New morphological data on the rare sigmodontine Mindomys hammondi (Rodentia, Cricetidae), an arboreal oryzomyine from north-western Andean montane forests

The monotypic rodent Mindomys Weksler, Percequillo & Voss, 2006 (Cricetidae, Sigmodontinae) is one of the rarest members of the speciose tribe Oryzomyini. As this species is restricted to the Chocó forests of the western Andean slope in northern Ecuador, our knowledge is based on a few specimens collected decades ago. Here we add the first data on some aspects of external anatomy (cheiridia examined in fresh, ears, rhinarium), genital anatomy (penis), soft anatomy (palate, stomach, caecum) and postcranial skeleton retrieved from a full adult male, recently trapped in Reserva Drácula, Carchi, Ecuador. Several features of this specimen, paradoxically the first to be added to Ecuadorian mammal collections, reinforce the view that Mindomys is an arboreal sigmodontine.


Introduction
The tribe Oryzomyini comprises the largest living assemblage of sigmodontine rodents, with a diversity reaching 30 genera (Brito et al. 2020;Percequillo et al. 2021). This remarkable richness, however, encompasses several genera, knowledge of which is limited to basic aspects of craniodental anatomy and external traits evaluated from museum skins. Examples of this are the rare monotypic Microakodontomys Hershkovitz, 1993, Mindomys Weksler, Percequillo & Voss, 2006and Sigmodontomys J. A. Allen, 1897. In these cases, the addition of a novel specimen can represent a significant input of data (e.g. see Amphinectomys; Chiquito and Percequillo 2016). The goal of the present note is to expand the basic anatomical and genetic knowledge of Mindomys hammondi (Thomas, 1913), based on a recently secured specimen.
After an extensive small mammal survey involving five years of trapping (a cumulative effort of 1,990 trapping nights, including 990 pit-fall nights) conducted by JB and collaborators at Reserva Drácula (1.006667°S, 78.2247°W, 1067 m alt., Parroquia Chical, Cantón Tulcán, Provincia Carchi, República del Ecuador; geographical coordinates taken by GPS at the trap line), a single specimen referable to Mindomys was collected. Obtained from a pit-fall trap set in a dense montane forest in the Chocó Ecoregion (Fig. 1), the animal was preserved as a carcass in skin with the skeleton cleaned and housed at the mammal collection of the Instituto Nacional de Biodiversidad (INABIO, Quito, Ecuador) under the number MECN 6228. It was a male with scrotal testes, an adult according to the wear of the molars (Fig. 2); external and craniodental measurements are provided in Appendix 1. Prior to this specimen, M. hammondi was known from a small sample of individuals mostly collected at or near its type locality (Mindo, Pichincha, Ecuador;Thomas 1913) during the first half of the past century Tirira and Azurduy Högström 2011;Percequillo 2015). The novel material from Reserva Drácula represents the first data, based on a fresh individual, of several traits related to external and soft anatomy. Here, these features are explored following contributions of Voss (1988), Carleton (1998) and Weksler (2006) for general external anatomy; Brown (1973) and Haidarliu et al. (2012Haidarliu et al. ( , 2013 for rhinarium topography; Quay (1954) and Carleton (1980) for soft palate morphology; Carleton (1973) for stomach gross morphology; Vorontsov (1967) for caecum anatomy; and Hooper and Musser (1964) for male genital anatomy.
According to Percequillo (2015: 360) in M. hammondi "the forefeet are robust and completely covered above by short brown hairs. The hind feet are densely covered by short hairs above that are overall whitish or grayish, but brown basally and white apically. Ungual tufts are short and sparse but extend to the tips of the claws. " The MECN 6228 allows improvement of this cheiridia description, based of museum skins. The fore foot has robust and proportionately stocky and short fingers (Fig. 3A, B). Dorsally, the metacarpal region is covered by long, but sparse brown hairs, while the fingers are coated with whitish hairs not concealing the dermal scales. Palmar anatomy involves five fleshy pads; although they are large, an important portion of the palmar surface is not formed by pads, but by squamated skin. In this respect, a significant space is left between the groups of interdigital pads and the palmar pads, suggesting it as one of the main axes to manus flexion. While the pollex is short and bearing a nail, the remaining fingers are roughly subequal in length and terminate in short claws, basally opened and covered by sparse whitish ungual tufts. Each main finger has four or five internal smooth rings and a turgent distal callus. The hind foot resembles the fore foot in dorsal coat, general finger morphology and ungual tufts development (Fig. 3C, D). The digits are comparatively short; the plantar portion is short and broad, acquiring a subtriangular outline. The interdigital pads are similar in size although pads 2-3 are slightly larger than 1-4; the hypothenar pad is small relative to the total plantar area. The latter is covered by scales surrounding the interdigital pads, but smooth between plantar pads. The inner surfaces of the fingers are basally annulated by scaled rings and distally annulated by smooth rings and terminate in well-developed calluses; short, but acute basally-opened claws tip all digits, including the hallux (Fig. 4A).
Ear and rhinarium morphology have generally not been addressed, except for general aspects (e.g. hairiness), in sigmodontine anatomical studies, probably because both structures are poorly preserved in museum skins. Percequillo (2015: 360) stated for the original series of M. hammondi that "both external and internal surfaces of the ears are well furred with short, entirely brown hairs. " The specimen MECN 6228 has a rather simple auricular pinna, bean-shaped, easily visible above head fur and with the concha and antitragus scarcely developed. In addition, the internal surface looks almost naked and colourless, being covered towards the margin by delicate sparse whitish hairs (Fig. 3E). In most muroids, the naked rhinarium is frequently overshadowed by haired folds of the muzzle; however, the surroundings of the nostrils and the internarial septum are often free from hair and sometimes offer a variety of morphological traits (Hill and Osman 1948;Brown 1973). The specimen MECN 6228 has a moderately large rhinarium with elongated lateral nostrils slightly dorsally covered by a tuft of hairs; the dorsum (sensu Brown 1973 or regio suprarhinarica, according to Haidarliu et al. 2012) is well-developed and looks pinkish. The nasal tubercles are bulbous and rounded, being crossed transversally by three faint grooves, defining the crus superius and crus inferius. Each nostril is basally accompanied by a "pinched" alanasi ( Fig. 3F).
Although the tail was described as covered by "long hairs that partially conceal large scales" and "the tail scales and hairs are blackish or dark brown and there is no dorsoventral countershading" (Percequillo 2015: 360), in the MECN 6228, it seems naked. Actually, the tail surface is covered by short and rigid caudal triplets of hair leaving the basal scutelation clearly visible. In addition, at least at the base of the tail, the longest hair of the triplet, the median one, covers two scale rows. The tail scales are hexagonal above and squared below and the dorsoventral countershading is marked (Fig. 4B, C).
According to the studied material, the soft palate has three diastemal (complete) rugae, a condition widespread in cricetids (Carleton 1980). On the contrary, palate (or interdental) rugae are at least six and much lower in relief compared to the interdental folds of other oryzomyines (Fig. 5). The MECN 6228 revealed no gallbladder; the absence of this organ is a synapomorphy for the tribe (Voss and Carleton 1993). Its stomach fits the unilocularhemiglandular condition (Fig. 6A, B), also a widespread condition within oryzomyines (Carleton 1973;Weksler 2006). A markedly thick bordering fold bisects the organ in more or less equal-sized halves; in addition, the glandular epithelium scarcely surpasses to the left the level of the oesophageal orifice. The corpus is almost entirely lined by rugged cornified epithelium and the pre-pyloric part is well developed. The incisura angularis is very shallow (Fig. 6B). The pre-caecum intestine accounts for 550 mm, while the post-caecum intestine is about 330 m in length. The caecum is neither haustrate nor sacculate, appearing as a single pouch of about 80 mm in length; its distal portion is produced as a clearly marked appendix (Fig. 6C). Although the entire intestine looks impressive because its length, the single condition of the caecum, plus the uncomplicated colonic region, suggest a moderate digestive efficiency (Björnhag 1994;see Vorontsov 1982 for additional data on oryzomyines).
Regarding its genital morphology, the specimen MECN 6228 showed that the bacular shaft is straight, tapering distally and terminating in a weakly developed head. There is a slight expansion along the medial part of the bony shaft. The base is broad and notched in dorsal and ventral view. The cartilaginous trident is about 40% of the shaft length and the medial digit protrudes slightly beyond the lateral ones (Fig. 7D). The glan penis is large in relation to its diameter with well-defined parotoid lobes and the terminal crater directed distally, its opening bordered by a ring of tissue and lacking spines (Fig. 7A-C). There are no previous data about the postcranial skeleton in Mindomys . The MECN 6228 revealed that the tuberculum of the first rib articulates with the transverse processes of the seventh cervical and first thoracic vertebrae and the second and third thoracic vertebrae have differentially elongated neural spines, with the dorsal end of the second markedly broadened (Fig. 8B). The vertebral column is also composed by 19 thoracicolumbar vertebrae, the 16 th with moderately developed anapophyses and the 17 th with little-developed anapophyses, along with 4 sacral vertebrae and 35 caudal vertebrae with complete haemal arches only in the first, second and third. Mindomys has 12 ribs. The scapular notch extends to half of the scapula and the scapular spine reaches the caudal border (Fig. 8A). A cursory inspection of the main long bones showed the presence of a supratrochlear foramen of the humerus. The tibia in the medial view exhibits a proximal curvature with a sigmoid shape and a well-developed tibial crest. The third trochanter of the femur is barely expanded laterally and reaches the distal half. The contact between the tibia and fibula occurs in the more distal part of these bones and the fibula reaches 65% of the length of the tibia (Fig. 8).
As was noted above with respect to several traits (e.g. ears and tail hairiness, general pes morphology), the MECN 6228 departs partially from the condition described by Percequillo (2015), based on the type series of M. hammondi (see also Weksler et al. 2006). We prefer to take these differences as an expression of the almost unexplored intraspecific variability for this taxon. Having said that, the type locality of M. hammondi, "Mindo, N.W. of Quito. Alt. 4213 ft. " (Thomas 1913: 570), the provenance of most of the known specimens for the species ), is separated from Reserva Drácula by about 132 kilometres and by the deep canyon formed by the Mira River (Fig. 9). At least for the recently described Pattonimus, the recognised species appear divided by the main river courses traversing the western montane forests in northern Ecuador and southern Colombia (Brito et al. 2020). A comparable scenario for Mindomys cannot be a priori discarded.  (MECN 6228;Reserva Drácula,Carchi,Ecuador). Abbreviations: C3-C7, third to seventh cervical vertebrae; dt, deltoid tuberosity; ftf, fusion of tibia and fibula; fh, fibular head; np, neural process; sf, supratrochlear foramen; sn, scapular notch; ssp, scapular spine; tc, tibial crest; tn, trochlear notch; ttr, third trochanter; T1, T2 and T3, first, second and third thoracic vertebrae. Scale bars: 10 mm.
The phylogenetic position of Mindomys was recently explored, based on a combination of morphological and molecular traits and the genus was resolved as a member of the clade containing Nephelomys and Pattonimus (Brito et al. 2020). DNA was extracted from a muscle sample of the MECN 6228 using the Bilton and Jaarola (1996) protocol. The mitochondrial gene Cytochrome b (Cyt-b) was amplified, using primers MVZ 05 and MVZ 16H and the thermal profile of Smith and Patton (1993). A phylogenetic reconstruction under Maximum Likelihood (ML) was performed in the RAxML (Stamatakis 2014) programme; the GTR + G model was used for each of the partitions (1 st , 2 nd and 3 rd position). In addition, the genetic distance amongst MECN 6228, M. hammondi (a specimen from Esmeraldas, see  Brito et al. 2020) and Mindomys sp. (unpublished material from Cordillera de Kutukú) was calculated. The sequence of MECN 6228 was located as sister (BS = 100) to a clade including M. hammondi and Mindomys sp. (Fig. 10). The genetic distances between the studied samples ranged from 2.45% to 5.28%.
Mindomys, Nephelomys and Pattonimus share a variety of common anatomical traits and seem to represent an in-situ radiation mainly restricted to Andean cloud forests (Brito et al. 2020). However, the former departs from the others as the most specialised of this group to exploit an arboreal life condition. This is particularly reflected in the pes form and size as was early recognised by Hershkovitz (1944), but also in manus geometry as described above. Since the MECN 6228 was trapped on ground, some kind of cursorial activity is supported for this rat. In any case, the apparent scarcity of Mindomys probably mirrors its arboreal condition rather than actual rarity. Although M. hammondi was recently classified as Endangered (Roach and Naylor 2019), Data Deficient seems a more appropriate category because almost nothing is known about this cricetid.
The MECN 6228 is the first specimen of Mindomys to be added to any Ecuadorian mammal collection after more than a century since its original description. At the generic level within sigmodontines, Megaoryzomys and Nesoryzomys still lack specimens in local repositories. If a healthy exercise of sovereignty is the appropriation of biodiversity through knowledge, much remains to be done in Ecuador. This context highlights the necessity to deepen programmes of inventory and collection (Monfils et al. 2020), as well as to improve access of scholars to these resources.