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Skull Ontogeny of Lycalopex Culpaeus (Carnivora: Canidae): Description of Cranial Traits and Craniofacial Sutures

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Skull Ontogeny of Lycalopex Culpaeus (Carnivora: Canidae): Description of Cranial Traits and Craniofacial Sutures DOI 10.1515/mammalia-2012-0028 Mammalia 2013; 77(2): 205–214 Valentina Segura * Skull ontogeny of Lycalopex culpaeus (Carnivora: Canidae): description of cranial traits and craniofacial sutures Abstract: Ontogenetic changes in the skull of Lycalopex about 163 mm in length. The pups nurse until they are culpaeus were studied in relation to feeding function and 2 months old and continue to depend on their parents performance at different age classes. Most cranial changes during a relatively short postweaning period; in this time, occurred in the orbitotemporal region and consisted of they learn to hunt until they are strong enough to fend for the visible appearance of structures that were later found themselves. Juveniles reach adult size at 7 months, and to be absent in juveniles. These changes were related to sexual maturity is attained during the first year (Crespo the development of the adult skull in order to capture, and De Carlo 1963 , Ewer 1973 ). kill, and process prey. In general, fusion occurred earlier The patterns of cranial ontogeny in canids have been in neurocranial sutures than in the splachnocranium, studied from diverse perspectives and using different although rostral sutures never became fused. The cranial approaches. Wayne (1986) studied ontogenetic trajec- sutures of culpeo are conservative, displaying few changes tories of skull growth in the domestic dog, using bivari- in suture type but some in suture fusion sequence. These ate and multivariate analyses. More recently, La Croix modifications occur during the first year, from the late et al. (2011a,b) examined the cranial growth and devel- juvenile stages, when individuals are similar to adults in opment of the coyote through two-dimensional geomet- general appearance and body size as well as in skull size. ric morphometric analyses and analyzed the ontogenetic However, it was noted that basicranial synchondroses relations between feeding performance, dentition, and became fused in the adult stages, indicating that longitu- feeding biomechanics. Drake (2011) studied heterochro- dinal growth could extend until this latter time. This could nic patterns in the skull morphology of domestic dogs be indicative not only of size change in adult specimens by using three-dimensional geometric morphometrics. but also of shape change. In a recently published work, Segura and Prevosti (2012) quantitatively analyzed the ontogenetic pattern of the Keywords: anatomy; development; ontogeny; skull; skull of Lycalopex culpaeus , using traditional and geomet- suture morphology. ric morphometric analyses. Although such works repre- sent important contributions to the knowledge of cranial ontogeny for canids in general and L. culpaeus in par- *Corresponding author : Valentina Segura, Divisi ó n Mastozoolog í a , ticular, several structural transformations and changes Museo Argentino de Ciencias Naturales “ Bernardino Rivadavia ” , Av. Á ngel Gallardo 470, CP 1405, Ciudad Aut ó noma de Buenos Aires , in sutural morphology have not yet been discussed or Argentina , e-mail: [email protected]; [email protected]; and detected using either geometric or linear morphometric CONICET, Consejo Nacional de Investigaciones Cient í ficas y analyses. These changes (some of which have high func- T é cnicas, Av. Rivadavia 1917, CP 1033, Ciudad Autónoma de Buenos tional meaning) may be difficult to study using quanti- Aires, Argentina tative analyses. For instance, the structural morphology of craniofacial sutures is linked to the mechanical strain caused by tensile and compressive forces (Henderson Introduction et al. 2005 ). Such sutures, formed by collagenous connec- tive tissue fibers that connect mineralized bones, allow Lycalopex culpaeus (Molina 1782), the culpeo fox, is the deformation and minor displacements, thus absorbing largest ( ≈ 10 kg) in its genus, and the second largest among and transmitting mechanical stresses, and play an impor- South American canids (Novaro 1997 ). The culpeo fox is tant role as growth sites in the growing skull (Wagemans distributed along the Andes and hilly regions of South et al. 1988 , Jaslow 1990 , Herring and Teng 2000 , Mao America, from Colombia to southern Chile and Argentina 2002 , Rice 2008 , Jasinoski et al. 2010 ). (Jim é nez and Novaro 2004 ). Culpeos are born with their In carnivores and other mammals, several morpho- eyes closed and at 2 days they weigh about 168 g and are metric changes along ontogeny have been related to the Brought to you by | De Gruyter / TCS Authenticated | 212.87.45.97 Download Date | 4/30/13 2:26 PM 206 V. Segura: Skull ontogeny of Lycalopex culpaeus optimization of feeding and biting (e.g., Abdala et al. 2001 , A3: complete permanent dentition with dentine horns Flores et al. 2006 , Segura and Flores 2009 , Flores et al. exposed on the cusps of premolars and molars; I3 at 2010 , Segura and Prevosti 2012 ), and similar changes have the same level of development as I1 and I2 been detected in phylogenetically distant species. Such patterns have been observed in published works that deal Although previous works have shown the existence of with the structural-descriptive morphology of the skull and some sexual dimorphism involving cranial and external sutural changes along ontogeny in carnivorans and other measurements in Lycalopex culpaeus (Crespo and De mammals (e.g., Garc í a-Perea 1996 , Giannini et al. 2006 , Carlo 1963 , Johnson and Franklin 1994 , Travaini et al. Segura and Flores 2009 , Flores and Barone 2012 ); however, 2000 ), no such dimorphism was observed in the char- these studies are limited to only a few species. acters or sutures discussed here (i.e., males and females In this work, I studied changes in the skull morphol- showed the same ontogenetic pattern). ogy and pattern of sutural change (i.e., type, degree of For the qualitative analysis, skull characters were fusion) in an ontogenetic series of Lycalopex culpaeus , compared across specimens in different ontogenetic exploring the relation of these changes with life history stages; the type and degree of fusion in sutures and events that took place during the development of indivi- synchondroses were examined, and the observed dif- duals. Despite some knowledge of the ontogeny of L. cul- ferences were described using the anatomical terminol- paeus (e.g., Crespo and De Carlo 1963 , Novaro 1997 , Segura ogy defined by Evans (1993) , Garc í a-Perea (1996) , and and Prevosti 2012 ), several skull characteristics with func- Gilbert (1997) . Although the anatomy of the whole skull tional meaning (e.g., development of processes, crests, has been explored in a functional context (e.g., Van Valk- and suture morphology) have not yet been assessed. Thus, enburgh 1991 , Van Valkenburgh and Koepfli 1993 , Slater in this widespread South American canid, this approach et al. 2009 ), in this work I focused only on those charac- will contribute to the knowledge and understanding of the ters that presented variation along the ontogeny of Lyca- development of the skull as a whole. lopex culpaeus . Depending on the shape of the apposed edges, sutures were classified following Evans ’ proposal for canid skulls (1993): plane suture, in which bones meet at a right-angled edge or surface; squamous suture, which Materials and methods articulates by overlapping of reciprocally beveled edges; serrated suture, which articulates by means of recipro- I studied a sample of 101 specimens of Lycalopex culpaeus cally alternating processes and depressions; and foliate collected in 1963 by Crespo and De Carlo in Argentina, suture, in which the edge of one bone fits into a fissure or Neuqu é n Province, Cat á n-Lil (39 ° 33 ′ S, 70 ° 35 ′ W), and recess of an adjacent bone. A suture was considered fused deposited in the mammal collection of Museo Argentino when it was no longer visible. de Ciencias Naturales Bernardino Rivadavia (MACN, see Appendix 1). In the sample, individuals ranged in age from 2 months to 11 years (Crespo and De Carlo 1963 , Zapata Results et al. 1997 ). Twenty-nine of the specimens did not show fully erupted teeth. Using the scheme followed by Segura Thirty morphological characters were identified that and Prevosti (2012) , I defined seven age classes based on changed along the ontogenetic series and did not show tooth eruption and wear (Figures 1 A – D and 2 ): intra-age class variation (Table 1 , Figures 1 and 2). Most J1: complete deciduous dentition present; permanent P1 changes occurred in the orbitotemporal region (10 charac- and p1 erupting ters), followed by the mandible (9), basicranial and audi- J2: permanent I1, i1, and i2 erupted; I2, M1, and m1 tory regions (4), rostrum (3), and palatal and occipital erupting regions (both with 2 characters). Twelve of them consisted J3: permanent incisors and canines erupted; M1 and p2 of the appearance of structures absent in juveniles (charac- erupted; P4, M2, and m2 erupting ters 4, 6, 8, 9, 11, 13, 18, 19, 20, 21, 27, and 30 in Table 1), while J4: permanent incisors, canines, and molars fully almost a third of those changes implied growth or enlarge- erupted; P3, p3, p4, and m3 erupting ment of structures already present in juveniles (characters A1: complete permanent dentition with no wear 12, 14, 15, 16, 17, 23, 24, 26, 28, and 29); a few changes implied A2: complete permanent dentition with slight wear; inci- a relative decrease in size or disappearance of structures sors, canines, premolars, and molars with blunt cusps with advancing age (characters 2, 3, 7, and 10), while some Brought to you by
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