of the country, especially in the state of Amazonas (RUSCHEL;

76 D. H. B. Maccagnan et al. in both sampling localities and was collected in light our understanding of how different species of cicadas in traps beginning in November and through January. Brazil are distributed and thus help in the development Its occurrence has been reported for Venezuela, of future conservation strategies. Ecuador, Bolivia and Argentina (SANBORN; HEATH, 2014; RUSCHEL; CARVALHO, 2018). Acknowledgments In Brazil, this species has been found to occur in the states of Roraima, Amazonas, Rondônia, The authors are grateful to Mr. João Batista Peres, Mato Grosso and Minas Gerais (SANBORN, Mr. Vilmar Rodrigues Peres and Ms. Solange dos 2008; BARRETO; PORFIRO, 2015; RUSCHEL; Santos Castro (AGROTEC) for the permit to access CARVALHO, 2018). the study sites. HCD is grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq),■ Carineta rufescens (Fabricius, 1803) (Figure 1C) – and ARSG and MOD thank the Universidade Estadual We collected three males of C. rufescens occurring de Goiás (UEG) for providing the Scientific Initiation in both sampling localities in the months of October Scholarships. Dr. A. Leyva (USA) helped with English and November. C. rufescens is easily recognized editing of the manuscript. by the presence of two black marks close to the ambient fissure of the pronotum. Its occurrence References has been recorded in French Guiana, Colombia and Peru (SANBORN, 2013). In Brazil, its occurrence ALVES, E. D. L. Frequência e probabilidade de chuvas no was reported in the states of Amazonas, Pará and município de Iporá-GO. Caminhos de Geografia, Uberlândia, v. Mato Grosso (METCALF, 1963; RUSCHEL; 12, n. 37, p. 65-72, 2011. CARVALHO, 2018). BARRETO, M. R.; PORFIRO, J. M. Espécies de (Hemiptera: Cicadidae) no estado de Mato Grosso, Brasil. EntomoBrasilis,■ Carineta spoliata (Walker, 1858) (Figure 1D) – We Vassouras, v. 8, n. 3, p. 426-248, 2015. collected four females of C. spoliata in both sampling BOULARD, M. Nouvelles cigales guyano-amazoniennes du sites during December and February. This is the genre Carineta (Homoptera, Tibicinidae). Nouvelle Revue smallest of the species collected and characterized d’Entomologie, Paris, v. 2, n. 4, p. 415-429, 1986. by a green color. Its occurrence has been recorded CHAMPANHET, J. -M. Nouvelles Carineta de l’Equateur et de in Venezuela, Colombia, Peru and Bolivia Bolivie (Cicadomorpha, Cicadoidae, Tibicinidae). Ecole Pratique (MARTINELLI; ZUCCHI, 1997; RUSCHEL; dês Hautes Etudes, Travaux Du Laboratoire Biologie et CARVALHO, 2018). C. spoliata was previously Evolution dês Insects Hemipteroidea, Paris, n. 11/12, p. 65-76, reported for Brazil in the states of Mato Grosso, 1999. Minas Gerais and São Paulo (MARTINELLI; DISTANT, W. L. Rhynchotal notes. XXXII. Annals and Magazine ZUCCHI, 1989; 1997; BARRETO; PORFIRO, of Natural History, London, V. 15, Ser. 7, p. 478-486, 1905. 2015; RUSCHEL; CARVALHO, 2018). DISTANT, W. L. A synonymic catalogue of Homoptera. Part I. Cicadidae. London: Trustees of the British Museum, 1906. 207 p. In Brazil, most cicadas belonging to the genus DUFFELS, J. P.; VAN DER LAAN, P. A. Catalogue of theCarineta are currently known to occur in the northern Cicadoidea (Homoptera, Auchenorhyncha) 1956-1980.region of the country, especially in the state of Amazonas Amsterdam: Kluwer Academic Pulishers Group, 1985. 414 p.(RUSCHEL; CARVALHO, 2018). In addition to MARTINELLI, N. M.; ZUCCHI, R. A. Cigarras associadasexpanding the range of these species, these new records ao cafeeiro. IV Gênero Carineta A. & S., 1843 (Homoptera,deserve special mention because the localities where the Tibicinidae, Tibicininae). Anais da Sociedade Entomológica docicadas were collected are situated in the Cerrado biome, Brasil, Londrina, v. 18, p. 13-22, 1989.which is considered a biodiversity hotspots in which MARTINELLI, N. M.; ZUCCHI, R. A. Cigarras (Hemiptera:hundreds of endemic species have been under the threat Cicadidae: Tibicinidae) associadas ao cafeeiro: distribuição,of extinction for some decades (STRASSBURG et al., hospedeiros e chave para as espécies. Anais da Sociedade2017). Therefore, the results presented here can foster Entomológica do Brasil, Londrina, v. 26, n. 1, p. 133-143, 1997. METCALF, Z. P. General catalogue of the Homoptera, Fascicle VIII, Cicadoidea. Part 2, Tibicinidae. Raleigh: North Carolina State College Contribution, 1963. 492 p.Revista Biotemas, 31 (4), dezembro de 2018

Record of Carineta in Goiás State, Brazil 77RUSCHEL, T. P.; CARVALHO, G. S. Cicadidae. 2018. Disponível SANBORN, A. F. Generic redescription, seven new species and aem: <http://fauna.jbrj.gov.br/fauna/faunadobrasil/720>. Acesso key to the Taphura Stål, 1862 (Hemiptera: Cicadidae: Cicadetttinae:em: 10 mar. 2018. Taphurini). Zootaxa, Auckland, v. 4324, n. 3, p.451-481, 2017a.SANBORN, A. F. New records of Brazilian cicadas including the SANBORN, A. F. A new species of Carineta Amyot & Audinet-description of a new species (Hemiptera: Cicadoidea, Cicadidae). Serville, 1843 (Hemiptera: Cicadoidea: Cicadidae) from Martinique.Neotropical Entomology, Londrina, v. 37, n. 6, p. 685-690, 2008. Proceedings of the Entomological Society of Washington, Washington, v. 119, n. 4, p. 629-636, 2017b.SANBORN, A. F. Catalogue of the Cicadoidea (Hemiptera:Auchenorrhyncha). London: Academic Press/Elsevier, 2013. SANBORN, A. F.; HEATH, M. S. The cicadas of Argentina with1002 p. new records, a new genus and fifteen new species (Hemiptera: Cicadoidea: Cicadidae). Zootaxa, Auckland, v. 3883, n. 1, p. 1-94,SANBORN, A. F. A New genus and new tribe of cicada from South 2014.America (Hemiptera: Cicadoidea: Cicadidae) with a note on thetaxonomic position of Ahomana Distant, 1905. Proceedings of the SHORTHOUSE, D. P. SimpleMappr, an online tool to produceEntomological Society of Washington, Washington, v. 116, n. 3, publication-quality point maps. 2010. Disponível em: <http://p. 339-348, 2014. www.simplemappr.net>. Acesso em: 08 mar. 2018.SANBORN, A. F. Generic redescription, two new species, and a STRASSBURG, B. B. N.; BROOKS, T.; FELTRAN-BARBIERI,key to the species of the cicada genus Ariasa Distant, 1905 with R.; IRIBARREM, A.; CROUZEILLES, R.; LOYOLA, R.;the description of a new genus (Hemiptera: Cicadidae: Cicadinae: LATAWIEC, A. E.; OLIVEIRA FILHO, F. J. B.; SCARAMUZZA,Fidicinini). Zootaxa, Auckland, v. 4137, n. 4, p. 501-519, 2016a. C.A. de M.; SCARANO, F. R.; SOARES-FILHO, B.; BALMFORD, A. Moment of truth for the Cerrado hotspot. Nature Ecology &SANBORN, A. F. Five new species, a new genus and a new record Evolution, Cambridge, v. 1, article no 0099, 2017.of cicadas from French Guiana with four new combinations andthree new synonymies (Insecta, Hemiptera, Cicadoidea, Cicadidae).Zoosystema, Paris, v. 38, n. 2, p. 177-199, 2016b. Revista Biotemas, 31 (4), dezembro de 2018

VVoolluume 3119 NNúmúmereor4o 1 p. 11--71713 ISSNe 2175-7925 22000168 DMeazreçmobroARTIGOSPupal parasitoids for the biological control of Diatraea saccharalis (Fabricius, 1794) (Lepidoptera:Crambidae) K. M. Endo et al....................................................................................................................................................................1Influência das águas do estuário do Rio Pará na fertilidade do solo das ilhas de várzea em Belém,Pará S. Brazão e Silva et al..........................................................................................................................................................15Avaliação do Índice de Estado Trófico como ferramenta para monitoramento de atividadesaquícolas em reservatórios continentais E. S. Pinho et al...................................................................................................................................................................23Padrões de distribuição e abundância de gastrópodes límnicos no município de Acaraú, Ceará:avaliando aspectos da Teoria da Biogeografia de Ilhas M. R. Santos e R. C. Maia...................................................................................................................................................35Conservation status of Astyanax biotae (Characiformes: Characidae) in Mato Grosso do Sul, upperParaná River basin, Brazil M. J. A. Vilela et al..............................................................................................................................................................47Nutritional potential of a novel sea asparagus, Salicornia neei Lag., for human and animal diets K. B. Doncato e C. S. B. Costa...........................................................................................................................................57COMUNICAÇÃO BREVESais inorgânicos no controle em pós-colheita de Penicillium digitatum (Pers.) Sacc. em laranja A. E. Brunetto et al..............................................................................................................................................................65SHORT COMMUNICATIONRecord of Carineta Amyot and Audinet-Serville, 1843 (Hemiptera: Cicadidae: Cicadettinae:Carinetini) in Goiás State, Brazil D. H. B. Maccagnan et al....................................................................................................................................................71 Este periódico está licenciado conforme Creative Commons Atribuição 4.0 Internacional.