Abstract
The genus Gracilinanus ranges from savannas to dense forests in South America, yet its systematics have never been thoroughly investigated across its wide distributional range. We assessed Gracilinanus phylogenetic relationships, species boundaries, and geographical limits using mtDNA sequences. Our analysis confirmed the distinctiveness of the six recognized species (G. aceramarcae, G. agilis, G. emiliae, G. marica, G. microtarsus, and G. peruanus), with a mean p-distance for interspecific nucleotide sequence divergences ranging from 13–16.2% and robust phylogenetic support (BPP > 0.95; BS > 75%). Refined species delimitation approaches (GMYC, PTP, ASAP) revealed potential cryptic diversity, suggesting up to 20 candidate species. Three geographically structured and divergent lineages (4.1–4.8% sequence divergence) were identified within G. agilis, extending its Cerrado range. Within G. emiliae, we found divergence values ranging from 4.7–5.7% and the first known record for the northeastern Atlantic Forest. Three divergent clades were recovered within G. microtarsus (9.0–9.8% sequence divergence), including a new lineage for the northern Atlantic Forest. For G. peruanus, we found two divergent lineages (7.2%) and the first documented occurrence for Amazonian lowland forest. This comprehensive sampling revealed greater genetic diversity in Gracilinanus, extending its geographic limits. Here we propose nine putative new species, emphasizing a hidden diversity that warrants formal description and further increases the taxonomic diversity of this genus. These newly identified lineages underscore the urgency of inventorying and conserving the threatened ecosystems of the Cerrado and Atlantic Forest hotspots.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Sequence data are deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and are publicly available. Datasets generated and/or analyzed during the current study are also available from the corresponding author upon request.
References
Abreu-Jr EF, Pavan SE, Tsuchiya MTN, Wilson DE, Percquillo AR (2020) Museomics of tree squirrels: a dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul. BMC Evol Biol 20:77. https://doi.org/10.1186/s12862-020-01639-y
Agra MF (1999) A new species of Solanum subgenus Leptostemonum (Solanaceae) from Chapada da Diamantina, Bahia, Brazil. Novon 9(3):292-295. https://doi.org/10.2307/3391723
Almeida FFM (1976) The system of continental rifts bordering the Santos Basin, Brazil. An Acad Bras Cienc 48(Suppl):15-26
Almeida FFM, Carneiro CDR (1998) Origem e evolução da Serra do Mar. Rev Bras Geociênc 28(2):135–150. https://doi.org/10.25249/0375-7536.1998135150
Amador LI, Giannini NP (2016) Phylogeny and evolution of body mass in didelphid marsupials (Marsupialia: Didelphimorphia: Didelphidae). Org Divers Evol 16:641-657. https://doi.org/10.1007/s13127-015-0259-x
Anderson RP, Gutiérrez EE, Ochoa-G J, García FJ, Aguilera M (2012) Faunal nestedness and species–area relationship for small non-volant mammals in “sky islands” of northern Venezuela. Stud Neotrop Fauna Environ 47(3):157-170. https://doi.org/10.1080/01650521.2012.745295
Antonelli A, Quijada-Mascareñas A, Crawford AJ, Bates JM, Velazco PM, Wüster W (2010) Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In: Hoorn C, Wesselingh FP (eds) Amazonia, Landscape and Species Evolution: a Look into the Past. Blackwell Publishing, Oxford, pp 386–404. https://doi.org/10.1002/9781444306408.ch24
Astúa D, Cherem JJ, Teta P (2022) Taxonomic checklist of living American marsupials. In: Cáceres NC, Dickman CR (eds) American and Australasian Marsupials. Springer, Cham. https://doi.org/10.1007/978-3-030-88800-8_31-1
Bezerra AMR, Castiglia R, Pereira LG, Moreira JC, Bonvicino CR (2020) Molecular systematics of the genus Necromys (Rodentia: Cricetidae: Sigmodontinae) reveals two cryptic and syntopic species in western Cerrado of Brazil. Zool Anz 285:147-158. https://doi.org/10.1016/j.jcz.2020.02.007
Bonvicino CR, Lazar A, Freitas TPT, Lanes RO, D’Andrea PS (2023). Diversification of South American didelphid marsupials. In: Cáceres NC, Dickman CR (eds) American and Australasian Marsupials. Springer, Cham. https://doi.org/10.1007/978-3-030-88800-8_14-2
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Drummond AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15(4):e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Brandão MV, Rocha PA, Dantas SP, Pascoal W (2014) New records of the elusive marsupial Gracilinanus emiliae (Didelphimorphia, Didelphidae) from the Brazilian Amazon basin and a range extension for the species. Mastozool Neotrop 21(2):325-330
Brennand PGG, Langguth A, Percequillo AR (2013) The genus Hylaeamys Weksler, Percequillo, and Voss 2006 (Rodentia: Cricetidae: Sigmodontinae) in the Brazilian Atlantic Forest: geographic variation and species definition. J Mammal 94(6):1346-1363. https://doi.org/10.1644/12-MAMM-A-312.1
Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchus fuscus (Passeriformes, Dendrocolaptidae): vicariance and recent demographic expansion in southern Atlantic forest. Biol J Linn Soc 91(1):73–84. https://doi.org/10.1111/j.1095-8312.2007.00775.x
Caramaschi FP, Nascimento FF, Cerqueira R, Bonvicino CR (2011) Genetic diversity of wild populations of the grey short-tailed opossum, Monodelphis domestica (Didelphimorphia: Didelphidae), in Brazilian landscapes. Biol J Linn Soc 104(2):251-263. https://doi.org/10.1111/j.1095-8312.2011.01724.x
Carnaval AC, Waltari E, Rodrigues MT, Rosauer D, VanDerWal J, Damasceno R, Prates I, Strangas M, Spanos Z, Rivera D, Pie MR, Firkowski CR, Bornschein MR, Ribeiro LF, Moritz C (2014). Prediction of phylogeographic endemism of an environmentally complex biome. Proc R Soc B 281:20141461. https://doi.org/10.1098/rspb.2014.1461
Casagrande AF, Santos-Filho MD (2019) Use of forest remnants and teak (Tectona grandis) plantations by small mammals in Mato Grosso, Brazil. Stud Neotrop Fauna Environ 54(3):181-190. https://doi.org/10.1080/01650521.2019.1656520
Costa LP (2003). The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30(1):71-86. https://doi.org/10.1046/j.1365-2699.2003.00792.x
Costa LP, Leite YL, Fonseca GA, Fonseca MT (2000) Biogeography of South American forest mammals: endemism and diversity in the Atlantic Forest. Biotropica 32(4):872-881. https://doi.org/10.1646/0006-3606(2000)032[0872:BOSAFM]2.0.CO;2
Costa LP, Leite YLR, Patton JL (2003) Phylogeography and systematics on two species of gracile mouse opossums, genus Gracilinanus (Marsupialia: Didelphidae) from Brazil. Proc Biol Soc Wash 116(2):275-292
Creighton GK, Gardner AL (2008) Genus Gracilinanus. In: Gardner AL (ed) Mammals of South America: Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, pp 43-49
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Díaz-Nieto JF, Jansa SA, Voss RS (2016a). Phylogenetic relationships of Chacodelphys (Marsupialia: Didelphidae: Didelphinae) based on “ancient” DNA sequences. J Mammal 97(2):394-404. https://doi.org/10.1093/jmammal/gyv197
Díaz-Nieto JF, Jansa SA, Voss RS (2016b) DNA sequencing reveals unexpected recent diversity and an ancient dichotomy in the American marsupial genus Marmosops (Didelphidae: Thylamyini). Zool J Linn Soc 176(4):914-940. https://doi.org/10.1111/zoj.12343
Dinerstein E, Olson D, Joshi A, Vynne C, Burgess ND, Wikramanayake E, Hahn N, Palminteri S, Hedao P, Noss R, Hansen M, Locke H, Ellis EC, Jones B, Barber CV, Hayes R, Kormos C, Martin V, Crist E, Sechrest W, Price L, Baillie JEM, Weeden D, Suckling K, Davis C, Sizer N, Moore R, Thau D, Birch T, Potapov P, Turubanova S, Tyukavina A, Souza N, Pintea L, Brito JC, Llewellyn OA, Miller AG, Patzelt A, Ghazanfar SA, Timberlake J, Kloser H, Shennan-Farpon Y, Kindt R, Lillesø JB, Breugel P, Graudal L, Voge M, Al-Shammari KF, Saleem M (2017). An ecoregion-based approach to protecting half the terrestrial realm. BioSci 67(6):534–545. https://doi.org/10.1093/biosci/bix014
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113. https://doi.org/10.1186/1471-2105-5-113
Faria MB, Nascimento FF, Oliveira JA, Bonvicino CR (2013) Biogeographic determinants of genetic diversification in the mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae). J Hered 104(5):613-626. https://doi.org/10.1093/jhered/est039
Faria MB, Lanes RO, Bonvicino CR (2019) Guia dos Marsupiais do Brasil. Sociedade Brasileira de Mastozoologia, Amélie Editora, São Caetano do Sul
Fegies AC, Carmignotto AP, Perez MF, Guilardi MD, Lessinger AC (2021) Molecular phylogeny of Cryptonanus (Didelphidae: Thylamyini): evidence for a recent and complex diversification in South American open biomes. Mol Phylogenet Evol 162:107213. https://doi.org/10.1016/j.ympev.2021.107213
Feijó A, Beltrão M, Costa-Pinto AL, Rocha PA, Freitas MA, Campos BATP, Astúa D, Cordeiro-Estrela P (2023). Mammals of the Pernambuco endemism center: diversity, biogeography, research gaps, and conservation concerns. In: Pereira Filho GA, França FGR, Alves RRN, Vasconcellos A (eds) Animal Biodiversity and Conservation in Brazil's Northern Atlantic Forest. Springer, Cham. https://doi.org/10.1007/978-3-031-21287-1_13
Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62(5):707-724. https://doi.org/10.1093/sysbio/syt033
Gali L, Pacifico R, Almeda F, Fidanza K (2022) Two new species of Microlicia (Melastomataceae) from Chapada Diamantina, Bahia, northeastern Brazil. Phytotaxa 544(1):52–60. https://doi.org/10.11646/phytotaxa.544.1.4
Gardner AL (2005) Order Didelphimorphia. In: Wilson DE, Reeder DM (eds) Mammal Species of the World. A Taxonomic and Geographic Reference. Johns Hopkins University Press, Baltimore, pp 15-24
Gardner AL, Creighton GK (1989) A new generic name for Tate’s microtarsus group of South American mouse opossums (Marsupialia: Didelphidae). Proc Biol Soc Wash 102(1):3-7
Geise L, Astúa D (2009) Distribution extension and sympatric occurrence of Gracilinanus agilis and G microtarsus (Didelphimorphia, Didelphidae), with cytogenetic notes. Biota Neotrop 9(4):269–276. https://doi.org/10.1590/S1676-06032009000400030
Falling Rain Software (2017) Global Gazetteer Version 2.3 http://www.fallingrain.com/world/index.html. Accessed on Jul 2023
Gonzaga LP, Carvalhaes AM, Buzzetti DR (2007) A new species of Formicivora antwren from the Chapada Diamantina, eastern Brazil (Aves: Passeriformes: Thamnophilidae). Zootaxa 1473(1):25–44. https://doi.org/10.11646/zootaxa.1473.1.2
Grazziotin FG, Monzel M, Echeverrigaray S, Bonatto SL (2006). Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest. Mol Ecol 15(13):3969-3982. https://doi.org/10.1111/j.1365-294X.2006.03057.x
Hershkovitz P (1992) The South American gracile mouse opossum genus Gracilinanus Gardner and Creighton, 1989 (Marmosidae, Marsupialia): a taxonomic review with notes on general morphology and relationships. Fieldiana Zool 70:1-56. https://doi.org/10.5962/bhl.title.3521
Jansa SA, Barker FK, Voss RS (2014) The early diversification history of didelphid marsupials: a window into South America's “Splendid Isolation”. Evol 68(3):684-695. https://doi.org/10.1111/evo.12290
Kimura MA (1980) Simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120. https://doi.org/10.1007/BF01731581
Ledo RMD, Colli GR (2017). The historical connections between the Amazon and the Atlantic Forest revisited. J Biogeogr 44(11):2551-2563. https://doi.org/10.1111/jbi.13049
Leite YL, Costa LP, Loss AC, Rocha RG, Batalha-Filho H, Bastos AC, Pardini R (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci USA 113(4):1008-1013. https://doi.org/10.1073/pnas.1513062113
Loss S, Costa LP, Leite YR (2011) Geographic variation phylogeny and systematic status of Gracilinanus microtarsus (Mammalia: Didelphimorphia: Didelphidae). Zootaxa 2761(1):1–33. https://doi.org/10.11646/zootaxa.2761.1.1
Maniatis T, Sambrook J, Fritsch EF (1982) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Matthew K, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturoock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes S, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinform 28(12):1647-1649. https://doi.org/10.1093/bioinformatics/bts199
Mendonça RFB, Colle AC, Freitas LC, Martins TF, Horta MC, Oliveira GMB, Pacheco R, Mateus LAF, Rossi RV (2020) Ectoparasites of small mammals in a fragmented area of the southern Amazonia: interaction networks and correlations with seasonality and host sex. Exp Appl Acarol 81:117-134. https://doi.org/10.1007/s10493-020-00491-5
Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, BurkHerrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055):521-524. https://doi.org/10.1126/science: 1211028
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the 2010 Gateway Computing Environments Workshop (GCE). New Orleans, LA, pp 1–8. https://doi.org/10.1109/GCE.2010.5676129
Miranda FR, Casali DM, Perini FA, Machado FA, Santos FR (2017) Taxonomic review of the genus Cyclopes Gray, 1821 (Xenarthra: Pilosa), with the revalidation and description of new species. Zool J Linn Soc 183(3):687-721. https://doi.org/10.1093/zoolinnean/zlx079
Mustrangi MA, Patton JL (1997) Phylogeography and Systematics of the Slender Mouse Opossum Marmosops (Marsupialia, Didelphidae). University of California Press, Publications in Zoology 130, Berkeley
Napoli MF, Junca FA (2006) A new species of the Bokermannohyla circumdata group (Amphibia: Anura: Hylidae) from Chapada Diamantina, state of Bahia, Brazil. Zootaxa 1244(1):57–68. https://doi.org/10.11646/zootaxa.1244.1.4
Napoli MF, Caramaschi U, Cruz CAG, Dias IR (2011) A new species of flea-toad, genus Brachycephalus Fitzinger (Amphibia: Anura: Brachycephalidae), from the Atlantic rainforest of southern Bahia, Brazil. Zootaxa 2739(1):33–40. https://doi.org/10.11646/zootaxa.2739.1.3
Nascimento FFD, Pereira LG, Geise L, Bezerra AM, D'Andrea PS, Bonvicino CR (2011) Colonization process of the Brazilian common vesper mouse, Calomys expulsus (Cricetidae, Sigmodontinae): a biogeographic hypothesis. J Hered 102(3):260-268. https://doi.org/10.1093/jhered/esr012
Nascimento FF, Lazar A, Menezes AN, Durans ADM, Moreira JC, Salazar-Bravo J, Bonvicino CR (2013) The role of historical barriers in the diversification processes in open vegetation formations during the Miocene/Pliocene using an ancient rodent lineage as a model. PLoS ONE 8(4):e61924. https://doi.org/10.1371/journal.pone.0061924
Nascimento FEDL, Mermudes JRM, Bravo F, Santos-Silva A (2017) Checklist, new species and new records of Cerambycidae (Insecta: Coleoptera) from Chapada Diamantina, Bahia state, Brazil. Zootaxa 4232(3):347–360. https://doi.org/10.11646/ZOOTAXA.4232.3.4
Palmeirim AF, Santos-Filho M, Peres CA (2020) Marked decline in forest–dependent small mammals following habitat loss and fragmentation in an Amazonian deforestation frontier. PLoS ONE 15(3):e0230209. https://doi.org/10.1371/journal.pone.0230209
Pataro L, Romero R, Roque N (2013) Four new species of Microlicia (Melastomataceae) from Chapada Diamantina, Bahia, Brazil. Kew Bull 68:285-293. https://doi.org/10.1007/S12225-013-9448-Y
Patton JL, Pardiñas UF, D’Elía G (2015) Mammals of South America, Volume 2: Rodents. University of Chicago Press, Chicago
Pavan SE, Jansa SA, Voss RS (2016) Spatiotemporal diversification of a low‐vagility Neotropical vertebrate clade (short‐tailed opossums, Didelphidae: Monodelphis). J Biogeogr 43(7):1299-1309. https://doi.org/10.1111/jbi.12724
Pires C, Weksler M, Lanes RO, Viana MC, Hingst-Zaher E, Faria MB, Alvarez MR, Bonvicino CR (2023) Systematics and biogeography of the Atlantic Forest endemic genus Juliomys (Rodentia: Cricetidae): A test of diversification hypothesis using mitochondrial data. J Mamm Evol 30:695-712. https://doi.org/10.1007/s10914-023-09661-9
Pons J, Barraclough T, Gomez-Zurita J, Cardoso A, Duran D, Hazell S, Kamoun S, Sumlin W, Vogler A (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55(4):595-609. https://doi.org/10.1080/10635150600852011
Puillandre N, Brouillet S, Achaz G (2020) ASAP: assemble species by automatic partitioning. Mol Ecol Resour 21(2):609-620. https://doi.org/10.1111/1755-0998.13281
Puillandre N (2021) ASAP (biotools:asap-assemble) https://bioinfo.mnhn.fr/abi/public/asap/. Accessed on Dec 2023
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901-904. https://doi.org/10.1093/sysbio/syy032
Reid NM, Carstens BC (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol 12(196). https://doi.org/10.1186/1471-2148-12-196.
Ribeiro AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotrop Ichthyol 4(2):225-246. https://doi.org/10.1590/S1679-62252006000200009
Rocha RG, Ferreira E, Loss AC, Heller R, Fonseca C, Costa LP (2015a) The Araguaia river as an important biogeographical divide for didelphid marsupials in central Brazil. J Hered 106(5):593-607. https://doi.org/10.1093/jhered/esv058
Rocha RG, Justino J, Leite YLR, Costa LP (2015b) DNA from owl pellet bones uncovers hidden biodiversity. Syst Biodivers 13(4):403-412. https://doi.org/10.1080/14772000.2015.1044048
Rodrigues MT, Freitas MA, Silva TFS (2009) New species of earless lizard genus Heterodactylus (Squamata: Gymnophthalmidae) from the highlands of Chapada Diamantina, state of Bahia, Brazil. J Herpetol 43(4):605-611. https://doi.org/10.1670/08-133.1
Rodrigues MT, Freitas MA, Silva TFS, Bertolotto CEV (2006) A new species of lizard genus Enyalius (Squamata, Leiosauridae) from the highlands of Chapada Diamantina, state of Bahia, Brazil, with a key to species. Phyllomedusa 5(1):11–24. https://doi.org/10.11606/issn.2316-9079.v5i1p11-24
Ronquist F, Teslenko M, Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539-542. https://doi.org/10.1093/sysbio/sys029
Satler JD, Carstens BC, Hedin M (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Syst Biol 62(6):805-823. https://doi.org/10.1093/sysbio/syt041
Semedo TBF, Brandão MV, Carmignotto AP, Silva Nunes M, Farias IP, Silva MNF, Rossi RV (2015) Taxonomic status and phylogenetic relationships of Marmosa agilis peruana Tate, 1931 (Didelphimorphia: Didelphidae), with comments on the morphological variation of Gracilinanus from central–western Brazil. Zool J Linn Soc 173(1):190-216. https://doi.org/10.1111/zoj.12203
Semedo TBF, Silva MNF, Carmignotto AP, Rossi RV (2021) Three new species of spiny mice, genus Neacomys Thomas, 1900 (Rodentia: Cricetidae), from Brazilian Amazonia. Syst Biodivers 19(8):1113-1134. https://doi.org/10.1080/14772000.2021.1980449
Semedo TBF, Saldanha J, Mendonca RB, Lima-Silva LG, Gutierrez EE, Rossi RV, Dalapicolla J, Brandao MV (2022) Distribution limits, natural history and conservation status of the poorly known Peruvian gracile mouse opossum (Didelphimorphia: Didelphidae). Stud Neotrop Fauna Environ https://doi.org/10.1080/01650521.2021.2024055
Silva MS, Barros NM, Ribas CC, Ferrand N, Morgante JS (2012) Divide to conquer: a complex pattern of biodiversity depicted by vertebrate components in the Brazilian Atlantic Forest. Biol J Linn Soc 107(1):39-55. https://doi.org/10.1111/j.1095-8312.2012.01919.x
Silva CR, Martins ACM, Castro IJ, Bernard E, Cardoso EM, Santos Lima D, Gregorin R, Rossi RV, Percequillo AR, Cruz Castro K (2013) Mammals of Amapá state, eastern Brazilian Amazonia: a revised taxonomic list with comments on species distributions. Mammalia 77(4):409-424. https://doi.org/10.1515/mammalia-2012-0121
Silva LGL, Ferreira DC, Rossi RV (2019) Species diversity of Marmosa subgenus Micoureus (Didelphimorphia, Didelphidae) and taxonomic evaluation of the white-bellied woolly mouse opossum Marmosa constantiae. Zool J Linn Soc 187(1):240-277. https://doi.org/10.1093/zoolinnean/zlz023
Srivathsan A, Meier R (2012) On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNAbarcoding literature. Cladistics 28:190-194. https://doi.org/10.1111/j.1096-0031.2011.00370.x
Suárez-Villota EY, Carmignotto AP, Brandão MV, Percequillo AR, Silva MJJ (2018) Systematics of the genus Oecomys (Sigmodontinae: Oryzomyini): molecular phylogenetic, cytogenetic and morphological approaches reveal cryptic species. Zool J Linn Soc 184(1):182-210. https://doi.org/10.1093/zoolinnean/zlx095
Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinform 26(12):1569-1571. https://doi.org/10.1093/bioinformatics/btq228
Tamura K, Stecher G, Kumar S (2021) MEGA 11: Molecular Evolutionary Genetics Analysis, Version 11. Mol Biol Evol 38(7):3022-3027. https://doi.org/10.1093/molbev/msab120
Tate GHH (1933) A systematic revision of the marsupial genus Marmosa. Bull Am Mus Nat Hist 66:1-250.
Thomé MTC, Zamudio KR, Giovanelli JGR, Haddad CFB, Baldissera FA, Alexandrino J (2010) Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic Forest. Mol Phylogenet Evol 55(3):1018-1031. https://doi.org/10.1016/j.ympev.2010.02.003
Thomé MTC, Sequeira F, Brusquetti F, Carstens B, Haddad CFB, Rodrigues MT, Alexandrino J (2016) Recurrent connections between Amazon and Atlantic forests shaped diversity in Caatinga four-eyed frogs. J Biogeogr 43(5):1045-1056. https://doi.org/10.1111/jbi.12685
Tonini JFR, Costa LP, Carnaval AC (2013) Phylogeographic structure is strong in the Atlantic Forest; predictive power of correlative paleodistribution models, not always. J Zoolog Syst Evol Res 51(2):114-121. https://doi.org/10.1111/jzs.12014
Valdez L, D'Elía G (2013) Differentiation in the Atlantic Forest: phylogeography of Akodon montensis (Rodentia, Sigmodontinae) and the Carnaval-Moritz model of Pleistocene refugia. J Mammal 94(4):911-922. https://doi.org/10.1644/12-MAMM-A-227.1
Vasconcelos LV, Simão-Bianchini R, França F (2016) Two new species of Ipomoea (Convolvulaceae) from the Chapada Diamantina of Bahia, Brazil. Brittonia 68:142-147. https://doi.org/10.1007/s12228-016-9411-y
Vieira EM, Camargo NF (2012) Padrões de uso vertical do hábitat por marsupiais brasileiros. In: Cáceres NC, Monteiro-Filho ELA (eds) Os Marsupiais do Brasil: Biologia, Ecologia e Evolução. Editora UFMS, Campo Grande, pp 347–364
Villela FNJ, Nogueira C (2011) Geologia e geomorfologia da estação ecológica Serra Geral do Tocantins. Biota Neotrop 11(1):217-230. https://doi.org/10.1590/S1676-06032011000100023
Vivo MD (1997) Mammalian evidence of historical ecological change in the Caatinga semiarid vegetation of northeastern Brazil. J Comp Biol 2(1):65-73
Voss RS (2022). An annotated checklist of recent opossums (Mammalia: Didelphidae). Bull Am Mus Nat Hist 455(1):1-76. https://doi.org/10.1206/0003-0090.455.1.1
Voss RS, Jansa SA (2009) Phylogenetic relationships and classification of didelphid marsupials, an extant radiation of New World metatherian mammals. Bull Am Mus Nat Hist 322:1-177. https://doi.org/10.1206/322.1
Voss RS, Lunde DP, Simmons NB (2001) The mammals of Paracou, French Guiana: a Neotropical rainforest fauna. Part 2. nonvolant species. Bull Am Mus Nat Hist 263:1-236. https://doi.org/10.1206/0003-0090(2001)263%3C0003:TMOPFG%3E2.0.CO;2
Voss RS, Yensen E, Tarifa T (2004) An introduction to Marmosops (Marsupialia: Didelphidae), with the description of a new species from Bolivia and notes on the taxonomy and distribution of other Bolivian congeners. Am Mus Novit 3466:1-40. https://doi.org/10.1206/0003-0082(2004)466<0001:AITMMD>2.0.CO;2
Voss RL, Lunde DP, Jansa SA (2005) On the contents of Gracilinanus Gardner & Creighton, 1989, with the description of a previously unrecognized clade of small didelphids marsupials. Am Mus Novit 3482:1-34. https://doi.org/10.1206/0003-0082(2005)482[0001:OTCOGG]2.0.CO;2
Voss RS, Fleck DW, Jansa SA (2009) On the diagnostic characters, ecogeographic distribution, and phylogenetic relationships of Gracilinanus emiliae (Didelphimorphia: Didelphidae: Thylamyini). Mastozool Neotrop 16(2):433-443
Voss RS, Fleck DW, Jansa SA (2019) Mammalian diversity and Matses ethnomammalogy in Amazonian Peru part 3: marsupials (Didelphimorphia). Bull Am Mus Nat Hist 432:1-90. https://doi.org/10.1206/0003-0090.432.1.1
Zacca T, Bravo F (2012) Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) da porção norte da Chapada Diamantina, Bahia, Brasil. Biota Neotrop 12(2):117-126. https://doi.org/10.1590/S1676-06032012000200012
Zanchetta LS, Rocha RG, Leite YLR (2019) Comparative phylogeography and demographic history of two marsupials of the Atlantic Forest in eastern Brazil. J Zoolog Syst Evol Res 57(3):632-641. https://doi.org/10.1111/jzs.12280
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013a) A general species delimitation method with applications to phylogenetic placements. Bioinform 29(22):2869-2876. https://doi.org/10.1093/bioinformatics/btt499
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013b). bPTP server: a Bayesian implementation of the PTP model for species delimitation. https://species.h-its.org/. Accessed on Sept 2023
Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas.
Acknowledgements
We would like to thank the researchers and curators of the mammalogical scientific collections for tissue samples and accession to vouchers, namely: Juliana Gualda and Dr. Mario de Vivo (MZUSP), Dr. Miguel T. Rodrigues (IBUSP), Dr. Alexandre R. Percequillo (LAMA), Dr. Ana Cristina Mendes-Oliveira (UFPA), and Dr. Cláudia Silva (IEPA). We also would like to thank all researchers and students who contributed in the field, surveying Gracilinanus specimens; to Renato K. Kimura and Silas C. Príncipe for technical support in the laboratory at UFSCar. To George M.T. Mattox and Mercival R. Francisco for their contributions as committee members of the LEF graduation thesis. To Monique R. Brito and Milena C. Telhe for the support in the analyses of the molecular species delimitation approaches.
Funding
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, #88887.615416/2021-00, Conselho Nacional de Desenvolvimento Científico e Tecnológico,grants #107282/2017-8, #408648/2023-6, #457444/2012-6; Fundação de Amparo à Pesquisa do Estado de São Paulo, #98/05075-7; #00/06642-4; #2011/20022-3; #2015/21259-8; #2017/23548-2; #2018/14091-1; #2020/12658-4; #2020/01378-0; #2022/12632-0.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study’s conception and design. Tissue acquisition was performed by Ana Paula Carmignotto. Material preparation, data collection, and edition of figures were performed by all authors. Analyses were performed by Larissa Eler Fernandes and writing was performed by all authors. All authors commented on previous versions of the manuscript, reading and approving the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10914_2024_9706_MOESM1_ESM.xlsx
Online Resource 1: Pairwise K2P divergence values (%) - mean (and range) - among lineages for G. agilis, G. emiliae, G. microtarsus and G. peruanus. (XLSX 17.3 KB)
10914_2024_9706_MOESM3_ESM.docx
Online Resource 3: Geographically-structured clades for G. microtarsus across altitudinal and mountain ranges. (DOCX 11.3 KB)
10914_2024_9706_MOESM4_ESM.docx
Online Resource 4: Time-scaled, fossil-calibrated phylogeny of Gracilinanus. Mean divergence (Ma, above nodes) and range (95% HPD, below nodes). (DOCX 12.2 KB)
Appendix 1
Appendix 1
List of localities of Gracilinanus specimens with DNA sequence data analyzed in the present study.
Number as in the map of Fig. 1. Information is presented in the following format: state or province, department or municipality, locality [geographic coordinates, with underline indicating coordinates not referred to the specific locality]: mtDNA lineage – field or voucher number.
Brazil
-
1.
Alagoas, Passo de Camaragibe, Barra de Camaragibe [09° 19’ S, 35° 25’ W]: Gracilinanus emiliae – PCM 05.
-
2.
Amapá, Ferreira Gomes, Igarapé do Braço, Floresta Nacional do Amapá [01º 18’ S, 51º 35’ W]: Gracilinanus emiliae – KC 96.
-
3.
Bahia, Camacan, Reserva Serra Bonita [15° 24’ S, 39° 29’ W]: Gracilinanus microtarsus – MTR 15893.
-
4.
Bahia, Caetité, Caetité [14° 04’ S, 42° 29’ W): Gracilinanus agilis – LBCE 3817.
-
5.
Bahia, Andaraí, Fazenda Santa Rita, 8 km E Andaraí [12° 48’ S, 41° 16’ W]: Gracilinanus agilis – UFMG 2496.
-
6.
Bahia, Jaborandi, Fazenda Sertão do Formoso [14° 48’ S, 45º 57’ W]: Gracilinanus agilis – CRB 1571.
-
7.
Bahia, Morro do Chapéu, Morro do Chapéu [11° 36’ S, 41° 12’ W]: Gracilinanus microtarsus – MTR 22561.
-
8.
Bahia, Rio de Contas, Rio de Contas [13° 35’ S, 41° 48’ W]: Gracilinanus agilis – MN 67593 (JAO 1171).
-
9.
Bahia, Jussari, RPPN Serra do Teimoso [15° 09’ S, 39° 31’ W]: Gracilinanus microtarsus – ST 207.
-
10.
Ceará, Crato, Chapada do Araripe 7 km SW Crato [07° 17’ S, 39° 27’ W]: Gracilinanus agilis – UFMG 2504.
-
11.
Ceará, Jaguaruana, Jaguaruana [04° 50’ S, 37° 47’ W]: Gracilinanus agilis – LBCE 5254.
-
12.
Espírito Santo, Castelo, Parque Estadual do Forno Grande [20° 30’ S, 41° 06’ W]: Gracilinanus microtarsus – LPC 1447.
-
13.
Espírito Santo, Serra, Área de Proteção Ambiental do Mestre Álvaro [20° 10’ S, 40° 19’ W]: Gracilinanus microtarsus – LPC 1410.
-
14.
Espírito Santo, Águia Branca, Mata da Lagoa, Sítio Krok [18° 58’ S, 40° 44’ W]: Gracilinanus microtarsus – YL 419.
-
15.
Espírito Santo, Ibiraçu, Morro da Vargem, Mosteiro Zen Budista [19° 50’ S, 40° 22’ W]: Gracilinanus microtarsus – MBML 2716.
-
16.
Espírito Santo, Domingos Martins, Parque Estadual de Pedra Azul [20° 24’ S, 40° 58’ W]: Gracilinanus microtarsus – UFES-CTA 831.
-
17.
Espírito Santo, Cariacica, Reserva Biológica Duas Bocas [20° 17’ S, 40° 31’ W]: Gracilinanus microtarsus – LPC 1092.
-
18.
Espírito Santo, Sooretama, Reserva Natural da Vale [19° 12’ S, 40° 06’ W]: Gracilinanus microtarsus – TAX 15.
-
19.
Espírito Santo, São José do Calçado, Sapucaia, Alegoria [21° 02’ S, 41° 43’ W]: Gracilinanus microtarsus – LPC 1377.
-
20.
Goiás, Cachoeira Alta, Cachoeira Alta [18° 43’ S, 51° 19’ W]: Gracilinanus agilis – CM 598.
-
21.
Goiás, Anápolis, Anápolis [16° 19’ S, 48° 58’ W]: Gracilinanus agilis – LBCE 9469.
-
22.
Goiás, Aporé, Aporé [18° 57’ S, 51° 55’ W]: Gracinanus agilis – LBCE 11947.
-
23.
Goiás, Cavalcante, Fazenda Fiandeira, Parque Nacional da Chapada dos Veadeiros, 65 km SSW Cavalcante [14° 04’ S, 47° 45’ W]: Gracilinanus agilis – CRB 895.
-
24.
Goiás, Luziânia, Luziânia [16° 14’ S, 47° 55’ W]: Gracilinanus agilis – LBCE 7500.
-
25.
Goiás, São Domingos, São Domingos [13° 23’ S, 46° 19’ W]: Gracilinanus agilis – LBCE 11997.
-
26.
Goiás, Caldas Novas, Usina Hidrelétrica de Corumbá 30 km SE Caldas Novas [17° 59’ S, 48° 31’ W]: Gracilinanus agilis – UHECO 4722.
-
27.
Goiás, Minaçu, Usina Hidrelétrica de Serra da Mesa [13° 49’ S, 48° 18’ W]: Gracilinanus agilis – UHESM 1759.
-
28.
Maranhão, Açailândia, Açailândia [04° 57’ S, 47° 30’ W]: Gracilinanus agilis – UFPAM 507.
-
29.
Maranhão, Carolina, Parque Nacional Chapada das Mesas [07° 19’ S, 47° 20’ W]: Gracilinanus agilis – APC 2340.
-
30.
Mato Grosso, Jaciara/Juscimeira, Jaciara/Juscimeira [16° 07’ S, 55° 01’ W]: Gracilinanus agilis – UFMT 3817.
-
31.
Mato Grosso, Poconé, Parque Nacional do Pantanal [17° 51’ S, 57° 25’ W]: Gracilinanus agilis – MZUSP 35192.
-
32.
Mato Grosso, Aripuanã, Serra do Expedito, 25 km Aripuanã [11° 03’ S, 59° 30’ W]: Gracilinanus peruanus – UFMT 1379.
-
33.
Mato Grosso, Poconé, Base de Pesquisas do Pantanal CENAP/IBAMA 110 km SSW Poconé [18° 45’ S, 57° 22’ W]: Gracilinanus agilis – UFMG 2497.
-
34.
Mato Grosso, Alto Araguaia, Fazenda Água Limpa [15° 17’ S, 58° 37’ W]: Gracilinanus peruanus – INPA 6740.
-
35.
Mato Grosso, Jauru, Fazenda Alto Jauru [15° 27’ S, 58° 26’ W]: Gracilinanus peruanus – INPA 6736.
-
36.
Mato Grosso, Araputanga, Fazenda Araputanga [15° 21’ S, 58° 26’ W]: Gracilinanus peruanus – INPA 6739.
-
37.
Mato Grosso, Barra do Garças, Fazenda Eldorado [15° 35’ S, 52° 17’ W]: Gracilinanus agilis – UFMT 2043.
-
38.
Mato Grosso, Araputanga, Fazenda Quatro Meninas [15° 20’ S, 58° 33’ W]: Gracilinanus peruanus – INPA 6741.
-
39.
Mato Grosso, Primavera do Leste, Margem esquerda do Rio Cumbuco [15° 13’ S, 54° 03’ W]: Gracilinanus agilis – UFMT 1039.
-
40.
Mato Grosso do Sul, Aquidauana, Aquidauana [20° 28’ S, 55º 47’ W]: Gracilinanus agilis – LBCE 4888.
-
41.
Mato Grosso do Sul, Cassilândia, Cassilândia [19° 06’ S, 51° 44’ W]: Gracilinanus agilis – LBCE 11949.
-
42.
Mato Grosso do Sul, Corumbá, Corumbá [19° 01’ S, 57° 39’ W]: Gracilinanus agilis – LBCE 5665.
-
43.
Mato Grosso do Sul, Rio Miranda, acima Passo do Lontra [19° 34’ S, 57° 00’ W]: Gracilinanus agilis – UFMG 2500.
-
44.
Minas Gerais, Itamonte, Itamonte [22° 17’ S, 44° 52’ W] Gracilinanus microtarsus – MP 499.
-
45.
Minas Gerais, Aiuruoca, Aiuruoca [21° 58’ S, 44° 36’ W] Gracilinanus microtarsus – MP 329.
-
46.
Minas Gerais, Brasilândia de Minas, Brasilândia de Minas [17° 01’ S, 46° 01’ W]: Gracilinanus agilis – MCNM 2189.
-
47.
Minas Gerais, Bocaiúva, Fazenda Corredor, Distrito Carne Seca [17° 06’ S, 43° 49’ W]: Gracilinanus agilis – UFMG 2433.
-
48.
Minas Gerais, Lagoa Santa, Fazenda das Bicas [19° 38’ S, 43° 53’ W]: Gracilinanus microtarsus – EDH 12.
-
49.
Minas Gerais, João Pinheiro, João Pinheiro [17° 44’ S, 46° 10’ W]: Gracilinanus agilis – MCNM 2243.
-
50.
Minas Gerais, Nova Ponte, Mata do Vasco, 12 km W Nova Ponte [19° 08’ S, 47° 40’ W]: Gracilinanus agilis – MVZ 197439.
-
51.
Minas Gerais, Belo Horizonte, Parque Aggeo Pio Sobrinho [19° 59’ S, 43° 58’ W]: Gracilinanus microtarsus – LPC 915.
-
52.
Minas Gerais, Santa Barbara, Parque do Caraça [19° 58’ S, 43° 25’ W]: Gracilinanus microtarsus – NM 04.
-
53.
Minas Gerais, São Gonçalo do Rio Preto, Parque Estadual do Rio Preto, 15 km S São Gonçalo do Rio Preto [18º 09’ S, 43° 23’ W]: Gracilinanus agilis – UFMG 2493.
-
54.
Minas Gerais, Coronel Murta, Ponte do Colatino, margem esquerda do Rio Jequitinhonha [16° 36’ S, 42° 12’ W]: Gracilinanus agilis – UFMG 2495.
-
55.
Minas Gerais, Tiradentes, Tiradentes [21º 07’ S, 44° 10’ W]: Gracilinanus microtarsus – MP 538.
-
56.
Minas Gerais, Lavras, Universidade Federal de Lavras [21° 14’ S, 44º 59’ W]: Gracilinanus microtarsus – MP 79.
-
57.
Pará, Santana do Araguaia, Fazenda Santa Fé [9° 38’ S, 50° 08’ W]: Gracilinanus emiliae – FSF 92 m.
-
58.
Pará, São Félix do Xingu, Terra do Meio [05° 52’ S, 52° 47’ S]: Gracilinanus emiliae – RBM 1141.
-
59.
Paraná, Ortigueira, Ortigueira [24° 13’ S, 50° 55’ W]: Gracilinanus microtarsus – ITM 192.
-
60.
Paraná, Pinhalão, Pinhalão [23° 47’ S, 50° 02’ W]: Gracilinanus microtarsus – ITM 014.
-
61.
Pernambuco, Buíque, Buíque, Parque Nacional do Catimbau [08° 35’ S, 37° 14’ W]: Gracilinanus agilis – AP 614.
-
62.
Piauí, Bom Jesus, Estação Ecológica de Uruçuí-Una, [08° 51’ S, 44° 58’ W]: Gracilinanus agilis – MZUSP 30484.
-
63.
Piauí, João Costa, João Costa [08° 03’ S, 42° 25’ W]: Gracilinanus agilis – LBCE 1240.
-
64.
Piauí, Guaribas, Parque Nacional Serra das Confusões [09° 12’ S, 43° 29’ W]: Gracilinanus agilis – DAM 23 e ARP 73.
-
65.
Rio de Janeiro, Rio de Janeiro, Pedra Branca-Colônia [22° 56’ S, 43° 29’ W]: Gracilinanus microtarsus – LBCE 4093.
-
66.
Rio de Janeiro, Teresópolis, Teresópolis [22° 25’ S, 42° 58’ W]: Gracilinanus microtarsus – LBCE 6662.
-
67.
Rondônia, Chupinguaia, Chupinguaia [12° 14’ S, 60° 44’ W]: Gracilinanus peruanus – UFMT 3816.
-
68.
Rondônia, Porto Velho, Estação Ecológica Mujica Nava [09° 26’ S, 64° 58’ W]: Gracilinanus peruanus – MJ 27.
-
69.
Rondônia, Porto Velho, Usina Hidrelétrica de Jirau [09° 20’ S, 64° 43’ W]: Gracilinanus peruanus – MJ 74.
-
70.
São Paulo, Capão Bonito, Base do Carmo, Fazenda Intervales [24° 20’ S, 48° 25’ W]: Gracilinanus microtarsus – MVZ 182056.
-
71.
São Paulo, Águas de Santa Bárbara, Estação Ecológica de Santa Bárbara [22° 48’ S, 49° 14’ W]: Gracilinanus agilis – APC 2614 and Gracilinanus microtarsus – APC 2403.
-
72.
São Paulo, Sorocaba, Floresta Nacional de Ipanema [23° 26’ S, 47° 37’ W]: Gracilinanus microtarsus – APC 1753.
-
73.
São Paulo, Pinhalzinho, Pinhalzinho [22° 47’ S, 45° 35’ W]: Gracilinanus microtarsus – CIT 974.
-
74.
São Paulo, Cotia, Reserva Florestal do Morro Grande [23° 39’ S, 47° 01’ W]: Gracilinanus microtarsus – AB 343.
-
75.
São Paulo, Santo André, Santo André [23° 40’ S, 46° 32’ W]: Gracilinanus microtarsus – StoAn 46.
-
76.
São Paulo, Ribeirão Grande, Sitio Paulino [24° 06’ S, 48° 23’ W]: Gracilinanus microtarsus – FB 373.
-
77.
São Paulo, Sorocaba, Universidade Federal de São Carlos [23° 35’ S, 47° 31’ W]: Gracilinanus microtarsus – APC 2026.
-
78.
São Paulo, Matão, Matão [21° 36’ S, 48° 22’ W]: Gracilinanus microtarsus – PF 3850.
-
79.
Tocantins, Aliança do Tocantins, Aliança do Tocantins [11° 18’ S, 48º 56’ W]: Gracilinanus agilis – BR-153 132.
-
80.
Tocantins, Lagoa da Confusão, Lagoa da Confusão [10° 47’ S, 49° 37’ W]: Gracilinanus agilis – RGR 426.
-
81.
Tocantins, Parque Nacional do Araguaia [10° 27’ S, 50° 29’ W]: Gracilinanus agilis – MN 60506 (ARB 48) and Gracilinanus agilis – MN 66268 (ARB 71).
-
82.
Tocantins, Pium, Parque Estadual do Cantão [9° 59’ S, 50° 02’ W]: Gracilinanus agilis – UFESMAM 1412.
Peru
83. Junín, Cordilheira de Vilcabamba [11° 40’ S, 73º 40’ W]: Gracilinanus aceramarcae – MUSM 13002.
84. Loreto, Nuevo San Juan, Rio Galvez [05° 15’ S, 73° 10’ W]: Gracilinanus emiliae – MUSM 15292.
Venezuela
85. Falcón, Serranía de San Luis, Parque Nacional J. C. ca. 10 km W + 4 km N Cabure, Sector Cerro Galicia [11° 11’ N, 69° 42’ W]: Gracilinanus marica – EBRG 24864.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Fernandes, L.E., Lessinger, A.C. & Carmignotto, A.P. New data from South American hotspots uncover a greater diversity in Gracilinanus (Didelphimorphia: Didelphidae) mouse opossums. J Mammal Evol 31, 13 (2024). https://doi.org/10.1007/s10914-024-09706-7
Accepted:
Published:
DOI: https://doi.org/10.1007/s10914-024-09706-7