Cockroache; Ecology, behavior & history - W.J. Bell

MICROBES IN AND ON FOODSTUFFS
Because of the intimate association of microbial consortia
and the substrate they are decomposing, both are ingested
by detritivores. It is the microbial material, rather
than the substrate that may serve as the primary source of
nutrients (Berrie, 1975; Plante et al., 1990; Anduaga and
Halffter, 1993; Gray and Boucot, 1993; Scheu and Setälä,
2002). Scanning electron micrographs show that millipedes,
for example, strip bacteria from the surface of
ingested leaf litter (Bignell, 1989), and similar to cockroaches,
they can be found feeding on corpses in advanced
stages of decay (Hoffman and Payne, 1969). Most
foods known to be included in the diet of cockroaches in
natural habitats are profusely covered with microbes.
Bacteria and fungi are present on leaves before they are
abscised, and their numbers increase rapidly as soon as
the litter has been wetted on the ground (Archibold,
1995). The floor of a tropical rainforest is saturated with
microbial decomposers, and as decay is successional, different
species of microbe are associated with different
parts of the process. A square meter of a tropical forest
floor may contain leaves from 50 or more plant species,
and each leaf type may have a different microflora and
microfauna. Microbial populations may also vary with
season, with climate, with soil, and with the structure of
the forest; there is no simple way to recognize all of the
variables (Stout, 1974). Dead logs, treeholes, bird and rodent
nests, bat caves, and other such cockroach habitats
are also microbial incubators. Bacteria are ubiquitous,
but flagellates, small amoebae, and ciliates are also important
agents of decomposition, and are associated with
every stage of plant growth and decline, from the phylloplane
to rhizosphere (Stout, 1974). Fermenting fruits and
plant exudates (e.g., oozing sap) support the growth of
yeasts, which are exploited as a source of nutrients in
many insect species (Kukor and Martin, 1986). Cockroaches
in culture favor overripe fruit, with the rotted
part of the fruit eaten first, and fruit fragments intercepted
by leaves in tropical forests are far from fresh. Blattella
vaga has been observed in large numbers around decaying
dates on the ground (Roth, 1985). Vertebrate feces
are obviously rich sources of microbial biomass, particularly
in bat caves, and, as discussed in Chapter 4, some
cave cockroaches apparently assimilate bacteria from ingested
soil.
THE ROLE OF MICROBES IN DIGESTION
The success of cockroaches within their nutritional environment
results in large part from their relationship with
microorganisms (Mullins and Cochran, 1987) at three
levels: the microbes that comprise the gut fauna, the microbes
found on ingested foodstuffs and fecal pellets, and
the intracellular bacteria in the fat body.
Hindgut Microbes
The guts of all cockroach species examined house a diverse
anaerobic microbiota, with ciliates, amoebae, flagellates,
and a heterogeneous prokaryotic assemblage,
including spirochetes (Kidder, 1937; Steinhaus, 1946;
Guthrie and Tindall, 1968; Bracke et al., 1979; Bignell,
1981; Cruden and Markovetz, 1984; Sanchez et al., 1994;
Zurek and Keddie, 1996; Lilburn et al., 2001). Methanogenic
bacteria, a good indicator of microbial fermentative
activity (Cazemier et al., 1997b), are found both free in
the gut lumen and in symbiotic association with ciliates
and mastigotes in most cockroach species tested (Bracke
et al., 1979; Gijzen and Barugahare, 1992; Hackstein and
Strumm, 1994). Nyctotherus (Fig. 5.1) can host more than
4000 methanogens per cell (Hackstein and Strumm,
1994), and hundreds to thousands of the ciliate can be
found in full-grown cockroaches (van Hoek et al., 1998).
Microbes are densely packed within the gut, but in a predictable
spatial arrangement; food is processed sequentially
by specific microbial groups as it makes its way
through the digestive system. Volatile fatty acids (VFAs)
are present in the hindgut, further suggesting the degradation
of cellulose and other plant polysaccharides
(Bracke and Markovetz, 1980). The hindgut wall of cockroaches
is permeable to organic acids (Bignell, 1980;
Bracke and Markovetz, 1980; Maddrell and Gardiner,
1980), indicating that the host may directly benefit from
the products of microbial fermentation. Long cuticular
spines and extensive infolding of the hindgut wall increase
surface area and provide points of attachment for
the microbes (Bignell, 1980; Cruden and Markovetz,
1987; Cazemier et al., 1997a). Finally, redox potentials indicate
conditions are more reducing than in other insect
species, with the exception of termites (Bignell, 1984).
These features of cockroach digestive physiology support
the notion that plant structural polymers play a significant
role in the nutritional ecology of Blattaria; however,
we currently lack enough information to appreciate
fully the subtleties of the interactions in the hindgut. It is
known to be a fairly open system, with a core group of
mutualists, together with a “floating”pool of microbes recruited
from those entering with food material (Bignell,
1977b, pers. comm. to CAN). Populations of the microbial
community shift dynamically in relation to the food
choices of the host.Whatever rotting substrate is ingested,
a suite of microbes responds and proliferates (Gijzen et
al., 1991, 1994; Kane and Breznak, 1991; Zurek and Keddie,
1998; Feinberg et al., 1999).
Cellulases are distributed throughout the cockroach
MICROBES: THE UNSEEN INFLUENCE 77