Printer Friendly

Food digestion by subterranean termites from the southeastern United States (Isoptera: Rhinotermitidae).

INTRODUCTION

The majority of termite species in the United States are economically important, with the eastern subterranean termite (Reticulitermes flavipes Kollar) and the Formosan subterranean termite (Coptotermes formosanus Shiraki) particularly serious threats to wooden structures (Su and Scheffrahn, 1990). Other subterranean termites (family Rhinotermitidae) found in the southeastern U.S. are Reticulitermes virginicus Banks, R. hageni Banks, and a species that received formal recognition recently, R. malletei Clement.

Termites are designated as either lower or higher termites based on differences in the digestive system. Specifically, lower termites harbor flagellate protozoa in the digestive tract that digest wood cellulose and hemicelluloses, while higher termites do not. The core food of lower termites is dead wood, with a preference for partially rotted wood (Noirot and Noirot-Timothee, 1969). Most termite species in the United States are lower termites.

Wood contains very little nitrogen. Lower termites obtain dietary nitrogen from nitrogen-fixing bacteria that inhabit the hindgut, as well as from uric acid digested by other bacteria harbored there (Breznak and Brune, 1994). Cannibalized termites are a source of uric acid for these bacteria, as well as stores mobilized from fat body (Breznak, 2000). Dietary nitrogen may also be present from other foods besides wood. Chitin, ingested by termites from cannibalism as well as from fungi in decayed wood, would provide the insect with dietary nitrogen if digestible (Waller and LaFage, 1987). Protein is contained in termite feces (Nation, 2002; Arquette et al., 2012) and may provide dietary nitrogen, as termites are coprophagous.

As the most abundant wood carbohydrate, cellulose is the main food of lower termites. It is a straight-chain polysaccharide made up of glucose molecules covalently bonded by beta linkages. Hydrogen bonding occurs between parallel cellulose molecules, resulting in a crystalline structure (O'Sullivan, 1997). This structure makes cellulose indigestible for most organisms. Efficient degradation of crystalline cellulose to glucose requires a combination of three enzymes. These are endoglucanases, exoglucanases, and beta glucosidases (Nation, 2002). Bacteria, protozoa, and fungi are among the few organisms that produce each of these enzymes. Termites synthesize endocellulase and beta glucosidase, but not exocellulase. Endocellulase produced by lower termites may increase the efficiency of wood digestion by protozoan symbionts harbored in the hindgut (Nakashima et al., 2002), and may even degrade some cellulose without exocellulase (Slaytor, 2000). Wood polysaccharides other than cellulose are collectively termed hemicelluloses, mainly xylan or mannan, and also require multiple enzymes for digestion.

Wood particles take about 24 hours to pass through lower termite gut (Breznak, 1982), most of that time being digested in food vacuoles of hindgut flagellate protozoa. These flagellates digest most wood cellulose eaten by termites (Trager, 1932; Hungate, 1938), and digest wood hemicelluloses as well (Yoshimura, 1995; Smith et al., 2007), but not much lignin (Yoshimura, 1995). If the flagellates are eliminated from the digestive tract, the insect soon starves. Bacteria, archaea, and yeasts are other microorganisms harbored in termite gut, some of which digest cellulose (Li et al., 2006).

Overall cellulase activity is measurable with a cellulosic substrate such as filter paper (Urbanszki et al., 2000). Individual enzyme activities can also be measured using substrates including carboxymethyl cellulose for endocellulase, and cellobiose for beta glucosidase. The dinitrosalicylic (DNSA) reducing sugar assay is commonly used for determination of sugars released from cellulase as well as hemicellulase activity assays.

While many protozoa are free-living, the flagellate protozoan symbionts of lower termites are only found in the digestive tract of their host. Types of flagellates vary between termites. For instance, Coptotermes fomosanus harbor three flagellate species. The largest, Pseudotrichonympha grassi, is found more at the forward region of hindgut. These engulf and digest cellulose and other wood polysaccharides, and expel undigested lignin via exocytosis (Yoshimura, 1995). Hodomastigitoides hartmanni is about evenly distributed through the hindgut (Lai et al., 1983). Dietary requirements for H. hartmanni appear to be different than for P. grassi, which cannot survive a diet of low molecular weight cellulose. Spirotrichonympha Liedyi is diminutive in size, and tends to occur in highest numbers toward the rectum. Rather than engulf wood particles, this species has been hypothesized to obtain dissolved nutrients from hindgut fluid (Yoshimura, 1995).

Past studies described changes in wood structure upon passage through lower termite gut from light microscopy as well as scanning and transmission electron microscopy (Yoshimura, 1995; Yamaoka and Nagatani, 1977). These studies reported changing shape of wood passing through the gut, the size and type of food engulfed and digested from protozoa, and the time taken for gut transit. Wood particles ingested by Formosan termites are less than 100 um in length (Yoshimura, 1995; Itakura et al., 1995). Smaller wood particles have more surface area (Watanabe and Tokuda, 2001) and are increasingly porous during digestion, giving additional areas upon which digestive enzymes can act (Matsumura et al., 1977).

Animals must quickly excrete excess nitrogen from breakdown of protein and purines. For insects, nitrogenous wastes are primarily ammonia or uric acid (Cochran, 1985; Chapman, 1998). Ammonia is usually the major nitrogenous waste produced by insects that live in aquatic or very moist environments. For insects that live in dry habitats, need to conserve body weight for flight, or have a dry diet, uric acid is typically the main nitrogenous waste (Chapman, 1998; Cochran, 1985). Types of nitrogenous wastes in insect feces have been determined for various orders. Blattaria is the best studied, with varying proportions of uric acid and ammonia identified for many cockroach species (Cochran, 1985). Uric acid also accumulates in cockroach as well as termite fat body, a process termed storage excretion (Chapman, 1998). Many cockroaches harbor uricolytic bacteria in their fat body that digest uric acid from adjacent storage sites (Cochran, 1985). Termites also store uric acid in fat body, but only one species, Mastotermes darwiniensis, harbors uricolytic bacteria there. For other termites, uric acid stored in fat body can only be digested if it is mobilized to the hindgut for digestion by uricolytic bacteria in the gut fluid (Potrikus and Breznak, 1980a and 1980b). Such uricolytic bacteria, identified so far only from Reticulitermes flavipes hindgut, likely digest most uric acid that reaches them (Potrikus and Breznak, 1980a and 1980b). Laboratory populations of R. flavipes can store uric acid in fat body in very high quantity (Potrikus and Breznak, 1980a and 1980b; Arquette et al., 2006), and would provide a substantial source of dietary nitrogen if mobilized to the hindgut for digestion. However, there is disagreement as to whether uric acid stores in fat body are mobilized or remain there permanently as a product of storage excretion (Breznak, 2000; Slaytor and Chappell, 1994; Slaytor, 2000).

Cellulose and chitin are the most abundant biopolymers in nature (Merzendorfer and Zimoch, 2003). Both are straight chain polysaccharides, with glucose subunits comprising cellulose and N-acetylglucosamine for chitin, linked together by beta 1, 4-glycosidic bonds. A main difference between cellulose and chitin is that cellulose contains no nitrogen, whereas chitin is about 7 percent nitrogen, which could be utilized in the termite's metabolism if digested (Waller and LaFage, 1987). Like cellulase and hemicellulase, multiple enzymes work together for chitin digestion. Chitinase is produced by insects at the time of molting, and is also found in the digestive tract of some insects. Examples include chitinase activity measured from labial glands of Acromyrmex octospinosus (Febvay et al., 1984) and from larvae and adults of a microphagous beetle species (Fukamizo et al., 1985). Chitinase has been determined to be present in the digestive tract of a few termites (Noirot and Noirot-Timothee, 1969; Mishra and San Sarma, 1981), but not others (Mishra and San Sarma, 1981).

The efficiency of food digestion by insects has been reported in numerous studies, for example by grasshoppers (Phillippe, 1991). Digestive efficiency of insects can be determined from comparing the amount of food eaten with that remaining undigested in feces. For termites, efficiency of lignocellulose digestion has been reported for C. formosanus and other species (Itakura et al. 1995; Hyodo et al. 1999; Mishra and Sen-Sarma 1979; Katsumata et al. 2007). Digestion of wood components for Formosan termites was reported based on assay of fecal material recovered from pine blocks and surfaces of laboratory arenas (Itakura et al. 1995; Hyodo et al. 1999). However, another study demonstrated Formosan termites held in similar conditions chew pieces from wood blocks without eating them, with accumulated wood particles impossible to separate from feces (Arquette, 2011).

LITERATURE CITED

Arquette, T.J. 2011. Study of food digestion and morphology of subterranean termites from Mississippi. Doctoral dissertation, Mississippi State University.

Arquette, T.J., Mallette, E.M., and Rodriguez, J.M. 2012. Uric Acid and Soluble Protein Content of Feces from Three Species of Subterranean Termites. Florida Entomologist 95: 218-220.

Arquette, T.J., Champagne, D.E., Brown, M.R., and Forschler, B.T. 2006. Evaluation of novel and traditional measures for vigor of laboratory-cultured termites, Reticulitermes flavipes (Kollar). Journal of Insect Physiology 52: 51-66.

Breznak, J.A. 1982. Intestinal Microbiota of Termites and other Xylophagous Insects.Annual Review of Microbiology 36: 323-323.

Breznak, J.A. 2000. Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. In: Termites: Evolution, Sociality, Symbioses, Ecology. Abe, T., D.E. Bignell, and M. Higashi [eds.]. Kluwer Academic Publishers, Boston.

Breznak, J.A., and Brune, A., 1994. Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology 39: 453-487.

Chapman, R.F. 1998. The Insects: Structure and Function, 4th ed. Cambridge University Press, Cambridge.

Cochran, D.G. 1985. Nitrogen excretion in cockroaches. Annual Review of Entomology 30: 29-49.

Febvay, G., Decharme, M., and Kermarrec, A. 1984. Digestion of chitin by the labial glands of Acromyrmex octospinosus Reich (Hymenoptera: Formicidae). Canadian Journal of Zoology 62: 229-234.

Fukamizo, T., Speirs, R., and Kramer K. 1985. Comparative biochemistry of mycophagous and non-mycophagous grain beetles: chitinolytic activities of foreign and sawtoothed grain beetles. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 81: 207-209.

Hungate, R.E., 1938. Studies on the nutrition of Zootermopsis. II. The relative importance of the termite and the protozoa in wood digestion. Ecology 19: 1-25.

Hyodo, F., Azuma, J.-I., and Abe, T. 1999. Estimation of effect of passage through the gut of a lower termite, Coptotermes formosanus Shiraki, on lignin by Solid-State CP/MAS 13 C NMR. Holzforschung 53: 244-246.

Itakura, S., Ueshima, K., Tanaka, H., and Enoki, A. 1995. Degradation of wood components by subterranean termite, Coptotermes formosanus Shiraki. Mokuzai Gakkaishi 41: 580-586.

Katsumata K.S., Jin, Z., Hori, K., and Iiyama, K. 2007. Structural changes in lignin of tropical woods during digestion by the termite, Cryptotermes brevis. Journal of Wood Science 53: 419-426.

Li, L., Frohlich, J., and Konig, H. 2006. Cellulose digestion in the termite gut. In: Intestinal Microorganisms of Termites and Other Invertebrates [H. Konig and A. Varma, eds.]. Berlin: Springer, 2006.

Lai, P.Y., Tamashiro, M., and Fujii, J.K., 1983. Abundance and distribution of the three species of symbiotic protozoa in the hindgut of C. formosanus. Proceedings of the Hawaiian Entomological Society 24: 271-276.

Merzendorfer, H., and Zimoch, L. 2003. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. Journal of Experimental Biology 206: 4393-4712.

Mishra, S.C., and Sen-Sarma, P.K. 1979. Studies on determioration of wood by insects III. Chemical composition of faecal matter, nest material and fungus comb of some Indian termites. Material und Organismen 14: 1-14.

Mishra, S.C., and Sen-Sarma, P.K. 1981. Chitinase activity in the digestive tract of termites (Isoptera). Material und Organismen 16: 157160.

Nakashima, K., Watanabe, H., Saitoh, H., Tokuda, G., and Azuma, J-I. 2002. Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochemistry and Molecular Biology 32: 777-784.

Nation, J. 2002. Insect Physiology and Biochemistry. CRC Press. Washington, DC.

Noirot, C., and Noirot-Timothee, C. 1969. The digestive system. In: Biology of Termites, vol. 1. Krishna, K., and F.M. Weesner [eds.] Academic Press. NY.

O'Sullivan, A.C. 1997. Cellulose: the structure slowly unravels. Cellulose 4: 173-207.

Philippe, L. 1991. Niche breadth and feeding in tropical grasshoppers. Insect Science and its Application 12: 201-208.

Potrikus, C.J., and Breznak, J.A. 1980a. Anaerobic degradation of uric acid by gut bacteria of termites. Applied and Environmental Microbiology 40: 125-132.

Potrikus, C.J., and Breznak, J.A. 1980b. Uric acid-degrading bacteria in guts of termites [Reticulitermes flavipes (Kollar)]. Applied and Environmental Microbiology 40: 117-124.

Slaytor, M. 2000. Energy metabolism in the termite and its gut microbiota. In: Termites:

Evolution, Sociality, Symbioses, Ecology. Abe, T., D.E. Bignell, and M. Higashi [eds.] Kluwer Academic Publishers. Boston.

Slaytor, M., and Chappell, D.J. 1994. Nitrogen metabolism in termites. Comparative Biochemistry and Physiology 107B: 1-10.

Smith, J.A., and Koehler, P.G. 2007. Changes in Reticulitermes flavipes (Isoptera: Rhinotermitidae) gut xylanolytic activities in response to dietary xylan content. Annals of the Entomological Society of America 100: 568-573.

Su, N.Y., and Scheffrahn, R. 1990. Economically important termites in the United States and their control. Sociobiology 17: 77-94.

Trager, W. 1932. A cellulase from the symbiotic intestinal flagellates of termites and of the roach Cryptocercus punctulatus. Biochemical Journal 26: 1763-1771.

Urbanszki K., Szakacs, G., and Tengerdy, R.P. 2000. Standardization of the filter paper activity assay for solid substrate fermentation. Biotechnology Letters 22: 65-69.

Waller, D.A. and LaFage, J.P. 1987. Nutritional ecology of termites. In: Nutritional Ecology Of Insects, Mites, and Spiders, and Related Invertebrates. Slansky, F. and J.G. Rodriguez [eds.] John Wiley and Sons. NY.

Watanabe, H. and Tokuda, G. 2001. Animal cellulases. Cellular and Molecular Life Sciences 58: 1167-1178.

Yamaoka, I., and Nagatani, Y. 1977. Cellulose digestion system in termite, Reticulitermes speratus (Kolbe). II. Ultrastructural changes related to the ingestion and digestion of cellulose by flagellate, Trichonympha agilis. Zoological Magazine 86: 34-42.

Yoshimura, T. 1995. Contribution of the protozoan fauna to nutritional physiology of the lower termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Wood Research 82: 68-129.

Tim J. Arquette (1,2)

(1) Mississippi State University South Branch Experiment Station, Poplarville, MS

(2) Mississippi State University Departments of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State, MS

Corresponding Author: Tim Arquette tia68@msstate.edu
COPYRIGHT 2013 Mississippi Academy of Sciences
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2013 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Arquette, Tim J.
Publication:Journal of the Mississippi Academy of Sciences
Article Type:Report
Geographic Code:1USA
Date:Apr 1, 2013
Words:2332
Previous Article:Building a trusted healthcare informatics platform: implementation of the enterprise data warehouse at the University of Mississippi Medical Center.
Next Article:Wood degradation in the digestive tract of the formosan subterranean termite (Isoptera: Rhinotermitidae).
Topics:

Terms of use | Privacy policy | Copyright © 2020 Farlex, Inc. | Feedback | For webmasters