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A Study on the Digestive Physiology of a Marine Polychaete (Eulalia Viridis) Through Microanatomical Changes of Epithelia During the Digestive Cycle

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A Study on the Digestive Physiology of a Marine Polychaete (Eulalia Viridis) Through Microanatomical Changes of Epithelia During the Digestive Cycle Microsc. Microanal. 21, 91–101, 2015 doi:10.1017/S143192761401352X © MICROSCOPY SOCIETY OF AMERICA 2014 A Study on the Digestive Physiology of a Marine Polychaete (Eulalia viridis) through Microanatomical Changes of Epithelia During the Digestive Cycle Ana P. Rodrigo, 1 Maria H. Costa, 1 António Pedro Alves de Matos,2 Francisco Carrapiço, 3 and Pedro M. Costa 1,* 1MARE—Marine and Environmental Sciences Centre/IMAR—Instituto do Mar, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, 2829-516 Caparica, Portugal 2Centro de Estudos do Ambiente e do Mar (CESAM)/Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Quinta da Granja, Monte de Caparica, 2829-511 Caparica, Portugal 3Centro de Biologia Ambiental (CBA), Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 Lisboa, Portugal Abstract: As for many invertebrates, the gut of marine polychaete species has key physiological functions. However, studies integrating microanatomical descriptions with physiological processes are scarce. The present investigates histological, histochemical and cytological changes in the alimentary canal during the digestive cycle of the marine annelid Eulalia viridis, a species that combines opportunist scavenging, predation and cannibalistic behavior. The gut is comprised of an eversible pharynx, esophagus, intestine and rectum. Three main phases of digestion were identified, namely, resting/secretory, absorptive and excretory. The intestinal epithelium is complex and exhibited the most significant changes regarding intracellular digestion, excretion and storage. Conversely, the pharynx and esophagus were chiefly important for enzyme secretion. The results also indicate the existence of two distinct types of secretory cells in the intestine, with likely distinct physiological roles. Some similarities have been found between the intestinal epithelia and the molluscan (especially cephalopod) digestive gland, as, for instance, the shedding of apical corpuscles by digestive cells at posterior stages of digestion. The findings indicate that the digestive process in this worm is complex and related to the many physiological roles that cells need to play in the presence of reduced organ differentiation. Key words: histology, histochemistry, phyllodocidae, gastrodermal cell types, digestive cycle INTRODUCTION emphasized that the alimentary canal, particularly the intestine, likely has several vital functions, a feature that, together with Marine polychaetes constitute the most diverse group within intracellular digestion, tends to fade in most higher-order Annelida, comprising about 80 known families that radiated animals. As a fact, in most marine invertebrates, especially about 500 m.a. ago and are phylogenetically linked to stem protostomes, the digestive epithelia exhibit complex changes annelids (see Bartolomaeus et al., 2005; Weigert et al., 2014). during digestion, implying structural alterations, changes These animals play an important ecological role in marine in biochemical composition and enzymatic machinery, and fi food chains as prey, predators, lter-feeders, or scavengers general responsiveness of the epithelium. However, such and are likewise important bioturbators of aquatic sediments as changes are far better described in the molluscan digestive deposit-feeders. As such, their multiple ecological niches are gland, especially in cephalopods (e.g., Semmens, 2002; Costa fl fi re ected in signi cant deviations from the standard polychaete et al., 2014), than for any other group of marine invertebrates. anatomy and physiology, resulting in high phenotypic variation Usually, the polychaete alimentary canal is divided into even within families or species (see, e.g., Tzetlin & Purschke, three parts: foregut, midgut and hindgut (Saulnier-Michel, 2005). However, in spite of their acknowledged importance, 1992; Jenkins et al., 2002). The foregut includes the buccal there are many gaps in the knowledge on the physiology of organ and the esophagus while the midgut allocates the sto- these organisms. In fact, even though the basic structure of the mach (when present) and the intestine. The hindgut comprises digestive system structure is documented for some polychaete the posterior most regions of the gut, which may or not be species (see Saulnier-Michel, 1992, for a review), there is still differentiated into a rectum (Jenkins et al., 2002). However, it is missing information in the knowledge of the microanatomy of the buccal organ, located in the foregut, which reveals the most the digestive epithelia, with particular respect to the changes significant interspecific variation, according to feeding habits, along the digestive, secretory and excretory cycles. It must be forming, for instance, an eversible pharynx (proboscis) or even being absent from filter-feeding groups (Tzetlin & Purschke, Received May 31, 2014; accepted October 10, 2014 2005). Most reports describe the polychaete intestine as a *Corresponding author. [email protected] tube-like structure, where the main cell type is the secretory cell 92 Ana P. Rodrigo et al. (Tzetlin et al., 1992; Tzetlin & Purschke, 2005). In some shore located at the Western Algarve coast, SW of Portugal polychaete species the presence of specialized absorptive and (37°22′57.81′′N, 8°49′30.71′′W). The animals were reared in secretory cells has been previously described and, in some the laboratory until processed for analyses, in a mesocosm cases, the latter have been divided into serous and mucous- environment with recirculation and periodic water changes. secreting cells (Saulnier-Michel et al., 1990). No reports The mesocosm included live mussels and barnacles of which were found on the relationship between cell types and the the worms were confirmed to prey on, in accordance to the physiology of polychaete digestion. findings of Olive (1975). ThemarineannelidEulalia viridis (Polychaeta: Errantia, Phyllodocidae) inhabits rocky shores, especially mussel beds, in Sample preparation intertidal areas, seeking protection during high tides under- Whole organisms were fixed using several solutions: Bouin’s neath clumps of mussels (Emson, 1977). Eulalia viridis is (10% v/v formalin and 7% v/v acetic acid picric acid added believed to be an opportunist scavenger, since scavenging to saturation); Carnoy’s (absolute ethanol, chloroform and (Morton, 2011) and simultaneous detrivore and predator glacial acetic acid, 6:3:1) and 2% v/v glutaraldehyde (in 0.2 M (Emson, 1977; Fauchald & Jumars, 1979) behaviors have been sodium cacodylate buffer, pH 7.4). Fixation in the two reported. It is acknowledged that E. viridis feeds mostly on former solutions was at room temperature for 24 h, followed barnacles, mussels and other worms of the same species by washing in Milli-Q (MQ) grade (18.2 MΩ cm) ultrapure (Emson, 1977; Morton, 2011). The worm, as in other phyllo- water (3 × 1 h) for samples fixed in Bouin’s and in absolute docids, makes use of its proboscis for collecting food items ethanol (3 × 1 h) for samples fixed in Carnoy’s. Fixation in through suction. Unlike many preying polychaete species they glutaraldehyde was done at 4°C for 2 h, followed by washing do not have jaws and rely on strong axial musculature typical of in cacodylate buffer (3 × 15 min), post-fixation in 1% m/v the family (see Michel, 1964; Tzetlin & Purschke, 2005). Oddly osmium tetroxide (OsO ) in cacodylate buffer in the dark for enough, herbivore feeding has never been described for this 4 1 h (4°C) and washed again in MQ water (3 × 10 min). species, expected for its conspicuous bright green color (Costa After fixation, the specimens were sectioned into six et al., 2013). Moreover, as for polychaetes in general, studies on portions, dehydrated in a progressive series of ethanol the relation between physiology and microanatomical changes (70–100% or 30–100% for glutaraldehyde-fixed samples) along the digestive process of this species are still lacking, with andembeddedinparaffin (xylene was used for intermediate the exception of a study on the pharynx that compared fasting infiltration). Some samples fixed in 2% glutaraldehyde v/v (in and satiated animals (Michel, 1969a). Detailed microscopy 0.2 M cacodylate buffer) and post-fixed in osmium tetroxide studies on the species concern spawning, reproduction (Olive, were embedded in Epon 812 (Sigma-Aldrich, St. Louis, MO, 1975; Rouse, 1988), microanatomy of the pharynx (Michel, USA), following Luft’s mixture. In brief: samples were dehy- 1964, 1969a), intestine (Michel, 1969b) and epidermis (Costa drated up to 100% acetone, intermediately infiltrated with et al., 2013) have been conducted. There are general anatomical Epon + 100% acetone (1:1) before final embedding and descriptions of the digestive tract of phyllodocids, which follows polymerization at 60°C in gelatine capsules. Other samples the basic annelid plan, although they lack a differentiated sto- fixed and post-fixed similarly were embedded in London Resin mach (Saulnier-Michel, 1992; Tzetlin & Purschke, 2005). White (LRW) (Fluka, Basel, Switzerland), using ethanol As for marine invertebrates in general, detailed histolo- for dehydration and ethanol + LRW (1:1) for intermediate gical studies are either absent or limited to a few key, studies. infiltration. Paraffinsections,3–5 µm thick, were obtained Histochemical techniques hold the advantage of being able to using a Jung RM 2035 rotary microtome (Leica Microsystems, demonstrate the presence, distribution and fate
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