A 3D journey on virtual surfaces and inner structure of ossa genitalia in Primates by means of a non-invasive imaging tool

Federica Spani,Matteo Bettuzzi,Monica Carosi,Maria Pia Morigi,Massimiliano Scalici,Carlo Meloro

doi:10.1371/journal.pone.0228131

Abstract

Novel bio-imaging techniques such as micro-Computed Tomography provide an opportunity to investigate animal anatomy and morphology by overcoming limitations imposed by traditional anatomical drawings. The primate genital bones are complex anatomical structures whose occurrence in both male penis (baculum) and female clitoris (baubellum) may be difficult to assess in individual cadavers. We tested a 3-step methodological protocol, including different techniques ranging from inexpensive/simple to more expensive/sophisticated ones, by applying it to a sample of primate species, and resulting in different levels of data complexity: (1) presence/absence manual palpation method; (2) 2D X-ray plates; 3) 3D micro-CT scans. Manual palpation failed on 2 out of 23 specimens by detecting 1 false negative and 1 false positive; radiography failed once confirming the false positive, however firmly disproved by micro-CT; micro-CT analysis reported the presence of 9 bacula out of 11 male specimens and 1 baubellum out of 12 female specimens. A different baculum position was identified between strepsirrhine and haplorrhine species. We also aim to assess micro-CT as a non-invasive technique providing updated anatomical descriptions of primate ossa genitalia. Micro-CT 3D volumes showed the surface of some bones as rough, with a jagged appearance, whereas in others the surface appeared very smooth and coherent. In addition, four main types of bone internal structure were identified: 1) totally hollow; 2) hollow epiphyses and solid diaphysis with few or several channels inside; 3) totally solid with intricate Haversian channels; 4) totally solid with some channels (structure of single baubellum scanned). Ossa genitalia appeared as a living tissue having its own Haversian-like channels. The high resolution of micro-CT 3D-images of primate genital bones disclosed additional form variability to that available from genital bone 2D images of previous studies, and showed for the first time new internal and external morphological characters. Moreover, micro-CT non-invasive approach proved appropriate to recover much of scientific knowledge still hidden and often neglected in both museum specimens and primate cadavers only destined to necropsy.

Highlights

Novel radiological techniques have greatly advanced our knowledge in animal morphology, allowing to quantify internal anatomy with higher degree of accuracy, using non-invasive approaches
We show how 3D high resolution virtual reconstructions of penile and clitoral bones reveal to be a precious source of knowledge in primates as well, disclosing for example (i) exact spatial position of bones inside tissues of external genitals, (ii) external and inner morphological variability, and (iii) the importance of relying on detailed 3D data in order to make meaningful comparative studies among primate species. 3D models of ossa genitalia have been stored in a permanent archive, available for further functional analyses
Micro-CT validated X-ray plates (X-rays) showing the presence of a baculum in 9 out of 11 male specimens, i.e., 5 strepsirrhines and 4 haplorrhines:1) Galagoides demidoff; 2) Galago gallarum; 3) Loris lydekkerianus; 4) Loris tardigradus; 5) Otolemur crassicaudatus; 6) Chlorocebus aethiops; 7) Mandrillus sphinx; 8) Papio cynocephalus; 9) Saguinus niger

Summary

Introduction

Novel radiological techniques have greatly advanced our knowledge in animal morphology, allowing to quantify internal anatomy with higher degree of accuracy, using non-invasive approaches. Bio-imaging techniques overcome these methodological limits since they produce virtual 3D models which, in addition, provide the access to more detailed descriptors of morphological variation. In comparison with other imaging techniques, the strengths of micro-CT lie in its high-resolution imaging, scanning efficiency, relative low cost, and totally non-destructive approach reaching a whole 3D inspection of the sample [7]. Micro-CT provides a reliable working platform enabling numerous morphological and functional imaging applications, suitable for small animals or other biological structures. This is the case of the primate small genital bones, known as baculum in males and baubellum in females

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Conclusion