Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-24T00:06:47.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular and morphological description of the first Hepatozoon (Apicomplexa: Hepatozoidae) species infecting a neotropical turtle, with an approach to its phylogenetic relationships

Published online by Cambridge University Press:  04 February 2021

Germán A. Gutiérrez-Liberato Open the ORCID record for Germán A. Gutiérrez-Liberato [Opens in a new window] ,
Ingrid A. Lotta-Arévalo ,
Cristian C. Rodríguez-Almonacid ,
Mario Vargas-Ramírez  and
Nubia E. Matta
Germán A. Gutiérrez-Liberato
Affiliation:
Facultad de Ciencias, Departamento de Biología, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia Facultad de Medicina, Departamento de Salud Pública, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia
Ingrid A. Lotta-Arévalo
Affiliation:
Facultad de Ciencias, Departamento de Biología, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia
Cristian C. Rodríguez-Almonacid
Affiliation:
Facultad de Ciencias, Departamento de Biología, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia
Mario Vargas-Ramírez
Affiliation:
Facultad de Ciencias, Estación de Biología Tropical Roberto Franco (EBTRF), Universidad Nacional de Colombia, Carrera 33 #33 −76, Villavicencio500005 Meta, Colombia Instituto de Genética, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia
Nubia E. Matta*
Affiliation:
Facultad de Ciencias, Departamento de Biología, Universidad Nacional de Colombia, Sede Bogotá. Carrera 30 No. 45-03, Bogotá111321, Colombia
*
Author for correspondence: Nubia E. Matta, E-mail: nemattac@unal.edu.co
Get access Rights & Permissions [Opens in a new window]

Abstract

Haemogregarines (Adeleorina) have a high prevalence in turtles. Nevertheless, there is only one Hepatozoon species described that infects Testudines so far; it is Hepatozoon fitzsimonsi which infects the African tortoise Kinixys belliana. Colombia harbours a great diversity of chelonians; however, most of them are threatened. It is important to identify and characterize chelonian haemoparasite infections to improve the clinical assessments, treatments and the conservation and reintroduction programs of these animals. To evaluate such infections for the Colombian wood turtle Rhinoclemmys melanosterna, we analysed blood from 70 individuals. By using the morphological characteristics of blood stages as well as molecular information (18S rRNA sequences), here we report a new Hepatozoon species that represents the first report of a hepatozoid species infecting a semi-aquatic continental turtle in the world. Although the isolated lineage clusters within the phylogenetic clades that have morphological species of parasites already determined, their low nodal support makes their position within each group inconclusive. It is important to identify new molecular markers to improve parasite species identification. In-depth research on blood parasites infecting turtles is essential for increasing knowledge that could assess this potential unknown threat, to inform the conservation of turtles and for increasing the state of knowledge on parasites.

Keywords

18S rRNAAdeleorinaChelonian blood parasitesHaemogregarinesHepatozoon new species
Type
Research Article
Information
Parasitology , Volume 148 , Issue 6 , May 2021 , pp. 747 - 759
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ball, GH (1967) Some blood sporozoans from East African reptiles. The Journal of Protozoology 14, 198–210. doi: 10.1111/j.1550-7408.1967.tb01983.xCrossRefGoogle ScholarPubMed
Ball, GH, Chao, J and Telford, SR Jr (1967) The life history of Hepatozoon Rarefaciens (Sambon and Seligmann, 1907) from Drymarchon Corais (Colubridae), and its experimental transfer to Constrictor Constrictor (Boidae). The Journal of Parasitology 53, 897–909 doi: 10.2307/3276805CrossRefGoogle Scholar
Barta, JR, Ogedengbe, JD, Martin, DS and Smith, TG (2012) Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology 59, 171–180.CrossRefGoogle ScholarPubMed
Bensch, S, Stjernman, M, Hasselquist, D, Örjan, Ö, Hannson, B, Westerdahl, H and Pinheiro, RT (2000) Host specificity in avian blood parasites: a study of Plasmodium And Haemoproteus Mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London. Series B: Biological Sciences 267, 1583–1589.CrossRefGoogle ScholarPubMed
Borges-Nojosa, DM, Borges-Leite, MJ, Maia, JP, Zanchi-Silva, D, da Rocha Braga, R and Harris, DJ (2017) A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas Nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil. Systematic Parasitology 94, 65–72.CrossRefGoogle Scholar
Börner, C (1901) Untersuchungen über Hämosporidien. I. Ein Beitrag zur Kenntnis des genus Haemogregarina Danilewsky. Z Wiss Zool Abt A 69, 398–416.Google Scholar
Borner, J, Pick, C, Thiede, J, Kolawole, OM, Kingsley, MT, Schulze, J, Cottontail, VM, Wellinghausen, N, Schmidt-Chanasit, J and Bruchhaus, I (2016) Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Molecular Phylogenetics and Evolution 94, 221–231.CrossRefGoogle ScholarPubMed
Carini, A (1909) Sur une hémogrégarine du Caiman Latirostris Daud. Bulletin de la Société de Pathologie Exotique 2, 471–472.Google Scholar
Clark, GM (1958) Hepatozoon griseisciuri N. sp.; a new species of Hepatozoon from the grey squirrel (Sciurus carolinensis Gmelin, 1788), with studies on the life cycle. The Journal of Parasitology 44, 52–63.10.2307/3274829CrossRefGoogle Scholar
Cook, CA, Smit, NJ and Davies, AJ (2009) A redescription of Haemogregarina Fitzsimonsi Dias, 1953 and some comments on Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) from southern African tortoises (Cryptodira: Testudinidae), with new host data and distribution records. Folia Parasitologica 56, 173–179.CrossRefGoogle Scholar
Cook, CA, Lawton, SP, Davies, AJ and Smit, NJ (2014) Reassignment of the land tortoise haemogregarine Haemogregarina Fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S rDNA sequence fragments. Parasitology 141, 1611–1620. doi: 10.1017/S003118201400081XCrossRefGoogle Scholar
Cook, CA, Netherlands, EC and Smit, NJ (2015) First Hemolivia from southern Africa: reassigning chelonian Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (Adeleorina: Karyolysidae). African Zoology 50, 165–173.CrossRefGoogle Scholar
Cook, CA, Netherlands, EC and Smit, NJ (2016) Redescription, molecular characterisation and taxonomic re-evaluation of a unique African monitor lizard haemogregarine Karyolysus paradoxa (Dias, 1954) n. comb. (Karyolysidae). Parasites & Vectors 9, 347.CrossRefGoogle Scholar
da Costa, SCG, Pessoa, SB, de Pereira, NM and Colombo, T (1973) The life history of Hepatozoon Leptodactyli (Lesage, 1908) Pessoa, 1970: a parasite of the common laboratory animal: the frog of the genus Leptodactylus. Memórias do Instituto Oswaldo Cruz 71, 1–8.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
Desser, SS (1990) Tissue “cysts” of Hepatozoon Griseisciuri in the grey squirrel, Sciurus carolinensis: the significance of these cysts in species of Hepatozoon. The Journal of parasitology, 76, 257–259. doi: 10.2307/3283027.Google ScholarPubMed
Desser, SS (1997) Blood parasites of the iguanid lizard, Ctenosaura similis from Costa Rica, with a description of Hepatozoon Gamezi n. sp. Journal of Eukaryotic Microbiology 44, 162–167.10.1111/j.1550-7408.1997.tb05954.xCrossRefGoogle Scholar
Dvořáková, N, Kvičerová, J, Hostovský, M and Široký, P (2015) Haemogregarines of freshwater turtles from Southeast Asia with a description of Haemogregarina Sacaliae sp. n. and a redescription of Haemogregarina pellegrini Laveran and Pettit, 1910. Parasitology 142, 816–826.10.1017/S0031182014001930CrossRefGoogle Scholar
Eldridge, BF (2004) The epidemiology of arthropod borne diseases. In Eldridge, BF and Edman, JD (eds), Medical Entomology: A Textbook on Public Health and Veterinary Problems Caused by Arthropods. New York, USA: Springer, pp. 165–185.10.1007/978-94-007-1009-2_6CrossRefGoogle Scholar
Escalante, AA, Freeland, DE, Collins, WE and Lal, AA (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences 95, 8124–8129.CrossRefGoogle ScholarPubMed
González, LP, Pacheco, MA, Escalante, AA, Maldonado, ADJ, Cepeda, AS, Rodríguez-Fandiño, OA, Vargas-Ramírez, M and Matta, NE (2019) Haemocystidium spp., a species complex infecting ancient aquatic turtles of the family Podocnemididae: First report of these parasites in Podocnemis Vogli from the Orinoquia. International Journal for Parasitology: Parasites and Wildlife 10, 299–309.Google ScholarPubMed
Guindon, S, Delsuc, F, Dufayard, J-F and Gascuel, O (2009) Estimating maximum likelihood phylogenies with PhyML. In Posada, D. (ed), Bioinformatics for DNA Sequence Analysis. Methods in Molecular Biology (Methods and Protocols). New Jersey, USA: Humana Press, pp. 113–137.10.1007/978-1-59745-251-9_6CrossRefGoogle Scholar
Han, H, Wu, Y, Dong, H, Zhu, S, Li, L, Zhao, Q, Wu, D, Pei, E, Wang, Y and Huang, B (2015) First report of Hepatozoon (Apicomplexa: Adeleorina) from king ratsnakes (Elaphe carinata) in Shanghai, with description of a new species. Acta Parasitologica 60, 266–274.CrossRefGoogle ScholarPubMed
Hayes, PM and Smit, NJ (2019) Molecular insights into the identification and phylogenetics of the cosmopolitan marine fish blood parasite, Haemogregarina bigemina (Adeleorina: Haemogregarinidae). International Journal for Parasitology: Parasites and Wildlife 8, 216–220.Google Scholar
Hoare, CA (1924) Hepatozoon adiei, n. sp. A blood parasite of an Indian eagle. Transactions of the Royal Society of Tropical Medicine and Hygiene 18, 63–66.CrossRefGoogle Scholar
Hwang, U-W and Kim, W (1999) General properties and phylogenetic utilities of nuclear ribosomal DNA and mitochondrial DNA commonly used in molecular systematics. The Korean Journal of Parasitology 37, 215–228.CrossRefGoogle ScholarPubMed
Javanbakht, H, Široký, P, Mikulíček, P and Sharifi, M (2015) Distribution and abundance of Hemolivia mauritanica (Apicomplexa: Haemogregarinidae) and its vector Hyalomma aegyptium in tortoises of Iran. Biologia 70, 229–234.10.1515/biolog-2015-0024CrossRefGoogle Scholar
Karadjian, G, Chavatte, J-M and Landau, I (2015) Systematic revision of the adeleid haemogregarines, with creation of Bartazoon N. g., reassignment of Hepatozoon Argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite 22, 22–31. doi: 10.1051/parasite/2015031Google Scholar
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.10.1093/nar/gkf436CrossRefGoogle ScholarPubMed
Kauffman, KL, Sparkman, A, Bronikowski, AM and Palacios, MG (2017) Vertical transmission of Hepatozoon in the garter snake Thamnophis elegans. Journal of Wildlife Diseases 53, 121–125.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kvičerová, J, Hypša, V, Dvořáková, N, Mikulíček, P, Jandzik, D, Gardner, MG, Javanbakht, H, Tiar, G and Široký, P (2014) Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist 165, 688–700.CrossRefGoogle ScholarPubMed
Landau, I, Michel, J, Chabaud, A and Brygoo, E (1972) Cycle biologique d’Hepatozoon Domerguei; discussion sur les caractères fondamentaux d'un cycle de Coccidie. Zeitschrift für Parasitenkunde 38, 250–270.10.1007/BF00329601CrossRefGoogle Scholar
Léveillé, AN, Ogedengbe, ME, Hafeez, MA, Tu, H-HA and Barta, JR (2014) The complete mitochondrial genome sequence of Hepatozoon Catesbianae (Apicomplexa: Coccidia: Adeleorina), a blood parasite of the green frog, Lithobates (Formerly Rana) clamitans. Journal of Parasitology 100, 651–657.CrossRefGoogle ScholarPubMed
Léveillé, AN, El Skhawy, N and Barta, JR (2020) Multilocus sequencing of Hepatozoon Cf. griseisciuri Infections in Ontario eastern gray squirrels (Sciurus carolinensis) uncovers two genotypically distinct sympatric parasite species. Parasitology Research 119, 713–724.CrossRefGoogle ScholarPubMed
Lotta, IA, Valkiūnas, G, Pacheco, MA, Escalante, AA, Hernández, SR and Matta, NE (2019) Disentangling Leucocytozoon Parasite diversity in the neotropics: descriptions of two new species and shortcomings of molecular diagnostics for leucocytozoids. International Journal for Parasitology: Parasites and Wildlife 9, 159–173.Google ScholarPubMed
Mackerras, MJ (1962) The life of a Hepatozoon (Sporozoa: Adeleidea) of varanid Lizards in Australia. Australian Journal of Zoology 10, 35–44.CrossRefGoogle Scholar
Maia, JP, Carranza, S and Harris, DJ (2016) Comments on the systematic revision of adeleid haemogregarines: are more data needed? Journal of Parasitology 102, 549–552.CrossRefGoogle ScholarPubMed
Martinsen, ES, Perkins, SL and Schall, JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium And closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.10.1016/j.ympev.2007.11.012CrossRefGoogle ScholarPubMed
Matta, NE, González, LP, Pacheco, MA, Escalante, AA, Moreno, AM, González, AD and Calderón-Espinosa, ML (2018) Plasmodium parasites in reptiles from the Colombia Orinoco-Amazon basin: a re-description of Plasmodium Kentropyxi Lainson R, Landau I, Paperna I, 2001 and Plasmodium Carmelinoi Lainson R, Franco CM, da Matta R, 2010. Parasitology Research 117, 1357–1370.CrossRefGoogle Scholar
Merino, S, Martínez, J, Masello, JF, Bedolla, Y and Quillfeldt, P (2014) First molecular characterization of a Hepatozoon species (Apicomplexa: Hepatozoidae) infecting birds and description of a new species infecting storm petrels (Aves: Hydrobatidae). The Journal of Parasitology 100, 338–343.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees, 1–8. doi: 10.1109/GCE.2010.5676129.Google Scholar
Netherlands, EC, Cook, CA, Du Preez, LH, Vanhove, MP, Brendonck, L and Smit, NJ (2018) Monophyly of the species of Hepatozoon (Adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitology 145, 1039–1050.CrossRefGoogle ScholarPubMed
O'Dwyer, LH, Moço, TC, dos Santos Paduan, K, Spenassatto, C, da Silva, RJ and Ribolla, PEM (2013) Description of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from Rattlesnakes (Crotalus Durissus terrificus) based on molecular, morphometric and morphologic characters. Experimental Parasitology 135, 200–207.CrossRefGoogle ScholarPubMed
Ogedengbe, JD, Hanner, RH and Barta, JR (2011) DNA Barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). International Journal for Parasitology 41, 843–850.CrossRefGoogle Scholar
Pacheco, MA, Matta, NE, Valkiūnas, G, Parker, PG, Mello, B, Stanley, CE Jr, Lentino, M, Garcia-Amado, MA, Cranfield, M and Kosakovsky Pond, SL (2017) Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Molecular Biology and Evolution 35, 383–403.CrossRefGoogle Scholar
Perkins, SL (2008) Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria. DNA Sequence 19, 471–478.CrossRefGoogle ScholarPubMed
Pessoa, S (1967) Notas sobre hemogregarinas de serpentes brasileiras. III: novas observações sobre hemogregarinas de serpentes das famílias Colubridae e Crotalidae. Revista Brasileira de Biologia 27, 159–164.Google Scholar
Pineda-Catalan, O, Perkins, SL, Peirce, MA, Engstrand, R, Garcia-Davila, C, Pinedo-Vasquez, M and Aguirre, AA (2013) Revision of hemoproteid genera and description and redescription of two species of chelonian hemoproteid parasites. The Journal of Parasitology 99, 1089–1098.CrossRefGoogle ScholarPubMed
Rambaut, A and Drummond, A (2010) FigTree v1. 3.1 Institute of Evolutionary Biology. University of Edinburgh.Google Scholar
Rambaut, A, Suchard, M, Xie, D and Drummond, A (2013) Tracer 1.6. Edinburgh, UK: University of Edinburgh.Google Scholar
Rodríguez, OA and Matta, NE (2001) Blood parasites in some birds from eastern plains of Colombia. Memorias do Instituto Oswaldo Cruz 96, 1173–1176.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rossow, JA, Hernandez, SM, Sumner, SM, Altman, BR, Crider, CG, Gammage, MB, Segal, KM and Yabsley, MJ (2013) Haemogregarine infections of three species of aquatic freshwater turtles from two sites in Costa Rica. International Journal for Parasitology: Parasites and Wildlife 2, 131–135.Google ScholarPubMed
Rueda-Almonacid, JV, Carr, JL, Mittermeier, RA, Rodríguez-Mahecha, JV, Mast, RB, Vogt, RC, Rhodin, AG, de la Ossa-Velásquez, J, Rueda, JN and Mittermeier, CG (2007) Las tortugas y los cocodrilianos de los países andinos del trópico. Serie de guías tropicales de campo 6, 412–423.Google Scholar
Smith, TG (1996) The genus Hepatozoon (Apicomplexa: adeleina). The Journal of Parasitology, 82, 565–585. doi: 10.2307/3283781.Google Scholar
Smith, T, Desser, S and Martin, D (1994) The development of Hepatozoon Sipedon sp. nov. (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the Northern water snake (Nerodia Sipedon sipedon), in the culicine vectors Culex Pipiens and C. territans, and in an intermediate host, the Northern leopard frog (Rana Pipiens). Parasitology Research 80, 559–568.CrossRefGoogle Scholar
Soares, P, Borghesan, TC, Tavares, LER, Ferreira, VL, Teixeira, MMG and Paiva, F (2017) Hepatozoon caimani Carini, 1909 (Adeleina: Hepatozoidae) in wild population of Caiman Yacare Daudin, 1801 (Crocodylia: Alligatoridae), Pantanal, Brazil. Parasitology Research 116, 1907–1916.10.1007/s00436-017-5467-1CrossRefGoogle Scholar
Telford, SR Jr (2008) Hemoparasites of the Reptilia. Color Atlas and Text. Boca Raton, Florida: CRC Press, Taylor and Francis Group, pp. 376.Google Scholar
Ujvari, B, Madsen, T and Olsson, M (2004) High prevalence of Hepatozoon Spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670–672.CrossRefGoogle ScholarPubMed
Úngari, LP, Santos, ALQ, O'Dwyer, LH, da Silva, MRL, de Melo Fava, NN, Paiva, GCM, de Pinto, RMC and Cury, MC (2018) Haemogregarina podocnemis sp. nov.: description of a new species of Haemogregarina Danilewsky 1885 (Adeleina: Haemogregarinaidae) in free-living and captive yellow-spotted river turtles Podocnemis Unifilis (Testudines: Podocnemididae) from Brazil. Parasitology Research 117, 1535–1548.10.1007/s00436-018-5817-7CrossRefGoogle ScholarPubMed
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Ratón, Florida: CRC Press.Google Scholar
Valkiūnas, G, Mobley, K and Iezhova, TA (2016) Hepatozoon ellisgreineri N. sp. (Hepatozoidae): description of the first avian apicomplexan blood parasite inhabiting granulocytes. Parasitology Research 115, 609–613.10.1007/s00436-015-4777-4CrossRefGoogle Scholar
Vargas-Ramirez, M, Carr, JL and Fritz, U (2013) Complex phylogeography in Rhinoclemmys Melanosterna: conflicting mitochondrial and nuclear evidence suggests past hybridization (Testudines: Geoemydidae). Zootaxa 3670, 238–254.CrossRefGoogle Scholar
Wenyon, CM (1926) Protozoology. A Manual for Medical Men, Veterinarians and Zoologists, vol. 2. London, UK: Tindall & Cox.CrossRefGoogle Scholar
Witsenburg, F, Salamin, N and Christe, P (2012) The evolutionary host switches of Polychromophilus: a multi-gene phylogeny of the bat malaria genus suggests a second invasion of mammals by a haemosporidian parasite. Malaria Journal 11, 53.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gutiérrez-Liberato et al. supplementary material

Gutiérrez-Liberato et al. supplementary material 1

Download Gutiérrez-Liberato et al. supplementary material(File)
File 67 KB
Supplementary material: File

Gutiérrez-Liberato et al. supplementary material

Gutiérrez-Liberato et al. supplementary material 2

Download Gutiérrez-Liberato et al. supplementary material(File)
File 12.5 KB
Supplementary material: File

Gutiérrez-Liberato et al. supplementary material

Gutiérrez-Liberato et al. supplementary material 3

Download Gutiérrez-Liberato et al. supplementary material(File)
File 19 KB
Supplementary material: Image

Gutiérrez-Liberato et al. supplementary material

Gutiérrez-Liberato et al. supplementary material 4

Download Gutiérrez-Liberato et al. supplementary material(Image)
Image 74.5 MB
Supplementary material: Image

Gutiérrez-Liberato et al. supplementary material

Gutiérrez-Liberato et al. supplementary material 5

Download Gutiérrez-Liberato et al. supplementary material(Image)
Image 15.7 MB