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Miscelanea sobre Bibimys (Rodentia, Sigmodontinae), un cricetido akodontino unico.

Miscellany on Bibimys (Rodentia, Sigmodontinae), a unique akodontine cricetid

Although the Argentinean mammalogist Elio Massoia (1936-2001) first "discovered" Bibimys in 1963 studying materials derived from owl pellets (E. Massoia, pers. comm. to UFJP in 1985), he spent about 2 decades to obtain trapped individuals. With 3 captured animals he named the genus and described the type species, Bibimys torresi (see Massoia, 1979). However, the action of this scholar was even more ample (Massoia, 1980) because he successfully connected the newly erected Bibimys with 2 previous and enigmatic nominal forms of the species group, from Brazil and from northeastern Argentina, both restricted by that time to their holotypes (Scapteromys labiosus Winge, 1887 and Akodon chacoensis Shamel, 1931, respectively). By the same time, Massoia (1983) documented the first notice on Bibimys populations in southern Misiones province, Argentina. Therefore, in about 5 years, a new cricetid was introduced to the sigmodontine radiation, having this genus 3 species and covering about 15[grados] of latitude in eastern tropical and subtropical South America. Up to date, despite several contributions added to the knowledge of Bibimys (Pardinas et al., 2015 and the references cited therein), the basic scenario delineated by Massoia (1979, 1983) of the 3 poorly known species remains mostly unchanged. Some issues about this rodent, such as soft anatomy, breeding, behavior, diet, among other aspects, are virtually unexplored.

Bibimys was the last member of the tribe Akodontini described from unnamed animals. The entire history of this genus is marked by the scarcity of trapped specimens. In fact, B. labiosus was described on an animal collected by Peter Lund in the first half of the XIX century (Winge, 1887); the second trapped and fully studied specimen was obtained 150 years later (Goncalves et al., 2005). The case of B. chacoensis runs in the same line: it was first described from a specimen collected in 1920 by P. Wetmore (Shamel, 1931) and redescribed from a new collected animal in 2005 (D'Elia et al., 2005). These sporadic additions, in time and space, coupled with small samples available in collections, surely favored the currently accepted alpha-taxonomy of the genus (Pardinas et al., 2015).

The goal of this note is to contribute to the knowledge of Bibimys in several aspects. Probably both the title and the contents of this work look like an old-fashioned paper. However, we are convinced that this genus exemplifies a case in which, in order to advance and to promote the interest of other scholars, the publication of miscellaneous results derived from small samples is justified.

The present contribution was based on the study of a few individuals (Appendix 1). Despite our efforts trapping in a variety of habitats, we only secured 2 specimens; in addition, we obtained 2 new animals collected by colleagues. Additionally, we explored some aspects of the bone anatomy using material retrieved from owl pellets. Several anatomical terms employed in this note were taken from Reig (1977; dental nomenclature), Carleton (1980; soft anatomy) and Voss (1988; general cricetid anatomy).

The type species of the genus, B. torresi Massoia, 1979, is today paradoxically the least known (for example, there is only 1 published photograph of a skull belonging to this species; see Nowak and Paradiso, 1983:599). According to Massoia (1979:1) the holotype was secured in the Estacion Experimental Agropecuaria (EEA) del INTA Delta del Parana (34[grados]10' S and 58[grados]51' W); the buildings of this experimental station are located on the left (north) margin of the Parana de las Palmas River, about 10 km downstream of Campana. Massoia (1979:3) recorded a second locality for torresi as "... confluencia del arroyo Las Piedras con el arroyo Cucarachas;" this place (34[grados]09' S and 58[grados]47' W) was adopted incorrectly as type locality by Honacki et al. (1982:400; see also Pereira et al., 2003:128). Few records were added posteriorly to the range of the species; apparently, all of them belong to island places in the Delta del Parana (Fig. 1). A putative exception is the record published by Pereira et al. (2003) for Reserva Natural Otamendi; it was based on material derived from an owl pellet sample collected and studied by M. Lezcano (see Pardinas, 1999). Although this sample was obtained near Laguna Grande and, therefore, in the heart of the Reserva Natural Otamendi, the possibility that the single specimen of B. torresi recorded came from the neighboring island territory cannot be totally discarded. In contrast, the record for Otamendi indicated by Dyzenchauz and Massarini (1999) is directly incorrect; the 3 animals karyotyped by these authors were collected by M. I. Sanchez Lopez and collaborators at the type locality (cf. Bonaventura et al., 1991). The materials derived from owl pellets reported as "Canal 6" by Massoia et al. (1989) have the same provenance. In fact, this channel is about 1 km downstream of the type locality. Finally, the record given as Establecimiento 'Las Carabelas" (34[grados]10' S and 58[grados]44' W) associated to the San Fernando County (Pardinas et al., 2015) is incorrect, since this locality belongs to the County of Campana and it is near the type locality. In summary, the known localities for B. torresi are very few and mostly located in the vicinities of the type locality. The single exception is the record for the confluence of Brazo Largo and Brazo Chico (33[grados]48' S and 58[grados]46' W; Massoia, 1983), which extends the distribution of this rodent about 40 km NNE from its terra typica.

However, the fact that is beyond doubt is that B. torresi had a huge range across Buenos Aires Province in the recent past (e.g., Pardinas, 1995, 1999, 2000; Scheifler et al., 2012). Late Holocene occurrences for this rodent are numerous and eloquent to confirm that the species reached southerly 38[grados]S (in the locality of Centinela del Mar, Buenos Aires, Argentina; Pardinas, 1999) and westerly 60[grados]W (in the archaeological site of Calera, Buenos Aires, Argentina; Scheifler et al., 2012). During the Late Holocene, B. torresi occupied an area of ca. 120 000 [km.sup.2], about one third of the total surface of the Buenos Aires Province. In addition, the younger occurrences in this past distribution are so recent (about 3 centuries ago; Pardinas, 1995, 2000) that is hard to imagine the magnitude and speed of the regional environmental change capable to trigger the range contraction suffered by B. torresi. Moreover, in contrast to its recent low abundance, this rodent was relatively abundant in the recent past. For example, in the rich assemblage recorded at the archaeological site "El Divisadero Monte 6" (near the southern border of Samborombon Bay, Buenos Aires, Argentina), B. torresi has a relative abundance of about 7% in a total sample of 301 sigmodontine cranial remains (representing 12 species; see Teta et al., 2013). A comparable frequency is displayed by this rodent in the assemblage of Calera, an open-air archeological site located approximately at the western portion of the Tandilia range system (Scheifler et al., 2012). Conversely, relative frequencies derived from recent owl pellet samples are very low (Supplementary 1, Table S1). Hence, B. torresi clearly lost territory and also suffered an ecological decline as a component of the small mammal assemblages. In a context of rapid retraction, the persistence of relictual isolated populations is nonetheless possible. For example, a current record originally referred to B. torresi as coming from Central-East Buenos Aires Province was discarded (Pardinas, 1996). However, the coastal fringe of Samborombon Bay, a flooding area of about 150 km in length, seems prima facie a suitable area to host this rodent. J. Bianchini (pers. comm. to UFJP in 1993) trapped there an unidentified sigmodontine that was karyotypically studied by P. Kiblisky, although never published, obtaining a diploid complement of > 60 chromosomes. Probably this animal was a true Bibimys; according to Dyzenchauz and Massarini (1999), who first reported a karyotype for the genus, B. torresi has a 2n = 70. The coastal environments of Samborombon Bay were never consistently sampled with respect to small mammals.

Several new records recently published partially changed the traditional scenario of 3 species with small ranges separated by large territory gaps. Actually, only B. torresi has a small area of distribution. Thanks to the new records reported for Brazil and Paraguay (e.g., D'Elia et al., 2008; Grazzini et al., 2015), both B. chacoensis and B. labiosus have their ranges virtually parapatric (Fig. 1). B. chacoensis is recorded in an arc bordering the north limit of the large combined wetlands of Neembucu and Ibera, running from eastern Chaco to the west, through southern Paraguay to southerncentral Misiones and northeastern Corrientes to the east (Pardinas et al., 2015). B. labiosus, even discarding some individuals misidentified by Diorio (2014:figures 5, 6, 9, among others), has been recorded in Brazilian localities from Rio Grande do Sul in the south to Minas Gerais in the north (Fig. 1). Interestingly, this latter species also suffered a recent contraction of its geographic range. According to the stratigraphical record of several archaeological sites in Rio Grande do Sul, B. labiosus was a moderately abundant element during most of the Holocene (e.g., Hadler et al., 2016). In parallel, the genus has extralimital records in Quaternary assemblages from the Brazilian state of Bahia (P. Hadler, pers. comm. to UFJP). Therefore, is safe to say that B. labiosus also lost important portions of its range during the Late Holocene.

Cranially Bibimys calls attention by the combination of a short rostrum with a rounded and enlarged braincase (Fig. 2); this pair of traits is unique among living akodontines (see also D'Elia et al., 2005; Goncalves et al., 2005). Both Winge (1887) and Shamel (1931) highlighted the dominating appearance of the neurocranium in this rodent. However, several akodontines (e.g., Lenoxus, Oxymycterus), an also other non-akodontine sigmodontines (e.g., Neomicroxus, some abrotrichines), have rounded enlarged braincases, although typically combined with pointed enlarged rostra. The short rostrum of Bibimys is characterized by a well-developed hook-shaped gnathic process (Fig. 3A). The infraorbital foramen is ovoid with a basal portion unusually ample (Fig. 3B); when cleaning manually the CNP 6067 (B. torresi) we detected a thick bundle traversing the ventral part of this foramen. Frontal sinuses are unique in Bibimys, because they are ample and internally delimited by a frontal crest but not inflated or rounded as is typical in akodontines (Fig. 3C). In the zygomatic arch (Fig. 3G), Bibimys is characterized by a broad maxillary portion, a large jugal which conforms the outer wall of the glenoid cavity (Fig. 3H), and a squamosal root posteriorly linked with the hamular process of the squamosal by a continuous ridge (Fig. 3D). In this portion of the skull another singularity is present; apparently both B. chacoensis and B. torresi lack the suspensory process of the squamosal that in most sigmodontines contacts the tegmen tympani; in addition, the latter structure displays a variable development (Fig. 3D). Coupled with the enlarged braincase, the foramen magnum is huge (Fig. 3E; see also Massoia, 1979). In turn, pterygoids are small and not winged (Fig. 3F). The mandible of Bibimys looks impressive by the combination of a wide and triangular coronoid process, a bulbous capsular projection located anteriorly (Fig. 3J) and an excavated angular process crossed by a single transverse crest (Fig. 3I).

The singularity of Bibimys is not restricted to its cranial anatomy. It is 1 of the few cricetids to have a mammary dotation (first reported here based on CNP 1891, B. chacoensis; Fig. 3) composed by 2 pairs located to the rear of the body. These mammae can be equated to the pairs abdominal and inguinal (cf. Voss and Carleton, 1993:fig. 8), being both so posteriorly displaced that the latter pair looks "vaginal" (Fig. 4). Soft palate (in B. torresi, CNP 6067; Supplementary 2, Fig. S1) has 3 diastemal and 4 interdental palatal rugae; in our count of the former we include an anterior ruga that could be alternatively interpreted as the anterior border of the interdiastemal palate and, hence, not a typical ruga (cf. figures and text in Myers et al., 1990:25-26). The interdental ruga 3 does not reach the palate midline. Both B. chacoensis (based on CNP 756 and CNP 1891) and B. torresi (CNP 6067) shares a hemiglandular-unilocular stomach, although the glandular portion is notably small (Supplementary 3, Fig. S2); the same pattern was reported for B. labiosus (Goncalves et al., 2005). No gall bladder was found in specimens CNP 756 (B. chacoensis) and CNP 6067 (B. torresi); in contrast, the scrutiny of the CNP 1891 (B. chacoensis) revealed a minute structure placed between lobules 3 and 4 of the liver than can be equated with a gall bladder. A gall bladder was recorded as present in B. labiosus (based on 2 individuals; see Goncalves et al., 2005) and also listed as a feature in the generic diagnosis constructed by D'Elia et al. (2005). Both intraspecific and intrageneric variation have been recorded in akodontines regarding this organ (see Geise et al., 2004).

A final issue we want to briefly discuss is the life style of Bibimys. Since its original description several authors attributed to these mice "fossorial" or "semi-fossorial" habits (e.g., Mas soia, 1979; Pardinas, 1996). However, it is hard to imagine any fossorial strategy for a terrestrial rodent living in periodically flooded areas, a widespread feature of the ranges occupied by both B. chacoensis and B. torresi. Even with a restricted view of requirements of a fossorial lifestyle, it is clear that Bibimys is not a fossorial sigmodontine. However, some anatomical traits displayed by this rodent can be associated mostly with adaptations to a feeding behavior based on the active search on ground surface and to root in litter and the upper part of the soil. The amazing and unique "pink" nose of Bibimys seems a delicate structure with sensory function (Supplementary 4-5, Videos S1-S2). The poorly developed manual and pedal claws depart from the expectation for a true fossorial rodent (see the discussions in Hershkovitz, 1966 and Pearson, 1984), but can be associated to general digging activities. Finally, the poor development of mystacial vibrissae suggests reduced participation in searching activities. There is no information about diet for Bibimys. However, the moderate degree of hipsodonty displayed by this rodent can be linked to the consumption of an important quantity of hard green material.

The phylogenetic position of Bibimys is still a matter of controversy (D'Elia et al., 2005; Pardinas et al., 2015). Most of the data here commented highlighted its singularity among the akodontine radiation (see also Goncalves et al., 2005). However, dental morphology in Bibimys is very close to those of Kunsia and Gyldenstolpia (Pardinas, 1996; Pardinas et al., 2008 [2009]). Akodontini is in need of a deep revision; fortunately, this task is in progress (C. Canon, pers. comm.) and the potential results illuminating the intergeneric relationships of Bibimys and associated taxa are exciting.

Recibido 13 febrero 2017. Aceptado 2 abril 2017. Editor asociado: E Lessa

Acknowledgments. This contribution was possibly thanks to several scholars that donated to our collection the animals trapped, including personal of the Instituto Nacional de Enfermedades Virales Humanas "Dr. Julio I. Maiztegui" and L. Antoniazzi, P. Beldomenico and J. Pereira. Material from Contreras Collection was kindly loaned by Y. Davies. J. Pereira and N. Fracassi freely shared data. J. Notarnicola, M. Lareschi, R. Robles and J. Sanchez assisted in the several field trips performed; also J. Notarnicola deserves the merit in obtaining the movies presented here as supplementary material. Funds for the cabinet research were derived from PICT (Agencia) 2014-1039 (to UFJP). We really appreciate the help received from the above-mentioned persons and institutions.


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Specimens studied in this contribution belong to following collections: Coleccion de Mamiferos and Coleccion de Material de Egagropilas y Afines "Elio Massoia" del Centro Nacional Patagonico (CNP and CNP-E, respectively; Puerto Madryn, Chubut, Argentina), Coleccion de Mamiferos del Museo Municipal de Ciencias Naturales y Tradicional de Mar del Plata "L. Scaglia" (MMP-Ma; Mar del Plata, Buenos Aires, Argentina), Coleccion Elio Massoia y familia (CEM; acquired by the Fundacion de Historia Natural Felix de Azara, Buenos Aires, Argentina), Coleccion Julio Contreras (C; acquired by the Fundacion de Historia Natural Felix de Azara, Buenos Aires, Argentina).

Bibimys chacoensis (n = 16). Argentina, Chaco Province: 7 km S Puerto Las Palmas (27[degrees] 9' 40.36" S and 58[degrees]40' 27.54" W), CNP 1891, a lactating female collected by C. Galliari on May 29, 2008; Escuela Jose Zubiaur, Cancha Larga (27[grados] 4' 36.8" S and 58[grados] 43' 50.9" W), CNP 756, a scrotal male collected by C. Galliari and U. Pardinas on July 7, 2000; Paso Mono, Las Palmas (27[degrees] 02' S and 58[degrees] 39' W), C-01580, an adult male collected by A. Contreras and Y. Davies on December 13, 1984. Misiones Province, Leandro N. Alem (27[degrees] 35' S and 55[degrees] 20' W), CNP 792, a scrotal male collected by INEVH on May 19, 2004; Misiones (exact locality not known), CEM 6963, an adult male collected by E. Massoia; Estancia Santa Ines (27[degrees] 31' S and 55[degrees] 51' W), CNP-E 187, cranial remains from owl pellets collected by S. Cirignoli and U. Pardinas on March 15, 2001; Campo Viera (27[degrees] 19' S and 55[degrees] 03' W), CEM 10110, 10117, 10126, 10133, 10137, cranial remains from owl pellets collected by J.C. Chebez and S. Heinonen Fortabat.

Bibimys torresi (n = 3). Argentina, Buenos Aires Province, 2.3 km NNW EEA del INTA Delta del Parana (34[degrees] 9' 23.41" S and 58[degrees] 52' 23.45" W), CNP 6067, an adult male collected by L. Antoniazzi and P Beldomenico on September 5, 2011; EEA del INTA Delta del Parana (34[degrees] 10' S and 58[degrees] 51' W), CEM 5067 (holotype; skin renumbered as C-005391), an adult male collected by E. Massoia, A. De Simone, E. Torres and A. Torres on December 15, 1975; MMP Ma 3705, an adult male collected by M. I. Sanchez Lopez on November 10, 1989.


Supplement 1: Table S1. Relative abundance of Bibimys torresi in owl pellet assemblages recorded in Delta del Parana area, Buenos Aires Province, Argentina.

Supplement 2: Fig. S1. Bibimys torresi (CNP 6067; Delta del Parana, Buenos Aires, Argentina): A. Soft palate in ventral view; B. Soft palate in lateral view; C. Anterior portion of the tongue in dorsal view. Abbreviations: d1 = diastemal ruga 1; d2 = diastemal ruga 2; d3 = diastemal ruga 3; in = incisor; M1 = first upper molar; r1 = palatal ruga 1; r2 = palatal ruga 2; r3 = palatal ruga 3; r4 = palatal ruga 4.

Supplement 3: Fig. S2. Stomach anatomy of an adult female of Bibimys chacoensis (CNP 1891; 7 km S Puerto Las Palmas, Chaco, Argentina). A. External appereance in ventral view; B. Partially dissected (note the small antrum cavity); C. Totally dissected ("butterfly").

Supplements 4-5: Video Si-Video S2. Videos taken in wild after trapping of an adult female of Bibimys chacoensis (CNP 1891; 7 km S Puerto Las Palmas, Chaco, Argentina) May 29, 2008.

Ulyses F. J. Pardinas (1), Damian Voglino (2), and Carlos A. Galliari (3)

(1) Instituto de Diversidad y Evolucion Austral (IDEAus-CONICET), Puerto Madryn, Chubut, Argentina. [Correspondence: Ulyses Pardinas <>]

(2) Museo de Ciencias Naturales Antonio Scasso, Don Bosco 580, San Nicolas de los Arroyos, Buenos Aires, Argentina.

(3) Centro de Estudios Parasitologicos y de Vectores (CEPAVE-CONICET-UNLP), La Plata, Buenos Aires, Argentina.

Caption: Fig. 1. Upper panel: Current (shading) and past (lined) geographic ranges for the 3 recognized species of Bibimys: A) B. labiosus; B) B. chacoensis; C) B. torresi. Lower panel: current recording localities for B. torresi in Delta del Parana. References: 1) EEA del INTA Delta del Parana (type locality); 2) 2.3 km NNW EEA del INTA Delta del Parana; 3) Canal 6; 4) Otamendi Natural Reserve near Laguna Grande; 5) Confluencia arroyo Las Piedras y Cucarachas; 6) Establecimiento "Las Carabelas;" 7) Confluencia Brazo Largo y Brazo Chico.

Leyenda: Fig. 2. Bibimys torresi (CNP 6067; Delta del Parana, Buenos Aires, Argentina), skull in dorsal I (A), ventral (B) and lateral (C) view, and right I mandible in labial (D) and lingual (E) view. I Scale = 10 mm. I

Caption: Fig. 3. Selected anatomical details on the skull and mandible of Bibimys torresi (CNP 6067; Delta del Parana, Buenos Aires, Argentina): A. Rostrum in lateral view; B. Rostrum in anterior view; C. Right interorbital region in dorsal view; D. Temporal region in lateral view; E. Occipital region in posterior view; F. Basal region in ventral view; G. Zygomatic arch in external view (arrow points the anterior expansion); H. Squamosal articular region in ventral view; I. Angular shelf in dorsal view; J. Vertical ramus in labial view. Abbreviations: ab = auditory bulla; ag = angular process; c = coronoid process; cj = capsular projection; cp = condyloid process; f = foramen magnum; f = frontal; fc = frontal crest; fs = frontal sinuse; gc = glenoid cavity; gp = gnathic process; i = incisor; if = infraorbital foramen; ju = jugal; ly = lacrimal; m = malleus; M = molar; ms = maseteric scar; ms = mesopterygoid fossa; n = nasal; o = occipital; pm = premaxillary; pp = parapterygoid plate; pt = pterygoids; sq = squamosal; sr = squamosal ridge; tt = tegmen tympani; z = zygomatic plate.

Caption: Fig. 4. Ventral view of an adult female of Bibimys chacoensis (CNP 1891; 7 km S Puerto Las Palmas, Chaco, Argentina) showing mammary dotation. Inset: detail of the genital region in caudal view. Abbreviations: a = anus; ap = abdominal pair; c = clitoris; ip = inguinal pair; la = left abdominal nipple; ra = rigth abdominal nipple; ri = right inguinal nipple; sn = supernumerary nipple; v = vagina.
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Author:Pardinas, Ulyses F.J.; Voglino, Damian; Galliari, Carlos A.
Publication:Mastozoologia Neotropical
Date:Jun 1, 2017
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