Research Article
Print
Research Article
New species of the Spiny Mouse genus Neacomys (Cricetidae, Sigmodontinae) from northwestern Ecuador
expand article infoNicolás Tinoco‡§|, Claudia Koch, Javier E. Colmenares-Pinzón#¤, Francisco X. Castellanos|¤, Jorge Brito|
‡ Pontificia Universidad Católica del Ecuador, Quito, Ecuador
§ Fundación Great Leaf, Quito, Ecuador
| Instituto Nacional de Biodiversidad (INABIO), Quito, Ecuador
¶ Leibniz Institute for the Analysis of Biodiversity Change/Museum Koenig, Bonn, Germany
# Universidad Industrial de Santander, Bucaramanga, Colombia
¤ Texas Tech University, Lubbock, United States of America

Corresponding author: Jorge Brito ( jorgeyakuma@yahoo.es )

Academic editor: Nilton Cáceres
© 2023 Nicolás Tinoco, Claudia Koch, Javier E. Colmenares-Pinzón, Francisco X. Castellanos, Jorge Brito.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Tinoco N, Koch C, Colmenares-Pinzón JE, Castellanos FX, Brito J (2023) New species of the Spiny Mouse genus Neacomys (Cricetidae, Sigmodontinae) from northwestern Ecuador. ZooKeys 1175: 187-221. https://doi.org/10.3897/zookeys.1175.106113
ZooBank: urn:lsid:zoobank.org:pub:44FB328A-081D-4232-AC75-C879C74A7D0B
Open Access

Abstract

Neacomys is a genus of small spiny or bristly sigmodontine rodents that are common components of mammalian faunas in multiple biomes on Central and South America. Recent studies on this group have demonstrated that there is cryptic diversity yet to be discovered within currently recognized species that have not received comprehensive revisions, as well as in areas that have been overlooked. Here we ratify this assertion by describing a new species previously misidentified as the Narrow-footed Spiny Mouse (Neacomys tenuipes) from the Chocó biogeographic region in northwestern Ecuador, Neacomys marci Brito & Tinoco, sp. nov. Distinctiveness of this entity is supported by the combination of the following morphological characters: small size (head-body length 65–85 mm); long tail (69–126% longer than head-body length); pale buff-colored but gray-based belly fur; white throat; hypothenar pad usually absent; long nasals; and a condylar process higher than the coronoid process. Likewise genetic distance analyses and phylogenetic reconstructions based on cytochrome-b (Cytb) sequence data indicate a clear divergence from typical populations of N. tenuipes, and a sister relationship between them. The results presented here increase the diversity of Neacomys to 24 species, placing it among the most diverse genera within the sigmodontine rodents.

Key words

Chocó biogeographic, Neacomys tenuipes, premontane forest

Introduction

Neacomys is a widely distributed genus of small spiny or bristly rodents that collectively occupy representative regions and habitats in easternmost Panama and the northern half of South America (Patton et al. 2015; Pardiñas et al. 2017; Caccavo and Weksler 2021; Semedo et al. 2021). Currently, 23 species are recognized within this group, occurring its highest concentration in the rainforests of the Amazon region (Hurtado and Pacheco 2017; Semedo et al. 2020, 2021; Brito et al. 2021a; Caccavo and Weksler 2021).

From the years 2017 through 2021, taxonomy of Neacomys has been remarkably dynamic and has resulted in the description of 11 species (Hurtado and Pacheco 2017; Sanchez-Vendizú et al. 2018; Semedo et al. 2020, 2021; Brito et al. 2021a; Caccavo and Weksler 2021; Colmenares-Pinzon 2021). The progress in the understanding of its diversity has been mainly achieved thanks to the exhaustive revision of material deposited in museum collections (Semedo et al. 2020, 2021; Caccavo and Weksler 2021), as well as increased collection efforts and implementation of molecular analyses (Brito et al. 2021a; Colmenares-Pinzon 2021). However, as there are still many unexplored areas in the heterogenous geography of South America and adjacent Central America (Panama), some of the currently recognized species have not undergone comprehensive taxonomic evaluations, and it is possible that the real diversity of the genus is underestimated.

The Chocó Biogeographic region is considered one of the most diverse hotspots in South America (Myers et al. 2000), yet one of the least studied regions for Neacomys despite its large extension (along the Pacific coasts of Panama, Colombia, and Ecuador). To date, only two species are known to occur in the Chocó, the Painted Bristly Mouse N. pictus, and the Narrow-footed Spiny Mouse N. tenuipes (Patton et al. 2015; Pardiñas et al. 2017). The former has been recorded from one locality in Panama (Goldman 1912), and is scarcely represented in museums, by fewer than 12 specimens collected more than 30 years ago (VertNet Database): the presence of N. tenuipes is supported by only three specimens from two localities in Colombia (Colmenares-Pinzon 2021), and by an unclear number of specimens from at least four localities in Ecuador (Jarrín 2001; Brito et al. 2021a). Poor knowledge about the distribution of Neacomys throughout the Chocó region is accompanied by a lack of genetic characterization. This has prevented the inclusion of N. pictus in phylogenetic analyses of the genus, and thus there are no clues about its relationship with respect to other species. In the case of the populations from the department of Cauca, Colombia, and those from Ecuador, this has precluded the possibility of addressing their degree of differentiation from typical N. tenuipes, or even determine if they represent different species as some authors have hypothesized [e.g., the first one has been treated as N. pusillus Allen, 1912 (Caccavo and Weksler 2021) whereas the second was treated as N. pictus Goldman, 1912 (Jarrín 2001)]. The uncertainty about the affinity of some populations to N. tenuipes illustrates a possible cause of an underestimated diversity within the genus, where some of the currently recognized species have not been reviewed in detail.

With the recent collections of several specimens resembling Neacomys tenuipes in previously unexplored areas of northwestern Ecuador, their genetic and morphological characterization, and their comparison with material from different museums, this work describing a new species constitutes a forward step towards a better understanding of the variation within what has been considered a widely distributed and homogeneous species, as well as of the real diversity of the genus in the Chocó biogeographic region.

Materials and methods

Specimens

Specimens of Neacomys from northwestern Ecuador reviewed here were mostly obtained from field expeditions conducted by JB and his team to two protected areas. Reserva Dracula was sampled during three consecutive nights in November 2016, January 2017, and July 2017, respectively, using 10–12 pitfall traps (20–60 liters), which yielded an effort of 430 traps/night. On the other hand, Reserva Canandé was also surveyed with 20 pitfall traps, and with 100 standard Sherman traps (7.5 × 9 × 27 cm) during four consecutive nights in November 2020, and during six nights in October 2022. Capture effort with the Sherman traps was 1,030 traps/night. In all three cases, all traps were placed near runways, holes, and other signs of small mammal activity, and baited with rolled oats mixed with vanilla and alternating with concentrates cattle feed (Voss et al. 2001; Brito et al. 2020). All activities related to the handling and collection of specimens were conducted according to the protocols approved by the American Society of Mammalogists (Sikes et al. 2016). Research permits were issued by the Ecuadorian Ministry of Environment (MAE-DNB-CM-2019-0126, MAAE-ARSFC-2020-0642, and MAATE-ARSFC-2022-2583).

Mounted dry skins, skeletons, fluid-preserved bodies, and tissue samples stored in 96% ethanol were deposited in the biological collections of the Instituto Nacional de Biodiversidad (INABIO; Quito, Ecuador). Initially, specimens from both reserves were identified as Neacomys tenuipes based on discrete morphological characters. Further comparisons were carried out between these specimens and additional material of the genus deposited in local and international mammal collections: Museo de la Escuela Politécnica Nacional (MEPN, Quito, Ecuador); Museo de Zoología de la Pontificia Universidad Católica del Ecuador (QCAZ, Quito, Ecuador); Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IAvH-M, Bogotá, Colombia); Museo de Historia Natural de la Universidad Industrial de Santander (UIS-MHN-M, Santander, Colombia); Museo de Historia Natural de la Universidad de Caldas (MHN-UCa-M, Caldas, Colombia) and Instituto Nacional de Biodiversidad (MECN, Quito, Ecuador). All studied material is listed in Appendix 1.

Morphological qualitative and quantitative comparisons

For the craniodental morphological comparisons the terminology follows Patton et al. (2000), Voss et al. (2001), Hurtado and Pacheco (2017), Sánchez-Vendizú et al. (2018), Semedo et al. (2020), and Caccavo and Weksler (2021). The soft anatomy was reviewed considering the concepts in Carleton (1973) and Pardiñas et al. (2020).

A detailed structural scrutiny of the skull of one specimen (MECN 6232; Estación Fisher, Ecuador) was done using a high-resolution micro-computed tomography (micro-CT) desktop scanner device (Bruker SkyScan 1173, Kontich, Belgium) at the Leibniz Institute for the Analysis of Biodiversity Change/Museum Koenig (LIB, Bonn, Germany). To avoid movements during the scanning process, the material was placed in a small plastic container embedded in cotton wool. Acquisition parameters comprised: an X-ray beam (source voltage 43 kV and current 116 μA) without the use of a filter; 960 projections of 500 ms exposure time each with a frame averaging of 4 recorded over 180° using rotation steps of 0.25 degrees, resulting in a scan duration of 55 min 28 s; a magnification setup generating data with an isotropic voxel size of 12.07 μm. The CT-dataset was reconstructed with N-Recon software (Bruker MicroCT, Kontich, Belgium) and rendered in three dimensions using CTVox for Windows 64 bits v. 2.6 (Bruker MicroCT, Kontich, Belgium).

All specimens were classified into five age classes defined by Semedo et al. (2020) and Caccavo and Weksler (2021) based on the level of eruption of the third molar and the wear of the occlusal surface of the molars. Only specimens between ages 3 and 6 were used in the quantitative morphological comparisons.

For these comparisons, a total of four external and 19 craniodental measurements were considered according to: Carleton and Musser (1989); Patton et al. (2000); Voss et al. (2001); Hurtado and Pacheco (2017); Sánchez-Vendizú et al. (2018); Semedo et al. (2020); Brito et al. (2021a). Four body measurements: head and body length (HBL); tail length (TL); hind foot length (HF); ear height (E); and body mass (w, in grams, g); condyloincisive length (CIL); length of incisive foramina (LIF); breadth of incisive foramina (BIF); length of upper diastema (LD); crown length of maxillary toothrow (LM); alveolar width (AW); breadth of palatal bridge (BPB); length of rostrum (LR); length nasal (LN); rostral width (RW-2); least interorbital breadth (LIB); orbital length (OL); breadth of zygomatic plate (BZP); zygomatic breadth (ZB); braincase breadth (BB); occipital condyle breadth (OCB); basioccipital length (BOL); cranial depth (CD); breadth of the first upper molar (BM1).

We recorded external measurements from tags, and for the craniodental measurements we used digital calipers to the nearest 0.01 mm in all presumed specimens of N. tenuipes recently collected in northwestern Ecuador. We also measured older specimens of the species and other members of the genus housed in museums in Colombia and Ecuador (see above).

The craniodental measurements from 108 specimens tentatively identified as N. tenuipes, N. cf. pictus, and N. rosalindae Sánchez-Vendizú, Pacheco & Vivas-Ruiz, 2018 were compiled in a matrix with 2,376 values. This dataset was analyzed in R v. 4.2.1 (R Core Team 2022) and inferred for missing values using the missMDA package (Josse and Husson 2016). The iterative PCA algorithm was preferred for this purpose with a maximum of 1,000 iterations and a 1e-6 threshold to assess convergence. The estimated number of components needed to predict the missing values were obtained by running 100 simulations with the leave-one-out cross-validation method. Morphological characters were checked for high degrees of correlation using Spearman’s coefficient, yet none were discarded since correlation values were ≤ 0.95. Non-parametric methods were preferred in all analyses (Šlenker et al. 2022).

Multivariate analyses performed in this study included Principal Component (PCA), and the K nearest neighbor classificatory Discriminant Analyses (KNN) with the MorphoTools2 package (Šlenker et al. 2022). For the latter, samples were grouped a priori as follows: 1) recently collected samples from northwestern Ecuador presumably belonging to N. tenuipes; 2) older museum specimens from northeastern Ecuador presumably belonging to N. cf. pictus; 3) typical N. tenuipes from Colombia; 4) N. rosalindae. To ensure that only invariant and non-linear characters were used in the KNN analysis, a stepwise discriminant analysis was conducted first and selected the following subset of characters: OL, LR, AW, BPB, CIL, HBL, LM, E, TL, LD, and ZB. Neacomys cf. pictus specimens were excluded because the total number of individuals (n = 2) was smaller than the total number of analyzed characters (Šlenker et al. 2022). The KNN results were plotted by centering and scaling the two variables that contributed the most to the discrimination of groups as predicted by the R2 and F-values of the stepwise analysis.

Individuals’ classification prediction was done using nine neighbors (k = 9) by estimating Euclidean distances through a cross-validation method. The precision of the classification was finally obtained as a percentage by comparing the model’s prediction to the a priori classification herein assigned.

Statistical tests for non-uniformly distributed data were calculated and plotted using the ggstatsplot package (Patil 2021), to verify for significant statistical differences in the variables inferred to exert a greater effect on taxon differences. A Kruskal-Wallis test was applied to determine if the groups’ medians were significantly different, followed by a Dunn test for a pairwise comparison of groups adjusting the p-value with the Holm method to control for the family-wise error rate (Holm 1979).

DNA extraction, amplification, and sequencing

DNA was extracted from muscle samples of the presumed specimens of N. tenuipes recently collected in northwestern Ecuador. The guanidine thiocinate protocol was used for DNA extraction (Bilton and Jaarola 1996). We amplified between 1000 and 1100 bases pair of mitochondrial gene Cytochrome b (Cytb); we used the forward primer MVZ05, and the reverse primers MVZ16H, MVZ14 (Smith and Patton 1993). The thermal profile for the amplification of Cytb included: an initial denaturation at 94 °C for 180 s, 35 cycles of denaturation at 94 °C for 45 s, primer annealing at 45 °C for 2 min, and the final elongation at 72 °C for 60s (Smith and Patton 1993; Bonvicino and Moreira 2001). The amplicons were sequenced at Macrogen Inc. in South Korea. The Cytb sequences were edited and assembled in the Geneious R11 program (https://www.geneious.com) and then verified to represent endogenous DNA of Neacomys by performing independent searches with the Basic Local Alignments Search Tool (BLAST) (Altschul et al. 1990).

Phylogenetic analyses

We tried to include representatives of the 23 known Neacomys species (Appendix 2), including some sequences from other genera of sigmodontine rodents that were used as outgroups (Appendix 2). The algorithm CLUSTAL-W was used for this purpose as implemented in Geneious R11. The ML tree was inferred using IQ-TREE (Nguyen et al. 2015). The BI analysis was conducted with MrBayes 3.2 (Ronquist et al. 2012), on the CIPRES Science Gateway platform (Miller et al. 2010), the analysis was carried out with two runs and four chains, were run for 10,000,000 generations, with a sampling every 1,000 generations and a burn-in of 0.25. Convergence was evaluated by the effective sample size (EES) and the potential scale reduction factor (PSRF). For most of the parameters the EES should be ≥ 200 and for the PSRF most of the values of the parameters should be between 1.0 and 1.2.

Genetic distances

We calculated an analysis of genetic divergence using an alignment restricted to the genus Neacomys obtained as described above. Uncorrected p-distances (intra and interspecific) were calculated with the MEGA X program (Kumar et al. 2018) and transformed to percentage values. The uncorrected p-distances were calculated in other works (Brito et al. 2021a; Colmenares-Pinzon; Semedo et al. 2020, 2021).

Results

Morphological qualitative and quantitative comparisons

Morphological qualitative revision and comparisons revealed that recently collected specimens and some older museum specimens from northwestern Ecuador are different from typical Neacomys tenuipes from Colombia in multiple discrete characters.

The two principal components of the PCA analysis explained 56.83% of the variation in the craniodental measurements, with CIL and RW-2 contributing to a greater extent to each one of them, respectively (Table 1). There was a clear overlap in the morphospace between recently collected samples from northwestern Ecuador and samples of the Rosalind’s bristly mouse, N. rosalindae. Older museum samples of N. cf. pictus, also from northwestern Ecuador, and typical samples of N. tenuipes from Colombia were recovered as two discrete groups (Fig. 1A). Likewise, typical N. tenuipes was completely discriminated in the KNN while recently collected samples (northwestern Ecuador) and N. rosalindae attained some degree of separation (Fig. 1B); the algorithm achieved accurate classification for samples from northwestern Ecuador, and N. rosalindae, with success rates of 91.3% and 95.8% respectively (Fig. 1B, Table 2).

Table 1.
Download as
CSV
XLSX

Results of the Principal Component Analysis (PCA). The overall contribution of each component is shown between parentheses, and the loadings with the highest absolute values in each component are bolded and displayed in rows. Character abbreviations are detailed in the text.

PC1 (42.59%) PC2 (14.24%)
HBL 0.1884563 0.113983562
TL 0.2082709 0.332087602
HF 0.2241264 0.201834179
E 0.1131424 0.207207965
CIL 0.3033246 -0.100529150
LIF 0.1912464 0.135697494
BIF 0.2025086 0.144585511
LD 0.2605398 -0.153473315
LM 0.2145628 0.119512958
AW 0.2830731 -0.049754832
BPB 0.1485273 -0.217453585
LR 0.1740795 0.138869902
LN 0.2325637 -0.007425074
RW-2 0.0203125 -0.517612008
LIB 0.2002134 -0.073239339
OL 0.1168325 -0.486171390
BZP 0.2230202 -0.171806332
ZB 0.2882257 -0.098729676
BB 0.2409027 -0.063978461
OCB 0.2474346 -0.078435817
BOL 0.2283143 -0.160505793
CD 0.1721603 -0.227526278
Table 2.
Download as
CSV
XLSX

Confusion matrix displaying the performance of the K nearest-neighbor classification for three Neacomys species. n represents the number of individuals used as input in the model. Values in “as species” columns represent the number of individuals assigned to each taxon, and the accuracy of the prediction is given as a percentage in the last column.

Taxon n as N. marci sp. nov. as N. rosalindae as N. tenuipes correct (%)
marci sp. nov. 23 21 2 0 91.30
rosalindae 62 1 61 0 95.08
tenuipes 21 0 0 21 100.00
Total 106 22 63 21 97.17
Figure 1. 

Morphometric and statistical analyses A scatterplots of the Principal Components B the K neighbor discriminant analyses. Each taxon is enclosed by a convex hull, and color codes are detailed in the legend C, D the distribution of the data is shown in a violin boxplot; the median of each taxon character is indicated with a black dot. Only statistically significant differences among taxa are shown with the p-adjusted Holm method (* p < 1e-3, ** p < 1e-4, *** p < 1e-9).

The characters chosen by the stepwise analysis as the greatest contributors to morphologic discrimination were OL (R2 = 0.96; F = 1287.68; p < 1e-15) and LR (R2 = 0.52; F = 55.21; p < 1e-15). The Kruskal-Wallis test revealed that the medians significantly differed across all groups (p < 1e-5), and the Dunn pairwise test proved that both characters were significantly different between all species with p-adjusted < 0.001 (Fig. 1C, D). These results constitute additional evidence supporting differentiation of the recently collected Ecuadorian specimens from typical specimens of N. tenuipes.

Genetic comparisons

Neacomys was recovered as a monophyletic group (BS: 100/ PP: 1.00; Fig. 2), with five nested subclades mostly congruent with the species groups mentioned by other authors (Hurtado and Pacheco 2017; Semedo et al. 2020; Brito et al. 2021a; Colmenares-Pinzon 2021). The inclusion of the Serrano Spiny Mouse, N. serranensis, and the Golden-belly Spiny Mouse N. auriventer to our phylogenetic analyses demonstrated that these morphologically and ecologically similar species are closely related, thus forming the novel “serranensis” group (Fig. 2). The ML analysis (Fig. 2) obtained the following relationship for the groups: “paracou” + [“spinosus” + {“serranensis” + (“dubosti” + “tenuipes”)}]. Relationships between species groups and between species in these groups were mostly consistent with previous phylogenetic hypotheses (Colmenares-Pinzon 2021; Brito et al. 2021a). The samples identified as Neacomys tenuipes from Ecuador and Colombia were grouped into two sister clades (Fig. 2), each clade presents high support Ecuador (100/1.00) and Colombia (86/0.86).

Figure 2. 

On the left is the Maximum Likelihood phylogenetic tree of the genus Neacomys based on the mitochondrial Cytb gene. On the right, Maximum Likelihood phylogenetic tree, extension of the “tenuipes” group. The numbers above the nodes represent the values of posterior (left) and bootstrap (right) probabilities. The * represents differences in the relationship found in the Bayesian Inference tree.

Calculated divergence between these two lineages was 4.35%±1.18% (Table 3), a value that is comparable with the divergences between well discrete species such as N. marajoara and N. xingu (4.0%), N. macedoruizi and N. aletheia (4.8%), N. vossi and N. xingu (5.4%), N. marajoara and N. vossi (5.5%), and N. macedoruizi and N. minutus (5.6%).

Table 3.
Download as
CSV
XLSX

Uncorrected genetic distances of species of the genus Neacomys formally described (21 species). We calculated the genetic distance based on the Cytochrome b gene. The values to the right of the diagonal are the standard deviation.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
1 N. serranensis 1.40 1.42 1.43 1.32 1.53 1.42 1.23 1.10 1.34 1.48 1.72 1.64 1.53 1.53 1.52 1.35 1.40 1.33 1.59 1.64
2 N. tenuipes 15.41 1.31 1.23 1.00 1.32 1.27 1.39 1.35 1.18 1.12 1.44 1.27 1.42 1.18 1.18 1.19 0.68 1.49 1.39 1.27
3 N. amoenus 14.25 13.80 0.47 1.50 1.74 1.46 1.35 1.31 1.56 1.07 1.11 1.25 1.41 1.40 1.40 1.43 1.30 1.42 1.27 1.32
4 N. carceleni 14.84 13.33 3.36 1.42 1.50 1.49 1.29 1.34 1.40 0.99 1.03 1.24 1.33 1.30 1.21 1.15 1.25 1.48 1.30 1.33
5 N. rosalindae 15.48 7.52 15.74 15.19 1.21 1.37 1.25 1.28 1.21 1.24 1.54 1.42 1.48 1.30 1.29 1.07 1.01 1.34 1.41 1.35
6 N. aletheia 16.16 11.10 16.19 16.14 11.21 1.60 1.44 1.67 1.50 1.42 1.69 1.46 1.45 1.62 1.06 0.83 1.32 1.57 1.63 1.58
7 N. musseri 16.14 11.95 14.77 16.16 12.36 14.21 1.41 1.52 1.40 1.29 1.69 1.38 1.31 1.47 1.44 1.36 1.36 1.56 1.41 1.43
8 N. paracou 15.18 15.59 16.26 15.88 15.50 16.88 17.32 1.39 1.49 1.33 1.52 1.22 1.31 1.41 1.40 1.33 1.59 1.43 1.53 1.32
9 N. dubosti 15.15 13.42 13.56 14.53 13.23 16.82 14.86 17.42 1.31 1.56 1.75 1.20 1.32 1.45 1.40 1.33 1.48 1.20 1.33 1.26
10 N. guianae 19.26 11.42 16.15 16.66 12.63 13.46 15.29 17.03 15.29 1.42 1.76 1.31 1.37 1.03 1.57 1.62 1.39 1.35 1.44 1.33
11 N. vargasllosai 15.29 13.08 9.56 8.94 13.85 15.12 13.68 14.49 14.99 15.79 1.09 1.31 1.42 1.23 1.38 1.34 1.23 1.65 1.45 1.36
12 N. spinosus 15.15 13.59 8.51 8.32 13.48 15.23 14.43 15.27 15.55 16.80 8.55 1.54 1.67 1.56 1.51 1.55 1.58 1.57 1.59 1.49
13 N. marajoara 15.48 12.68 13.44 13.78 13.92 13.93 15.42 15.11 10.23 15.00 14.21 15.71 0.77 1.46 1.44 1.24 1.24 1.47 1.12 0.88
14 N. xingu 15.39 13.10 14.27 14.23 13.99 13.09 14.60 16.63 11.11 15.21 14.54 16.61 4.17 1.51 1.45 1.23 1.39 1.57 1.08 0.87
15 N. jau 18.22 12.97 17.13 16.33 13.19 14.80 15.32 15.10 13.91 8.91 15.01 15.36 14.66 15.39 1.46 1.48 1.40 1.50 1.46 1.37
16 N. minutus 16.30 11.10 15.38 15.69 12.59 7.66 12.60 16.32 14.63 13.90 14.51 14.96 14.67 14.01 14.71 0.81 1.18 1.34 1.30 1.47
17 N. macedoruizi 15.28 10.43 15.22 14.65 11.21 4.91 13.87 15.80 14.23 13.50 14.84 14.73 13.80 12.61 14.60 5.68 1.19 1.44 1.36 1.36
18 N. marci sp. nov. 15.26 4.35 14.86 14.21 8.43 11.66 12.84 15.43 14.31 12.38 14.27 14.09 13.46 14.19 13.37 10.55 10.87 1.65 1.41 1.31
19 N. auriventer 12.55 14.95 12.99 14.34 14.30 15.85 15.21 16.00 14.42 17.00 16.14 13.57 15.48 14.80 15.04 14.29 14.89 15.86 1.41 1.57
20 N. elieceri 16.26 14.52 14.36 14.02 14.72 15.64 15.28 17.56 11.95 16.06 15.03 16.08 9.64 7.70 13.84 13.56 15.03 15.01 14.30 1.02
21 N. vossi 15.76 12.80 13.86 14.14 14.16 14.63 16.27 16.64 11.16 15.10 13.65 15.73 5.76 5.63 13.62 15.38 14.58 13.75 14.76 8.23

These results, along with those from the morphological qualitative and quantitative comparisons constitute strong evidence of cryptic diversity within N. tenuipes and that therefore, recently collected specimens from northwestern Ecuador (Chocó Biogeographic region) represent a species clearly distinct from Colombia. Accordingly, this new species is described as follows.

Taxonomy

Family Cricetidae Fisher, 1867

Subfamily Sigmodontinae Wagner, 1843

Tribe Oryzomyini Vorontsov, 1959

Neacomys Thomas, 1959

Type species

Neacomys tenuipes Thomas, 1900: holotype UKNHM 1899.10.3.74; type locality “Guaquimay, near Bogota,” Cundinamarca, Colombia.

Neacomys marci Brito & Tinoco, sp. nov.

https://zoobank.org/79122A9B-991F-4B46-AEDE-BD740EEB4EB4
Marc’s White-throated Spiny Mouse Ratón espinoso de Marc

Neacomys tenuipes: Brito et al. 2021a; Curay et al. 2022 (non Neacomys tenuipes Thomas, 1900).

Holotype

MECN 6232 (field number JBM 2307), an adult female captured on 18 November 2020, by J. Brito, J. Curay and K. Cuji, preserved as dry skin, skull, and skeleton, with muscle and liver sample preserved in 95% ethanol.

Measurements of holotype (in mm)

HBL 70; TL 84; HF 20; E 13; w 14.5; CIL 18.5; LIF 2.9; BIF 1.4; LD 5.3; LM 2.5; AW 4; BPB 2.1; LR 6.4; LN 8.2; RW-2 4; LIB 4.2; OL 6.6; BZP 1.7; ZB 11; BB 10.4; OCB 5; BOL 3.1; CD 8.1; BM1 0.8. All measurements of the type series are listed in Table 4.

Table 4.
Download as
CSV
XLSX

Summary of morphometric measurements of all specimens in mm. Species names are accompanied by number of analyzed individuals between parentheses. Mean and standard deviation values are shown between parentheses. Abbreviations of characters are detailed in the text.

N. marci sp. nov. (n = 23) N. cf. pictus (n = 2) N. rosalindae (n = 62)* N. tenuipes (n = 21)**
HBL 62–85(71.39±4.74) 79–90(84.5±7.78) 62–99(75.43±6.52) 70–97(82.21±6.68)
TL 50–88(79.66±9.59) 76–89(82.5±9.19) 61.5–87(76.56±5.34) 80–108(97.44±7.02)
HF 18–22(20.26±1.25) 22–23(22.5±0.71) 17–23(19.86±1.07) 20–23.3(22.16±0.85)
Ear 10–16(12.96±1.49) 14 11–20(13.74±1.45) 13–17(14.94±1.19)
CIL 17.5–18.9(18.31±0.36) 21.48–22.52(22±0.74) 16.8–19.5(18.17±0.56) 17.9–19.9(18.96±0.64)
LIF 2.1–3.1(2.83±0.23) 3.16–3.5(3.33±0.24) 1.9–3.5(2.83±0.23) 2.6–3.7(3.12±0.27)
BIF 1.3–1.6(1.5±0.09) 1.5–1.71(1.6±0.15) 1.2–1.6(1.39±0.09) 1.4–1.9(1.57±0.11)
LD 4.9–5.6(5.25±0.13) 6.32–6.5(6.41±0.13) 4.6–5.9(5.2±0.25) 4.8–5.8(5.4±0.28)
LM 2.3–2.7(2.55±0.1) 3.2–3.24(3.22±0.03) 2.4–2.8(2.61±0.09) 2.6–2.9(2.81±0.1)
AW 3.8–4.3(4.04±0.12) 4.75–4.87(4.81±0.09) 3.5–4.1(3.81±0.17) 3.9–4.4(4.14±0.12)
BPB 2.1–2.5(2.25±0.12) 2.76–2.77(2.76±0.01) 1.9–2.8(2.35±0.17) 2.2–2.5(2.3±0.1)
LR 5.1–6.7(6.2±0.39) 5.88–7.58(6.73±1.2) 5.9–7.4(6.61±0.29) 6.3–7.5(6.98±0.37)
LN 7.3–8.6(8.04±0.35) 8.81–9.22(9.02±0.29) 6.9–8.9(8.08±0.34) 7.3–9.2(8.42±0.53)
RW-2 3.8–4.3(4.06±0.13) 4.83–5.05(4.94±0.16) 3.4–4.5(3.96±0.21) 3.2–3.7(3.43±0.14)
LIB 4.2–4.6(4.41±0.13) 4.68–5.05(4.86±0.26) 3.7–4.6(4.16±0.22) 4.1–4.7(4.38±0.13)
OL 6.2–8.1(6.8±0.36) 8.26–8.83(8.54±0.4) 6.5–7.7(7±0.25) 3.1–4.1(3.54±0.26)
BZP 1.6–2.1(1.83±0.12) 2.3–2.5(2.38±0.13) 1.4–2.1(1.79±0.13) 1.6–2.1(1.87±0.12)
ZB 10.4–11.3(10.94±0.24) 12.6–13.1(12.87±0.33) 9.8–11.5(10.67±0.39) 10.2–11.9(11.21±0.41)
BB 10.2–10.8(10.54±0.17) 10.9–11.3(11.13±0.26) 9.2–10.7(10.09±0.3) 9.9–11.2(10.51±0.3)
OCB 5.03–5.58(5.33±0.15) 6–6.1(6.05±0.07) 4.7–5.5(5.12±0.17) 4.9–5.9(5.36±0.26)
BOL 2.7–3.17(2.94±0.13) 3.56–3.83(3.7±0.19) 2.4–3.3(2.88±0.17) 2.7–3.3(2.98±0.15)
CD 7.54–8.63(7.9±0.24) 8.64–8.75(8.7±0.08) 7.3–8.5(7.82±0.22) 7.4–8.3(7.84±0.23)

* = Sánchez–Vendizú et al. (2018); ** = Caccavo and Weksler (2021).

Type locality

Reserva Dracula, Estación Fisher, Parroquia Chical, Cantón Tulcán, Provincia Carchi, Ecuador, Coordinates: 1.006667, -78.2247; WGS84 taken by GPS at the site of collection; elevation 1,067 m.

Paratypes

(n = 38). MECN 6230, adult male, and MECN 6233, adult female, preserved as dry skin and cleaned skull, collected in Provincia de Carchi, Reserva Dracula, Estación Fisher (1.006667, -78.2247, 1,067 m.) on 18 November 2020, by J. Brito, J. Curay and K. Cuji. MECN 6231, adult male, preserved as dry skin and cleaned skull, collected in Provincia de Carchi, Reserva Dracula, Estación Fisher (1.006667, -78.2247, 1,067 m.) on 20 November 2020, by J. Brito, J. Curay and K. Cuji. MECN 6238, MECN 6239, MECN 6240, MECN 6241, adult males, and MECN 6237, MECN 6242, adult females, preserved in 75% ethanol, collected in Provincia de Carchi, Reserva Dracula, Estación Fisher (1.006667, -78.2247, 1,067 m.) on 21 November 2020, by J. Brito, J. Curay and K. Cuji. MECN 6479, adult male, preserved in 75% ethanol, collected in Provincia de Carchi, Reserva Dracula, Estación Fisher (1.006667, -78.2247, 1,067 m.) on 30 March 2021, by J. Brito. J. Castro, Z. Villacís and J. Guaya. MECN 5339, MECN 5340, MECN 5374, MECN 5375, adult males, preserved as cleaned skulls and carcasses in ethanol, MECN 5370, MECN 5373, adult males, preserved in ethanol, MECN 5372, adult female, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Carchi, Reserva Drácula, Peñas Blancas (0. 973758, -78.210173, 1,290 m) on 27 November 2016, by J. Brito, J. Robayo and H. Yela. MECN 5357, adult male, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Carchi, Reserva Dracula, Pailón (0.992406, -78.237714, 1,270 m) on 29 November 2016, by J. Brito, J. Robayo and H. Yela. MECN 6013, juvenile male, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Carchi, Reserva Dracula, Pailón (0.992406, -78.237714, 1,270 m) on 7 November 2017, by J. Brito, J. Curay and R. Vargas. MECN 5919, adult male, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Carchi, Reserva Dracula, Pailón Alto (0.97415, -78.2176, 1,630 m) on 28 March 2018, by J. R. Vargas and M. Esparza. MECN 5904, adult male, preserved as dry skin and cleaned skull, MECN 6014, adult male, MECN 6015, juvenile male, MECN 6016, adult female, preserved in ethanol, collected in Peñas Blancas on 7 November 2017, by J. Brito, J. Curay and R. Vargas. MECN 6570, adult male, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Imbabura, Parroquia Lita, Aguinaga (0.78125, -78.318113, 1,400 m) on 1 March 2020, by S. Erazo and D. Mantilla. MECN 6271, adult male, preserved in ethanol, collected in Provincia de Imbabura, Reserva Río Manduriacu (0.309547, -78.856631, 1,200 m) on 12 September 2019, by R. Peña. MECN 6766, adult female, preserved as skin dry, skull and skeleton, collected in Pichincha, Reserva Chontaloma (0.18138, -78.90516, 630 m) on 15 March 2021, by S. Pozo and C. López. MECN 7125, juvenile female, preserved as cleaned skull and carcass in ethanol, collected in Pichincha, El Progreso (0.164608, -78.767156, 1,140 m) on 21 September 2021, by R. Garcia. QCAZ 18677, adult male, preserved as dry skin and clean skull / jaw, collected in Pichincha, Reserva Mashpi (0.166600, -78.880000, 900 m) on 26 September 2019, by J. Cook and J. Dunnum. MECN 7563, MECN 7568, adult females, and MECN 7569 adult male, preserved as dry skins and cleaned skulls, MECN 7572, adult female, and MECN 7560, 7561, 7565, 7570, 7573 adult males, preserved as cleaned skull and carcass in ethanol, collected in Provincia de Esmeraldas, Reserva Canandé, Gualpí de los Cayapas (0.56479, -79.06104, 450 m) on 14–16 October 2022, by J. Brito, J. Guaya, and A. Aguilar.

Etymology

Named in honor of Marc Hoogeslag of Amsterdam, the Netherlands. He was co-founder and leader of the innovative Land Acquisition Fund of the International Union for the Conservation of Nature - Netherlands, which helps local groups throughout the world to establish new ecological reserves and conserve endangered species. Fundacion EcoMinga’s Reserva Manduriacu, the habitat of this new species, is one of the many reserves which have benefited from Marc’s program. The species epithet is formed from the surname “Marc” taken as a noun in the genitive case, adding the Latin suffix “i” (ICZN 31.1.2).

Diagnosis

A species of Neacomys with the following combination of characters: small size (head-body length 65–85 mm), long tail (69–126% longer than head and body length), belly fur pale buff but with gray based hairs, white throat, long nasals (which extend well beyond the plane of the lacrimal), condylar process higher than coronoid process, M1 anterocone divided, M1 with broad protoflexus; m1–m3 with wide hypoflexids.

Morphological description

The following description was based on all specimens available. Neacomys marci sp. nov. is a spiny mouse of small size (head and body length 65–85 mm). The dorsal pelage is dark brown (Fig. 3); soft hairs are mixed with spines; on average dorsal hairs are 9–10 mm in length. The soft hair is tricolor, with a light brown band at the base, an orange band in the middle and a black apical band. The posterior mystacial vibrissae are thick and long (34 mm), surpassing the auricular pinnae when ad pressed back; two superciliary vibrissae, the longest measuring 39 mm, extending to the middle of the dorsum. One medium-sized genal vibrissae (32 mm) are also present, which are more slender than the mystacial vibrissae. The ears are large (12–16 mm) and oval in outline. Although the ears seem to be naked, they are covered with short black fringe of hair. The base of the internal ears is yellowish cream and the edges are dark, the hairs are yellowish and medium in size. A small pale orange postauricular patch is present.

Figure 3. 

Live specimen of Neacomys marci sp. nov. in its natural habitat (MECN 6230, Estación Fisher, Ecuador). Please note the color of a living animal.

The pelage on the throat is white (Fig. 4A) and extends up to the corners of the mouth. The ventral pelage is pale buff but with gray base, and the hairs are on average 3.0–3.5 mm in length at the middle of the belly. The tail is uniformly dark, slender, and long (69–126% longer than head and body length). It is covered with rectangular scales (13 or 14 rows/cm near the base), with three dark brown hispid hairs emerging from the base of each scale, not longer than 1.5–2 scale rows. The hairs of the terminal portion of the tail form a small tuft (< 3 mm). Females have eight mammae arranged in pectoral, thoracic, abdominal, and inguinal pairs.

Figure 4. 

Ventral views of the skin of A Neacomys marci sp. nov. (MECN 6232, holotype; Estación Fisher, Ecuador), and B Neacomys tenuipes (UIS-MHN-M 1723; Finca La Bufalera, Colombia). Note the white-furred throat in N. marci sp. nov. (arrowed).

The manus is slender and short. The first digit is reduced with a long and wide claw. The other claws are short and curved. Ungual tufts are white and extend beyond the claw ends. The dorsal surface with evident brown scales; each scale has three dark brown hairs and sometimes the central hair is the longest. Long carpal vibrissae can reach the claw of digit V. The digits are relatively large; digit I is substantially shorter than digit II; digit II is shorter than digit III; digit III is slightly larger than digit IV; digit IV is larger than digit V.

Hind feet are long and slender (18–22 mm); the ungual tufts are white, abundant and extend well beyond the edge of the claws (Fig. 5A, D). Their dorsal surface has a small metatarsal patch, with brown scales (Fig. 5D); each scale has three dark brown hairs. Large number of granules covers most of the plantar surface, including the spaces between the pads and reaching the anterior border of the thenar pad. The four interdigital pads are elevated and similar in size; pads II and III are separated by a small interspace, while pads II and IV are separated by an interspace of similar size than pad I (Fig. 5A). The hypothenar pad is very small or absent, while the thenar pad is well developed, large and elevated anteriorly. Digits are relatively short; digit I reaches the base of digit II; digit II is slightly shorter than digit III; digit III is slightly larger than digit IV; digit IV is larger than digit V; digit V reaches halfway of the first phalanx of digit IV (Fig. 5A, D); claws are short, recurved and basally opened.

Figure 5. 

Ventral (A–C) and dorsal (D–F) views of the hind foot of Neacomys marci sp. nov. (A, D MECN 6232, holotype; Estación Fisher, Ecuador), N. tenuipes (B, E MHN-UCa-M 4019, Colombia), and N. rosalindae (C, F MECN 5824; Cordillera de Kutukú, Ecuador). Figures are not to scale to facilitate comparisons. Abbreviations: h = hypothenar, t = thenar, ut = ungual tufts.

The cranium is moderately large for the genus (average CIL = 18.2 mm) with the braincase showing a convex profile (Fig. 6). The dorsal profile of the cranial roof is flat from the nasals to the middle of the frontals, then rises at the back of the frontals and slopes gently down the parietals toward the occiput; the rostrum is long and slender; premaxillae are slightly shorter than nasals, not extending anteriorly beyond incisors, without forming a rostral tube; gnathic process is very small; the suture between the nasal bones and the premaxillary reaches the root of the zygomatic bone; the nasal bone is wide at the base and gradually widens forward (Fig. 7); the interorbital region is narrow; the supraorbital edges are small and sharp; the zygomatic notches are shallow and wide while seen from above; in the olfactory sagittal plane are two frontoturbinals, one interturbinal and three ethmoturbinals present (Fig. 8F); the lachrymal is small, with contact in equal proportions with the frontal and maxillary; the post-nasal depression is shallow; the fronto-parietal suture is V-shaped; the parietal is restricted to the dorsal portion of the skull; the braincase is rounded and inflated. A gnatic process is not developed; the zygomatic plate is wide and excavated (> M1 length) and slightly inclined backward; the zygomatic arch slender and without a jugal; a squamosal-alisphenoid groove is visible through the translucent braincase (Fig. 8B, E), with a perforation where it crosses the depression for the masticatory nerve; the stapedial foramen is present and small, the carotid canal is small, and the petrotympanic fissure is expressed (Figs 8C); the cephalic arterial supply is primitive (pattern 1 of Voss 1988); the alisphenoid strut is absent; an anterior opening of the alisphenoid canal is absent; the postglenoid foramen is large; the subsquamosal fenestra is small and the hamular process of the squamosal is long; a small tegmen tympani is present (Fig. 8A); there is no contact between the anterodorsal edge of the ectotympanic and the mastoid tubercle, which leads to an opened ectotympanic ring (Fig. 8A); the orbicular apophysis of the malleus is wide and elongate (oval in shape), with its longitudinal axis inclined towards the manubrium; mastoid bears no dorsolateral fenestra; the paraoccipital process is short.

Figure 6. 

Three-dimensional reconstruction of the skull of Neacomys marci sp. nov., based on micro-CT data of the holotype (MECN 6232; Estación Fisher, Ecuador): cranium in dorsal, ventral, and lateral view, and left hemimandible in labial view. Scale bar: 5 mm.

Figure 7. 

Selected aspects of qualitative anatomy contrasted in the crania (dorsal view = A, ventral view = B) based on data of Neacomys marci sp. nov. (left; MECN 6232, holotype; Estación Fisher, Ecuador) and Neacomys tenuipes (right; UIS-MHN-M 1723; Finca La Bufalera, Colombia). The figure portrays differences between the characteristics of these species as follows: N. marci sp. nov. has the longest nasal (n) extending well beyond the plane of the lacrimals (la), larger molars (m), and a low sagittal ridge (sr). Figures are not to scale to facilitate comparisons.

Figure 8. 

A selected anatomical features of the skull of Neacomys marci sp. nov. based on the holotype (MECN 6232; Estación Fisher, Ecuador): posterior portion of the skull in lateral view B lateral view of alisphenoid bone region C right auditory region in ventral view D ventral view of basicranial region E dorsal view (roofing bones of braincase removed) of basicranial region F cross-section of the cranium. Abbreviations: ab, auditory bulla; bet, bony Eustachian tube; bmt, buccinators-masticatory trough; bo, basioccipital; bs, basisphenoid; cc, carotid canal; etI, ethmoturbinal I; etII, ethmoturbinal II; etIII, ethmoturbinal III; fo, foramen ovale; ft1, frontoturbinal 1; ft2, frontoturbinal 2; it, interturbinal; ls, lamina semicircularis; mas, mastoid capsule; mlf, middle lacerate foramen; palc, posterior opening of the alisphenoid canal; pet, petrosal; pgf, postglenoid foramen; ppp, posterior palatal pits; ps, presphenoid; sag, squamosal alisphenoid groove; sfr, sphenofrontal foramen; stf, stapedial foramen; ssf, subsquamosal fenestra; tt, tegmen tympani; Pictures are three-dimensional reconstructions based on micro-CT data.

The Hill foramen is tiny; the incisive foramina are short, ending well anterior to the M1s anterior faces; the capsular process of the premaxillary is well developed; the palate is wide and long with the anterior border of the mesopterygoid fossa not reaching M3s posterior faces; the palatal foramina are small; the posterolateral pits are long and paired, and located parallel to the anterior part of the mesopterygoid fossa; the mesopterygoid fossa is broad as the parapterygoid plates, with the anterior margin U-shaped (Fig. 8D); the shape of the pterygoid plate is not expanded, and has straight margin; the sphenopalatine vacuities are elongated and narrow, occupying the posterior part of the presphenoid area; the presphenoid is wide (Fig. 8D); the auditory bullae are small and flask-shaped; the Eustachian tube is short, wide and gradually constricted; the petrosals are well-exposed; the anterior bullae process is in contact with the posterior margin of the pterygoid plate (Fig. 8C); the basioccipital depressions are deep, forming an recognizable crest; the anterior border of the foramen magnum is narrow, with a conspicuous notch.

The mandible with masseteric crest in line with procingulum of m1; the coronoid process is small, slender, and bended backwards; the sigmoid notch is oval; the condylar process is large and robust; the capsular process is forming a rounded elevation that lies below the coronoid process; the angular notch is shallow, and the angular process is blunt.

The incisors are opistodont, without grooves, and with yellowish enamel; the molars are brachydont and terraced (Fig. 9A); the main cusps of the upper and lower molars are opposed. The M1 is rounded in outline; the procingulum is narrower than the rest of the molar, with a rounded anteromedian fossette present; anterocone divided; the protoflexus is broad; the mesoflexus is small; the metaflexus is large and wide; the posteroloph is small. The M2 with indistinct protoflexus; the anteroloph is small; the mesoflexus is short and wide; the mesoloph is short; the mesofosette is rounded (Fig. 9A); the posteroloph is similar to M1. The M3 has a small paraflexus and indistinct hypoflexus. The upper molars have three roots each. The m1 is rectangular in outline; the procingulum is not divided into labial and lingual conulids; the protoflexid is short and wide; the hypoflexid is wide; the mesoflexid is large and wide; the mesolophid is large; the posteroflexid is short and broad; the mesofosette is large. The m2 is square in outline; the protoflexid is large and narrow; the hypoflexid is wide and inclined with direction towards the posteroflexid; the mesoflexid is short and wide; the mesolophid is short and wide; the mesofosette is very small. The m3 is anteriorly-posteriorly compressed, having a wide hypoflexid and a small anterolabial cingulum. The lower molars have two roots each.

Figure 9. 

A, B occlusal view of the right upper, and C, D right lower tooth row of: (A, C) Neacomys marci sp. nov. (MECN 6232, holotype; Estación Fisher, Ecuador) and (B, D) N. tenuipes (B UIS-MHN-M 1723; Finca La Bufalera, Bolívar, Colombia, and D MHN-UCa-M 3647; Acevedo, Huila, Colombia). Abbreviations: alc, anterolabial conule; pf, paraflexus; f, mesofosette; pc, procingulum.The arrows indicate the direction of the mesoflexus with the hypoflexus.

The tuberculum of the first rib articulates with the transverse processes of the seventh cervical and the first thoracic vertebrae; the second thoracic vertebra has a differentially elongated neural spine; 19 thoracicolumbar vertebrae, the 16th with moderately developed anapophyses; four sacrals; 33 or 34 caudals, with complete hemal arches in the second, third and fourth; 12 ribs.

The gall bladder is absent. The stomach is unilocular and hemiglandular; the cornified epithelium lines the corpus, while the glandular epithelium occupies the antrum and is slightly extended to the left of the esophageal opening; the bordering fold is notorious for being thick and long, surpassing the left level of the incisura angularis; the incisura angularis is moderately deep and the plica angularis is well expressed with a well-developed pars pyloricus (Fig. 10).

Figure 10. 

Stomach of Neacomys marci sp. nov. (MECN 7568; Reserva Río Canandé, Ecuador) A dorsal view B ventral view. Abbreviations: b, bordering fold; d, duodenum; co, cornified epithelium; ge, glandular epithelium; i, incisura angularis; e, esophagus.

Comparisons with similar species

Neacomys marci sp. nov. differs from its sister species N. tenuipes mainly in ventral coloration, N. marci sp. nov. is pale buff with white throat, while N. tenuipes is completely white to pale orange (Fig. 4). Additionally, N. marci sp. nov. has a slight bicolor at the base tail, while N. tenuipes has a clear bicolor at the base. The condylar process in N. marci sp. nov. is higher than the coronoid process, while in N. tenuipes most are lower than the coronoid process, some are equal to the coronoid process. At the molar level, N. marci sp. nov. has a narrow anterocone of M1, while in N. tenuipes it is wide (Fig. 4). In N. marci sp. nov. the hypoflexus of M3 is indistinct or absent, while in N. tenuipes it is present and well evident.

Another species from the Chocó Biogeographic region with which Neacomys marci sp. nov. could be confused is N. pictus. Both species have white throats, however N. marci sp. nov. has pale buff ventral color and N. pictus is faintly plumbeous basally on the belly. Neacomys marci sp. nov. has the interorbital region (in ventral view) with developed ridges, projecting like ledges; whereas N. tenuipes it is hidden under the maxilla. The mastoid is ossified in N. marci sp. nov. while in N. tenuipes it is most perforated. Other comparisons are summarized in Table 5.

Table 5.
Download as
CSV
XLSX

Selected morphological comparisons between Neacomys species distributed in the Chocó Biogeographic region. Characters obtained analyzing photos of the holotype and the description supplied by Colmenares-Pinzon (2021) * and Caccavo and Weksler (2021) **.

Characters Neacomys marci sp. nov. (n = 30) Neacomys tenuipes* Neacomys pictus**
Tail length most subequal to HBL most subequal to HBL subequal to HBL
Tail color unicolor bicolor most bicolor
Hypothenar pad absent present –
Ventral fur color pale buff, with white throat completely white to pale orange faintly plumbeous basally on belly, with throat white
Lacrimal bones equal contact with frontal and maxillary bones equal contact with frontal and maxillary or major contact with maxillary bone major contact with maxillary bone
Post nasal depression shallow most deep shallow
Supraorbital crests crests developed and inflexed posteriorly crests developed and inflexed posteriorly most with crests developed and inflexed posteriorly
Parietal restricted to the dorsal portion of the skull restricted to the dorsal portion of the skull restricted to the dorsal portion of the skull
Mastoid ossification ossified ossified or perforated most perforated
Shape of diastema flat flat with a small bump below the zygomatic plate
Incisive foramina position distant to M1 close or distant to M1 close to M1
Posterolateral palatal pits unique or shallow opening Most unique or shallow opening unique or shallow opening, or multiple openings
Interorbital region (ventral view) with developed ridges, projecting like ledges with developed ridges, projecting like ledges hidden under the maxilla
Condylar process higher than coronoid process lower than coronoid process, some equal to coronoid process lower than coronoid process, some equal to coronoid process
M1, shape of anterocone narrow wide wide
M1, shape of mesoloph most straight most straight curved
M3, hypoflexus absent present present

Distribution

Neacomys marci sp. nov. is known from six localities in the provinces of Carchi, Pichincha, and Esmeraldas, in northwestern Ecuador (Fig. 11).

Figure 11. 

Topographic map of northern South America. Sampling localities of three Neacomys species are shown with color codes described in the legend. Neacomys marci sp. nov. localities correspond to the Chocó biogeographic region in northwestern Ecuador (type locality is shown with black circle).

Natural history

The distributional range of the species is thus far limited to the Chocó Biogeographical region (Myers et al. 2000), where it occupies the lower subtropical and lower montane ecosystems (Ceron et al. 1999), in an altitudinal range from 450 to 1,630 m (Fig. 12). These forests are characterized by having a tree cover of approximately 30 m height. Most of the vegetation belongs to the families Araceae, Melastomataceae, Cyclanthaceae, Bromeliaceae, and to the ferns. Additionally, the following species of rodents and marsupials were recorded as living in sympatry: Melanomys caliginosus, Mindomys hammondi, Oecomys sp., Rhipidomys latimanus, Tanyuromys thomasleei, Pattonimus musseri, Sigmodontomys alfari, and Transandinomys bolivaris, the heteromyid Heteromys australis, the marsupials Chironectes minimus, Mamosops caucae, and Marmosa isthmica, and the squirrel Microsciurus mimulus.

Figure 12. 

Habitat where specimens of Neacomys marci sp. nov. have been collected in this study A Piemontane forest, and B Chocó rainforest.

Discussion

With the description of Neacomys marci sp. nov. the diversity of the genus reaches 24 formally recognized species, of which 14 (60%) have been described in the last five years (Hurtado and Pacheco 2017; Sánchez-Vendizú et al. 2018; Semedo et al. 2020; Brito et al. 2021a; Caccavo and Weksler 2021; Colmenares-Pinzon 2021; Semedo et al. 2021). Such dynamism has not been seen recently in the taxonomy of any other group of oryzomyine rodents and places Neacomys as the most diverse group within the tribe, and the third most diverse within the subfamily Sigmodontinae, only comparable to the genus Oligoryzomys (Hurtado 2021).

Results presented here confirm that comprehensive revisions of currently recognized species, i.e., by morphological and genetic characterizations, as well as collection of specimens in unexplored regions are fundamental to unveil cryptic diversity in groups of small mammals. Particularly for Neacomys, species once considered as homogeneous throughout a wide distribution, such as N. minutus, N. spinosus, or N. tenuipes have been split into multiple taxa. For N. tenuipes, Caccavo and Weksler (2021) recognized populations from Venezuela as different (N. leilae Caccavo & Weksler, 2021), whereas in this study, we found enough evidence to propose a separation of the populations from northwestern Ecuador into N. marci sp. nov. Likewise, other authors have noticed clear differences in other populations from the Chocó region in Colombia, whose genetic characterization is pending, to validate the name N. pusillus. On the other hand, it is worth mentioning that other specimens from northwestern Ecuador reviewed here and tentatively identified as N. cf. pictus (QCAZ 708 and MECN 3050), seem to differ notably from this species and from any other species of Neacomys. Further collections and the generation of genetic data from this population could result in the recognition of a new species, which ultimately demonstrates that the number of species within the genus will continue to increase.

The rainforests of northwestern Ecuador have both high biodiversity and endemism due to the biogeographic influence of the Chocó and Andes Mountains (Myers et al. 2000). For example, a variety of oryzomyines of the genera Pattonimus, Sigmodontomys, Tanyuromys, Transandinomys, and “Handleyomys” (Pine et al. 2012; Patton et al. 2015; Brito et al. 2020) are endemic to the Chocó forests. Despite this, our knowledge of the sigmodontine biodiversity of this hotspot is still incomplete.

It is important to mention that after more than two centuries of active research in mastozoology (Tirira 2014), intensive fieldwork was conducted in few places in Ecuador. Examples for those sites in the eastern Andes are Papallacta (Voss 2003), Guandera Biological Reserve (Lee et al. 2015), and Sangay National Park (Brito and Ojala-Barbour 2016), and in the western Andes are Cajas National Park (Barnett 1999), Otonga Reserve (Jarrín 2001), Pululahua Geobotanical Reserve (Curay et al. 2019), Polylepis Forest (Ojala-Barbour et al. 2019), Reserva Dracula (Brito et al. 2020, 2022a), and Lita (Curay et al. 2022). The interest in complementary biodiversity studies has led to the prioritization of intensive field work, using a variety of trapping techniques (e.g., live traps, spring traps, and pitfall traps), and has also triggered revisions of museum specimens. For example, in the last five years, these approaches have led to the description of at least 14 new sigmodontine: five Chilomys (see Brito et al, 2022a), three Thomasomys (see Brito et al. 2019; Brito et al. 2021b; Lee et al. 2022), one Tanyuromys (see Timm et al. 2018), one Ichthyomys (Fernández de Córdova et al. 2020), two Pattonimus (Brito et al. 2020), one Neacomys (Brito et al. 2021a), and one Mindomys (Brito et al. 2022b). This burgeoning richness will surely reorganize part of our understanding of Neotropical cricetids. This context highlights the urgency of establishing national and comprehensive inventory and collection programs, including sampling in previously studied areas as well as improving scholarly access to these resources.

Acknowledgements

Work at Reserva Dracula was undertaken with the field and logistic assistance of Jenny Curay, Karen Kuji, Zaskya Villacís, Jhandry Guaya, Yuleidy Castro, Rubí García, Rocío Vargas, and the unrestricted support of Fundación EcoMinga and its current director, Javier Robayo. Glenda Pozo is thanked for invaluable field assistance. To the rangers of EcoMinga, especially H. Yela, R. Peña, and M. Canticus, gratitude for their intense efforts with field logistics. Julio Carrion and Daniela Reyes are acknowledged for their assistance in the molecular biology laboratory at INABIO. We want to highlight the labor of the Rainforest Trust and their “Species Legacy” program, the Orchid Conservation Alliance, The Youth Land Trust, University of Basel and Fundación EcoMinga for their efforts to protect these montane forests. The Fundación de Conservación Jocotoco supported the expedition to the Reserva Canandé, with special thanks to Chiara Correa for her logistical coordination. Pamela Sánchez-Vendizú kindly provided morphometric measurements of Neacomys rosalindae, while Aldo Caccavo shared photographs of the holotypes N. pictus and N. tenuipes pusillus. Santiago F. Burneo provided access to the QCAZ collection (mammals museum). Mario Yanez kindly helped with Fig. 12B. Suggestions from Thiago Semedo, Pablo Teta and Lou Jost helped improve the quality of the manuscript. To these mentioned persons and institutions, our deep gratitude.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study has been supported by the following funds: Fundación EcoMinga and Fundación de Conservación Jocotoco.

Author contributions

Nicolás Tinoco performed the experiments, analyzed the molecular data, prepared figures and/or tables, authored or reviewed drafts of the paper, and approved the final draft. Claudia Koch and Javier Colmenraes-Pinzón performed the experiments, analyzed the data, authored or reviewed drafts of the paper, and approved the final draft. Francisco Castellanos performed the experiments, analyzed the morphometrics data, prepared figures and/or tables, authored or reviewed drafts of the paper, and approved the final draft. Jorge Brito conceived and designed the study, performed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the paper, acquired the funds, and approved the final draft.

Author ORCIDs

Nicolás Tinoco https://orcid.org/0000-0002-2196-1199

Claudia Koch https://orcid.org/0000-0002-7115-2816

Javier E. Colmenares-Pinzón https://orcid.org/0000-0003-2828-5522

Francisco X. Castellanos https://orcid.org/0000-0003-0955-8185

Jorge Brito https://orcid.org/0000-0002-3410-6669

Data availability

All of the data that support the findings of this study are available in the main text.

References

  • Allen JA (1912) Mammals from western Colombia. Bulletin of the American Museum of Natural History 31: 71–95.
  • Barnett AA (1999) Small mammals of the Cajas Plateau, southern Ecuador: Ecology and natural history. Bulletin of the Florida Museum of Natural History 42: 161–217.
  • Bilton DT, Jaarola M (1996) Isolation and purification of vertebrate DNAs. In: Clapp JP (Ed.) Species Diagnostics Protocols: PCR and Other Nucleic Acid Methods in Molecular Biology. Totowa: Humana Press, 25–37. https://doi.org/10.1385/0-89603-323-6:25
  • Bonvicino C, Moreira M (2001) Molecular phylogeny of the genus Oryzomys (Rodentia: Sigmodontinae) based on cytochrome b DNA sequences. Molecular Phylogenetics and Evolution 18(2): 282–292. https://doi.org/10.1006/mpev.2000.0878
  • Brito J, Tinoco N, Curay J, Vargas R, Reyes-Puig C, Romero V, Pardiñas UFJ (2019) Diversidad insospechada en los Andes de Ecuador: Filogenia del grupo cinereus de Thomasomys y descripción de una nueva especie (Rodentia, Cricetidae). Mastozoología Neotropical 26(2): 1–22. https://doi.org/10.31687/saremMN.19.26.2.0.04
  • Brito J, Koch C, Percequillo AR, Tinoco N, Weksler M, Pinto CM, Pardiñas UFJ (2020) A new genus of oryzomyine rodents (Cricetidae, Sigmodontinae) with three new species from montane cloud forests, western Andean cordillera of Colombia and Ecuador. PeerJ 8: e10247. https://doi.org/10.7717/peerj.10247
  • Brito J, Tinoco N, Burneo S, Koch C, Arguero A, Vargas R, Pinto CM (2021a) A new species of spiny mouse, genus Neacomys (Cricetidae: Sigmodontinae) from Cordillera del Cóndor, Ecuador. Mastozoología Neotropical 28: 001–022. https://doi.org/10.31687/saremMN.21.28.1.0.23
  • Brito J, Vaca-Puente S, Koch C, Tinoco N (2021b) Discovery of the first Amazonian Thomasomys (Rodentia, Cricetidae, Sigmodontinae): A new species from the remote Cordilleras del Cóndor and Kutukú in Ecuador. Journal of Mammalogy 102(2): 615–635. https://doi.org/10.1093/jmammal/gyaa183
  • Brito J, Tinoco N, Pinto CM, García R, Koch C, Fernandez V, Burneo S, Pardiñas UFP (2022a) Unlocking Andean sigmodontine diversity; five new species of Chilomys (Rodentia: Cricetidae) from the montane forests of Ecuador. PeerJ 10: e13211. https://doi.org/10.7717/peerj.13211
  • Brito J, Koch C, Tinoco N, Pardiñas UF (2022b) A new species of Mindomys (Rodentia, Cricetidae) with remarks on external traits as indicators of arboreality in sigmodontine rodents. Evolutionary Systematics 6(1): 35–55. https://doi.org/10.3897/evolsyst.6.76879
  • Caccavo A, Weksler M (2021) Systematics of the rodent genus Neacomys Thomas (Cricetidae: Sigmodontinae): two new species and a discussion on carotid patterns. Journal of Mammalogy 102(3): 852–878. https://doi.org/10.1093/jmammal/gyab037
  • Carleton MD (1973) A survey of gross stomach morphology in New World Cricetinae (Rodentia, Muroidea), with comments on functional interpretations. Miscellaneous Publications, Museum of Zoology. University of Michigan 146: 1–43.
  • Carleton MD, Musser CG (1989) Systematic studies of Oryzomyine rodents (Muridae, Sigmodontinae): A synopsis of Microryzomys. Bulletin of the American Museum of Natural History 191: 1–83.
  • Cerón C, Palacios W, Valencia R, Sierra R (1999) Las formaciones naturales de la Costa del Ecuador. In: Sierra R (Ed.) Propuesta Preliminar de un Sistema de Clasificación de Vegetación Para el Ecuador Continental. Quito: Proyecto INEFAN/GERF-BIRF and Ecociencia.
  • Colmenares-Pinzon JE (2021) Calling for a reassessment of rodent diversity in Colombia: description of a new species of Neacomys (Cricetidae: Oryzomyini) from the Magdalena Valley, with a new phylogenetic hypothesis for the genus and comments on its diversification. Zootaxa 4920(4): 451–494. https://doi.org/10.11646/zootaxa.4920.4.1
  • Curay J, Mantilla D, Brito J (2022) Diversity of small non-volant mammals of Lita, northwestern Imbabura, Ecuador. Check List 18(3): 709–719. https://doi.org/10.15560/18.3.709
  • Férnandez de Córdova JF, Nivelo-Villavicencio C, Reyes-Puig C, Pardiñas UFJ, Brito J (2020) A new species of crab-eating rat of the genus Ichthyomys, from Ecuador (Rodentia, Cricetidae, Sigmodontinae). Mammalia 84(4): 377–391. https://doi.org/10.1515/mammalia-2019-0022
  • Hurtado N, Pacheco V (2017) Revision of Neacomys spinosus (Thomas, 1882) (Rodentia: Cricetidae) with emphasis on Peruvian populations and the description of a new species. Zootaxa 4242(3): 401–440. https://doi.org/10.11646/zootaxa.4242.3.1
  • Jarrín P (2001) Mamíferos en la niebla Otonga, un bosque nublado del Ecuador. Quito: Museo de Zoología, Centro de Biodiversidad y Ambiente, Pontificia Universidad Católica del Ecuador.
  • Josse J, Husson F (2016) missMDA: A Package for Handling Missing Values in Multivariate Data Analysis. Journal of Statistical Software 70(1): 1–31. https://doi.org/10.18637/jss.v070.i01
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549. https://doi.org/10.1093/molbev/msy096
  • Lee TE, Ritchie AR, Vaca-Puente S, Brokaw JM, Camacho MA, Burneo SF (2015) Small mammals of Guandera Biological Reserve, Carchi Province, Ecuador and comparative Andean small mammal ecology. Occasional Papers, Museum of Texas Tech University 334: 1–17.
  • Lee Jr TE, Tinoco N, Brito J (2022) A new species of Andean mouse of the genus Thomasomys (Cricetidae, Sigmodontinae) from the eastern Andes of Ecuador. Vertebrate Zoology 72: 219–233. https://doi.org/10.3897/vz.72.e78219
  • Miller M, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. New Orleans: Gateway Computing Environments Workshop (GCE), 1–8. https://doi.org/10.1109/GCE.2010.5676129
  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772): 853–858. https://doi.org/10.1038/35002501
  • Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–274. https://doi.org/10.1093/molbev/msu300
  • Ojala-Barbour R, Brito J, Teska WR (2019) A comparison of small mammal communities in two High-Andean Polylepis woodlands in Ecuador. ACI Avances en Ciencias e Ingenierías 11(2): 208–221. https://doi.org/10.18272/aci.v11i2.516
  • Pardiñas UFJ, Ruelas D, Brito J, Bradley LC, Bradley RD, Garza NO, Kryštufek B, Cook J, Cuéllar Soto E, Salazar-Bravo J, Shenbrot G, Chiquito E, Percequillo A, Prado J, Haslauer R, Patton J, Leon-Paniagua L (2017) Cricetidae (true hamsters, voles, lemmings and new world rats and mice)—species accounts of Cricetidae. In: Wilson DE, Lacher Jr TE, Mittermeier RA (Eds) Handbook of the mammals of the world. Rodents II. Barcelona, Spain, 280–535.
  • Pardiñas UF, Canon C, Galliari CA, Brito J, Hoverud BN, Lessa G, De Oliveira JA (2020) Gross stomach morphology in akodontine rodents (Cricetidae: Sigmodontinae: Akodontini): a reappraisal of its significance in a phylogenetic context. Journal of Mammalogy 101(3): 835–857. https://doi.org/10.1093/jmammal/gyaa023
  • Patton JL, Pardinas UFJ, D’Elia G (2015) Mammals of South America. 2. Rodents. University of Chicago Press. Chicago, Illinois.
  • Pine RH, Timm RM, Weksler M (2012) A newly recognized clade of trans-Andean Oryzomyini (Rodentia: Cricetidae), with description of a new genus. Journal of Mammalogy 93(3): 851–870. https://doi.org/10.1644/11-MAMM-A-012.1
  • R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  • Ronquist F, Teslenko M, Van Der Mark P, Ayres D, Darling AA, 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. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Sánchez-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(3913): 1–38. https://doi.org/10.1206/3913.1
  • Semedo TBF, Da Silva MNF, Gutierrez EE, Ferreira DC, Da Silva Nunes M, Mendes-Oliveira AC, Farias IP, Rossi RV (2020) Systematics of Neotropical spiny mice, genus Neacomys Thomas, 1900 (Rodentia: Cricetidae), from southeastern Amazonia, with descriptions of three new species. American Museum Novitates 3958(3958): 1–43. https://doi.org/10.1206/3958.1
  • Semedo TBF, Da Silva MNF, Carmignotto AP, Rossi RV (2021) Three new species of spiny mice, genus Neacomys Thomas, 1900 (Rodentia: Cricetidae), from Brazilian Amazonia. Systematics and Biodiversity 19(8): 1113–1134. https://doi.org/10.1080/14772000.2021.1980449
  • Sikes RS (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 97(3): 663–688. https://doi.org/10.1093/jmammal/gyw078
  • Smith MF, Patton JL (1993) The diversification of South American murid rodents: Evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, Linnean Society of London 50(3): 149–177. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x
  • Timm RM, Pine RH, Hanson JD (2018) A new species of Tanyuromys Pine, Timm, and Weksler, 2012 (Cricetidae: Oryzomyini), with comments on relationships within the Oryzomyini. Journal of Mammalogy 99(3): 608–623. https://doi.org/10.1093/jmammal/gyy042
  • Tirira DG (2014) Historia de la Mastozoología en Ecuador. In: Ortega J, Martínez JL, Tirira DG (Eds) Historia de la Mastozoología en Latinoamérica, las Guayanas y el Caribe. Quito, México: Editorial Murciélago Blanco y Asociación Ecuatoriana de Mastozoología, 205–244.
  • Voss RS (1988) Systematics and ecology of ichthyomyine rodents (Muroidea): patterns of morphological evolution in a small adaptive radiation. Bulletin of the American Museum of Natural History 188: 258–493.

Appendix 1

Studied specimens belong to the following mammal collections: CTUA, Colección Teriológica de la Universidad de Antioquia, Colombia; USNM, National Museum of Natural History, Smithsonian Institution, USA; FMNH, Field Museum of Natural History, USA; AMNH, American Museum of Natural History, USA; TTU, Texas Tech University, USA; IAvH-M, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia; UIS-MHN-M, Universidad Industrial de Santander, Santander, Colombia; MHN-UCa-M, Universidad de Caldas, Caldas, Colombia; MECN, Instituto Nacional de Biodiversidad, Quito, Ecuador; MEPN, Museo de la Escuela Politécnica Nacional, Quito, Ecuador; QCAZ, Museo Pontificia Universidad Católica del Ecuador, Quito, Ecuador.

Neacomys marci sp. nov. (n = 39): Ecuador, Carchi, Reserva Drácula, Estación Fisher: MECN 6232 (holotype), MECN 6230, 6231, 6233, 6237–6242, 6479; Pailón: MECN 5357, 6013; Pailón Alto: MECN 5919; Peñas Blancas: MECN 5339–40, 5370, 5372–75, 5904, 6014–16; Imbabura, Ibarra, Lita, Aguinaga: MECN 6570; Cotacachi, García Moreno, Reserva Río Manduriacu: MECN 6271; Pichincha, Pacto, El Progreso: MECN 7125; Reserva Chonta Loma: MECN 6766; Reserva Masphi: QCAZ 18677; Esmeraldas, Reserva Canandé, Gualpí de los Cayapas: MECN 7560–61, 7563, 7565, 7568–70, 7572–73.

Neacomys tenuipes (n = 60): Colombia, Antioquia, Amalfi: CTUA 2599; Cisneros, 11 Km S and 30 Km E: USNM 499543–45; El Carmen de Viboral, Vereda el Porvenir, Cañón del Río Melcocho; IAvH-M 10291–302; Sonsón, Río Negrito, 15 Km E: FMNH 70130, 70134; Valdivia, 4 Km S, Quebrada de Oro: FMNH 70126; Zaragoza: IAvH-M 2934–35, 2938, 2956, 2959, 2961, 2968, 2980, 3756; 25 Km S, 22 Km W, at la Tirana: USNM 499541, 499546–47, 499549–52, 499554, 499556–59, 499578–79; BOLIVAR, Cantagallo, Vereda Santo Domingo, Finca La Bufalera: UIS-MHN-M 1720, 1723, 1762; Boyacá, Muzo: FMNH 71778; Caldas, Manizales, Ecoparque Los Alcázares: MHN-UCa-M 1761; Samaná, Río Hondo: FMNH 71748, 71762, 71766; Parque Nacional Natural Selva de Florencia, Vereda San Antonio, microcuenca Las Mercedes: MHN-UCa-M 1627–8; Cundinamarca, Medina, Vereda Periquito: IAvH-M 10230; Paime: AMNH 69182; Chocó, Riosucio (IAvH-M 5029–30; Huila, Acevedo, Río Aguas Claras: FMNH 71776; MHN-UCa-M 3647; Santander, Lebrija, Vereda Portugal, Granja El Puente: UIS-MHN-M 927.

Neacomys tenuipes pusillus (n = 1): Colombia, from San José, Cauca: AMNH 31695 (holotype).

Neacomys rosalindae (n = 25): Ecuador, Morona Santiago, Taisha: MECN 476, 468–69; Orellana, Pompeya Sur: MECN 776, 791, 793, 968, 994, 1006; Comunidad Jabalí: MECN 2333; Pastaza, Lorocachi: MEPN 12363, 12371–72, 12387; Bameno: MEPN 12433, 12468, 12470–71, 12474–78; Zamora Chinchipe, Tundayme: MECN 5689–90.

Neacomys pictus (n = 2): Panama, from Cana, Darien: USNM 178717 (holotype), TTU 39148.

Neacomys cf. pictus (n = 2): Ecuador, Esmeraldas, Muisne, Río San Francisco: MECN 3058; Cotopaxi, Reserva La Otonga: QCAZ 808.

Appendix 2

Table A1.
Download as
CSV
XLSX

List of specimens included in the phylogenetic analyses. For each terminal species, catalog access numbers and GenBank accessions are provided. An asterisk * denotes holotypes.

Taxa Cytb Catalog number or collector Locality
OUTGROUPS:
Microryzomys altissimus EU579502 QCAZ 8353 Ecuador, Azuay
Microryzomys minutus EU258535 MVZ 166666 Perú, Cusco
Oligoryzomys flavescens GU185922 P32 Uruguay, San José
Oreoryzomys balneator EU579510 AMNH 268144 Perú, Cajamarca
Oryzomys palustris EU074639 EVG 06 USA, Florida
Scolomys melanops AF527419 KU 158213 Perú, San Jacinto
Scolomys juruaense AF108696 INPA 2489 Brazil, Río Jurua
Scolomys ucayalensis EU579518 AMNH 272721 Peru. Loreto
Thomasomys baeops KR818876 TEL 1960 Ecuador, Carchi
Thomasomys daphne AF108673 MVZ 171502 Peru, Puno
Thomasomys ischyurus AF108675 MVZ 182003 Peru, Cajamarca
Thomasomys kalinowskii AF108678 MVZ 172598 Peru, Junin
Thomasomys paramorum KR818893 TEL 2380 Ecuador, Carchi
Thomasomys taczanowskii KR818885 TEL 2388 Ecuador, Carchi
Thomasomys vulcani KR818904 TEL 2746 Ecuador, Carchi
INGROUP:
Neacomys elieceri MT462054 JUR 19 Brazil, Pará
Neacomys elieceri MT462055 UFPA 1413 Brazil, Pará
Neacomys elieceri MT462056 JUR 042 Brazil, Pará
Neacomys elieceri MT462057 MPEG 42901 Brazil, Pará
Neacomys marajoara KX752072 MPEG 40443 Brazil, Pará
Neacomys marajoara KX752074 MEPG 40439 Brazil, Pará
Neacomys marajoara KX752075 MPEG 40440 Brazil, Pará
Neacomys marajoara KX752080 MPEG 40446 Brazil, Pará
Neacomys marajoara MT462067 MPEG 40441 Brazil, Pará
Neacomys marajoara MT462068 MPEG 40435 Brazil, Pará
Neacomys marajoara MT462069 MPEG 40434 Brazil, Pará
Neacomys marajoara MT462070 MPEG 40432 Brazil, Pará
Neacomys marajoara MT462071 MPEG 40431 Brazil, Pará
Neacomys marajoara MT462072 MPEG 40429 Brazil, Pará
Neacomys vossi MT462024 UFPA 1277 Brazil, Pará
Neacomys vossi MT462025 UFPA 1284 Brazil, Pará
Neacomys vossi MT462026 UFPA 1647 Brazil, Pará
Neacomys vossi MT462027 UFPA 1467 Brazil, Pará
Neacomys vossi MT462028 UFPA 1583 Brazil, Pará
Neacomys vossi MT462029 UFPA 1577 Brazil, Pará
Neacomys vossi MT462030 UFPA 1691 Brazil, Pará
Neacomys vossi MT462031 UFPA 1520 Brazil, Pará
Neacomys vossi MT462032 UFPA 1654 Brazil, Pará
Neacomys vossi MT462033 UFPA 1487 Brazil, Pará
Neacomys vossi MT462073 UFPA 1736 Brazil, Pará
Neacomys vossi MT462074 UFPA 1444 Brazil, Pará
Neacomys vossi MT462075 UFPA 1391 Brazil, Pará
Neacomys xingu KX752073 MPEG 41804 Brazil, Pará
Neacomys xingu KX752076 MPEG 41805 Brazil, Pará
Neacomys xingu KX792080 USNM MDC 593 Brazil, Pará
Neacomys xingu MG262333 MZUSP 29540 Brazil, Mato Grosso
Neacomys xingu MT462058 UFMT 1275 Brazil, Pará
Neacomys xingu MT462059 UFMT 1273 Brazil, Pará
Neacomys xingu MT462060 UFMT 1268 i Brazil, Pará
Neacomys xingu MT462061 MPEG 41805 Brazil, Pará
Neacomys xingu MT462062 MPEG 42019 Brazil, Pará
Neacomys xingu MT462063 MPEG 41996 Brazil, Pará
Neacomys xingu MT462064 PSA 69 Brazil, Pará
Neacomys xingu MT462065 MPEG 41991 Brazil, Pará
Neacomys xingu MT462066 PSA 46 Brazil, Pará
Neacomys paracou FM210765 V 1097 Guyana, Saul
Neacomys paracou FM210766 ROM 114143 Suriname, Brokopongo
Neacomys paracou FM210767 ROM 114315 Suriname, Brokopongo
Neacomys paracou FM210768 ROM 114317 Suriname, Brokopongo
Neacomys paracou FM210769 ROM 114324 Suriname, Brokopongo
Neacomys paracou FM210770 V 1689 Guyana, Mont St. Marcel
Neacomys paracou FM210782 ROM 114325 Suriname, Brokopongo
Neacomys paracou FM210783 V 2002 Guyana, Caiman
Neacomys paracou FM210784 V 1702 Guyana, Nouragues
Neacomys paracou KP778279 ROM 114317 Suriname, Brokopongo
Neacomys paracou KP778309 ROM 114143 Suriname, Brokopongo
Neacomys paracou KP778398 ROM:114150 Suriname, Brokopongo
Neacomys paracou KP778425 ROM 114023 Suriname, Brokopongo
Neacomys paracou KX752077 MPEG 39998 Brazil, Pará
Neacomys paracou KX752078 IEPA 2466 Brazil, Amapa
Neacomys paracou KX792078 ROM 101026 Guyana, Barima-Waini
Neacomys paracou KX792079 ROM 101114 Guyana, Barima-Waini
Neacomys paracou MT462042 CN 279 Brazil, Pará
Neacomys paracou MT462043 CN 263 Brazil, Pará
Neacomys paracou MT462044 CN 186 Brazil, Pará
Neacomys paracou MT462045 CN 184 Brazil, Pará
Neacomys paracou MT462046 CN 129 Brazil, Pará
Neacomys paracou MT462047 CN 70 Brazil, Pará
Neacomys paracou MT462048 CN 66 Brazil, Pará
Neacomys paracou MT462049 INPA 7089 Brazil, Amazonas
Neacomys paracou MT462050 INPA 7138 Brazil, Amazonas
Neacomys auriventer MW512656 MEPN 11863 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512657 MEPN 11870 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512658 MEPN 12079 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512659 MPEN 12086 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512660 MPEN 12110 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512661 MEPN 12306 Ecuador, Zamora Chinchipe
Neacomys auriventer MW512662 MEPN 12312 Ecuador, Zamora Chinchipe
Neacomys serranensis* MT536172 UIS-MHN-M 1608 Colombia, Santander
Neacomys serranensis MT536173 UIS-MHN-M 1928 Colombia, Santander
Neacomys amoenus AF108701 MVZ 155015 Peru, Amazonas
Neacomys amoenus GU126521 MVZ 155014 Peru, Amazonas
Neacomys amoenus JQ966232 UFES 1730 Brazil, Mato Grosso
Neacomys amoenus KX792021 LHE 1417 Bolivia, Santa Cruz
Neacomys amoenus KX792022 USNM 584543 Bolivia, Santa Cruz
Neacomys amoenus KX792023 LHE 1558a Bolivia, Santa Cruz
Neacomys amoenus KX792024 MZ-USP/CIT 371 Brazil, Mato Grosso
Neacomys amoenus KX792025 MZ-USP/CIT 519 Brazil, Mato Grosso
Neacomys amoenus KX792026 MZ-USP/CIT 520 Brazil, Mato Grosso
Neacomys amoenus KX792027 MZ-USP/CIT 534 Brazil, Mato Grosso
Neacomys amoenus KX792028 MZ-USP/CIT 555 Brazil, Mato Grosso
Neacomys amoenus KX792029 MZ-USP/CIT 569 Brazil, Mato Grosso
Neacomys amoenus KX792030 MZ-USP/CIT 665 Brazil, Mato Grosso
Neacomys amoenus KX792031 MZ-USP/CIT 678 Brazil, Mato Grosso
Neacomys amoenus KX792032 INPA 3060 Brazil, Acre
Neacomys amoenus KX792033 INPA 3062 Brazil, Acre
Neacomys amoenus KX792034 MNFS 1263 Brazil, Acre
Neacomys amoenus KX792035 MVZ 193758 Brazil, Acre
Neacomys amoenus KX792036 MVZ 193767 Brazil, Acre
Neacomys amoenus KX792037 MVZ 190364 Brazil, Amazonas
Neacomys amoenus KX792038 MVZ 190365 Brazil, Amazonas
Neacomys amoenus KX792039 MVZ 190367 Brazil, Amazonas
Neacomys amoenus KX792040 MVZ 190372 Brazil, Amazonas
Neacomys amoenus KX792041 USNM 588051 Peru, Cusco
Neacomys amoenus KX792042 USNM 588096 Peru, Cusco
Neacomys amoenus KX792043 MRR 778 Peru, Cusco
Neacomys amoenus KX792044 MRR 799 Peru, Cusco
Neacomys amoenus KX792049 MVZ 155015 Peru, Amazonas
Neacomys amoenus KY859733 MUSM 45055 Peru, Huánuco
Neacomys amoenus KY886320 MUSM 40760 Peru, Junin
Neacomys amoenus KY886321 MUSM 41445 Peru, Junin
Neacomys amoenus KY886322 MUSM 35698 Peru, Loreto
Neacomys amoenus KY886323 MUSM 17990 Peru, Loreto
Neacomys amoenus MG262329 PEU 960057 Brazil, Mato Grosso
Neacomys amoenus MG262330 PEU 960064 Brazil, Mato Grosso
Neacomys amoenus MG262331 M 97024 Brazil, Mato Grosso
Neacomys amoenus MG262332 M 968559 Brazil, Mato Grosso
Neacomys amoenus MT462015 INPA 3059 Brazil, Acre
Neacomys amoenus MT462016 INPA 3064 Brazil, Acre
Neacomys amoenus MT462017 INPA 3063 Brazil, Acre
Neacomys amoenus MT462019 MVZ 190634 Brazil, Amazonas
Neacomys amoenus MT462020 MVZ 190635 Brazil, Amazonas
Neacomys amoenus MT462021 INPA 3057 Brazil, Amazonas
Neacomys amoenus MT462022 USNM 584544 Bolivia, Santa Cruz
Neacomys amoenus MT462076 UFMT 1763 Brazil, Mato Grosso
Neacomys amoenus MT462077 UFMT 1757 Brazil, Mato Grosso
Neacomys amoenus MT462078 UFMT 1669 Brazil, Mato Grosso
Neacomys amoenus MT462079 UFMT 1659 Brazil, Mato Grosso
Neacomys amoenus MT462080 UFMT 1637 Brazil, Mato Grosso
Neacomys amoenus MT462081 UFMT 1374 Brazil, Mato Grosso
Neacomys amoenus MT462082 UFMT 1373 Brazil, Mato Grosso
Neacomys amoenus MT462083 UFMT 1370 Brazil, Mato Grosso
Neacomys amoenus MT462084 INPA-MSANB 46 Brazil, Rondonia
Neacomys amoenus MT462085 INPA-MSAFM 02 Brazil, Rondonia
Neacomys amoenus MT462086 UFMT 3382 Brazil, Mato Grosso
Neacomys amoenus MT462087 UFMT 3380 Brazil, Mato Grosso
Neacomys carceleni EU579504 MVZ 155014 Peru, Amazonas
Neacomys carceleni KX792045 ROM 104474 Ecuador, Pastaza
Neacomys carceleni KX792046 ROM 105278 Ecuador, Pastaza
Neacomys carceleni KX792047 ROM 105290 Ecuador, Pastaza
Neacomys carceleni KX792048 USNM 574567 Ecuador, Pastaza
Neacomys carceleni KY859736 MUSM 45714 Peru, Loreto
Neacomys carceleni KY859737 PSV 204 Peru, Loreto
Neacomys carceleni KY859738 ROM 105282 Ecuador, Pastaza
Neacomys carceleni MT462018 ROM 105264 Ecuador, Napo
Neacomys carceleni MW512665 QCAZ 10364 Ecuador, Orellana
Neacomys carceleni MW512666 QCAZ 15251 Ecuador, Orellana
Neacomys carceleni MW512667 QCAZ 15253 Ecuador, Orellana
Neacomys carceleni MW512668 QCAZ 15254 Ecuador, Orellana
Neacomys carceleni MW512669 QCAZ 15805 Ecuador, Orellana
Neacomys carceleni MW512670 QCAZ 15807 Ecuador, Orellana
Neacomys carceleni MW512671 QCAZ 15813 Ecuador, Orellana
Neacomys carceleni MW512672 QCAZ 15814 Ecuador, Orellana
Neacomys carceleni MW512673 QCAZ 15815 Ecuador, Orellana
Neacomys carceleni MW512674 QCAZ 15817 Ecuador, Orellana
Neacomys carceleni MW512675 QCAZ 16124 Ecuador, Orellana
Neacomys carceleni MW512676 QCAZ 16125 Ecuador, Orellana
Neacomys carceleni MW512677 QCAZ 16404 Ecuador, Orellana
Neacomys carceleni MW512678 QCAZ 16406 Ecuador, Orellana
Neacomys carceleni MW512679 QCAZ 16407 Ecuador, Orellana
Neacomys carceleni MW512680 QCAZ 16408 Ecuador, Orellana
Neacomys carceleni MW512681 QCAZ 16412 Ecuador, Orellana
Neacomys carceleni MW512682 QCAZ 16422 Ecuador, Orellana
Neacomys carceleni MW512683 QCAZ 16423 Ecuador, Orellana
Neacomys carceleni MW512684 QCAZ 16424 Ecuador, Orellana
Neacomys carceleni MW512685 QCAZ 4614 Ecuador, Tungurahua
Neacomys carceleni MW512686 QCAZ 5308 Ecuador, Pastaza
Neacomys carceleni MW512687 QCAZ 7013 Ecuador, Sucumbíos
Neacomys carceleni MW512688 QCAZ 7182 Ecuador, Sucumbíos
Neacomys carceleni MW512689 QCAZ 7249 Ecuador, Sucumbíos
Neacomys carceleni MW512690 QCAZ 7251 Ecuador, Sucumbíos
Neacomys carceleni MW512691 QCAZ 8163 Ecuador, Orellana
Neacomys carceleni MW512692 QCAZ 8827 Ecuador, Morona Santiago
Neacomys carceleni MW512693 QCAZ 8828 Ecuador, Morona Santiago
Neacomys carceleni MW512694 QCAZ 8832 Ecuador, Morona Santiago
Neacomys carceleni MW512695 QCAZ 8859 Ecuador, Morona Santiago
Neacomys carceleni MW512696 QCAZ 15818 Ecuador, Orellana
Neacomys spinosus KX258228 MUSM 36924 Peru, Amazonas
Neacomys spinosus KY886327 MUSM 36928 Peru, Amazonas
Neacomys vargasllosai KX258225 MUSM 35076 Peru, Puno
Neacomys vargasllosai KX258226 MUSM 35080 Peru, Puno
Neacomys vargasllosai KX258227 MUSM 35083 Peru, Puno
Neacomys vargasllosai KX792082 MVZ 172650 Peru, Puno
Neacomys vargasllosai MT462013 MVZ 172654 Peru, Puno
Neacomys vargasllosai MT462014 MVZ 172655 Peru, Puno
Neacomys aletheia KX792064 INPA 3050 Brazil, Amazonas
Neacomys aletheia* KX792066 INPA 3891 Brazil, Amazonas
Neacomys aletheia KX792067 MPEG/JUR 3 Brazil, Amazonas
Neacomys aletheia KX792070 MVZ 190362 Brazil, Amazonas
Neacomys aletheia KY754054 MVZ 193750 Brazil, Amazonas
Neacomys aletheia KY886324 MUSM 15994 Peru, Loreto
Neacomys aletheia KY886325 MUSM 15993 Peru, Loreto
Neacomys aletheia KY886326 INPA 3056 Brazil, Amazonas
Neacomys aletheia MT462011 INPA 3055 Brazil, Amazonas
Neacomys aletheia MT462012 INPA 3053 Brazil, Amazonas
Neacomys guianae FM210778 CM 76847 Suriname, Nickerie
Neacomys guianae FM210779 CM 76849 Suriname, Saramacca
Neacomys guianae MT462037 INPA 7102 Brazil, Amazonas
Neacomys guianae MT462038 INPA 7100 Brazil, Amazonas
Neacomys jau KX792059 MNFS 2017 Brazil, Amazonas
Neacomys jau KX792060 MNFS 2023 Brazil, Amazonas
Neacomys jau KX792061 MNFS 2084 Brazil, Amazonas
Neacomys jau KX792062 MNFS 2104 Brazil, Amazonas
Neacomys jau MT462051 MPEG 45483 Brazil, Amazonas
Neacomys macedoruizi KY859731 MUSM 45054 Peru, Huánuco
Neacomys macedoruizi* KY859732 MUSM 45053 Peru, Huánuco
Neacomys marci sp. nov. Pending QCAZ 18677 Ecuador, Pichincha
Neacomys marci sp. nov. Pending MECN 5339 Ecuador, Carchi
Neacomys marci sp. nov. Pending MECN 5340 Ecuador, Carchi
Neacomys marci sp. nov. Pending MECN 7569 Ecuador, Esmeraldas
Neacomys marci sp. nov. Pending MECN 7564 Ecuador, Esmeraldas
Neacomys marci sp. nov. Pending MECN 7568 Ecuador, Esmeraldas
Neacomys tenuipes* KX792081 BM 1899.10.3.34 Colombia, Cundinamarca
Neacomys tenuipes MT536165 UIS-MHN-M 927 Colombia, Santander
Neacomys tenuipes MT536169 MHN-Uca 1627 Colombia, Caldas
Neacomys tenuipes MT536170 MHN-Uca 1628 Colombia, Caldas
Neacomys tenuipes MT543038 MPIII 32 Colombia, Antioquia
Neacomys tenuipes MT536171 MHN-UCa 1761 Colombia, Caldas
Neacomys tenuipes MT536166 UIS-MHN-M 1720 Colombia, Bolívar
Neacomys tenuipes MT536167 UIS-MHN-M 1723 Colombia, Bolívar
Neacomys tenuipes MT536168 UIS-MHN-M 1762 Colombia, Bolívar
Neacomys tenuipes MT543037 CTUA 2599 Colombia, Antioquia
Neacomys minutus s. s. KX792063 INPA 3047 Brazil, Amazonas
Neacomys minutus s. s. KX792065 INPA 3051 Brazil, Amazonas
Neacomys minutus s. s. KX792068 MVZ 190359 Brazil, Amazonas
Neacomys minutus s. s. KX792069 MVZ 190361 Brazil, Amazonas
Neacomys minutus s. s. KX792071 MVZ 190363 Brazil, Amazonas
Neacomys minutus s. s. KX792072 MVZ 191209 Brazil, Amazonas
Neacomys minutus s. s. KY859739 MVZ 190360 Brazil, Amazonas
Neacomys minutus s. s. KY859740 MNFS 1734 Brazil, Amazonas
Neacomys minutus s. s. KY859741 MNFS 1787 Brazil, Amazonas
Neacomys minutus s. s. MT462008 INPA 3048 Brazil, Amazonas
Neacomys minutus s. s. MT462009 INPA 3049 Brazil, Amazonas
Neacomys minutus s. s. MT462010 INPA 2689 Brazil, Amazonas
Neacomys musseri EU579503 AMNH 272676 Peru, Loreto
Neacomys musseri KX792074 MVZ 171487 Peru, Cusco
Neacomys musseri KX792076 AMNH 272687 Peru, Loreto
Neacomys musseri KX792077 KU 144300 Peru, Madre de Dios
Neacomys musseri KY754055 MVZ 193763 Brazil, Acre
Neacomys musseri KY859742 MVZ 171488 Peru, Cusco
Neacomys rosalindae KX792050 ROM 104560 Ecuador, Napo
Neacomys rosalindae KX792051 ROM 105265 Ecuador, Napo
Neacomys rosalindae KX792052 ROM 105314 Ecuador, Napo
Neacomys rosalindae KX792053 ROM 105315 Ecuador, Napo
Neacomys rosalindae KX792054 MVZ 153530 Perú, Amazonas
Neacomys rosalindae KX792055 KU 158172 Peru, Loreto
Neacomys rosalindae KX792056 TK 73307 Peru, Loreto
Neacomys rosalindae KX792057 TK 73347 Peru, Loreto
Neacomys rosalindae KX792058 TK 73493 Peru, Loreto
Neacomys rosalindae KY826416 MUSM 45717 Peru, Loreto
Neacomys rosalindae KY859730 MVZ 155299 Peru, Amazonas
Neacomys rosalindae KY859743 MUSM 45720 Peru, Loreto
Neacomys rosalindae KY859744 MUSM 45719 Peru, Loreto
Neacomys rosalindae KY859745 MUSM 45718 Peru, Loreto
Neacomys rosalindae KY859746 MUSM 45721 Peru, Loreto
Neacomys rosalindae KY859747 MUSM 45731 Peru, Loreto
Neacomys rosalindae KY859748 MUSM 45716 Peru, Loreto
Neacomys rosalindae KY859749 MUSM 45730 Peru, Loreto
Neacomys rosalindae KY859750 MUSM 45733 Peru, Loreto
Neacomys rosalindae KY859751 MUSM 45729 Peru, Loreto
Neacomys rosalindae KY859752 MUSM 45728 Peru, Loreto
Neacomys rosalindae KY859753 MUSM 45727 Peru, Loreto
Neacomys rosalindae KY859754 MUSM 45734 Peru, Loreto
Neacomys rosalindae KY859755 MUSM 44964 Peru, Loreto
Neacomys rosalindae KY859756 MUSM 44967 Peru, Loreto
Neacomys rosalindae KY859757 MUSM 44966 Peru, Loreto
Neacomys rosalindae KY859758 MUSM 44968 Peru, Loreto
Neacomys rosalindae KY859759 MUSM 44972 Peru, Loreto
Neacomys rosalindae KY859760 MUSM 44969 Peru, Loreto
Neacomys rosalindae KY859761 MUSM 44971 Peru, Loreto
Neacomys rosalindae* KY859762 MUSM 44963 Peru, Loreto
Neacomys rosalindae KY859763 VPT 4794 Peru, Loreto
login to comment