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Gross stomach morphology in akodontine (: : ): a reappraisal of its significance in a phylogenetic context

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Journal of Mammalogy, XX(X):1–23, 2020 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 DOI:10.1093/jmammal/gyaa023

Gross stomach morphology in akodontine rodents (Cricetidae: Sigmodontinae: Akodontini): a reappraisal of its significance in a phylogenetic context

Ulyses F. J. Pardiñas,*, Carola Cañón, Carlos A. Galliari, Jorge Brito , Nuria Bernal Hoverud, Gisele Lessa, and João Alves de Oliveira Instituto de Diversidad y Evolución Austral (IDEAus-CONICET), Boulevard Brown 2915, 9120 Puerto Madryn, Chubut, (UFJP, CC) Centro de Estudios Parasitológicos y de Vectores (CEPAVE, CONICET-UNLP), calle 120 entre 61 y 62, 1900 La Plata, Buenos Aires, Argentina (CAG) Instituto Nacional de Biodiversidad (INABIO), Rumipamba 341 y Av. de los Shyris, casilla: 17-07-8976, Quito, Ecuador (JB) Wildlife Conservation Society, Programa Bolivia, Casilla 3-35181, San Miguel, La Paz, Bolivia (NBH) Museu de Zoologia, Departamento de Biologia , Universidade Federal de Viçosa, 36571-000 Viçosa, Minas Gerais, Brasil (GL) Museu Nacional, UFRJ, Quinta da Boa Vista, Rio de Janeiro 20940-040, Brasil (JAO) * Correspondent: [email protected]

Akodontini, the second largest tribe within sigmodontine rodents, encompasses several stomach morphologies. This is striking because most sigmodontine groups of comparable taxonomic rank are very conservative in this respect. Based on extensive sampling of newly dissected specimens (213 stomachs representing 36 species), as well as published examples, covering almost all akodontine living genera (15 of 16), we undertook a reappraisal of the gross morphology of this organ. We then mapped this information, together with gallbladder occurrence, in a refined multilocus molecular phylogeny of the tribe. We surveyed three different configurations of stomachs in akodontines, according to the degree of development and location of the glandular epithelium; in addition, two minor variations of one of these types were described. Of the five major clades that integrate Akodontini, four are characterized by a single stomach morphology, while one clade exhibits two morphologies. Mapping stomach type on the phylogeny recovered two configurations for the most recent ancestor of Akodontini. A revised survey of gallbladder evidence also revealed overlooked congruencies. The observed stomach diversity and its arrangement in the phylogeny, along with additional morphological characters and the genetic diversity among the main clades, supports the necessity of changes in the current classification of the tribe. Recognition of subtribes or partitioning of Akodontini into several additional tribes of equal rank could be suitable options.

Key words: discoglandular, gallbladder, Scapteromyini, unilocular-hemiglandular

Akodontini, la segunda mayor tribu de los roedores sigmodontinos, presenta varias morfologías de estómago. Esto es extraño porque la mayor parte de los grupos comparables de sigmodontinos son muy conservadores en este aspecto. Sobre la base de una extensa muestra de nuevos especímenes diseccionados (213 estómagos representando 36 especies), como así también de ejemplos publicados, abarcando la casi totalidad de los géneros vivientes de akodontinos (15 de 16), efectuamos una re-evaluación de la anatomía gruesa de este órgano. Luego, mapeamos esta información, conjuntamente con la ocurrencia de vesícula biliar, en una filogenia molecular multilocus refinada para la tribu. Detectamos tres configuraciones diferentes de estómagos en akodontinos, de acuerdo con el grado de desarrollo y localización del epitelio glandular; adicionalmente, fueron descriptas dos variantes menores de estos tipos. De los cinco clados principales recobrados en Akodontini, cuatro están caracterizados por una única configuración de morfología del estómago y uno exhibe dos morfologías. Las reconstrucciones de los caracteres asociados al estómago sobre la filogenia concuerdan en recuperar dos

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configuraciones en el ancestro más reciente de Akodontini. Una revisión de la evidencia de la vesícula biliar también reveló congruencias hasta ahora inadvertidas. La diversidad estomacal observada y su disposición en la filogenia junto con otros caracteres morfológicos, más la diversidad genética entre los clados principales, sugieren la necesidad de cambios en la clasificación vigente de la tribu. El reconocimiento de subtribus o la partición de los Akodontini en varias unidades de rango tribal podrían ser opciones adecuadas.

Key words: Palabras clave, discoglandular, Scapteromyini, unilocular-hemiglandular, vesícula biliar

The gross morphology of the stomach was a substantive ele- histological techniques. We therefore discuss neither aspects ment in the classification of cricetid rodents during the 1960s of gland occurrences and distributions nor histochemical is- and 1970s. Vorontsov’s anatomical research of the digestive sues. Brief included notes about gastric arterial irrigation (inter- system (e.g., Vorontsov 1959, 1962, 1967, 1979, 1982) played preted according to Greene 1935:figure 246) are derived from a crucial role in the conformation of cricetid tribes (Vorontsov blood vessels that remained attached to the ectal surface of the 1959). However, despite extensive work by Carleton (1973, stomach, mainly when organs were examined in fresh speci- 1980, 1981), the relevance of the studies of stomach mor- mens. All studied materials (213 stomachs representing 36 spe- phology progressively fell by the wayside. Although data on cies) are listed in Appendix. For those taxa we could not directly gross stomach morphology frequently are included in phylo- study (i.e., , Kunsia, and Podoxymys), published genetic analyses (e.g., Steppan 1995; Weksler 2006; Pardiñas descriptions were followed (Carleton 1973; Bezerra et al. 2007; et al. 2015d), there is as yet no clear understanding about the and Emmons and Patton 2012, respectively), emended in some significance of its role, if any, in classificatory frameworks. instances through a reinterpretation of stomach anatomy based With respect to the cricetid subfamily Sigmodontinae, most of on the originally provided figures. the currently recognized 11 tribes contained therein are typified Anatomical terms employed in the present contribution are by a singular stomach morphology (Vorontsov 1967; Carleton those defined by Carleton (1973, 1980, 1981), with minor add- 1973). and Phyllotini, for example, two of the lar- itions according to Vorontsov (1967, 1979), Musser and Durden gest tribal assemblages, exhibit a single-chambered organ where (2002), and Langer (1985, 2017). Carleton (1973:10) recognized glandular and cornified epithelia are distributed more or less two main stomach configurations: unilocular-hemiglandular subequally (Carleton 1973; Weksler 2006). Even minor tribes stomachs (single-chambered organs with a shallow incisura (in number of genera) such as , Andinomyini, and angularis), and bilocular-discoglandular stomachs, in which Euneomyini, despite trenchant differences among their mem- the main cavity is partially divided by a deep incisura angularis bers in many respects, are conservative in stomach morphology “...imparting a more strongly-defined bipartite condition,” and (Pardiñas et al. 2015d; Salazar-Bravo et al. 2016; Teta et al. 2017). in which the glandular epithelium is restricted to the fundus However, akodontines encompass at least three main types of of the stomach or confined into a pouch (= diverticulum in stomach design judged on the basis of the extension and location Vorontsov 1967:figure 100; = glandular pouch in Musser and of the glandular epithelium (Vorontsov 1967; Carleton 1973). Durden 2002:figure 22). Although Carleton (1973:24) regarded Based on an extensive sample of newly dissected specimens the akodontine as a bilocular-discoglandular as well as previously published examples, we herein describe sigmodontine, he highlighted that the stomach in this , as the diversity of stomach morphologies in Akodontini. We then well as in and in the , is unilocular map these data on a molecular phylogeny to explore the dis- (Carleton 1973:25). To clarify this terminological issue, we re- tribution of stomach type variation observed throughout the stricted the use of the term bilocular for those stomachs in which tribe, and its potential agreement with the major clades re- the incisura angularis deeply dissects the main cavity. Under covered in the phylogeny. Based on this evidence, as well as this restriction, all akodontines studied thus far have unilocular additional data from occurrence of the gallbladder, diets, and stomachs, and several also show the discoglandular condition. the aforementioned molecular information, we argue the need To the best of our knowledge, there are no sigmodontines with for changes in the current classification of the tribe. a bilocular stomach sensu Carleton (1973). Langer (2017:204) supported this hypothesis, stating that “in Sigmodontinae, there is considerable variability in mucosal lining, but no separation Materials and Methods of gastric forms into a bilocular organ.” In parallel, we made an Gross stomach assessment.—Examined specimens (mostly extensive survey to explore the presence or absence of a gall- adults) consisted of fresh or fluid-preserved bodies from which bladder, examining fresh or fixed specimens, complemented with we removed viscera. were collected in accordance with pertinent literature (Voss 1991; Geise et al. 2004; Appendix). the guidelines of the American Society of Mammalogists (Sikes Phylogenetic analyses and character mapping.—Data on et al. 2016). Fresh or fixed infilled stomachs were photographed gross stomach morphology and gallbladder were mapped externally in ventral view, then dissected along the midsagittal on a molecular phylogeny of Akodontini combining five in- plane to expose the internal gross anatomy. Inspections were dependent loci, based on the data set of Salazar-Bravo et al. made by stereomicroscope magnification, focusing on the (2016). We extended the taxonomic and genetic coverage appearance of structures and epithelia, but not employing within Akodontini, adding sequences generated within the PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 3 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 framework of the doctoral dissertation of one of the authors with the highest AIC score was selected for inclusion in this (CC), and also retrieved additional sequences from GenBank study. In both analyses, we used the concatenated tree obtained (Supplementary Data SD1). Except for , the re- by ML and the morphological matrix above indicated. maining 15 genera of Akodontini were included. DNA sam- pling included the mitochondrial protein-coding Cytochrome b Results (Cytb) gene and four unlinked nuclear loci: exon 6 of the gene coding for the dentin matrix (DMP1), first exon of the nuclear Gross stomach anatomy.—We surveyed stomach gross mor- gene interphotoreceptor retinoid-binding protein (IRBP), exon phology in 15 of the 16 genera currently recognized in the tribe 10 of the growth hormone receptor (GHR), and the single exon Akodontini. All possess a single-chambered (i.e., unilocular) of the recombination activation 1 gene (RAG1). For each tip, stomach where two types of epithelia, cornified and glandular, nucleotide sequences were gathered from a single specimen can be detected; this type is therefore known hemiglandular. or species; however, composite tips were constructed in some Overall, the incisura angularis is shallow and scarcely extends instances. In the concatenated matrix, for those tips with in- beyond the esophageal opening. complete loci, we used the ambiguous state character “n.” We Three main types of gross stomach morphology: Types A, B, considered taxa/individuals that had at least two genes repre- and C.—Type A is a classic unilocular-hemiglandular stomach: sented from the five employed in this study. DNA sequence cornified and glandular epithelium lines the internal walls of edition and alignment were carried out with CodonCode the stomach in approximate correspondence with the corpus Aligner (CodonCode, Dedham, Massachusetts), and ClustalX and antrum, respectively; both types of epithelia are separated 2.0 (Larkin et al. 2007), respectively. The combined DNA data by a flap termed a bordering fold that imparts to the stomach, set was subjected to phylogenetic analysis using a maximum when viewed from inside, a more or less equally 2-chambered likelihood (ML) approach (Felsenstein 1981) and Bayesian morphology (Fig. 1). Two variants can be associated with Inference (BI—Huelsenbeck et al. 2001) with the partition this configuration. Subtype ′A is a unilocular-hemiglandular scheme identified by PartitionFinder (Lanfear et al. 2012). The stomach with slightly reduced glandular epithelium (called ML tree was inferred using IQ-TREE version 1.6.0 software “subhemiglandular” following Langer 2017:figure 4.82). (Nguyen et al. 2015) implemented in the IQ-TREE web server Similar to Type A in general appearance, the glandular epithe- (Trifinopoulos et al. 2016) using LG+I+G4 substitution as the lium is in this configuration more clearly restricted to the an- best-fit model. Statistical support for individual nodes of the trum, departing from the “equally 2-chambered” morphology. ML phylogenetic tree was estimated using the ultrafast boot- Subtype A″ implies the opposite condition, in which the glan- strap value (1,000 iterations). For BI analysis, we performed dular epithelium slightly advances to the left, producing a more two independent runs, each consisting of 107 iterations where reduced coverage of the cornified epithelium over the corpus. chains were sampled every 1,000 generations. To assess con- Type B is a unilocular-discoglandular stomach: corpus and vergence, we plotted the log-likelihood values against genera- antrum mostly lined by cornified epithelium but showing tion time for each run in Tracer v.1.5 (Rambaut and Drummond distinct textures and separated by a false bordering fold (see 2009). The first 25% of the trees obtained were discarded as “Discussion”); glandular epithelium restricted to a circular burn-in, and the remaining trees were used to construct a ma- well-marked zone placed on the fundus of the stomach and cir- jority rule consensus tree and to obtain the support for each cled by the bordering fold; glandular zone continuous with the clade as posterior probability values. The phylogenetic con- main lumen of the stomach. sensus trees were visualized using the FigTree software v.1.4.2 Type C is a unilocular-diverticular stomach (following (Rambaut 2014); for the focus of our study, each genus-level Langer 2017:figure 4.82): corpus and antrum lined by cornified clade was collapsed, yielding intergeneric relationships only. epithelium without a false bordering fold; glandular epithelium To provide a hypothesis regarding the evolution of the occurs only in an almost closed diverticulum (or pouch) situ- stomach and gallbladder characters in Akodontini, we con- ated on the greater curvature about opposite the esophageal or- structed a morphological matrix composed of the following ifice. This pouch is lined with a thick glandular mucosa and characters: i) stomach type (according to the typification es- connects with the main cavity of the stomach through an orifice tablished below), and the absence or presence of ii) bordering placed to the left (and therefore pointing to the corpus); bor- fold (see “Discussion”), iii) pouch or diverticulum, and iv) dering fold absent. gallbladder (Supplementary Data SD2). To evaluate changes in stomach and gallbladder characteristics across the molec- Reappraisal of Stomach Morphology for Akodontine Genera ular phylogeny, we employed two approaches. First, we used Akodon.—Approximately 40 species currently are regarded parsimony-based optimization in Mesquite software v.3.10 as valid within this genus, the largest of the tribe (Pardiñas (Maddison and Maddison 2011) with the Fitch (1971) parsi- et al. 2015b). Stomach morphology was described by Carleton mony model. Under this model, the multistate character states (1973; including: A. aerosus, A. azarae, A. boliviensis, are unordered and can transform directly to each other and back A. cursor, A. dayi, A. mimus, and A. montensis), Vorontsov again. The second approach was conducted using the software (1979; A. azarae), Dorst (1973; A. boliviensis), Myers et al. RASP v.4.1 (Reconstruct Ancestral State in Phylogenies—Yu (1990; several members of the boliviensis group of Akodon); et al. 2015), performed under the Auto Run option; the model Myers and Patton (1989; Akodon siberiae), Rouaux et al. (2003; 4 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 1.—Main types of stomach configurations figured as internal views in conventional anatomical position, exemplified by Akodon mollis (Type A; JBM 2172); labiosus (Type A, Subtype A′; MZUFV 4465); Deltamys kempi (Type A, Subtype A″; CNP 5756); Scapteromys aquaticus (Type B; CNP 6409); and iheringi (Type C; CNP 1933). Anatomical features indicated are: an, antrum; b, bordering fold; ce, cornified epithelium; co, corpus; d, duodenum; di, diverticulum (or pouch); e, esophagus; eo, esophageal opening; fb, false bordering fold; fv, fornix ventricularis; ge, glandular epithelium; m, muscular wall; o, ostium; pa, pars pylorica; py, pylorus; r, rugae. Main incisures (= plicas) are indicated by yellow arrows, clockwise, praepylorica, angularis, and cardialis.

A. azarae), and Finotti et al. (2012; A. cursor). Illustrated stom- dissections added specimens representing main groups of spe- achs for the genus are restricted to schematic drawings provided cies recognized in the genus (Smith and Patton 2007; Jayat et al. by Vorontsov (1962, 1967; A. azarae; Supplementary Data 2010; Coyner et al. 2013), including A. aerosus, A. albiventer, SD3) and a photograph by Finotti et al. (2012; A. cursor). Our A. azarae, A. budini, A. cursor, A. dayi, A. dolores A. iniscatus, PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 5 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

A. mimus, A. mollis, A. montensis, A. philipmyersi, A. polopi, a false bordering fold, as there is no division in the nature of the A. simulator, A. spegazzinii, and A. toba. Data from literature in intervening epithelia. A large pars pylorica area has thick mus- addition to our study therefore include approximately 50% of the cular walls and occupies almost half of the antrum. The pouch generic diversity. The single stomach morphology so far docu- also is impressive because it is completely surrounded by broad mented in Akodon corresponds to Type A; no obvious differences walls that almost obliterate the lumen; it connects the main cavity were found among the examined species (Figs. 2A–J; Finotti through an aperture that opens to the corpus. A freshly dead spec- et al. 2012:figure 1). Teta et al. (2007:45) reported that “the bor- imen showed that the sanguineous irrigation of the diverticulum is dering fold is nearly semicircular in Deltamys and some Akodon mostly from the gastroepiploic artery (Supplementary Data SD5). species (e. g., ) or straight as in some members of Brucepattersonius.—This poorly studied genus had its the A. boliviensis group (Myers et al., 1990).” However, we sus- stomach morphology described and illustrated by Hershkovitz pect that what those authors interpreted as specific features more (1998:230, figure 20; Brucepattersonius griserufescens). probably are artifacts and subtle differences produced by the de- We added observations based on seven specimens referred gree of expansion of the stomach, especially the corpus and an- to Brucepattersonius iheringi, thereby including two of the trum, when the structure was fixed. The specimens of A. azarae four species currently recognized in the genus (Pardiñas et al. we examined did not display a “semicircular” borderline, but a 2017a; Abreu-Júnior and Percequillo 2019). Stomach mor- “straight” one (Fig. 2D). Notwithstanding, a subadult A. iniscatus phology corresponds to Type C (Figs. 2P–T). A moderately without a fully extended antrum had a “semilunar” limit between spongy corpus is delimited from a thick-walled antrum by an the glandular and muscular epithelia (Fig. 2F). Minor differences almost imperceptible false bordering fold. Glandular epithe- were noted with respect to the thickness of the glandular epithe- lium is restricted to a pouch, well-expressed when the stomach lium, judged from the wall exposition when the antrum was trans- is viewed externally, connected to the main lumen by a minute versally sectioned. Akodon mimus, for example (Fig. 2H), shows orifice. Hershkovitz (1998:figure 20) indicated the occurrence a remarkably thickened antrum, internally lined by a rugged sur- of a bordering fold as an imprecise division between the pouch face, contrasting with the condition displayed by the antrum in and the main cavity of the stomach. To our understanding, Type A. azarae, in which walls are thin and the internal surface smooth. C stomachs lack a bordering fold because the glandular epithe- In several species, we noted the persistence of circulatory system lium is not in contact with the cornified epithelium. remains, independent from the quality of preservation of the spec- Castoria.—Stomach morphology of this monotypic genus, imen. In particular, Akodon spp. showed the left gastric artery based on a single specimen studied by Pardiñas et al. (2016:105, usually divided in two main branches at the level of the center supplementary figure 5), corresponds to Type A (Figs. 3A and of the organ, one of them running along the anatomical limit be- 3B). The corpus is slightly larger than the antrum due to a tween corpus and antrum (Supplementary Data SD4). moderately developed fornix ventricularis. The bordering fold Bibimys.—Stomach morphology for this genus was de- bisects the stomach on a straight line from near the incisura scribed by Gonçalves et al. (2005:126; for B. labiosus) and angularis to a point opposite to it on the greater curvature. Both described and illustrated by Pardiñas et al. (2017b:246, sup- the incisura angularis and the incisura praepylorica are well- plementary figure 2; for B. chacoensis). Herein we added marked, defining a narrow prepyloric section. specimens of B. labiosus, thereby including two of the three Deltamys.—The stomach of Deltamys kempi was described species recognized in the genus (Pardiñas et al. 2015a). The and illustrated by Teta et al. (2007:45, figure 1); we studied single stomach morphology found in Bibimys corresponds to seven specimens of the same species, one of three included Type A, Subtype A′ (Figs. 2K–M). A large corpus lined by thin in the genus (Quintela et al. 2017). Stomach morphology cor- cornified epithelium visually contrasts with a small antrum, responds to Type A (Figs. 3C and 3D), with a weak but per- both regions separated by a thin bordering fold. Corpus ental ceptible tendency to Subtype A″. In several of the dissected surface is moderately spongy. Glandular epithelium covers specimens, the bordering fold is slightly displaced to the left of the antrum appearing restricted to the right of the esophageal the esophageal opening, producing a more limited extension of opening, a feature expressed externally by a differential colora- the cornified epithelium in the antrum. According toTeta et al. tion of the organ, which also corresponds to the wider walls of (2007:45), D. kempi has a “nearly semicircular” bordering fold, the stomach in this portion. Two well-marked incisures define a a condition that we did not record in our study. pars pylorica characterized by a convolute ental surface. Gyldenstolpia.—There is no information about this genus, Blarinomys.—The stomach of B. breviceps, the single species which is lacking either preserved fluid material in collections currently recognized in the genus, was described and illustrated or published information on soft anatomy. Based on the overall by Geise et al. (2008:figure 7; seeTeta and Pardiñas 2015:209) craniodental similarity among Gyldenstolpia, Kunsia, and based on one individual; we dissected 22 specimens. Stomach Scapteromys (Pardiñas et al. 2009), our hypothesis is that the morphology corresponds to Type C (Figs. 2N and 2O). This organ stomach configuration of the former will be of Type B or C. is impressive in its well-developed corpus and antrum, both with Juscelinomys.—The stomach was described and illus- spongy appearance, the glandular epithelium being confined to a trated by Emmons and Patton (2012:288, figure 4) based caudal pouch. The division between corpus and antrum is marked on Juscelinomys huanchacae, one of the two species in this by a smooth shift in the direction and texture of the cornified genus (Emmons 2015). The fluid-preserved material, housed rugae. In some individuals, the division is concealed by a ridge at the Museo de Historia Natural “Noel Kempff Mercado,” with the appearance of a typical bordering fold. However, it is was lost (K. Rivero: pers. comm. to U. F. J. Pardiñas, January 6 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 2.—Stomach morphology (when paired, ventral external and internal views, respectively; otherwise as noted) in members of the Akodontini: A, B: (JBM 1963); C, D: Akodon azarae (CG 948); E: (internal view; CML 11110); F: Akodon iniscatus (internal view; CNP 6410); G: oenos (internal view; CNP 6334); H: Akodon mimus (internal view; NBH 762-2016); I, J: Akodon mollis (MECN 5679); K, L: (CNP 1891); M: (internal view; MZUFV 4470); N, O: Blarinomys breviceps (MZUFV 4451); P, Q, R: Brucepattersonius iheringi (external, internal with content, internal without content; CNP 5507); S, T: B. iheringi (CNP 1932). All figures scaled to an approximate equal size.

2017); an internal view of the stomach was not illustrated by The stomach is of the bilocular-discoglandular type Emmons and Patton (2012). Emmons and Patton (2012:288) (Carleton 1973), with a thick discoid glandular pouch describe that, positioned below and on the side of the antrum… The PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 7 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 3.—Stomach morphology (when paired, ventral external and internal views, respectively; otherwise as noted) in members of the Akodontini: A, B: Castoria angustidens (CNP 449); C, D: Deltamys kempi (CNP 5756); E, F: Lenoxus apicalis (NBH 753-2016); G, H: amoenus (NBH 42-2015); I, J: Necromys lasiurus (CNP 4727); K, L: N. lasiurus (CNP 5244); M, N: N. obscurus scagliarum (CNP 6035); O, P: N. lasiurus temchuki (CG 752); Q: N. lactens (internal view; CML 11485); R: N. urichi (internal view; MACN 188); S, T: Oxymycterus hiska (NBH 13-2015). All figures scaled by row to an approximate equal size.

glandular pouch has a large, thin “bordering fold” The ostium appears to have a ring of muscle around (Carleton 1973) covering most of the area above the the opening. pouch in the antrum. A small circular ostium opens into the antrum, similar to that figured by Bezerra et al. Beyond what we consider to be an incorrect reference to a (2007:8) for Kunsia tomentosus (Lichtenstein, 1830). “bilocular” type (see “Materials and Methods”), the description 8 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 clearly fits a Type C stomach as defined herein. In addition, 1969:24), Carleton (1973; O. quaestor, O. rufus), and summar- the ostium does not open to the antrum, but into the corpus ized by Hershkovitz (1994:7–11). We examined specimens of (Bezerra et al. 2007:figure 2). five species (O. hiska [n = 1]; O. quaestor [n = 2; under the nom- Kunsia.—The stomach was described and illustrated by inal form O. misionalis]; O. nigrifrons [n = 1]; O. paramensis Bezerra et al. (2007:7, figure 2) based on K. tomentosus, the [n = 6]; and O. rufus [n = 5]), although only minimally covering single species recognized in the genus. Its morphology fits the noteworthy richness of this genus (Oliveira and Gonçalves Type C. The main cavity of this sacciform stomach is lined by 2015; Peçanha et al. 2019). Stomach morphology detected in cornified epithelium; corpus and antrum are subequal in size Oxymycterus conforms with Type C (Figs. 3S, 3T, and 4A–I). and delimited by a false bordering fold, which runs from a point Compared with other Type C genera, the glandular pouch looks slightly to the right of the esophageal opening to contact the smaller and the cornified epithelium surface smoother, less posterior wall of the stomach. The glandular epithelium is con- textured, and almost lacking a perceptible anatomical limit be- fined to a basal pouch that connects to the main cavity through tween corpus and antrum. When fully expanded, the stomach a minute orifice opening to the corpus. The antrum is anteriorly acquires a sacciform appearance (Figs. 4A–C). enlarged in a prepyloric sector well-differentiated by a shallow Podoxymys.—The stomach of the single recognized spe- incisura praepylorica and is lined anteriorly–posteriorly. cies, P. roraimae, was described and illustrated by Carleton Lenoxus.—For this monotypic genus, stomach morphology (1973:15, figure 5A), as “…unilocular but departs somewhat was described by Patton (2015:231): “Lenoxus [apicalis] pos- from a hemiglandular pattern. The bordering fold intersects sesses a unilocular-discoglandular stomach, with the glandular the lesser curvature at a point midway between the incisura epithelium confined to a diverticulum located on the greater angularis and pylorus. Consequently, some cornified epithe- curvature.” Our dissections reinforce Patton’s observation, the lium occupies the part of the antrum to the right of the esoph- stomach corresponding to Type C (Figs. 3E and 3F). Ental ap- ageal opening.” This description fits with stomach Type A, pearance is dominated by strongly muscular walls of the main Subtype A′ as herein defined. cavity, where the identity of the corpus is mostly produced by a Scapteromys.—The stomach morphology was described for convoluted fornix ventricularis. There is no perceptible anatom- the three species currently recognized in the genus (Carleton ical limit between corpus and antrum beyond the distinct direc- 1973; Quintela et al. 2014). We inspected 10 specimens of tion of the rugae, extensively lining both surfaces. The pouch S. aquaticus. The stomach in Scapteromys conforms with Type enclosing the glandular epithelium is comparatively large, B (Figs. 4J–L and 5A–C). This configuration is characterized encircled by thick secretive walls with an opening “channel” by a restriction of the glandular epithelium to the fundic por- directed to the left. A broad prepyloric region is well-marked tion of the stomach and the coexistence both of false and true by a shallow plica praepylorica and a plica located near the bordering folds. The former is a thick cordon that conceals the right limit of the pouch. In some individuals (NBH 1329, NBH limit between corpus and antrum, running from a point located 2017) the prepyloric region is marked by a perceptible ridge immediately to the right of the esophageal opening. The true running between the two mentioned incisures. Whether or not bordering fold encircles the fundus of the stomach where the this region is homologous with the antrum in Lenoxus deserves glandular epithelium is limited. Both folds contact perpendic- further scrutiny. ularly. Although somewhat dependent on ontogenetic stage, Necromys.—This genus was studied by Carleton (1973; the walls of the glandular portion generally are thicker overall. N. lasiurus and N. obscurus) and Dorst (1973; N. amoenus); When the stomach is not totally distended, its external appear- there nevertheless is a lack of published figures to document ance resembles stomachs of Type C, an impression also pro- the morphology of the stomach in this speciose genus (Pardiñas vided by the plicas located at both sides of the fundus (Fig. 4J). et al. 2015c). Descriptions provided herein are based on our dis- .—There are no previously published data on the sected specimens belonging to N. amoenus (n = 2), N. lactens soft anatomy of this genus with two species (Pardiñas and Teta (n = 4), N. lasiurus (including specimens of the nominal forms 2015). Based on fluid-preserved specimens of T. cerradensis N. benefactus [n = 7] and N. temchuki [n = 7]), N. obscurus (n = 2), the stomach can be referred to Type A (Figs. 4D and (n = 6), and N. urichi (n = 1). Basic morphology of the stomach 4E). The corpus is characterized by thin walls and is lined by fits Type A (Figs. 3G–R), with a slight but obvious tendency regularly folded (“plicated”) cornified epithelium; the antrum of the glandular epithelium to invade the corpus (Subtype A″). is internally smooth and thin-walled. The latter is reflected by the position occupied by the bordering Thaptomys.—Briefly characterized as “…hemiglandular- fold, displaced to the right of the esophageal opening. This ten- unilocular, with a reduced glandular area” (Teta et al. 2015:277), dency is more clearly expressed in N. obscurus (Fig. 3N), but we provide an emended description of the stomach in this mon- also evident in several samples of N. lasiurus. In addition, the otypic genus based on 12 dissected specimens. The stomach bordering fold resembles a thick junction (N. urichi; Fig. 3R), morphology detected in Thaptomys nigrita conforms to Type although the corpus coat can be moderately thin. A (Figs. 5F–J). The stomach is sacciform but the corpus can be Oxymycterus.—First described more than a century ago greatly expanded, projecting the fornix ventricularis well be- (Tullberg 1899), morphology of the stomach in Oxymycterus yond the esophageal opening. A straight bordering fold equally was extensively studied by Vorontsov (1962, 1967, 1979; based bisects the stomach from a point immediately to the right of the on O. nasutus [as O. rufus]; Supplementary Data SD3; Barlow esophagus; therefore, it lacks a reduced glandular portion. The PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 9 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 4.—Stomach morphology (when paired, ventral external and internal views, respectively; otherwise as noted) in members of the Akodontini: A, B, C: Oxymycterus quaestor (external, internal with content, internal without content; CG 817); D, E: O. nigrifrons (NBH 27-2015); F, G: O. paramensis jacentior (NBH 165-2015); H, I: O. rufus (CNP 6308); J, K: Scapteromys aquaticus (CNP 6405); L: S. aquaticus (internal view; CNP 6409). All figures scaled to an approximate equal size. corpus is lined by plicated, superficially spongy (in juvenile) to Akodontini is typified by its high degree of gallbladder var- smooth (in adults) cornified epithelium. The antrum is covered iability, including intrapopulational (e.g., Bibimys labiosus), by smooth glandular epithelium; the prepyloric region is well- interpopulational (e.g., Necromys lasiurus, Oxymycterus defined but lacks differential features. dasytrichus), intrageneric (e.g., Akodon montensis within Akodon), and intergeneric variation (Supplementary Data Gallbladder Occurrence SD6; see also Fig. 6). Of the 14 genera of Akodontini with Combining published data (Voss 1991; Geise et al. 2004) as gallbladder information (no data for Juscelinomys and well as evidence from newly dissected animals (Appendix), Gyldenstolpia), six have the organ (Castoria, Deltamys, 10 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 5.—Stomach morphology (when paired, ventral external and internal views, respectively; otherwise as noted) in members of the Akodontini: A, B, C: Scapteromys aquaticus (external fresh, external fixed, and internal views; CG 853); D, E: Thalpomys cerradensis (MN 75703); F, G: Thaptomys nigrita (CG 828); H, I: T. nigrita (juvenile; LTU 859); J: T. nigrita (internal view of an old adult; CG 841). All figures scaled by row to an approximate equal size.

Kunsia, Podoxymys, Scapteromys, and Thalpomys), three lack it of Brazilian populations lacking the gallbladder as reported by (Blarinomys, Brucepattersonius, and Lenoxus), and the remaining Geise et al. (2004:211) cannot be ruled out, although we suspect five genera show either presence or absence (Akodon, Bibimys, it could be another instance of misidentification of this organ due Necromys, Oxymycterus, and Thaptomys; Table 1). Of the 17 spe- to its small size. cies of Akodon examined, only A. montensis consistently lacked a gallbladder (Pardiñas et al. 2003; Geise et al. 2004). Specimens Stomach Morphologies and Gallbladder Occurrence Mapped with or without a gallbladder have been reported for B. chacoensis, on Akodontini Phylogeny B. labiosus, O. dasytrichus, N. lasiurus, and T. nigrita. We dis- Five major clades were retrieved from the enriched molecular- sected three specimens of B. labiosus from Mata do Paraíso based phylogeny constructed for this study; these groups were (Minas Gerais, Brasil). These lacked a gallbladder, although labeled 1 through 5 (Fig. 6). Group 1, including the genera two animals from the same population previously were reported Akodon, Deltamys, Castoria, Necromys, Thalpomys, Thaptomys, as having this organ (Gonçalves et al. 2005). In addition, for the and Podoxymys, displays stomach Type A. Group 2, sister to specimen of B. chacoensis that we previously reported as possibly group 1 and formed by Juscelinomys and Oxymycterus, have having a gallbladder (Pardiñas et al. 2017b), we now conclude that stomach Type C. The same is true for group 3, sister to {1 + 2}, our observation was erroneous. To the best of our understanding, as the genera Blarinomys, Brucepattersonius, and Lenoxus, both species of Bibimys have well-developed mesenteric tissues at also have Type C stomachs. Group 4, sister to {3 {1 + 2}} and the liver level that could be confounded with a small gallbladder in including Kunsia and Scapteromys, encompasses stomachs of poorly fixed material (Supplementary Data SD7). For T. nigrita, all Type C and B, respectively. Finally, group 5, Bibimys, is re- specimens examined from Misiones (Argentina; n = 11) revealed trieved as sister to {4 {3 {2 − 1}}}, and has stomach Type A, minute gallbladders (Supplementary Data SD8). The possibility Subtype A′. In summary, the correlation between clades and PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 11 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 6.—Summary of the Akodontini diversity in stomach morphology, gallbladder occurrence, and diet. The phylogenetic framework is a molecular-based tree; numbers for each node are bootstrap and posterior probabilities support values, respectively. Principal clades recognized are indicated by encircled numbers 1–5. Gallbladder is mapped as green (present), red (absent), or both. Diet is depicted as indications of important food items (arthropods, , green material, and fruits/seeds). Each rectangle represents ca. 25% (data summarized from Supplementary Data SD11). gross stomach morphologies is almost perfect except for group of Type A, A′, or C, lacking a pouch, with bordering fold 4, in which two configurations coexist. present, and with or without a gallbladder. The results of the The reconstructions yielded no major conflicts between both RASP analysis for the same node recovered wider results for analytic approaches used except for a few nodes (Fig. 7). Our the characters related to the diverticulum, bordering fold, and character mapping based on parsimony reconstruction illus- gallbladder. In the latter analysis, the ancestor’s stomach type trates the ancestral states for the Akodontini possess stomachs could be of Type A′ or C, the pouch could be present or absent 12 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Table 1.—Distribution of the gallbladder among akodontine genera angularis, sometimes coupled with a sulcus on the greater cur- (compiled from several sources; see Supplementary Data SD6). vature, confers a bicameral appearance to the stomach (in Genus Gallbladder Remarks Cricetus—Carleton 1973:11). Akodontines that have been examined never have a noticeable incisura angularis, beyond Akodon Present or absent Absence recorded in one species (A. montensis) that the fundus of this plica clearly surpasses the level of the Bibimys Present or absent Probably absent gastroesophageal junction (Fig. 8A). (see the main text) The corpus typically is crossed by lines denoting folding Blarinomys Absent or plication which allows the distension of the stomach when Brucepattersonius Absent Castoria Present full. Plication is visible internally and externally, but its de- Deltamys Present gree of expression varies greatly, from almost nonexistent in Gyldenstolpia ? Kunsia or Oxymycterus, to well-marked in Akodon, Bibimys, or Juscelinomys ? Kunsia Present Thaptomys (Fig. 8B). The thin-walled corpus is lined by strati- Lenoxus Absent fied squamous epithelium in some murids (Walters et al. 2014) Necromys Present or absent Absence recorded in some and the same probably is true for akodontines. In several mem- N. lasiurus samples bers of the tribe, the internal surface of the corpus is character- Oxymycterus Present or absent Absence recorded in some O. dasytrichus samples ized by well-developed and extensively distributed longitudinal Podoxymys Present rugae (in Scapteromys; Fig. 8C) or convoluted spongy-like Scapteromys Present rugae (“horns”) concentrated in the fornix ventricularis (in Thalpomys Present Thaptomys Present or absent Probably absent (see the main text) Blarinomys; Fig. 8D). This kind of substratum is associated with the digestion of starch and/or glycogen (Carleton 1973). A mostly unstudied portion of the stomach in sigmodontines (occurrence: 50% absence, 50% absence/presence), a similar is the pars pylorica or prepyloric section (pyloric pouch of result for the bordering fold (50% presence, 50% absence/pres- Dearden 1969), i.e., the portion of the antrum immediately an- ence), and the gallbladder present. Most of the ancestral states terior to the pylorus (Vorontsov 1967:figure 97). This results of the tribe’s nodes agree between the two analyses. The main from most sigmodontines lacking unequivocal differentiation difference resides in the reconstruction of gallbladder history in of the pars pylorica, in contrast with the almost 3-chambered the nodes that group clades 1 and 2 and the node that groups all condition (i.e., pars pylorica, antrum, and corpus) of several genera except Bibimys. arvicolines, cricetines, and neotomines (Vorontsov 1967, 1982; Carleton 1973, 1981). However, this gastric feature is moder- Genetic Distances ately expressed in some akodontines and usually marked with Intrageneric Cytb divergence values slightly surpass 10% for two plicae (several species of Akodon, Brucepattersonius, two speciose genera (Akodon and Necromys), but also was im- Scapteromys). The pars pylorica can express thickened mus- portant (> 5%) for several paucispecific taxa (e.g., Blarinomys, cular walls (Fig. 1) and a noticeable change in the design of the Deltamys). The latter values make a sharp contrast with respect squamous epithelium (Fig. 8E). to those of other poorly speciose genera, such as Bibimys or The bordering fold (= borderline fold sensu Vorontsov Thaptomys, and suggest a broad array of evolutionary his- 1967:figure 100; “limiting ridge” sensu Luciano and Reale tories. The intergeneric comparison yields deep divergence 1992; grenzfalte or corpopyloric fold, according to Perrin and values between the genera of groups 3 (including Blarinomys, Kokkinn 1986; or mucosal lining sensu Langer 2017) was de- Brucepattersonius, and Lenoxus; > 13.5%), 4 (Kunsia and scribed as “a pronounced ridge that marks the juncture of the Scapteromys; > 15.5%), and 5 (Bibimys; > 15%), and the re- two types of gastric mucosa (cornified squamous epithelium maining akodontines (groups 1 and 2). Similarly, the results and glandular epithelium) lining the internal surface of the show profound differences among the main groups, where the stomach” (Carleton 1973:10). All the genera with stomach Type maximum value is reached by the comparison between clades 1 A have a definite classic bordering fold, which roughly coin- and 4, followed by 2 and 4, and clades 1 and 5 (Supplementary cides with the anatomical limit between the corpus and the an- Data SD9). trum. By definition, those taxa where the glandular epithelium is restricted to a pouch lack a bordering fold, simply because both types of gastric mucosa are not in contact (Fig. 8G). Our Discussion dissections failed to detect any kind of bordering fold such as Stomach anatomical traits.—Carleton (1973) focused at- those illustrated as present in B. griserufescens by Hershkovitz tention on the development of the incisura angularis, a fea- (1998:figure 20B). However, the indication made by Geise ture almost unmentioned in the present contribution. Almost et al. (2008:figure 7) of a “bordering fold” crossing the stomach all studied sigmodontines are characterized by a shallow in- of Blarinomys perpendicularly deserves attention in connection cisura angularis, a condition also shared by tylomyines and with our findings. As Blarinomys has a Type C stomach, the strongly departing from that in remaining cricetid subfamilies bordering fold is absent by definition, but a perceptible ana- (Toepfer 1891; Tullberg 1899; Vorontsov 1967, 1979, 1982; tomical ridge crosses the cornified epithelium in some indi- Carleton 1973, 1980, 1981). A major penetration of the incisura viduals. The same condition is observed in some, but not all, PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 13 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 7.—Parsimony ancestral character state reconstruction of stomach configuration, selected anatomical traits, and gallbladder occurrence, in the tribe Akodontini, carried out in Mesquite (A) and RASP (B). Squares to the right of the phylogeny indicate current character state(s) observed in the genera; circles associated with the clades show the reconstruction of the ancestral state for each node. Types and subtypes of stomachs are A, A′, A″, B, and C (see main text for definitions); red = absent; green = present.

Type C genera (e.g., Kunsia) and also in Scapteromys, which always opening into the corpus (Figs. 8G–I). It has been noted has a Type B stomach. The latter deserves a further comment that “the ostium appears to have a ring of muscle around the regarding this structure, which is clearly marked, thick, and opening” (Emmons and Patton 2012:288; for Juscelinomys). convoluted, giving a bipartite appearance to the stomach from Our dissections reveal nothing similar to a muscular sphincter its ectal surface (Supplementary Data SD10). The described there. However, given that minutely triturated macroscopic ridges or folds are prima facie not separating types of stomach food particles apparently have never been observed in the di- mucosae, but in the instance of Scapteromys the textural change verticulum, some kind of closing mechanism seems necessary. side by side of the stomach ental surface is notable (Fig. 8F). Inspected from the main stomach cavity, the opening appears as We term this ridge a false bordering fold, in an attempt to dif- a pore surrounded by squamous epithelium (Fig. 8H). It differs ferentiate its nature from the classic (or true) bordering fold from the condition described for the neotomine Onychomys, (Fig. 8F). The false bordering fold probably is an expression of where the aperture is larger and located in the center of the roof the anatomical limit between corpus and antrum in Type B or C of the pouch (Horner et al. 1965; Vorontsov 1967). stomachs. We are uncertain as to whether false bordering folds The few observations collected on the gastric circulatory are homologous among the several taxa examined. Luciano system suggest that a well-branched left gastric artery charac- and Reale (1992) indicated that the peculiar histological ar- terize several of the members of the group with Type A stom- chitecture of the bordering fold in and the presence of achs (e.g., Akodon, Thaptomys). This artery has a main vessel numerous brush cells suggest that this structure not only rep- running approximately at the anatomical limit between corpus resents the transitional zone between two types of epithelia but and antrum, but expresses several subdivisions to irrigate the that it might have a more specific function. Nevertheless, as walls of the latter. In contrast to this condition, at least one Langer (2017:204) pointed out, “In Sigmodontinae, there is member with stomach Type C (Oxymycterus) shows the left considerable variability in mucosal lining (= bordering fold), gastric artery mostly as a unique branch directed to the pouch but no separation of gastric form into a bilocular organ.” (Supplementary Data SD4). The pouch wherein glandular epithelium is confined in stom- Stomach morphology diversity within the sigmodontines.— achs of Type C has received considerable attention relative to Combining previous findings and those reported herein we other minimally studied gastric anatomical traits (Vorontsov determined that three types—one with two subtypes—of 1967, 1979, 1982; Carleton 1973). All the genera studied with stomach gross morphology are present in the Akodontini, a glandular pouch have secretive walls of uniform thickness based on examination of 15 of its 16 genera. As such, this is (Figs. 8G and 8I). The pocket lumen usually is collapsed in the sigmodontine tribe with the broadest diversity of stomach fixed specimens, except those in those of larger-bodied species morphologies reported to date. Akodontine members share (e.g., Lenoxus apicalis, Oxymycterus judex); Blarinomys is an with many sigmodontines the widespread “unilocular- exception (Fig. 8G). In Type C stomachs, a small or minus- hemiglandular” condition (sensu Carleton 1973), here re- cule aperture typically connects the pouch with the main cavity, ferred to as Type A. We observed two additional stomach 14 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Fig. 8.—Stomach anatomical details in the Akodontini, illustrated as internal views in conventional anatomical position (otherwise, as noted). A: Esophageal opening region in N. obscurus (CNP 6030; reversed); B: corpus ental surface in B. labiosus (MZUFV 4465); C: corpus ental surface in S. aquaticus (CNP 6405); D: fornix ventricularis ental surface in B. breviceps (MZUFV 4463); E: pars pylorica ental surface in S. aquaticus (CNP 6405); F: fundus region in S. aquaticus (CNP 6409); G: pouch (or diverticulum) in B. breviceps (MZUFV 4463; reversed); H: fundus in B. breviceps (MZUFV 4463; partially dorsal view, reversed; scale = 1 mm); I: right corner of the diverticulum in B. iheringi (CNP 1933). For the reference of anatomical features indicated, see Fig. 1; others employed are: a, incisura angularis; c, incisura cardialis; fd, fold; y, incisura praepylorica. PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 15 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 configurations, termed here Types B and C. The former is ex- (Reeder et al. 2006; Bradley et al. 2007; Miller and Engstrom clusive to Scapteromys, including a unique structure in stomach 2008; Platt et al. 2015). has a single unilocular- anatomy herein called a false bordering fold. The latter con- hemiglandular morphology (Carleton 1973), but there is figuration is present in at least six genera, also incorporating a considerable stomach morphological diversity displayed by singular characteristic in an almost isolated pouch containing neotomine tribes. Two contrasting configurations have been de- the glandular epithelium. We recognize two variations of the scribed in the Neotomini (Carleton 1973:22) and substantive Type A stomach. Although similar in morphology, one of these variation has been recorded among the Peromyscini, although subtypes (subhemiglandular sensu Langer 2017) is exclusive to with a clear dominance of discoglandular and “pouched” stom- two emblematic genera in the Akodontini. Podoxymys, a taxon achs (Carleton 1973). Included in the latter tribe, Onychomys is endemic to the Tepuis (Anthony 1929), has the glandular epi- recognized by its singular type of “pouched” stomach, associ- thelium slightly more restricted to the antral region. This is a ated with the specialized alimentary habits of these carnivorous unique condition, distinguished by Carleton (1973) and here desert cricetids (Horner et al. 1965; Vorontsov 1967, 1979). termed Subtype A′. An almost similar anatomy is displayed Integrating evidence.—Connecting stomach morphology in Bibimys, a poorly known genus associated with perisylvan with diet in is a common practice (Langer 2017). Tropical and Subtropical grasslands (Pardiñas et al. 2017b). However, as already highlighted for rodents, a reductive ap- The variety in stomach configurations of akodontines sur- proach is poorly supported by data and can lead to biased con- passes that of remaining sigmodontine tribes. Oryzomyini (ca. clusions (Perrin and Curtis 1980; Chivers and Langer 1994; 30 genera) and Phyllotini (11 genera), the two other speciose Hume 1994, 2002). Thus, the analysis of stomach morphology sigmodontine tribes, each are typified by a single stomach mor- in exclusivity, without consideration of remaining important phology (Vorontsov 1962, 1967; Carleton 1973; Patton and parts of the digestive system, must be avoided (Carleton 1981; Hafner 1983; Carleton and Musser 1989; Steppan 1995:53; Langer 2002, 2017; Langer and Clauss 2018). The caecum and Weksler 2006:59). This also is true for taxonomically minor proximal colon play a major role in food assimilation (Björnhag tribal assemblages such as the Abrotrichini (five genera—Teta 1994; Hume 1994, 2002; Langer 2017). These features have not et al. 2017), Andinomyini (two genera—Salazar-Bravo et al. been studied in sigmodontines (Vorontsov 1967). In addition, 2016), and Euneomyini (three genera—Pardiñas et al. 2015d). almost nothing is known about microbial diversity in the diges- The Wiedomyini (four genera sensu Gonçalves et al. 2020) tive system of these cricetids. In two neotomines with bilocular lack data to be accurately judged. Finally, Ichthyomyini and stomachs (Neotoma bryanti and Neotoma albigula—Kohl Thomasomyini, each with five genera, demonstrate moderate et al. 2011, 2014), bacterial richness estimated for the stomach variation in the extension of glandular epithelium. It ranges was similar to that detected in the caecum and large intestine, from “half-to-half” stomachs (Type A as defined herein) to in- highlighting the importance of the bacterial community for the stances where the glandular epithelium covers the antral side initial digestion of fiber, recycling of endogenous nitrogen, and of the greater curvature (e.g., aureus—Carleton detoxification of dietary toxins. This is a subject that requires 1973:figure 4) or moderate portions of the antrum (e.g., attention to illuminate the physiological evolution of digestion , —Carleton 1973:figure 6). The gastric in sigmodontines (Domínguez-Bello and Robinson 1991). condition in the poorly known thomasomyine Aepeomys was A brief attempt at integrating stomach morphology, gall- recorded as with “glandular epithelium… restricted to a small, bladder, and diet, with phylogeny can be made, albeit within pouch-like structure on the greater curvature (closely resem- the framework of the cautionary context presented above. Diet bling the condition illustrated by Carleton [1973: fig. 5C] for in akodontines similarly is a scarcely examined topic (Madden Oxymycterus rutilans)” (Voss et al. 2002:15). 2015; Pardiñas et al. 2017a). However, some detailed studies It is not easy to explain why the Akodontini are so vari- exist, with the caveat that they included relatively few spe- able in stomach morphology. Akodontines are a rich group cies (Barlow 1969; Pizzimenti and de Salle 1980; Ellis et al. in general body morphology, dietary habits, and life modes 1994; Suárez and Bonaventura 2001; Solari 2007; Talamoni (D’Elía and Pardiñas 2015). However, they do not distinctly et al. 2008; Pinotti et al. 2011; Sahley et al. 2015). Of the 16 surpass oryzomyines in these attributes (Weksler 2006; Patton akodontine genera, we have sparse but quantitative data for spe- et al. 2015). Phylogenetically, the hypotheses most extensively cies in Akodon, Brucepattersonius, Necromys, Oxymycterus, advanced for the subfamily indicate comparable diversifica- Scapteromys, and Thaptomys. For Blarinomys, Deltamys, tion times for the main tribes included in Oryzomyalia (Parada Juscelinomys, Kunsia, and Lenoxus, there only is anecdotal in- et al. 2013; Salazar-Bravo et al. 2016; Steppan and Schenk formation or qualitative data based on cursory inspection of a 2017). We therefore are unable to explain evolutionary differ- few samples of stomach contents. Finally, food items consumed ences between Akodontini and the other sigmodontine clades are largely unreported for Bibimys, Castoria, Gyldenstolpia, in stomach diversity. Podoxymys, and Thalpomys (Fig. 6; Supplementary Data Extending comparisons to other cricetid subfamilies is diffi- SD11). cult because their phylogenetic relationships have not recently Genera of group 1 (Fig. 6), characterized by stomachs of Type been revised. At least for neotomines, several emblematic A, are primarily omnivorous and have a gallbladder. Within genera (i.e., Neotoma, , ) and tribes this group, Necromys, probably the akodontine with the highest (e.g., Peromyscini) are in need of systematic examinations degree of plant consumption, shows the stomach Subtype A″. 16 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

Those of group 2, with stomachs of Type C, at least regarding apparent, but more extensive and detailed research is essential Oxymycterus, are carnivorous and also have a gallbladder. The to validate such a hypothesis.” We are still far from this type of same diet tendency is apparent for the genera of group 3, also comprehensive approach with respect to akodontines. with Type C stomachs, but lacking the gallbladder. Kunsia and Towards a new classification of the Akodontini.—Stomach Scapteromys are difficult to reconcile, as each has a different morphological diversity has traditionally sown doubts on stomach morphology (Types C and B, respectively) and both akodontine classification.Vorontsov (1959:136) distinguished have a gallbladder. Kunsia has a diet composed of insects and “Akodontini” (including Akodon, Blarinomys, Lenoxux plant material, and Scapteromys is omnivorous. Finally, the sole [sic], Microxus, , Oxymycterus, Podoxymys, and member of group 5, Bibimys, has a stomach Type A, Subtype ) from “Akodontini incertae sedis” (Scapteromys A′, lacks a gallbladder, and is hypothesized to exhibit a diet and ). A “discoglandular” condition in Scapteromys similar to that of Kunsia (Fig. 6). was noted as special by Carleton (1973:28): “…representatives Few generalizations can be made from these data. of the scapteromyine, oxymycterine, and ichthyomyine groups Apparently, diets with a marked tendency to carnivory (insects, depart conspicuously from the hemiglandular condition... The arachnids, and earthworms) express “pouched” stomachs, with discoglandular stomach of Scapteromys tumidus warrants spe- the gallbladder present or not. Reduction and confinement of cial attention. Vorontsov (1967: pl. 120, p. 54) postulated a form the glandular epithelium has been reported in other special- of stomach intermediate to a unilocular-hemiglandular stomach ized, carnivorous muroids (Horner et al. 1965; Vorontsov 1967, and the unilocular-pouched seen in examples of Oxymycterus. 1982; Genest-Villard 1968; Carleton 1973; Langer 2017). The stomach of Scapteromys exactly fulfills this morphological Omnivorous or seasonally/geographically variable diets are as- grade.” The “pouched” stomach of Oxymycterus similarly has sociated with stomachs where both types of gastric epithelia been considered unique since Tullberg (1899). are subequally distributed in the stomach, the gallbladder typi- We propose the hypothesis that stomach diversity in cally being present (Carleton 1973). Variable distribution of the akodontines implies that the tribe as currently constituted likely gallbladder in sigmodontines, as well as in other rodents, is a is a composite, that is: made up of more than one diagnosable recurrent and not well-understand phenomenon (Higashiyama tribe or subtribe. Additional morphological characters such as et al. 2018). the rhinarium type, robustness, develop- Overall, akodontines are mostly carnivorous, with a clear ment, and dentition complexity support this hypothesis. High tendency for consumption of arthropods (e.g., Barlow 1969; levels of genetic divergence of the main akodontine clades also Pizzimenti and de Salle 1980; Talamoni et al. 2008; Pardiñas support a division of the Akodontini. Thus, we propose that the et al. 2017a; Missagia et al. 2019). Some species specialize morphological evidence, including stomach diversity and ge- in ants and termites (Oxymycterus—Redford 1984, 1987; netic divergence, contrasts with the Cytb-based classification Juscelinomys—Emmons and Patton 2012), although available advanced by Smith and Patton (1999:104): “It would be possible data are insufficient to establish these forms as myrmecophagous to keep the scapteromyines, as represented by Scapteromys and (McNab 1984; Merritt 2010). Several species eat variable Kunsia, as a monophyletic tribal group only if the akodontines amounts of plant material (Brandán 1995; Castellarini et al. were split into two separate tribes... An alternative choice… 2003), but this item, at least for the taxa with recorded data would be to expand the Akodontini to include Scapteromys (Supplementary Data SD11), almost never surpasses 40% of and Kunsia. We have followed this second alternative in our the diet (but see Talamoni et al. 2008). Carnivorous habits are tribal arrangement…” An “expanded akodontine” classification reflected in akodontine molars, as they typically are brachydont was accepted from subsequent Cytb- and IRBP-based analyses or mesodont (Reig 1987). Few members of the tribe display (D’Elía 2003; D’Elía et al. 2003, 2005) and constitutes the hypsodonty; Bibimys, Kunsia, and Necromys, display somewhat current dominant paradigm of akodontine tribal classification higher crowns, probably associated with moderate plant exploi- (D’Elía and Pardiñas 2015; Salazar-Bravo et al. 2016), including tation (Miranda Ribeiro 1914; Hershkovitz 1966; Massoia and or not the use of “divisions” such as those proposed by D’Elía Fornes 1967; Diório 2014; Pardiñas et al. 2017b). Recently, (2003). However, Smith and Patton (1999:104) also advanced Missagia et al. (2019) reported isotopic data from hair samples an alternative hypothesis, where the “… akodontines were split of numerous akodontines (covering 15 genera). Their study re- into two separate tribes, with Akodon, Thaptomys, Bolomys, and vealed that most species have relative high δ 15N values, sug- Oxymycterus in one tribe and Blarinomys, Brucepattersonius, gesting they include more animal matter in their diet than other and Lenoxus in the other.” In addition, some refinements were sigmodontine rodents; these results must be taken with caution offered by D’Elía (2003:319–320), “…further work is needed because considerable variation in isotopic signatures also was to clarify the basal pattern of the akodontine differentiation... observed. For the time being, it seems adequate to continue to recognize After an assessment of the digestive system (including Akodontini (sensu Smith and Patton, 1999). However, in order molars, stomachs, liver, gallbladder, and caecum) in 19 species to emphasize the current knowledge of the phylogenetic rela- of African muroids, Perrin and Curtis (1980:32) concluded that tionships within this large clade, it is of interest to informally “It would be premature and incorrect to conclude by stating recognize well-supported internal divisions.” that gut morphology was directly correlated with diet in ei- Adjustments to the classificatory scheme of akodontines with ther Murid or Cricetid rodents. Certainly such tendencies are respect to diversity of the group have been informally advanced PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 17 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

(Pardiñas et al. 2017a). Based on stomach morphology and gall- J. Pardiñas, A. Formoso, P. Teta, J. Torres, D. Udrizar-Sauthier, bladder distribution, a morphological review in progress, and a D. Podestá, S. Cirignoli, P. Ortiz, R. Vargas, and L. Pereira. refreshed molecular-based phylogeny, a “reduced akodontine” The Bolivian specimens studied herein were collected under alternative is tempting. However, a single character complex the research permit MMAYANMABCCGDF/DGBAP/UVSAP (stomach and gallbladder morphology) is insufficient to support 354/2015; field efforts were possible thanks to the support from a new scheme. As Voss (1992:33) remarked “special recognition M. Hidalgo Cossio, the Identidad Madidi team, and the people for favored characters, however, has no place in rational system- from the communities inside Madidi; Wildlife Conservation atic practice.” An integrative analysis is required to illuminate this Society, under the chief direction of R. Wallace, Director of issue. It is important to realize that the main components of the the Greater Madidi – Tambopata Landscape Program, and the digestive system integrate a complex of characters, not just a sin- Gordon and Betty Moore Foundation financed the field study gular isolated trait. In this respect, Langer (2017:204) concluded as part of the Identidad Madidi initiative. We thank the curators “…a clear relationship among the gastric form, mucosal lining who made specimens available for study, namely R. Barquez and and trophic category cannot be deduced from the available ma- M. Díaz (CML), D. Flores and S. Lucero (MACN), and D. Verzi terial, but systematic relationships between Cricetidae seems to (MLP). Field and laboratory assistance, including obtaining the play a role in the selection of food.” photographs as well as dissections and anatomical help provided Most authors have highlighted difficulties in evaluating available by E. Cuéllar, O. Torrico, F. Galliari, L. De Santis, and R. Robles genealogical relationships among tribes within the Oryzomyalia has our deep recognition. Special thanks to P. Langer, the greatest (Steppan and Schenk 2017). According to Lessa et al. (2014:3), living student of mammalogy visceral systems, who kindly read “…phylogenetic relationships among tribes remain uncertain, the manuscript and provided constructive criticism. Our recogni- as does the placement of several distinct genera. At present, tion also goes to J. L. Patton, who offered significant advice in only the sister relationship of Sigmodontini + Ichthyomyini critical moments, to L. Carraway, who made important editorial and a large clade that includes all other sigmodontines (des- efforts, and specially to R. Martin, who generously read the en- ignated as Oryzomyalia by Steppan et al. 2004) are well sup- tire manuscript and promoted numerous corrections. This con- ported...” As these approaches focused on traditionally recognized tribution was made under the economic support and laboratory tribes, they overlooked important resolved relationships among equipment provided by grant Agencia Nacional de Promoción smaller suprageneric units. Whether these units are supertribes, Científica y Tecnológica 2014-1039 (to UFJP); in the field, ac- tribes, or subtribes, probably depends on dynamic systematic tivities to collect part of the studied material were undertaken paradigms. Thus, these “second-order relationships” deserve with critically important economic resources derived from grants attention. Returning to the phylogeny of the Akodontini, the po- Agencia Nacional de Promoción Científica y Tecnológica 2010- tential connection between our groups 1 and 2 is a recurrent theme 0924 (to G. Navone), 2015-1348 (to M. Lareschi), and 2015-1564 (Hershkovitz 1966; Hinojosa et al. 1987; Reig 1987). The stomach (to M. Lareschi). We are deeply indebted to the above-mentioned topology we obtained matches the recognition of two units of persons and institutions. This is GEMA (Grupo de Estudios de tribal or subtribal level: one composed of Akodon, Deltamys, Mamíferos Australes) contribution #30. Castoria, Necromys, Podoxymys, Thalpomys, and Thaptomys, that most likely should be considered Akodontini sensu stricto, and the other restricted to Juscelinomys plus Oxymycterus, that could be Supplementary Data considered the Oxymycterini. Members of the former exhibit Type Supplementary data are available at Journal of Mammalogy A stomachs, whereas those of the latter have stomachs of Type online. C. Both groups have a gallbladder. A third stomach assemblage, Supplementary Data SD1.—GenBank accession numbers sister to both, is composed of Blarinomys, Brucepattersonius, and for all the genetic sequences included in this study. Lenoxus, all members of which share Type C stomachs and lack Supplementary Data SD2.—Morphological character the gallbladder. A fourth assemblage, Scapteromyini, sister to the states (stomach and gallbladder) for 15 Akodontini genera. previously mentioned groups, includes Kunsia plus Scapteromys Supplementary Data SD3.—Stomachs of Akodon azarae (and possibly Gyldenstolpia), which have stomach Types B or C, and Oxymycterus rufus as illustrated by Vorontsov (1967). and a gallbladder. Finally, a monotypic assemblage, restricted to Supplementary Data SD4.—Gastric arterial details in Bibimys, which typically lacks a gallbladder, possibly represents some akodontine rodents: (A) Akodon azarae (CG 948; fixed); a first split of this entire “akodontine” branch of the sigmodontine (B) Akodon mollis (JBM 2008; fresh); (C) Necromys lasiurus tree. Focusing on “second-order relationships,” the sigmodontine (CG 739; fresh); (D) Thaptomys nigrita (CG 828; fixed); (E) radiation gains further clarity even without a dense record. T. nigrita (CG 841; fixed); (F)Oxymycterus quaestor (CG 817; A refreshed approach to soft anatomy will play a major role in this fresh). References: an, antrum; co, corpus; lg, left gastric ar- intellectual process. tery; po, pouch. Supplementary Data SD5.—Epiploic irrigation in Blarinomys breviceps (MZUFV 4451) Acknowledgments Supplementary Data SD6.—Gallbladder distribution in The field efforts of many persons collecting material here studied akodontine species. are greatly appreciated. This large list includes, among others to Supplementary Data SD7.—Dissections to expose gall- M. Lareschi, J. Notarnicola, J. Sánchez, R. Robles, E. Cuéllar, bladder in Bibimys labiosus (A, B; based on MZUFV 4465) and 18 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

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Appendix JBM 2167, JBM 2168*, JBM 2169, JBM 2170, JBM 2171, JBM 2172*, JBM 2173*); Parque Nacional Sangay, −2.17358°, −78.5029° Specimens examined are deposited in the following mammal collec- (MECN 5636, MECN 5650, MECN 5673, MECN 5676*, MECN tions: CNP, Colección de Mamíferos del Centro Nacional Patagónico, 5679*). Chubut, Argentina; CML, Colección Mamíferos Lillo, Tucumán, Akodon montensis (n = 24).—Argentina: Chaco; 7 km NW Puerto Argentina; MACN, Colección Nacional de Mastozoología, Museo Las Palmas, −27.00014167°, −58.002025° (CNP 3093). Misiones; Argentino de Ciencias Naturales “Bernardino Rivadavia,” Buenos Parque Provincial Piñalito, −26.08335278°, −53.00229444° (CG Aires, Argentina; MECN, Colección de Mastozoología del Instituto 776*, CG 797*, CG 806*, CG 819*); Club de Pesca Parana-í Nacional de Biodiversidad (INABIO), Quito, Ecuador; MLP, Colección Guazú, −26.00069444°, −54.13361111° (CNP 4007, CNP 3051*); de Mastozoología del Museo de La Plata, La Plata, Argentina; MN, Parque Provincial Urugua-í, −25.85267222°, −54.16736389° (CNP Museu Nacional, Rio de Janeiro, Brazil; MZUFV, Museu de Zoologia, 3703); Parque Provincial Cruce Caballero, sendero Carayá Pytha, Departamento de Biologia Animal, Universidade Federal de Viçosa, −26.00011111°, −53.15127778° (CNP 3030*); Parque Provincial Viçosa, Minas Gerais, Brazil. Specimens listed with numbers of col- Moconá, sendero Chachí, −27.15003889°, −53.0667° (CNP 3004*); lector or field catalogues, including CG (Carlos Galliari), JBM (Jorge Refugio Moconá, −27.00250278°, −53.08345556° (CNP 4003*, Brito Molina), LTU (Proyecto Localidades Típicas Ulyses Pardiñas), CNP 4004*, CNP 4013*, CNP 4011*, CNP 4012*); Reserva de Usos NBH (Nuria Bernal Hoverud), and UP (U. Pardiñas), will be depos- Múltiples Guaraní, −26.08357222°, −54.05085833° (UP 1006*, CNP ited in the following collections: CNP (those of CG, LTU, and UP), 4015, CNP 4006, CNP 4010, CNP 4002, CNP 4008, CNP 4025*); MECN (those of JBM), and Colección Boliviana de Fauna, La Paz, Reserva de Vida Silvestre Urugua-í, Fundación Vida Silvestre, Bolivia (those of NBH). Specimens marked with an * were surveyed −25.96799167°, −54.10231111° (CNP 3707*, CNP 3716*). for ocurrence of a gallbladder. Akodon philipmyersi (n = 4).—Argentina: Misiones; Estancia Santa Akodon aerosus (n = 6).—Ecuador: Morona Santiago; Kutukú, Inés, −27.01916667°, −55.03397222° (CNP 3013*, CNP 3019*, CNP −2.7872°, −78.1316° (JBM 1865*, JBM 1866, JBM 1963*); 3020*, CNP 3021*). Tungurahua; Baños, Reserva Vizcaya, −1.3885°, −78.3947° (JBM Akodon polopi (n = 3).—Argentina: Córdoba; Pampa de Achala, 2024*, JBM 2109); Zamora Chinchipe; Machinaza, −3.7825°, Repetidora La Posta, −31.617490°, −64.871729° (CNP 5162, CNP −79.0890° (JBM 2197). 5163*, CNP 5164). (n = 4).—Argentina: Jujuy; Sierra de Zenta, Akodon simulator (n = 2).—Argentina: Jujuy; El Ceibal, −24.30°, −23.127524°, −65.203076° (CNP 5490, CNP 5075*, CNP 6062*, −65.28° (CNP 1532*, CNP 1533). CNP 6063). Akodon spegazzinii oenos (n = 5).—Argentina: Mendoza; 10 km SSE Akodon azarae (n = 7).—Argentina: Buenos Aires; arroyo de las Bardas Blancas, −35.948534°, −69.738480° (CNP 6334*); río Atuel, Brusquitas, −38.242501°, −57.778947° (UP 349*), laguna Chascomús, margen izquierdo, 500 m aguas abajo puente RP 175, −34.751404°, −35.544033°, −58.079576° (CG 948*, CG 950*, CG 951), Rojas −68.298153° (CNP 5311*, CNP 5312*). San Juan; Parque Nacional (MLP 1.I.03.34, MLP 1.I.03.41). Formosa; Estación de Animales San Guillermo (CNP 3244*, CNP 3245*). Silvestres Guaycolec, Ruta Nacional 11, km 1201, −25.983166°, Akodon toba (n = 1).—Argentina: Chaco; Río de Oro, a 300 −58.165439° (CG 447). m río arriba del puente que atraviesa la RP 33, −26.78426389°, Akodon budini (n = 3).—Argentina: Jujuy; El Matadero, 26.2 km −58.95216944° (CNP 5275*). SE Tilcara (CML 11110, CML 11113). Salta; El Queñoal, 54 km W Bibimys chacoensis (n = 2).—Argentina: Chaco; 7 km S Puerto Las San Andrés (CML 11118). Palmas, −27.00014167°, −58.002025° (CNP 1891*); Cancha Larga, Akodon cursor (n = 1).—Brasil: Minal Gerais; Mata do Paraíso, −27.04°, −58.70° (CNP 756*). −20.802314°, −42.858728° (MZUFV 4481). Bibimys labiosus (n = 3).—Brasil: Minas Gerais; Mata do Paraíso, Akodon dayi (n = 2).—Bolivia: Franz Tamayo; Cargadero, −20.802314°, −42.858728° (MZUFV 4465*, MZUFV 4470*, −14.57857°, −68.97891° (NBH 701–2016*), Mamacona, −14.4694°, MZUFV 4469*). −68.19128° (NBH 545B-2016). Blarinomys breviceps (n = 22).—Brasil: Minas Gerais; Mata Akodon dolores (n = 9).—Argentina: Catamarca; camino do Paraíso, −20.802314°, −42.858728° (MZUFV 4443*, MZUFV Trampasacha-Chumbicha, −28.845059°, −66.297142° (CNP 3871*). 4444, MZUFV 4445*, MZUFV 4446, MZUFV 4447, MZUFV Córdoba; Deán Funes (CNP 430*, CNP 4730*); inmediaciones Parque 4448, MZUFV 4449, MZUFV 4450, MZUFV 4451, MZUFV 4452, Provincial Chancani, −31.377818°, −65.384082° (CNP 4731*, CNP MZUFV 4453, MZUFV 4454, MZUFV 4455, MZUFV 4456, MZUFV 4732), Quilino (CNP 4891); Neuquén, 1 km aguas abajo puente RN 4457, MZUFV 4458, MZUFV 4459, MZUFV 4460, MZUFV 4461, 40 sobre río Neuquén, −37.415438°, −70.225558° (CNP 2381*), calle MZUFV 4462*, MZUFV 4463*, MZUFV 4464*). América del Sur, 200 m toma de agua, Neuquén, −38.93°, −68.05° Brucepattersonius iheringi (n = 7).—Argentina: Misiones; Parque (CNP 2346, CNP 2351). Provincial Urugua-í, −25.85267222°, −54.16736389° (CNP 5507*); Akodon iniscatus (n = 9).—Argentina: Buenos Aires; Bahía RP2, 6 km NE Arroyo Paraíso, −27.03547222°, −54.01941667° (CNP San Blas, −40.58°, −62.26° (CNP 784*); Chubut, Playa Fracasso, 1933*); Salto El Paraíso, −27.05272222°, −54.03452778° (CNP −42.431242°, −64.127858° (CNP 1408, CNP 1440, CNP 1458); Playa 1932*); Refugio Moconá, −27.00250278°, −53.08345556° (CNP Doradillo, −42.650295°, −64.983151° (CNP 1411*); Bahía Crácker, 1999*); alrededores del asentamiento aborigen Kaaguy Poty, 1 km al −42.950721°, −64.479390° (CNP 1421, CNP 1438); Los Altares, NNO de la intersección de la Ruta Provincial 7 y el arroyo Cuña Pirú, −43.876265°, −68.414632° (CNP 1417); Parque Eólico “Malaspina,” −27.087500°, −54.952500° (CNP 1973*); Parque Provincial Moconá, −44.973447°, −67.057394° (CNP 6410*). sendero de la Gruta, −27.15097778°, −53.06673889° (CNP 2331*); Akodon mimus (n = 5).—Bolivia: Franz Tamayo; Isañuyoj, arroyo Liso, −27.106122°, −54.985288° (CNP 2368*). −14,6286°, −69,04595° (NBH 762 2016*, NBH 783 2016*, NBH 824 Castoria angustidens (n = 1).—Argentina: Misiones; RP2, 6 km NE 2016*, NBH 862 2016, NBH 865 2016). Arroyo Paraíso, −27.03547222°, −54.01941667° (CNP 449*). Akodon mollis (n = 14).—Ecuador: Chimborazo; Birón, cuenca alta Deltamys kempi (n = 7).—Argentina: Buenos Aires; La Balandra, del río Santa Rosa, 0.0202°, −78.4931° (MECN 5201, MECN 5202*, Club de Pesca La Terraza, −34.08485278°, −57.03566389° (CNP PARDIÑAS ET AL.—AKODONTINE STOMACH MORPHOLOGY 23 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020

581*, CNP 893, CNP 3086*, CNP 3087, CNP 5756); Ciudad Oxymycterus paramensis jacentior (n = 6).—Argentina: Jujuy; San Autónoma de Buenos Aires, Reserva Ecológica Costanera Sur (CNP Francisco, −23.60°, −64.95° (CNP 6298*, CNP 6301*); río Lozano, 3 6295*, CNP 6297*). km aguas arriba RN 9, León, −24.02°, −65.46° (CNP 6299). Bolivia: Lenoxus apicalis (n = 4).—Bolivia: Franz Tamayo; Cargadero, Franz Tamayo; Isañuyoj, −14,6286°, −69,04595° (NBH 779 2016); −14.57857°, −68.97891° (NBH 725 2016*, NBH 753 2016*); Sarayoj, Puina (NBH 165 2015, NBH 166 2015). −14.61473154°, −68.18715487° (NBH 1329 2017*, NBH 1377 2017*). Oxymycterus quaestor (n = 2).—Argentina: Misiones; Parque Necromys amoenus (n = 2).—Bolivia: Franz Tamayo; Machariapo, Provincial Piñalito, −26.08335278°, −53.00229444° (CG 785*, CG −14.68502°, −68.27521° (NBH 25 2015*, NBH 42 2015*). 817*). Necromys lactens (n = 4).—Argentina: Jujuy; San Francisco, Oxymycterus rufus (n = 5).—Argentina: Buenos Aires; Estación −23.60°, −64.95° (CNP 4124), río Lozano, 3 km aguas arriba RN 9, San José, −38.177597°, −59.009897° (CNP 6307*, CNP 6308*); León, −24.02°, −65.46° (CNP 6040). Salta; Abra de Volcán, 38.8 km Sierra de la Ventana, Campamento Base, −38.069240°, −62.022805° ENE Humahuaca (CML 11483); El Queñoal, 54 km O San Andrés (UP 309). Entre Ríos; Villa Elisa, −32.13406944°, −58.08358611° (CML 11485). (CG 847*, CG 849*). Necromys lasiurus benefatus (n = 7).—Argentina: Buenos Aires; 5 km N Scapteromys aquaticus (n = 10).—Argentina: Buenos Aires; La Monte Hermoso, −38.93°, −61.30° (CNP 5244). Chaco; 5 km NW Puerto Balandra, Club de Pesca La Terraza, −34.08485278°, −57.03566389° Las Palmas, −27.00138889°, −58.00008333° (CNP 3036). Córdoba; Deán (CNP 6404, CNP 6405, CNP 6406*, CNP 6407*, CNP 6408*, Funes (CNP 4727*, CNP 4780*, CNP 432*, CNP 694, CNP 698). CNP 6409*). Corrientes; Ea. Loma Alta, La Cruz, −29.00211667°, Necromys lasiurus temchuki (n = 7).—Argentina: Misiones; −57.00027222° (CNP 6307*). Entre Ríos; Villa Elisa, −32.13406944°, Estancia Santa Inés, −27.01916667°, −55.03397222° (CNP 3041, −58.08358611° (CNP 6308*). Formosa; Estación de Animales CNP 3043, CG 752*, CG 750*, CG 772*, CG 774*); EEA INTA Villa Silvestres Guaycolec, Ruta Nacional 11, km 1201, −25.96931389°, Miguel Lanús, −27.08419444°, −55.05097222° (CNP 3042*). −58.15256389° (CNP 5067*, CG 437*). Necromys lasiurus? (n = 1).—Bolivia: Abel Iturralde; Pampas de Thalpomys cerradensis (n = 2).—Brasil: Distrito Federal; Parque Heath, −13.045870°, −68,837956° (NBH 1025 2017). Nacional de Brasília (MN 75700*, MN 75703*). Necromys obscurus (n = 6).—Argentina: Buenos Aires; Estación Thaptomys nigrita (n = 12).—Argentina: Misiones; 2 km aguas San José, −38.177597°, −59.009897° (CNP 6030*, CNP 6035*), abajo desembocadura Parana-í Guazú, −26.675574°, −54.813855° Arroyo de las Brusquitas, −38.22761111°, −57.779° (CNP 2380, CNP (CNP 3009*); asentamiento aborigen Kaaguy Poty, 1 km al 3039, CNP 3055, CNP 3056). NNO de la intersección de la Ruta Provincial 7 y el arroyo Cuña Necromys urichi (n = 1).—Venezuela: exact locality not recorded Pirú, −27.087500°, −54.952500° (CNP 1970*, CNP 2370, CNP (MACN 188). 2371*, CNP 2372*); Parque Provincial Piñalito, −26.08335278°, Oxymycterus hiska (n = 1).—Bolivia: Franz Tamayo; Machariapo, −53.00229444° (CG 791*, CG 828*, CG 841*); Parque Provincial −14.68502°, −68.27521° (NBH 13 2015*). Urugua-í, −25.85267222°, −54.16736389° (CNP 4262*); Refugio Oxymycterus nigrifrons (n = 1).—Bolivia: Franz Tamayo; Moconá, −27.00250278°, −53.08345556° (CNP 3011*, CNP 3008*, Machariapo, −14.68502°, −68.27521° (NBH 27 2015*). LTU 859*).

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