Agriculture Reference
In-Depth Information
forests by the epigeic earthworm species
there have been no fungal-feedingÏpreference
studies for this species (however, the overall effect of this invasion is covered in the later section
discussing changes in the soil biota caused by colonizing earthworms). During grazing on organic
matter, earthworms ingest not only fungi, but also a range of other organisms (bacteria, algae,
protozoa, nematodes) associated with that material (Edwards and Fletcher 1988; Brown 1995; see
D. octaedra,
Chapter 12
this volume).
Considerable attention has been given to the fate of the major components of the microbial
community that arrive in earthworm guts as a result of the consumption of soil and plant litter.
Following intake of these materials, they are mixed in the earthworm gizzard, which leads to a
considerable increase in microbial activity. These microorganisms are exposed, in all parts of the
earthworm gut, to conditions different from those in noningested soil (i.e., significantly higher
water contents and pH conditions). Moreover, in the earthworm foregut, there is a high content of
soluble organic matter derived from the input of intestinal mucus, which declines greatly in the
mid- and hindgut (Trigo and Lavelle 1993, 1995). This mucus production, to various degrees,
occurs in a wide range of earthworm species (Trigo et al. 1999).
In all parts of the earthworm gut, there are much higher respiration rates than in uningested
soil (Trigo and Lavelle 1993, 1995). However, there is no evidence of corresponding increases in
microbial biomass (Scheu 1992; Daniel and Anderson 1992; Tiunov and Scheu 2000a.). This might
indicate a decrease in the metabolic efficiency of the microbial community in the earthworm gut.
These observations lead to a concept of a mutualistic digestion of organic matter in earthworm
guts (i.e., the existing gut microbial community, which is frequently dormant because of lack of
easily assimilable carbon resources) is activated by secreted intestinal mucus under the suitable gut
temperature and moisture conditions, and the decomposition of organic matter in the gut contents
is enhanced to the mutual benefit of both the microorganisms and the earthworm. This so-called
paradox was documented and reviewed comprehensively by Brown et al. (2000).
With respect to the fate of bacteria, particularly fungi, during transit through the earthworm
gut, there has been considerable debate that usually stems from differences in the methods used
for studying these organisms. Cultural studies, although very useful in some specific cases, have
given way to other approaches (e.g., quantitative estimates of total bacterial and fungal commu-
nities). These approaches include direct observations of microorganisms by methods such as
epifluorescence microscopy (e.g., Scheu and Parkinson 1994a; Kristufek et al. 1995), image
analysis with epifluorescence microscopy (Schholzer et al. 1999), and transmission electron
microscopy (Kristufek et al. 1994) and the use of whole cell hybridization (Fischer et al. 1995).
Bacterial populations in the earthworm crop or gizzard are usually higher than in the surrounding
soil. During transit through the earthworm gut, these numbers have been reported to increase greatly
(e.g., Parle 1963; Edwards and Bohlen 1996), and usually numbers in earthworm casts are sub-
stantially greater than those in the surrounding soil (Edwards and Fletcher 1988). These increases
in bacterial populations may be caused not only by microbial growth, but also by bacterial spore
germination (Fischer et al. 1995). Wolter and Scheu (1999) showed a somewhat different pattern
of bacterial populations using
cultured in field samples of beech forest soil. Here, there
were increases in numbers of bacteria from the crop to the gizzard to the foregut, then no significant
changes to the hindgut. As stated, there is evidence for change in total microbial biomass during
transit through the earthworm gut. As well as increases in bacterial populations, there have been
reports of increases in bacterial cell size in the earthworm gut (Fischer et al. 1997; Wolter and
Scheu 1999). These increases parallel the increases in gut water content mentioned in this section.
It appears that many groups of bacteria and actinomycetes can pass unharmed through the earth-
worm gut (e.g., Gram-negative organisms, spore formers, and actinomycetes during gut transit)
(Edwards and Fletcher 1988). However, mortality of some species (e.g.,
L. terrestris
Bacillus cereus
var.
mycoides, Serratia marcescens, Escherichia coli
) has been recorded (Lee 1985).
A high percentage of earthworm gut bacteria are ultimately dispersed in earthworm casts,
and few are dispersed while adhering to the earthworm body surfaces. This dispersal is of
