Underwater photogrammetry for close-range 3D imaging of dry-sensitive objects: The case study of cephalopod beaks
Corresponding Author
Marjorie Roscian
Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France
Mécanismes Adaptatifs et Evolution (Mecadev), Muséum National d'Histoire Naturelle, CNRS, Bâtiment d'Anatomie Comparée, Paris, France
Correspondence
Marjorie Roscian, Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, 8 rue Buffon, CP 38, 75005 Paris, France.
Email: [email protected]
Contribution: Conceptualization (lead), Formal analysis (lead), Methodology (lead), Visualization (lead), Writing - original draft (lead)
Search for more papers by this authorAnthony Herrel
Mécanismes Adaptatifs et Evolution (Mecadev), Muséum National d'Histoire Naturelle, CNRS, Bâtiment d'Anatomie Comparée, Paris, France
Contribution: Project administration (equal), Supervision (equal), Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorRaphaël Cornette
Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
Contribution: Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorArnaud Delapré
Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
Contribution: Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorYves Cherel
Centre d'Etudes Biologiques de Chizé, UMR7372, CNRS-La Rochelle Université, Villiers-en-Bois, France
Contribution: Resources (equal), Writing - review & editing (equal)
Search for more papers by this authorIsabelle Rouget
Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France
Contribution: Project administration (equal), Supervision (equal), Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorCorresponding Author
Marjorie Roscian
Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France
Mécanismes Adaptatifs et Evolution (Mecadev), Muséum National d'Histoire Naturelle, CNRS, Bâtiment d'Anatomie Comparée, Paris, France
Correspondence
Marjorie Roscian, Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, 8 rue Buffon, CP 38, 75005 Paris, France.
Email: [email protected]
Contribution: Conceptualization (lead), Formal analysis (lead), Methodology (lead), Visualization (lead), Writing - original draft (lead)
Search for more papers by this authorAnthony Herrel
Mécanismes Adaptatifs et Evolution (Mecadev), Muséum National d'Histoire Naturelle, CNRS, Bâtiment d'Anatomie Comparée, Paris, France
Contribution: Project administration (equal), Supervision (equal), Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorRaphaël Cornette
Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
Contribution: Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorArnaud Delapré
Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
Contribution: Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorYves Cherel
Centre d'Etudes Biologiques de Chizé, UMR7372, CNRS-La Rochelle Université, Villiers-en-Bois, France
Contribution: Resources (equal), Writing - review & editing (equal)
Search for more papers by this authorIsabelle Rouget
Centre de Recherche en Paléontologie-Paris (CR2P), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France
Contribution: Project administration (equal), Supervision (equal), Validation (equal), Writing - review & editing (equal)
Search for more papers by this authorAbstract
- Technical advances in 3D imaging have contributed to quantifying and understanding biological variability and complexity. However, small, dry-sensitive objects are not easy to reconstruct using common and easily available techniques such as photogrammetry, surface scanning, or micro-CT scanning. Here, we use cephalopod beaks as an example as their size, thickness, transparency, and dry-sensitive nature make them particularly challenging. We developed a new, underwater, photogrammetry protocol in order to add these types of biological structures to the panel of photogrammetric possibilities.
- We used a camera with a macrophotography mode in a waterproof housing fixed in a tank with clear water. The beak was painted and fixed on a colored rotating support. Three angles of view, two acquisitions, and around 300 pictures per specimen were taken in order to reconstruct a full 3D model. These models were compared with others obtained with micro-CT scanning to verify their accuracy.
- The models can be obtained quickly and cheaply compared with micro-CT scanning and have sufficient precision for quantitative interspecific morphological analyses. Our work shows that underwater photogrammetry is a fast, noninvasive, efficient, and accurate way to reconstruct 3D models of dry-sensitive objects while conserving their shape. While the reconstruction of the shape is accurate, some internal parts cannot be reconstructed with photogrammetry as they are not visible. In contrast, these structures are visible using reconstructions based on micro-CT scanning. The mean difference between both methods is very small (10−5 to 10−4 mm) and is significantly lower than differences between meshes of different individuals.
- This photogrammetry protocol is portable, easy-to-use, fast, and reproducible. Micro-CT scanning, in contrast, is time-consuming, expensive, and nonportable. This protocol can be applied to reconstruct the 3D shape of many other dry-sensitive objects such as shells of shellfish, cartilage, plants, and other chitinous materials.
CONFLICT OF INTEREST
None declared.
Open Research
DATA AVAILABILITY STATEMENT
Scans from computed tomography are available in the archive of the AST-RX platform in Paris and in National History Museum imaging archive in London, UK. Table S1: List of specimens used for the computation of mean distances can be found in DRYAD : https://doi.org/10.5061/dryad.4mw6m9095.
Supporting Information
| Filename | Description |
|---|---|
| ece37607-sup-0001-TableS1.odsapplication/excel, 28.2 KB | Table S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Abadie, A., Boissery, P., & Viala, C. (2018). Georeferenced underwater photogrammetry to map marine habitats and submerged. The Photogrammetric Record, 164(33), 448–469.
- Agrafiotis, P., Skarlatos, D., Forbes, T., Poullis, C., Skamantzari, M., & Georgopoulos, A. (2018). Underwater photogrammetry in very shallow waters: Main challenges and caustics effect removal. The International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences, XLII(2), 15–22.
10.5194/isprs-archives-XLII-2-15-2018 Google Scholar
- Baltsavias, E. P. (1999). A comparison between photogrammetry and laser scanning. ISPRS Journal of Photogrammetry & Remote Sensing, 54, 83–94.
- Bell, C. M., Hindell, M. A., & Burton, H. R. (1997). Estimation of body mass in the southern elephant seal. Mirounga Leonina. Marine Mammal Science, 13(4), 669–682.
- Bianco, G., Gallo, A., Bruno, F., & Muzzupappa, M. (2013). A comparative analysis between active and passive techniques for underwater 3D reconstruction of close-range objects. Sensors, 13, 11007–11031.
- Broeckhoven, C., & Du Plessis, A. (2018). X-ray microtomography in herpetological research: A review. Amphibia Reptilia, 39(4), 377–401.
- Bythell, J., Pan, P., & Lee, J. (2001). Three-dimensional morphometric measurements of reef corals using underwater photogrammetry techniques. Coral Reefs, 20, 193–199.
- Carlson, W. D., Rowe, T., Ketcham, R. A., & Colbert, M. (2003). Applications of high-resolution X-ray computed tomography in petrology, meteoritics and palaeontology. The Geological Society of London, 215, 7–22.
10.1144/GSL.SP.2003.215.01.02 Google Scholar
- Cherel, Y. (2020). A review of southern ocean squids using nets and beaks. Marine Biodiversity, 50(6), 1–42.
- Cherel, Y., & Hobson, K. A. (2005). Stable isotopes, beaks and predators: A new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proceedings of the Royal Society B: Biological Sciences, 272, 1601–1607.
- Christiansen, F., Sironi, M., Moore, M. J., Di, M., Marcos, M., Hunter, R., Duncan, A. W., Gutierrez, R., & Uhart, M. M. (2019). Estimating body mass of free - living whales using aerial photogrammetry and 3D volumetrics. Methods in Ecology and Evolution, 10, 2034–2044.
- Cignoni, P., Callieri, M., Corsini, M., Dellepiane, M., Ganovelli, F., & Ranzuglia, G. (2008). MeshLab: An open-source mesh processing tool. In 6th Eurographics Italian Chapter Conference 2008 –Proceedings (pp. 129–136).
- Clarke, M. R. (1962). The identification of cephalopod "beaks" and the relationship between beak size and total body weight. Bulletin of the British Museum (Natural History) Zoology, 8(10), 419–490.
- Clarke, M. R. (1986). A Handbook for the Identification of Cephalopod Beaks. Clarendon Press.
- De Menezes, M., Rosati, R., Ferrario, V. F., & Sforza, C. (2010). Accuracy and Reproducibility of a 3-Dimensional Stereophotogrammetric. Journal of Oral and Maxillofacial Surgery, 68, 2129–2135.
- Digital Fish Library (2009). Retrieved from http://www.digitalfishlibrary.org/library/. Accessed: 2020-05-02.
- Drap, P., Merad, D., Mahiddine, A., Seinturier, J., Gerenton, P., Peloso, D., & Boï, J.-M. (2013a). Automating the measurement of red coral in situ using underwater photogrammetry and coded targets. ISPRS - International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences, 2, 231–236.
10.5194/isprsarchives-XL-5-W2-231-2013 Google Scholar
- Drap, P., Merad, D., Mahiddine, A., Seinturier, J., Peloso, D., Boï, J.-M., Chemisky, B., & Long, L. (2013b). Underwater photogrammetry for archaeology. What will be the next step? International Journal of Heritage in the Digital Era, 2(3), 375–394. https://doi.org/10.1260/2047-4970.2.3.375
10.1260/2047?4970.2.3.375 Google Scholar
- Drap, P., Seinturier, J., Scaradozzi, D., Gambogi, P., Long, L., & Gauch, F. (2006). Photogram-metry for virtual exploration of underwater. In XXI International CIPA Symposium.
- Fau, M., Cornette, R., & Houssaye, A. (2016). Photogrammetry for 3D digitizing bones of mounted skeletons: Potential and limits. Comptes Rendus - Palevol, 15, 968–977.
- Figueira, W., Ferrari, R., Weatherby, E., Porter, A., Hawes, S., & Byrne, M. (2015). Accuracy and precision of habitat structural complexity metrics derived from underwater photogrammetry. Remote Sensing, 7, 16883–16900.
- Fourie, Z., Damstra, J., Gerrits, P. O., & Ren, Y. (2011). Evaluation of anthropometric accuracy and reliability using different three-dimensional scanning systems. Forensic Science International, 207, 127–134.
- Franco-Santos, R. M. & Alves Gonzalez Vidal, E. (2020). Tied hands: Synchronism between beak development and feeding-related morphological changes in ommastrephid squid paralarvae. Hydrobiologia, 847, 1943–1960. https://doi.org/10.1007/s10750-020-04223-z
- Giacomini, G., Scaravelli, D., Herrel, A., Veneziano, A., & Russo, D. (2019). 3D photogrammetry of bat skulls: Perspectives for Macro - evolutionary Analyses. Evolutionary Biology, 46, 249–259.
- Gibelli, D., Pucciarelli, V., Poppa, P., Cummaudo, M., Dolci, C., Cattaneo, C., & Sforza, C. (2018). Three-dimensional facial anatomy evaluation: Reliability of laser scanner consecutive scans procedure in comparison with stereophotogrammetry. Journal of Cranio-Maxillofacial Surgery, 46(10), 1807–1813.
- Gignac, P. M., & Kley, N. J. (2018). The utility of dicect imaging for high-throughput comparative neuroanatomical studies. Brain, Behavior and Evolution, 91, 180–190.
- Gignac, P. M., Kley, N. J., Clarke, J. A., Colbert, M. W., Morhardt, A. C., Cerio, D., Cost, I. N., Cox, P. G., Daza, J. D., Early, C. M., Echols, M. S., Henkelman, R. M., Herdina, A. N., Holliday, C. M., Li, Z., Mahlow, K., Merchant, S., Müller, J., Orsbon, C. P., … Witmer, L. M. (2016). Diffusible iodine-based contrast-enhanced Computed Tomography (diceCT): An emerging tool for rapid, high-resolution, 3-d imaging of metazoan soft tissues. Journal of Anatomy, 228(6), 889–909.
- Golikov, A., Ceia, F., Sabirov, R., Ablett, J., Gleadall, A., Gudmundsson, G., Hoving, H. J., Judkins, H., Pálsson, J., Reid, A., Rosas-Luis, R., Shea, E. K., Schwarz, R., & Xavier, J. C. (2019). The first global deep-sea stable isotope assessment reveals the unique trophic ecology of Vampire Squid Vampyroteuthis infernalis (Cephalopoda). Scientific Reports, 9, 19099.
- Guery, J., Hess, M., & Mathys, A. (2017). Photogrammetry. In Digital techniques for documenting and preserving cultural heritage (pp. 229–235). Arc Humanities Press.
10.2307/j.ctt1xp3w16.26 Google Scholar
- Haleem, A., & Javaid, M. (2019). 3D scanning applications in medical field: A literature-based review. Clinical Epidemiology and Global Health, 7, 199–210.
- Houle, D., Govindaraju, D. R., & Omholt, S. (2010). Phenomics: The next challenge. Nature Reviews Genetics, 11(12), 855–866.
- Hussien, D. A., Abed, F. M., & Hasan, A. A. (2019). Stereo photogrammetry vs computed tomography for 3D medical measurements. Karbala International Journal of Modern Science, 5(4), 201–212.
10.33640/2405-609X.1130 Google Scholar
- Kazhdan, M., & Hoppe, H. (2013). Screened poisson surface reconstruction. ACM Transactions on Graphics, 32(3), 13.
- Kikuzawa, Y. P., Toh, T. C., Ng, C. S. L., Sam, S. Q., Taira, D., Afiq-Rosli, L., & Chou, L. M. (2018). Quantifying growth in maricultured corals using photogrammetry. Aquaculture Research, 49(6), 2249–2255.
- Kraus, K., & Waldhäusl, P. (1997). Manuel de photogrammétrie - Principes et procédés fondamentaux. Hermes Sci.
- Lange, I., & Perry, C. T. (2020). A quick, easy and non-invasive method to quantify coral growth rates using photogrammetry and 3D model comparisons. Methods in Ecology and Evolution, 11, 714–726.
- Lidke, D. S., & Lidke, K. A. (2012). Advances in high-resolution imaging - techniques for three-dimensional imaging of cellular structures. Journal of Cell Science, 125, 2571–2580.
- Luhmann, T., Robson, S., Kyle, S., & Boehm, J. (2020). Close-Range Photogrammetry and 3D imaging. De Gruyter.
- Maas, H.-G. (2015). On the accuracy potential in underwater/multimedia photogrammetry. Sensors, 15(8), 18140–18152.
- Mathys, A., Semal, P., Brecko, J., & Van den Spiegel, D. (2019). Improving 3D photogrammetry models through spectral imaging: Tooth enamel as a case study. PLoS One, 14(8), e0220949. https://doi.org/10.1371/journal.pone.0220949
- Metscher, B. D. (2009). MicroCT for comparative morphology: Simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiology, 9(1), 11. https://doi.org/10.1186/1472-6793-9-11
- Miserez, A., Rubin, D., & Waite, J. H. (2010). Cross-linking chemistry of squid beak. Journal of Biological Chemistry, 285(49), 38115–38124.
- Miserez, A., Schneberk, T., Sun, C., Zok, F. W., & Waite, J. H. (2008). The transition from stiff to compliant materials in squid beaks. Science, 319(5871), 1816–1819.
- Olinger, L. K., Scott, A. R., Mcmurray, S. E., & Pawlik, J. R. (2019). Growth estimates of Caribbean reef sponges on a shipwreck using 3D photogrammetry. Scientific Reports, 9(1), 1–12.
- Ormestad, M., Amiel, A., & Röttinger, E. (2013). Chapter 9: Ex-situ macro photography of marine life in imaging marine life (pp. 210–233). John Wiley & Sons Ltd.
- Pears, N., Liu, Y., & Bunting, P. (2012). 3D imaging, analysis and applications. Springer.
10.1007/978-1-4471-4063-4 Google Scholar
- R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/. Accessed: 2020-08-18.
- Rasmussen, A. S., Lauridsen, H., Laustsen, C., Jensen, B., Pedersen, S., Uhrenholt, L., Boel, L. W., Uldbjerg, N., Wang, T., & Pedersen, M. (2010). High-resolution ex vivo magnetic resonance angiography: A feasibility study on biological and medical tissue. BMC Physiology, 10(3), 1–8.
- Remondino, F., & El-Hakim, S. (2006). Image-based 3D modelling: A review. The Photogram-metric Record, 21(115), 269–291.
- Richardson, M. (2013). Techniques and principles in three-dimensional imaging: An introductory approach. IGI Global.
- Sansoni, G., Trebeschi, M., & Docchio, F. (2009). State-of-the-art and applications of 3D imaging sensors in industry, cultural heritage, medicine, and criminal investigation. Sensors, 9, 568–601.
- Scalici, M., Traversetti, L., Spani, F., Bravi, R., Malafoglia, V., Persichini, T., & Colasanti, M. (2016). Using 3D virtual surfaces to investigate molluscan shell shape. Aquatic Living Resources, 29, 207. https://doi.org/10.1051/alr/2016019
- Schlager, S. (2017). Morpho and Rvcg - Shape Analysis in R, chapter 9 (pp. 217–256). Academic Press Inc.
- Skarlatos, D., & Kiparissi, S. (2012). Comparision of laser scanning, photogrammetry and SFM-MVS pipeline applied in structures and artificial surfaces. ISPRS Annals of the Photogrammetry, Remote Sensing and Spatial Information Sciences, XXII.
- Staudinger, M. D., Dimkovikj, V. H., France, C. A. M., Jorgensen, E., Judkins, H., Lindgren, A., Shea, E. K., & Vecchione, M. (2019). Trophic ecology of the deep-sea cephalopod assemblage near Bear Seamount in the Northwest Atlantic Ocean. Marine Ecology Progress S, 629, 67–86.
- Tafforeau, R., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., Kay, R., Lazzari, V., Marivaux, L., Nel, A., Nemoz, C., Thibault, X., Vignaud, P., & Zabler, S. (2006). Applications of X-ray synchrotron micro-tomography for non-destructive 3D studies of paleontological specimens. Applied Physics A, 83, 195–202.
- Tan, Y., Hoon, S., Guerette, P. A., Wei, W., Ghadban, A., Hao, C., Miserez, A., & Waite, J. H. (2015). Infiltration of chitin by protein coacervates defines the squid beak mechanical gradient. Nature Chemical Biology, 11(7), 488–495.
- Uchikawa, K., Sakai, M., Wakabayashi, T., & Ichii, T. (2009). The relationship between par-alarval feeding and morphological changes in the proboscis and beaks of the neon flying squid Ommastrephes bartramii. Fisheries Science, 75, 317–323.
- Uyeno, T. A., & Kier, W. M. (2005). Functional morphology of the cephalopod buccal mass: A novel joint type. Journal of Morphology, 264(2), 211–222.
- Varón-González, C., Fraimout, A., Delapré, A., Debat, V., & Cornette, R. (2020). Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii. RoyalSociety Open Science, 7, 191577.
- Vázquez-Arellano, M., Griepentrog, H. W., Reiser, D., & Paraforos, D. S. (2016). 3-D imaging systems for agricultural applications | a review. Sensors, 16, 618.
- Walter, T., Shattuck, D. W., Baldock, R., Bastin, M. E., Carpenter, A. E., Duce, S., Ellenberg, J., Fraser, A., Hamilton, N., Pieper, S., Ragan, M. A., Schneider, J. E., Tomancak, P., & Hériché, J.-K. (2010). Visualization of image data from cells to organisms. Nature Publishing Group, 7, 26–41.
- Xavier and Cherel (2009). Cephalopod beak guide for the southern ocean. British Antarctic Survey.
- Young, R. E., Vecchione, M., & Mangold, K. M. (2019). The Tree of Life Web Project : Cephalopoda Cuvier 1797. Octopods, squids, nautiluses, etc.. Retrieved from http://tolweb.org/Cephalopoda/19386/2019.03.26. Accessed: 2020-01-14.
- Zanette, I., Daghfous, G., Weitkamp, T., Gillet, B., Adriaens, D., Langer, M., Cloetens, P., Helfen, L., Bravin, A., Peyrin, F., Baumbach, T., Dischler, J.-M., Loo, D. V., Praet, T., Poirier-Quinot, M., & Boistel, R. (2013). Chapter 7: Looking Inside Marine Organisms with Magnetic Resonance and X-ray Imaging (pp. 122–184). John Wiley & Sons Ltd.
- Zelditch, M. L., Swiderski, D. L., & David, S. H. (2012). Geometric Morphometrics for Biologists: A primer. Academic Press Inc.
- Ziegler, A., Ogurreck, M., Steinke, T., Beckmann, F., Prohaska, S., & Ziegler, A. (2010). Op-portunities and challenges for digital morphology Comment. Biology Direct, 5, 45.
