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Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae): first report in Sergipe State, Brazil

Abstract

INTRODUCTION:

This study reports the first occurrence of Psammolestes tertius (Hemiptera, Reduviidae, Triatominae) in the state of Sergipe, Brazil.

METHODS:

In 2020, 95 specimens were collected from the municipality of Porto da Folha, Sergipe, Brazil.

RESULTS:

This finding expands the geographical distribution of the species from 15 states in Brazil to 16 and increases the biodiversity of triatomines in the state of Sergipe.

CONCLUSIONS:

The presence of P. tertius in the state of Sergipe demonstrated a wider distribution of this species in northeastern Brazil.

Keywords:
Biogeography; Caatinga; Geographical distribution; Kissing bugs

Described by Jeannel (1919)11. Jeannel R. Henicocephalidae et Reduviidae. In: Jeannel R. Voyage de Ch. Alluaud et R. Jeannel en Afrique orientale. Paris: Librairie Albert Schulz; 1919. p. 131-314., the subfamily Triatominae is recognized by mandatory hematophagy. Various species are important vectors of Trypanosoma cruzi (Chagas 1909) (Kinetoplastida, Trypanosomatidae), the etiologic agent of Chagas disease, while others are of little importance from an epidemiological point of view, especially those with low adaptability to artificial ecotopes22. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their Significance as Vectors of Chagas’ Disease. Bull Am Mus Nat Hist. 1979;163:123-520.. Currently, the subfamily Triatominae contains more than 150 species, grouped into five tribes and 18 genera33. Galvão C. Taxonomia dos vetores da doença de Chagas da forma a molécula, quase três séculos de história. In: Oliveira J, Alevi KCC, Camargo LMA, Meneguetti DUO. Atualidades em Medicina Tropical no Brasil Vetores: Vetores. 1ª ed. Rio Branco: Stricto Sensu; 2020. p. 9-37.,44. Alevi KCC, de Oliveira J, Garcia ACC, Cristal DC, Delgado LMG, de Freitas Bittinelli I, et al.Triatoma rosaisp. nov. (Hemiptera, Triatominae): A New Species of Argentinian Chagas Disease Vector Described Based on Integrative Taxonomy. Insects. 2020;11(12): 2-24..

The genus Psammolestes Bergroth, 1911 is a monophyletic group comprising only three species: P. arthuri Pinto, 1926; P. coreodes Bergroth, 1911; and P. tertius Lent and Jurberg, 196555. Oliveira J, Alevi KCC, Ravazi A, Herrera HM, Santos FM, Azeredo-Oliveira MTV, et al. New evidence of the monophyletic relationship of the genus Psammolestes Bergroth, 1911 (Hemiptera, Reduviidae, Triatominae). Am J Trop Med Hyg. 2018; 99(6):1485-8.. Despite the genus Psammolestes having a close association with birds, they are not the only source of food for these triatomines in nature. For other groups, for example mammals, have already been found inhabiting the nests of birds66. Oliveira J, Alevi KCC, Fonseca EOL, Souza OMF, Santos CGS, Azeredo-Oliveira MTV, Da Rosa JA. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res. 2016;15(2):2-6.,77. Diotaiuti LG, Bezerra CM, Soare CJ, Costa LM, Barbosa SE. Description of an amazing nest of caatinga cachalote Pseudoseisura cristata infested by Psammolestes tertius in Tauá, State of Ceará, Northeastern Brazil. Rev Patol Trop. 2018;47(2):125-31..

Species of the genus Psammolestes have been found in nests of several bird families: Dendrocolaptidae (woodcreepers), Troglodytidae (house wren and long-billed wren), Furnariidae (rufous-fronted thornbird and rufous hornero), Icteridae (troupial, oropendola, yellow oriole, and yellow-rumped)88. Silva ANB, Diotaiuti L, Câmara ACJ, Oliveira PIC, Galvão LMC, Chiari E, Souza RCM. First report of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Rio Grande do Norte state, Brazil. Check List. 2018;14(6):1109-13.

9. Barretto MP, Albuquerque RDR. Estudos sobre reservatorios e vectores silvestres do Trypanosoma cruzi. XXXIII. Infecção experimental e natural do Psammolestes tertius Lent & Jurberg, 1965 pelo T. cruzi. Rev Inst Med Trop. 1969;11:4.

10. Cruz-Guzmán PJ, Morocoima A, Chique JD, Ramones-Quintero J, Uzcátegui MT, Carrasco HJ. Psammolestes arthuri naturalmente infectado con Trypanosoma cruzi encontrado en simpatría con Rhodnius prolixus y Triatoma maculata en nidos de aves en el Estado Anzoátegui, Venezuela. Saber (Cumaná). 2014;26(4):428-40.

11. Pifano F. Anotaciones acerca del Psammolestes arthuri (Pinto, 1926) (Hemiptera, Heteroptera,Triatomidae) reduvideo hematófago encontrado en nidos de "cucarachero de monte (probablemente, Dendrocolaptidae) en un sector de los valles de Yaracuy. Su impo. Gac Med Caracas. 1938;45:241-5.

12. Pinto C, Lent H. Sobre as espécies do gênero Psammolestes Bergroth, 1911 (Hemiptera, Triatomidae). Ann Acad Bras Sci. 1935;7:333-7.
-1313. Sherlock IA, Guitton N. Fauna Triatominae do estado da Bahia - Brasil III - Notas sobre ecótopos silvestres e o gênero Psammolestes. Mem Inst Oswaldo Cruz. 1974;72(1-2):91-101..

Psammolestes tertius is distributed in all geographic regions of Brazil: the Southeast (Minas Gerais and São Paulo), Midwest (Goiás and Mato Grosso), North (Pará and Tocantins), Northeast (Alagoas, Bahia, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, and Rio Grande do Norte), and South (Paraná), and in Peru (San Martín)66. Oliveira J, Alevi KCC, Fonseca EOL, Souza OMF, Santos CGS, Azeredo-Oliveira MTV, Da Rosa JA. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res. 2016;15(2):2-6.,88. Silva ANB, Diotaiuti L, Câmara ACJ, Oliveira PIC, Galvão LMC, Chiari E, Souza RCM. First report of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Rio Grande do Norte state, Brazil. Check List. 2018;14(6):1109-13.,1414. Galvão C. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. 289 p.,1515. Paiva VF, Rosa JÁ, Ceretti Junior W, Marrelli MT, Oliveira J. Confirmation of the first report of Psammolestes tertius Lent and Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Paraná State, Brazil. Rev Soc Bras Med Trop, 2021, 54: e0485-2020.. The comparison of two different populations of P. tertius showed associations with different species of Furnariidae birds from the states of Ceará and Minas Gerais. The use of different RAPD markers has demonstrated intraspecific variability, possibly related to environmental changes characteristic of Caatinga and Cerrado1616. Soares RPP, Barbosa SE, Borges EC, Melo Júnior TA, Romanha AJ, Dujardin JP, et al. Genetic Studies of Psammolestes tertius (Hemiptera, Reduviidae, Triatominae) Using Male Genital Morphology, Morphometry, Isoenzymes, and Random Amplified Polymorphic DNA. Biochem Genet. 2001;39(1-2):1-13.. However, this variability was not corroborated by a cytogenetic comparison of two populations (Bahia and Ceará) carried out by Oliveira et al.66. Oliveira J, Alevi KCC, Fonseca EOL, Souza OMF, Santos CGS, Azeredo-Oliveira MTV, Da Rosa JA. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res. 2016;15(2):2-6..

In the Sergipe state, northeastern Brazil, all the following species have already been reported: Panstrongylus lutzi Neiva and Pinto, 1926; P. megistus Burmeister, 1835; P. geniculatus Latreille, 1811; Rhodnius neglectus Lent, 1954; R. zeledoni Stal, 1859; Triatoma brasiliensis Neiva, 1911; T. melanocephala Neiva and Pinto, 1923; T. pseudomaculata Corrêa and Spínola, 1964; T. petrocchiae Pinto and Barreto 1925; T. rubrofasciata De Geer, 1773; and T. tibiamaculata Pinto, 19261414. Galvão C. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. 289 p.,1717. Castro-Filho J, Silveira AC. Distribution of Chagas disease in Brazil. Rev Bras Malariol Doencas Trop. 1979;31:85-98.

18. Silveira AC. Entomological Survey (1975-1983). Rev Soc Bras Med Trop . 2011;44(suppl. 2):26-32.

19. Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT. Geographic Distribution of Chagas disease vectors in Brazil based on Ecological Niche Modeling. Trop Med Infect Dis. 2012;1-15.

20. Lima AFR, Jeraldo VLS, Silveira MS, Madi RR, Santana TBK, Melo CM. Triatomines in dwellings and outbuildings in an endemic area of Chagas disease in northeastern Brazil. Rev Soc Bras Med Trop . 2012;45(6):701-6.
-2121. Melo CM, Cruz ACFG, Lima AFR, Silva LR, Madi RR, Jeraldo VLS, Mercado R. Triatomine Fauna and Recent Epidemiological Dynamics of Chagas Disease in an Endemic Area of Northeast Brazil. Can J Infect Dis Med Microbiol. 2018; 1-13.. Although Sergipe borders Bahia and Alagoas, which are states where P. tertius occurs, this is the first record of this species in that state.

Sergipe has an area of approximately 21,926.908 km2, corresponding to 0.26% of the national territory, and an estimated population of 2.06 million. It comprises 75 municipalities distributed in three climatic regions: semi-arid, agreste, and humid coastal2222. SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe). “Banco de dados Geoespacial-Atlas Digital sobre Recursos Hídricos de Sergipe, v.12.14,” SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe), Aracaju, Brazil, 2014.,2323. IBGE. Censo Demográfico 2010. [Internet] Instituto Brasileiro de Geografia e Estatística. 2010. Available from: https://censo2010.ibge.gov.br/sinopse/index.php?dados=0&uf=28.
https://censo2010.ibge.gov.br/sinopse/in...
. The municipality where insects were collected is Porto da Folha (9° 54′ 34″ S; 37° 16′ 41″ W), which has an area of 876.67 km² and is 156 km from the state capital, Aracaju (Figure 1).

FIGURE 1:
Geographical localization of the Sergipe state (Orange), highlighting Porto da Folha, Sergipe (purple) and the Brazilian northeast in green.

New records: Brazil, Sergipe, municipality of Porto da Folha, within the Getirana village. Three adults and 20 nymphs were collected from nests of birds popularly known as casaca-de-couro [Pseudoseisura cristata (Spix, 1824)]. The 3 adults (2 females and 1 male) were collected alive at 17:45 h local time on January 13, 2020 (first record). The second collection included 9 males, 10 females, and 55 nymphs of the species P. tertius; these and other insects were associated with nests of casaca-de-couro birds [P. cristata located on Mimosa tenuiflora trees (Willd.) Poiret]. The females and males were collected alive at 15:35 h local time on January 14, 2020 (last record).

Both specimens were identified as P. tertius based on their head characteristics (Figure 2). Since their heads are slightly longer than broad, at the level of the eyes, with a moderate slope behind the ocelli, the pronotal anterolateral angles are very short and obtuse. On the other hand, P. coreodes has a head with a length equal to or slightly shorter than the width at the level of the eyes, with a sharp slope behind the ocelli, and the anterolateral angles of the pronotum are cuspidal². The analyzed specimens were deposited in the José Maria Soares Barata entomological collection in batch format with the voucher CEJMSB 861.

FIGURE 2:
Psammolestes tertius. (A) Female. (B) Detail of head.

The genus Psammolestes comprises three species and seems to have specialized in exploiting bird nest microhabitats, mainly in the family Furnariidae1515. Paiva VF, Rosa JÁ, Ceretti Junior W, Marrelli MT, Oliveira J. Confirmation of the first report of Psammolestes tertius Lent and Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Paraná State, Brazil. Rev Soc Bras Med Trop, 2021, 54: e0485-2020.. These species are distributed in South America and have clear ecological niche differences. A recent study based on distributional data predicted the potential geographical distribution of the three Psammolestes species using ecological niche modeling. The models suggest that P. arthuri are distributed in warm and humid areas, P. coreodes occupy the driest and coldest areas, and P. tertius have intermediate climatological limits and occur at the highest altitudes. For P. tertius, this potential area includes the Rio Grande do Norte state2424. Gurgel-Gonçalves R, Silva RB. Analysis of the geographical distribution of Psammolestes Bergroth (Heteroptera: Reduviidae) in South America with new records of Psammolestes tertius Lent & Jurberg. Zootaxa. 2009;2033:41-8.. Therefore, this record of a new point of occurrence of P. tertius is very important for future work and reinforces the results obtained in a theoretical model by Gurgel-Gonçalves and Silva2525. Gurgel-Gonçalves R, Cuba CAC. Estrutura de populações de Rhodnius neglectus e Psammolestes tertius Lent & Jurberg (Hemiptera, Reduviidae) em ninhos de pássaros (Furnariidae) presentes na palmeira Mauritia flexuosa no Distrito Federal, Brasil. Rev Bras Zool. 2007;24(1):157-63..

In addition to the probable influence of climatic zones and altitude variations in the distribution of P. tertius, another potential means of dispersion to other regions is that its eggs are secreted with adhesive substances during oviposition and can adhere to substrates such as bird feathers. This association with birds, mainly as vehicles of migratory dispersion, may eventually favor the passive capture of these species of triatomines in new areas of occurrence2525. Gurgel-Gonçalves R, Cuba CAC. Estrutura de populações de Rhodnius neglectus e Psammolestes tertius Lent & Jurberg (Hemiptera, Reduviidae) em ninhos de pássaros (Furnariidae) presentes na palmeira Mauritia flexuosa no Distrito Federal, Brasil. Rev Bras Zool. 2007;24(1):157-63.,2626. Ribeiro Junior G, Silva-Santos CG, Noireau F, Dias-Lima A. Potencial de Dispersão de algumas espécies de Triatomíneos (Hemiptera: Reduviidae) por aves migratórias. Sitientibus Sér Ciên Bio. 2006;6(4):324-8.. It is worth highlighting that the knowledge about triatomine species that have these passive dispersion mechanisms, combined with the results obtained from the theoretical model of Gurgel-Gonçalves and Silva2525. Gurgel-Gonçalves R, Cuba CAC. Estrutura de populações de Rhodnius neglectus e Psammolestes tertius Lent & Jurberg (Hemiptera, Reduviidae) em ninhos de pássaros (Furnariidae) presentes na palmeira Mauritia flexuosa no Distrito Federal, Brasil. Rev Bras Zool. 2007;24(1):157-63., is fundamental for future studies on new species and to auxiliary entomology programs in Brazil.

ACKNOWLEDGMENTS

We thank the agents of epidemiological surveillance: Marcos Vinicius Alves do Santos, Sandro Cardoso Valença and Edson Rodrigues do Nascimento for their support in the field in Porto da Folha and Canindé de São Francisco, both in the state of Sergipe, Brazil. The authors also thank Antonio Fernando Vianna de Assis Lima for the logistical support.

REFERENCES

  • 1
    Jeannel R. Henicocephalidae et Reduviidae. In: Jeannel R. Voyage de Ch. Alluaud et R. Jeannel en Afrique orientale. Paris: Librairie Albert Schulz; 1919. p. 131-314.
  • 2
    Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their Significance as Vectors of Chagas’ Disease. Bull Am Mus Nat Hist. 1979;163:123-520.
  • 3
    Galvão C. Taxonomia dos vetores da doença de Chagas da forma a molécula, quase três séculos de história. In: Oliveira J, Alevi KCC, Camargo LMA, Meneguetti DUO. Atualidades em Medicina Tropical no Brasil Vetores: Vetores. 1ª ed. Rio Branco: Stricto Sensu; 2020. p. 9-37.
  • 4
    Alevi KCC, de Oliveira J, Garcia ACC, Cristal DC, Delgado LMG, de Freitas Bittinelli I, et al.Triatoma rosaisp. nov. (Hemiptera, Triatominae): A New Species of Argentinian Chagas Disease Vector Described Based on Integrative Taxonomy. Insects. 2020;11(12): 2-24.
  • 5
    Oliveira J, Alevi KCC, Ravazi A, Herrera HM, Santos FM, Azeredo-Oliveira MTV, et al. New evidence of the monophyletic relationship of the genus Psammolestes Bergroth, 1911 (Hemiptera, Reduviidae, Triatominae). Am J Trop Med Hyg. 2018; 99(6):1485-8.
  • 6
    Oliveira J, Alevi KCC, Fonseca EOL, Souza OMF, Santos CGS, Azeredo-Oliveira MTV, Da Rosa JA. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res. 2016;15(2):2-6.
  • 7
    Diotaiuti LG, Bezerra CM, Soare CJ, Costa LM, Barbosa SE. Description of an amazing nest of caatinga cachalote Pseudoseisura cristata infested by Psammolestes tertius in Tauá, State of Ceará, Northeastern Brazil. Rev Patol Trop. 2018;47(2):125-31.
  • 8
    Silva ANB, Diotaiuti L, Câmara ACJ, Oliveira PIC, Galvão LMC, Chiari E, Souza RCM. First report of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Rio Grande do Norte state, Brazil. Check List. 2018;14(6):1109-13.
  • 9
    Barretto MP, Albuquerque RDR. Estudos sobre reservatorios e vectores silvestres do Trypanosoma cruzi. XXXIII. Infecção experimental e natural do Psammolestes tertius Lent & Jurberg, 1965 pelo T. cruzi Rev Inst Med Trop. 1969;11:4.
  • 10
    Cruz-Guzmán PJ, Morocoima A, Chique JD, Ramones-Quintero J, Uzcátegui MT, Carrasco HJ. Psammolestes arthuri naturalmente infectado con Trypanosoma cruzi encontrado en simpatría con Rhodnius prolixus y Triatoma maculata en nidos de aves en el Estado Anzoátegui, Venezuela. Saber (Cumaná). 2014;26(4):428-40.
  • 11
    Pifano F. Anotaciones acerca del Psammolestes arthuri (Pinto, 1926) (Hemiptera, Heteroptera,Triatomidae) reduvideo hematófago encontrado en nidos de "cucarachero de monte (probablemente, Dendrocolaptidae) en un sector de los valles de Yaracuy. Su impo. Gac Med Caracas. 1938;45:241-5.
  • 12
    Pinto C, Lent H. Sobre as espécies do gênero Psammolestes Bergroth, 1911 (Hemiptera, Triatomidae). Ann Acad Bras Sci. 1935;7:333-7.
  • 13
    Sherlock IA, Guitton N. Fauna Triatominae do estado da Bahia - Brasil III - Notas sobre ecótopos silvestres e o gênero Psammolestes Mem Inst Oswaldo Cruz. 1974;72(1-2):91-101.
  • 14
    Galvão C. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. 289 p.
  • 15
    Paiva VF, Rosa JÁ, Ceretti Junior W, Marrelli MT, Oliveira J. Confirmation of the first report of Psammolestes tertius Lent and Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) in Paraná State, Brazil. Rev Soc Bras Med Trop, 2021, 54: e0485-2020.
  • 16
    Soares RPP, Barbosa SE, Borges EC, Melo Júnior TA, Romanha AJ, Dujardin JP, et al. Genetic Studies of Psammolestes tertius (Hemiptera, Reduviidae, Triatominae) Using Male Genital Morphology, Morphometry, Isoenzymes, and Random Amplified Polymorphic DNA. Biochem Genet. 2001;39(1-2):1-13.
  • 17
    Castro-Filho J, Silveira AC. Distribution of Chagas disease in Brazil. Rev Bras Malariol Doencas Trop. 1979;31:85-98.
  • 18
    Silveira AC. Entomological Survey (1975-1983). Rev Soc Bras Med Trop . 2011;44(suppl. 2):26-32.
  • 19
    Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT. Geographic Distribution of Chagas disease vectors in Brazil based on Ecological Niche Modeling. Trop Med Infect Dis. 2012;1-15.
  • 20
    Lima AFR, Jeraldo VLS, Silveira MS, Madi RR, Santana TBK, Melo CM. Triatomines in dwellings and outbuildings in an endemic area of Chagas disease in northeastern Brazil. Rev Soc Bras Med Trop . 2012;45(6):701-6.
  • 21
    Melo CM, Cruz ACFG, Lima AFR, Silva LR, Madi RR, Jeraldo VLS, Mercado R. Triatomine Fauna and Recent Epidemiological Dynamics of Chagas Disease in an Endemic Area of Northeast Brazil. Can J Infect Dis Med Microbiol. 2018; 1-13.
  • 22
    SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe). “Banco de dados Geoespacial-Atlas Digital sobre Recursos Hídricos de Sergipe, v.12.14,” SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe), Aracaju, Brazil, 2014.
  • 23
    IBGE. Censo Demográfico 2010. [Internet] Instituto Brasileiro de Geografia e Estatística. 2010. Available from: https://censo2010.ibge.gov.br/sinopse/index.php?dados=0&uf=28
    » https://censo2010.ibge.gov.br/sinopse/index.php?dados=0&uf=28
  • 24
    Gurgel-Gonçalves R, Silva RB. Analysis of the geographical distribution of Psammolestes Bergroth (Heteroptera: Reduviidae) in South America with new records of Psammolestes tertius Lent & Jurberg. Zootaxa. 2009;2033:41-8.
  • 25
    Gurgel-Gonçalves R, Cuba CAC. Estrutura de populações de Rhodnius neglectus e Psammolestes tertius Lent & Jurberg (Hemiptera, Reduviidae) em ninhos de pássaros (Furnariidae) presentes na palmeira Mauritia flexuosa no Distrito Federal, Brasil. Rev Bras Zool. 2007;24(1):157-63.
  • 26
    Ribeiro Junior G, Silva-Santos CG, Noireau F, Dias-Lima A. Potencial de Dispersão de algumas espécies de Triatomíneos (Hemiptera: Reduviidae) por aves migratórias. Sitientibus Sér Ciên Bio. 2006;6(4):324-8.
  • Financial Support: The first author supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the second by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). This work is financed by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Apoio à Pesquisa e à Inovação Tecnológica do Estado de Sergipe (FAPITEC), within the scope of the CAPES/FAPITEC/SE - n. 10/2016 PROMOB.

Data availability

Data citations

SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe). “Banco de dados Geoespacial-Atlas Digital sobre Recursos Hídricos de Sergipe, v.12.14,” SEMARH-Sergipe (Secretaria de Meio Ambiente e Recursos Hídricos de Sergipe), Aracaju, Brazil, 2014.

Publication Dates

  • Publication in this collection
    22 Mar 2021
  • Date of issue
    2021

History

  • Received
    26 Oct 2020
  • Accepted
    21 Jan 2021
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