Fetal bone development in the lowland paca (Cuniculus paca, Rodentia, Cuniculidae) determined using ultrasonography

Abstract

Studying the timing of the main events of embryonic and fetal development may clarify the strategies adopted by species to maximize neonatal survival and the consequences of these events for their life history. This study describes bone development during the fetal phase of the lowland paca (Cuniculus paca), comparing it with other precocial or altricial species, and its relationship with the species’ adaptive strategies. A total of 102 embryos/fetuses obtained over the course of 17 years through collaboration with local subsistence hunters in the Amazon were analyzed. Measurements of mineralization of the axial and appendicular skeletons were performed by ultrasonography using a 10–18‐MHz linear transducer. The chronological order of occurrence of mineralization in relation to the total dorsal length (TDL) was: skull (TDL = 4.1 cm); vertebral bodies (TDL = 4.6 cm); scapula, humerus, radius, ulna, ilium, ischium, femur, tibia, and fibula (TDL = 6.7 cm); ribs (TDL = 7.8 cm); clavicle (TDL = 8.5 cm); metacarpi/metatarsi (TDL = 11 cm); phalanges (TDL = 15 cm); tarsus (TDL = 18 cm); patella (TDL = 23 cm); and carpus (TDL = 27.2 cm). Secondary ossification centers first appeared in the femoral distal epiphysis (TDL = 16.6 cm) and tibial proximal epiphysis (TDL = 18.4 cm). Advanced fetuses (TDL > 30 cm, 97% gestational period) presented mineralization in all primary and most secondary centers. Compared to other species, paca neonates have a well‐developed skeletal system at birth, which is important for their independent postnatal locomotion. Our results may contribute to the monitoring of bone development in other wild species, helping us to understand their life history, and serving as parameters for comparisons between precocial and altricial mammals.

Ultrasound evaluation of fetal bone development in the collared (Pecari tajacu) and white‐lipped peccary (Tayassu pecari)

“…In peccaries, the first US signs of mineralization of the skull occur at the end of the initial third of the gestational period, similar to those observed in domestic pigs at 37 days of gestation (26% of the GP; Daneze et al, 2012) and sheep (29% GP; Harris, 1937), other precocial wild species, such as lowland paca ( Cuniculus paca ; 28% GP; Silva et al, 2020), and even altricial species, such as the owl monkey ( Aotus azarai infulatus ; 26% GP; Monteiro et al, 2011), humans (26% GP; Rosignoli et al, 2010; Jin et al, 2016), and marmosets ( Callithrix jacchus ; 27% GP; Phillips, 1976). Thus, the timing of first signs of bone mineralization is similar in precocial and altricial species, showing that the early embryo and fetal development of the skeletal system are similar in mammals (Evans & Sack, 1973).…”

“…The CRL is considered one of the selection parameters to calculate the gestational period, especially in the first stages of pregnancy (Butt et al, 2014). Similarly, the TDL may be used as an index for wild species because its values are not influenced by the handling in ultrasonography (El Bizri et al, 2017; Silva et al, 2020). Thus, measuring TDL may be an alternative method to estimate the fetal length and gestational age of conceptuses, avoiding bias due to changes in a fetal position (Andrade, Monteiro, El Bizri, Vicente, et al, 2018).…”

“…The early bone development is similar in altricial and precocial animals, with the development of the axial skeleton and primary ossification centers of long bones that allow first muscle insertions (Muir, 2000; Sinowatz, 2010). However, divergences in bone development are observed as gestation progresses, and precocial species show a more complete bone gestational development in primary and secondary ossification centers than altricial species (Li & Smith, 2019; Modina et al, 2019; Phillips, 1976; Silva et al, 2020).…”

“…The ultrasonography evaluation was based on the methodology proposed by Silva et al (2020). The skull was evaluated at the sagittal section of the interthalamic level to obtain the biparietal diameter (BPD), occipitofrontal diameter (OFD), and head circumference (HC).…”

“…The evaluation of the pelvic limb was conducted similarly to that performed on the thoracic limb, assessing the total length (mineralized and non-mineralized parts), the length of the mineralized parts, and width (near to acetabulum) of the ilium and ischium. In the pubis, the length and width of the mineralized parts were evaluated (Silva et al, 2020). The examination of the femur, tibia, and fibula was similar to the humerus (Figure 3).…”