International Journal of Morphology
On-line version ISSN 0717-9502
Int. J. Morphol. vol.25 no.3 Temuco Sept. 2007
Int. J. Morphol., 25(3)597-602, 2007.
The Hypertrophy of the Tympanic Bulla in Three Species of Dasypodids (Mammalia, Xenarthra) from Argentina
La Hipertrofia de la Bula Timpánica en Tres Especies de Dasipódidos (Mammalia, Xenarthra) de Argentina
*Squarcia, Silvia Margarita; *Sidorkewicj, Nora Silvia; **Casanave, Emma Beatriz
* Cátedra de Anatomía Comparada, **Cátedra de Fisiología Animal, Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur (UNS), 8000. Bahía Blanca, Argentina.
SUMMARY: The morphology and relative size of the tympanic bulla of three species of dasypodids from Argentina, Chaetophractus villosus, C. vellerosus and Zaedyus pichiy, were studied. The bulla was observed to be morphologically similar and evidently hypertrophied in the three species. The degree of hypertrophy was higher in C. vellerosus and C. villosus than in Z pichiy. By means of ANCOVA it was clear that, although C. villosus has a bigger skull than C. vellerosus, the relative size of their tympanic cavity was similar in both species. On the other hand, the skull of C. vellerosus and Z pichiy are of similar size but the bulla was relatively shorter in the later.
KEY WORDS: Chaetophractus villosus; Chaetophractus vellerosus; Zaedyus pichiy; Middle ear; Tympanic bulla.
RESUMEN: Fueron estudiados la morfología y el tamaño relativo de la bula timpánica, en tres especies de dasipódidos de la Argentina, Chaetophractus villosus, C. vellerosus and Zaedyus pichiy. Se observaron una morfología similar y una hipertrofia evidente en la bula en las tres especies. El grado de hipertrofia fue mayor en C. vellerosus y C. villosus que en Z pichiy. Mediante ANCOVA se demostró que, aunque el cráneo de C. villosus es mayor que el de C. vellerosus, el tamaño relativo de la bula fue similar en ambas especies. Por otra parte, la bula de Z pichiy es relativamente más pequeña que la de C. vellerosus, a pesar que sus cráneos son de tamaño similar.
PALABRAS CLAVE: Chaetophractus villosus; Chaetophractus vellerosus; Zaedyus pichiy; Oído medio; Bula timpánica.
Dasypodidae (Xenarthra) is a family of fossorial (i. e. burrowing) neotropical mammals, commonly known as armadillos, that are vastly distributed in South America, particularly in Argentina, constituting an important part of the native fauna of the continent (Gardner, 2005).
The dasypodids have been the subject of anatomical, physiological and phylogenetic studies, and some species have become important models in biomedical research (Squarcia et al, 1994, 1999, 2006; Gaudin, 2003; Casanave et al., 2006; Galindez et al., 2006; Casanave & Galindez, 2007). However, the knowledge about some biological aspects of the group is still incomplete.
The bony covering of the middle ear, the tympanic bulla, has been extensively studied in a fairly large number of mammalian groups. This cranial structure is well known to be enlarged in many subterranean and desert species, namely rodents, insectivorous, marsupials and some carnivores, which is believed to be an adaptation to increase low-frequency hearing (Burda et al, 1990a; Mason, 2001,2003; Huang et al, 2002; Schleich & Vasallo, 2003). However, reports on armadillos are scarce, and the only known contributions on the morphology of the bulla in these animals come from Frechkop & Yepes (1949), Roig (1971), Segall (1976), Patterson et al. (1989) and Wible & Gaudin (2004). All these authors described large and inflated bulla for several dasypodids, better developed than in any other group of xenarthrans.
The aim of the present work was to perform a comparative study on the morphology and relative size of the tympanic bulla in three ubiquitous representatives of south American dasypodids, the larger hairy armadillo Chaetophractus villosus (Desmarest, 1804), the screaming hairy armadillo C. vellerosus (Gray, 1865) and the pichi Zaedyus pichiy (Desmarest, 1804). It is hoped to contribute with a more in-depth knowledge of these species, and to provide a significant basis for future physiological and ecological studies on this widely varying group.
MATERIAL AND METHOD
Three species of armadillos, the larger hairy armadillo Chaetophractus villosus (n = 86), the screaming hairy armadillo C. vellerosus (n = 34) and the pichi Zaedyus pichiy (sub-species Z p. pichiy, n = 26) were involved in this study. All specimens examined are from the dasypodid's collection of the Laboratory of Comparative Anatomy (Department of Biology, National University of the South, Argentina). The sample was collected from an area of approximately 80 km around the city of Bahía Blanca (38° 42' S, 62° 16' W), Argentina. Only adults of each of the species were used in the analysis in order to eliminate age variation (Morris, 1972).
The total length of the bulla (TLB) and the total length of the skull (TLS), considered as a good indicator of the cranial size, were recorded in each species by means of a digital calliper (0.01 mm). The relationship between these two parameters was evaluated for each species using a percent bullar hypertrophy index (BHI), as follows: (TLB/TLS)x100.
Descriptive statistics including arithmetic means and standard deviation were calculated for each of the measured traits in the three species. Mean values were compared between species by means of Least Significant Difference (LSD) following one-way ANOVA (Snedecor & Cochran, 1980), and differences were considered significant when p < 0.05. The relationship between TLB and TLS (as covariable) were calculated, and an analysis of covariance (ANCOVA; p < 0.05) was performed to check the presumed relationships between these parameters in the three species (Snedecor & Cochran).
The three species under study, C. villosus, C. vellerosus and Z pichiy are similar in the morphology of the auditory region. They possess well-expanded, swollen bullae, which are totally ossified in the adults and no indication of the limits between the tympanic and the entotympanic bones are evident. These structures, dome-shaped and obliquely orientated in the basicranium (Fig. 1), hide the three middle ear ossicles (malleus, incus and stapes).
Significant differences were detected in the absolute size of the bulla between the three species, being mean TLB + SD: 12.7 mm + 0.5 mm for C. villosus, 10.6 mm + 0.2 mm for C. vellerosus, and 9.1 mm + 0.4 mm for Z pichiy (p < 0.05 in all cases).
The skull size TLS was significantly different in C. villosus (91.1 + 2.7 mm) with respect to the other two species (p < 0.05), but no significant differences were detected between C. vellerosus (66.1 + 1.8 mm) and Z. pichiy (66.8 ± 1.6 mm) (p = 0.12).
The BHI was highest in C. vellerosus (15.16 to 16.64 %; mean: 15.98 %), intermediate for C. villosus (12.61 to 14.97 %; mean: 13.96 %) and lowest for Z pichiy (12.33 to 14. 66 %; mean: 13.52 %).
The analysis of covariance between TLS (covariable) and TLB showed that, size factor of the skull excluded, there were no significant differences in the relative size of the bulla
It has been stressed that it would be ecologically advantageous for the hearing of fossorial mammals to be tuned towards low frequencies, which have been shown to be better propagated than higher frequencies in underground tunnels (Fleischer, 1978). Higher frequencies are presumably absorbed by the walls of the tunnels, whereas lower frequencies are weakened because of reflection at the walls (HeihetaL, 1986).
Several authors attempted to find morphological parameters of the middle ear apparatus for the improved audition to the low-frequency airborne sound. These adaptations include heavy auditory ossicles with loose ligamentar attachments, large tympanic membranes and an increased bullar volume (Burda et ah, 1990a, 1992; Webster & Plassmann, 1992; Mason, 2004). Indeed, the huge amount of factors involved is very complex, so that there has not been possible to identify general evolutive trends that allowed explaining a convergent pattern of evolution under similar selective pressures (Nevo, 1979; Novacek, 1993; Mason, 2001).
The adaptation of the acoustic ability to a wide range of low-frequency sounds has been well studied in subterranean mammals, mainly rodents (Bruns et ah, 1988; Burda et al, 1989, 1990b, 1992; Müller & Burda, 1989; Heffner & Heffner, 1990; Schleich & Busch, 2004; Schleich & Vasallo). Harrison (1970) hypothesised that an increase in the bullar volume results in the formation of a resonating chamber that sharpens the hearing for a sound frequency range corresponding to the rodent's own cry.
The tympanic bulla is also greatly enlarged in saltatorial rodents and other mammals that live in arid environments, and may provide habitat-specific survival value (Lay, 1972; Webster & Webster, 1984; Van der Straeten & Dieterlen, 1992; Webster & Plassmann; Huang et al). An enlarged tympanic bulla causes increased amplification of sound that allows the rodent to detect an approaching predator early (Sheets, 1989). The same author also suggested that in some species an increase in the size of the bulla could be equaled by the balancing and stabilizing activities of the ears. From the results of the present work, we verified an evident degree of hypertrophy in the tympanic bulla of the armadillos C. villosus, C. vellerosus and Z pichiy. Roig stated that the buhar hypertrophy in dasypodids augment as the species acquire increasingly eremic characters. Within this family, he mentioned three well differentiated groups according to the relative size of the tympanic cavity: i- species with no-evident hypertrophied bullae (mean bullar hypertrophy index between 4.80 and 9.09 %), that live in wet environments; ii-species with moderately hypertrophied bullae (mean index between 10.47 and 12.59 %), that range in their distribution from semi humid to semi arid biotopes; and iii- species with evidently hypertrophied bullae (mean index between 14.38 and 17.28), that are typical inhabitants of arid and semi-arid environments. The same author included in the latest group the genera Chaetophractus, Zaedyus and Chlamyphorus, and reported a different degree of hypertrophy among them. He found the lowest values of the bullar hypertrophy index for C. villosus, intermediate values for Z pichiy and the pink fairy armadillo Chlamyphorus truncatus, and the highest values for C. vellerosus. From the results of the present study, we agree with Roig in that the value of hypertrophy index was highest in C. vellerosus and lower in C. villosus. However, we disagree in the results from Z pichiy, because our index value indicates that this species would belong to the group with moderate degree of hypertrophy according to Roig's classification. Two main variability sources may be involved in this disagreement. First of all, the cited author did not mentioned the age of the animals used, consequently an age-dependent factor could be implied as generating some variability in the development of the bony structures (see Baptista et al, 2000). Secondly, and more important, intraspecific differences related with geographical variation could also exist (López-Fuster et al, 2000; Popov & Ivanova, 2002; Mazák, 2004). In fact, Roig used animals of Z p. caurinus coming from Mendoza (central west Argentina), an area that is characterised by its extreme droughty conditions. On the contrary, Z p. pichiy distinguish itself for be able to enter in less arid environments. Differences between these two subspecies for several cranial characters are available from Squarcia & Casanave (1999).
Finally, the ANCOVA was a very important tool to demonstrate that although C. villosus has a bigger skull than C. vellerosus, the relative size of their tympanic cavity is similar in both species. On the other hand, the skull of C. vellerosus and Z pichiy are of similar size but the bulla is relatively shorter in the later.
It can be concluded that, although there is not physiological information about the auditory apparatus in dasypodids, and the structure of the middle ear per se is not enough to explain their hearing capacity, the hypertrophy observed in the species under study would be a valuable starting point for testing the adaptive value of auditory specializations in the group.
Baptista, T.L.; Richardson, C. & Kunz, T.H. Postnatal growth and age estimation in free-ranging bats: a comparison of longitudinal and cross-sectional sampling methods. J. Mammal, 81(3):709-18, 2000. [ Links ]
Bruns, V.; Miiller, M.; Hofer, W.; Heth, G. & Nevo, E. Inner ear structure and electrophysiological audiograms of the subterranean mole rat, Spalax ehrenbergi. Hear. Res., 33:1-10, 1988. [ Links ]
Burda, H.; Bruns, V. & Nevo, E. Middle ear and cochlear receptors in the subterranean mole-rat, Spalax ehrenbergi. Hear. Res., 39:225-30,1989. [ Links ]
Burda, H.; Bruns, V & Müller, M. Sensory adaptations in subterranean mammals. Prog. Clin. Biol. Res., 335:269-93, 1990a. [ Links ]
Burda, H.; Nevo, E. & Bruns, V. Adaptive differentiation of ear structures in subterranean mole-rats of the Spalax ehrenbergi Superspecies in Israel. Zool. Jb. Syst., 777:369-82, 1990b. [ Links ]
Burda, H.; Bruns, V. & Hickman, G. C. The ear in subterranean Insectívora and Rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear. J. Morphol., 274:49-61,1992. [ Links ]
Casanave, E. B. & Galindez, E. J. The spleen of the armadillo: lessons of organ adaptation. In: Loughry, J. & Vizcaino, S. (eds.)., Biology of the Xenarthra, Chapter 11. University of Florida Press. ISBN: 9780813031651 (in press). [ Links ]
Casanave, E. B.; Bermúdez, P. M. & Polini, N. N. Principal coagulation factors and natural anticoagulants in the armadillo Chaetophractus villosus (Mammalia, Xenarthra, Dasypodidae). Comp. Clin. Pathol, 14 (4):210-6, 2006. [ Links ]
Fleischer, G. Evolutionary principles of the mammalian middle ear. Adv. Anat. Embryol. CellBiol, 55:1-70,1978. [ Links ]
Frechkop, S. & Yepes, J. Etude systematique et zoogéographique des Dasypodidés conserves a l'lnstitut. Bull. Inst. Roy. Sc. Nat., Bruxelles, 25(5):1-56, 1949. [ Links ]
Galindez, E; Estecondo, S. & Casanave, E. The spleen of a specially adapted mammal, the little hairy armadillo Chaetophractus vellerosus, (Xenarthra, Dasypodidae). A light and electron microscopic study. Int. J. Morphol, 24 (3):339-48, 2006. [ Links ]
Gardner, A. L. Order Cingulata. In: Wilson, D. E. & Reeder, D. M. (eds.). Mammal Species of the World, 3rd ed., Johns Hopkins University Press, Baltimore, MD, pp. 94-9, 2005. [ Links ]
Gaudin, T. J. Phylogeny of the Xenarthra (Mammalia). Senckerbergiana Biol., 83 (7):27-40, 2003. [ Links ]
Harrison, D. L. Fit to Survive: Evolutionary adaptations of both form and habit help make Arabia's desert mammals. Saudi Aramco World, 21(1 ):30-2, 1970. [ Links ]
Heffner, R. S. & Heffner, H. E. Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear. Res., 46:239-52, 1990. [ Links ]
Heth, G.; Frankenberg, E. & Nevo, E. Adaptive optimal sound for vocal communication in tunnels of a subterranean mammal (Spalax ehrenbergi). Experientia, 42:1287-9,1986. [ Links ]
Huang, G. T.; Rosowski, J. J.; Ravicz, M. E. & Peake, W. T. Mammalian ear specializations in arid habitats: structural and functional evidence from sand cat (Felis margarita). J. Comp. Physiol, 188:663-81, 2002. [ Links ]
Lay, D. M. The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents. J. Morphol, 735:41-120,1972. [ Links ]
López-Fuster, M. J.; Pérez-Hernández, R.; Ventura, J. & Salazar, M. Effect of environment on skull-size variation in Marmosa robinsoni in Venezuela. J. Mammal, 81 (3): 829-37, 2000. [ Links ]
Mason, M. J. Middle ear structures in fossorial mammals: a comparison with non-fossorial species. J. Zool. Lond., 255:467-86,2001. [ Links ]
Mason, M. J. Morphology of the middle ear of golden moles (Chrysochloridae). J. Zool. Lond., 260:391-403,2003. [ Links ]
Mason, M. J. The middle ear apparatus of the tuco-tuco Ctenomys sociabilis (Rodentia, Ctenomyidae). J. Mammal, 85 (4):797-805, 2004. [ Links ]
Mazák, J. H. On the sexual dimorphism in the skull of the tiger (Panthera tigris). Mammal. Biol, 69 (6):392-400, 2004. [ Links ]
Morris, P. A review of mammalian age determination methods. Mammal Rev., 2:69-104, 1972. [ Links ]
Müller, M. & Burda, H. Restricted hearing range in a subterranean rodent, Cryptomys hottentotus. Naturwissenschaften, 76:134-5, 1989. [ Links ]
Nevo, E. Adaptive convergence and divergence of subterranean mammals. Annu. Rev. Ecol Syst., 10:269-308, 1979. [ Links ]
Novacek, M. J. Patterns of Diversity in the Mammalian Skull In: Hanken, J. & Hall, B. K. (eds.). The Skull. University of Chicago Press, Chicago: pp. 438-545, 1993. V 2. [ Links ]
Patterson, B.; Segall, W. & Turnbull, W. D. The ear region in xenarthrans (= Edentata: Mammalia) Part I. Cingulates. Fieldiana, Geology, N. S., 18: 1-46, 1989. [ Links ]
Popov, V. V. & Ivanova, T. I. Comparative craniometrical analysis and distributional patterns of medium-sized horseshow bats (Chiroptera: Rhinolophidae) in Bulgaria. Folia Zool, 51(3):187-200, 2002. [ Links ]
Roig, V. G. La hipertrofia de la bula timpánica y su significado adaptativo en los edentados de zonas áridas. Deserta, 2:87-97,1971. [ Links ]
Schleich, C. E. & Busch, D. C. Functional morphology of the middle ear of Ctenomys talarum (Rodentia: Octodontidae). J. Mammal, 85(2):290-5, 2004. [ Links ]
Schleich, C. E. & Vasallo, A. I. Bullar volume in subterranean and surface-dwelling caviomorph rodents. J. Mammal, 84 (1)185-9, 2003. [ Links ]
Segall, W. Further observations on the ear in fossorial mammals with special considerations of Chlamyphorus truncatus (Harían). Acta Anal, 94:431-44,1976. [ Links ]
Sheets, B. S. Cranial anatomy ofJaculus orientalis (Rodentia, Dipodoidea): New evidence for close relationship of dipodoid and muroid rodents. Undergraduate Honors Thesis, Baruch College, New York, 37 p., 1989. [ Links ]
Snedecor, G. W. & Cochran, W. Statistical Methods. 7th ed. Iowa State University Press, USA, 1980. [ Links ]
Squarcia, S. M. & Casanave, E. B. Discriminación entre las subspecies de Zaedyus pichiy, Mammalia, Dasypodidae, utilizando caracteres morfométricos craneanos. Physis, Sección C, 57 (132-3):19-24,1999. [ Links ]
Squarcia, S. M.; Casanave, E. B. &Cirone, G. R. Morfometría craneana de Chaetophractus villosus (Mammalia, Dasypodidae). An. Mus. Hist. Nat. Valparaíso, 22:103-6, 1994. [ Links ]
Squarcia, S. M.; Casanave, E. B. & Cirone, G. R. Sexual dimorphism in Chaetophractus villosus (Mammalia, Dasypodidae) based on craniometrical characters. An. Mus. Hist. Nat. Valparaíso, 24:91-4, 1999. [ Links ]
Squarcia, S. M.; Sidorkewicj, N. S. & Casanave, E. B. Cranial Osteology of the Armadillo Chaetophractus villosus (Mammalia, Xenarthra, Dasypodidae). Int. J. Morphol, 24 (4):541-1, 2006. [ Links ]
Van der Straeten, E. & Dieterlen, F. Craniometrical comparison of tour populations of Praomys jacksoni captured at different heights in Eastern Zaire (Kivu). Mammalia, 56 (1):125-31,1992. [ Links ]
Webster, D. B. & Plassmann, W. Parallel evolution of low-frequency sensitivity in old world and new world desert rodents. In: Webster, D. B.; Popper, A. N. & Fay R. R. (eds.). The evolutionary biology of hearing. Springer, Berlin Heidelberg New York, pp. 625-31,1992. [ Links ]
Webster, D. B. & Webster, M. The specialized auditory system of kangaroo rats. Contrib. Sens. Physiol, 5:161-96,1984. [ Links ]
Wible, J. R. & Gaudin, T. J. On the cranial osteology of the yellow armadillo Euphractus sexcinctus (Dasypodidae, Xenarthra, Placentalia). Ann. Carnegie Mus., 73(3):117-96, 2004. [ Links ]
Prof. Dra. Silvia M. Squarcia
Received: 24-05-2007 Accepted: 27-06-2007
This study was funded by SGCyT (UNS), Project 24/B122, and by ANPCyT, BID 1728/OC PICTR 074/03.