Bone histology of Broad-snouted Caiman Caiman latirostris (Crocodylia: Alligatoridae) as tool for morphophysiological inferences in Crocodylia

Abstract

Bone histology is an important tool for the interpretation of life patterns in animals of the past and extant fauna. The crocodylians have been studied as important inferential models for morphophysiological characteristics. We aimed to characterize the osteohistology of captive Caiman latirostris, identifying its microanatomy related to growth rates, ontogeny, and environmental conditions. We analyzed five pairs of humeri (proximal elements of the appendicular skeleton) and ribs (axial skeleton) of females’ caiman. Ribs showed, in general, woven-fibered tissues, with low vascularization and parallel-fibered bone and many resorption and erosion cavities. It presented lines of arrested growth (LAGs) in three individuals, without skeletochronological compatibility. Humeri showed a gradient of woven-fibered to parallel-fibered and lamellar-zonal bone as the individuals aging. We observed compacted coarse cancellous bone (CCCB) and a higher number of LAGs in older specimens. Ribs remodel faster than humerus, showing an intra-individual histovariability. The humeri indicated an evident growth pattern with different ontogeny stages and growth rates in different ages. Fast-growing tissues are uncommon in crocodylians, but basal metabolism and optimal growth conditions can lead to this. Bone histology of C. latirostris shows patterns that can be used as inferential models for extant and extinct groups, but we encourage further studies for a better understanding, under different environmental conditions, such as temperature and food availability.

Ontogenetic and interelemental study of appendicular bones of Caiman latirostris Daudin, 1802 sheds light on osteohistological variability in crocodylians

“…However, given that Moleón et al (2023) found that temperature had no effect on digestion in C. latirostris , caution that perhaps other factors may also be affecting growth. Curiously, the humerus of a 1‐year‐old C. latirostris studied previously (Mascarenhas‐Junior et al, 2021; Figure 13) did not show growth marks as we observed in our specimens. The specimens studied by Mascarenhas‐Junior et al (2021) were also captive specimens that were housed in Porto Feliz, São Paulo, Brazil, where the average temperatures are higher than in Santa Fé, Argentina (where our specimens were recovered from; 21.2°C and 19.1°C, respectively; Climate Data, 2023).…”

“…Curiously, the humerus of a 1‐year‐old C. latirostris studied previously (Mascarenhas‐Junior et al, 2021; Figure 13) did not show growth marks as we observed in our specimens. The specimens studied by Mascarenhas‐Junior et al (2021) were also captive specimens that were housed in Porto Feliz, São Paulo, Brazil, where the average temperatures are higher than in Santa Fé, Argentina (where our specimens were recovered from; 21.2°C and 19.1°C, respectively; Climate Data, 2023). Thus, we propose that the additional LAGs we observed in our young individuals are in response to the prevailing harsh environmental conditions they encountered in the first few months of their lives.…”

“…These alternating periods of growth are evidenced by variations in the type of bone tissue and in the presence of growth marks (either line of arrested growth [LAGs], or LAGs associated with annuli; e.g., Andrade & Sayão, 2014; Chinsamy, 2023; Chinsamy‐Turan, 2005; Company & Pereda‐Suberbiola, 2017; Hutton, 1986; Klein et al, 2009; Lee, 2004; Peabody, 1961; de Ricqlès et al, 2003; Tucker, 1997; Tumarkin‐Deratzian, 2007; Wink et al, 1987; Woodward et al, 2011). Although the microstructure of long bones of crocodylians shows a preponderance of parallel‐fibered bone (PFB) (e.g., A. mississippiensis, Crocodylus niloticus Laurenti, 1768, Gavialis gangeticus [Gmelin, 1789], Dyrosaurid ; Chinsamy, 1991; Hutton, 1986; Lee, 2004; Padian et al, 2004; Peabody, 1961; Reid, 1990; Tucker, 1997; Woodward et al, 2011, 2014), the presence of woven bone (WB) and fibrolamellar bone (FLB) has been also observed in captive specimens, in sick individuals, and in wild juveniles and adults (e.g., Andrade et al, 2018; Chabreck & Joanen, 1979; Chinsamy, 1991; Enlow, 1969; Horner et al, 2001; Mascarenhas‐Junior et al, 2021; Reid, 1996; de Ricqlès et al, 2003; Tumarkin‐Deratzian, 2007; Werning, 2013; Woodward et al, 2014). The correlation between the organization of the bone matrix, growth dynamics, and environmental seasonality has been supported in different species of Crocodylia such as Alligator (Woodward et al, 2011, 2014), Crocodylus (Peabody, 1961; Hutton, 1986), Gavialis (de Buffrénil, 1982), and Caiman (Andrade et al, 2018).…”

“…Foote (1911) and Enlow and Brown (1956) were among the first to describe the histology of long bones and osteoderms of living crocodylians, and since then, numerous studies have been carried out on both, extant (e.g., Audije‐Gil et al, 2023; de Buffrénil, 1982; Chinsamy, 1991, 1993a, 1993b; Cubo et al, 2012; Erickson & Brochu, 1999; Hutton, 1986; Klein et al, 2009; Lee, 2004; Mascarenhas‐Junior et al, 2021; Rainwater et al, 2021; Tucker, 1997; Tumarkin‐Deratzian, 2007; Werning, 2013; Woodward et al, 2011, 2014), and extinct taxa of this group (e.g., Andrade & Sayão, 2014; Company & Pereda‐Suberbiola, 2017; Erickson & Brochu, 1999; Padian et al, 2004; Pellegrini et al, 2021; Sayão et al, 2016). It is noteworthy that, although studies on bone microstructure of Crocodylia are becoming more numerous, the diversity of species studied remains scarce.…”

“…It is noteworthy that, although studies on bone microstructure of Crocodylia are becoming more numerous, the diversity of species studied remains scarce. In this regard, although much research has focused on the Alligatoridae clade (e.g., especially on Alligator mississippiensis Daudin, 1801; Klein et al, 2009; Lee, 2004; Tumarkin‐Deratzian, 2007; Woodward et al, 2011, 2014), few studies have been done on Caimaninae (Andrade et al, 2018; Mascarenhas‐Junior et al, 2021), and so far, only the study by Mascarenhas‐Junior et al (2021) focuses on the histology of humerus and rib of juveniles C. latirostris from Brazil. Also, although the osteohistology of living crocodiles has been reasonably well published, most of the works analyze either an ontogenetic series of a single bone element or numerous postcranial bones from single juvenile or subadult specimens of a particular species (e.g., Audije‐Gil et al, 2023; Chinsamy, 1991, 1993a, 1993b; Lee, 2004; Woodward et al, 2014), and currently there are no studies that have analyzed the overall osteohistological changes that occur in the skeleton during growth (see below).…”