Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Bezerra, Alexandra M. R. Phallic Morphology of Kunsia tomentosus (Rodentia: ) Mastozoología Neotropical, vol. 12, núm. 2, julio-diciembre, 2005, pp. 227-232 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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PHALLIC MORPHOLOGY OF KUNSIA TOMENTOSUS (RODENTIA: SIGMODONTINAE)

Alexandra M. R. Bezerra

PPG Biologia , Dept. de Zoologia, Universidade de Brasília, Brasília, DF (CEP 70910-900), ,

Key words. Baculum. Glans penis. Kunsia tomentosus. Scapteromyine group. Sigmodontinae.

The genus Kunsia Hershkovitz, 1966 com- 1980; Musser and Carleton, 1993; Miranda et prises two species, K. tomentosus al., 1999). However, Smith and Patton (1999) (Lichtenstein, 1830) and K. fronto (Winge, based on evidence from molecular characters 1887). The type locality of K. tomentosus was (Cyt b) from Kunsia, Scapteromys, restricted by Hershkovitz (1966) to the Uru- Akondontini spp., among other sigmodontine guay River, in southeastern Brazil. This spe- , questioned their systematic relation- cies was also recorded in Goiás, Mato Grosso, ship, which was corroborated recently by Minas Gerais, and Rondônia States, Brazil, and D’Elía (2003) using nuclear and mitochondrial in northeast Bolivia (Hershkovitz, 1966; DNA sequences (now including Bibimys), and Emmons, 1999; Miranda et al., 1999; Santos- verified that Scapteromyini is not monophyl- Filho et al., 2001; Rodrigues et al., 2002). etic. Gonçalves et al. (2005) in a phenetic Kunsia tomentosus is the largest living comparison using phallic morphology from sigmodontine; however, it is a very rare spe- K. fronto planaltensis, Bibimys labiosus, and cies, resulting in a few specimens deposited in Scapteromys tumidus discussed the affinity scientific collections. Due to this scarcity, data among them and also questioned the relation- on distribution, morphology, ecology, and bi- ship of Bibimys with the other two genera. ology are very rudimentary (Machado et al., Studies on male phallus in rodents have often 1998). been done by authors with purely descriptive Kunsia has been grouped with the genera purposes (Didier, 1962) or addressing the taxo- Scapteromys Waterhouse, 1837 and Bibimys nomic implications suggested by observed Massoia, 1979, in the tribe Scapteromyini, variability (e.g., Hooper and Hart, 1962; based on morphology of skull, teeth, and eco- Hooper and Musser, 1964; Lidicker, 1968; logical characters (Massoia, 1979, 1980; Reig, Pessôa et al., 1996; Colak et al., 1998). The 1980; Pardiñas, 1996). This tribe comprises morphology of the baculum has been used in sigmodontine rodents with long claws, systematic studies of rodents (e.g., Hershkovitz, palustrine, semi-aquatic and fossorial habits, 1962; Patton, 1987; Pessôa et al., 1998; Silva, which inhabits open areas of central and south- 1998), suggesting that the study of the phallus eastern Brazil, Uruguay, and parts of Argen- may be a source of morphologic information tina and Bolivia (Hershkovitz, 1966; Massoia, about the rodents diversification. The aim of

Recibido 8 diciembre 2004. Aceptación final 28 junio 2005. 228 Mastozoología Neotropical, 12(2):227-232, Mendoza, 2005 A. M. R. Bezerra www.cricyt.edu.ar/mn.htm this study is to describe the phallic morphol- and took three days. The baculum was dis- ogy of K. tomentosus comparing and discuss- sected from surrounding tissues under a stereo ing the phallic similarities with other genera microscope. Next, the baculum was stocked traditionally included in the Scapteromyini. successively in 20, 40, 80 and finally in 100% The glans penis was taken from an adult glycerin, each step taking one day. specimen collected at the Emas National Park, The measurements were taken with a 9X Goiás State (18° 15' 50'’ S, 52° 53' 33'’ W), Opaque Base Magnifier Edmund Scientific@ Brazil, now housed at the Coleção de with millimeter precision (0.1 mm). The mea- Mamíferos, Departamento de Zoologia, sures, modified from Hooper (1958), are as Universidade de Brasília, Distrito Federal, follows: 1) Total bacular length (TBL), inclu- Brazil, with the number UNB 1705. The bacu- sive terminal digits; 2) proximal baculum lum was deposited in the Museu Nacional - length (PL), osseous part; 3) distal baculum Universidade Federal do Rio de Janeiro, Bra- length (DL), cartilaginous part; 4) lateral digit zil, with the number MN 62568. length (LD); 5) middle digit length (MD); 6) The methodology to clear, stain and pre- proximal baculum osseous breadth (PB), serve the penis, and the terminology of struc- greater breadth in bottom of osseous baculum; tures follows Hooper (1958) and Lidicker 7) distal baculum osseous breadth (DB), greater (1968). The penis was taken from a specimen breadth in top of osseous baculum. All illus- fixed in 10% formalin in the field and main- trations were made with the aid of a camera tained in 70% ethanol. The external morphol- lucida. ogy of glans penis was analyzed before the The comparisons of the phallic morphology clearing process because structures, such as among the genera were performed using: spines, may be damaged or lost because of Hooper and Musser (1964) and Hershkovitz KOH action. After the analysis of external (1966) for Scapteromys, and Gonçalves et al. morphology, the penis was cleared and stained (2005) for Bibimys and K. fronto planaltensis. to examination of position of the baculum Glans. The glans penis is long, sub-cylin- inside of the penis. KOH 4% was used for drical and straight (Fig. 1). The measurements two days to clear the specimen. The process are: total length, with the apical mound in- of staining was done in 0.003% Alizarin Red, cluded, 7.5 mm; apical mound length 0.5 mm;

a bc

d

Fig. 1. Glans penis of Kunsia tomentosus (MN 62568) in views: a) ventral, b) dorsal, c) right lateral, and d) apical end. Bar=1 mm. PHALLIC MORPHOLOGY OF KUNSIA TOMENTOSUS 229

greatest diameter 3.2 mm. The epidermis of inverted heart. The distal end is almost straight, the ventral surface is smooth from its base as with a tenuous median depression, and nar- far as approximately the middle of the penis; row, capped by the distal portion of baculum. the remainder of the epidermis up to the ex- A small and tenuous back-ventral projection ternal rim of the terminal crater is covered emerges laterally on the ventral surface near with single-pointed, uniformly distributed the middle of the shaft. The dorsal part of the spines. On its dorsal surface, but from the osseous baculum has a delicate medial crest middle of the glans towards the base of the extended from the distal end until not much penis, the spines are distributed in the medial past the middle of the baculum. convergence, giving a “V” aspect to the distri- The distal portion of the baculum is carti- bution of the spines. On the middle of the laginous and has three digits that are not di- ventral surface arises a raphe that ranges from vided in the base, the lateral digits are smaller the prepuce to the external edge of terminal than the medial digit, which is long and ven- crater, giving the impression of a bisected tral, and flattened dorsally. It was not observed penis. The external edge of the terminal crater the presence of small bones inside the digits. is not corrugate, but presents single-pointed, The measures of baculum analyzed were TBL uniformly distributed spines. The internal edge = 7.0 mm, PL = 5.8 mm, DL = 1.2 mm, LD of the terminal crater is smooth and without = 1.0 mm, MD = 1.3 mm, PB = 1.8 mm and spines, and contains the urethral flap, the DB = 0.9 mm. bacular mound and the dorsal papilla. The The phallic morphology of K. tomentosus urethral flap extends beyond the crater rim, is shares with K. fronto, Scapteromys, and long, not much higher than wide, bifurcate (two Bibimys only the bacular mound slightly tri- lobules) and without spines. The bacular furcated and a reduction of the cartilaginous mound, whose extremity is above the edge of capsule of the baculum (Table 1), as already terminal crater, is a unique mass that has three delicate projections, that probably refers to the lateral and medial digits of the distal portion of the baculum. The lateral projections are a a b c little smaller than the medial bacular mound, and are dorsally curved. The dorsal papilla, which is localized immediately behind the medial flank of the bacular mound, is a simple structure, lacking spines, and flattened dorsum- ventrally. The dorsal papilla is much smaller than the urethral flap, having almost all its extent on the inside of the terminal crater, only exposing the apical end above of edge of the crater. Baculum. The length of the baculum is nearly equal to the length of the glans, and is composed by a long and osseous part, the proximal portion, and a short and cartilagi- nous part, the distal portion (Fig. 2). The proxi- mal portion of the baculum is a convex shaft, which becomes narrow at the distal end and wide at the proximal end. The proximal end of the osseous baculum is ventrally concave Fig. 2. Baculum of Kunsia tomentosus (MN 62568) and has a medial notch that seems to divide it in views: a) ventral, b) dorsal, and c) right into two parts, giving it the appearance of an lateral. Bar=1 mm. 230 Mastozoología Neotropical, 12(2):227-232, Mendoza, 2005 A. M. R. Bezerra www.cricyt.edu.ar/mn.htm

Table 1 Phallic characters conditions of Kunsia tomentosus, K. fronto planaltensis, Bibimys labiosus, and Scapteromys tumidus.

K. fronto Scapteromys CHARACTERS Kunsia tomentosus Bibimys labiosus* planaltensis* tumidus**

BACULAR MOUND Slightly trifurcated, Slightly trifurcated Slightly trifurcated, Slightly trifurcated, no spinous spinous epidermis no spinous epidermis epidermis

GLANS WALL Spiny throughout Unknown Spiny throughout Spiny throughout EPIDERMIS body wall and edge body wall, but shows body wall, but of crater collar of non-spinous shows collar of epidermis on edge non-spinous crater epidermis on edge crater

DORSAL PAPILLA Simple, dorso- Simple Simple, dorso- Simple ventrally flattened; ventrally flattened (Hershkovitz, no spines (two individuals) or 1966) or multilobate (one multilobate individual); no spine (Hooper and Musser, 1964); spines in some specimens

URETHRAL FLAP Two-lobed, no Four-lobed Two lobed, spines Four lobed, spines spines

CARTILAGINOUS Reduced, tri-peaked Reduced, tri- Reduced to a single Reduced, tri or bi- BACULUM peaked cap peaked

PROXIMAL Inverted heart- Spoon-shaped Paddle-shaped Spoon-shaped PORTION OF THE shaped, medial OSSEOUS notch BACULUM

* After Gonçalves et al. (2005). ** After Hooper and Musser (1964) and Hershkovitz (1966). observed and discussed by Gonçalves et al. Scapteromys. Neither Kunsia species showed (2005), being a derived condition among South this condition of character (present work and American Sigomodontinae (Sportono, 1992). Gonçalves et al., 2005), nevertheless only one The dorsal papilla showed two conditions, individual of each species of Kunsia was taken simple and multilobate. All the genera showed to analyses of phallic morphology, not being the simple dorsal papilla, a condition common possible to assess any pattern of variability in to other Sigmodontinae, while the multilobate this character. dorsal papilla was present in Bibimys and Two-lobed urethral flap was the only exclu- Scapteromys only. This condition is shared sive character shared between K. tomentosus with microtines (see Hooper and Musser, and Bibimys, but this was with spines in the 1964), and Gonçalves et al. (2005) suggested latter. The phallic characters shared between that this can be a plesiomorphic character or Kunsia spp. and Scapteromys are the convex may have arisen independently in Bibimys and gross baculum basally expanded and the pres- PHALLIC MORPHOLOGY OF KUNSIA TOMENTOSUS 231

ence of three cartilaginous digits undivided in Musser, 1964; Hershkovitz, 1966; Massoia, the base. The general shape of the glans penis 1979; Gonçalves et al., 2005). Therefore, for in K. tomentosus and Scapteromys spp. (long, a more comprehensive approach to the mor- sub-cylindrical and straight, with the bacular phologic patterns of phallic apparatus in the mound extending little beyond the crater rim) tribe sensu D’Elía (2003), larger is more alike than Bibimys, which showed a and more representative samples of both gen- conspicuous bacular mound in a flame-like era and species of the tribe are necessary. shape. Moreover, Bibimys presents the bacular mound covered with spinous epidermis, a I thank Reginaldo Constantino and Ulyses Pardiñas for condition not present in K. tomentosus and special comments to this paper, and Daniel O. Mesquita for reviewing the earlier versions of the text. Also I am Scapteromys spp. grateful to reviewers Guillermo D’Elía, Pablo R. K. tomentosus presents the glans wall epi- Gonçalves, Pablo Teta, and Marcelo Weksler for mak- dermis covered with spines throughout almost ing helpful comments that greatly improved the manu- all of its body and the edge of crater, which script. This study is one of the results of the project “Vertebrates of Emas National Park” led by Flávio H. differs from Bibimys and Scapteromys, which G. Rodrigues and supported by Fundação O Boticário have a collar of non-spinous epidermis on the de Proteção à Natureza/ MacArthur Foundation, Wild- edge of crater (condition present in others life Conservation Society, BP Conservation/ BirdLife In- sigmodontines, e. g., , Calomys, ternational/ Fauna and Flora International and Conser- vation International do Brasil/ Anhauser-Bush. The Holochilus and Neacomys; Hooper and Instituto Brasileiro do Meio Ambiente and Recursos Musser, 1964). The condition of this charac- Naturais Renováveis – IBAMA provided research per- ter is unknown for K. fronto. mission and the support at the Emas National Park. The D’Elía (2003) and D’Elía et al. (2005) us- Conselho Nacional de Desenvolvimento Científico e Tecnológico provided fellowship to the author (CNPq ing molecular characters showed that the Procs. 141899/2004-2). Scapteromyini tribe sensu Massoia (1979) is not monophyletic and cannot be grouped with LITERATURE CITED any other group less inclusive than Akodontini, although K. tomentosus and Scapteromys spp. COLAK E, N YIGIT, M SOZEN, and S OZKURT. 1998. formed a natural group. Gonçalves et al. Study on Taxonomic Status of Microtus subterraneus (de Selys Longchamps, 1836) and Microtus majori (2005), based on phenetic comparisons of the Thomas, 1906 (Mammalia: Rodentia) in Turkey. phallic morphology of B. labiosus, found one Turkish Journal of Zoology 22:119-130. specimen with well-differentiated glans diverg- D’ELÍA G. 2003. Phylogenetics of Sigmodontinae (Ro- ing in several characters from K. fronto dentia, , ), with special reference to the akodont group, and with additional comments planaltensis and S. tumidus. on historical biogeography. Cladistics 19:307-323. Kunsia spp. and Scapteromys shared more D’ELÍA G, UFJ PARDIÑAS, and P MYERS. 2005. An characters between each other than any of these introduction to the genus Bibimys (Rodentia: shared with Bibimys, as this last genus seems Sigmodontinae): Phylogenetic position and alpha . Pp. 211-246, in: Mammalian diversifica- to be more divergent. However, these simi- tion in the Neotropics: from chromosomes to larities are ambiguous because the polarity of phylogeography (Special volume in honor of JL these characters are unknown and several of Patton) (E Lacey and P Myers, eds.). University of them occur in the other sigmodontine rodents, California Publication on Zoology, Berkeley, Cali- fornia. as previously observed by Gonçalves et al. DIDIER R. 1962. Note sur l’os penien de quelques (2005). Any conclusion based on morphology rongeurs de l’Amerique du Sud. Mammalia 26:408- from only one individual is preliminary be- 430. cause little could be known about the intraspe- GONÇALVES PR, JA OLIVEIRA, MC OLIVEIRA, and LM PESSÔA. 2005. Morphological and cytogenetic cific variability. At present, few genera and analyses of Bibimys labiosus (Winge, 1887) (Ro- representative species of each division of dentia, Sigmodontinae): implications for its affini- Akodontini sensu D’Elía (2003) have the phal- ties with the Scapteromyine group. Pp.175-209, in: lic morphology described, and is usually based Mammalian diversification in the Neotropics: from chromosomes to phylogeography (Special volume in in small samples (e.g., this work; Hooper and honor of JL Patton) (E Lacey and P Myers, eds.). 232 Mastozoología Neotropical, 12(2):227-232, Mendoza, 2005 A. M. R. Bezerra www.cricyt.edu.ar/mn.htm

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