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Description on anatomy and histology of Echinometra mathaei (Echinoidea: Camarodonta: Echinometidae), the Persian Gulf sea urchin

Echinoids were collected at depth of 0-5 m from coastal water of Larak Island, the Persian Gulf in January 2016. Soft tissues of the animal including peristome, peritoneum, gills, podium, ampulla, axial organ, gonads and food canal were taken and fixed in %10 formalin. Five micron sections were stained by hematoxylin and eosin method and studied under light microscope. The anatomy and histology of organs including peristome, peritoneum, gills, podium, ampulla, axial organ, gonads and food canal were investigated. In oral view, peristome, mouth, teeth, gills, spines, and pedicellariae were the six major compartments. Correspondence K Pooshang Bagheri, Venom and Biotherapeutics Molecules Lab, Medical Biotechnology Dept, Biotechnology Research Center, Pasteur Institute of Iran, Tehran, Iran (e-mail: k_bagheri@pasteur.ac.ir). Aboral view was seen as a round shape consisted of tube feet, spines, pedicellariae, madreporite, genital plate, ocular plate and anus. In both oral and aboral view seven types of spines and five types of pedicellariae were reported. Histological evaluation showed the organization of their layers and cells. In this study some anatomical and histological features of the Persian Gulf Echinometra mathaei were characterized. The data presented in this paper could be illuminating the path for marine biologists, anatomists, and histologists to use this creature in their desired research areas, basic or industrial approaches.


Sample collection
Five specimens of E. mathaei ranged from 55 to 70 g were collected manually at depth of 0 to 5 m from coastal waters of Larak island, The Persian Gulf (26°51'12" N 56°21'20" E) in January 2016. The specimens were kept alive and transferred to the laboratory. The specimens were maintained in a flow-through aquarium and were acclimatized at least for two weeks prior to experiments. Genus and species of the collected specimens were determined based on morphological determinants described by Price (1983 and1986).

Anatomy
To study of the anatomy of the specimen, its general characteristics including shape, size, color, spines, tube feet, and shell were investigated.
External view was classified to oral and aboral poles. In oral view, mouth and its peripherals (i.e. teeth, peristome, and pedicellariae) were investigated. In aboral view, anus, madreporite, gonopores, and genital plate and foramen were studied.
Before access to internal organs, to ethically manipulation of the specimens, they incubated on ice for 45 min. In internal view, coelomic cavity, digestive system, Aristotle's lantern, ampulla, gonads, epithelium (Peritoneum), and axial organ were evaluated.
All of observations were macroscopically documented by a digital camera (canon kiss x3).

Histology
Internal organs including epithelium, tube feet, ampulla, axial organ, digestive system, peristome, and gonads were removed on ice and fixed in buffered formal (10%, pH = 7) (Sigma Co. Germany) . After 48 h, the tissue samples were processed in an automated tissue processor and embedded in paraffin wax. The sections at 4-5 µm thick were prepared and stained with hematoxylin and eosin (H&E) stain.

Taxonomy of E. mathaei
The position of this genus is presented in Table 1.

Anatomy
External anatomy was classified to oral and aboral views. In general view, peristome, tube feet, spines, pedicellariae, and gills were seen.
E. mathaei was spherical in shape and had a dark violet or brown color. The size of our samples was varied from 4 to 8 cm. The average weight of the samples was 65 ± 5 g.

Oral view
In oral view, peristome, mouth, teeth, and gills were the four major compartments (Fig.1).

Peristome and mouth
Peristome consisted of a peripheral layer in red color ( Fig. 2A) that was free of spines and a few small pedicellariae located on its surface ( tissues in pink color were located in the below of each tooth (Fig. 2B). In semi-or complete closed mouth view, an array of many overlapped conical tissues was seen in pink to red color that was surrounded by a circular dark red line (Fig. 2B). Since, 5 pairs of small thick tube feet were located just in the periphery of the mouth, it was speculated that these were interfering to tightly sticking to the desired food to immobilizing it to be dispersed by the teeth.

Spine
The large spines were conical rods that small parallel grooves conducted from their base to the head. The head seemed to be smaller and thinner than the pink body (Fig. 3). The body of spine was originated from a flat red or brown base. A white spotted margin between base and rod was shown under normal or artificial light.
The colors of large spines under flash light were green to brown from the base to the head whereas in normal light the spine color was dark brown.
All spines were conical dark brown rods that originated from a red-brown flat base.
Some miniaturized spines were located between tiny, mini and small size spines in oral and aboral views (Fig. 3).  The pedicellariae were distributed between the spines and tube feet in oral and aboral surfaces ( Fig. 4 and 7).

Tube feet
Three kinds of tube feet were seen. The two of them were large in size and other type was very small. The two large ones were distributed in oral and aboral views in five rows that were classified to two types including oral and aboral tube feet.
Oral tube foot was consisted of a small cylindrical tube that terminated toward a larger discus head. It was white with a small central foramen. A small bilateral groove was also conducted from shell to head. Aboral tube foot had a thinner cylindrical tube that terminated toward a smaller discus head. It had a similar bilateral groove too.
Small tube feet were located in the periphery of mouth between pedicellariae. Their shapes were the same as large one except for its light red discus head and dark brown dwarf thick body.
The numbers of small tube feet were 10 feet that located in pairs in a circle external line in reference to the mouth cavity ( Fig. 1, 4, and 5).

Gills
Five pairs of gills resembling undulating white mass were located in the periphery of peristome. Each of them had several main branches that accessory branches were originated from the main one and protruded toward the surface ( Fig.1 and 5).

Aboral view
Aboral view was seen as a round shape consisted of tube feet, all kinds of aforementioned spines, pedicellariae, madreporite, genital plate, ocular plate and anus ( Fig. 6A).
In this view, anus was surrounded by a few series of small spines (Fig. 6A, B). Tube feet were exposed in five radial rows in pairs ( A. Ten meridional rows of tube feet, or podia, expand between the oral and aboral poles. The ten rows of tube feet were decorated into five ambulacra including two rows of tube feet each. The ambulacra were separated by zones without tube feet, known as inter-ambulacral zone. B. The periproct was a small region at the aboral pole circumfluent the anus.

Test
The test was seen as an oval shaped light green hemisphere. The pores corresponding to a tube foot located on test as four pairs and in some cases five pairs that elongated in a semi-circle line between two spines. One of each pore in alternate between the tubercle of two spines had larger size (Fig. 9).

Internal anatomy
In internal view, Aristotle's lantern, peritoneal membrane and cavity, axial organ, water vascular system, gonad, and digestive system were characterized. Digestive system was attached by mesenteries on the walls of the test (Fig. 10).

The nervous system
The nervous system had a simple plan but it is difficult to observe the neural ring in dissections. There was a large nerve ring surrounding the mouth inside the lantern. Five nerves radiate followed the radial canals of the water vascular system that was originated from the nerve ring (Fig. 10). Figure 10. Demonstration of the digestive and nervous systems. Internal organs were located in peritoneal cavity that dissected from other organ by peritoneal membrane. The gonads were surrounded by this membrane. Esophagus was originated from aboral end of the lantern and conducted to stomach. Intestine was shown as vesiculated organs that located in peritoneal cavity and fastened to internal skeleton by several ligaments.

Peritoneum (Peritoneal membrane)
Peritoneum was adjacent to all internal organs, including gonads, digestive system and Aristotle lanterns, and was filled with a liquid called the coelomic fluid. The outer and inner layers of peritoneum were adjacent to the internal skeleton and the coelomic fluid, respectively ( Fig. 11, 12). ossicles and related muscles within each ones; these largest bone-like structures resembled a pyramid. The pyramids can act as 'jaws', in the sense that they support the teeth. The five pyramids kept up five fragments called rotulas that attached to them by protractor and retractor muscles which provided extension and flexion of the lantern (Fig. 11).

Aristotle's lantern
A bony appendix designated 'perignathic girdle' was elongated from test to internal space (Fig.11). The girdle joined the test to the lantern out of the muscle groups. The lantern included four different groups of muscles including protractors, retractors, interpyramidals and compass elevators.
Protractor muscles were lengthening from the aboral surface of the pyramids to the pergnathic girdle. Retractor muscles were extended from the internal oral pole of the pyramid to the auricles (Fig. 11, 12).

Figure 11
. Anatomical demonstrations of the Arisototle's lantern and other internal organs. The lantern was elongated from oral to aboral end. In this view, it conducted to a pyramidal section that five teeth are protruded from. In aboral view, five curved forks were elongated from lateral body to ring canal. Five radial canals were located between those curved forks surrounded by peripharengial coelom. Reproductive system as a plenty of yellow-golden gonads is located in the periphery of the cavity that ended to five gonopores in aboral view.  (Fig. 13).

Water vascular system
The water-vascular system started from madreporite through the body (Fig. 6). The madreporite directed to stone canal that was linked into an axial organ, resembling an oval shape sac. The stone canal was a tiny, short, and clear tube that came from one side of the madreporite and opens into the ring canal or water ring (Fig. 13). The ring canal was encircling the mouth which extended to five radial canals. Each of five radial canals made its way to an ambulacrum on the test and then led to the ampulla from which the podia (tube feet) were originated (Fig. 13). Figure 13. Demonstration of water vascular system. Water vascular system was originated from madreporite and ended to tube feet. Axial organ was originated from the lower part of madreporite that connected to ring canal. Five radial canals was branched from ring canal that elongated to water canal from which paired ampullae were originated from and protruded as tube feet toward external environment.

Histology Peristome
Peristome is composed of two main layers including a surface dense multi-layered called 'lip' and connective tissue inner layer. The lips contain medium size cells with highly basophilic dense nucleus and moderately eosinophilic cytoplasm (Fig. 14).

Gills
In the cross section of gill, main and accessory brunches were observed. Lumen's wall was figured by two layers of cells which surrounded the inner connective tissue layer (Fig.16).

Podium (tube foot)
In cross section of a tube foot from lumen to external layer, the cell layers included a basophilic epithelium layer, highly eosinophilic elongated muscles ordered like flagella bundles, a moderately eosinophilic connective tissue, a compact layer bearing neural cell layer with highly basophilic nucleus and highly eosinophilic cytoplasm, and finally several arrows of epithelial cells (Fig.17). the boundaries of these tubules (Fig.19). Reproductive cells were located centrally and their N/C ratio was significantly high (Fig. 20).    E. mathaei like other species of the sea urchins has a specialized jaw structure to permit them to feed effectively on algae. This similarity is might due to similar diet for crushing the soft and hard foods. Kaneko (1975), Cook and Kelly (2007) were stated that E. mathaei can feed from algae but this question is claimed that, why these hard teeth are observed in their mouth. We proposed that E. mathaei can feed from hard materials that must be investigated in future studies.

Discussion
Anatomical and histological descriptions of the food canal of regular echinoids were given by Chadwick (1900) and Stott (1955). Even though E. mathaei is a common sub tidal species along the world`s oceans, no detailed anatomical and histological studies on its digestive system have been made yet.
Some limited studies about axial organ had been conducted by Millott and Vevers (1964), Bachmann and Goldschmid (1978), Anteunis, Leclerc, Vial, Brillouet, Luquet, Robineaux and Binaghi (1985), and Welsch and Rehkamper (1987). They were stated that the axial organ Meanwhile, similar cells are seen inside the tissue, which have similar morphology to exiting cells. These cells seem to be migrating to the perineum interior layer. Liebman (1950) suggested that peritoneum epithelium is the source of coelomocytes in Arbacia punctulata.  (Tyler, 1939;Nichols, Bishop & Sime 1985). In Echinoidea the gonads are either ovaries or testes and are different in color.

Conclusion
In this study some anatomical and histological