Two of the major organic components of dead leaves and wood are cellulose and lignin. These pose considerable digestive problems for animal consumers, most of which are not capable of manufacturing the enzymatic machinery to deal with them. Cellulose catabolism (cellulolysis) requires cellulase enzymes. Without these, detritivores are unable to digest the cellulose component of detritus, and so cannot derive from it either energy to do work or the simpler chemical modules to use in their own tissue synthesis. Cellulases of animal origin have been definitely identified in remarkably few species, including a cockroach and some higher termites in the subfamily Nasutitermitinae (Martin, 1991) and the shipworm Teledo navalis, a marine bivalve mollusc
... competition and mutualism
Figure 11.12 The range of mechanisms that detritivores adopt for digesting cellulose (cellulolysis). (After Swift et al., 1979.)
Ingestion of cellulose by detritivore
Cellulases of soil and litter microflora acting on plant detritus before ingestion and/or on feces which are reingested that bores into the hulls of ships. In these organisms, cellulolysis poses no special problems.
The majority of detritivores, lacking their own cellulases, rely on the production of cellulases by associated decomposers or, in some cases, protozoa. The interactions range from obligate mutualism between a detritivore and a specific and permanent gut microflora or microfauna, through facultative mutualism, where the animals make use of cellulases produced by a microflora that is ingested with detritus as it passes through an unspecialized gut, to animals that ingest the metabolic products of external cellulase-producing microflora associated with decomposing plant remains or feces (Figure 11.12).
A wide range of detritivores appear to have to rely on the exogenous microbial organisms to digest cellulose. The invertebrates then consume the partially digested plant detritus along with its associated bacteria and fungi, no doubt obtaining a significant proportion of the necessary energy and nutrients by digesting the microflora itself. These animals, such as the spring-tail Tomocerus, can be said to be making use of an 'external rumen' in the provision of assimilable materials from indigestible plant remains. This process reaches a pinnacle of specialization in ambrosia beetles and in certain species of ants and termites that 'farm' fungus in specially excavated gardens (see Chapter 13).
Clear examples of obligate mutualism are found amongst certain species of cockroach and termite that rely on symbiotic bacteria or protozoa for the digestion of structural plant polysac-charides. Nalepa et al. (2001) describe the evolution of digestive mutualisms among the Dictyoptera (cockroaches and termites) from cockroach-like ancestors in the Upper Carboniferous that fed on rotting vegetation and relied on an 'external rumen'. The next stages involved progressive internalization of the microbiota associated with plant detritus, from indiscriminate coprophagy (feeding on feces of a variety of detritivorous species) through increasing levels of gregarious and social behavior that ensured neonates received appropriate innocula of gut biota. When proctodeal trophallaxis (the direct transfer of hindgut fluids from the rectal pouch of the parent to the mouth of the newborn young) evolved in certain cockroaches and lower termites, some microbes were captured and became ecologically dependent on the host. This specialized state ensured the direct transfer of the internal rumen, particularly those components that would degenerate if exposed to the external environment. In lower termites, such as Eutermes, symbiotic protozoa may make up more than 60% of the insect's body weight. The protozoa are located in the hindgut, which is dilated to form a rectal pouch. They ingest fine particles of wood, and are responsible for extensive cellulolytic activity, though bacteria are also implicated. Termites feeding on wood generally show effective digestion of cellulose but not of lignin, except for Reticuli-termes, which has been reported to digest 80% or more of the lignin present in its food.
Given the versatility apparent in the evolutionary process, it may seem surprising that so few animals that consume plants can produce their own cellulase enzymes. Janzen (1981) has argued that cellulose is the master construction material of plants 'for the same reason that we construct houses of concrete in areas of high termite activity'. He views the use of cellulose, therefore, as a defense against attack, since higher organisms can rarely digest it unaided. From a different perspective, most detritivores rely on microbial cellulases - they do not have their own woodlice rely on ingested microbial organisms cockroaches and termites rely on bacteria and protozoa why no animal cellulases?
Figure 11.13 The distribution of gut content categories of springtails (n = 6255) (Collembola; all species combined) in relation to depth in the litter/soil of beech forests in Belgium. (After Ponge, 2000.)
^ Empty guts ^ Mycorrhizae ^ Higher plant material Microalgae Pollen ^ Fungal material ^ Feces
it has been suggested that cellulolytic capacity is uncommon simply because it is a trait that is rarely advantageous for animals to possess (Martin, 1991). For one thing, diverse bacterial communities are commonly found in hindguts and this may have facilitated the evolution of symbiont-mediated cellulolysis. For another, the diets of plant-eaters generally suffer from a limited supply of critical nutrients, such as nitrogen and phosphorus, rather than of energy, which cellulolysis would release. This imposes the need for processing large volumes of material to extract the required quantities of nutrients, rather than extracting energy efficiently from small volumes of material.
Because microbes, plant detritus and animal feces are often very intimately associated, there are inevitably many generalist consumers that ingest all these resources. In other words, many animals simply cannot manage to take a mouthful of one without the others. Figure 11.13 shows the various components of the gut contents of 45 springtail species (all species combined) collected at different depths in the litter and soil of beech forests in Belgium. Species that occurred in the top 2 cm lived in a habitat derived from beech leaves at various stages of microbial decomposition where microalgae, feces of slugs and woodlice, and pollen grains were also common. Their diets contained all the local components but little of the very abundant beech litter. At intermediate depths (2-4 cm) the springtails ate mainly spores and hyphae of fungi together with invertebrate feces (particularly the freshly deposited feces of enchytraeid pot worms). At the lowest depths, their diets consisted mainly of mycorrhizal material (the springtails browsed the fungal part of the fungal/plant root assemblage) and higher plant detritus (mainly derived from plant roots). There were clear interspecific differences in both depth distributions and the relative importance of the different dietary components, and some species were more specialized feeders than others (e.g. Isotomiella minor ate only feces whereas Willemia aspinata ate only fungal hyphae). But most consumed more than one of the potential diet components and many were remarkably generalist (e.g. Protaphorura eichhorni and Mesaphorura yosii) (Ponge, 2000).
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