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Micro-Computed Tomography and Histology to Explore Internal Morphology in Decapod Larvae

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Micro-Computed Tomography and Histology to Explore Internal Morphology in Decapod Larvae www.nature.com/scientificreports OPEN Micro-computed tomography and histology to explore internal morphology in decapod larvae Received: 12 April 2018 Diego Castejón 1, Javier Alba-Tercedor 2, Guiomar Rotllant1, Enric Ribes3, Mercè Durfort3 & Accepted: 10 September 2018 Guillermo Guerao4 Published: xx xx xxxx Traditionally, the internal morphology of crustacean larvae has been studied using destructive techniques such as dissection and microscopy. The present study combines advances in micro- computed tomography (micro-CT) and histology to study the internal morphology of decapod larvae, using the common spider crab (Maja brachydactyla Balss, 1922) as a model and resolving the individual limitations of these techniques. The synergy of micro-CT and histology allows the organs to be easily identifed, revealing simultaneously the gross morphology (shape, size, and location) and histological organization (tissue arrangement and cell identifcation). Micro-CT shows mainly the exoskeleton, musculature, digestive and nervous systems, and secondarily the circulatory and respiratory systems, while histology distinguishes several cell types and confrms the organ identity. Micro-CT resolves a discrepancy in the literature regarding the nervous system of crab larvae. The major changes occur in the metamorphosis to the megalopa stage, specifcally the formation of the gastric mill, the shortening of the abdominal nerve cord, the curving of the abdomen beneath the cephalothorax, and the development of functional pereiopods, pleopods, and lamellate gills. The combination of micro-CT and histology provides better results than either one alone. Decapods are an important economic resource that mobilizes billions of dollars per year in fshery and aqua- culture production1, and decapod larvae play a crucial role in population dynamics, species dispersal, settle- ment, and recruitment in marine environments2. Te capacity to explore their internal morphology in detail is important in order to understand these organisms from a functional and evolutionary perspective3–5, but few detailed studies have been made on this topic6–10. Dissection and histology are the most classical approach, but their invasiveness leads to the alteration and destruction of the specimens11. Te study of internal morphology received a signifcant advance with the arrival of confocal laser scanning microscopy (CLSM), which uses stacks of two-dimensional sections to reconstruct three-dimensional models12,13. Tis approach has been applied in non-insect pancrustaceans for the study of embryos and larvae, but it is limited by light penetration and the staining properties of the tissues14–16. A further advance was achieved with the development of micro-computed tomography (micro-CT), which uses the X-ray absorption properties of tissues to obtain the two-dimensional sections required for the recon- struction of a three-dimensional model and provides higher resolution and deeper penetration than CLSM11,17–20, allowing to look at the internal morphology of the whole animal without the need of dissection or histology4. In adult decapods, this technology has been applied in spiny lobsters to study the ossicles of the stomach21, in carid- ean shrimps to study the alimentary tract22, and in brachyuran crabs to describe their general anatomy23 and the female reproductive system24. It has also been applied to measure the volume of parasitic rhizocephalan structures inside the host body of adult decapods25. Recently, Spitzner et al.10 published a micro-CT–based study focusing on the organogenesis of larvae of the shore crab, Carcinus maenas, demonstrating the value of this technique. Micro-CT is a powerful tool for studying internal morphology but still has some limitations with regard to discriminating adjacent structures with similar X-ray absorbance and resolving the tissue arrangement. Tose 1Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37–49, 08003, Barcelona, Spain. 2Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Campus de Fuente Nueva s/n, 18071, Granada, Spain. 3Unitat de Biologia Cel·lular, Departament de Biologia Cel·lular, Fisiologia i Immunologia, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028, Barcelona, Spain. 4Independent researcher, 08028, Barcelona, Spain. Correspondence and requests for materials should be addressed to D.C. (email: diego.castejon. [email protected]) or J.A.-T. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:14399 | DOI:10.1038/s41598-018-32709-3 1 www.nature.com/scientificreports/ Figure 1. Zoea I, sagittal plane. General diagram (A). Histology, haematoxylin-eosin (B). Micro-CT volume rendering reconstruction (C). Abbreviations: AC, anterior caeca; ANC, abdominal nerve cord; CL, cortical layer of the ganglion; CS, cardiac stomach; ESO, oesophagus; G, glands; H, heart; HT, hindgut tract; M, muscles; MGl, midgut gland; MT, midgut tract; N, neuropile of the ganglion; PA, posterior aorta; PS, pyloric stomach; TGM, thoracic ganglionic mass; S, syncerebrum. limitations might be solved by combining micro-CT with histological sections. Hence, the main objective of the present study was to test the combination of micro-CT and histology for studying the general internal mor- phology of a representative decapod, the common spider crab (Maja brachydactyla Balss, 1922), during its larval stages. Results Micro-CT and histology show the internal organs and other inner structures of the larval stages of M. brachy- dactyla, zoea (Figs 1–2) and megalopa (Figs 3–6), resolving their identifcation and distribution. Te internal gross morphology (location and shape of the inner structures) is similar in micro-CT and histology (Figs 1–6). Micro-CT shows better results for studying the shape, volume, and location of several organs, resolving the gross morphology of the anatomy and the relationship among organs (Figs 1–4). Te main limitation of micro-CT lies in the difculty of identifying adjacent structures with similar X-ray absorptive properties. Histology improves the identifcation of structures with similar X-ray absorptive properties and discerns their tissue arrangement and cellular organization (Figs 1–2 and 5–6). Te resolution of micro-CT discriminates primarily the digestive and nervous systems, the musculature, the exoskeleton, and the eyes, and secondarily the respiratory and circulatory systems (Figs 1–4 and Supplementary Figs (S)8, 11, 13, 15, 17–19 and Videos 1–4). Te digestive system is located medially, between the circulatory system (positioned dorsally) and the nervous system (positioned ventrally). It is composed of the oesophagus, stomach, midgut tract, midgut caeca, midgut gland (also known as the hepatopancreas), and hindgut (Figs 1–6 SCIENTIFIC REPORTS | (2018) 8:14399 | DOI:10.1038/s41598-018-32709-3 2 www.nature.com/scientificreports/ Figure 2. Zoea I, dorso-ventral plane of the digestive system. General diagram (A). Histology, haematoxylin- eosin (B). Micro-CT volume rendering reconstruction (C). Abbreviations: CS, cardiac stomach; E, eye; HT, hindgut tract; M, muscles; MGl, midgut gland; MT, midgut tract; P, pereiopods, PA, posterior aorta; PS, pyloric stomach. and S1–17 and Videos 1–3). Te nervous system is composed of an anterior syncerebrum26 (“brain”), the thoracic ganglionic mass, and an abdominal nerve cord formed by a pair of fused nervous chains (Figs 1, 3, 4C and 5 and S1, 3–6, 8, 10, 11, 14, 15, 17 and Videos 1–3). Histology resolves in detail the circulatory and respiratory systems, and reveals the diferent glands. Te circulatory system includes a dorsal heart associated with the main arteries (Figs 1–3, 4A, 5 and 6 and S1, 3–7, 9, 10, 12, 14, 16). Te respiratory system increases in complexity afer the moult to megalopa, with the formation of gills in the branchial chamber (S14, 15 and 19). Te reproductive SCIENTIFIC REPORTS | (2018) 8:14399 | DOI:10.1038/s41598-018-32709-3 3 www.nature.com/scientificreports/ Figure 3. Micro-CT volume rendering reconstructions of diferent latero-sagittal sections of the megalopa larva from close to the lateral external wall toward the inner-medial body (A–C). Abbreviations: (*), cardio- pyloric valve; AC, anterior caeca; ANC, abdominal nerve cord; CS, cardiac stomach; ESO, oesophagus; G, glands; H, heart; HT, hindgut tract; LT, lateral tooth of the gastric mill; M, muscles; MGl, midgut gland; MT, midgut tract; PS, pyloric stomach; TGM, thoracic ganglionic mass; S, syncerebrum. system is not identifed in any larval stage. Te elements of the digestive system and nervous system are the easiest organs to observe, so they are described in detail below. Te oesophagus is a short tube that communicates the mouth opening to the ventral foor of the stomach (Figs 1, 3, 5 and S1, 3, 6). In micro-CT, the oesophagus shows a narrowing at the juncture with the stomach (Figs 1C and 3C). Histology reveals a lumen lined by a simple epithelium covered apically by a very thin cuti- cle (Figs S3, 6) and a continuous band of circular muscles (Figs 1B and S1). Te nervous system surrounds the oesophagus (S3) laterally and anteriorly forms a syncerebrum (Figs 1, 3, 5 and S1, 6). Histology also reveals small groups of rosette glands associated with the mouth opening, labrum and mouthparts (Figs 1, 5 and S1, 6), and the antennal glands located on the base of the antennae (S3). Te oesophagus is followed by the stomach; it is subdivided into the cardiac and pyloric stomach by the cardio-pyloric valve (Figs 1–6 and S1–3, 6–13). Te stomach of the zoea sustains thick, large setae over the cardio-pyloric valve (S2, 3). The pyloric stomach has postero-ventral pouches protecting the pyloric filters (S10–13). Te stomach undergoes a drastic change afer the moult to megalopa: the cardiac stomach enlarges antero-laterally and develops the ossicle armature and gastric mill (Figs 3–6 and S6–9). Micro-CT shows the single propyloric and urocardiac ossicles and the paired pterocardiac and zygocardiac ossicles (Fig. 4A), while the sharp teeth of the gastric mill are observed by either micro-CT (Fig. 3C and Video 1 time 0:40-0:45) or his- tology (S6, 7 and 9).
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