Osteological alterations in the tucuxi Sotalia fluviatilis ( Cetacea , Delphinidae )

We present a description of osteological alterations observed in the tucuxi, Sotalia fluviatilis (Gervais, 1853) from a sample of 43 specimens. Fractures were the most frequent alterations in the sample (16%), occurring in various regions of the skeleton such as the ribs, hyoid apparatus, transverse and neural processes of vertebrae and scapula. We observed three individuals with ankylosis between the cervical vertebrae and two individuals with morphological changes (cranio-caudally elongated hemal arch and flattened cranial margin of the scapula). The only observed pathology was a case of osteomyelitis in the left dentary, which caused the loss of teeth, deformation of the associated alveoli and the formation of a medial fistula (lingual) for drainage of purulent material. This represents the first record of osteomyelitis in S. fluviatilis.

The study of pathologies and other alterations in the bones and teeth of extant and fossil mammals has permitted an indirect mean to understanding adaptive processes, habits, lifestyle and diet, biomechanical and nutritional diseases.The correct identification of anatomical variation from specific patterns is fundamental in Zoology, where the frequent lack of such knowledge often leads to taxonomic errors (Ferigolo, 1987).Different events can leave permanent marks on the bones and reveal important aspects of the life history of a particular animal, but it is not always a simple matter to recognize which processes are involved (Simões-Lopes et al., 2008).
Fractures in different regions of the skeleton, deformities, adaptive changes in response to aging of the spine and diseases of exogenous origin have been previously recorded for Guiana Dolphins Sotalia guianensis (Van Bénéden, 1864) (Furtado & Simões-Lopes, 1999;van Bressem et al., 2007;Simões-Lopes et al., 2008), but until now this subject has not been addressed in its congener, the tucuxi [Sotalia fluviatilis (Gervais, 1853)].The current study aims to detail some of the osteological alterations that have been observed for the first time in S. fluviatilis individuals from different areas of the Amazon basin.
Observed changes from regular osteological pattern in these skeletal specimens were grouped into three distinct categories: disease (osteomyelitis), trauma and atypical morphological changes according Kompanje (1999).We analyzed specimens representing all age groups, determined according to the degree of fusion in cranial sutures and vertebral epiphysis (Dawbin et al., 1970;Perrin, 1975;Ito & Miyazaki, 1990).Diagnoses and descriptions were realized according to the methods of Kompanje (1995a,b, 1999), van Bressem et al. (2007) and Simões-Lopes et al. (2008).ABSTRACT.We present a description of osteological alterations observed in the tucuxi, Sotalia fluviatilis (Gervais, 1853) from a sample of 43 specimens.Fractures were the most frequent alterations in the sample (16%), occurring in various regions of the skeleton such as the ribs, hyoid apparatus, transverse and neural processes of vertebrae and scapula.We observed three individuals with ankylosis between the cervical vertebrae and two individuals with morphological changes (cranio-caudally elongated hemal arch and flattened cranial margin of the scapula).The only observed pathology was a case of osteomyelitis in the left dentary, which caused the loss of teeth, deformation of the associated alveoli and the formation of a medial fistula (lingual) for drainage of purulent material.This represents the first record of osteomyelitis in S. fluviatilis.

RESULTS
We observed 11 cases of osteological alterations in 25.6% of all the samples (Tab.I).No osteological alterations associated with senescence were observed.
Changes due to pathology.Osteomyelitis: We found one case of osteomyelitis (infectious spondylitis) in the midline region of the left dentary bone of one specimen (INPA MA 056).Inflammation caused the loss of teeth, local deformation of the alveoli and the formation of a medial fistula (lingual) for the purpose of draining purulent material (Fig. 1, Tab.I).
Fractures have also been reported in cetaceans (Sweeney & Hidway, 1975;Simões-Lopes et al., 2008;Groch et al., 2012).The locations and types of fractures that have been observed in cetaceans can be related to distinct causes, such as surface fractures of the fins, scapula, ribs or jaw being caused by agonistic interactions or even collisions with boats (de Smet, 1977;Ogden, 1981;Montes et al., 2004;Gerholdt, 2006;Simões-Lopes et al., 2008).However, deeper fractures, such as those which may occur in the transverse and neural processes of the vertebrae, cannot be easily attributed to external trauma, since these bones are protected by an extremely thick layer of fat and muscle (de Smet, 1977;Simões-Lopes et al., 2008).These types of fractures may be caused by excessive tension on the osteo-articular tendon structures.In such cases, it is possible that stress fractures related to locomotors muscles of cetaceans have origins in these processes especially in the thoracic region and lumbar region that serves as a potent source for the locomotor muscles of cetaceans (Simões-Lopes et al., 2008).Fractures of the hyoid apparatus must present a distinct and still unknown origin.
On the other hand, ankylosis of vertebrae is usually associated with fractures and osteomyelitis or spondyloarthritis, reducing the range of movement of the affected structures (Kompanje, 1995a(Kompanje, ,b, 1999;;Montes et al., 2004).However, the formation of large bulky syndesmophytes replacing the other parts of annulus fibrosus and leaving to an intervertebral bridge are typical from the spondyloarthritis (Kompanje, 1999).
Anatomical variation is not always a synonymous of pathology (Ferigolo, 1987), however, it is difficult to determine whether such variation reflects cases of congenital malformation or if it is simply a part of normal intra-specific morphological variation.The presence of an open neural canal in the cervical vertebrae (particularly in the Ce3 and Ce4) has been previously documented as a typical characteristic of S. guianensis in southern Brazil (Fettuccia & Simões-Lopes, 2004).However, observations of the cervical vertebrae in specimens of S. guianensis from other locations in South America confirm that an open neural process may also occur in the Ce7 in 19 to 30% of all individuals of this species (n = 222) (unpublished data) and as much as 20% of S. fluviatilis individuals (n = 31).Thus, the open neural canal in Ce3, Ce4, and Ce7 observed here is interpreted as a commonly observed feature in the two species of Sotalia, rather than a congenital malformation as suggested by van Bressem et al. (2007) and Laeta et al. (2010).
This particular case reinforces the importance of studies addressing intraspecific and interspecific morphological variation, to avoid erroneous generalizations about certain taxa, such as attributing what is actually normal variation to a case of pathology or malformation.For example, degenerative joint diseases of the human spine have long been erroneously attributed to the stress of maintaining an upright posture.However, studies of the quadruped mammals, which do not assume an upright posture, have shown that the onset of such changes in aquatic animals is actually quite common and not exclusive to bipedal animals (Ferigolo, 1983).
Pathological skeletal changes were found to be uncommon in S. fluviatilis, but this may be related to the limited sample size of the sample in regards to individuals with complete skeletons.We stress the importance of analyzing complete skeletons in studies that aim to make inferences about entire populations, considering the real possibility of underestimating the degree of osteological alterations, since very often only the skull is collected and pathologies can be limited to other parts of the skeleton.

Fig 1 .
Fig 1. Occlusal view of the left dentary of Sotalia fluviatilis (Gervais, 1853) (INPA MA 056) modified by osteomyelitis.The medial region of the dentary shows the formation of a fistula and deformation of the alveoli.Pathology indicated by the arrow.Scale bar, 3 cm.