Digestive Physiology Overview

The study of digestive physiology involves the spatial organization of digestive events in the insect gut. Digestive enzymes that participate in primary digestion (cleavage of polymers like protein and starch), secondary digestion (action on oligomers exemplified by polypeptides and dextrans), and final digestion (hydrolysis of dimers as dipeptides and disaccharides) are assayed in different gut compartments. Samples of the ectoperitrophic space contents (Fig. 1) are collected by puncturing the midgut ceca with a capillary or by washing the luminal face of midgut tissue. Midgut tissue enzymes are intracellular, glycocalyx-associated or microvillar membrane-bound. In addition to the distribution of digestive enzymes, the spatial organization of digestion depends on midgut fluxes. Gut fluid fluxes are inferred with the use of dyes. Secretory regions transport injected dye into the gut lumen, whereas absorbing regions accumulate orally fed dyes. Upon studying the spatial organization of the digestive events in insects of different taxa and diets, it was realized that the insects may be grouped relative to their digestive physiology, assuming they have common ancestors. Those putative ancestors correspond to basic gut plans from which groups of insects may have evolved by adapting to different diets.

FIGURE 5 Diagrammatic representation of water fluxes (dashed arrows) and of the circulation of digestive enzymes (solid arrows) in putative insect ancestors that correspond to the major basic gut plans. In Neoptera ancestors (A), midgut digestive enzymes pass into the crop. Countercurrent fluxes depend on the secretion of fluid by the Malpighian tubules and its absorption by the ceca. Enzymes involved in initial, intermediate, and final digestion circulate freely among gut compartments. Holometabola ancestors (B) are similar except that secretion of fluid occurs in posterior ventriculus. Panorpoid (Lepidoptera and Diptera assemblage) ancestors (C) display countercurrent fluxes like Holometabola ancestors, midgut enzymes are not found in crop, and only the enzymes involved in initial digestion pass through the peritrophic membrane. Enzymes involved in intermediate digestion are restricted to the ectoperitrophic space and those responsible for terminal digestion are immobilized at the surface of midgut cells. Cyclorrhapha ancestors (D) have a reduction in ceca, absorption of fluid in middle midgut, and anterior midgut playing a storage role. Lepidoptera ancestors (E) are similar to panorpoid ancestors, except that anterior midgut replaced the ceca in fluid absorption. Hemiptera ancestors (F) lost crop, ceca, and fluid-secreting regions. Fluid is absorbed in anterior midgut.

FIGURE 5 Diagrammatic representation of water fluxes (dashed arrows) and of the circulation of digestive enzymes (solid arrows) in putative insect ancestors that correspond to the major basic gut plans. In Neoptera ancestors (A), midgut digestive enzymes pass into the crop. Countercurrent fluxes depend on the secretion of fluid by the Malpighian tubules and its absorption by the ceca. Enzymes involved in initial, intermediate, and final digestion circulate freely among gut compartments. Holometabola ancestors (B) are similar except that secretion of fluid occurs in posterior ventriculus. Panorpoid (Lepidoptera and Diptera assemblage) ancestors (C) display countercurrent fluxes like Holometabola ancestors, midgut enzymes are not found in crop, and only the enzymes involved in initial digestion pass through the peritrophic membrane. Enzymes involved in intermediate digestion are restricted to the ectoperitrophic space and those responsible for terminal digestion are immobilized at the surface of midgut cells. Cyclorrhapha ancestors (D) have a reduction in ceca, absorption of fluid in middle midgut, and anterior midgut playing a storage role. Lepidoptera ancestors (E) are similar to panorpoid ancestors, except that anterior midgut replaced the ceca in fluid absorption. Hemiptera ancestors (F) lost crop, ceca, and fluid-secreting regions. Fluid is absorbed in anterior midgut.

Neopteran insects evolved along three lines: the Poly-neoptera (which include Blattodea, Isoptera, and Orthoptera), the Paraneoptera (which include Hemiptera), and the Holometabola (which include Coleoptera, Hymenoptera, Diptera, and Lepidoptera). Polyneoptera and Paraneoptera evolved as external feeders occupying the ground surface, on vegetation, or in litter, and developed distinct feeding habits. Some of these habits are very specialized (e.g., feeding wood and sucking plant sap), implying adaptative changes of the digestive system. Major trends in the evolution of Holometabola were the divergence in food habits between larvae and adults and the exploitation of new food sources, exemplified by endoparasitism and by boring or mining living or dead wood, foliage, fruits, or seeds. This biological variation was accompanied by modifications in the digestive system. Among the panorpoid Holometabola (an assemblage that includes Diptera and Lepidoptera), new selective pressures resulted from the occupation of more exposed or ephemeral ecological niches. Following this trend, those pressures led to shortening life spans, so that the insects may have more generations per year, thus ensuring species survival even if large mortality occurs at each generation. Associated with this trend, the digestive system evolved to become more efficient to support faster life cycles.

The basic plan of digestive physiology for most winged insects (Neoptera ancestors) is summarized in Fig. 5A. In these ancestors, the major part of digestion is carried out in the crop by digestive enzymes propelled by antiperistalsis forward from the midgut. Saliva plays a minor role or no role at all in digestion. After a while, following ingestion, the crop contracts, transferring digestive enzymes and partly digested food into the ventriculus. The anterior ventriculus is acid and has high carbohydrase activity, whereas the posterior ventriculus is alkaline and has high proteinase activity. This differentiation along the midgut may be an adaptation to the instability of ancestral carbohydrases in the presence of proteinases. The food bolus moves backward in the midgut of the insect by peristalsis. As soon as the polymeric food molecules have been digested to become small enough to pass through the peritrophic membrane, they diffuse with the digestive enzymes into the ectoperitrophic space (Fig. 1). The enzymes and nutrients are then displaced toward the ceca with a countercurrent flux caused by secretion of fluid at the Malpighian tubules and its absorption back by cells (similar to Figs. 3A, C) at the ceca (Fig. 5A), where final digestion is completed and nutrient absorption occurs. When the insect starts a new meal, the ceca contents are moved into the crop. As a consequence of the countercurrent flux, digestive enzymes occur as a decreasing gradient in the midgut, and lower amounts are excreted.

The Neoptera basic plan is the source of that of the Polyneoptera orders and evolved to the basic plans of Paraneoptera and Holometabola. Lack of data limits the proposition of a basic plan to a single Paraneoptera order, Hemiptera. Symbiont microorganisms may occur in large numbers in insect gut. For example, the bacteria Nocardia rhodnii may represent up to 5% of the Rhodnius prolixus midgut dry weight. The symbionts are believed to provide nutrient factors (such as B vitamins or fermentation end products) to the host. Microorganism symbionts have rarely been associated with digestion, and the few that are known are implicated with cellulose digestion only.

Polyneoptera blattodea and mantodea Cockroaches, which are among the first neopteran insects to appear in the fossil record, are extremely generalized in most morphological features. They are usually omnivorous. In spite of the lack of detailed data on midgut fluxes and enzyme distribution, it is thought that digestion in cockroaches occurs as described for the Neoptera ancestor (Fig. 5A), except that part of the final digestion of proteins occurs on the surface of midgut cells. Another difference observed is the enlargement of hindgut structures (Fig. 2C), noted mainly in wood-feeding cockroaches. These hindgut structures harbor bacteria producing acetate and butyrate from ingested wood or other cellulose-containing materials. Acetate and butyrate are absorbed by the hindgut of all cockroaches, but this activity is more remarkable with wood roaches. Cellulose digestion may be accomplished by bacteria, but there is evidence that wood roaches have their own cellulases. Mantids have a capacious crop, and a short midgut and hindgut. It is probable that the major part of digestion takes place in their crops.

isoptera Termites are derived from and are more adapted than wood roaches in dealing with refractory materials such as wood and humus. Associated with this specialization, they lost the crop and midgut ceca and enlarged their hindgut structures (Fig. 2D). Termites digest cellulose with their own cellulase, and the products pass from the midgut into the hindgut, where they are converted into acetate and butyrate by hindgut bacteria as in wood roaches. Symbiotic bacteria are also responsible for nitrogen fixation in hindgut, resulting in bacterial protein. This is incorporated into the termite body mass after being expelled in feces by one individual and being ingested and digested by another. This explains the ability of termites to develop successfully in diets very poor in protein.

orthoptera Grasshoppers feed mainly on grasses, and their digestive physiology clearly evolved from the neopteran ancestor. Carbohydrate digestion occurs mainly in the crop, under the action of midgut enzymes, whereas protein digestion and final carbohydrate digestion take place at the anterior midgut ceca. The abundant saliva (devoid of significant enzymes) produced by grasshoppers saturate the absorbing sites in the midgut ceca, thus hindering the countercurrent flux of fluid. This probably avoids excessive accumulation of noxious wastes in the ceca, and makes possible the high relative food consumption observed among locusts in their migratory phases. Starving grasshoppers present midgut countercurrent fluxes. Cellulase found in some grasshoppers is believed to facilitate the access of digestive enzymes to the plant cells ingested by the insects by degrading the cellulose framework of cell walls. Crickets are omnivorous or predatory insects with most starch and protein digestion occurring in their capacious crop (Fig. 2B).

Paraneoptera hemiptera The characteristics of the Paraneoptera ancestors cannot be inferred because midgut function data are available only for Hemiptera. The Hemiptera comprise insects of several suborders (e.g., cicadas, leafhoppers, aphids, and fulgorids) that feed almost exclusively on plant sap, and insects of the taxon Heteroptera (e.g., assassin bugs, plant bugs, stinkbugs, and lygaeid bugs) that are adapted to different diets. The ancestor of the entire order is supposed to be a sapsucker similar to present-day cicadas and fulgorids.

The hemipteran ancestor (Fig. 5F) differs remarkably from the neopteran ancestor, as a consequence of adaptations to feeding on plant sap. These differences consist of the lack of crop and anterior midgut ceca, loss of the enzymes involved in initial and intermediate digestion and loss of the peritrophic membrane associated with the lack of luminal digestion, and, finally, the presence of hemipteran midgut cells (Fig. 3H), which have their microvilli ensheathed by an outer (perimi-crovillar) membrane. The perimicrovillar membrane maintains a constant distance from the microvillar membrane, extends toward the luminal compartment with a dead end, and limits a closed compartment, the perimicrovillar space (Fig. 3H). Ongoing research suggests that aphids have modified perimicrovillar membranes.

Sap-sucking Hemiptera may suck phloem or xylem sap. Phloem sap is rich in sucrose (0.15-0.73 M) and relatively poor in free amino acids (15-65 mM) and minerals, whereas xylem fluid is poor in amino acids (3-10 mM) and contains monosaccharides (about 1.5 mM), organic acids, potassium ions (about 6 mM), and other minerals. Thus, except for dimer (sucrose) hydrolysis, no food digestion is necessary in sapsuckers. The major problem facing a sap-sucking insect is to absorb nutrients, such as essential amino acids, that are present in very low concentrations in sap. Amino acids may be absorbed according to a hypothesized mechanism that depends on perimicrovillar membranes. In phloem feeders such as aphids, this process may have an assimilation efficiency of 55% for amino acids and only 5% for sugars, whereas in xylem feeders such as leafhoppers, about 99% of dietary amino acids and carbohydrates are absorbed.

Organic compounds in xylem sap need to be concentrated before they can be absorbed by the perimicrovillar system. This occurs in the filter chamber (Fig. 2P) of Cicadoidea and Cercopoidea, which concentrates xylem sap 10-fold, or in the filter chamber of Cicadelloidea (phloem feeders), which is able to concentrate dilute phloem about 2.5-fold. The filter chamber consists of a thin-walled, dilated anterior midgut in close contact with the posterior midgut and the proximal ends of the Malpighian tubules. This arrangement enables water to pass directly from the anterior midgut to the Malpighian tubules, concentrating food in midgut.

The evolution of Heteroptera was associated with regaining the ability to digest polymers. Because the appropriate digestive enzymes were lost, these insects instead used enzymes derived from lysosomes. Lysosomes are cell organelles involved in intracellular digestion carried out by special proteinases referred to as cathepsins. Compartmentalization of digestion was maintained by the perimicrovillar membranes as a substitute for the lacking peritrophic membrane. Digestion in the two major Heteroptera taxa—Cimico-morpha, exemplified by the blood feeder R. prolixus, and Pentatomorpha, exemplified by the seed sucker Dysdercus peruvianus—is similar. The dilated anterior midgut stores food and absorbs water and, at least in D. peruvianus, also absorbs glucose. Digestion of proteins and absorption of amino acids occur in the posterior ventriculus. Most protein digestion occurs in lumen with the aid of a cysteine proteinase and ends in the perimicrovillar space under the action of aminopeptidases and dipeptidases. Many

Heteroptera feed on parenchymal tissues of plants. In some of these insects, excess water passes from the expanded anterior midgut to the closely associated midgut ceca, which protrude from the posterior midgut (Fig. 2Q). These ceca may also contain symbiont bacteria.

Holometabola

The basic gut plan of the Holometabola (Fig. 5B) is similar to that of Neoptera except that fluid secretion occurs in the posterior ventriculus by cells similar to Fig. 3F, instead of by the Malpighian tubules. Because the posterior midgut fluid, unlike Malpighian tubular fluid, does not contain wastes, the accumulation of wastes in ceca is decreased. There is an evolutionary trend leading to the loss of anterior midgut ceca in holometabolous insects and an increase in the use of anterior ventricular cells for water absorption. Ceca loss probably further decreases the accumulation of noxious substances in the midgut, which would be more serious in insects that have high relative food consumption rates, such as is common among Holometabola. Digestive systems may change remarkably between larvae and adults of holometabolous insects. Despite these changes, adult digestive systems probably evolved in parallel to larval systems because, except for minor differences, the compartmentalization of digestion in larvae and adults seems to be similar.

The basic plan of Coleoptera and Hymenoptera did not evolve dramatically from the Holometabola ancestor, whereas the basic plan of Diptera and Lepidoptera (panorpoid ancestor, Fig. 5C) presents important differences. Thus, panorpoid ancestors have countercurrent fluxes like Holometabola ancestors but differ from these in the lack of crop digestion, in midgut differentiation in luminal pH, and in which compartment is responsible for each phase of digestion. In Holometabola ancestors, all phases of digestion occur in the endoperitrophic space (Fig. 1), whereas in panorpoid ancestors only initial digestion occurs in that region. In the latter ancestors, intermediate digestion is carried out by free enzymes in the ectoperitrophic space and final digestion occurs at the midgut cell surface by immobilized enzymes. The free digestive enzymes do not pass through the peritrophic membrane because they are larger than the peritrophic membrane pores. Immobilized enzymes may be either soluble enzymes entrapped in the cell glycocalyx or membrane-bound enzymes, which are those embedded in the lipid bilayer forming the microvillar membranes (intrinsic proteins). As a consequence of the compartmentalization of digestive events in panorpoid insects, there is an increase in the efficiency of digestion of polymeric food by allowing the removal of the oligomeric molecules from the endoperitrophic space, which in turn is powered by the recycling mechanism associated with the midgut fluxes. Because oligomers may be substrates or inhibitors for some polymer hydrolases, their presence should decrease the rate of polymer degradation. A fast polymer degradation ensures that polymers are not excreted, hence increases their digestibility. Another consequence of compartmentalization is an increase in the efficiency of oligomeric food hydrolysis by allowing the transference of oligomeric molecules to the ectoperitrophic space and by restricting oligomer hydrolases to this compartment. In these conditions, oligomer hydrolysis occurs in the absence of probable partial inhibition (because of nonproductive binding) by polymer food and presumed nonspecific binding by nondispersed undigested food. This process leads to the production of food monomers only in the neighborhood of the midgut cell surface, causing an increase in the concentration of the final products of digestion close to their transporters, thus facilitating absorption.

coleoptera Larvae and adults of Coleoptera usually display the same feeding habit; that is, both are plant feeders (although adults may feed on the aerial parts, whereas the larvae may feed on the roots of the same plant) or both are predatory. Coleoptera ancestors are like Holometabola ancestors except for the anterior midgut ceca, which were lost and replaced in function by the anterior midgut. Nevertheless, there are evolutionary trends leading to a great reduction or loss of the crop and, similar to panorpoid orders, occurrence of final digestion at the surface of midgut cells. Thus, in predatory Carabidae most of the digestive phases occur in the crop by means of midgut enzymes, whereas in predatory larvae of Elateridae initial digestion occurs extraorally by the action of enzymes regurgitated onto their prey. The preliquefied material is then ingested by the larvae, and its digestion is finished at the surface of midgut cells. The entire digestive process occurs in the larval endoperitrophic space of Dermestidae. In Tenebrionidae, the final digestion of proteins takes place at midgut cell surface; in Curculionidae and Cerambycidae, the final digestion of all nutrients is carried out at midgut cell surface. It has been proposed that Cerambycidae larvae acquire the capacity to digest cellulose by ingesting fungal cellulases while feeding on fungus-infested wood. In contrast, Coccinellidae adults use their own cellulase to digest cellulose. The distribution of enzymes in gut regions of adult Tenebrionidae is similar to that of their larvae. This suggests that the overall pattern of digestion in larvae and adults of Coleoptera is similar even though (in contrast to adults) beetle larvae usually lack a crop. Insects of the series Cucujiformia (which includes Tenebrionidae, Chrysomelidae, Bruchidae, and Curculionidae) have cysteine proteinases in addition to (or in place of) serine proteinases as digestive enzymes, suggesting that the ancestors of the whole taxon were insects adapted to feed on seeds rich in serine proteinase inhibitors.

Scarabaeidae and several related families are relatively isolated in the series Elateriformia and evolved considerably from the Coleoptera ancestor. Scarabid larvae, exemplified by dung beetles, usually feed on cellulose materials undergoing degradation by a fungus-rich flora. Digestion occurs in the midgut, which has three rows of ceca (Fig. 2F), with a ventral groove between the middle and posterior row. The alkalinity of gut contents increase to almost pH 12 along the midgut ventral groove. This high pH probably enhances cellulose digestion, which occurs mainly in the hindgut fermentation chamber (Fig. 2F), likely through the action of bacterial cell-bound enzymes. The final product of cellulose degradation is mainly acetic acid, which is absorbed through the hindgut wall. Whether scarabid larvae ingest feces to obtain nitrogen compounds, as described above for termites, is a matter of controversy.

hymenoptera Hymenoptera comprise several primitive suborders (including sawflies and horntails) and Apocrita. Apocrita are divided into Parasitica, which are parasites of other insects, and Aculeata, in which the piercing ovipositor of Parasitica evolved into a stinging organ. The first Apocrita were probably close to the ichneumon flies, whose larvae develop on the surface or inside the body of the host insect. Probably because of that, the larvae of Apocrita present a midgut that is closed at its rear end, and remains unconnected with the hindgut until the time of pupation. Hymenoptera ancestors differ from the Holometabola ancestor in the lack of anterior midgut ceca, which are replaced by the anterior midgut in the function of fluid absorption, and in the absence of midgut enzymes in the crop. Wood wasp larvae of the genus Sirex are believed to be able to digest and assimilate wood constituents by acquiring cellulase, xylanase, and possibly other enzymes from fungi present in wood on which they feed. In larval bees, most digestion occurs in the endoperitrophic space. Counter-current fluxes seem to occur, but the midgut luminal pH gradient hypothetically present in the Hymenoptera ancestor was lost.

Adult bees ingest nectar and pollen. Sucrose from nectar is hydrolyzed in the crop (Fig. 2I) by the action of a sucrase from the hypopharyngeal glands. After ingestion, pollen grains extrude their protoplasm into the ventriculus, where digestion occurs. Worker ants feed on nectar, honeydew, plant sap, or partly digested food regurgitated by their larvae. Thus, they seem to display only intermediate and (or) final digestion.

diptera The Diptera evolved along two major lines: an assemblage of suborders corresponding to the mosquitoes, including the basal Diptera, and the suborder Brachycera, which includes the most evolved flies (Cyclorrhapha). The Diptera ancestor is similar to the panorpoid ancestor (Fig. 5C) in having the enzymes involved in intermediate digestion free in the ectoperitrophic fluid (mainly in the large ceca), whereas the enzymes of terminal digestion are membrane bound at the midgut cell microvilli. Although these characteristics are observed in most nonbrachyceran larvae, the more evolved of these larvae may show reduction in size of midgut ceca (e.g., Culicidae, Fig. 2k). Nonhematophagous adults store liquid food (nectar or decay products) in their crops. Digestion occurs in their midgut as in larvae. Nectar ingested by mosquitoes (males and females) is stored in the crop, and digested and absorbed at the anterior midgut. Blood, which is sucked only by females, passes to the posterior midgut, where it is digested and absorbed.

The Cyclorrhapha ancestor (Fig. 5D) evolved dramatically from the panorpoid ancestor (Fig. 5C), apparently as a result of adaptations to a diet consisting mainly of bacteria. Digestive events in Cyclorrhapha larvae are exemplified by larvae of the house fly Musca domestica. These larvae ingest food rich in bacteria. In the anterior midgut there is a decrease in the starch content of the food bolus, facilitating bacteria death. The bolus now passes into the middle midgut where bacteria are killed by the combined action of low pH, a special lysozyme, and an aspartic proteinase. Finally, the material released by bacteria is digested in the posterior midgut, as is observed in the whole midgut of insects of other taxa. Countercurrent fluxes occur in the posterior midgut powered by secretion of fluid in the distal part of the posterior midgut and its absorption back into the middle midgut. The middle midgut has specialized cells for buffering the luminal contents in the acidic zone (Fig. 3D), in addition to those functioning in fluid absorption (Fig. 3A). Except for a few bloodsuckers, Cyclorrhaphan adults feed mainly on liquids associated with decaying material (rich in bacteria) in a way similar to house fly adults. That is, they salivate (or regurgitate their crop contents) onto their food. After the dispersed material has been ingested, starch digestion is accomplished primarily in the crop by the action of salivary amylase. Digestion is followed in the midgut, essentially as described for larvae. The stable fly, Stomoxys calcitrans, stores and concentrates the blood meal in the anterior midgut and gradually passes it to the posterior midgut, where digestion takes place, resembling what occurs in larvae. These adults lack the characteristic cyclorrhaphan middle midgut and the associated low luminal pH. Stable flies occasionally take nectar.

lepidoptera Lepidopteran ancestors (Fig. 5E) differ from panorpoid ancestors because they lack midgut ceca, have all their digestive enzymes (except those of initial digestion) immobilized at the midgut cell surface, and present long-necked goblet cells (Fig. 3B) and stalked goblet cells (Fig. 3E) in the anterior and posterior larval midgut regions, respectively. Goblet cells excrete K+ ions, which are absorbed from leaves ingested by larvae. Goblet cells also seem to assist anterior columnar cells in water absorption and posterior columnar cells in water secretion. Although most lepidopteran larvae have a common pattern of digestion, species that feed on unique diets generally display some adaptations. Tineola bisselliella (Tineidae) larvae feed on wool and display a highly reducing midgut for cleaving the disulfide bonds in keratin to facilitate proteolytic hydrolysis of this otherwise insoluble protein. Wax moths (Galleria mellonella) infest beehives and digest and absorb wax. The participation of symbiotic bacteria in this process is controversial. Another adaptation has apparently occurred in lepidopteran adults that feed solely on nectar. Digestion of nectar requires only the action of an a-glucosidase (or a P-fructosidase) to hydrolyze sucrose, the major component present. Nectar-feeding lepidopteran adults have amylase in salivary glands and several glycosidases and peptidases in the midgut. The occurrence of the whole complement of digestive enzymes in nectar-feeding moths may explain, at least on enzymological grounds, the adaptation of some adult Lepidoptera to new feeding habits such as blood and pollen.

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