Biol Fertil Soils (1998) 26:155–156
© Springer-Verlag 1998
S H O RT C O M M U N IC AT I O N
M. Zimmer · W. Topp
Do woodlice (Isopoda: Oniscidea) produce endogenous cellulases?
Received: 4 April 1997
Abstract In studies on digestive processes and microorganisms in the gut of the common woodlouse, Porcellio scaber (Isopoda: Oniscidea), we observed marked contradictions between the activity of cellulolytic enzymes and the number of microorganisms. The anterior hindgut exhibited the highest cellulolytic activity, but was characterized by low microbial counts. Due to the presence of endosymbiotic bacteria in the midgut lobes that appear to produce cellulases, we suggest that the cellulases that are active in the hindgut of woodlice are of endogenous origin. Key words Terrestrial isopods · Gut microflora · Endosymbiotic bacteria · Cellulase · Cellulose digestion · Decomposition
Introduction Woodlice (Isopoda: Oniscidea) are involved in the decomposition of leaf litter (e.g. Cameron and LaPoint 1978) that mainly consists of cellulose and other “digestibility reducing” macromolecules (e.g. Szegi 1988). It has generally been assumed that woodlice do not possess endogenous cellulases, but utilize microbial enzymes that they ingest with food (e.g. Hassall and Jennings 1975; Kozlovskaja and Striganova 1977; Kukor and Martin 1986). Although many terrestrial arthropods lack endogenous cellulases (reviewed in Martin 1983), recent studies suggest that some litter- and wood-feeding invertebrates may possess endogenous cellulolytic enzymes (e.g. Slaytor 1992; Treves and Martin 1994).
M. Zimmer · W. Topp Department of Zoology – Physiological Ecology, University of Cologne, Weyertal 119, D-50931 Cologne, Germany, Fax: (221) 470-5038; e-mail:
[email protected]
Materials and methods In order to examine the distribution of cellulase activity in the gut of the common woodlouse, Porcellio scaber, we removed the hindgut and the midgut lobes from the body of adult isopods (cf. Zimmer 1997) to determine their biochemical and microbiological characteristics. The activity of cellulolytic enzymes was measured according to the method described by Zimmer and Topp (1997) using crystalline a-cellulose as substrate. Microbial cells were counted after staining with acridine orange (Francisco et al. 1973), and the number of colony-forming bacteria and fungi was determined as in Treves and Martin (1994). We estimated the percent of cellulolytic microorganisms from the number of microbial colonies (Teather and Wood 1982).
Results and discussion Uesbeck and Topp (1995) recently described decreased consumption rates and digestibility in Oniscus asellus after it had foraged on sterilized leaf litter. Zimmer and Topp (1997) observed that the reproduction of Porcellio scaber decreased after it fed on litter with little microbial activity. In the present study on the cellulase activity and number of microbes in the gut of P. scaber, we did not observe any correlation between cellulolytic activity and the number of ingested bacteria or fungi (Table 1). Hassall and Jennings (1975) observed that cellulolytic activity was greatest in the anterior hindgut of P. scaber. They concluded that the breakdown of cellulose in the food by microbial enzymes mainly takes place in this part of the gut. These findings are in agreement with our results (Table 1), as cellulase activity in the anterior hindgut was found to be 10–50 times higher than that of the litter. The posterior hindgut exhibited significantly less cellulolytic activity than the anterior hindgut, although this was still 2–15 times greater than that observed in litter. In contrast to the study of Hassall and Jennings (1975), we also observed cellulase activity in the midgut lobes, which exceeded that of the litter 3–30 fold. This result is in agreement with those of Hartenstein (1964) and Hames and Hopkin (1989). The numbers of microbes in the different sections of the gut of P. scaber were inversely proportional to the cel-
156 Table 1 Cellulase activity and counts of microorganisms in the hindgut of Porcellio scaber compared to leaf litter. Data are given as the range of the percentage values obtained from the anterior and posterior hindgut (n = 9) with respect to the mean values of litter ( = 100%) on which the isopods fed (n = 9)
Cellulase activity Total microbial counts a Cellulolytic microorganisms Platable actinomycetes Platable bacteria Platable fungi
Anterior hindgut
Posterior hindgut
1000–5000 60–130 70–110 10–75 1–10 10–35
200–1500 70–150 90–150 50–200 80–110 20–75
a
Including platable actinomycetes, bacteria and fungi, and non-platable microorganisms
lulase activity (Table 1). The anterior hindgut exhibited the highest cellulase activity but was characterized by a low microbial count. Compared to the other sections of the gut, the anterior hindgut contained the lowest number of microorganisms (Table 1). A similar number of cellulolytic microorganisms was observed in the hindgut and in the litter (Table 1). Our results were comparable to those of Wood and Griffiths (1988), as we found no platable microorganisms in the midgut lobes, but did observe high numbers of obligate endosymbiotic bacteria. The number of these microorganisms significantly exceeded the total microbial count of the litter. The cellulolytic activity observed in the midgut lobes may be due to the presence of these non-platable microorganisms. Furthermore, the inverse relationship between cellulase activity and microbial counts in the hindgut of P. scaber can be explained by the hypothesis that the endosymbiotic bacteria of the midgut lobes produce extracellular cellulases. This hypothesis contrasts with the external rumen hypothesis described by Hassall and Rushton (1985) which proposed that faecal pellets of terrestrial isopods act as an “external rumen” by supporting enhanced microbial activity (Hassall and Rushton 1985). If our hypothesis on the origin of cellulases in woodlice were correct, then the importance of faeces as a source of microbial cellulases would be reduced. In conclusion, our results strongly suggest that the cellulase that is active in the gut of P. scaber mainly originates from the endosymbiotic bacteria of the midgut lobes, or is even produced by the animal itself (Hartenstein 1964). Further research on this topic is in progress.
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