The First Quaternary Record of the Rodent Akodon kadiweu Brandão, Percequillo, D'Elía, Paresque, & Carmignotto, 2021 (Rodentia: Cricetidae: Sigmodontinae)

© 2022 Academia Sinica, Taiwan Open Access The First Quaternary Record of the Rodent Akodon kadiweu Brandão, Percequillo, D'Elía, Paresque, & Carmignotto, 2021 (Rodentia: Cricetidae: Sigmodontinae) Marcus Vinicius Brandão1,2,3,* , Natália Lima Boroni4,5,6 , Ana Paula Carmignotto2, Fernando Araujo Perini5, Leandro de Oliveira Salles6, and Alexandre Reis Percequillo3 1Programa de Pós-Graduação em Sistemática, Taxonomia Animal e Biodiversidade, Museu de Zoologia; Universidade de São Paulo; São Paulo, SP, Brazil. *Correspondence: E-mail: [email protected] (Brandão) 2Laboratório de Diversidade Animal/Sistemática de Mamíferos; Departamento de Biologia; Universidade Federal de São Carlos, Campus Sorocaba, Sorocaba, SP, Brazil. E-mail: [email protected] (Carmignotto) 3Laboratório de Mamíferos; Departamento de Ciências Biológicas; Escola Superior de Agricultura “Luiz de Queiroz”; Universidade de São Paulo; Piracicaba; SP, Brazil. E-mail: [email protected] (Percequillo) 4Programa de Pós-Graduação em Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. E-mail: [email protected] (Boroni) 5Laboratório de Evolução de Mamíferos, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. E-mail: [email protected] (Perini) 6Mastozoologia, Departamento de Vertebrados, Universidade Federal do Rio de Janeiro; Museu Nacional; Rio de Janeiro, RJ, Brazil. E-mail: [email protected] (Salles) Received 12 April 2022 / Accepted 22 September 2022 / Published 22 December 2022 Communicated by Tzu-Ruei Yang Rodents of the genus Akodon comprise 41 extant species, and are considered the most diverse genus of the tribe Akodontini. The most recently described extant species is Akodon kadiweu, known exclusively from Serra da Bodoquena, a karstic region located in Mato Grosso do Sul state, Brazil. Some sub-fossil and fossil specimens of Akodon have been reported in recent years for Brazil, but most remain unidentified at the species level. Here we examine the identity of Quaternary specimens of Akodon sp. from the limestone cave Nossa Senhora Aparecida, located in Serra da Bodoquena. Quantitative characters allowed the distinction of Akodon sp. specimens from smaller and larger congeners, and skull qualitative characters of nasal, interorbital region, supraorbital margins, zygomatic notches, zygomatic plate, incisive foramina, mesopterygoid fossa, mandible and molars allowed to identify these individuals as A. kadiweu. Our results revealed the first known past representatives of Akodon to be recorded in Mato Grosso do Sul, as well as western Brazil. Key words: Akodontini, Cerrado, Grass mouse, Paleontology, South America. BACKGROUND The genus Akodon (Rodentia, Cricetidae, Sigmodontinae) has received considerable attention in several areas of study in the last years, including taxonomy, phylogenetics, morphology, cytogenetics and ecology, among others (Pardiñas et al. 2015 2017; Ávila et al. 2016; Jiménez and Pacheco 2016; Maestri et al. 2016; Hernandez et al. 2017; Machado et al. 2020; Jayat et al. 2020; Vilela et al. 2020; Ruelas et al. 2020; Brandão et al. 2021). Akodon is the most diverse genus of the tribe Akodontini, comprising 41 extant species (Pardiñas et al. 2017; Brandão et al. 2021), which are spread in a wide range of habitats in South America, Citation: Brandão MV, Boroni NB, Carmignotto AP, Perini FA, Salles FO, Percequillo AR. 2022. The first Quaternary record of the rodent Akodon kadiweu Brandão, Percequillo, D'Elía, Paresque, & Carmignotto, 2021 (Rodentia: Cricetidae: Sigmodontinae). Zool Stud 61:78. doi:10.6620/ ZS.2022.61-78. Zoological Studies 61:78 (2022) doi:10.6620/ZS.2022.61-78 1 © 2022 Academia Sinica, Taiwan from sea level to high Andean altitudes, and from tropical and subtropical forests to semidesert areas in Patagonia (Pardiñas et al. 2015 2017). Nevertheless, species diversity is not yet fully known and recent studies based on integrative approaches suggest a higher number of valid taxa (Pardiñas et al. 2015 2017; Jayat et al. 2020; Ruelas et al. 2020), including the recent description of a new species, Akodon kadiweu Brandão, Percequillo, D’Elía, Paresque and Carmignotto, 2021 from Serra da Bodoquena, Mato Grosso do Sul, in western Brazil. Although there has been improvement in our knowledge on living forms of the genus (e.g., Jiménez and Pacheco 2016; Jayat et al. 2020; Ruelas et al. 2020; Brandão et al. 2021), subfossil and fossil records of Akodon from Brazil, as well as from most of South America, remain poorly understood, mostly due to the lack of samples or difficulty in assigning fragmented material to valid names, either to fossil or living species. Considering that Akodon johannis Reig, 1987 may be related to the genus Thaptomys (Reig. op. cit.), at least two extinct species of Akodon are known from non-recent material: A. clivigenis (Winge, 1887) and A. lorenzinii Reig, 1987 (Pardiñas et al. 2002 2015). The oldest known record of the genus is A. lorenzinii from the Pliocene of Argentina, in Mar del Plata, Buenos Aires province (Reig 1987), but the fossil record indicates Akodon was more widespread during the Pleistocene and Holocene, with records found in Argentina (Pardiñas et al. 2002; Pardiñas and Teta 2012; Quintana 2016), Paraguay (Torres et al. 2015), Uruguay (Ubilla 1996), Ecuador (Fejfar et al. 1993) and Brazil (Castro and Langer 2011; Hadler et al. 2016; Stutz et al. 2017 2018; Roth 2018). Among these records, A. clivigenis was described based on a single specimen collected by the naturalist Peter Wilhelm Lund in the 19th century from Quaternary deposits of Lagoa Santa, Minas Gerais (Winge 1887), and became the only species of Akodon from Brazil known exclusively from past material. In Brazil, at least five Akodon taxa were identified in different suband fossiliferous sites across the country, from Late Pleistocene to Holocene, all in caves and rock shelters (Table 1). Sites in the Cerrado biome include records of A. clivigenis and A. cursor from Lagoa Santa, Minas Gerais (Winge 1887); Akodon cf. lindberghi from Gruta dos Moura, Tocantins (Tobelém et al. 2013); Akodon sp.1 and Akodon sp.2 from Gruta do Urso, Tocantins (Pires et al. 2018); Akodon sp.1 and Akodon sp.2 from Caverna Carneiro, Goiás (Boroni 2019); and Akodon sp. from Caverna Nossa Senhora Aparecida, Serra da Bodoquena, Mato Grosso do Sul (Salles et al. 2006; Boroni et al. 2020). Caverna Nossa Senhora Aparecida (NSA cave) is located in Serra da Bodoquena, a mountainous region in western Brazilian Cerrado, characterized by a vegetation Table 1. Akodon species with fossil records at different fossiliferous sites in Brazil. Adapted from Boroni (2019). YBP = years before present Taxon Locality Reference Date interval Akodon clivigenis Lagoa Santa - MG Winge (1887) Akodon cursor Lagoa Santa - MG Winge (1887) Akodon azarae Sangão site - RS Roth (2018) Present to 6.285 YBP Deobaldino Marques site - RS Roth (2018) Present to 6.285 YBP Akodon cf. azarae Adelar Pilger site - RS Hadler et al. (2016) 3.000 to 8.010 YBP Sangão site - RS Stutz et al. (2018) 3.730 to 8.800 YBP Akodon cf. lindberghi Gruta dos Moura cave - TO Tobelém et al. (2013) Akodon cf. cursor Toca da Barra da Janela do Antonião cave - PI Guérin et al. (1996) Akodon sp. Igrejinha cave - GO Salles et al. (1999) Akodon sp. Carneiro cave - GO Boroni (2019) Present to 2.500 YBP Present to 13.300 YBP 13.300 to 121.500 YBP Akodon sp. Abismo Iguatemi site - SP Castro and Langer (2011) 10.000 to 14.000 YBP Akodon sp. Adelar Pilger site - RS Hadler et al. (2016) Present to 3.000 YBP 3.000 to 6.150 YBP Akodon sp. Afonso Garivaldino Rodrigues site - RS Stutz et al. (2017) 7.250 to 9.430 YBP Akodon sp. Sangão site - RS Stutz et al. (2018) 3.730 to 8.800 YBP Akodon sp. Sangão site - RS Roth (2018) Present to 6.285 YBP Akodon sp. Deobaldino Marques site - RS Roth (2018) Present to 6.285 YBP Akodon sp. Gruta do Urso cave - TO Pires et al. (2018) 3.800 to 22.000 YBP Akodon sp. Nossa Senhora Aparecida cave - MS Boroni et al. (2020) page 2 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan mosaic, including grasslands, shrublands, marshlands, and semideciduous and deciduous forests (Eiten 1972; RADAMBRASIL 1982). Serra da Bodoquena is located in a karstic area with significant cave density, consisting of pure dolostones and limestones of the Corumbá Group (Ediacaran age) that, during the formation of Gondwana, were partially deformed in the Paraguay Mobile Belt (Alvarenga et al. 2009; Campanha et al. 2011). Due to these characteristics, the region allowed expressive fossilization of Quaternary mammals, from megafauna such as giant ground sloths, saber tooth cats, and others, to small sigmodontine rodents, including records of Akodon sp. (Salles et al. 2006; Perini et al. 2009 2011; Boroni et al. 2020). The specimens of Akodon sp. were initially recorded by Salles et al. (2006), and later accessed by Boroni et al. (2020) in order to provide further comparisons to congeners (A. lindberghi and A. montensis), but no precise identification could be retrieved. The description of a new species of Akodon from Serra da Bodoquena, naturally prompted Brandão et al. (2021) to provide a few comments on the nearly topotypical Akodon sp., but these authors were not able to reach a conclusion of their identity without a proper evaluation of the specimens. Here, we evaluate the specimens from NSA cave and compare them with the three species of Akodon that currently occur in Mato Grosso do Sul, A. kadiweu, A. montensis and A. toba (Pardiñas et al. 2015; Brandão et al. 2021), since the Holocene and Pleistocene cave fauna from Brazil are represented by a mosaic of living and extinct species inhabiting the region. We also included comparisons with other recent congeners from nearby regions, as well as with Akodon clivigenis, the only extinct Akodon representative occurring in the Cerrado, in order to propose a hypothesis for the taxonomic identification of this material at the species level. MATERIALS AND METHODS We examined a total of 96 specimens of extant species of Akodon known to occur in Mato Grosso do Sul (A. kadiweu, A. montensis and A. toba) and the nearby lowlands of Chaco in Paraguay, Cerrado in central and western Brazil, and the natural grasslands in northern Argentina (A. azarae, A. lindberghi, and A. philipmyersi, respectively). From the cave deposit assemblage of NSA cave, a total of 33 cranial remains of Akodon sp. (sensu Boroni et al. 2020) were examined. Four NSA cave specimens were measured, photographed and then sent for radio-carbon dating (Boroni et al. 2020), so they do not have voucher numbers. We refer to the past samples from Serra da Bodoquena as NSA cave Akodon sp. from hereafter. The specimens examined (Table S1) are deposited in the following mammal collections: Brazil: Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais; Museu Nacional (MN), Universidade Federal do Rio de Janeiro, Rio de Janeiro; Museu de Zoologia da Universidade de São Paulo (MZUSP), São Paulo; Argentina: Colección de Mamíferos del Centro Nacional Patagónico (CNP), Puerto Madryn, Chubut; and U.S.A.: National Museum of Natural History (USNM), Washington, D.C; Field Museum of Natural History (FMNH), Chicago; University of Michigan Museum of Zoology (UMMZ), Ann Arbor. We examined high resolution digital pictures from the specimen of Habrothrix clivigenis (= Akodon clivigenis) deposited in the Zoological Museum, Natural History Museum of Denmark (ZMUC), Copenhagen, Denmark (also see Hansen 2012). See table S1 for the complete list of specimens and localities. We compared the following cranial qualitative morphological characters among these species: nasal, interorbital region, supraorbital margins, zygomatic notches, zygomatic plate, incisive foramina, mesopterygoid fossa, mandible and molars. The craniodental nomenclature and descriptions follow Reig (1977), Voss (1988), Myers (1990) and Weskler (2006). We classified specimens in five age-classes based on the pattern of tooth wear established by Myers (1990). For morphometric analyses, we used seven craniodental measurements, taken with digital calipers to the nearest 0.01 mm following the definitions of Myers (1990), Percequillo et al. (2017), Boroni et al. (2020): Least interorbital breadth (LIB), representing the least distance across the frontal bones; Length of upper molars (LM), from the anterior surface of M1 to posterior margin of M3; Breadth of zygomatic plate (BZP), measured across the central area of zygomatic plate; Breadth of first upper molar (BM1), greatest crown breadth of the M1 across the paracone-protocone; Length of lower molars (lm), from the anterior surface of m1 to posterior margin of m3; Breadth of first lower molar (bm1), greatest crown breadth of the m1 across the paracone-metacone; Greatest mandible length (GML), from the most anterior point of the mandible to the posterior point of the mandible (at the condyloid process in Akodon). Descriptive univariate statistics (mean ± standard deviation, range, and sample size) are provided for all craniodental measurements of adults. As our sample of A. kadiweu is small, for each species we pooled specimens from all age classes (2 to 5) available for study. To explore the morphometric variation among specimens of Akodon, we used Principal component analysis (PCA) and Discriminant function analysis page 3 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan (DFA) with extracted variance-covariance matrix of log10-transformed metric characters of skull and mandible, separately. We also use biplot and boxplot graphs using absolute values to determine size categories based on the dispersion values and to compare samples. All statistical analyses were performed in the software SPSS Statistics 19.0 (SPSS Inc. 2008). RESULTS Morphological variation The best-preserved cranial remains of specimens of NSA cave Akodon sp. are represented by upper and lower molars, either in individual maxillae (N = 9), mandible (N = 23), or partial skull (N = 1). The morphometric comparisons of these cranial structures were useful to discriminate species of the genus Akodon. The length of the upper molar series (LM; Table 2) of A. toba are the largest, followed by those of A. montensis, A. kadiweu, A. azarae, NSA cave Akodon sp., A. philipmyersi, and A. lindberghi, that exhibits the smallest molar series. Likewise, the length of the lower molar series (lm) decreases in size from A. toba, A. montensis, A. kadiweu, A. azarae, NSA cave Akodon sp., A. philipmyersi, to A. lindberghi. The same pattern of size variation is observed in relation to the breadth of first upper (BM1) and lower molars (bm1; Table 2). The biplot of dental characters (Fig. 1) reveals that specimens of A. toba exhibit long and wide molars, Table 2. Descriptive statistics (mean ± SD; range and sample size - N) for craniodental measurements (in millimeters) of adults of Akodon sp. from Nossa Senhora Aparecida (NSA) cave, Serra da Bodoquena, Mato Grosso do Sul, Brazil, and geographically close congeners Akodon azarae Akodon kadiweu Akodon lindberghi Akodon montensis LIB 4.29 ± 0.09 4.23–4.40 (3) 5.09 ± 0.07 5.04–5.18 (3) 4.52 ± 0.19 4.22–4.82 (10) 4.94 ± 0.18 4.68–5.47 (19) BZP 2.19 ± 0.04 2.14–2.23 (3) 2.28 ± 0.28 2.00–2.56 (3) 1.83 ± 0.11 1.66–2.06 (10) 2.52 ± 0.14 2.23–2.73 (19) LM 4.13 ± 0.41 4.10–4.18 (3) 4.42 ± 0.07 4.33–4.47 (3) 3.74 ± 0.13 3.54–4.02 (10) 4.18 ± 0.14 3.96–4.65 (19) BM1 1.12 ± 0.06 1.08–1.20 (3) 1.17 ± 0.05 1.12–1.21 (3) 1.07 ± 0.03 1.03–1.17 (10) 1.23 ± 0.05 1.11–1.34 (19) lm 4.30 ± 0.06 4.23–4.36 (3) 4.46 ± 0.12 4.37–4.60 (3) 3.86 ± 0.13 3.62–4.06 (10) 4.39 ± 0.16 4.02–4.64 (19) bm1 1.03 ± 0.05 0.97–1.09 (3) 1.12 ± 0.02 1.10–1.14 (3) 0.91 ± 0.08 0.72–1.02 (10) 1.04 ± 0.06 0.90–1.15 (19) GML 13.37 ± 0.52 12.80–13.83 (3) 14.13 ± 1.12 13.48–15.43 (3) 11.73 ± 0.38 11.32–12.64 (10) 14.98 ± 0.55 13.79–16.15 (19) Akodon philipmyersi NSA cave Akodon sp. Akodon toba LIB 4.52 ± 0.14 4.3–4.72 (11) 4.38 (1) 4.98 ± 0.13 4.79–5.09 (4) BZP 2.01 ± 0.09 1.93–2.14 (11) 1.97 ± 0.13 1.75–2.22 (8) 2.95 ± 0.27 2.34–2.96 (4) LM 3.95 ± 0.11 3.78–4.10 (11) 4.05 ± 0.20 3.91–4.20 (2) 4.80 ± 0.13 4.67–4.99 (4) BM1 1.13 ± 0.06 1.05–1.21 (11) 1.14 ± 0.07 1.05–1.28 (10) 1.28 ± 0.03 1.25–1.34 (4) lm 4.00 ± 0.11 3.78–4.14 (11) 4.16 ± 0.12 3.91–4.35 (9) 4.97 ± 0.23 4.76–5.28 (4) bm1 1.10 ± 0.10 0.92–1.21 (11) 1.01 ± 0.05 0.89–1.15 (23) 1.11 ± 0.03 1.08–1.15 (4) GML 11.57 ± 0.17 11.30–11.9 (11) 11.57 ± 1.13 9.31–12.62 (9) 15.27 ± 1.02 14.15–16.51 (4) page 4 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan Fig. 1. Biplot graph displaying the length of upper molars (LM) versus the breadth (BM1) of M1, and length of lower molars (lm) versus breadth (bm1) of m1 of seven species of Akodon showing the different size categories. page 5 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan versus small and narrow molars of most specimens of A. lindberghi. The remaining specimens exhibit an intermediate condition, with most specimens of A. montensis and A. kadiweu presenting larger molars than A. philipmyersi, A. azarae and NSA cave Akodon sp., with the latter slightly overlapping with these intermediate-size species. The cranial measurements based on the skull and mandible fragments of NSA cave Akodon sp., such as the breadth of zygomatic plate and least interorbital constriction, and length of mandible, also follow a similar size pattern among the species studied (Table 2). The breadth of zygomatic plate (BZP) is smallest in A. lindberghi, followed by A. philipmyersi, NSA cave Akodon sp., A. azarae, A. kadiweu, A. montensis and A. toba, with the last two referring to the largests species. The least interorbital breadth (LIB) is narrower in A. azarae, followed by NSA cave Akodon sp., A. lindberghi, A. philipmyersi, A. kadiweu, A. montensis and A. toba. Although the range of variation in the length of mandible is higher in NSA cave Akodon sp. (9.31–12.62 mm), its mean is equal to A. philipmyersi (11.57 mm) and only slightly smaller than A. lindberghi (11.73 mm). Thus, the length of mandible is smaller in A. philipmyersi, A. lindberghi and NSA cave Akodon sp., followed by A. azarae, A. kadiweu, A. montensis and A. toba (Table 2). The boxplot of cranial (Fig. 2) and mandible (Fig. 3) characters reveals the pattern of variation among specimens, with specimens of A. toba and A. lindberghi being the largest and smallest species, respectively, while other species are intermediate in size. We found some variables that distinguish some species from the others: low values of LIB for A. azarae; high values of LM and lm for A. toba; and low values of GML for A. lindberghi, A. philipmyersi, and NSA cave Akodon sp. The first two principal components together summarized 94.9% and 93.47% of the total variation in the PCA of the skull and mandible, respectively (Fig. 4). All morphometric characters are positively correlated Fig. 2. Boxplots of the ratio of cranial measurements of seven species of Akodon. Outliers are represented by dots. Variables are defined in the text. page 6 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan with PC1, which reflects size (Voss and Marcus 1992) and accounted for 86.51 and 68.72% of the variation of the skull and mandible, respectively. The scatterplots between PC1 versus PC2 show partial segregation among samples, with two species almost entirely isolated from the others: A. lindberghi and A. toba, the smallest and largest species. The remaining taxa are intermediate in size, with NSA cave Akodon sp. slightly overlapping with all species, except A. montensis. PC2, which accounted for 8.39 and 24.75% of the variation of the skull and mandible, respectively, revealed a similar pattern of separation among groups. Akodon lindberghi and A. toba are the most distinctive species in size and shape of the skull as shown by the results of PC1 and PC2, respectively (Fig. 4). The dispersal of individual scores of principal components is quite similar to the dispersion of specimens on the univariate scatterplots, with A. lindberghi and A. toba representing the extremes of variation. The DFA indicates that the first two canonical variables (DF1 and DF2) from the cranial variation were responsible for 78.54% and 13.55% of the total variance, respectively, which together compose 92.09% of the total variation (Fig. 5). The canonical correlation showed moderate association between DF1 and the pre-defined groups of the analysis, revealing that this function discriminated the groups in a similar way as depicted by the PCA analysis and the univariate scatterplots: the smallest and largest species (A. lindberghi and A. toba, respectively) segregated in relation to the remaining taxa of intermediate size. One interesting piece of data of the DFA concerns the predicted classification, which reveals that a total of 66.1% of the specimens were correctly classified and 33.9% were not, including NSA cave Akodon sp. identified as A. kadiweu, A. philipmyersi or A. azarae (11%, 22% and 11%, respectively) but never as A. lindberghi, A. montensis or A. toba (Table 3). Qualitative cranial characters can also be used to distinguish species. The dorsal view of the skull reveals differences in three characters: nasal, zygomatic notches and interorbital region (Fig. 6). The nasals of A. kadiweu, A. lindberghi and A. philipmyersi present notably curved margins that acuminate posteriorly (U-shaped in A. philipmyersi and V-shaped in the other species), when compared to sub-parallel straighter margins of A. montensis (V-shaped posteriorly) and A. toba (V-shaped or squared posteriorly), and the slightly curved margins of A. azarae (somewhat squared posteriorly). Moreover, the nasals of A. philipmyersi are moderate in length, as well as the ones from A. azarae and A. toba (extending slightly beyond premaxillaefrontal suture), when compared to the longer nasals of A. kadiweu, A. montensis, and A. lindberghi (extending well beyond premaxillae-frontal suture). Although the anterior portion of rostrum and the nasals are broken in NSA cave Akodon sp. specimen (MN 58086), the shape and extension of the suture between nasals and premaxillae-frontal are similar to those found in A. kadiweu and A. lindberghi. The zygomatic notch is Fig. 3. Boxplots of the ratio of mandible measurements of seven species of Akodon. Outliers are represented by dots. Variables are defined in the text. page 7 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan notably deep in A. toba and shallow in A. kadiweu and A. lindberghi, while A. azarae, A. philipmyersi and A. montensis exhibit an intermediate condition (i.e., neither deep or shallow). Although the zygomatic notches of the NSA cave Akodon sp. specimen (MN 58086) are filled with sediment, it is possible to see that they are as shallow as in A. kadiweu and A. lindberghi. Although the interorbital region is hourglass shaped in all species, including those of NSA cave Akodon sp., the interorbital constriction is more pronounced in A. montensis and A. toba when compared to the other species, in which lateral margins of the supraorbital region are much less curved, and the interorbital constriction is less evident. Moreover, only the supraorbital margins of A. toba are distinctly sharp, contrary to the smoother margins of the other taxa. In the ventral view of the skull some important diagnostic features can also be observed (Fig. 7). The posterior margins of incisive foramina reach the protoflexus or anterior portion of protocone level of M1 in A. kadiweu, and the mid or posterior portion of the protocone in A. montensis and A. toba, while in A. azarae, A. philipmyersi and A. lindberghi they reach the hypoflexus level (or, in a few specimens, slightly anterior in A. philipmyersi, or slightly posterior in A. lindberghi). The incisive foramina and the majority of Fig. 4. Distribution of the factorial scores in the first (PC1) and second principal (PC2) components of log-transformed craniometric variables of skull (above) and mandible (below) of adult specimens of Akodon. page 8 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan the palatal region of the preserved skull of the NSA cave Akodon sp. specimen (MN 58086) is encrusted with sediment. However, a partially clean (without sediment) portion of the palate of this specimen is aligned with the anterior portion of protocone of M1, with no trace of the incisive foramina. Thus, the posterior margins of the incisive foramina of the preserved skull of NSA cave Akodon sp. (MN 58086) is probably located anteriorly Fig. 5. Distribution of the factorial scores in the first (DF1) and second (DF2) canonical variates of the discriminant function analysis (DFA) of log-transformed craniometric variables of the skull of adult specimens of Akodon. The DFA could not be performed using the data of mandibles separately due to the low number of measurements. Table 3. Classification matrix for Akodon spp. obtained by discriminant function analysis concerning the probabilities of classifying each species correctly into one of the seven species Predicted classification results (%) * Species A. azarae A. kadiweu A. lindberghi A. montensis A. azarae 100% A. kadiweu 33% 33% A. lindberghi 70% A. montensis 89% A. philipmyersi 9% 27% Akodon sp. 11% 11% A. toba Predicted classification results (%) * Species A. philipmyersi Akodon sp. A. toba Total A. azarae 100% A. kadiweu 33% 100% A. lindberghi 20% 10% 100% A. montensis 5% 5% 100% A. philipmyersi 18% 45% 100% Akodon sp. 22% 56% 100% A. toba 100% 100% * A total of 66.1% of the specimens were correctly classified. page 9 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan Thus, effort should be made in the future to investigate this issue after larger series of specimens of past and recent series of A. kadiweu are available in scientific collections. In NSA cave, specimens of Akodon kadiweu were found from the stratigraphic units (S.U.) 2, 4 and 7, but no date estimates are available for these stratigraphic profiles (see Boroni et al. 2020). The specimens from S.U. 7 are from the surface of the cave floor and suggest a recent presence of the genus in NSA area, along with typical Sigmodontinae of the Cerrado biome, as Necromys lasiurus, Thalpomys lasiotis, Calomys tener, Fig. 10. Range distribution of extant and fossil species of Akodon in Brazil and Paraguay. Localities: 1 – Fazenda Califórnia, Parque Nacional da Serra da Bodoquena (Brandão et al. 2021); 2 – Nossa Senhora Aparecida cave, Serra da Bodoquena (Boroni et al. 2020); 3 – Carneiro cave (Boroni 2019); 4 – Igrejinha cave (Salles et al. 1999); 5 – Gruta dos Moura cave (Tobelém et al. 2013); 6 – Gruta do Urso cave (Pires et al. 2018); 7 – Toca da Barra da Janela do Antonião cave (Guérin et al. 1996); 8 – Lagoa Santa (Winge 1887); 9 – Abismo Iguatemi site (Castro and Langer 2011); 10 – Garivaldino site (Stutz et al. 2017); 11 – Adelar Pilger site (Hadler et al. 2016); 12 – Deobaldino Marques site (Roth 2018); 13 – Sangão site (Stutz et al. 2018); 14 – Risso Cave, Paraguay (Torres et al. 2015). Also see table 1. Gray area was based on the geographic range of the extant species of genus Akodon according to Pardiñas et al. (2015). N page 16 of 19Zoological Studies 61:78 (2022) © 2022 Academia Sinica, Taiwan Cerradomys and Pseudoryzomys simplex. Along with A. kadiweu, other open-habitat sigmodontines were also recorded in deeper strata S.U. 4 and 2, such as Kunsia tomentosus, Wiedomys sp. and Graomys cf. chacoensis. Studies on past assemblages of Sigmodontinae rodents show high diversity during the Holocene and Late Pleistocene, followed by pronounced changes in abundance and geographic range, with extinction occurring well into recent times (e.g., Winge 1887; Voss and Myers 1991; Pardiñas et al. 2002; Pardiñas and Teta 2011 2013; Pires et al. 2018; Boroni 2019; Neves et al. 2020). These community shifts are associated with the environmental alterations especially during glacial and interglacial periods, leading to retraction and expansion of forested and open areas during the Pleistocene and Holocene epochs (Cartelle 1999; Bueno et al. 2016). For instance, the Quaternary mammalian fauna recorded in Serra da Bodoquena suggests different conditions in the past than nowadays, characterized by open vegetation formations with flooded areas (Salles et al. 2006; Boroni et al. 2020). In Risso Cave, Paraguay, the fossiliferous site closest to our sample, approximately 180 km southwest of NSA cave, Quaternary remains also corroborate this paleoenvironmental scenario, including remains of species of Sigmodontinae, such as Akodon cf. toba and Holochilus chacarius, species typical of open and flooded vegetation (Torres et al. 2015). The genera recovered in the deeper stratigraphic layers (i.e., Kunsia, Wiedomys and Graomys) do not currently occur in Serra da Bodoquena, suggesting regional extinctions for some species over the Quaternary in this region, as their preferred habitat become unavailable with landscape changes over time. CONCLUSION A few past records of Akodon from Brazil have been identified to species level, such as A. clivigenis and A. cursor from Lagoa Santa (Winge 1887; Paula-Couto 1950). Here, we provided the taxonomic identity of A. kadiweu, a past representative of Akodon from Serra da Bodoquena, which helps us understand the evolutionary history of this genus in South America, and at the same time increase our knowledge of this recently described and poorly known taxon, currently restricted to a limited portion of western Brazil. Acknowledgments: We thank the curators and staff that generously granted us access to the collections under their care: U.F.J. Pardiñas (CNP); J.A. Oliveira and M. Weksler (MN); D. Lunde (USNM); A. Ferguson and B. Patterson (FMNH); C. Thompson and P. Myers (UMMZ); and J.G. Barros, L.F. Silveira, and M. Vivo (MZUSP). We also thank Kapser Lykke Hansen for valuable data on the specimen of Akodon clivigenis; James L. Patton and P. Myers for their kindness and generosity for sharing data about Akodon; and the editor and reviewers for valuable suggestions that improved the manuscript. This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP #2000/06642-4 to APC, #2019/05374-2 to MVB, #2009/16009-1 and #2016/20055-2 and #2020/114440 to ARP); Science Visiting Scholarship (FMNH); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Finance Code 001, to NLB); and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq # 304156/2019-1 to ARP). Authors’ contributions: MVB, NLB, APC, FAP, LOS and ARP designed the study. MVB, NLB, APC, FAP, and LOS performed the sampling collections. MVB and NLB collected and analyzed the data and prepared illustrations. MVB, NLB, APC, FAP, LOS and ARP prepared the manuscript. All authors approved the final version of the manuscript. Competing interests: The authors declare that they have no conflicts of interest. 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Abbreviations: CNP, Colección de Mamíferos del Centro Nacional Patagónico; MN, Museu Nacional, Universidade Federal do Rio de Janeiro; MZUSP, Museu de Zoologia da Universidade de São Paulo; UFMG, Universidade Federal de Minas Gerais; UMMZ, University of Michigan Museum of Zoology; USNM, National Museum of Natural History; FMNH, Field Museum of Natural History. (download) page 19 of 19Zoological Studies 61:78 (2022)