6 The Digestive System

Carol Bucking and W. Gary Anderson

CONTENTS

6.1 Overview

6.2 Primary Function of the Digestive System

6.3 Digestive System Morphology

6.3.1 Buccal Cavity, Pharynx, and Associated Structures

6.3.2 Oesophagus

6.3.3 Stomach

6.3.4 Intestine

6.3.5 Colon and Rectum

6.3.6 Associated Organs

6.3.7 Microbiome

6.4 Future Perspectives

Acknowledgements

References

6.1 Overview

The primary function of the digestive system is to deliver fuels and building blocks to sustain life and to eliminate wastes. This occurs via anatomical structures that reflect the specific function they provide to the organism. From a broad perspective, the digestive system is a simple tube connecting the organism to the environment, delivering supplies brought in via the buccal cavity and eliminating wastes via the anus, most simply illustrated by the gross anatomy of the hagfish digestive tract (Figure 6.1). This conduit can have several names, including the gastrointestinal tract (GIT), the alimentary canal, the digestive tract, or more colloquially, the gut. The connection to the environment and essential provisioning of fuels to the body drive adaptations within the digestive system across many biological levels, from molecular and cellular to morphological, much of which will be the focus of this chapter.

FIGURE 6.1 Gastrointestinal tract of the Pacific hagfish, Eptatretus stoutii. FG: foregut; HG: hindgut.
Photo credit Alyssa Weinrauch.

6.2 Primary Function of the Digestive System

The primary function of the digestive system, digestion, can be defined as the mechanical, chemical, and enzymatic breakdown of food into metabolizable substances that are subsequently absorbed and distributed for use by the body. The type of food consumed can be used to distinguish and categorize fish as detritivores, herbivores, carnivores, or omnivores. These distinctions are often extremely informative, as the type of food consumed frequently drives structural and biochemical adaptations.

The mechanical breakdown of food is primarily achieved by the action of specialized teeth and/or other grinding or muscular surfaces, and is a species-specific occurrence that is largely shaped by dietary niche. Indeed, the morphology of teeth can provide an indicator of dominant diet and can be used to model trophic diversification (Hellig et al., 2010). Teeth in fishes are not restricted to the dentary or oral jaw but can also be found on pharyngeal jaws and/or the vomer or palatine bones, such as in the lingcod, Asemichthys taylori (Galloway et al., 2016). In the case of stomachless fish (discussed shortly), compensation in the form of pharyngeal teeth or a gizzard is often present to provide mechanical breakdown (Fänge and Grove, 1979).

Hydrochloric acid (HCl), one of the chemical components of digestion and produced in the stomach, is necessary for activating the zymogen pepsinogen into the active proteolytic enzyme pepsin, responsible for the cleavage and breakdown of proteins. The strong acid also lowers the pH of the stomach (e.g. Nikolopoulou et al., 2011), providing acidic catabolism and denaturation of ingested material. The genes encoding pepsinogen as well as the H+-ATPase responsible for HCl formation are expressed in gastric glands of the fish stomach, specifically the singular acid (oxyntic)- and pepsinogen (peptic)-secreting oxynticopeptic cells (e.g. Gawlicka et al., 2001). The secretion of both HCl and pepsinogen appears to be species specific (e.g. Bucking and Wood, 2009 vs. Nikolopoulou et al., 2011) and is likely modified by abiotic factors such as feeding patterns and/or circadian rhythms (e.g. Yúfera et al., 2012). Further along the GIT, bile is required for efficient lipid digestion (Rørvik et al., 2000), providing emulsifiers for hydrophobic nutrients, forming micelles for transport, and activating enzymatic catabolism.

Digestion represents the catabolism of carbohydrates, proteins, and/or lipids into easily absorbed nutrients (i.e. sugars, amino acids, and fatty acids and glycerol, respectively), and each type of macromolecule has specific enzymes designed for efficient catabolism. A review of enzyme locations and functions in the fish GIT is found in Bakke et al. (2011). Not surprisingly, the enzyme expression profile found in the gut is often diet specific, with herbivorous and omnivorous fishes tending to have higher ratios of protease:amylase activities compared with carnivorous fishes (Hidalgo et al., 1999). However, caution is urged against forming overly broad generalizations, as a lack of correlation with diet has also been detected (Chakrabarti et al., 1995), and phylogeny has been presented as a major driver of enzyme expression patterns over diet (German et al., 2004). Finally, the enzymatic components of digestion can be endogenously produced by the enterocytes, liver, and/or pancreas, or in some cases obtained from exogenous sources (e.g. cellulase; Kuz’mina, 2008; Castillo and Gatlin, 2015).

Once catabolized, the nutrients are then transported across the gastrointestinal epithelium. Transcellular transport (across the apical and basolateral membranes of the enterocytes lining the GIT) is supported by a diverse and plentiful array of transporters. Paracellular diffusion is possible but considered to be insignificant (Oxley et al., 2007). Generally speaking, sugars are transported by Na+-linked transporters such as SGLTs or channels such as GLUTs, while amino acids and di- and tri-peptides are transported through specific amino acid and peptide transporters. Lipid transport is less well studied but is assumed to progress as in mammals, with diffusion or facilitated transport of fatty acids released from micelles upon contact with the intestinal mucosa. Nutrient transport is a well-covered field with numerous reviews and books (e.g. Bakke et al., 2011; Halver, 2013), and thorough discussion is beyond our scope here.

Digestion is affected by numerous factors beyond the explicit enzyme and transport activities. The rate at which food is captured will determine the rate at which it is provided to the system for processing in both teleosts (e.g. Higham, 2011) and elasmobranchs (e.g. Wilga and Ferry, 2015). Once it is captured, the rate of processing (g of digesta g−1 of body mass−1 h−1) can be controlled by the animal and/or set by the food (e.g. Jackson et al., 1987). Gastric evacuation rate investigations have revealed a variety of patterns, including exponential, linear, and logarithmic models (e.g. Jobling, 1987). Using these models alongside physiological experiments, GIT evacuation rates were shown to be inversely proportional to predator size (e.g. reviewed by Bromley, 1994; Gillum et al., 2012). The anatomy of the GIT also affects digestion rates, with narrow sphincters restricting and controlling digesta movement (Edwards, 1971; Kionka and Windell, 1972). Further, the length and/or diameter of the intestine can control digestion times (MacDonald et al., 1982); indeed, a larger intestine diameter or length may represent an adaptation to increase nutrient assimilation in many herbivores for more efficient digestion (Sibly and Calow, 1986; Munoz and Ojeda, 2000).

6.3 Digestive System Morphology

The functions of the digestive system are supported through various anatomical organs that combine to form the organ system with a ‘front end’ – mouth and buccal cavity, which is responsible for capture and mechanical processing of food, and a ‘back end’ – oesophagus to rectum, which is associated with digestion, assimilation of nutrients, and removal of waste. It is important to note that evolution of ‘back-end’ function would necessarily influence ‘front-end’ form and function, and vice versa. Here, we will focus on the back end of the gut, summarizing centuries of investigation in fish gut anatomy and physiology. We refer the reader to more in-depth reviews of the physiology of the fish gut (e.g. Al-Hussani, 1949; Harder, 1975; Clements and Raubenheimer, 2005; Wilson and Castro, 2011) and include recent examinations of functional relevance and evolution for some of the more intriguing modifications of the fish gut.

With more than 30,000 species of fishes (Nelson et al., 2016), there is an amazing array of modifications related to environment, trophic niche, dominant diet, and life stage, with a number of examples of convergent evolution (a trait that has evolved independently in different species) of key structures within the GIT (Wilson and Castro, 2011; Agyriou et al., 2016). Teleosts occupy a variety of trophic levels and ecological niches, thus demanding a variety of specific functions from their digestive systems (Kapoor et al., 1975; Fänge and Grove, 1979; Wilson and Castro, 2011). Conversely the gut of elasmobranchs is relatively anatomically uniform despite a broad range in dietary preferences across species (Bucking, 2015). That said, where gross morphology may not reveal specializations to the naked eye, it is safe to assume that differences must exist. Several accessory organs, such as the liver, gallbladder, and pancreas, are associated with the GIT, completing the digestive system (Table 6.1). With exciting advancements being made regarding the contribution of the bacterial communities in the gut to the physiology of fishes, more recently under consideration as an accessory organ is the GIT microbiome (Table 6.1).

Table 6.1 Overview of Structure and Function of the Digestive System

Structure

Function

Buccal Cavity and Oesophagus

Filtration, mechanical digestion, mucus production, nervous signalling, osmoregulation, respiration

Stomach

Absorption, chemical and enzymatic digestion, hormonal and nervous signalling, pathogen protection, respiration

Intestine

Absorption, chemical and enzymatic digestion, hormonal and nervous signalling, respiration

Rectum and Colon

Defecation, final processing of contents

Accessory Organs

Liver

Chemical and enzyme production and secretion

Gallbladder

Storage and release of enzyme and chemical components for breakdown of macromolecules

Pancreas

Exocrine – enzyme production and secretion Endocrine – production of hormones involved in regulation of carbohydrate, amino acid, and lipid uptake

Intestinal Microbiome

Enterocyte proliferation, enzyme production, nutrient transport and storage, gene expression regulation, immunity

6.3.1 Buccal Cavity, Pharynx, and Associated Structures

There is a vast array of information on the anatomy of the head and cranium, and detailed reviews are available on the morphology and feeding mechanics in fish (e.g. Higham, 2011; Wilga and Ferry, 2015). Mucus produced in the buccal cavity may play a role in trapping food particles in suspension-feeders (Sanderson et al., 1996), but there is little evidence of enzymatic catabolism for digestion (Al-Hussani, 1949) as seen in higher vertebrates. Posterior to the buccal cavity is the pharynx, containing the gill slits located in the ventrolateral walls. There are nutrient digestion processes supported here by anatomical adaptations in the form of gill rakers for filtering and trapping food particles. These structures are of particular importance in ram or filter feeding. For example, the pharyngeal epithelium of the basking shark contains papillae that may additionally aid in food particle capture and movement (Matthews and Parker, 1950). Finally, the buccal cavity contains taste buds, acting as peripheral sense organs and transmitting information to the central nervous system, which show ultrastructural heterogeneity among taxa (Reutter et al., 2000).

6.3.2 Oesophagus

The oesophagus is a short tube-like structure connecting the buccal cavity with the rest of the intestinal tract (see Figures 6.2 through 6.4). Entry into the oesophagus is controlled by a sphincter that is closed except when passing food. There is usually a proximal and a distal portion in the oesophagus, which serve differing functions, often related to diet and/or life history. One universal feature of the oesophagus in fishes is numerous mucus-secreting cells, which probably lubricate the mucosa, aiding the passage of food in addition to protecting the oesophageal epithelium from chemical and/or physical damage as food passes (Yamamoto and Hirano, 1978). The oesophagus also plays a role in desalination of imbibed seawater in marine teleosts, reducing the osmolality from ~1000 to 500 mOsm.L−1, absorbing NaCl at an approximate ratio of 1:1 (reviewed in Grosell, 2014). The transport mechanisms of either sodium or chloride in this region of the marine teleost intestine are not well understood, but recent identification of sodium binding by the mucus (Wong et al., 2018) has revealed a potential novel mechanism for the removal of sodium from imbibed seawater. This substantial contribution to the desalination of imbibed seawater in marine teleosts is clearly linked to the overall osmoregulatory function of the gut in marine teleosts (reviewed in Grosell, 2014).

FIGURE 6.2 Gastrointestinal tract of the ratfish, Hydrolagus colliei. C: colon; E: oesophagus; SV: spiral valve.
Photo credit Alyssa Weinrauch.
FIGURE 6.3 Gastrointestinal tract of the North Pacific spiny dogfish, Squalus suckleyi. C: colon; CS: cardiac stomach; E: oesophagus, P: pylorus; PS: pyloric stomach; RG: rectal gland; SV: spiral valve.
Photo credit Alyssa Weinrauch.
FIGURE 6.4 Gastrointestinal tract of the lake sturgeon, Acipenser fulvescens. AI: anterior intestine; CS: cardiac stomach; E: oesophagus, P: pylorus; PC: pyloric caeca; PS: pyloric stomach; SV: spiral valve.
Photo credit Alyssa Weinrauch.

The oesogastric region connects the oesophagus to the stomach and can be a valve-like structure, as observed in some elasmobranchs, but in most actinopterygians (ray-finned fishes), there is an absence of any valve structure; there is simply an abrupt transition from non-glandular tissue to gastric glandular tissue (Kapoor et al., 1975; Fänge and Grove, 1979).

6.3.3 Stomach

Posterior to the oesophagus is a gastric region, which may or may not contain a stomach. The agastric phenotype is found throughout the fishes and is one example of convergent evolution, as it is found in lampreys and hagfish (Agnathans; Figure 6.1), ratfish and rabbitfish (Chimera); Figure 6.2), lungfish (Lipidosireniformes), and close to 20% of the ray-finned fishes (Wilson and Castro, 2011). Using genomic and transcriptomic mapping, almost all genes associated with gastric gland function were found to be absent in the stomachless ballan wrasse, Cheilinus undulatus (Lie et al., 2018). Why stomach loss has repeatedly occurred in the fish lineage is at present unknown. Possible hypotheses were put forward by Wilson and Castro (2011); however, in each of their hypotheses, Wilson and Castro (2011) provide examples of species and/or mechanisms that are counter to their arguments, underscoring the need for continued research to understand the driving factors in the evolution of stomach (and indeed, gut) form and function in the fishes. Importantly, the agastric phenotype is absent in the sharks, skates, and rays (Elasmobranchii) and non-teleostean ray-finned fishes: bichir, gar, sturgeons, paddlefish, and bowfin. Curiously, all these clades possess a spiral valve as a major, or minor (Figures 6.3 and 6.4), component of their intestine.

When present, the stomach is used for storage of ingested food as well as the initial chemical and enzymatic breakdown of food and absorption of ions, as introduced earlier. It is the first real glandular component of the fish gut and is a uniquely vertebrate innovation, distinguished by secretion of gastric juice containing HCl and pepsinogen (Smit, 1968). The anatomy of the stomach in those species that possess one varies between three forms: U (or J or siphon shaped), Y (or caecal shaped), and straight (Wilson and Castro, 2011). The U shape appears to be the most prevalent across the ray-finned fishes and sharks, skates, and rays; it will normally accommodate a large meal size and therefore could be considered a site for food storage. There are two primary sections: the anterior/cardiac or fundic stomach, immediately posterior to the oesophagus, is followed by the posterior or pyloric stomach (see Figure 6.3). A Y-shaped stomach has been reported for a number of species, including the teleosts Regalecus (oarfish) and Anguilla (eel). The blind-ended sac or caecum is thought to act as a food storage site (Barrington, 1957), which makes sense in the highly active predators Scomber (mackerel), which consume large amounts of prey over a short period when encountering shoals of bait fish (Suyehiro, 1941). The straight or sac-like stomach is rare in fishes but has been described in the Esocidae (pike) and the Tetraodontiformes (ocean sunfish/pufferfish) (Suyehiro, 1941).

The lumen of the gut is basically an opening to the environment, and with the ingestion of food and/or water, there is the potential for invasion of aquatic pathogens across the mucosa and into the fish. Mucus in fish is recognized as a major chemical and physical barrier (reviewed in Cain and Swain, 2011); however, gastric secretions in the stomach also serve as a barrier to pathogenic invasion in vertebrates that may damage or interfere with the existing biome community in the intestine (see later) or indeed, the host itself (Martinsen et al., 2005).

The stomach may also function as an air-breathing organ. This requires increased vascularization of the stomach wall and a substantial reduction in the thickness of the stomach wall in comparison to non-air-breathing species (reviewed in Nelson and Dehn, 2011). The majority of, and certainly the most well-studied, air-breathing fishes are found in neo-tropical zones and belong to the family Loriicaridae (Graham, 1999). The stomach as an air-breathing organ is often accompanied by a reduction in gastric gland activity in favour of oxygen uptake. Interestingly, the intestine in many of these species, such as the armoured catfishes, is exceptionally long and thus may be a compensation for the reduced chemical digestion available in the stomach (Nelson et al., 2007).

6.3.4 Intestine

Posterior to the stomach (if present) is the intestinal portion of the GIT, separated from the pyloric stomach by a circular band of muscle fibre forming the pyloric valve or sphincter (see pylorus in Figures 6.3 and 6.4), where the majority of chemical and enzymatic catabolism and nutrient absorption takes place.

In species lacking a stomach, an obvious anatomical and functional demarcation between the two may be lacking (see Figure 6.2). The portion immediately posterior to the stomach is often referred to as the small intestine or the anterior intestine. In most fishes studied to date, the entire length of the post-gastric region of the intestine (intestine + caeca) is capable of active nutrient transport (Ferraris and Ahearn, 1984; Bakke-McKellep et al., 2000). Even the enterocytes of the most distal region contain a brush border (Murray et al., 1996); however, such studies have not extended to elasmobranchs. The absorption of nutrients seems to occur at a greater rate in proximal intestinal regions as opposed to distal regions in both in vitro (Collie, 1985; Buddington and Diamond, 1987; Jutfelt et al., 2007) and in vivo (Diaz et al., 1997; Hernandez-Blasquez et al., 2006) studies. Certainly, most proteinaceous-derived material appears to be absorbed across the proximal region of the intestine (Fänge and Grove, 1979; Stroband and van der Veen, 1981), but there are, as always, exceptions, such as in the white sturgeon, where the posterior spiral valve (Figure 6.4) seemed to play a greater role in nutrient acquisition in comparison to anterior regions of the intestine (Buddington et al., 1987).

The optimization of enzyme degradation of food particles and absorption of nutrients in the intestine is largely dependent on surface area; this is most easily achieved by simply increasing the length of the organ and/or the surface area of the mucosa. The latter component is central to nutrient absorption with primary, secondary, and tertiary folds in the intestinal mucosa and the presence of microvilli at the brush border on the apical surface of intestinal epithelial cells that can contribute up to 90% of the total surface area in some tilapia (Frierson and Foltz, 1992). It may seem intuitive to suggest that the length of the fish intestine should be related to dominant diet type. For example, the lower digestibility of herbivorous diets tends toward a longer intestine in herbivorous fishes (Clements and Raubenheimer, 2005), with the high nutrient availability in carnivorous diets generally resulting in a shorter intestine in carnivorous fishes. However, fish intestinal length and mass are also related to other key factors, such as physical space available in the abdominal cavity, allowing for a large liver and the development of embryos in viviparous elasmobranch species (Wetherbee and Cortés, 2012); meal size/type; satiation state (fasted vs. satiated); fish size for some species but not others (reviewed by Barrington, 1957); activity levels: tunafish are known to have particularly long intestines relative to less active ambush predators such as pike (Suyehiro, 1941); and development stage (Clements and Raubenheimer, 2005). Thus, the gross morphology of the intestine cannot immediately be correlated with dietary habits or trophic niche; indeed, there are examples of strictly carnivorous, agastric species (cyprinid Aspius aspius) (Dabrowski, 1993) or short intestine length in herbivorous species (Horn, 1989), nor does intestinal length necessarily correlate with gut evacuation time (Hofer, 1988).

One structure worthy of further discussion is the spiral, scroll, or roll valve that occurred early in the vertebrate lineage (Argyriou et al., 2016). It is absent in the derived ray-finned fishes (teleosts) but is found in non-teleostean ray-finned fishes (Acipenseriformes, Amiiformes, Polypteriformes, and Lepisosteiformes) and is ubiquitous in the sharks, skates, rays, and chimeras (Harder, 1975; Wilson and Castro, 2011). In the non-teleostean ray-finned fishes, the valve forms the posterior region of the intestine (Figure 6.4), varying in size (Argyriou et al., 2016), whereas in the elasmobranchs, it is the intestinal region of the gut (Figure 6.3), and in the agastric Holocephali, the spiral portion begins approximately one-third down the length of the gut from the oesophagus (Figure 6.2). While the spiral valve is considered a primitive form of the intestine, its absence in the hagfish (Figure 6.1) but presence in the lampreys, combined with recent fossil records, provides evidence that the spiral valve is another example of convergent evolution in the fish intestine (Argyriou et al., 2016). In the non-teleostean actinopterygians, the anterior intestine links the stomach to the spiral valve through a series of loops that can be long (bowfin and gar), medium (sturgeon and paddlefish; Figure 6.4), or short (bichir). From a functional perspective, the spiral valve shortens the total length of the intestine; however, the potential reduction in surface area with the loss in length is offset by the spiral, scroll, or roll arrangement of the mucosa, resulting in a substantial increase in surface area, up to threefold in ring-type valve structures or sixfold in conicospiral configurations (Bertin, 1958).

Naturally, the more turns in the spiral, the greater the surface area, and attempts have been made to correlate the number of turns with the ecology of the animal. An increase in the number of turns was historically considered to be largely influenced by diet (Qingweng and Yuanding, 1985; Holmgren and Nilsson, 1999; Wetherbee and Cortés, 2012). Indeed, in large elasmobranchs that may consume considerable meal sizes, such as the great white, Carcharodon carcharius; thresher sharks, Allopidae; whale shark, Rhinchodon typus; and basking shark, Cetorhinus maximus, the spiral valve has a tight ring-type structure with a large number of folds (Qingwen and Yuanding, 1985) compared with the less compact spiral shape found in smaller predatory sharks such as Squalus suckleyi (Figure 6.3). With correction for relatedness, larger animals tend to have an increase in the number of turns in the spiral valve, but there is reasonable consistency in the number of folds within a species regardless of size (Agryriou et al., 2016).

The driving factors causing the evolution of the spiral valve are unclear. One notion in elasmobranchs is a conservation of space in the coelomic cavity to accommodate embryonic development and liver size (Moss, 1984; Wetherbee and Cortés, 2012). It seems that space constraints for embryonic development would not be relevant for males, and there is no evidence of sexual dimorphism in spiral valve morphology in elasmobranchs. What is uniform in elasmobranchs and chimeras is a large liver. The high fat content of the liver makes it a buoyancy aid in elasmobranchs and holocephalans that lack a swim bladder (Baldridge, 1972), and there is no evidence indicating sexual dimorphism of liver size in these fishes, so similar restrictions on available space in the coelomic cavity would apply regardless of sex. However, similar space constraints (at least in terms of liver size) do not exist in the non-teleost ray-finned fishes and therefore cannot be used to explain the retention of a spiral valve in those fishes.

Additional structures related to digestive function include the pyloric caecae found in many teleosts (~60% of all species; Hossain and Dutta, 1996) and a few elasmobranchs (Buddington and Diamond, 1987; Holmgren and Nilsson, 1999). The number of caecae is species dependent and ranges from a single blind-ended structure (Figure 6.4) to over 1000 (Suyehiro, 1941; Rahimullah, 1945). The length, diameter, and shape of caecae vary greatly across the fishes; however, prevailing evidence suggests that function is similar (absorption of nutrients and ions) across those species that have them (Buddington and Diamond, 1987). Investigation into the role of caecae in rainbow trout revealed functional heterogeneity both along the gut (from anterior to posterior) as well as along the individual caecae from proximal to the intestinal lumen to the distal tip (Williams et al., 2019). Pyloric caecae are another example of convergent evolution in the fish gut.

6.3.5 Colon and Rectum

The colon and rectum connect to the anus, which forms the posterior valve to the environment and controls the elimination of wastes through defecation. The function of this region of the intestine is not as clear as in mammals, but roles in water absorption (e.g. Bucking and Wood, 2006) and assimilation of nutrients by endocytosis (e.g. Stroband and van der Veen, 1981) are the most clearly studied. Extensive muscular layers are found in this section, clearly distinguishing it from the intestine. The ileorectal valve separates the intestine from the rectum and is usually linked with a thickening of the muscle layer and/or a reduction of the diameter of the intestine (Harder, 1975; Kapoor et al., 1975). Further, the epithelium in the rectum is stratified compared with the columnar cells observed in the intestine (Holmgren and Nilsson, 1999). In elasmobranchs, there is clear separation between the spiral valve and the rectum, and it was recently shown that the rectum may have a role in solute balance in the little skate, Leucoraja erinacea, prior to evacuation of gut contents into the environment (Anderson et al., 2010).

6.3.6 Associated Organs

The anterior intestine is connected to the liver and pancreas, which are responsible for producing numerous enzymatic and chemical components of digestion. These components are then secreted into the GIT lumen, where they exert their effects via several ducts. The liver produces bile, which is stored in the gallbladder before secretion into the anterior intestine via the biliary duct. Bile production rates are generally similar across teleosts (Grosell et al., 2000) and elasmobranchs (Boyer et al., 1976). Control of bile secretion may be via a gastrin- or CCK-like peptide, as in other vertebrates (Andrews and Young, 1988). Gastrin and CCK-like peptide have been detected in elasmobranch (Hansen, 1975; Vigna, 1979) and teleost (Kurokawa et al., 2003) gastric mucosa.

The pancreas in fishes has both endocrine and exocrine functions and varies from a discrete, easily identifiable organ in elasmobranchs and chimeras to a diffuse network of cells embedded in the wall of the digestive tract in many teleosts. The exocrine pancreas produces digestive enzymes for protein (Holmgren and Nilsson, 1999) and fat (Sternby et al., 1983) digestion and occasionally chitinases when insects and crustaceans are a large dietary component (Fänge et al., 1979). These secretions are stimulated by gastric acid additions to the anterior intestine (Babkin, 1929, 1933), although limited work has occurred since these early studies.

6.3.7 Microbiome

A microcosm of bacteria, fungi, and archaea exists in the digestive tract of fishes. And while it is often considered to be its own system, its intimate ties to the digestive tract in terms of both location and function necessitate its inclusion here as an associated organ. We will focus on bacteria here, but be aware that there are more contributors to the microbiome, such as fungi and other unicellular organisms. The GIT microbiome bacteria can be classified as autochthonous or allochthonous. Autochthonous bacteria adhere to the intestine and colonize the surface and are generally thought of as the functional microbiome. Allochthonous bacteria are transiently found in the gut, likely due to ingestion, and do not form permanent colonies. Work on the microbiome has exploded in the last 10–15 years, driven mainly through technological advances in DNA sequencing. These new studies show that there are species-specific microbiomes in fishes that are environmentally dependent (Sullam et al., 2012) and shaped by unknown host factors as well as age, starvation, pollutants, and diet (reviewed by Nayak, 2010; Ghanbari et al., 2015; Wang et al., 2018). Further, it appears that the microbial communities display heterogeneity along the tract in terms of both number of bacteria (e.g. Navarrete et al., 2009) as well as their identity (e.g. Zhou et al., 2009). Generally speaking, deep sequencing has revealed that the autochthonous bacterial communities found in the fish intestine contain an enormous variety of microorganisms (e.g. Nayak, 2010). This variety can be not only between host species but also within host species gathered from the same geographical location (e.g. Star et al., 2013). The fish gut can contain an average of 109 bacteria per gram of intestinal content (Nayak, 2010), and the predominant phyla are Proteobacteria, Fusobacteria, Firmicutes, Bacteroidetes, and Actinobacteria (e.g. Wang et al., 2018).

We are just beginning to understand the functional importance of the fish gut microbiome, including roles such as epithelial renewal and cell proliferation (Rawls et al., 2004; Cheesman et al., 2011), nutrient transport (Rawls et al., 2004; Bates et al., 2006) and storage (Semova et al., 2012; Camp et al., 2012), as well as immunity (Galindo-Villegas et al., 2012). An important function of the microbiome is probably to aid in nutrient absorption by supplementing or providing digestive enzymes (Nayak, 2010; Ray et al., 2012), and the contribution of exogenous sources of digestive enzymes to fish has been studied for decades. For example, early studies have revealed cellulase activity in the stomachs (Stickney and Shumway, 1974) and intestines of vertebrates (e.g. Das and Tripathi, 1991); however, it is more than likely that this is contributed by endosymbionts like bacteria (Saha and Ray, 1998). In fact, it appears that the microbiome is capable of contributing numerous enzymes, including amylase, lipase, and proteases (Ray et al., 2012).

6.4 Future Perspectives

Without question, the vast majority of functional and morphological information regarding the digestive system in fishes has come from species of commercial importance. Understandably, describing basic gut physiology in these species has huge financial implications for the aquaculture industry given the need for sourcing viable food types and creating sustainable aquaculture resources. Additionally, the advent of modern molecular techniques has led to significant advances in understanding the role of the microbiome. By restricting research to this small proportion of species, we are limiting our knowledge and potentially obscuring important evolutionary drivers and patterns. More needs to be done in terms of understanding the molecular triggers for development of key gut structures in non-model fishes as well as their functional relevance. For example, three illustrations of convergent evolution of gross morphological features of the fish gut have been highlighted: gastric vs. agastric; presence vs. absence of pyloric caecae; and presence vs. absence of a spiral valve. As investigation of non-commercially relevant species continues, we will be able to unravel the functional evolution of these structures in vertebrates. Additionally, understanding the importance of the microbiome in fish physiology promises to yield novel and intriguing lines of research that undoubtedly will feed into innovative applications in the aquaculture industry, promoting nutrient uptake and growth in food fishes.

Acknowledgements

Research conducted by CB and WGA is supported by funding from the Natural Sciences and Engineering Research Council of Canada Discovery Grant Program. The authors thank Dr. Alyssa Weinrauch for the pictures and associated artwork presented in this chapter and staff at Bamfield Marine Science Centre (BMSC) for assistance with the collection and maintenance of the marine fishes displayed in this chapter, in particular Dr. Eric Clelland for facilitating research conducted at BMSC.

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