A new species of Pterygodermatites (Spirurida: Rictulariidae) in Marmosa constantiae Thomas, 1904 from an ecotone area of the biomes Cerrado/Amazon in the Mato Grosso State, Brazil

A new species of nematode, Pterygodermatites (Paucipectines) sinopiensis n. sp. is described based on specimens recovered from the intestine of the white-bellied woolly mice opossum, Marmosa constantiae, trapped in the municipality of Sinop, Mato Grosso state, Brazil. The genus Pterygodermatites has 21 species described in mammals worldwide, and to date, only two species have been described for marsupials in Brazil. The new species is characterized by the presence of 23 small denticles and by the presence of 38–40 and 65 pairs of the cuticular processes in male and female species, respectively. Additionally, male species possess three ventral precloacal fans, and in female species, the cuticular processes are divided into 41 pairs of comb-like and 24 pairs of spine-like processes; the vulva opens approximately in pair 41. This study describes the parasite species fifth of marsupials in the Neotropical region.


Introduction
The marsupial Marmosa constantiae Thomas, 1904 has a geographic distribution restricted to the central region of South America, occurring in the regions of Bolivia, Argentina, Paraguay, and west-central Brazil (1). It has an arboreal habit, often found in the understory of forests and only occasionally on the ground with an insectivorousomnivorous feeding habit (2)(3)(4). .
The Cerrado and Amazon biomes exhibit great biodiversity of small wild mammals but are still little studied (5), as well as their endoparasites, mainly helminths.
The transitional phytogeography of the state of Mato Grosso in the north is formed by ecotones from Cerrado/Amazon biomes and is characterized by two ecotones: seasonal semideciduous forest/ombrophilous forest and seasonal deciduous forest/ombrophilous forest (6).
The first helminth in M. constantiae was nematodes belonging to the subfamily Subulurinae Travassos, 1914, genus Subulura eliseae (7). The morphological characteristics of the genus Pterygodermatites Wedl, 1861 are based on the oral opening position and the total number of cuticular projections, the number of prevulvar cuticular projections in female species, the positions of the papillae on the posterior end, and the size of the spicules in male species (8). The subgenus Paucipectines occurs mainly in the Americas and parts of Asia and includes 21 described species found in rodents, marsupials, bats, and armadillos (9, 10).
Here, we report a new species of Pterygodermatites parasitizing M. constantiae, thus contributing to the inventory of the helminth biodiversity of this host. The stomach, the intestine, the lungs, and the thoracic and abdominal cavities of the hosts were searched for helminths. All helminths found were collected and processed according to Hoffman (11) and stored in 70% ethanol. For morphological characterization, specimens were clarified in 50% glycerol, and drawings were produced with the aid of a camera lucida attached to a Nikon Eclipse E200MVR light microscope (Nikon Corporation, Tokyo, Japan). The structures observed using a compound microscope (Zeiss Standard 20) were measured from digital images captured by TCapture Imaging Application software Version 5.1.1.0 (N). All measurements are given in micrometers, with mean ± SD, and followed by parentheses for the range (minimum and maximum). The prevalence, abundance, and mean intensity of parasitism of the helminth species found were calculated according to Bush et al. (12).

Materials and methods
For scanning electron microscopy (SEM), four specimens (two male and two female species) were processed according to a protocol modified by Souza et al. (13). Then, the samples were critical point dried in CO 2 , mounted on metal stubs, and coated with gold (20 nm). Specimens were examined using a JEOL JSM-6390 LV microscope (JEOL, Tokyo, Japan) at the Rudolf Barth Electron Microscopy Platform Oswaldo Cruz Institute, Fiocruz PDTIS/FIOCRUZ.

Results
A total of 93 specimens (four male and 89 female species, sex ratios 1/22) of helminths of the genus Pterygodermatities were obtained in the small intestine from 16 host specimens among the 53 marsupials examined.

Description General morphology
Small-sized nematodes, with the body slightly widened at the posterior end, with thick cuticles are present. The oral opening is apical asymmetric, with somewhat hexagonal, thick margins, and is surrounded by four pairs of papillae, two cephalic pairs, and two internal labial pairs. Amphids are laterals. Six denticles on each lateroventral margin and 11 denticles on the dorsal margin are present in both sexes. Buccal capsule with thick walls and strongly sclerotized, with three esophageal teeth, the dorsal with irregular edges, and the lateroventral teeth sharp ( Figures 1A-C). Two subventral rows of cuticular projections are organized in pairs in both sexes, appearing spine-like along the body, with variable shape, size, and distance from each other, according to their location, starting at end of the buccal capsule and ending at the anus in females and in males anteriorly of ventral fans ( Figures 1A, 2a,d). A single type of cuticular .
/fvets. .   projection was present in males (combs), and two different types were present in females: simple spines and combs.
Male (holotype and one paratype, two specimens studied by SEM) The  Figure 1B). The dimension of the total esophagus was 600 ± 106.78 (534-760) length, the muscular portion was 240 ± 93.5 (143-368), and the glandular portion was 359 ± 157.5 (313-551). The nerve ring was located at 141 ± 11.6 (125-148) from the anterior end and the excretory pore, and deirids were not observed, curved ventrally at the posterior end. Ten pairs of basal-like type papillae, arranged as two pairs of precloacal papillae, 1 pair ad-cloacal, and seven pairs post cloacal, the last organized into four pairs of sessile papillae close to the cloacal opening, arranged in two pairs on each side, followed by more three pairs arranged at the same distance to each other, up to the tip of the tail (Figures 2h-j). Phasmids were between the ninth and the tenth pair of papillae ( Figure 2j). Three, semicircular cuticular fans were located on the ventral surface of the body, anterior to the first pair of precloacal papillae (Figures 1D, 2g). Spicules were unequal in size, with the left being 108 ± 25.6 (81-111) long and the right being 74 ± 21.1 (53-95) long. Gubernaculum was small, coneshaped, and poorly sclerotized, with a dimension of 18 ± 1.5 (17-20) long ( Figure 1D).

Remarks
According to Quentin (8), the morphology of the buccal capsule of the specimen described, especially the apical position of the oral opening, enables us to include in the subgenus Pterygodermatites   (8). Pterygodermatites (Paucipectines) sinopiensis n. sp. by presenting the morphology of the buccal capsule hexagonal, the apical position of the oral opening, enables us to include them in the subgenus P. (Paucipectines). Although the number of prevulvar cuticular processes (41) is higher than that established by  for the diagnosis of the subgenus as well as by Ezquiaga et al. (14), we also propose that the range of this character needs to be revised since other species included in this subgenus also have a high number of prevulvar cuticular processes (8,14).
In this study, we expand the number of described species in Brazil to four: P. (P.) elegans, P. (P.) zygodontomis, P. (P.) jagerskioldi, and P. (P.) sinopiensis n. sp. Therefore, the new species is the 22nd species of the subgenus described worldwide. At this time, of the 22 species described for this subgenus, we found parasites of rodents (13), armadillos (2), marsupials (5), and bats (2).
Evaluating the group of host species of the family Didelphidae, we considered that the helminth fauna studied so far is incomplete. Analyzing just the genus Transition areas often do not receive attention for biodiversity conservation strategies, although these areas may generate responses about the host-parasite relationship. The Cerrado-Amazon transition area is situated in a strongly anthropized area and even in these conditions; it is the habitat of four species of Marmosa (M. budini, M. murina, M. demerarae, and M. constatiae). In this sense, further investigations into the remaining species of these host groups are necessary to understand the associated parasitological fauna, which could result in the description of numerous new species of helminths, such as representatives of Pterygodermatites.

Data availability statement
The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: http://zoobank. org/, A86526C1-26BF-42F5-B2C5-163914BE3F64.

Author contributions
BA analyzed and measured the helminths, produced the illustrations, and wrote the manuscript. NC analyzed and measured the helminths and revised the manuscript. RR and RP collected host marsupials and parasitic helminths and revised the manuscript. AJ reviewed all the stages of the study. All the authors reviewed and approved the final version of the manuscript.
the Universidade Federal Mato Grosso for the donation of the helminths used in this study.