1. Introduction
Oratosquilla oratoria, commonly known as the Japanese mantis shrimp, is classified under the Class Malacostraca, within the Suborder Hoplocarida, and belongs to the Infraorder Stomatopoda [1]. It is a marine benthic creature with an extremely wide distribution, found from the coastal regions of Russia, throughout Japan and China, down to the Malay Peninsula, and across the Hawaiian Islands [1,2]. O. oratoria has high ecological and economic value. As a key species in the food chain of coastal soft mud and sandy sediment communities [3], O. oratoria plays a significant role in the balance of the marine benthic food web [4]. In China, O. oratoria is the most commercially valuable species among the Stomatopods. It has now become an essential component of China’s inshore economic fisheries [5,6]. Additionally, O. oratoria is highly favored for its rich nutritional value and tender texture, making it a popular choice for consumption. However, with the continuous increase in its economic value, overfishing of O. oratoria from the ocean has led to significant survival pressures on its population [7,8].
In order to scientifically manage and sustainably utilize O. oratoria, it is necessary to increase research on their fundamental biological aspects. Existing studies have found that O. oratoria have extremely strong raptorial claws, capable of preying on a variety of organisms, including crustaceans, mollusks, and fishes [9,10,11], which denotes a quite diverse diet. The characteristics of an animal’s digestive system can directly reflect its ability to absorb nutrients from food [12,13,14]. In other words, the digestive system of O. oratoria needs to adapt to the characteristics of its diverse diet composition. The digestive system of Malacostraca generally comprises the foregut for grinding and filtering, midgut for chemical digestion, hindgut for temporary storage of waste materials, and digestive glands for releasing digestive fluids [13,15]. However, relevant research has shown that the influence of their habitats and dietary habits will lead to the adaptation of the digestive system of different species, thus showing certain differences [16,17], such as morphological differences in the mouthparts [18,19], variations in the gastric mill [20,21,22] and differences in the development extent of the hepatopancreas [23,24]. Therefore, it is essential to conduct research on the external and internal morphological features of O. oratoria’s digestive system to better understand their nutritional requirements.
In recent years, scholars have concentrated their research on O. oratoria in areas such as reproductive biology [25,26], population structure and genetic diversity within populations [27], and systematics and molecular genomics [28]. Although one study provided a description of the gastric armature in Stomatopoda [29] and another provided a simple description of O. oratoria’s digestive tract [30], systematic and comprehensive studies on the overall morphology and histology of O. oratoria’s digestive system are currently lacking.
This paper analyzed the components of the digestive system of O. oratoria and described the characteristics of each organ by histological and ultrastructural methods, aiming to enrich the research of O. oratoria’s biology. It is a basis for understanding their digestive process.
2. Materials and Methods
2.1. O. oratoria Collection
O. oratoria specimens used in this experiment were collected in May 2024 from the area near the Yellow River estuary in the Bohai Sea (N 37°20′ to 37°30′, E 119°01′ to 119°19′) when they were in the anecdysis [31]. A total of 32 mixed-sex adult O. oratoria samples, with strong vigor and no disability, were carefully selected from the catches. They were placed in a foam box, covered with ice, and then immediately transported back to the lab for dissection.
2.2. Morphological Observation
First, the body length and the body weight of O. oratoria samples (112.27 ± 16.34 mm; 18.99 ± 7.25 g) were measured. Then, they were subjected to frost anesthesia to induce loss of vitality and death, followed by dissection. We followed the ‘Guidelines for Experimental Animals’ of the Ministry of Science and Technology (Beijing, China; No. [2006] 398, 30 September 2006) when conducting the dissection. The body of O. oratoria was opened along the dorsal midline, and the digestive system was meticulously removed with surgical forceps and scissors, ensuring that all associated appendages were carefully excised. Subsequently, we observed the digestive system and the morphological characteristics of every organ. We utilized a Nikon D610 (Tokyo, Japan) to carry out photographic documentation. Then, we measured and recorded the dimensions of each organ. Finally, we crafted a schematic diagram of the digestive system’s architecture utilizing Adobe Photoshop 2022 (Adobe Incorporated, San Jose, CA, USA).
2.3. Histological Observation
We performed routine histological analysis on eight distinct regions of O. oratoria to examine their histological structures: the labrum, esophagus, cardiac stomach, cardio-pyloric valve, pyloric stomach, midgut, hindgut, and hepatopancreas. First of all, we cut each sample into tissue sections approximately 5 mm in size and immersed them in Bouin’s solution for fixation. Following a 24-h fixation, the samples were subjected to a graded series of alcohol for dehydration and xylene for clarification. Subsequently, the samples were embedded in paraffin wax using a stepwise temperature increase to 52 °C, 56 °C, and finally 58 °C. Next, we sectioned the paraffin-embedded samples using a Leica Histocore BIOCUT (Leica, Nussloch, Germany) rotary microtome to obtain continuous sections with a thickness of 4 to 6 μm. Subsequently, we stained the thin sections using the Hematoxylin-eosin-stained method. This method can stain the cell nuclei blue with Hematoxylin and the cytoplasm pink with Eosin to facilitate the observation of cell morphology and the structural hierarchy of tissues. Finally, we sealed the microscope slide with thin tissue sections using neutral resin. After that, we observed the prepared sections using an OLYMPUS CX33 trinocular microscope (Olympus, Tokyo, Japan) with a 12-megapixel IMAGE SC1200C color camera system. The images were captured and processed by the Cap Studio (Image Technology company, Su Zhou, Jiangsu Province, China) and Image J v.1.53a (National Institutes of Health, Bethesda, MD, USA) software.
Due to the unique morphological structures of the cardiac stomach, cardio-pyloric valve, pyloric stomach, midgut, and hindgut, we utilized HITACHI SU8100 Scanning Electron Microscopy (Hitachi, Tokyo, Japan) to observe their ultrastructure. Firstly, we collected the aforementioned organs, carefully sectioned them into tissue blocks with a volume of less than 3 mm3, and rinsed them with a saline solution. After fixing the tissue blocks in 2.5% glutaraldehyde at room temperature in the dark for 2 h, they were transferred to storage at 4 °C. Then, the fixed samples were rinsed with 0.1 M phosphate-buffered saline (PBS) at a pH of 7.4. Subsequently, the samples were subjected to a graded alcohol dehydration series. Next, we proceeded to dry the samples with a Quorum K850 critical point dryer (Quorum Technologies, Nussloch, Baden-Württemberg, Germany). Subsequently, we sputter-coated them with a platinum film using a HITACHI MC1000 ion sputter coater (Hitachi, Tokyo, Japan). Ultimately, the prepared samples were observed and photographed under a SEM operating at a working voltage of 3 kV.
2.4. Statistical Analysis
The experimental data are presented as the mean ± standard deviation (Mean ± SD). Statistical analyses were performed using SPSS v.27 (IBM Corporation, Chicago, IL, USA). Before statistical analysis, all data were tested for the normality of distribution and homogeneity of variances with SPSS. One-way analysis of variance (ANOVA) was utilized for multiple group comparisons, with statistical significance defined as p < 0.05. Duncan’s multiple range test is employed to further determine which groups exhibit significant differences.
3. Results
3.1. Composition of the Digestive System
The digestive system of O. oratoria consists of the digestive tract and digestive glands. The digestive tract includes the mouthparts, foregut, midgut, hindgut, and anus. The foregut comprises the esophagus, cardiac stomach, and pyloric stomach. The mouthparts are located on the ventral side of the cephalothorax. The foregut is situated within the cephalothorax. The midgut begins at the posterior end of the cephalothorax at the fifth thoracic segment and extends to the fifth abdominal segment. The hindgut starts at the sixth abdominal segment and terminates at the telson. The anus is located on the ventral side of the telson. The digestive glands include both the small digestive glands and the large digestive gland that constitute substantial organs. The small digestive glands, such as the minor salivary glands, esophageal glands, and mucous glands, are distributed within the walls of the digestive tract. The large digestive gland is the well-developed hepatopancreas, also known as the midgut gland. It is the longest organ in the digestive system. It spans from the posterior region of the cephalothorax to the telson (Figure 1).
The morphological parameters of the digestive system of O. oratoria are shown in Table 1. The results suggest that the Intestines length index (ILI) and Hepatosomatic index (HSI) are 70.82% and 3.83%.
3.2. Characteristics of Different Organs in the Digestive System
3.2.1. Mouthparts
The mouthparts are located on the ventral side of the cephalothorax, serving as the feeding organs of O. oratoria. The mouthparts are made up of a labrum and eight pairs of appendages (Figure 2). The first three pairs of appendages are cephalic, with a pair of hard mandibles and two pairs of maxillae in sequence from the inside out. The last five pairs are the thoracic appendages, also known as the five pairs of maxillipeds. The mouth, defined by the labrum and surrounding mouthparts, houses a pair of complex chitinous tooth-like structures known as the mandibular-gastric mill apparatus. The base of this functional complex is located outside the cardiac stomach and beneath the mouth, as shown in Figure 2 (*). Each mandibular-gastric mill apparatus is divided into the outer and inner branch, as shown in Figure 2 (MGA). The outer branch, known as the incisor lobe, serves as the mandible. It is situated beneath the mouth with a pale hue. It presents a row of robust teeth, numbering seven on each flank. The inner branch, the molar lobe, appears light brown and operates as the gastric grinding teeth. It protrudes into the cardiac stomach, as shown in Figure 2 (MOL). This branch boasts two rows of sturdy teeth, seven on each side. In addition, it has a sharp tooth at the end. The molar lobe also has the palp of the mandible, which is approximately one-third the length of the lobe itself. The first maxillae come in pairs (Figure 2: FM), each with two branches. One branch closely adheres to the mandible, which is milky white, thick, and soft in texture. The second branch is white and transparent, covered with a soft exoskeleton, with more fluff. Besides, the second also has two rows of yellow, tooth-like soft exoskeletons on the edge, growing side by side with the incisor lobe of the mandible. Both branches are covered in a fine layer of fluff on their surfaces. The second maxillae come in pairs (Figure 2: SM). They’re white and see-through with a soft, leafy feel to them. They are characterized by a delicate fringe of fluff along their edges. In a resting state, they encircle the labrum, mandibles, and first maxillae. Through observation, it has been observed that they will swing back and forth during feeding. These two pairs of maxillae can protect the mouth. The outermost layer of the mouthparts consists of the first, second, third, fourth, and fifth maxillipeds. Among them, the second maxillipeds, known as raptorial claws, are developed (Figure 2: SMD).
The histological structure of the labrum consists of the chitinous layer, mucosal epithelial layer, submucous layer, muscularis, and outer membrane (Figure 3a). The chitinous layer is relatively thick, serving to reduce injury to the oral mucosa from sharp food particles. The mucosal epithelial layer is composed of simple columnar epithelial cells and an underlying basement membrane. The nuclei of the mucosal epithelial cells are centrally located and oval in shape. The basement membrane forms a papillary projection. The projection may serve as a gustatory receptor, which is composed of oval-shaped taste cells [32,33]. The submucosal epithelial layer is a loose connective tissue. The layer contains clustered alveolar-like glandular structures (diameter: 187.16 ± 47.20 μm), which are called the minor salivary glands of the oral mucosa (Figure 3b). The central part of these glands is the gland lumen, and the outer layer is composed of simple cuboidal epithelial cells. These cells have distinct boundaries and constitute the secretory portion of the gland. The muscularis is well-developed, facilitating the chewing movements. This layer is primarily composed of oblique muscles that extend to the mucosal epithelial layer. Lastly, the outer membrane contains mucous cells that secrete mucus.
3.2.2. Foregut
Esophagus
The esophagus is a short, thick tube that connects the labrum to the cardiac stomach, with no distinct boundaries between the three (Figure 4a). The esophagus shares a similar histological structure with the labrum, including a chitinous layer, mucosal epithelial layer, submucous layer, muscularis, and outer membrane (Figure 4b). The chitinous layer is relatively thick. The mucosal epithelial cells are low columnar with large and centrally located nuclei. The submucous layer contains esophageal glands (height: 81.36 ± 1.16 μm, width: 27.37 ± 2.32 μm) and mesenchyme. The muscularis is well-developed, primarily consisting of circular muscles.
Cardiac Stomach
The cardiac stomach, which is a triangular sac-like structure, is located in the center of the cephalothorax. It is smaller at the front and larger at the back, accounting for about 12.85 ± 1.41% of the body length (Figure 1 and Figure 4a). Upon dissection, it was observed that the central part of the entire stomach cavity has black pigmentation, which gradually decreases as it radiates outward, with the sides being transparent in color. The gastric grinding teeth, which are the molar lobe of the mandibular-gastric mill apparatus, are located in the cardiac stomach (Figure 2).
The wall of the cardiac stomach is composed, from the inside out, of the chitinous layer, mucosal epithelial layer, submucous layer, muscularis, and outer membrane (Figure 5a,b). The chitinous layer is uneven and thinner than the esophagus, with specialized tufts of setae on the surface (Figure 5c,d). Each seta branches into 3–6 strands, all directed towards a fixed orientation. The setae are secreted by the seta-producing sacs, which are recessed areas formed by the mucosal epithelial layer protruding towards the submucosal side. They have various morphologies, like flask-shaped or square, which are filled with dense tissue inside (Figure 5b). The mucosal epithelial layer is relatively thin and is composed of simple columnar cells and a basement membrane. The nuclei of these cells are centrally located and oval-shaped. The basement membrane has undulating edges on its inner and outer margins. Mucous cells are distributed in the mucosal epithelial layer. The well-developed submucous layer is a type of loose connective tissue. The muscularis is also well-developed, with no clear boundary with the submucous layer. This layer is primarily composed of circular muscles, longitudinal muscles, and a small number of oblique muscles. The longitudinal muscles are bundled and flanked by circular muscles on both sides. The oblique muscles could reach the mucosal epithelial layer. The cardiac stomach is connected to the cephalothorax through the outer membrane. Additionally, the setae and gastric grinding teeth constitute the primary filter of the cardiac stomach.
The posterior ventral wall of the cardiac stomach specializes in a rounded chitinous valve, which is perpendicular to the subsequent digestive tract structures, known as the cardio-pyloric valve (Figure 1). The cardio-pyloric valve, with its axial symmetry, presents a central elevation that gradually slopes down to form a flat plane on both sides. Moreover, this structure is characterized by its brownish-yellow color. The histological structure of the cardio-pyloric valve, from top to bottom, consists of the chitinous layer, mucosal epithelial layer, submucous layer, muscularis, and outer membrane (Figure 6a–c). The chitinous layer extends from the center of the cardio-pyloric valve to both sides, thickening into a sickle shape and invaginating into the mucosal epithelial layer (Figure 6b). The mucosal epithelial layer is composed of tall columnar epithelial cells. The nuclei of the columnar epithelial cells, which are oval or round in shape, are positioned at the top of the cells. The submucosal epithelial layer contains tightly packed cells and fibers. The muscularis is primarily longitudinal muscles, which have a clear boundary with the submucosal layer. The ultrastructure displays a uniform arrangement of longitudinal muscles (Figure 6d), along with a dense reticulum of fibers on the surface. These reticular fibers, which are extremely fine, form an intricate network and exhibit granular proteoglycans adhering to their surface (Figure 6e). Additionally, the muscular layer at both ends of the cardio-pyloric valve is connected to the invaginated chitinous layer through the mucosal epithelium. The valve is securely attached to the inner wall of the cardiac stomach by an outer membrane comprised of simple cuboidal cells.
Pyloric Stomach
The pyloric stomach, which immediately follows the cardio-pyloric valve, accounts for about 4.12 ± 0.52% of the body length. Although it is relatively small in volume, its structure is quite complex. The dorsal midline along the pyloric stomach and the ventral wall are both thickened to form a chitinous plate, dividing the stomach into two chambers. The center of the surface of both chambers has oval-shaped black pigmentation (Figure 1).
The cross-sectional view of the pyloric stomach reveals a triangular shape. The gastric cavity is divided into two chambers, also known as the pyloric antrum, which are structurally identical but differ in size. The histological structure consists of the outer membrane, muscularis, chitinous layer, the mucosal epithelial layer, and submucosal layer (Figure 7a,b). The outermost layer is the outer membrane, which includes some mucous cells. The muscularis is predominantly composed of circular muscles. The chitinous layer is uniquely located in the pyloric region of the stomach and is reminiscent of the shape of sheep’s horns. It is divided into ventral and lateral projections. The ventral projection, known as the ampullary crest, is a short columnar chitinous layer that protrudes into the gastric cavity. The ventral projection unevenly divides the pyloric stomach into two chambers. The two ventral projections are connected by a network of radiating connective tissue. The lateral projection, located on the sides, is a tall columnar chitinous layer connected to the ventral projection. It is known as the superior ampullary crest. Outside the lateral and ventral projections, there are two layers of chitinous material with a spiky appearance, referred to as the glandular filter. The first layer consists of robust spicules that are regularly arranged. The second layer is the seta plate (Figure 8a), composed of short, fine setae arranged in parallel arrangement (Figure 8b). The end of the seta plate features a dense array of long and spiky setae (Figure 8c). Both chambers contain large and chrysanthemum-like connective tissues known as the lateral antral sacs. The connective tissue is composed of mucosal epithelial cells and submucosal epithelial cells. The mucosal epithelial cells are elongated columnar. The submucosal cortex is formed by short oval cells that are tightly connected. Together with the glandular filter, the lateral antral sacs form the secondary filter of the pyloric stomach.
3.2.3. Midgut
The midgut accounts for about 59.39 ± 3.36% of the body length. It is the longest part of the digestive tract. The midgut, characterized by its tubular and elongated shape, is notable for its significant elasticity, featuring a smooth surface and thin walls (Figure 1). The thickness of the intestinal wall is 368.12 ± 9.71 μm. When empty, the midgut appears transparent; when not empty, it shows a pulpy residue of digested food. The midgut lacks the cecum at both the anterior and posterior ends.
The midgut wall, from inner to outer layers, consists of the mucosal epithelial layer, submucosal layer, muscularis, and outer membrane (Figure 9a,b). The mucosal epithelial layer includes simple columnar cells, which protrude into the intestinal lumen, forming longitudinal folds known as midgut villus. This significantly increases the contact area between the midgut and food. This layer contains many mucous cells. Mucous cells are scattered throughout the mucosal epithelial layer. The free surface of the mucosal epithelial cells is covered with dense microvilli (Figure 10a,b). These microvilli (diameter: 0.11 ± 0.01 μm) have spherical substances (diameter: 0.31 ± 0.05 μm) on their surface, which are possibly related to digestion (Figure 10b). The muscularis, primarily composed of thin circular muscles, is distributed within the submucosal layer and is not clearly demarcated from it. The midgut is connected to the hepatopancreas through the thin outer membrane, which is the outermost layer of the midgut wall.
3.2.4. Hindgut and Anus
The hindgut constitutes roughly 11.44 ± 0.88% of body length. It is a tubular segment with a diameter exceeding that of the midgut (Figure 1). The thickness of the intestinal wall is 899.75 ± 17.00 μm. It is slender at the front and broader at the rear, presenting a light-yellow tint. The hindgut has an opening at the anus on the ventral aspect of the telson.
The hindgut’s histological structure is similar to the midgut. From the innermost to the outermost, there are the mucosal epithelial layer, submucous layer, muscularis, and outer membrane (Figure 11a–c). The wall of the hindgut bends towards the lumen, folding into larger longitudinal ridges, which are known as hindgut villi. The ends of adjacent villus connect, making the intestinal wall extremely convoluted. The mucosal epithelial cells are composed of simple columnar cells with round or oval nuclei, which include mucous cells. They feature microvilli on their free surface (Figure 12a,b) but lack the spherical substances that were found on the microvilli in the midgut. The microvilli’s diameter is 0.13 ± 0.01 μm, which is slightly larger than the midgut. The submucosal layer is not distinct. The muscularis is primarily composed of longitudinal muscles, which is different from the midgut. Lastly, the outer membrane is thin.
3.2.5. Hepatopancreas
The hepatopancreas is exceptionally well-developed, with a soft consistency. It is a large and grayish-white digestive gland that is symmetrical on both sides, accounting for 76.60 ± 3.14% of the body length and 3.83 ± 0.56% of the body weight of O. oratoria. The hepatopancreas is an accessory gland of the midgut, with an extremely wide coverage, enveloping the pyloric stomach, midgut, and hindgut. It branches out on both sides, extending portions of the gland to the junction points of each body segment, with a complement of ten branches per side (Figure 1).
The main trunk of the hepatopancreas is the primary hepatic duct, with branches being the secondary hepatic ducts. The primary hepatic duct includes the central gland (Figure 9a) and several hepatic tubules. The secondary hepatic ducts consist only of hepatic tubules. The histological structure of the central gland is composed of the mucosal epithelial layer, submucosal layer, and outer membrane (Figure 13a,b). The mucosal epithelial layer of the central gland contains numerous longitudinal folds (height: 330.43 ± 80.55 μm) that are morphologically similar to those of the midgut. A glandular duct is distributed in the submucosal layer every two folds. The outer membrane is thin and distinct. The hepatic tubules are a tightly packed cluster of secretory tubules. The histological structure of the hepatic tubules is relatively simple, consisting only of the mucosal epithelial layer and the outer membrane, with a central lumen (Figure 13c,d). The mucosal epithelial cells are all simple columnar cells, including blister cells (BC), resorptive cells (RC), fibrillar cells (FC), and embryonic cells (EC). The BC feature a large vacuole; the most numerous cells are the tall and columnar RC with centrally located nuclei, the FC typically have nuclei at the base, and the EC have large round nuclei [14]. All the hepatic tubules are closely connected by the outer membrane.
3.2.6. Tissue Morphology Measurement and Analysis
This study measures several histology structures of different organs in the digestive tract of O. oratoria, including chitin thick, mucosal epithelial layer or villus height, submucosal layer thick, longitudinal muscle thick, circular muscle thick, and outer membrane thick. After ANOVA, the differences among various organs across different structures were found to be significant, with p-values all less than 0.001, indicating significant differences in the mean values of different organs across these structures. We present the results of the morphological measurements, analyzed by Duncan’s test, in Table 2. The results indicate that the thick of chitin in the five sites was significantly different. The pyloric stomach is the thickest at 359.43 μm, followed by the labrum at 155.70 μm. The labrum is much thicker than the esophagus. The pyloric stomach is much thicker than the cardiac stomach. The highest height of mucosal epithelial cells is the hindgut. The labrum has the smallest mucosal epithelial layer height. As can be seen from the results, the height of the villi in the hindgut is larger than the midgut, which is about 3.20 times that of the midgut. The thick of the submucosal layer of the foregut was generally larger than the midgut and hindgut. Muscles control the peristalsis of the stomach wall. The longitudinal muscles were only found in the cardiac stomach, the valves within it, and the hindgut, with muscle thick of the cardio-pyloric valve > cardiac stomach > hindgut. The thick of the circular muscle, from large to small, is the esophagus> pyloric stomach> cardiac stomach> labrum> midgut. Only the cardia-pyloric valve and hindgut do not have the circular muscle. There are no significant differences in circular muscle thick between the cardia and pyloric stomach. The labrum’s outer membrane is the thickest, while the hindgut is the thinnest. There are significant differences between them.
4. Discussion
This study found that the digestive system of O. oratoria, which belongs to Stomatopoda, shares similar characteristics with decapod crustaceans [14,34,35]. It has a segmented digestive tract that includes the foregut, midgut, and hindgut, with the digestive gland being the hepatopancreas. The study also discovered certain unique features of O. oratoria’s digestive system. Firstly, we found that the O. oratoria’s mouthparts are more complex, which serves to chop and grind the food [36]. The basic structure of the mouthparts in Decapods is well-known. Decapods primarily have a pair of mandibles, two pairs of maxillulae, and three pairs of maxillipeds [36,37], while O. oratoria has a pair of mandibles, two pairs of maxillulae, and five pairs of maxillipeds. This difference in accessory mouthparts is attributed to their predatory strategies. Decapods are mainly omnivorous [38], whereas Stomatopods are primarily carnivorous [10]. Therefore, O. oratoria may require more complex mouthparts to adapt to their feeding habit. Secondly, O. oratoria’s esophagus, which is flexible, can swallow food into the stomach and expel any indigestible or mistakenly ingested food, functionally similar to other crustaceans [39]. However, morphologically, O. oratoria’s esophagus is short and thick, and the esophageal wall itself does not form a closed structure. But it, together with the labrum, forms a closed loop with the mandibles beneath the mouth, which is different from decapods [14]. Additionally, small salivary glands that secrete mucus and esophageal glands were found, which can both lubricate food and reduce damage to the digestive tract caused by sharp food. The small salivary glands are larger in morphology than the esophageal glands. Lastly, we found that the stomach of O. oratoria is the organ for physical digestion, while the main organs for chemical digestion and absorption are the midgut and hepatopancreas located behind it, which is a general characteristic of crustaceans [40]. The most important point is that the stomach, midgut, and hepatopancreas have some unique attributes, and these differences are the main features that distinguish O. oratoria’s digestive system from other crustaceans. This also helps O. oratoria to survive in the long process of natural selection and occupy a higher ecological position among marine benthic organisms [4]. The following is a detailed description of the differences.
4.1. Structural and Functional Relationship of the Stomach in O. oratoria
The stomach of crustaceans lacks low pH and abundant proteases for chemical digestion, but it has complex grinding and filtering structures for physical digestion [41]. Like other crustaceans [42,43], the stomach of O. oratoria is divided into the cardiac stomach and the pyloric stomach. The cardiac stomach is used for mechanical grinding and breaking down of food, mainly achieved by the gastric mill. Inside the cardiac stomach, food is broken down from larger fragments into smaller particles [43]. The pyloric stomach is primarily used for filtering and flattening food particles, mainly achieved through the glandular filter. After passing through the pyloric stomach, food particles are transformed into finer pulp [14]. The uniqueness of O. oratoria’s stomach is precisely reflected in the special structures of the gastric mill and the glandular filter. These are the most representative features of O. oratoria’s foregut.
The term “gastric mill” was first introduced by Huxley (1880) in his description of the digestive system of the decapod Astacus fluviatilis [44]. The gastric mill actually refers to the collective chitinous structures with grinding functions in the cardiac stomach [45], capable of crushing food into small particles. Our study found that the gastric mill of O. oratoria includes setae and gastric grinding teeth. We speculate that the setae may serve to protect the cardiac stomach and grind food [42]. Gastric grinding teeth are the most typical structure of the gastric mill. Decapods such as Trichodactylidae [46], Maja brachydactyla [47], and Homarus americanus [24] have a variety of gastric grinding teeth, including plate-like median teeth and exquisite accessory lateral teeth [48]. O. oratoria only has one type of gastric grinding teeth that are morphologically similar to the accessory lateral teeth of Decapods [49]. Reddy’s study on Squilla nepa [29] also found similar structures. Therefore, we believe this is a simplification in the morphology of gastric grinding teeth and an adaptation of the Stomatopoda to specific lifestyles or predatory patterns. It will reduce the physical investment in diverse gastric grinding teeth, making energy utilization more efficient. Specifically, this study found that the gastric grinding teeth and mandibles of O. oratoria are integrated. The mandibles are used for tearing, and the gastric grinding teeth for grinding. The two functions process at the same time, ingeniously integrating structural and functional unity. Compared with the independence of the two in Decapods [23,49], the mandibular-gastric mill apparatus can improve the utilization rate of physical capabilities. It may speed up the efficiency of mechanical grinding. Regarding the nature of this apparatus being a mandible or a gastric mill, we suspect that it is derived from the mandible. The reason is that the base of this apparatus is outside the cardiac stomach and under the mouth instead of being in the cardiac stomach (Figure 2: *). The part of the gastric grinding teeth (the molar lobe) of this apparatus is suspended within the cardiac stomach. The molar lobe that enters the cardiac stomach may be the result of O. oratoria’s evolution to improve its predation efficiency continuously. To be specific, we speculate as follows: O. oratoria directly swallows its prey into the cardiac stomach to seize it or prevent it from escaping. Once ingested, the prey is then further chewed and processed within the cardiac stomach. This study also found that the distance between the mouth and the cardiac stomach is extremely small, and the relatively short esophagus between them is not sufficient to form an obstacle. The molar lobe of this apparatus has the innate condition to directly penetrate into the cardiac stomach and perform chewing movements within it. After a long period of evolution, this combination formed. We found that the number of teeth on the gastric grinding teeth of O. oratoria is fixed (Figure 2), which may be used for age determination [50], classification of Stomatopoda, and other research in the future. In addition, we speculate that the cardia-pyloric valve, which is at the posterior cardiac stomach, can deform under the mechanical action of the muscles [42]. This deformation can regulate the size of the passage between the cardiac stomach and the pyloric stomach to prevent the backflow of food.
The structure of the glandular filter located in the pyloric stomach of O. oratoria is subtly intricate, consisting of two layers, which are robust spicules and seta plate. We speculate that its functions are mainly reflected in the following aspects. Firstly, the pyloric stomach uses contractions of its muscle to induce the deformation of its glandular filter and rhythmic movements of itself, further physically squeezing and filtering the food [14]. Secondly, the pyloric stomach is divided into a dorsal chamber connected to the midgut and a ventral chamber [30], with the glandular filter in the ventral chamber being taller than that in the dorsal chamber. It is hypothesized that the ventral chamber primarily processes larger food particles, while the dorsal chamber mainly deals with smaller ones. Through the combined action of the spicules and seta plates of the two chambers’ glandular filters, the food is progressively refined and processed into sufficiently small pulp that can then enter the midgut from the dorsal chamber of the pyloric stomach.
4.2. Differences Between the Midgut and Hindgut of O. oratoria
In crustaceans, the midgut is an important digestive organ for food digestion and absorption, and the hindgut primarily serves to store metabolic waste [51]. The digestive waste is expelled from anus [51]. This study found that the functions of the midgut and hindgut in O. oratoria are like this, but they also have some differences.
The relative lengths of the midgut and hindgut in crustaceans can reflect their ability to digest and absorb food. The relative range between the two exhibits species-specific traits, potentially influenced by the dietary habits and functional differences of the gut. The most distinctive feature of O. oratoria’s digestive tract morphologically is the extreme length of the midgut, which accounts for approximately 66.28% of the total length of the body. This ratio is similar to that of crustaceans that feed on small fish, shrimp, shellfish, and algae, such as Penaeus orientalis [52] and Metapenaeus bennettae [53]. This proportion is higher than that of Cambarus clarkii, which feeds on small planktonic plants and animals and has a midgut ratio accounting for 11.45% of its body length [54]. Nonetheless, the ratio of O. oratoria falls short of that observed in the carnivorous decapod Panulirus ornatus. This species, which has a diet predominantly consisting of animal matter, exhibits a significantly higher percentage, with the midgut constituting 74.18% of its body length [55]. Additionally, the hindgut of O. oratoria accounts for approximately 12.88% of its body length. This proportion is higher than the 7.48% observed in P. ornatus [55] but lower than the 48.48% found in C. clarkii [54]. The aforementioned conditions indicate that there is a close relationship between feeding habit and digestive tract structure in malacostracans. Omnivorous and carnivorous species have a relatively high proportion of the midgut in the digestive tract. In contrast, herbivorous or plankton-feeding species have a higher proportion of hindgut in their digestive tract. We also speculate that, under the premise of ensuring functionality, a shorter hindgut is more conducive to reducing body weight and physical burden, thereby enhancing the agility of movement.
This study observed that although the histological structures of the midgut and hindgut in O. oratoria are morphologically similar in forming intestinal villi, the thickness of the hindgut wall is about 2.44 times that of the midgut, and the height of the villi are approximately 3.20 times of the midgut, respectively. The diameter of the hindgut microvilli is also slightly larger than the midgut microvilli. Additionally, SEM shows that the midgut villi are rich in spherical substances (Figure 10b), which may be electron-dense vesicles released by midgut epithelial digestive cells via microvilli during secretory activity [56,57], which are not present in the hindgut (Figure 12b). The types of muscle tissue in the intestinal walls are also different, with the midgut having circular muscles and the hindgut having longitudinal muscles. This seems to indicate that during the digestion process, the midgut wall mainly undergoes radial expansion, while the hindgut primarily moves through longitudinal peristalsis. Decapoda and other crustaceans do not have a chitin lining on the midgut surface, which is derived from the endoderm, while the hindgut, derived from the ectoderm, does have it [14]. However, no chitin lining was observed on the surfaces of the midgut and hindgut in O. oratoria, suggesting that both the two sections may be derived from the endoderm. Further confirmation is needed.
4.3. Functions of the Hepatopancreas of O. oratoria
The hepatopancreas is an accessory organ of the midgut in O. oratoria. HSI is an indicator that reflects the relative energy storage of crustaceans [58]. The hepatosomatic index (HSI) of O. oratoria’s hepatopancreas is 3.83%, which is relatively low compared to some shrimp and crab species, where HSI values range from 2% to 8.41% [59,60]. This suggests that O. oratoria likely does not rely heavily on its hepatopancreas for energy storage. However, in terms of coverage area, the hepatopancreas of O. oratoria is extremely well-developed. In most crustaceans, such as Paralithodes camtschaticus [23] and Metapenaeus bennettae [53], the hepatopancreas is only concentrated near the stomach and the anterior part of the midgut. The hepatopancreas of P. ornatus is even smaller, merely encircling the stomach [55]. However, in our study, the hepatopancreas of O. oratoria not only surrounds the midgut but also encloses both the pyloric stomach and the hindgut. It indicates that the hepatopancreas of O. oratoria has a wider contact area with the digestive tract compared to other crustaceans.
Crustaceans’ hepatopancreas is involved in the digestive and absorptive processes, thereby significantly enhancing the digestive function and metabolic level [29,61,62,63]. The first manifestation is the abundant expression of digestive enzymes in the hepatopancreas [64]. These enzymes are produced by the F-cells in the functional cells of the glandular tubules and enter the midgut [65]. The second is reflected in the ability of their absorptive cells to absorb small molecular nutrients [40]. This study found that the hepatopancreas of O. oratoria has this type of functional cell as well. Therefore, it is speculated that, like other crustaceans, the hepatopancreas of O. oratoria can both absorb nutrients and secrete digestive substances into the midgut. What is different in O. oratoria is that the large coverage area of the hepatopancreas over the digestive tract may be to facilitate the delivery of more enzymes to it, effectively enhancing digestive capacity.
5. Conclusions
In summary, this study provides a systematic and comprehensive description of the morphological, histological, and functional characteristics of O. oratoria’s digestive system. Our findings support the division of labor among the organs of O. oratoria’s digestive system, similar to decapod crustaceans. This is the first study to discover the small salivary glands on the labrum. Notably, we observed the mandibular-gastric mill apparatus and evenly arranged bifurcated setae in the cardiac stomach. There is a sophisticated glandular filter in the pyloric stomach of O. oratoria, with fine spicules and seta plate. The midgut, which is the longest segment of the digestive tract and accounts for 59.39% of body length, has villi covered with dense microvilli. The villi of the hindgut are 3.20 times taller than those of the midgut. The hepatopancreas encircles the entire pyloric stomach, midgut, and hindgut. The hepatosomatic index (HSI) is approximately 3.83%. These are suited to O. oratoria’s carnivorous feeding habits. This enriches the study of the digestive system in Stomatopoda. The results of this study provide theoretical support for future research on the nutritional composition changes in populations of different waters or different life stages and the impact of water and climate changes on the digestive system (especially the height of intestinal mucosa and HSI of the hepatopancreas).
Conceptualization, R.W. and L.W.; methodology, L.W; software, R.W.; validation, P.Y.; formal analysis, F.L.; investigation, R.W., L.W. and S.Q.; resources, L.W.; data curation, R.W. and F.L.; writing—original draft preparation, R.W.; writing—review and editing, R.W., L.W. and P.Y.; visualization, R.W.; supervision, F.L.; project administration, L.W. and S.Q.; funding acquisition, S.Q. All authors have read and agreed to the published version of the manuscript.
All procedures carried out in this study have been approved by the Ethics Committee of Yantai University on May 12th, with the approval code No. YTU20240512.
Not applicable.
The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.
We extend our sincere thanks to Zhang Jiantong, the Fisheries Resources and Ecological Environment Laboratory of Yantai University, and the individuals who have dedicated their efforts to review this manuscript. Thank you all for your contributions.
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. Digestive System of O. oratoria from the dorsal aspect. Abbreviation: second maxillipeds (SMD): which is a component of the mouthparts, esophagus (ES): Only visible from the ventral aspect, cardiac stomach (CS), mandibular-gastric mill apparatus (MGA), molar lobe (MOL), incisor lobe (INL), cardio-pyloric valve (CPV), pyloric stomach (PS), foregut (FG), midgut (MG), hepatopancreas (HP), hindgut (HG), anus (AN).
Enlarge this image.Figure 2. Composition of the mouthparts. Abbreviation: labrum (LA), mandibular-gastric mill apparatus (MGA), molar lobe (MOL), incisor lobe (INL), cardiac stomach (CS), first maxillae (FM), second maxillae (SM), first maxillipeds (FMD), second maxillipeds (SMD)/raptorial claw, third maxillipeds (TMD), fourth maxillipeds (FOM), fifth maxillipeds (FIM). “*” indicates the location of MGA’s base.
Enlarge this image.Figure 3. Histological structure of the labrum. (a) Longitudinal section of the labrum. Utilize Hematoxylin-eosin staining for microscopic observation at a magnification of 100 (HE×100); (b) The minor salivary gland (HE×200). Abbreviation: chitinous layer (CL), mucosal epithelial cell (MEC), basement membrane (BM), submucous layer (SUL), oblique muscle (OM), outer membrane (OUM), minor salivary gland (MSG), gustatory receptor (GR), mucous cell (MC).
Enlarge this image.Figure 4. Location and histological structure of the esophagus. (a) The Location of the esophagus; (b) Longitudinal section of the esophagus, HE×100. Abbreviation: cardiac stomach (CS), esophagus (ES), labrum (LA), chitinous layer (CL), mucosal epithelial layer (MEL), submucous layer (SUL), circular muscle (CM), oblique muscle (OM), esophageal gland (EG), mesenchyme (ME).
Enlarge this image.Figure 5. Histological structure of the cardiac stomach. (a) Longitudinal section of the cardiac stomach, HE×100; (b) Transverse section of the flask-shaped or square seta-producing sac of the cardiac stomach, HE×100; (c,d) The surface of the cardiac stomach observed with a Scanning Electron Microscope at 1000 and 3000 magnifications (SEM×1000, 3000). Abbreviation: chitinous layer (CL), basement membrane (BM), simple columnar cell (SCO), submucous layer (SUL), circular muscle (CM), longitudinal muscle (LM), outer membrane (OUM), oblique muscle (OM), seta-producing sac (SES), mucous cell (MC).
Enlarge this image.Figure 6. Histological structure of the cardio-pyloric valve. (a–c) Transverse section from the cardio-pyloric valve, HE×40, 100, 100; (d,e) The muscle surface of the cardiac stomach, (SEM×100, 3000). Abbreviation: chitinous layer (CL), mucosal epithelial layer (MEL), longitudinal muscle (LM), simple cuboidal cell (SCU), fiber (FI), proteoglycan (PR).
Enlarge this image.Figure 7. Histological structure of the pyloric stomach. (a) Longitudinal section of the pyloric stomach, HE×40; (b) Transverse section of the pyloric stomach, HE×40. Abbreviation: ampullary crest (AC), superior ampullary crest (SAC), seta (SE), mucosal epithelial layer (MEL), circular muscle (CM), submucous layer (SUL), spicule (SP), seta plate (SEP), digestive cavity (DC), mucous cell (MC), outer membrane (OUM).
Enlarge this image.Figure 8. Histological structure of the pyloric stomach. (a) Seta plate in the pyloric stomach, SEM×300. (b,c) Setae and spiky setae, SEM×3000. Abbreviation: seta (SE), Spiky setae (SSE).
Enlarge this image.Figure 9. Histological structure of the midgut. (a) Transverse section of the midgut and central gland, HE×40; (b) Transverse section of the midgut, HE×200. Abbreviation: midgut (MI), midgut villus (MV), central gland (CG), hepatic tubules (HT), outer membrane (OUM), mucosal epithelial layer (MEL), submucous layer (SUL), circular muscle (CM), mucous cell (MC), digestive cavity (DC).
Enlarge this image.Figure 10. Histological structure of the midgut. (a,b) Inner surface of the midgut, SEM×1000, 3000. Abbreviation: mucosal epithelial cells (MEC), midgut microvilli (MMV), spherical substances (SS).
Enlarge this image.Figure 11. Histological structure of the hindgut. (a–c) Transverse section of the hindgut, HE×40, 100, 200. Abbreviation: hindgut (HI), digestive cavity (DC), hindgut villus (HV), longitudinal muscle (LM), mucous cell (MC), mucosal epithelial layer (MEL), outer membrane (OUM).
Enlarge this image.Figure 12. Histological structure of the hindgut. (a,b) Inner surface of the hindgut, SEM×1000, 3000. Abbreviation: mucosal epithelial cells (MEC), hindgut microvilli (HMV).
Enlarge this image.Figure 13. Histological structure of the hepatopancreas. (a,b) The central gland, HE×100, 200; (c,d) The hepatic tubules, HE×100, 400. Abbreviation: glandular duct (GD), outer membrane (OUM), mucosal epithelial cells (MEC), hepatic tubule (HT), blister cell (BC), resorptive cell (RC), fibrillar cell (FC), embryonic cell (EC).
Measurement of morphological traits in the digestive indexes of O. oratoria (Mean ± SD, n = 32).
| Index | Parameters |
|---|---|
| Midgut length (mm) | 66.28 ± 7.73 |
| Hindgut length (mm) | 12.88 ± 2.23 |
| Hepatopancreas weight (g) | 0.74 ± 0.33 |
| MGP (%) | 59.39 ± 3.36 |
| ILI (%) | 70.82 ± 3.21 |
| HSI (%) | 3.83 ± 0.56 |
Notes: Some morphological parameters were calculated as follows: (1). Midgut proportion (MGP) (%) = midgut length/body length × 100. (2). Intestines length index (ILI) (%) = (midgut length + hindgut length)/body length × 100. (3). Hepatosomatic index (HSI) (%) = hepatopancreas weight/body weight × 100.
Thickness or height of specific morphology structures present in the digestive tract in O. oratoria (μm, Mean ± SD, n = 30).
| Structures | Labrum | Esophagus | Cardiac | Cardio-Pyloric | Pyloric | Midgut | Hindgut |
|---|---|---|---|---|---|---|---|
| Chitin thick | 155.70 ± | 70.4 ± | 15.53 ± | 84.06 ± | 359.43 ± | - | - |
| Mucosal epithelial layer or Villus height | 43.41 ± | 60.5 ± | 60.26 ± | 84.83 ± | 200.39 ± | 217.41 ± | 695.96 ± |
| Submucosal layer thick | 920.72 ± | 616.78 ± | 1091.13 ± | 189.62 ± | 117.01 ± | 87.55 ± | 19.24 ± |
| Longitudinal muscle thick | - | - | 250.81 ± | 416.1 ± | - | - | 74.58 ± |
| Circular muscle thick | 58.46 ± | 166.48 ± | 107.45 ± | - | 115.48 ± | 54.70 ± | - |
| Outer membrane thick | 170.07 ± | 39.57 ± | 56.19 ± | 21.41 ± | 70.48 ± | 19.74 ± | 9.35 ± |
Note: “-” indicates that this structure has not been observed in this part. The same traits with the same superscript letter on the same line indicate no significant difference between groups (p > 0.05). On the contrary, there is a significant difference (p < 0.05).
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; Fangrui Lou; Yang, Pei; Qiu, Shengyao; Wang, Lei