Lavelle, P.

Trigo, D.

Horizon / Pleins textes

Acta Zool. Fennìca 196:129-131 ISBN 951-9481-41-9 ISSN O00 1-7299 
Helsinki 28 February 1995 
XI International Colloquium on Soil Zoology, Jyväskylä, Finland, 10-14 August, 1992 
O Finnish Zoological and Botanical Publishing Board 1995 
Soil changes during gut transit through Octohsion hcteum Oerley 
(Lumbricidae, Oligochaeta) 
D. Trigo & P. Lavelle 
- 
Trigo, D., Departainentu de Biologia Aniinal I, Facultad de Ciericia~ Biol&icas, Universidad 
Coniphrtmse de Madrid, 28040 Madrid, Spain. 
Luvelle, P., Lnhomioire d’ Ecologie des Sols Tropicaux? ORSTO11.I/UI~iversite‘ P. et M. Curie, 72 ruirte 
d’Airhiay, 93143 Bondy Cedex, Frmce 
Physico-chemical and hiological measurements were camed out on gut contents and casts of Octulasion 
lacreimn, an earthworm species frequently foun temperate regions of Northem Spain. The content of 
water, water-soluble organic matter and bH w ïÎcreased inihe anteripr part of the gut. The water- 
soluble compounds decreased in the medium and pos’terior parts of the gut and were almost absent in 
casts. The mean oxygen consumption in the gut content increased about two‘to three times suggesting a 
microbial activation in the gut. These results support the hyprjthesis of a mutualistic dige\tion system 
also in temperate endogeic earthworms. 
. 
1. Introduction 
Earthworm activities cause iniportant modifications in 
physico-chemical and biological properties of soils, in par- 
ticular in the drilosphere, affecting cartwn cycling, microbial 
activity, nutrient release, soil aggregation and dynamics of 
organic matter, (Bhatnagar 1975, Lee I985 Martin 1991 and 
Martin et al. 1991). 
Measurements of several physico-chemical and biologi- 
cal paraneters in the gut content of two endogeic mesohumic 
tropical earthworm species, Millsonia ~inoniala and 
Porrios~~~lcr cowtliriinrs (Barois & Lavelle 1986, Barois 
19871, indicate thc existence of a mutualjstic relationship 
between microflora and earthworms for the exploitation of 
soil organic matter. Similar obsenations carried out on the 
tropical oligohurnic earthworm, Dicliogaster ierrm-nigrae, 
which feeds on deeper soil horizons, and two epigeic tropical 
species Ainyithos coi~icis and A i n y r t h  grmilis, (Barois & 
Lavelle 1956) suggest that mutualistic digestion generally 
occurs in tropical earthworms of different ecological catego- 
ries @lartin 1988. Barois 1992). We (Trigo Lavelle 1993), 
studied the same processes in a scmiaquatic temperate 
earthworm, Allolobciplzora Inolleri concluding that a 
mutualistic digestion system is also present in this species. 
We also hypothesized that digestion is largely perfomled by 
the microflora of the ingested soil; the addition of high 
amounts of water and water-soluble organic matter in the 
anterior part of the gut results in a dramatic increase in 
microbial activity, and t i d i e r  digestion of organic matter by 
these activated nlicroorganisms. This process is analogous to 
the ”priming effect” (Jenkinson 1966). 
In this study we seek evidence of a similar mutualistic 
digestion system in an endogeic earthworm species living in 
temperate regions, by measuring some physico-chemical and 
biological parameters (water content, pH. microbial respira- 
tion and water-soluble organic matter) in noningested soil, in 
different parh ofthe gut and in fresh casts. 
2. Material and methods 
Specimens of O. lacteiirn and soil from the 0-1 5 cm layer 
were collected from an irrigated meadow at Rubio-Boyueixón 
(La Coruña, Spain) 29TNGS8. The soil had a content 
of sand, silt and clay of 38.40 and 22%. respectively. The 
pH was 5.8, and the soil organic matter content was 9%. 
After sampling, the earthworms were kept in plastic boxes. 
fed with soil in which they had been collected, and sieved 
with a 2 mm screen; the culture temperature was maintained 
between 17 and 21T .  
Samples of gut content were obtained after killing the 
earthworms by immersion in boiling water for one secont. 
OWSTOM Fomds Documentalre 
m 
_- 
3. Keslllts 
'"1 Water-soluble organic 
matter (%) 
I 
d''l Water content in..i 
- 
5iC ANT MID PUS CAST 
-L---r--r-l--- 
Oxygeii consumption 
O 4'h) 
Fig 1 Physico-chemical parameters measured in soil (SOL), 
casts (CAST) and gut contents (ANT, hllD, POS) of 
Ocfolasrclri hcfeim 
4. Discussion 
Table 1. Analysis of variarice of water-soluble organic matter, pH, water content, and oxygen consumption in soil (S),  
anterior gut (A), rriidqut (M).  posterior gut (P), and casts (C). * P c  0.05, It P.C 0.01; ns  not significant. 
.- - 
Water-soluble OM PH Water content O2 consumption 
A M P C  A M P C  A M P C  A M P C  
- -  
** t t  t l  11 t l  I .  * ns n5 ns ns 
* *  *(I * *  ns **  * *  
" +  t l  *. .. s 
A 
M 
P ris 
1-15 n s  
ns  
f l  ns  ns  '* 
11s " t. t f  +. * *  11s ris 
f t  * *  
ACTA ZOOL. FENNTCA Vol. 196 Trigo & Lavelle: Soil changes in gut of Octolasion 13 1 
accessibility of organic matter to soil microorganisms (Barois 
& Lavelle 1956). The intestinal mucus may not only func- 
tion as an easily assimilable source of energy for microor- 
ganisms, it may also be a source of lytic enzymes, e.g. 
chitinases. cellulases and amylases (Loquet & Vinceslas 
1987, Laverack 1963) as proposed by Martin et al. (1987). 
After being hydrolyzed, part of this mucus may be reabsorbed 
by the worms simultaneously with the compounds produced 
by the degradation of soil organic matter. A rapid assessment 
of the amounts of energy required to produce the large 
quantities of mucus shows that part of it is necessarily 
reabsorbed and recycled within the earthworm. 
The increase in soil pH during gut transit may be related 
to mucus production and to the activity of the Morren glands 
that secrete carbonates (Prentcí 1979). 
Results of the present study indicate that the digestion 
processes in the gut of O. lacterm are similar to those de- 
scribed for the tropical species M. unoiiurlu and P. coreflirurics 
(Barois 1987, Barois & Lavelle 19861, D. ferrue-nigrue 
(Martin 1988) and Amylyntlius corficis and A. grucilis (Barois 
1992). Furthermore. this process is the same as that de- 
scribed for,4. molleri (Trigo & Lavelle 1993), a semiaquatic 
oligochaete living in temperate climates. The soil ingested 
by the worm is enriched with large amounts of mucus and 
water in the anterior gut, while pH is neutralized. These 
processes result in an activation of microflora, which further 
digest soil organic matter in the middle and posterior parts of 
the gut. The earthworm may absorb assimilable organic 
matter released by digestion of the activated soil microflora. 
This hypothesis is supported by the fact that the amount of 
assimilable carbon is at a maximum in the anterior part of the 
gut, whereas the peak of microbial respiration was found in 
the medium and posterior parts. 
The secretion of water-soluble organic components was 
considerably higher in the temperate species studied than in 
tropical ones. This may be due to lower soil temperatures in 
teniperate zones, limiting the microbial activity, and thus a 
higher production of mucus is necessary to activate it, whereas 
in the tropical species, the higher temperatures allow a lower 
mucus production. 
Regarding to the water content of the gut, the temperate 
worm A. molleri (Trigo & Lavelle 1993) shows a progres- 
sive increase along the gut, whereas O. lucreirni tends to 
maintain it, with a slight decrease in casts. On the other hand, 
tropical species show a reduction of water content along the . gut. Casts of P. coretlwirriw, a tropical earthworm from hu- 
mid pastures, still retain 85% of the water contained in the 
anterior gut, and only lS% is reabsorbed. For M. urzomulu, a 
species living in humid savannas and subject to seasonal 
water stress, the water content of casts is only 50% of that 
measured in the anterior part of the gut. It seems clear that 
the changes during the gut transit are related to environmen- 
tal conditions. In species under dry conditions, water reten- 
tion processes are dominant, whereas in moist to wet envi- 
ronments water elimination processes predominate. 
As a conclusion. the obtained results for O. lacfercm 
agree with the existence of a mutualistic digestion system, as 
proposed by Barois & Lavelle (1986). 
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