Although coprophagy simply means feeding on fecal material, it is an extremely complex, multifactorial behavior (Ullrich et al., 1992; Nalepa et al., 2001a). Fecal ingestion can be subdivided into several broadly overlapping categories, depending on the identity of the depositor, the nature of the fecal material, the developmental stage of the coprophage, and the degree to which feces are a mainstay of the diet. Many cockroaches feed on the feces of vertebrates, such as Periplaneta spp. in sewers or caves, desert cockroaches attracted to bovine and equine dung (Schoenly, 1983), and a variety of species attracted to bird droppings (Fig. 5.2). Here we highlight the feces of invertebrate detritivores (including conspecifics) as a source of cockroach food, and divide the behavior into three, not mutually exclusive categories.

Fig. 5.2 Unidentified nymph feeding on bird excrement, Ecuador. Photo courtesy of Edward S. Ross.

Microbes Refractory Metabolites,

°„ transient or digested food item exoenzymes gut fauna = of free living microbes

IUI of resident gut fauna of host

Microbes Refractory Metabolites,

°„ transient or digested food item exoenzymes gut fauna = of free living microbes

IUI of resident gut fauna of host

Fig. 5.3 Detritivore-microbial interactions during coproph-agy. When a cockroach feeds on a refractory food item (A), any starches, sugars, lipids present are digested, and endogenous cellulases permit at least some structural polysaccharides to be degraded as well. Much of the masticated litter, however, may be excreted relatively unchanged (B), and serve as substrate for microbial growth (C). Ingested microbes, whether from the substrate (D) or from the fecal pellets of conspecifics (C), may be digested, passed in the feces, or selectively retained as mu-tualists. Microbes on the food item, on the feces, and in the hindgut are sources of metabolites and exoenzymes of possible benefit to the insect (E). Metabolites of the insect and of the gut fauna excreted with the feces (F) may be used by microbes colonizing the pellets or reingested by the host during co-prophagy. Various authors shift the balance among these components, depending on the arthropod, its diet, its environment, and its age. From Nalepa et al. (2001a), with the permission of Birkhäuser Verlag.

Coprophagy as a Source of Microbial Protein and Metabolites

As food, the feces of detritivores are not fundamentally different from rotting organic matter; the feces of many differ very little from the parent plant tissue (Webb, 1976; Stevenson and Dindal, 1987; Labandeira et al., 1997). The differences that do occur, however, are important ones: feces are higher in pH, have a greater capacity to retain moisture, have increased surface to volume ratios, and generally occur in a form more suitable for microbial growth (McBrayer, 1973). Fecal pellets are colonized by a succession of microbes immediately after gut transit, with microflora increasing up to 100-fold (Lodha, 1974; Anderson and Bignell, 1980; Bignell, 1989). Fragmentation of litter is particularly important for bacterial growth, for unlike fungi, whose hyphae can penetrate tissues, bacterial growth is largely confined to surfaces (Dix and Webster, 1995; Reddy, 1995).The process is similar to gardeners creating a compost pile: microbially mediated decomposition occurs best when plant litter is moist and routinely turned. Coprophagy exploits the microbial consortia concentrated on these recycled cellulose-based foodstuffs (Fig. 5.3); the microorganisms serve not only as a source of nutrients and gut mutualists, but they also "predigest" recalcitrant substrates. Microbial dominance is so pronounced that fecal pellets may be considered living organisms. They consist largely of living cells, they consume and release nutrients and organic matter, and they serve as food for animals higher on the food chain (Johannes and Satomi, 1966).

Coprophagy as a Mechanism for Passing Hindgut Mutualists

All developmental stages feed on feces, but coprophagy is most prevalent in the early instars of gregarious domestic cockroaches (B. germanica, P. americana, P. fuliginosa) (Shimamura et al., 1994; Wang et al., 1995; Kopanic et al., 2001). Feces contain protozoan cysts, bacterial cells, and spores, and are the primary source of inoculative microbes (Hoyte, 1961a; Cruden and Markovetz, 1984). Very young cockroaches, with a hindgut volume of 1 ^l, already show significant bacterial activity (Cazemier et al., 1997a). Repeated ingestion of feces is no doubt required, however, because a successional colonization of the various gut niches by microbes is the norm (Savage, 1977). Obligate anaerobes have to be preceded by facultative anaerobes, and a complex bacterial community has to precede protozoan populations (Atlas and Bartha, 1998). Because cockroach aggregations are generally species specific, horizontal transmission of microbial mutualists from contemporary conspecifics may be considered typical. Mixed-species aggregations are occasionally re ported (Roth and Willis, 1960). Neonates, then, may also have sporadic access to interspecific fecal material. Analysis of rDNA repeats from the cockroach hindgut ciliate Nyctotherus indicates that there is a significant phyloge-netic component to the distribution of the ciliates among hosts, but transpecific shifts do occur (van Hoek et al., 1998). The longevity of cysts and spores in fecal pellets would contribute to transmission across species; cysts of Nyctotherus are estimated to survive 20 weeks under favorable conditions (Hoyte, 1961b).

We have little information on transmission of gut mu-tualists in non-gregarious species. In subsocial species of cockroaches or those with a short period of female brooding, transmission is probably vertical, via filial co-prophagy (Nalepa et al., 2001a). In Cryptocercus spp. in-tergenerational transfer occurs via proctodeal trophal-laxis (Seelinger and Seelinger, 1983; Nalepa, 1984), the direct transfer of hindgut fluids from the rectal pouch of a donor to the mouth of a receiver (McMahan, 1969). We do not know the mechanism of microbial transmission in oviparous species that abandon the egg case. Perhaps the female defecates in the vicinity of the ootheca, or the eggs are preferentially deposited near conspecific feces. Alternatively, neonates may acquire their gut biota directly from ingested detritus. Metabolically complementary consortia of microbes are always present on ingested organic material, because the microorganisms are themselves using it as a food source (Costerton, 1992; Shapiro, 1997). The mode of transmission of gut microbes in cockroaches is related to the degree of host-microbe interdependence and to host social behaviors; these three comprise a co-varying character suite (Troyer, 1984; Ewald, 1987; Nalepa, 1991; Chapter 9).

Coprophagy as a Mechanism for Passing Cockroach-Derived Substances

A coprophage has access to the metabolites, soluble nutrients, exoenzymes, and waste products of microbes both proliferating on feces and housed in the host digestive system, but also to products that originate from the insect host itself. The excretion of urate-containing fecal pellets by some blattellids can be a mode of intraspecific nitrogen transfer (Cochran, 1986b; Lembke and Cochran, 1990), discussed below. There are behaviorally distinct defecation behaviors in P. americana associated with physically different feces, and certain types of feces are eaten by early instars more frequently than others. Young nymphs were the only developmental stage observed feeding on the more liquid feces smeared on the substrate (Deleporte, 1988). Adult Cryptocercus punctulatus occasionally produce a fecal pellet that provokes a feeding frenzy in their offspring, while other pellets are nibbled or ignored (Fig. 5.4) (Nalepa, 1994). This behavior was also

Fig. 5.4 First instars of Cryptocercus punctulatus massed on and competing for a fecal pellet recently excreted by the adult female. Only certain pellets induce this behavior. Photo by C.A. Nalepa.

noted in C. kyebangensis as "clumping behavior" (Park et al., 2002). The basis of the appeal of these pellets is unknown.

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