Oxymycterus itapeby, Pecanha, Quintela, Ribas, Althoff, Maestri, Goncalves, and Freitas, 2019

Bezerra, Alexandra Maria Ramos, Bonvicino, Cibele Rodrigues, Oliveira, Leony Dias de, Castiglia, Riccardo & Lazar, Ana, 2025, New data on the rare Oxymycterus itapeby and the Anajatuba hantavirus host Oligoryzomys mattogrossae (Rodentia: Cricetidae): the importance of surveys in challenging-to-access environments in the Brazilian Cerrado, Journal of Natural History 59 (17 - 20), pp. 1227-1247 : 1235-1242

Geographic distribution, morphology and aspects of natural history of Oxymycterus itapeby

The Águas Emendadas Ecological Station represents a new locality for O. itapeby , expanding the presently known species range northwards by more than 830 km ( Figure 5 ). The specimens from ESECAE exhibit an overall tawny-brown dorsal fur colour, with lighter ventral colouration described as ‘olive’ according to Ridgway (1886), and without evident lateral delimitation ( Figure 6 ).

The two specimens of O. itapeby analysed exhibited a unilocular-pouched (or discoglandular) stomach ( Figure 7 ), featuring an incisura angularis that does not extend beyond the level of the oesophagus opening, and lacking a bordering fold. The stomach morphology corresponds to Type C as described by Pardiñas et al. (2020). The stomach has a two-chambered morphology, with the corpus three times larger than the antrum. The antrum is covered by cornified epithelium and is confined to a large prepyloric region, while the corpus is large and features a gauzier and smoother cornified epithelium. The glandular epithelium is confined to a diverticulum (or ‘pouch’) located on the right side of the antrum, with a minute aperture (ostium) connecting the glandular pouch to the lumen of the stomach, in the corpus side.

The stomach measurements before dissection were 28 mm width × 25 mm height (ARB 874/MPEG 46617) and 28 mm width × 24 mm height (ARB 876/MPEG 46618). The contents of the two dissected stomachs included fragments of poneromorph ants (family Formicidae ) and some flake cornflour (used as bait). Fourteen ant individuals were found inside the stomach of specimen ARB 874/MPEG 46617, and eight individuals were found in specimen ARB 876/MPEG 46618.

Distribution of and new data on Oxymycterus itapeby

Oxymycterus itapeby is a Brazilian endemic species, known only from 11 specimens. Until recently, only the five specimens from the original description were known ( Peçanha et al. 2019): the holotype and the paratype from type locality, in Itapevi municipality (ca. 23.5948S, 46.9752W), São Paulo state, and three specimens (represented by tissue samples only) from two localities ( one specimen at 24.2620S, 49.9486W and two others at 24.1990S, 49.6069W) in Jaguariaíva municipality, Paraná state ( Peçanha et al. 2019) . This species was described based on two taxidermied skins and skulls housed at the Museu de História Natural ‘ Capão do Imbuia’ (Curitiba, Paraná state, Brazil), and on molecular analysis, but nothing is known about the natural history of the species. The type specimens were collected in 1996, the tissue samples are from 1991 ( one specimen) and 2004 ( two specimens), and the species description was published in 2019 ( Peçanha et al. 2019). The original habitats where the specimens were collected are not known in detail, as the description of the habitats of type series and sequences was based on the present-day characteristics of the area where they were originally captured.

In 2023, as part of a study on organochlorine pesticide contamination in small mammals ( Capella et al. 2023), six specimens of O. itapeby were found in Itatiaia National Park ( 22.3733S, 44.7025W), Rio de Janeiro state, Brazil. The specimens ( four females and two males) were captured during November 2016 (rainy season) with Sherman® live traps (7.64 × 9.53 × 30.48 cm). Body length ranged from 207 to 332 mm and weight from 58 to 67 g ( Capella et al. 2023). Although the authors provided information on the voucher collections and codes, they did not report the vegetation type sampled or the species identification procedure. Oxymycterus species are considered terrestrial and habitat specialist species ( Hershkovitz 1994), primarily found in moist and open habitats, as well as at the edges of gallery forests ( Bonvicino and Bezerra 2003; Carmignotto et al. 2022), but they also are found in non-flooded upland forests in the Amazon ( Abreu-Junior et al. 2016). The three juvenile specimens collected by us were found in seasonally flooded open grassland. The present record increases the number of known specimens to 14 and extends the species’ range by more than 830 km northwards, into core Cerrado domain. Previous records are from the Atlantic Forest (the type locality and Itatiaia National Park ) and the transitional Cerrado-Atlantic Forest (IBGE – Instituto Brasileiro de Geografia e Estatística 2004). Despite the wide geographic distance between previously known localities and the new record, the haplotype of our specimen shows no significant genetic distance from other specimens (1.0–1.5%), indicating scarce geographic structuring. It is possible that O. itapeby specimens collected along suitable habitats (ie flooded grasslands associated to ‘veredas’, but also possibly humid forests) may have been erroneously identified as other morphologically similar sympatric Oxymycterus species. In fact, O. itapeby phenotypically differs from O. dasytrichus , which occurs along coastal eastern and south-central Brazil, only in terms of cranial morphology and centroid size. It also differs from O. delator , which has a wide distribution from north-eastern and central Brazil to Paraguay, a larger body size, and dark-brown pelage colouration ( Oliveira and Gonçalves 2015; Peçanha et al. 2019).

It should also be noted that this is the second record of O. itapeby inside a protected area. Previous records ( Peçanha et al. 2019) are from highly disturbed localities that have undergone habitat changes due to agribusiness and urban expansion, with the type locality being particularly close to the São Paulo megalopolis. The first record inside a protected area is from Itatiaia National Park , located in a mountainous area of Atlantic Forest domain, harbouring preserved ‘campos de altitude’ (field vegetation type on igneous and metamorphic rocks above 1500 m altitude; Vasconcelos 2011) and Ombrophilous Altimontane Forest ( Capella et al. 2023). ESECAE is an island of natural landscape surrounded by highways in a region undergoing urban and agribusiness expansions, which have fragmented and severely altered its natural areas. These impacts affect the structure of vertebrate communities (e.g. snakes – França and Araújo 2007; birds – Borges and Marini 2010). Urban extension also contributes to increased predation and attacks on wildlife by domestic animals ( Marinho-Filho et al. 1998), and vehicle collisions resulting in roadkills ( Rodrigues et al. 2013; Ramalho et al. 2021; personal observation during the fieldwork – a roadkilled Lycalopex vetulus was found in front of the Ecological Station’s main entrance; it was taxidermied by us and deposited in the Mammal Collection of University of Brasília, Federal District, Brazil, with the number UNB 4070).

The genus Oxymycterus is known by its conserved karyotype, with diploid number 54 and autosomal fundamental number ranging from 62 to 64 (see Paresque et al. 2018; Peçanha et al. 2019). The karyotype of O. itapeby is described here for the first time and is characterised by 2n = 54 and FNa = 64. Svartman and Almeida (1993), who sampled at the same locality as us – the Águas Emendadas Ecological Station – recorded a karyotype of 2n = 54 and FN = 64 for specimens identified as ‘ Oxymycterus sp’. This karyotype is the same as that found in the sympatric species in central Brazil, O. delator ( Bonvicino et al. 2014) , which also shown a karyotype of 2n = 54 and FNa = 62 ( Bonvicino et al. 2005).

The internal view of stomach morphology of O. itapeby specimens is similar to that of O. rufus shown in fig. 5C (as Oxymycterus rutilans ) by Carleton (1973) and in Fig. 4H–I of Pardiñas et al. 2020. However, the external morphology resembles the stomachs of Necromys lasiurus (an akodontini species) shown in Figs 3K–L and O–P of Pardinãs et al. 2020. The pouch glandular epithelium has a more lateral position when compared to other Oxymycterus species. In fact, this structure is positioned completely on the right lateral side of the antrum, while in other species of the genus it has a more distal position ( Carleton 1973; Hershkovitz 1994; Pardiñas et al. 2020). There is no data available on gross stomach morphology of the sister species to O. itapeby , ie O. amazonicus and O. delator , for comparison of the position of pouch glandular epithelium to determine whether it is an individual phenotype or a trait with phylogenetic signal ( Pardiñas et al. 2020).

The stomach contents of the two analysed specimens included only ants as prey items (and flaked cornflour used as bait base). The gross stomach morphology of Oxymycterus species (with glandular epithelium confined to a diverticulum or pouched) is also found in other muroid rodent species with a specialised carnivorous diet (see Pardiñas et al. 2020 for discussion). In fact, Oxymycterus species are described as carnivorous, primarily feeding on invertebrates (including hard-shelled ones such as ants and termites, or soft ones like worms and larvae), but also consume seeds and plant tissues ( Redford 1984, 1987; Suarez 1994; Barbero et al. 2021). During laboratory predation tests, Redford (1984) observed that Oxymycterus delator (identified as Oxymycterus roberti in his study) actively preys on termites by trailing their scent tracking, displaying no size or nutritional quality preferences among termite species. However, it did show preference for termite species that possess soldiers with mechanical or chemical-mixed defence mechanisms rather than species with only chemical-based defence. We note that the poneromorph ants found in the stomach contents of O. itapeby exhibit soldier-worker caste dimorphism.

The data herein presented agree with the hypothesis that gallery forests and dry forests act as corridors for small nonvolant mammals into the Cerrado of central Brazil, with the Atlantic Forest (also the Amazon) sharing taxa with this domain ( Costa 2003; Bonvicino et al. 2014; Carmignotto et al. 2014, 2022). ESECAE is situated in a region that encompasses the headwaters of two basins contributing to the Atlantic Forest and Amazon, playing a fundamental role in the presence of the shared fauna. Oxymycterus itapeby was recently categorised as Data Deficient during the threat assessment of mammal species in Brazil ( ICMBio 2024). We hope that the new data presented here will contribute to increasing the knowledge of this species. Despite the expansion of its geographic distribution, the protected area where the species was found remains limited and subjected to severe negative impacts.

Figures

Figure 3. Genetic relationships of Oligoryzomys mattogrossae based on (A) maximum likelihood (ML) tree using cytochrome b (mt-Cytb) sequence data considering the HKY+G + I model. Nodal support indices are indicated at the node (ML/BI). (B) Phylogenetic TCS parsimony network reconstruction. Missing haplotypes are indicated by dashes and black circles. The size of the coloured circles is proportional to the number of individuals for each haplotype. (C) Map showing the two main hydrographic basins (pink and green areas) where the sequenced specimens were collected. The colours of the sample sites match the lineages identified by ML and TCS; the triangle is Águas Emendadas Ecological Station (ESECAE) (this study); and the numbers refer to the localities in Table 1 and Supplementary material I. BI: Bayesian inference, ML: Maximum likelihood.

Figure 4. Genetic relationships of Oxymycterus itapeby based on (A) a maximum likelihood (ML) tree using cytochrome b (mt-Cytb) sequence data considering the HKY +G + I model. Nodal support indices are indicated at the node (ML/BI). Terminal labels include GenBank accession numbers for the sequences downloaded from GenBank or specimen catalogue numbers for those sequences obtained in this study.The sequences of the new specimens from Águas Emendadas Ecological Station (ESECAE) are recovered well nested in the clade of O. itapeby; the holotype (GenBank sequence number MK331135; MHNCI 3595) is indicated with a red line. (B) Phylogenetic TCS parsimony network reconstruction including sequences of O. amazonicus (green dots and line), O. delator (blue dots and line), and O. itapeby (orange dots and line; the red dot is haplotype from holotype, and the violet dot represents haplotypes from the new specimens collected in the ESECAE). Missing haplotypes are indicated by dashes and black circles. The size of the coloured circles is proportional to the number of individuals for each haplotype.

Figure 5. Map showing the original distribution of the Brazilian endemic Oxymycterus itapeby based on Peçanha et al. (2019) and Capella (2023), from the transitional Atlantic Forest–Cerrado region in south–south-eastern Brazil, and the new records extending the distribution to Águas Emendadas Ecological Station (ESECAE), Planaltina, Federal District, in the core area of the Cerrado domain.

Figure 6. Male individual of (A) Oxymycterus itapeby (ARB 876/MPEG 46618) captured at Águas Emendadas Ecological Station (ESECAE), Brasília, DF, Brazil. (B) seasonal flooded ‘campo de murundum’ where the three new specimens were captured. (C) Microhabitat with the Sherman type trap used for the captures.

Figure 7. Gross stomach morphology of Oxymycterus itapeby. Specimen ARB 874/MPEG 46617 in (A) ventral external view with contents, and (B) ventral internal view without contents. The frontal section shows the glandular epithelium confined in a diverticulum (= pouch) (after Carleton 1973). Abbreviations: di: diverticulum (= pouch); o: ostium. Scale bar: 10 mm.