ABSTRACT
Peru holds a high mammalian diversity in its Amazonian region, with 326 species. However, our knowledge about the actual diversity is still considered incomplete, and the molecular information for those species in genetic databases is even less comprehensive. To assess the availability of genetic information for Peruvian Amazonian mammals relative to known diversity, we surveyed the Amazonian mammals with at least one molecular marker in the most widely used repositories for nucleotide sequences, GenBank and BOLD Systems. Our survey focused on widely used molecular markers in evolutionary biology-cytochrome b [cyt-b], cytochrome oxidase I [COI], 12S ribosomal RNA [12S], and the mitogenome [mit]-derived from Peruvian Amazon mammals. Additionally, to gain insights into the current mammalian sampling effort in Peruvian Amazonia, we generated a map of unique sampling localities and a heat map, utilizing 41951 records, which identified six major information gaps. This comprehensive analysis found 1597 genetic sequences corresponding to 180 mammalian species (55.2% of Peruvian Amazonian species): COI (38 species), cyt-b (167 species), 12S (56 species), and mitogenome (16 species). Taxonomically, Rodentia (53 species, four markers), Chiroptera (63 species, three markers), and Didelphimorphia (27 species, four markers) represented most molecular data, with a concentration of molecular markers in the orders Chiroptera (703) and Rodentia (499). Geographically, the Loreto department has the largest genetic information (530 records, 99 species). These results confirm a worrying underrepresentation of Peruvian Amazonian diversity in molecular databases. Consequently, we advocate for the use of scientific collections as an alternative source to systematically generate genetic information for the Amazonian mammal diversity in Peru to compensate for the current underrepresentation.
KEY WORDS:
Biodiversity; barcoding; bioinformatics; museomics; Neotropics
INTRODUCTION
The western Amazonian subdivision of the Neotropical lowland rainforests was defined by Wallace (1854Wallace AR (1854) On the monkeys of the Amazon. Proceedings of the Zoological Society of London 1852: 107-110.) as the region that extends west of the Rio Negro and Rio Madeira. Zoogeographically, it was recognized as a western Amazonian subregion by Voss and Emmons (1996Voss RS, Emmons L (1996) Mammalian diversity in Neotropical lowland rainforests: A preliminary assessment. Bulletin of the American Museum of Natural History 230: 1-115.). This subregion is renowned for its status as a biodiversity hotspot, particularly for several faunistic groups (Erwin et al. 2004Erwin TL, Pimienta MC, Murillo OE, Aschero V (2004) Mapping patterns of β-diversity for beetles across the western Amazon basin: A preliminary case for improving conservation strategies. Proceedings of the California Academy of Sciences 56: 72-85., Stotz et al. 1996Stotz DF, Fitzpatrick JW, Parker TE III, Moskowitz DK (1996) Neotropical birds, ecology, and conservation. University of Chicago Press, Chicago, 502 pp., Young et al. 2004Young BE, Stuart SN, Chanson JS, Cox NA, Boucher TM (2004) Disappearing jewels: The status of New World amphibians. NatureServe, Arlington, 60 pp., Ceballos and Ehrlich 2006Ceballos G, Ehrlich PR (2006) Global mammal distributions, biodiversity hotspots, and conservation. Proceedings of the National Academy of Sciences 103: 19374-19379.), and it stands out as the most biodiverse Amazonian subregion for mammals (Voss and Emmons 1996, Arévalo-Sandi et al. 2021Arévalo-Sandi AR, Gonçalves ALS, Onizawa K, Yabe T, Spironello WR (2021) Mammal diversity among vertical strata and the evaluation of a survey technique in a central Amazonian forest. Papéis Avulsos de Zoologia 61: e20216133. https://doi.org/10.11606/1807-0205/2021.61.33
https://doi.org/10.11606/1807-0205/2021....
, Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
).
Situated below 1000 m above sea level (m.a.s.l.), western Amazonia has an annual rainfall of more than 2000 mm (FAO 1988FAO (1988) FAO/Unesco soil map of the world, revised legend, with corrections and updates. World Soil Resources Report 60. FAO, Rome, 119 pp., Voss and Emmons 1996Voss RS, Emmons L (1996) Mammalian diversity in Neotropical lowland rainforests: A preliminary assessment. Bulletin of the American Museum of Natural History 230: 1-115., Cavalcante et al. 2020Cavalcante RBL, Ferreira DBS, Pontes PRM, Tedeschi RG, da Costa CPW, de Souza EB (2020) Evaluation of extreme rainfall indices from CHIRPS precipitation estimates over the Brazilian Amazonia. Atmospheric Research 238: 104879. https://doi.org/10.1016/j.atmosres.2020.104879
https://doi.org/10.1016/j.atmosres.2020....
). Notably, unlike other Amazonian subregions, it presents extensive areas of intact tropical humid forest, and it is likely to maintain stable climatic conditions in the face of global warming (Killeen et al. 2007Killeen TJ, Douglas M, Consiglio T, Jørgensen PM, Mejia J (2007) Dry spots and wet spots in the Andean hotspot. Journal of Biogeography 34(8): 1357-1373. https://doi.org/10.1111/j.1365-2699.2006.01682.x
https://doi.org/10.1111/j.1365-2699.2006...
). However, the region faces significant threats from anthropogenic activities, including human population growth, an increase in transportation routes (e.g., the Interoceánica highway), illegal mining, and deforestation. These activities cause pollution, habitat destruction, and biodiversity loss, which threatens the sustainability of resources in the region (Fearnside 1996Fearnside PM (1996) Amazonian deforestation and global warming: Carbon stocks in vegetation replacing Brazil’s Amazon forest. Forest Ecology and Management 80(1): 21-34. https://doi.org/10.1016/0378-1127(95)03647-4
https://doi.org/10.1016/0378-1127(95)036...
, 2006Fearnside PM (2006) tropical deforestation and global warming. Science 312(5777): 1137-1137. https://doi.org/10.1126/science.312.5777.1137c
https://doi.org/10.1126/science.312.5777...
, García-Dávila et al. 2014García-Dávila CR, Castro-Ruiz D, Sánchez-Ribeiro H, Ismiño-Orbe RA, Rengifo-Trigoso D, García-Vásquez A, Tello-Martín JS, Chota-Macuyama W, Duponchelle F, Renno JF (2014) Diversidad de ictioplancton en los ríos Curaray, Arabela y Napo (Amazonía peruana). Folia Amazónica 23(1): 67-78. https://doi.org/10.24841/fa.v23i1.9
https://doi.org/10.24841/fa.v23i1.9...
, 2015García-Dávila C, Castro-Ruiz D, Renno J-F, Chota-Macuyama W, Carvajal-Vallejos FM, Sanchez H, et al. (2015) Using barcoding of larvae for investigating the breeding seasons of pimelodid catfishes from the Marañón, Napo and Ucayali rivers in the Peruvian Amazon. Journal of Applied Ichthyology 31(S4): 40-51. https://doi.org/10.1111/jai.12987
https://doi.org/10.1111/jai.12987...
) and the survival of many indigenous ethnic groups, which have proven to contribute with the conservation of biota (Orta-Martínez and Finer 2010Orta-Martínez M, Finer M (2010) Oil frontiers and indigenous resistance in the Peruvian Amazon. Ecological Economics 70(2): 207-218. https://doi.org/10.1016/j.ecolecon.2010.04.022
https://doi.org/10.1016/j.ecolecon.2010....
, Fernández-Llamazares et al. 2021Fernández-Llamazares Á, López-Baucells A, Velazco PM, Gyawali A, Rocha R, Terraube J, Cabeza M (2021) The importance of indigenous territories for conserving bat diversity across the Amazon biome. Perspectives in Ecology and Conservation 19(1): 10-20. https://doi.org/10.1016/j.pecon.2020.11.001
https://doi.org/10.1016/j.pecon.2020.11....
, Villén-Pérez et al. 2022Villén-Pérez S, Anaya-Valenzuela L, Conrado da Cruz D, Fearnside PM (2022) Mining threatens isolated indigenous peoples in the Brazilian Amazon. Global Environmental Change 72(102398): 1-11. https://doi.org/10.1016/j.gloenvcha.2021.102398
https://doi.org/10.1016/j.gloenvcha.2021...
).
The Peruvian Amazonia has an area of 661,000 km2 (Oliveira et al. 2007Oliveira PJC, Asner GP, Knapp DE, Almeyda A, Galván-Gildemeister R, Keene S, Raybin RF, Smith RC (2007) Land-use allocation protects the Peruvian Amazon. Science 317(5842): 1233-1236. https://doi.org/10.1126/science.1146324
https://doi.org/10.1126/science.1146324...
) and belongs to the Selva baja ecoregion (sensu Brack-Egg 1986Brack-Egg A (1986) Las ecorregiones del Perú. Boletín de Lima 44: 57-70.). This ecoregion, characterized by a tropical lowland forest ecosystem situated on the eastern flank of the Andes, spans across several departments, including Loreto, Ucayali, Madre de Dios, and portions of the Amazonas, Ayacucho, Cajamarca, Cusco, Huancavelica, Huánuco, Junín, Pasco, San Martín, and Puno (Finer et al. 2008Finer M, Jenkins CN, Pimm SL, Keane B, Ross C (2008) Oil and gas projects in the western Amazon: threats to wilderness, biodiversity, and indigenous peoples. Plos One 3(8): e2932. https://doi.org/10.1371/journal.pone.0002932
https://doi.org/10.1371/journal.pone.000...
). Also, this ecoregion harbors an impressive diversity of mammals, with 326 species equivalents to 56.50 % of the total Peruvian mammal species (Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
, Rengifo et al. 2022Rengifo EM, D’Elía G, García G, Charpentier E, Cornejo FM (2022) A new species of titi monkey, genus Cheracebus Byrne et al., 2016 (Primates: Pitheciidae), from Peruvian Amazonia. Mammal Study 48(1): 1-16. https://doi.org/10.3106/ms2022-0019
https://doi.org/10.3106/ms2022-0019...
). Despite this substantial diversity and the pivotal ecological roles played by mammals in their ecosystems, their current diversity is still underestimated (Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
) and their molecular information is even less comprehensive (Noreña et al. 2018Noreña A, González Muñoz A, Mosquera-Rendón J, Botero K, Cristancho MA (2018) Colombia, an unknown genetic diversity in the era of Big Data. BMC Genomics 19(Suppl. 8): 61-73. https://doi.org/10.1186/s12864-018-5194-8
https://doi.org/10.1186/s12864-018-5194-...
). This lack of information is also mirrored at the regional level since the diversity of mammals in only two departments was thoroughly analyzed: the Loreto department with 261 species of mammals (Diaz et al. 2021Diaz S, Sánchez-Vendizú P, Graham-Angeles L, Pacheco V (2021) Diversidad y conservación de los mamíferos mayores de Loreto, Perú. Revista Peruana de Biología 28(especial): 269-302. https://doi.org/10.15381/rpb.v28iespecial.21910
https://doi.org/10.15381/rpb.v28iespecia...
, Graham-Angeles et al. 2021Graham-Angeles L, Sánchez-Vendizú P, Diaz S, Pacheco V (2021) Diversidad y conservación de los murciélagos de Loreto, Perú. Revista Peruana de Biología 28(especial): 1-56. https://doi.org/10.15381/rpb.v28iespecial.21917
https://doi.org/10.15381/rpb.v28iespecia...
, Sánchez-Vendizú et al. 2021Sánchez-Vendizú P, Graham-Angeles L, Diaz S, Pacheco V (2021) Diversidad y estado de conservación de pequeños mamíferos de Loreto, Perú. Revista Peruana de Biología 28(special): e21907. https://doi.org/10.15381/rpb.v28iespecial.21907
https://doi.org/10.15381/rpb.v28iespecia...
) and the Ucayali department with 192 species (Quintana et al. 2009Quintana H, Pacheco V, Salas E (2009) Diversidad y conservación de los mamíferos de Ucayali, Perú. Ecología Aplicada 8(1-2): 91-103.); however, the molecular information available for the species of mammals occurring in both departments were not estimated.
Biodiversity assessments and the molecular information on species are critical to prioritizing conservation strategies (Karp et al. 1997Karp A, Edwards KJ, Bruford M, Funk S, Vosman B, Morgante M, Seberg O, Kremer A, Boursot P, Arctander P, Tautz D, Hewitt GM (1997) Molecular technologies for biodiversity evaluation: Opportunities and challenges. Nature Biotechnology 15(7): 625-628. https://doi.org/10.1038/nbt0797-625
https://doi.org/10.1038/nbt0797-625...
, Arif and Khan 2009Arif IA, Khan HA (2009) Molecular markers for biodiversity analysis of wildlife animals: A brief review. Animal Biodiversity and Conservation 32(1): 9-17.). In this contribution, we aim to update our knowledge of the diversity of mammals throughout the Peruvian Amazonia by identifying regions with limited or no mammal records, and assessing the quantity of genetic information available for mammalian specimens collected in the Peruvian Amazonian region in the most used public databases, Barcode of Life Data Systems (BOLD) and National Center for Biotechnology Information (NCBI; GenBank).
MATERIAL AND METHODS
Study area
The Peruvian Amazonian region encompasses the territory on the eastern flank of the Andes, below 1000 m.a.s.l., which is equivalent to the “lowland rainforest” (sensu Voss and Emmons 1996Voss RS, Emmons L (1996) Mammalian diversity in Neotropical lowland rainforests: A preliminary assessment. Bulletin of the American Museum of Natural History 230: 1-115.). The biogeographic studies have also divided the lowland rainforest into two ecoregions: “selva baja” and “sabana de palmeras” (sensu Brack-Egg 1986Brack-Egg A (1986) Las ecorregiones del Perú. Boletín de Lima 44: 57-70.) or recently into three: “Bosque Húmedo Amazónico”, “Bosque Muy Húmedo Premontano”, and “Bosque Seco Oriental” (sensu Britto 2017Britto B (2017) Actualización de las ecorregiones terrestres de Perú propuestas en el Libro Rojo de plantas endémicas del Perú. Gayana Botánica 74(1): 15-29. https://doi.org/10.4067/S0717-66432017005000318
https://doi.org/10.4067/S0717-6643201700...
). The Peruvian Amazonia contains several major river basins, such as the Marañón River (1414 km) and the Ucayali River (1771 km), which join to form the Amazonas River with an extension of 713 km in Peruvian territory.
Specimen records
A preliminary mammal species list was built based on Gardner (2007Gardner AL (2007) Mammals of South America. University of Chicago Press, Chicago, vol. 1, 669 pp.), Pacheco et al. (2009Pacheco V, Cadenillas R, Salas E, Tello C, Zeballos H (2009) Diversidad y endemismo de los mamíferos del Perú. Revista Peruana de Biología 16(1): 5-32., 2020Pacheco V, Graham-Angeles L, Diaz S, Hurtado CM, Ruelas D, Cervantes OK, Serrano JE (2020) Diversidad y distribución de los mamíferos del Perú por departamentos y ecorregiones I. Revista Peruana de Biología 27(3): 289-328. https://doi.org/10.15381/rpb.v27i3.18356
https://doi.org/10.15381/rpb.v27i3.18356...
, 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
), and Patton et al. (2015Patton JL, Pardiñas UFJ, D’Elía G (2015) Mammals of South America. University of Chicago Press, Chicago , vol. 2, 1290 pp.). The records of these species were then downloaded from the online databases GBIF (https://www.gbif.org) and VERTNET (http://vertnet.org). These include data from the most important worldwide collections, such as the American Museum of Natural History, New York (AMNH); Field Museum of Natural History, Chicago (FMNH); Museum of Vertebrate Zoology, University of California, Berkeley (MVZ); Museum of Natural Science, Louisiana State University, Baton Rouge (LSUMZ); Florida Museum of Natural History, University of Florida, Gainesville (FLMNH); University of Kansas Biodiversity Institute, Kansas (KU); Natural History Museum of Los Angeles County, Los Angeles (LACM); Museum of Comparative Zoology, Cambridge (MCZ); Museum of Southwestern Biology, Albuquerque (MSB); Michigan State University, East Lansing (MSU); Oklahoma Museum of Natural History, Norman (OMNH); Royal Ontario Museum, Toronto (ROM); The Texas A&M Biodiversity Research and Teaching Collections, Texas, formerly the Texas Cooperative Wildlife Collection, College Station (TCWC); Museum of Texas Tech University, Lubbock (TTU); Museum of Zoology, University of Michigan, Ann Arbor (UMMZ); and the National Museum of Natural History, Washington (USNM). A major source of information was the mammalian collection of the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima (MUSM). The nomenclature was updated based Pacheco et al. (2020Pacheco V, Graham-Angeles L, Diaz S, Hurtado CM, Ruelas D, Cervantes OK, Serrano JE (2020) Diversidad y distribución de los mamíferos del Perú por departamentos y ecorregiones I. Revista Peruana de Biología 27(3): 289-328. https://doi.org/10.15381/rpb.v27i3.18356
https://doi.org/10.15381/rpb.v27i3.18356...
, 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
) and recent literature. Geographic coordinates, elevation, and locality data were verified using gazetteers in Gardner et al. (2007), Patton et al. (2015), Diaz et al. (2021Diaz S, Sánchez-Vendizú P, Graham-Angeles L, Pacheco V (2021) Diversidad y conservación de los mamíferos mayores de Loreto, Perú. Revista Peruana de Biología 28(especial): 269-302. https://doi.org/10.15381/rpb.v28iespecial.21910
https://doi.org/10.15381/rpb.v28iespecia...
), Graham-Angeles et al. (2021Graham-Angeles L, Sánchez-Vendizú P, Diaz S, Pacheco V (2021) Diversidad y conservación de los murciélagos de Loreto, Perú. Revista Peruana de Biología 28(especial): 1-56. https://doi.org/10.15381/rpb.v28iespecial.21917
https://doi.org/10.15381/rpb.v28iespecia...
), and Sánchez-Vendizú et al. (2021Sánchez-Vendizú P, Graham-Angeles L, Diaz S, Pacheco V (2021) Diversidad y estado de conservación de pequeños mamíferos de Loreto, Perú. Revista Peruana de Biología 28(special): e21907. https://doi.org/10.15381/rpb.v28iespecial.21907
https://doi.org/10.15381/rpb.v28iespecia...
). These data are contained in Supplementary File 1
Supplementary Material 1
Supplementary File 1. List of mammalian records of the Peruvian Amazonia employed for preparing maps in Fig. 1. Geographic coordinates, elevation, and locality data were verified using gazetteers (see Material and Methods), but most specific names remain as have appeared in the original database.
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Gazetter data.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Link: https://doi.org/10.3897/zoologia.41.e23110
.
To gain a comprehensive understanding of mammal sampling area throughout the Peruvian Amazonia, we compiled a dataset encompassing all available mammalian records in these collections (Supplementary File 1
Supplementary Material 1
Supplementary File 1. List of mammalian records of the Peruvian Amazonia employed for preparing maps in Fig. 1. Geographic coordinates, elevation, and locality data were verified using gazetteers (see Material and Methods), but most specific names remain as have appeared in the original database.
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Gazetter data.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Link: https://doi.org/10.3897/zoologia.41.e23110
). This dataset was used to prepare two maps. The first map shows a representation of unique localities (each record with different geographic coordinates) over the three ecoregions (sensu Britto 2017Britto B (2017) Actualización de las ecorregiones terrestres de Perú propuestas en el Libro Rojo de plantas endémicas del Perú. Gayana Botánica 74(1): 15-29. https://doi.org/10.4067/S0717-66432017005000318
https://doi.org/10.4067/S0717-6643201700...
): Bosque Húmedo Amazónico (BHA), Bosque Muy Húmedo Pre-Montano (BMHP), and Bosque Seco Oriental (BSO). The second map (heat map), elaborated using the Kernel density method with 3 km cells and a 25 km ratio, shows the areas with the largest concentration of collection records and those with gaps of information (i.e., areas with none or less than 1% of all records). Maps were built with ArcMap v.10.3. In addition, we scaled the availability of records and unique localities per ecoregion, estimating the effort per area (1000 km2) in each case. Analyses were performed in ArcMap v.10.3.
Molecular data
The search in GenBank was carried out in the Nucleotide database of NCBI (https://www.ncbi.nlm.nih.gov/nuccore) using the advanced mode search tool, with the command (((genus) AND species) AND molecular marker). After entering the command, we carried out a manual search, looking for records from Peru. Because this geographic information is sometimes missing, we checked in the metadata for the catalogue number, the title of the journal article, or any other information that would indicate that the sequence was generated from a specimen collected in Peru. When a catalog number was available, we searched the online database of the corresponding museum; and for journal articles, the accession number of GenBank was searched within the article or the supplementary information if needed. The search in BOLD (http://www.boldsystems.org) was carried out looking for “scientific name” + Peru using the search tool. The molecular markers assessed were cytochrome b (cyt-b), cytochrome oxidase I (COI), 12S ribosomal RNA (12S), and the mitochondrial genome (mit). The search process was done until the end of August 2023. Valid records were interpreted as those with current scientific names, synonyms, and geographic data. Records obtained were sorted in a main database as follows: order>family>genus>species. A list of Amazonian mammalian species with records of nucleotide sequences per department and type of marker is presented in Supplementary File 2
Supplementary Material 2
Supplementary File 2. Updated list of mammalian species from Peruvian Amazonia and nucleotide sequence availability per department and type of marker. (Am) Amazonas, (Cu) Cusco, (Hu) Huánuco, (Lo) Loreto, (Ma) Madre de Dios, (Pu) Puno, (Uc) Ucayali, (N) no nucleotide sequence. The column labeled “n.l.” designates records lacking speci fic locality information, except for their presence in Peru.
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Species list.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Link: https://doi.org/10.3897/zoologia.41.e23110
, that include recent taxonomic changes (Silva et al. 2022Silva FE, do Amaral JV, Roos C, Bowler M, Röhe F, Sampaio R, et al. (2022) Molecular phylogeny and systematics of bald uakaris, genus Cacajao Lesson, 1840 (Primates: Pitheciidae), with the description of a new species. Molecular Phylogenetics and Evolution 173: 107509. https://doi.org/10.1016/j.ympev.2022.107509
https://doi.org/10.1016/j.ympev.2022.107...
, Cláudio et al. 2023Cláudio VC, Novaes RL, Gardner AL, Nogueira MR, Wilson DE, Maldonado JE, Oliveira J, Moratelli R (2023) Taxonomic re-evaluation of New World Eptesicus and Histiotus (Chiroptera: Vespertilionidae), with the description of a new genus. Zoologia 40: e22029. https://doi.org/10.1590/S1984-4689.v40.e22029
https://doi.org/10.1590/S1984-4689.v40.e...
, Sandoval et al. 2024Sandoval EDP, Jędrzejewski W, Molinari J, Vozdova M, Cernohorska H, Kubickova S, et al. (2024) Description of Bisbalus, a new genus for the Gray Brocket, Mazama cita Osgood, 1912 (Mammalia, Cervidae), as a step to solve the Neotropical Deer puzzle. Taxonomy 4(1): 10-26.). Moreover, a list of threatened and endemic Peruvian species from Amazonia was built, based on the Servicio Nacional Forestal y de Fauna Silvestre (SERFOR 2018SERFOR (2018) Libro Rojo de la Fauna Silvestre Amenazada del Perú. Servicio Nacional Forestal y de Fauna Silvestre, Lima, 547 pp.), describing whether or not they have genetic information.
RESULTS
We assembled a comprehensive dataset of 41,951 mammalian records from 1237 unique localities for 326 species from the Peruvian Amazonia (Fig. 1A, Supplementary File 1 Supplementary Material 1 Supplementary File 1. List of mammalian records of the Peruvian Amazonia employed for preparing maps in Fig. 1. Geographic coordinates, elevation, and locality data were verified using gazetteers (see Material and Methods), but most specific names remain as have appeared in the original database. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Gazetter data. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). Our data showed that the Bosque Húmedo Amazónico (BHA) and the Bosque Muy Húmedo Pre-Montano (BMHP) comprised most mammalian records with 65.7 and 43.2 records per 1000 km2, respectively (Fig 1A, Table 1), whereas only 8.8 records per 1000 km2 come from the Bosque Seco Oriental (BSO) (Table 1). However, estimates of the number of unique localities per 1000 km2 showed that the BSO (the smallest area) has the same number of unique localities sampled per area (1.9) as the BHA (the largest area), whereas the BMHP has only 1.2 unique localities per 1000 km2 (Table 1).
(A) Distribution map of unique localities sampled for mammals over the Peruvian Amazon ecoregions sensu Britto (2017Britto B (2017) Actualización de las ecorregiones terrestres de Perú propuestas en el Libro Rojo de plantas endémicas del Perú. Gayana Botánica 74(1): 15-29. https://doi.org/10.4067/S0717-66432017005000318
https://doi.org/10.4067/S0717-6643201700... ). (B) Heat map of the Peruvian Amazonian region showing record densities of mammals available in collections. The red ellipses highlight major information gaps identified: 1) Putumayo area, 2) northern Marañón area, 3) Marañón-Ucayali interfluvial area, 4) Yavarí-Ucayali interfluvial area, 5) Ucayali and Madre de Dios area.
Number of records and unique record localities for mammalian specimens from the Peruvian Amazonia by ecoregions sensu Britto (2017Britto B (2017) Actualización de las ecorregiones terrestres de Perú propuestas en el Libro Rojo de plantas endémicas del Perú. Gayana Botánica 74(1): 15-29. https://doi.org/10.4067/S0717-66432017005000318
https://doi.org/10.4067/S0717-6643201700... ).
The heat map showed several areas with none or less than 1% of mammalian records, which are considered major information gaps (Fig. 1B). These critical regions include: 1) Putumayo area; 2) northern Marañón area; 3) Marañón-Ucayali interfluvial area; 4) Yavarí-Ucayali interfluvial area; and 5) Ucayali and Madre de Dios area. The first four critical areas are mostly in the Loreto department, and the Ucayali and Madre de Dios area is in the Ucayali and Madre de Dios departments. All these critical areas are in remote areas relatively far from large cities. For example, area 5 is about 250 km from Puerto Maldonado, and area 1 is about 400 km from Iquitos.
The molecular search in GenBank or BOLD recovered 1597 DNA sequences (genes and mitochondrial genomes), which correspond to 180 of the 326 species of Peruvian Amazonian mammals (55.21%) (Supplementary Files 2 Supplementary Material 2 Supplementary File 2. Updated list of mammalian species from Peruvian Amazonia and nucleotide sequence availability per department and type of marker. (Am) Amazonas, (Cu) Cusco, (Hu) Huánuco, (Lo) Loreto, (Ma) Madre de Dios, (Pu) Puno, (Uc) Ucayali, (N) no nucleotide sequence. The column labeled “n.l.” designates records lacking speci fic locality information, except for their presence in Peru. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species list. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 -4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). The orders Chiroptera (n = 703 sequences) and Rodentia (n = 499) had the largest number of DNA sequences, whereas no genetic data is available for Sirenia and Cingulata (Fig. 2A, Supplementary File 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). The orders Chiroptera and Rodentia had the largest number of species with sequence data (63 and 53 species, respectively), whereas the orders Pilosa (2), Lagomorpha (1), and Perissodactyla (1) showed the lowest number of species with sequence data (Fig. 2A, Supplementary File 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). The orders Artiodactyla, Didelphimorphia, Perissodactyla, Pilosa, and Rodentia have species with nucleotide sequences for all the molecular markers assessed in this study (12S, COI, cyt-b, and mit). The orders Primates and Chiroptera included species with sequences for three molecular markers (12S, COI, and cyt-b), Carnivora diversity was represented with two molecular markers (cyt-b and 12S) and Lagomorpha with only one molecular marker (Fig. 2B, Supplementary File 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ).
(A) Number of species per order of Peruvian Amazonia mammals and nucleotide sequences availability. (B) Number of nucleotide sequences per molecular marker and taxonomic order.
Cytochrome b (cyt-b) was the molecular marker with the highest number of records (1411 records for 167 species), whereas the complete mitochondrial genome was the less frequent (23 for 16 species) (Table 2, Supplementary Files 3 Supplementary Material 3 Supplementary File 3. Nucleotide sequence account per molecular marker available for Peruvian Amazonian mammal grouped by the taxonomic categories of order and family. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Sequence account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 , 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). The markers 12S and COI are represented by 70 (56 species) and 93 sequences (38 species), respectively (Table 2, Supplementary Files 3 Supplementary Material 3 Supplementary File 3. Nucleotide sequence account per molecular marker available for Peruvian Amazonian mammal grouped by the taxonomic categories of order and family. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Sequence account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 , 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ). By order, the cyt-b had the highest frequency in Chiroptera (623 sequences for 54 species) and Rodentia (437 sequences for 52 species), whereas the lowest number of cyt-b sequences was recorded for Artiodactyla (6 sequences for 5 species) (Fig. 2B, Supplementary Files 3 Supplementary Material 3 Supplementary File 3. Nucleotide sequence account per molecular marker available for Peruvian Amazonian mammal grouped by the taxonomic categories of order and family. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Sequence account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 , 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ).
Number of nucleotide sequences available for mammalian species from Peruvian Amazon listed by molecular marker and department.
The COI marker had the highest frequency in Chiroptera (56 sequences for 18 species) and the lowest in Perissodactyla (1) and Didelphimorphia (1). The molecular marker 12S registered the largest number of species in Rodentia (27 sequences for 19 species) and Chiroptera (24 sequences for 21 species), whereas Perissodactyla, Lagomorpha, and Pilosa had only one sequence each. The highest number of mitoge nomes were found in Rodentia (17 in 10 species), whereas Didelphimorphia, Pilosa, and Perissodactyla had only one mitogenome each (Fig. 2B; Supplementary Files 3 Supplementary Material 3 Supplementary File 3. Nucleotide sequence account per molecular marker available for Peruvian Amazonian mammal grouped by the taxonomic categories of order and family. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Sequence account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 , 4 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ).
At the family level, Cervidae, Tayassuidae, Didelphidae, Tapiridae, Bradypodidae, Cuniculidae, Echimyidae, and Sciuridae had species with nucleotide sequences for all the molecular markers assessed, whereas Felidae, Procyonidae, Atelidae, Pitheciidae, and Dasyproctidae had sequences only for cyt-b. The family Choloepodidae had sequences only for COI. The families Furipteridae, Leporidae, and Dinomyidae had sequences only for the marker 12S (Supplementary File 3 Supplementary Material 4 Supplementary File 4. Number of mammalian species from the Peruvian Amazonia with molecular information arranged by molecular marker and taxonomic order. Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al. Data type: Species account. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/zoologia.41.e23110 ).
Loreto is the department with the largest number of species with at least one molecular marker (99), followed by Cusco (56) and Madre de Dios (52) departments, whereas Ayacucho (3), and Pasco (3) departments have the lowest number of species (Table 3). Loreto is also the department with the highest number of sequences (530), followed by Cusco (141), and Madre de Dios (135), whereas Ayacucho and Pasco departments have the lowest number of sequences (3 and 6, respectively) (Table 2).
According to SERFOR (2018SERFOR (2018) Libro Rojo de la Fauna Silvestre Amenazada del Perú. Servicio Nacional Forestal y de Fauna Silvestre, Lima, 547 pp.), 22 Peruvian Amazonian species of mammals are considered threatened, and 11 of them are not represented by any molecular data obtained from Peruvian Amazonian specimens. With regard to endemism, 3 of the 5 known endemic species are not represented by any molecular data (Table 4).
Number of mammalian species from the Peruvian Amazonia with nucleotide sequences available, arranged by molecular marker and department.
Threatened species of mammals from the Peruvian Amazonia according to SERFOR (2018SERFOR (2018) Libro Rojo de la Fauna Silvestre Amenazada del Perú. Servicio Nacional Forestal y de Fauna Silvestre, Lima, 547 pp.), including information on endemism (E) and nucleotide sequences availability in genetic repositories. None = Lack of nucleotide sequences).
DISCUSSION
Peru is renowned for hosting an impressive array of mammalian species (579 species) and is the country with the highest mammalian diversity in western Amazonia (326 species) (Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
, Rengifo et al. 2022Rengifo EM, D’Elía G, García G, Charpentier E, Cornejo FM (2022) A new species of titi monkey, genus Cheracebus Byrne et al., 2016 (Primates: Pitheciidae), from Peruvian Amazonia. Mammal Study 48(1): 1-16. https://doi.org/10.3106/ms2022-0019
https://doi.org/10.3106/ms2022-0019...
). However, here we show that significant information gaps persist in at least five under-sampled areas across the Peruvian Amazonia (Fig. 1B). These areas situated at considerable distances from major cities, pose significant challenges to comprehensive sampling due to the extraordinary effort and costs required for access (Mena et al. 2021Mena JL, Yagui H, Tejeda V, Bonifaz E, Bellemain E, Valentini A, et al. (2021) Environmental DNA metabarcoding as a useful tool for evaluating terrestrial mammal diversity in tropical forests. Ecological Applications 31(5): e02335. https://doi.org/10.1002/eap.2335
https://doi.org/10.1002/eap.2335...
). Our identified information gaps align with previous analyses conducted for the Loreto and Ucayali departments by Quintana et al. (2009Quintana H, Pacheco V, Salas E (2009) Diversidad y conservación de los mamíferos de Ucayali, Perú. Ecología Aplicada 8(1-2): 91-103.), Diaz et al. (2021Diaz S, Sánchez-Vendizú P, Graham-Angeles L, Pacheco V (2021) Diversidad y conservación de los mamíferos mayores de Loreto, Perú. Revista Peruana de Biología 28(especial): 269-302. https://doi.org/10.15381/rpb.v28iespecial.21910
https://doi.org/10.15381/rpb.v28iespecia...
), Graham-Angeles et al. (2021Graham-Angeles L, Sánchez-Vendizú P, Diaz S, Pacheco V (2021) Diversidad y conservación de los murciélagos de Loreto, Perú. Revista Peruana de Biología 28(especial): 1-56. https://doi.org/10.15381/rpb.v28iespecial.21917
https://doi.org/10.15381/rpb.v28iespecia...
), and Sánchez-Vendizú et al. (2021Sánchez-Vendizú P, Graham-Angeles L, Diaz S, Pacheco V (2021) Diversidad y estado de conservación de pequeños mamíferos de Loreto, Perú. Revista Peruana de Biología 28(special): e21907. https://doi.org/10.15381/rpb.v28iespecial.21907
https://doi.org/10.15381/rpb.v28iespecia...
). Among these areas, the Northern Marañón, the Marañón-Ucayali, and the Madre de Dios areas are of the greatest concern because very few or no records document their diversity.
The number of available sequences of Amazonian mammalian species deposited in genetic databases generated from Peruvian specimens (1597 DNA sequences for 180 species) clearly is not representing the hyper diverse status recognized for the Peruvian Amazonia (326 species). This under representation can be attributed to various factors, including the inaccessibility of remote regions for specimen collection, resource limitations in generating genetic data within regional laboratories, scarcity of accessible laboratories, or legal restrictions on genetic data access (Aguilar et al. 2010Aguilar C, Ramírez C, Rivera D, Siu-Ting K, Suarez J, Torres C (2010) Anfibios andinos del Perú fuera de Áreas Naturales Protegidas: amenazas y estado de conservación. Revista Peruana de Biología 17(1): 5-28. https://doi.org/10.15381/rpb.v17i1.46
https://doi.org/10.15381/rpb.v17i1.46...
, Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
).
Our data is also consistent with earlier genetic assessments emphasizing the scant representation of Peruvian mammalian species in genetic databases. Rojas et al. (2018Rojas R, Castro JC, García-Dávila C (2018) Situación actual de la base de dato genéticos de vertebrados de la región Loreto, Perú. Folia Amazónica 27(2): 151-162. https://doi.org/10.24841/fa.v27i2.442
https://doi.org/10.24841/fa.v27i2.442...
) found that for all sequences of vertebrates available for the Loreto department, only 8.92% corresponded to mammals. On a different scale, Noreña et al. (2018Noreña A, González Muñoz A, Mosquera-Rendón J, Botero K, Cristancho MA (2018) Colombia, an unknown genetic diversity in the era of Big Data. BMC Genomics 19(Suppl. 8): 61-73. https://doi.org/10.1186/s12864-018-5194-8
https://doi.org/10.1186/s12864-018-5194-...
) estimated that only 1.13 % of the Peruvian mammals are represented with genetic sequences in GenBank and only 13 records in BOLD System. We then posit that the low representation of Peruvian biodiversity in genetic databases is of great concern. This becomes even more critical when considering nuclear data, which are generated in lower proportion than mitochondrial data. For example, only six new species of sigmodontine rodents described in the last decade have included nuclear data (Dalapicolla and Percequillo 2020Dalapicolla J, Percequillo A (2020) Species concepts and taxonomic practice in the integrative taxonomy era: an example using South American rodents. Boletim da Sociedade Brasileira de Mastozoologia 88: 36-54.).
The genetic marker most frequently employed for Amazonian mammals varied by taxonomic group. For example, cyt-b was largely the most frequent molecular marker for rodents and marsupials, likely due to the marker reliability in phylogenetic reconstructions and molecular identification at the species level (Graybeal 1993Graybeal A (1993) The phylogenetic utility of cytochrome b: lessons from bufonid frogs. Molecular Phylogenetics and Evolution 2(3): 256-269. https://doi.org/10.1006/mpev.1993.1024
https://doi.org/10.1006/mpev.1993.1024...
, Bradley and Baker 2001Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. Journal of Mammalogy 82(4): 960-973. https://doi.org/10.1644/1545-1542(2001)082<0960:ATOTGS>2.0.CO;2
https://doi.org/10.1644/1545-1542(2001)0...
, Tobe et al. 2010Tobe SS, Kitchener AC, Linacre AMT (2010) Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome b and cytochrome oxidase subunit I mitochondrial genes. Plos One 5(11): e14156. https://doi.org/10.1371/journal.pone.0014156
https://doi.org/10.1371/journal.pone.001...
). Whereas the marker COI was preferred for genetic identification of bats (Clare et al. 2011Clare EL, Lim BK, Fenton MB, Hebert PDN (2011) Neotropical bats: Estimating species diversity with DNA barcodes. Plos One 6(7): e22648. https://doi.org/10.1371/journal.pone.0022648
https://doi.org/10.1371/journal.pone.002...
) due to the development of the Barcoding project and the BOLD system platform (Hebert et al. 2013Hebert PD, DeWaard JR, Zakharov EV, Prosser SW, Sones JE, McKeown JT, et al. (2013) A DNA ‘Barcode Blitz’: Rapid digitization and sequencing of a natural history collection. Plos One 8(7): e68535. https://doi.org/10.1371/journal.pone.0068535
https://doi.org/10.1371/journal.pone.006...
). On the other hand, the low representation of mitogenomic sequences is likely a methodological constraint. Mitogenomes for mammals are on average ~18 to 20kb in size (Rand 1993Rand DM (1993) Endotherms, ectotherms, and mitochondrial genome-size variation. Journal of Molecular Evolution 37: 281-295. https://doi.org/10.1007/BF00175505
https://doi.org/10.1007/BF00175505...
) and are generally assembled either by whole genome sequencing (WGS) with genome skimming (Trevisan et al. 2019Trevisan B, Alcantara DMC, Machado DJ, Marques FPL, Lahr DJG (2019) Genome skimming is a low-cost and robust strategy to assemble complete mitochondrial genomes from ethanol preserved specimens in biodiversity studies. PeerJ 13(7): e7543. https://doi.org/10.7717/peerj.7543
https://doi.org/10.7717/peerj.7543...
, Janiak et al. 2022Janiak MC, Silva FE, Beck RM, de Vries D, Kuderna LF, Torosin NS, et al. (2022) Two hundred and five newly assembled mitogenomes provide mixed evidence for rivers as drivers of speciation for Amazonian primates. Molecular Ecology 31(14): 3888-3902. https://doi.org/10.1111/mec.16554
https://doi.org/10.1111/mec.16554...
), or by tiling PCRs where genomes are assembled in many pieces (Schenk et al. 2017Schenk D, Song G, Ke Y, Wang Z (2017) Amplification of overlapping DNA amplicons in a single-tube multiplex PCR for targeted next-generation sequencing of BRCA1 and BRCA2. Plos One 12: e0181062. https://doi.org/10.1371/journal.pone.0181062
https://doi.org/10.1371/journal.pone.018...
, Totawa et al. 2020). WGS methods require high quality samples with unfragmented DNA, which are not easily available, and both methods require access to high throughput sequencing (HTS) capabilities. Although HTS has resulted in ways to generate full mitogenomes at low cost by multiplexing, the technology itself is not widely distributed globally (Watsa et al. 2020aWatsa M, Wildlife Disease Surveillance Focus Group (2020a) Rigorous wildlife disease surveillance. Science 369(6500): 145-148. https://doi.org/10.1126/science.abc0017
https://doi.org/10.1126/science.abc0017...
, Urban et al. 2023Urban L, Perlas A, Francino O, Martí-Carreras J, Muga BA, Mwangi JW, et al. (2023) Real-time genomics for One Health. Molecular Systems Biology 19: e11686. https://doi.org/10.15252/msb.202311686.
https://doi.org/10.15252/msb.202311686...
), and difficult to access within Peru (Carrillo-Larco et al. 2022Carrillo-Larco RM, Guzman-Vilca WC, Leon-Velarde F, Bernabe-Ortiz A, Jimenez MM, Penny ME, et al. (2022) Peru - Progress in health and sciences in 200 years of independence. The Lancet Regional Health - Americas 7: 100148. https://doi.org/10.1016/j.lana.2021.100148
https://doi.org/10.1016/j.lana.2021.1001...
). Fortunately, the 17 mitogenomes generated for rodents show the transition to the Genomic era in rodent systematic as pointed out by Lessa et al. (2014Lessa EP, Cook JA, D’Elía G, Opazo JC (2014) Rodent diversity in South America: transitioning into the genomics era. Frontiers in Ecology and Evolution 2: 1-7. https://doi.org/10.3389/fevo.2014.00039
https://doi.org/10.3389/fevo.2014.00039...
) and D’Elía et al. (2019D’Elía G, Fabre PH, Lessa EP (2019) Rodent systematics in an age of discovery: recent advances and prospects. Journal of Mammalogy 100(3): 852-871. https://doi.org/10.1093/jmammal/gyy179
https://doi.org/10.1093/jmammal/gyy179...
).
Regarding taxonomic level, our data showed the disproportion of genetic data available among taxonomic orders. The orders Chiroptera and Rodentia comprised the largest amount of genetic data (1202 sequences). Although these are the two most diverse orders in Peru (Pacheco et al. 2021Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
https://doi.org/10.15381/rpb.v28i4.21019...
), the genetic data represented only the 44.4% and 79.1% of their species present in Peruvian Amazonia, respectively. On the other hand, medium-size or large charismatic species such as primates and carnivores had comparatively little genetic data (only 235 sequences for only 64 species). Apparently, there is still the perception that medium-size or large mammals lack taxonomic problems; therefore, studies of genetic structure and genetic variability have not been developed with similar intensity as in small rodents, bats, or marsupials. Recent publications on the felid genus Leopardus (Nascimento et al. 2021Nascimento FOD, Cheng J, Feijó A (2021) Taxonomic revision of the pampas cat Leopardus colocola complex (Carnivora: Felidae): an integrative approach. Zoological Journal of the Linnean Society 191(2): 575-611. https://doi.org/10.1093/zoolinnean/zlaa043
https://doi.org/10.1093/zoolinnean/zlaa0...
) and the howler monkeys of the genus Alouatta (Ruiz-García et al. 2017Ruiz-García M, Cerón Á, Sánchez-Castillo S, Rueda-Zozaya P, Pinedo-Castro M, Gutierrez-Espeleta G, Shostell JM (2017) Phylogeography of the Mantled Howler Monkey (Alouatta palliata; Atelidae, Primates) across its geographical range by means of mitochondrial genetic analyses and new insights about the phylogeny of Alouatta. Folia Primatologica 88(5): 421-454. https://doi.org/10.1159/000480502
https://doi.org/10.1159/000480502...
) that have analyzed the phylogeographic structure of these taxa have resulted in taxonomic changes. Also, the difficulty in obtaining collecting permits for large species is a deterrent for scientific research (Gannon et al. 2007Gannon WL, Sikes RS, The Animal Care and Use Committee of the American Society of Mammalogists (2007) Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research. Journal of Mammalogy 88(3): 809-823. https://doi.org/10.1644/06-MAMM-F-185R1.1
https://doi.org/10.1644/06-MAMM-F-185R1....
). Fortunately, non-invasive methods are now available to obtain genetic material, such as from hair, saliva, blood (Waits and Petkau 2005Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: A review of applications and recommendations for accurate data collection. The Journal of Wildlife Management 69(4): 1419-1433. https://doi.org/10.2193/0022-541X(2005)69[1419:NGSTFW]2.0.CO;2, Henry et al. 2011Henry P, Henry A, Russello MA (2011) A noninvasive hair sampling technique to obtain high quality DNA from elusive small mammals. Journal of Visualized Experiments 49: e2791. https://doi.org/10.3791/2791
https://doi.org/10.3791/2791...
, Flagstad et al. 2012Flagstad Ø, Pradhan NMB, Kvernstuen LG, Wegge P (2012) Conserving small and fragmented populations of large mammals: Non-invasive genetic sampling in an isolated population of Asian elephants in Nepal. Journal for Nature Conservation 20(3): 181-190. https://doi.org/10.1016/j.jnc.2012.01.006
https://doi.org/10.1016/j.jnc.2012.01.00...
, Ferreira et al. 2018Ferreira CM, Sabino-Marques H, Barbosa S, Costa P, Encarnação C, Alpizar-Jara R, et al. (2018) Genetic non-invasive sampling (gNIS) as a cost-effective tool for monitoring elusive small mammals. European Journal of Wildlife Research 64(46): 1-15. https://doi.org/10.1007/s10344-018-1188-8
https://doi.org/10.1007/s10344-018-1188-...
, Aylward et al. 2022Aylward CM, Grahn RA, Barthman-Thompson LM, Kelt DA, Sacks BN, Statham MJ (2022) A novel noninvasive genetic survey technique for small mammals. Journal of Mammalogy 103(6): 1441-1447. https://doi.org/10.1093/jmammal/gyac070
https://doi.org/10.1093/jmammal/gyac070...
), which help to partially overcome the need of collecting medium size or large mammals. However, vouchers and associated information are desirable by museum collections, when possible, to carry on research that could be impossible or difficult without whole-organism specimen such as the discovery and description of new species, the origins and spread of infectious diseases among other topics (Bakker et al. 2020Bakker FT, Antonelli A, Clarke JA, Cook JA, Edwards SV, Ericson PGP, et al. (2020) The Global Museum: natural history collections and the future of evolutionary science and public education. PeerJ 8: e8225. https://doi.org/10.7717/peerj.8225
https://doi.org/10.7717/peerj.8225...
, Thompson et al. 2021Thompson CW, Phelps KL, Allard MW, Cook JA, Dunnum JL, Ferguson AW, et al. (2021) Preserve a voucher specimen! The critical need for integrating natural history collections in infectious disease studies. mBio 12(1): e02698. https://doi.org/10.1128/mBio.02698-20
https://doi.org/10.1128/mBio.02698-20...
, Johnson et al. 2023Johnson KR, Owens IFP, The Global Collection Group (2023) A global approach for natural history museum collections. Science 379(6638): 1192-1194. https://doi.org/10.1126/science.adf6434
https://doi.org/10.1126/science.adf6434...
, Nachman et al. 2023Nachman MW, Beckman EJ, Bowie RCK, Cicero C, Conroy CJ, Dudley R, et al. (2023) Specimen collection is essential for modern science. Plos Biology 21(11): e3002318. https://doi.org/10.1371/journal.pbio.3002318
https://doi.org/10.1371/journal.pbio.300...
).
From the conservation point of view, it is of great concern the lack of genetic information in three Amazonian endemic species and 11 threatened species according to SERFOR (Table 4). We raise awareness of these concerns and call for an urgent program to study these important species. Several of these endemic and threatened species are difficult to find or collect because rareness, secretive habits or restricted by the Peruvian legislation, obtaining tissue samples from museum specimens is an alternative, since scientific collections are currently recognized as an important museomic resource (Gauthier et al. 2020Gauthier J, Pajkovic M, Neuenschwander S, Kaila L, Schmid S, Orlando L, Alvarez N (2020) Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland. Molecular Ecology Resources 20(5): 1191-1205. https://doi.org/10.1111/1755-0998.13167
https://doi.org/10.1111/1755-0998.13167...
, Jin et al. 2020Jin M, Zwick A, Ślipiński A, de Keyzer R, Pang H (2020) Museomics reveals extensive cryptic diversity of Australian prionine longhorn beetles with implications for their classification and conservation. Systematic Entomology 45(4): 745-770. https://doi.org/10.1111/syen.12424
https://doi.org/10.1111/syen.12424...
, Castañeda-Rico et al. 2022Castañeda-Rico S, Edwards CW, Hawkins MT, Maldonado JE (2022) Museomics and the holotype of a critically endangered cricetid rodent provide key evidence of an undescribed genus. Frontiers in Ecology and Evolution 10: 930356. https://doi.org/10.3389/fevo.2022.930356
https://doi.org/10.3389/fevo.2022.930356...
, Fong et al. 2023Fong JJ, Blom MP, Aowphol A, McGuire JA, Sutcharit C, Soltis PS (2023) Editorial: Recent advances in museomics: revolutionizing biodiversity research. Frontiers in Ecology and Evolution 11: 188172. https://doi.org/10.3389/fevo.2023.1188172
https://doi.org/10.3389/fevo.2023.118817...
). For example, several genes and mitogenomes have been obtained from Amazonian species from Peruvian scientific collections (e.g., Abreu-Jr et al. 2020Abreu-Jr EF, Pavan SE, Tsuchiya MTN, Wilson DE, Percequillo AR, Maldonado JE (2020) Museomics of tree squirrels: A dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul. BMC Evolutionary Biology 20: 1-25. https://doi.org/10.1186/s12862-020-01639-y
https://doi.org/10.1186/s12862-020-01639...
, Ruelas and Pacheco 2022Ruelas D, Pacheco V (2022) New morphological data and phylogenetic position of the rare Short-tailed Opossum Monodelphis ronaldi (Didelphimorphia: Didelphidae) with new records. Mammalian Biology 102(1): 189-204. https://doi.org/10.1007/s42991-021-00219-x
https://doi.org/10.1007/s42991-021-00219...
, Pacheco and Ruelas 2023Pacheco V, Ruelas D (2023) Systematic revision of Thomasomys cinereus (Rodentia: Cricetidae: Sigmodontinae) from northern Peru and southern Ecuador, with descriptions of three new species. Bulletin of the American Museum of Natural History 461(1): 1-72.). Museum collections have become an important and diverse genetic resource that can help fill the genetic information gaps of species for conservation, systematic, or economic purposes (Watsa et al. 2020bWatsa M, Wildlife Disease Surveillance Focus Group (2020b) Response to Vanhove et al. and Colella et al. Science 370(6518): 774-775. https://doi.org/10.1126/science.abe9392
https://doi.org/10.1126/science.abe9392...
, Mulcahy et al. 2022Mulcahy DG, Ibáñez R, Jaramillo CA, Crawford AJ, Ray JM, Gotte SW, et al. (2022) DNA barcoding of the National Museum of Natural History reptile tissue holdings raises concerns about the use of natural history collections and the responsibilities of scientists in the molecular age. Plos One 17(3): e0264930. https://doi.org/10.1371/journal.pone.0264930
https://doi.org/10.1371/journal.pone.026...
).
We also found that our results for the Loreto department (99 species with 530 sequences) are higher than the 34 species and 175 sequences reported by Rojas et al. (2018Rojas R, Castro JC, García-Dávila C (2018) Situación actual de la base de dato genéticos de vertebrados de la región Loreto, Perú. Folia Amazónica 27(2): 151-162. https://doi.org/10.24841/fa.v27i2.442
https://doi.org/10.24841/fa.v27i2.442...
), although this difference could be due to the search tool employed. Rojas et al. (2018Rojas R, Castro JC, García-Dávila C (2018) Situación actual de la base de dato genéticos de vertebrados de la región Loreto, Perú. Folia Amazónica 27(2): 151-162. https://doi.org/10.24841/fa.v27i2.442
https://doi.org/10.24841/fa.v27i2.442...
) used a data mining algorithm implemented in the Rentrez package for R (Winter 2017Winter DJ (2017) Rentrez: An R package for the NCBI eUtils API. The R Journal 9(2): 520-526.), whereas our data was constructed using an exhaustive approach, analyzing species by species in the molecular repositories. Our data showed that the Rentrez algorithm in Rojas et al. (2018Rojas R, Castro JC, García-Dávila C (2018) Situación actual de la base de dato genéticos de vertebrados de la región Loreto, Perú. Folia Amazónica 27(2): 151-162. https://doi.org/10.24841/fa.v27i2.442
https://doi.org/10.24841/fa.v27i2.442...
) recovered only 34.34 % of the genetic sequences available, mainly because some sequences on repositories have incomplete data. For example, if a sequence missed the word “Peru” it will never be recovered by informatic methods. Exhaustive search, species by species, although laborious, recovered 65.66 % more information than the Rentrez package. Therefore, we strongly suggest the researchers include complete geographic data of localities in GenBank and linked to the complete information of the museum or collection where the record was taken, as is currently done in BOLD System. The BOLD is a platform specifically built to work with biodiversity data (Hebert et al. 2013Hebert PD, DeWaard JR, Zakharov EV, Prosser SW, Sones JE, McKeown JT, et al. (2013) A DNA ‘Barcode Blitz’: Rapid digitization and sequencing of a natural history collection. Plos One 8(7): e68535. https://doi.org/10.1371/journal.pone.0068535
https://doi.org/10.1371/journal.pone.006...
) and let to make updates since taxonomic changes could happens in the light of more genetic, morphological, or ecological information.
Our findings underscore a significant gap in the representation of genetic information for the Peruvian Amazonia, indicating a lag behind contemporary research standards. The inclusion of molecular data from Peruvian Amazonia, in an integral approach with non-molecular data, could help to resolve the systematic status of several species complex (Sanchez-Vendizú et al. 2018Sanchez-Vendizú P, Pacheco V, Vivas-Ruiz D (2018) An introduction to the systematics of Small-Bodied Neacomys (Rodentia: Cricetidae) from Peru with descriptions of two new species. American Museum Novitates 3913: 1-38., Velazco and Patterson 2019Velazco PM, Patterson BD (2019) Small mammals of the Mayo River Basin in northern Peru, with the description of a new species of Sturnira (Chiroptera: Phyllostomidae). Bulletin of the American Museum of Natural History 429: 1-67., Ruelas and Pacheco 2022Ruelas D, Pacheco V (2022) New morphological data and phylogenetic position of the rare Short-tailed Opossum Monodelphis ronaldi (Didelphimorphia: Didelphidae) with new records. Mammalian Biology 102(1): 189-204. https://doi.org/10.1007/s42991-021-00219-x
https://doi.org/10.1007/s42991-021-00219...
). Moreover, what we know of the diversity of mammals in the Peruvian Amazonia remains notably incomplete. With only a fraction of the Peruvian Amazonian species documented in genetic databases, it is imperative to undertake swift and comprehensive measures. Urgent initiatives, expanded inventories, enhanced scientific collections and laboratories, and collaboration with government entities are essential to safeguard these species from extinction.
ACKNOWLEDGMENTS
We thank Jeanpierre Zavaleta, Oscar Apari, and Katherine Vera for helping with the database curation. This research was supported by the CONCYTEC through the fund FONDECYT within the contest’s framework “Proyectos de Investigación Básica”, process 039-2021-FONDECYT.
LITERATURE CITED
- Abreu-Jr EF, Pavan SE, Tsuchiya MTN, Wilson DE, Percequillo AR, Maldonado JE (2020) Museomics of tree squirrels: A dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul. BMC Evolutionary Biology 20: 1-25. https://doi.org/10.1186/s12862-020-01639-y
» https://doi.org/10.1186/s12862-020-01639-y - Aguilar C, Ramírez C, Rivera D, Siu-Ting K, Suarez J, Torres C (2010) Anfibios andinos del Perú fuera de Áreas Naturales Protegidas: amenazas y estado de conservación. Revista Peruana de Biología 17(1): 5-28. https://doi.org/10.15381/rpb.v17i1.46
» https://doi.org/10.15381/rpb.v17i1.46 - Arévalo-Sandi AR, Gonçalves ALS, Onizawa K, Yabe T, Spironello WR (2021) Mammal diversity among vertical strata and the evaluation of a survey technique in a central Amazonian forest. Papéis Avulsos de Zoologia 61: e20216133. https://doi.org/10.11606/1807-0205/2021.61.33
» https://doi.org/10.11606/1807-0205/2021.61.33 - Arif IA, Khan HA (2009) Molecular markers for biodiversity analysis of wildlife animals: A brief review. Animal Biodiversity and Conservation 32(1): 9-17.
- Aylward CM, Grahn RA, Barthman-Thompson LM, Kelt DA, Sacks BN, Statham MJ (2022) A novel noninvasive genetic survey technique for small mammals. Journal of Mammalogy 103(6): 1441-1447. https://doi.org/10.1093/jmammal/gyac070
» https://doi.org/10.1093/jmammal/gyac070 - Bakker FT, Antonelli A, Clarke JA, Cook JA, Edwards SV, Ericson PGP, et al. (2020) The Global Museum: natural history collections and the future of evolutionary science and public education. PeerJ 8: e8225. https://doi.org/10.7717/peerj.8225
» https://doi.org/10.7717/peerj.8225 - Brack-Egg A (1986) Las ecorregiones del Perú. Boletín de Lima 44: 57-70.
- Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. Journal of Mammalogy 82(4): 960-973. https://doi.org/10.1644/1545-1542(2001)082<0960:ATOTGS>2.0.CO;2
» https://doi.org/10.1644/1545-1542(2001)082<0960:ATOTGS>2.0.CO;2 - Britto B (2017) Actualización de las ecorregiones terrestres de Perú propuestas en el Libro Rojo de plantas endémicas del Perú. Gayana Botánica 74(1): 15-29. https://doi.org/10.4067/S0717-66432017005000318
» https://doi.org/10.4067/S0717-66432017005000318 - Carrillo-Larco RM, Guzman-Vilca WC, Leon-Velarde F, Bernabe-Ortiz A, Jimenez MM, Penny ME, et al. (2022) Peru - Progress in health and sciences in 200 years of independence. The Lancet Regional Health - Americas 7: 100148. https://doi.org/10.1016/j.lana.2021.100148
» https://doi.org/10.1016/j.lana.2021.100148 - Castañeda-Rico S, Edwards CW, Hawkins MT, Maldonado JE (2022) Museomics and the holotype of a critically endangered cricetid rodent provide key evidence of an undescribed genus. Frontiers in Ecology and Evolution 10: 930356. https://doi.org/10.3389/fevo.2022.930356
» https://doi.org/10.3389/fevo.2022.930356 - Cavalcante RBL, Ferreira DBS, Pontes PRM, Tedeschi RG, da Costa CPW, de Souza EB (2020) Evaluation of extreme rainfall indices from CHIRPS precipitation estimates over the Brazilian Amazonia. Atmospheric Research 238: 104879. https://doi.org/10.1016/j.atmosres.2020.104879
» https://doi.org/10.1016/j.atmosres.2020.104879 - Ceballos G, Ehrlich PR (2006) Global mammal distributions, biodiversity hotspots, and conservation. Proceedings of the National Academy of Sciences 103: 19374-19379.
- Cláudio VC, Novaes RL, Gardner AL, Nogueira MR, Wilson DE, Maldonado JE, Oliveira J, Moratelli R (2023) Taxonomic re-evaluation of New World Eptesicus and Histiotus (Chiroptera: Vespertilionidae), with the description of a new genus. Zoologia 40: e22029. https://doi.org/10.1590/S1984-4689.v40.e22029
» https://doi.org/10.1590/S1984-4689.v40.e22029 - Clare EL, Lim BK, Fenton MB, Hebert PDN (2011) Neotropical bats: Estimating species diversity with DNA barcodes. Plos One 6(7): e22648. https://doi.org/10.1371/journal.pone.0022648
» https://doi.org/10.1371/journal.pone.0022648 - D’Elía G, Fabre PH, Lessa EP (2019) Rodent systematics in an age of discovery: recent advances and prospects. Journal of Mammalogy 100(3): 852-871. https://doi.org/10.1093/jmammal/gyy179
» https://doi.org/10.1093/jmammal/gyy179 - Dalapicolla J, Percequillo A (2020) Species concepts and taxonomic practice in the integrative taxonomy era: an example using South American rodents. Boletim da Sociedade Brasileira de Mastozoologia 88: 36-54.
- Diaz S, Sánchez-Vendizú P, Graham-Angeles L, Pacheco V (2021) Diversidad y conservación de los mamíferos mayores de Loreto, Perú. Revista Peruana de Biología 28(especial): 269-302. https://doi.org/10.15381/rpb.v28iespecial.21910
» https://doi.org/10.15381/rpb.v28iespecial.21910 - Erwin TL, Pimienta MC, Murillo OE, Aschero V (2004) Mapping patterns of β-diversity for beetles across the western Amazon basin: A preliminary case for improving conservation strategies. Proceedings of the California Academy of Sciences 56: 72-85.
- FAO (1988) FAO/Unesco soil map of the world, revised legend, with corrections and updates. World Soil Resources Report 60. FAO, Rome, 119 pp.
- Fearnside PM (1996) Amazonian deforestation and global warming: Carbon stocks in vegetation replacing Brazil’s Amazon forest. Forest Ecology and Management 80(1): 21-34. https://doi.org/10.1016/0378-1127(95)03647-4
» https://doi.org/10.1016/0378-1127(95)03647-4 - Fearnside PM (2006) tropical deforestation and global warming. Science 312(5777): 1137-1137. https://doi.org/10.1126/science.312.5777.1137c
» https://doi.org/10.1126/science.312.5777.1137c - Fernández-Llamazares Á, López-Baucells A, Velazco PM, Gyawali A, Rocha R, Terraube J, Cabeza M (2021) The importance of indigenous territories for conserving bat diversity across the Amazon biome. Perspectives in Ecology and Conservation 19(1): 10-20. https://doi.org/10.1016/j.pecon.2020.11.001
» https://doi.org/10.1016/j.pecon.2020.11.001 - Ferreira CM, Sabino-Marques H, Barbosa S, Costa P, Encarnação C, Alpizar-Jara R, et al. (2018) Genetic non-invasive sampling (gNIS) as a cost-effective tool for monitoring elusive small mammals. European Journal of Wildlife Research 64(46): 1-15. https://doi.org/10.1007/s10344-018-1188-8
» https://doi.org/10.1007/s10344-018-1188-8 - Finer M, Jenkins CN, Pimm SL, Keane B, Ross C (2008) Oil and gas projects in the western Amazon: threats to wilderness, biodiversity, and indigenous peoples. Plos One 3(8): e2932. https://doi.org/10.1371/journal.pone.0002932
» https://doi.org/10.1371/journal.pone.0002932 - Fong JJ, Blom MP, Aowphol A, McGuire JA, Sutcharit C, Soltis PS (2023) Editorial: Recent advances in museomics: revolutionizing biodiversity research. Frontiers in Ecology and Evolution 11: 188172. https://doi.org/10.3389/fevo.2023.1188172
» https://doi.org/10.3389/fevo.2023.1188172 - Flagstad Ø, Pradhan NMB, Kvernstuen LG, Wegge P (2012) Conserving small and fragmented populations of large mammals: Non-invasive genetic sampling in an isolated population of Asian elephants in Nepal. Journal for Nature Conservation 20(3): 181-190. https://doi.org/10.1016/j.jnc.2012.01.006
» https://doi.org/10.1016/j.jnc.2012.01.006 - Gannon WL, Sikes RS, The Animal Care and Use Committee of the American Society of Mammalogists (2007) Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research. Journal of Mammalogy 88(3): 809-823. https://doi.org/10.1644/06-MAMM-F-185R1.1
» https://doi.org/10.1644/06-MAMM-F-185R1.1 - García-Dávila CR, Castro-Ruiz D, Sánchez-Ribeiro H, Ismiño-Orbe RA, Rengifo-Trigoso D, García-Vásquez A, Tello-Martín JS, Chota-Macuyama W, Duponchelle F, Renno JF (2014) Diversidad de ictioplancton en los ríos Curaray, Arabela y Napo (Amazonía peruana). Folia Amazónica 23(1): 67-78. https://doi.org/10.24841/fa.v23i1.9
» https://doi.org/10.24841/fa.v23i1.9 - García-Dávila C, Castro-Ruiz D, Renno J-F, Chota-Macuyama W, Carvajal-Vallejos FM, Sanchez H, et al. (2015) Using barcoding of larvae for investigating the breeding seasons of pimelodid catfishes from the Marañón, Napo and Ucayali rivers in the Peruvian Amazon. Journal of Applied Ichthyology 31(S4): 40-51. https://doi.org/10.1111/jai.12987
» https://doi.org/10.1111/jai.12987 - Gardner AL (2007) Mammals of South America. University of Chicago Press, Chicago, vol. 1, 669 pp.
- Gauthier J, Pajkovic M, Neuenschwander S, Kaila L, Schmid S, Orlando L, Alvarez N (2020) Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland. Molecular Ecology Resources 20(5): 1191-1205. https://doi.org/10.1111/1755-0998.13167
» https://doi.org/10.1111/1755-0998.13167 - Graham-Angeles L, Sánchez-Vendizú P, Diaz S, Pacheco V (2021) Diversidad y conservación de los murciélagos de Loreto, Perú. Revista Peruana de Biología 28(especial): 1-56. https://doi.org/10.15381/rpb.v28iespecial.21917
» https://doi.org/10.15381/rpb.v28iespecial.21917 - Graybeal A (1993) The phylogenetic utility of cytochrome b: lessons from bufonid frogs. Molecular Phylogenetics and Evolution 2(3): 256-269. https://doi.org/10.1006/mpev.1993.1024
» https://doi.org/10.1006/mpev.1993.1024 - Hebert PD, DeWaard JR, Zakharov EV, Prosser SW, Sones JE, McKeown JT, et al. (2013) A DNA ‘Barcode Blitz’: Rapid digitization and sequencing of a natural history collection. Plos One 8(7): e68535. https://doi.org/10.1371/journal.pone.0068535
» https://doi.org/10.1371/journal.pone.0068535 - Henry P, Henry A, Russello MA (2011) A noninvasive hair sampling technique to obtain high quality DNA from elusive small mammals. Journal of Visualized Experiments 49: e2791. https://doi.org/10.3791/2791
» https://doi.org/10.3791/2791 - Janiak MC, Silva FE, Beck RM, de Vries D, Kuderna LF, Torosin NS, et al. (2022) Two hundred and five newly assembled mitogenomes provide mixed evidence for rivers as drivers of speciation for Amazonian primates. Molecular Ecology 31(14): 3888-3902. https://doi.org/10.1111/mec.16554
» https://doi.org/10.1111/mec.16554 - Jin M, Zwick A, Ślipiński A, de Keyzer R, Pang H (2020) Museomics reveals extensive cryptic diversity of Australian prionine longhorn beetles with implications for their classification and conservation. Systematic Entomology 45(4): 745-770. https://doi.org/10.1111/syen.12424
» https://doi.org/10.1111/syen.12424 - Johnson KR, Owens IFP, The Global Collection Group (2023) A global approach for natural history museum collections. Science 379(6638): 1192-1194. https://doi.org/10.1126/science.adf6434
» https://doi.org/10.1126/science.adf6434 - Karp A, Edwards KJ, Bruford M, Funk S, Vosman B, Morgante M, Seberg O, Kremer A, Boursot P, Arctander P, Tautz D, Hewitt GM (1997) Molecular technologies for biodiversity evaluation: Opportunities and challenges. Nature Biotechnology 15(7): 625-628. https://doi.org/10.1038/nbt0797-625
» https://doi.org/10.1038/nbt0797-625 - Killeen TJ, Douglas M, Consiglio T, Jørgensen PM, Mejia J (2007) Dry spots and wet spots in the Andean hotspot. Journal of Biogeography 34(8): 1357-1373. https://doi.org/10.1111/j.1365-2699.2006.01682.x
» https://doi.org/10.1111/j.1365-2699.2006.01682.x - Lessa EP, Cook JA, D’Elía G, Opazo JC (2014) Rodent diversity in South America: transitioning into the genomics era. Frontiers in Ecology and Evolution 2: 1-7. https://doi.org/10.3389/fevo.2014.00039
» https://doi.org/10.3389/fevo.2014.00039 - Mena JL, Yagui H, Tejeda V, Bonifaz E, Bellemain E, Valentini A, et al. (2021) Environmental DNA metabarcoding as a useful tool for evaluating terrestrial mammal diversity in tropical forests. Ecological Applications 31(5): e02335. https://doi.org/10.1002/eap.2335
» https://doi.org/10.1002/eap.2335 - Mulcahy DG, Ibáñez R, Jaramillo CA, Crawford AJ, Ray JM, Gotte SW, et al. (2022) DNA barcoding of the National Museum of Natural History reptile tissue holdings raises concerns about the use of natural history collections and the responsibilities of scientists in the molecular age. Plos One 17(3): e0264930. https://doi.org/10.1371/journal.pone.0264930
» https://doi.org/10.1371/journal.pone.0264930 - Nachman MW, Beckman EJ, Bowie RCK, Cicero C, Conroy CJ, Dudley R, et al. (2023) Specimen collection is essential for modern science. Plos Biology 21(11): e3002318. https://doi.org/10.1371/journal.pbio.3002318
» https://doi.org/10.1371/journal.pbio.3002318 - Nascimento FOD, Cheng J, Feijó A (2021) Taxonomic revision of the pampas cat Leopardus colocola complex (Carnivora: Felidae): an integrative approach. Zoological Journal of the Linnean Society 191(2): 575-611. https://doi.org/10.1093/zoolinnean/zlaa043
» https://doi.org/10.1093/zoolinnean/zlaa043 - Noreña A, González Muñoz A, Mosquera-Rendón J, Botero K, Cristancho MA (2018) Colombia, an unknown genetic diversity in the era of Big Data. BMC Genomics 19(Suppl. 8): 61-73. https://doi.org/10.1186/s12864-018-5194-8
» https://doi.org/10.1186/s12864-018-5194-8 - Oliveira PJC, Asner GP, Knapp DE, Almeyda A, Galván-Gildemeister R, Keene S, Raybin RF, Smith RC (2007) Land-use allocation protects the Peruvian Amazon. Science 317(5842): 1233-1236. https://doi.org/10.1126/science.1146324
» https://doi.org/10.1126/science.1146324 - Orta-Martínez M, Finer M (2010) Oil frontiers and indigenous resistance in the Peruvian Amazon. Ecological Economics 70(2): 207-218. https://doi.org/10.1016/j.ecolecon.2010.04.022
» https://doi.org/10.1016/j.ecolecon.2010.04.022 - Pacheco V, Cadenillas R, Salas E, Tello C, Zeballos H (2009) Diversidad y endemismo de los mamíferos del Perú. Revista Peruana de Biología 16(1): 5-32.
- Pacheco V, Graham-Angeles L, Diaz S, Hurtado CM, Ruelas D, Cervantes OK, Serrano JE (2020) Diversidad y distribución de los mamíferos del Perú por departamentos y ecorregiones I. Revista Peruana de Biología 27(3): 289-328. https://doi.org/10.15381/rpb.v27i3.18356
» https://doi.org/10.15381/rpb.v27i3.18356 - Pacheco V, Diaz S, Graham-Angeles L, Flores-Quispe M, Calizaya-Mamani G, Ruelas D, Sánchez-Vendizú P (2021) Lista actualizada de la diversidad de los mamíferos del Perú y una propuesta para su actualización. Revista Peruana de Biología 28(4): 9-38. https://doi.org/10.15381/rpb.v28i4.21019
» https://doi.org/10.15381/rpb.v28i4.21019 - Pacheco V, Ruelas D (2023) Systematic revision of Thomasomys cinereus (Rodentia: Cricetidae: Sigmodontinae) from northern Peru and southern Ecuador, with descriptions of three new species. Bulletin of the American Museum of Natural History 461(1): 1-72.
- Patton JL, Pardiñas UFJ, D’Elía G (2015) Mammals of South America. University of Chicago Press, Chicago , vol. 2, 1290 pp.
- Quintana H, Pacheco V, Salas E (2009) Diversidad y conservación de los mamíferos de Ucayali, Perú. Ecología Aplicada 8(1-2): 91-103.
- Rand DM (1993) Endotherms, ectotherms, and mitochondrial genome-size variation. Journal of Molecular Evolution 37: 281-295. https://doi.org/10.1007/BF00175505
» https://doi.org/10.1007/BF00175505 - Rengifo EM, D’Elía G, García G, Charpentier E, Cornejo FM (2022) A new species of titi monkey, genus Cheracebus Byrne et al., 2016 (Primates: Pitheciidae), from Peruvian Amazonia. Mammal Study 48(1): 1-16. https://doi.org/10.3106/ms2022-0019
» https://doi.org/10.3106/ms2022-0019 - Rojas R, Castro JC, García-Dávila C (2018) Situación actual de la base de dato genéticos de vertebrados de la región Loreto, Perú. Folia Amazónica 27(2): 151-162. https://doi.org/10.24841/fa.v27i2.442
» https://doi.org/10.24841/fa.v27i2.442 - Ruelas D, Pacheco V (2022) New morphological data and phylogenetic position of the rare Short-tailed Opossum Monodelphis ronaldi (Didelphimorphia: Didelphidae) with new records. Mammalian Biology 102(1): 189-204. https://doi.org/10.1007/s42991-021-00219-x
» https://doi.org/10.1007/s42991-021-00219-x - Ruiz-García M, Cerón Á, Sánchez-Castillo S, Rueda-Zozaya P, Pinedo-Castro M, Gutierrez-Espeleta G, Shostell JM (2017) Phylogeography of the Mantled Howler Monkey (Alouatta palliata; Atelidae, Primates) across its geographical range by means of mitochondrial genetic analyses and new insights about the phylogeny of Alouatta Folia Primatologica 88(5): 421-454. https://doi.org/10.1159/000480502
» https://doi.org/10.1159/000480502 - Sanchez-Vendizú P, Pacheco V, Vivas-Ruiz D (2018) An introduction to the systematics of Small-Bodied Neacomys (Rodentia: Cricetidae) from Peru with descriptions of two new species. American Museum Novitates 3913: 1-38.
- Sánchez-Vendizú P, Graham-Angeles L, Diaz S, Pacheco V (2021) Diversidad y estado de conservación de pequeños mamíferos de Loreto, Perú. Revista Peruana de Biología 28(special): e21907. https://doi.org/10.15381/rpb.v28iespecial.21907
» https://doi.org/10.15381/rpb.v28iespecial.21907 - Schenk D, Song G, Ke Y, Wang Z (2017) Amplification of overlapping DNA amplicons in a single-tube multiplex PCR for targeted next-generation sequencing of BRCA1 and BRCA2. Plos One 12: e0181062. https://doi.org/10.1371/journal.pone.0181062
» https://doi.org/10.1371/journal.pone.0181062 - Sandoval EDP, Jędrzejewski W, Molinari J, Vozdova M, Cernohorska H, Kubickova S, et al. (2024) Description of Bisbalus, a new genus for the Gray Brocket, Mazama cita Osgood, 1912 (Mammalia, Cervidae), as a step to solve the Neotropical Deer puzzle. Taxonomy 4(1): 10-26.
- SERFOR (2018) Libro Rojo de la Fauna Silvestre Amenazada del Perú. Servicio Nacional Forestal y de Fauna Silvestre, Lima, 547 pp.
- Silva FE, do Amaral JV, Roos C, Bowler M, Röhe F, Sampaio R, et al. (2022) Molecular phylogeny and systematics of bald uakaris, genus Cacajao Lesson, 1840 (Primates: Pitheciidae), with the description of a new species. Molecular Phylogenetics and Evolution 173: 107509. https://doi.org/10.1016/j.ympev.2022.107509
» https://doi.org/10.1016/j.ympev.2022.107509 - Stotz DF, Fitzpatrick JW, Parker TE III, Moskowitz DK (1996) Neotropical birds, ecology, and conservation. University of Chicago Press, Chicago, 502 pp.
- Thompson CW, Phelps KL, Allard MW, Cook JA, Dunnum JL, Ferguson AW, et al. (2021) Preserve a voucher specimen! The critical need for integrating natural history collections in infectious disease studies. mBio 12(1): e02698. https://doi.org/10.1128/mBio.02698-20
» https://doi.org/10.1128/mBio.02698-20 - Tobe SS, Kitchener AC, Linacre AMT (2010) Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome b and cytochrome oxidase subunit I mitochondrial genes. Plos One 5(11): e14156. https://doi.org/10.1371/journal.pone.0014156
» https://doi.org/10.1371/journal.pone.0014156 - Trevisan B, Alcantara DMC, Machado DJ, Marques FPL, Lahr DJG (2019) Genome skimming is a low-cost and robust strategy to assemble complete mitochondrial genomes from ethanol preserved specimens in biodiversity studies. PeerJ 13(7): e7543. https://doi.org/10.7717/peerj.7543
» https://doi.org/10.7717/peerj.7543 - Urban L, Perlas A, Francino O, Martí-Carreras J, Muga BA, Mwangi JW, et al. (2023) Real-time genomics for One Health. Molecular Systems Biology 19: e11686. https://doi.org/10.15252/msb.202311686
» https://doi.org/10.15252/msb.202311686 - Velazco PM, Patterson BD (2019) Small mammals of the Mayo River Basin in northern Peru, with the description of a new species of Sturnira (Chiroptera: Phyllostomidae). Bulletin of the American Museum of Natural History 429: 1-67.
- Villén-Pérez S, Anaya-Valenzuela L, Conrado da Cruz D, Fearnside PM (2022) Mining threatens isolated indigenous peoples in the Brazilian Amazon. Global Environmental Change 72(102398): 1-11. https://doi.org/10.1016/j.gloenvcha.2021.102398
» https://doi.org/10.1016/j.gloenvcha.2021.102398 - Voss RS, Emmons L (1996) Mammalian diversity in Neotropical lowland rainforests: A preliminary assessment. Bulletin of the American Museum of Natural History 230: 1-115.
- Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: A review of applications and recommendations for accurate data collection. The Journal of Wildlife Management 69(4): 1419-1433. https://doi.org/10.2193/0022-541X(2005)69[1419:NGSTFW]2.0.CO;2
- Wallace AR (1854) On the monkeys of the Amazon. Proceedings of the Zoological Society of London 1852: 107-110.
- Watsa M, Wildlife Disease Surveillance Focus Group (2020a) Rigorous wildlife disease surveillance. Science 369(6500): 145-148. https://doi.org/10.1126/science.abc0017
» https://doi.org/10.1126/science.abc0017 - Watsa M, Wildlife Disease Surveillance Focus Group (2020b) Response to Vanhove et al. and Colella et al. Science 370(6518): 774-775. https://doi.org/10.1126/science.abe9392
» https://doi.org/10.1126/science.abe9392 - Winter DJ (2017) Rentrez: An R package for the NCBI eUtils API. The R Journal 9(2): 520-526.
- Young BE, Stuart SN, Chanson JS, Cox NA, Boucher TM (2004) Disappearing jewels: The status of New World amphibians. NatureServe, Arlington, 60 pp.
ADDITIONAL NOTES
-
ZooBank register
-
How to cite this article
Pacheco V, Martínez-Altamirano J, Mena JL, Diaz S, Sánchez-Vendizú P, Arana A, Salinas L, Arana C, Arakaki M, Tobler MW, Watsa M (2024) Disproportion between the Peruvian Amazonian megadiverse mammalian fauna and the available molecular information. Zoologia 41: e23110. https://doi.org/10.1590/S1984-4689.v41.e23110 -
Published by
Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)
Supplementary Material 1
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Gazetter data.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Supplementary Material 2
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Species list.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Supplementary Material 3
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Sequence account.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Supplementary Material 4
Authors: V Pacheco, J Martínez-Altamirano, JL Mena, et al.
Data type: Species account.
Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Edited by
Editorial responsibility
Publication Dates
-
Publication in this collection
16 Aug 2024 -
Date of issue
2024
History
-
Received
31 Dec 2023 -
Accepted
19 June 2024