Passive air transportation of an amphibian lethal pathogen in high elevation sites: practical applications for protected areas conservation in the State of São Paulo

• Grant number: 19/18335-5
• Support Opportunities: BIOTA-FAPESP Program - Regular Research Grants
• Start date: June 01, 2020
• End date: January 31, 2022
• Field of knowledge: Biological Sciences - Zoology
• Agreement: Secretaria de Meio Ambiente, Infraestrutura e Logística - Fundação Florestal
• Principal Investigator: Luis Felipe de Toledo Ramos Pereira
• Grantee: Luis Felipe de Toledo Ramos Pereira
• Host Institution: Instituto de Biologia (IB). Universidade Estadual de Campinas (UNICAMP). Campinas , SP, Brazil
• Associated researchers: Camila Inés Zornosa Torres ; Carolina Lambertini ; Guilherme Augusto Alves ; Joice Ruggeri Gomes ; Laszlo Karoly Nagy ; Luisa de Pontes Ribeiro ; Mariana Retuci Pontes ; Raquel Fernanda Salla Jacob

Abstract

The chytrid fungus Batrachochytrium dendrobatidis (Bd) is recognized worldwide as one of the main causative agents of amphibian population declines and extinctions over the last 50 years. The same is valid for the Brazilian Atlantic Forest, where a portion of the amphibian species may have been extinct by this fungus. Although Bd is already widespread in the biome, new die off events may still occur. Consequently we must develop methods that allow constant, relatively inexpensive and feasible monitoring to be carried out with the help of local non-amphibian personnel. Thus, the present project aims to study water sources as an indicator of Bd infection in native anuran populations at high elevation areas (near to or above 1000 m above sea level). We propose to investigate four areas in the Atlantic Forest, within Conservation Units, in order to subsidize monitoring and conservation action plans when needed. Water from rains, fog and water bodies (lakes and streams) will be sampled using environmental DNA (eDNA) techniques as well as sampling anurans diretlty. We will correlate amphibian infection data with genetic information obtained from water samples. If we find a clear and constant relationship, we will be suggesting a novel management and conservation tool for the state protected areas. (AU)

Scientific publications

(36)

(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)

REBOUCAS, RAONI; DOS SANTOS, MARCILEIDA M.; DA SILVA MARTINS, ANA GLAUCIA; ROSA DOMINGOS, ADAO HENRIQUE; SANTOS, ISAIAS; TOLEDO, LUIS FELIPE. Warming drives cryptic declines of amphibians in eastern Brazil{*}. Biological Conservation, v. 256, APR 2021. (16/25358-3, 19/18335-5)

DE ANDRADE, FELIPE SILVA; HAGA, ISABELLE AQUEMI; LYRA, MARIANA LUCIO; GAZONI, THIAGO; ZARACHO, VICTOR; BAPTISTA HADDAD, CELIO FERNANDO; TOLEDO, LUIS FELIPE; GIARETTA, ARIOVALDO ANTONIO. eographic distributions ofPseudopaludicola bolivianaand congeneric long-legged species (Anura: Leiuperinae. Studies on Neotropical Fauna and Environment, v. 57, n. 1, SEP 2020. (19/18335-5, 17/26162-8, 15/10728-7, 16/25358-3, 13/50741-7)

ZORNOSA-TORRES, CAMILA; LAMBERTINI, CAROLINA; TOLEDO, LUIS FELIPE. Amphibian chytrid infections along the highest elevational gradient of the Brazilian Atlantic Forest. DISEASES OF AQUATIC ORGANISMS, v. 144, p. 99-106, 2021. (16/25358-3, 19/18335-5)

GREENSPAN, SASHA E.; MIGLIORINI, GUSTAVO H.; LYRA, MARIANA L.; PONTES, MARIANA R.; CARVALHO, TAMILIE; RIBEIRO, LUISA P.; MOURA-CAMPOS, DIEGO; HADDAD, CELIO F. B.; TOLEDO, LUIS FELIPE; ROMERO, GUSTAVO Q.; et al. Warming drives ecological community changes linked to host-associated microbiome dysbiosis. NATURE CLIMATE CHANGE, v. 10, n. 11, p. 1057+, NOV 2020. (16/25358-3, 18/12225-0, 18/23622-0, 13/50741-7, 17/26162-8, 17/09052-4, 19/18335-5)

SERRANO, JANAINA DE ANDRADE; TOLEDO, LUIS FELIPE; SALES, LILIAN PATRICIA. Human impact modulates chytrid fungus occurrence in amphibians in the Brazilian Atlantic Forest. PERSPECTIVES IN ECOLOGY AND CONSERVATION, v. 20, n. 3, p. 7-pg., 2022-07-01. (19/18335-5, 16/25358-3)

RUGGERI, J.; PONTES, M. R.; RIBEIRO, L. P.; GENDREAU, K. L.; SOUSA, R. L. M.; TOLEDO, L. F.. Predominant prevalence of Ranavirus in southern Brazil, a region with widespread occurrence of the amphibian chytrid. ANIMAL CONSERVATION, v. N/A, p. 12-pg., 2023-10-05. (18/23622-0, 16/25358-3, 17/01917-6, 20/00099-0, 13/50741-7, 19/18335-5)

PRADO, JOELMA S.; ERNETTI, JULIA R.; PONTES, MARIANA RETUCI; FELIPE TOLEDO, L.. Chytrid in the clouds: an alternative passive transport of a lethal pathogen for amphibians. Hydrobiologia, v. N/A, p. 13-pg., 2023-04-16. (16/25358-3, 19/18335-5, 20/02991-8, 20/00099-0)

DE-OLIVEIRA-NOGUEIRA, CARLOS HENRIQUE; SOUZA, UBIRATA FERREIRA; MACHADO, THAYNARA MENDES; FIGUEIREDO-DE-ANDRADE, CAIO ANTONIO; MONICO, ALEXANDER TAMANINI; SAZIMA, IVAN; SAZIMA, MARLIES; TOLEDO, LUIS FELIPE. Between fruits, flowers and nectar: The extraordinary diet of the frog Xenohyla truncata. FOOD WEBS, v. 35, p. 4-pg., 2023-06-01. (16/25358-3, 19/18335-5)

LAMBERTINI, CAROLINA; ERNETTI, JULIA R.; MISSASSI, ALEXANDRE F. R.; JORGE, RAFAEL F.; DA SILVA LEITE, DOMINGOS; LIMA, ALBERTINA P.; TOLEDO, LUIS FELIPE. Chytrid fungus in amphibians from the lowland Brazilian Amazon. DISEASES OF AQUATIC ORGANISMS, v. 152, p. 11-pg., 2022-12-15. (16/25358-3, 19/18335-5)

JOYCE MARA DELPRÁ-CACHULO; ERNESTO PEREDO-RIVERA; JORGE PALACIO-NÚÑEZ; LUÍS FELIPE TOLEDO; ALEJANDRA OLIVERA-MÉNDEZ; JUAN FELIPE MARTÍNEZ-MONTOYA; ANA BEATRIZ CAROLLO ROCHA-LIMA. Influence of environmental variables on the spatiotemporal distribution of anurans during the reproductive season in south-eastern Brazil. Acta zoológica mexicana, v. 40, 2024-10-25. (19/18335-5, 16/25358-3)

REBOUCAS, RAONI; DOS SANTOS, MARCILEIDA M.; DA SILVA MARTINS, ANA GLAUCIA; ROSA DOMINGOS, ADAO HENRIQUE; SANTOS, ISAIAS; TOLEDO, LUIS FELIPE. Warming drives cryptic declines of amphibians in eastern Brazil*. Biological Conservation, v. 256, p. 5-pg., 2021-02-27. (19/18335-5, 16/25358-3)

FREITAS, MARIANE DE OLIVEIRA; TOLEDO, LUIS FELIPE. Treefrogs with distinct advertisement calls produce similar territorial signals. BIOACOUSTICS-THE INTERNATIONAL JOURNAL OF ANIMAL SOUND AND ITS RECORDING, v. 30, n. 4, p. 389-401, JUL 4 2021. (19/18335-5, 16/25358-3)

REBOUCAS, RAONI; BECKER, C. GUILHERME; BACON, JAMIE P.; TOLEDO, LUIS FELIPE. Anthropogenic habitat modification linked to deformities in Cururu Toads from Fernando de Noronha. SALAMANDRA, v. 57, n. 3, p. 389-399, AUG 15 2021. (16/25358-3, 19/18335-5)

LUZ NUNES-DE-ALMEIDA, CARLOS HENRIQUE; BATISTA HADDAD, CELIO FERNANDO; TOLEDO, LUIS FELIPE. A revised classification of the amphibian reproductive modes. SALAMANDRA, v. 57, n. 3, p. 413-427, AUG 15 2021. (11/51694-7, 19/18335-5, 14/23388-7, 14/50342-8, 08/50325-5, 13/50741-7)

LEAL, FERNANDO; ZORNOSA-TORRES, CAMILA; AUGUSTO-ALVES, GUILHERME; DENA, SIMONE; PEZZUTI, TIAGO LEITE; LEITE, FELIPE; LOURENCO, LUCIANA BOLSONI; GARCIA, PAULO; TOLEDO, LUIS FELIPE. Head in the clouds: a new dwarf frog species of the Physalaemus signifer clade (Leptodactylidae, Leiuperinae) from the top of the Brazilian Atlantic Forest. EUROPEAN JOURNAL OF TAXONOMY, v. 764, p. 119-151, AUG 19 2021. (16/25358-3, 19/03170-0, 11/09239-0, 19/18335-5)

MOURA-CAMPOS, DIEGO; GREENSPAN, SASHA E.; V. DIRENZO, GRAZIELLA; NEELY, WESLEY J.; TOLEDO, LUIS FELIPE; BECKER, C. GUILHERME. Fungal disease cluster in tropical terrestrial frogs predicted by low rainfall. Biological Conservation, v. 261, SEP 2021. (16/25358-3, 19/18335-5)

MORENO-DE-LIMA, PSIQUE LAIS; LAMBERTINI, CAROLINA; BECKER, C. GUILHERME; REBOUCAS, RAONI; TOLEDO, LUIS FELIPE. Presence of invasive American bullfrogs may reduce infectious disease in a native frog species. DISEASES OF AQUATIC ORGANISMS, v. 149, p. 6-pg., 2022-01-01. (16/25358-3, 19/18335-5)

LYRA, MARIANA L.; MONTEIRO, JULIANE P. C.; RANCILHAC, LOIS; IRISARRI, IKER; KUENZEL, SVEN; SANCHEZ, EUGENIA; CONDEZ, THAIS H.; ROJAS-PADILLA, OMAR; SOLE, MIRCO; TOLEDO, LUIS FELIPE; et al. Initial Phylotranscriptomic Confirmation of Homoplastic Evolution of the Conspicuous Coloration and Bufoniform Morphology of Pumpkin-Toadlets in the Genus Brachycephalus. TOXINS, v. 13, n. 11, NOV 2021. (17/26281-7, 14/50342-8, 18/09691-0, 19/18335-5, 16/25358-3, 13/50741-7)

TOLEDO, LUIS FELIPE; POTSCH DE CARVALHO-E-SILVA, SERGIO; TELLES DE CARVALHO-E-SILVA, ANA MARIA PAULINO; GASPARINI, JOAO LUIZ; BAETA, DELIO; REBOUCAS, RAONI; HADDAD, CELIO F. B.; BECKER, C. GUILHERME; CARVALHO, TAMILIE. A retrospective overview of amphibian declines in Brazil's Atlantic Forest. Biological Conservation, v. 277, p. 7-pg., 2022-12-14. (13/50741-7, 16/25358-3, 19/18335-5)

LIMA, NATALYA DE ARAUJO PEDROSA; REBOUCAS, RAONI; TOLEDO, LUIS FELIPE; LISBOA, CYBELE SABINO. Influence of urban noise in call traits of the Atlantic Forest treefrog Bokermannohyla hylax. ZOOLOGISCHER ANZEIGER, v. 300, p. 6-pg., 2022-07-19. (19/18335-5, 16/25358-3)

MOROTI, MATHEUS DE TOLEDO; SEVERGNINI, MARCOS RAFAEL; BOLOVON, JOAO PEDRO; TOLEDO, LUIS FELIPE; MUSCAT, EDELCIO. Filling the knowledge gaps of Paratelmatobius mantiqueira (Anura: Leptodactylidae): tadpole, acoustic repertoire, and life history traits. Journal of Natural History, v. 56, n. 37-40, p. 22-pg., 2022-10-18. (19/18335-5, 16/25358-3)

GREENSPAN, SASHA E.; PELOSO, PEDRO; FUENTES-GONZALEZ, JESUALDO A.; BLETZ, MOLLY; LYRA, MARIANA L.; MACHADO, IBERE F.; MARTINS, RENATO A.; MEDINA, DANIEL; MOURA-CAMPOS, DIEGO; NEELY, WESLEY J.; et al. Low microbiome diversity in threatened amphibians from two biodiversity hotspots. ANIMAL MICROBIOME, v. 4, n. 1, p. 9-pg., 2022-12-29. (13/50741-7, 14/16320-7, 16/25358-3, 19/18335-5)

DE ANDRADE, FELIPE SILVA; HAGA, ISABELLE AQUEMI; LYRA, MARIANA LUCIO; GAZONI, THIAGO; ZARACHO, VICTOR; BAPTISTA HADDAD, CELIO FERNANDO; TOLEDO, LUIS FELIPE; GIARETTA, ARIOVALDO ANTONIO. Geographic distributions ofPseudopaludicola bolivianaand congeneric long-legged species (Anura: Leiuperinae). Studies on Neotropical Fauna and Environment, v. 57, n. 1, p. 17-pg., 2020-09-10. (19/18335-5, 13/50741-7, 17/26162-8, 15/10728-7, 16/25358-3)

BARDIER, CECILIA; MANEYRO, RAUL; TOLEDO, LUIS FELIPE. The Correlates of in situ Larval Survivorship of the Threatened South American Toad Melanophryniscus montevidensis (Anura, Bufonidae). South American Journal of Herpetology, v. 17, n. 1, p. 33-42, AUG 2020. (14/23388-7, 19/18335-5, 16/25358-3)

MEDINA, DANIEL; GREENSPAN, SASHA E.; CARVALHO, TAMILIE; BECKER, C. GUILHERME; TOLEDO, LUIS FELIPE. Co-infecting pathogen lineages have additive effects on host bacterial communities. FEMS MICROBIOLOGY ECOLOGY, v. 97, n. 4, APR 2021. (19/18335-5, 18/08650-8, 16/25358-3)

DELAZERI, FRANCIELI; ERNETTI, JULIA R.; DE BASTIANI, VELUMA I. M.; LINGNAU, RODRIGO; TOLEDO, LUIS FELIPE; LUCAS, ELAINE M.. Forest cover influences chytrid infections in populations of Boana curupi, a threatened treefrog of south Brazil. DISEASES OF AQUATIC ORGANISMS, v. 144, p. 133-142, 2021. (20/02994-7, 16/25358-3, 19/18335-5)

ROTENBERG, ELSIE; MUSCAT, EDELCIO; STUGINSKI, DANIEL RODRIGUES; TOLEDO, LUIS FELIPE; MOROTI, MATHEUS DE TOLEDO. Paratelmatobius mantiqueira Pombal & Haddad, 1999 (Anura: Leptodactylidae): New specimens and rectification of the type locality of a rare species from the Serra da Mantiqueira, southeastern Brazil. Zootaxa, v. 4845, n. 3, p. 447-450, SEP 3 2020. (19/18335-5, 16/25358-3)

SALES, LILIAN P.; REBOUCAS, RAONI; TOLEDO, LUIS FELIPE. Native range climate is insufficient to predict anuran invasive potential. Biological Invasions, v. 23, n. 8, p. 2635-2647, AUG 2021. (19/18335-5, 16/25358-3)

FORTI, LUCAS RODRIGUEZ; SAMPAIO, MARIA RITA DE MELO; PIRES, CLARA RESENDE; SZABO, JUDIT K.; TOLEDO, LUIS FELIPE. Torrent frogs emit acoustic signals of a narrower spectral range in habitats with longer-lasting biotic background noise. Behavioural Processes, v. 200, p. 10-pg., 2022-07-08. (19/18335-5, 16/25358-3)

WEBB, REBECCA J.; ROBERTS, ALEXANDRA A.; WYLIE, STEPHEN; KOSCH, TIFFANY; TOLEDO, LUIS FELIPE; MERCES, MARCIA; SKERRATT, LEE F.; BERGER, LEE. on-detection of mycoviruses in amphibian chytrid fungus (Batrachochytrium dendrobatidis) from Australi. FUNGAL BIOLOGY, v. 126, n. 1, p. 75-81, JAN 2022. (16/25358-3, 19/18335-5)

DE ANDRADE, FELIPE SILVA; HAGA, ISABELLE AQUEMI; FERREIRA, JOHNNY SOUSA; RECCO-PIMENTEL, SHIRLEI MARIA; TOLEDO, LUIS FELIPE; BRUSCHI, DANIEL PACHECO. A new cryptic species of Pithecopus (Anura, Phyllomedusidae) in north-eastern Brazil. EUROPEAN JOURNAL OF TAXONOMY, v. 723, p. 108-134, NOV 4 2020. (15/10728-7, 16/25358-3, 19/18335-5)

MCDONALD, COBY A.; BECKER, C. GUILHERME; LAMBERTINI, CAROLINA; TOLEDO, L. FELIPE; HADDAD, CELIO F. B.; ZAMUDIO, KELLY R.. Host immune responses to enzootic and invasive pathogen lineages vary in magnitude, timing, and efficacy. Molecular Ecology, v. 32, n. 9, p. 19-pg., 2023-03-02. (16/25358-3, 19/18335-5)

REBOUCAS, RAONI. White-edged cowards: high-pitched treefrogs will be attacked by those with orange legs. BEHAVIOUR, v. 160, n. 1, p. 25-pg., 2023-12-01. (16/25358-3, 19/18335-5)

DA SILVA MARTINS, ANA GLAUCIA; REBOUCAS, RAONI; SANTOS, ISAIAS; ROSA DOMINGOS, ADAO HENRIQUE; TOLEDO, LUIS FELIPE. Influence of tail injury on the development of Neotropical elegant treefrog tadpoles. Acta Herpetologica, v. 17, n. 1, p. 8-pg., 2022-06-01. (16/25358-3, 19/18335-5)

TOLEDO, LUIS FELIPE; ZANOTTI, ALEXANDRE P.; DE LIMA SILVA BEZERRA, LISANDRA MARIA; ABRAHAO, CARLOS; LISBOA, CYBELE SABINO. Occasional herpetofaunal introductions into and from the archipelago of Fernando de Noronha, Brazil. SPIXIANA, v. 45, n. 2, p. 5-pg., 2023-02-01. (16/25358-3, 19/18335-5)

RIBEIRO, LUISA P.; TOLEDO, LUIS FELIPE. An overview of the Brazilian frog farming. Aquaculture, v. 548, n. 2, FEB 15 2022. (16/25358-3, 19/18335-5, 18/23622-0)