Annals of the Entomological Society of America

Published by: Entomological Society of America



Annals of the Entomological Society of America 97(6):1242-1251. 2004
doi: 10.1603/0013-8746(2004)097[1242:PCFFCA]2.0.CO;2

Protist Communities from Four Castes and Three Species of Reticulitermes (Isoptera: Rhinotermitidae)

J. L. Lewis and B. T. Forschler

Department of Entomology, University of Georgia, 413 Biological Sciences Building, Athens, GA 30602

Abstract

Previous studies indicate subterranean termite protist communities are qualitatively similar within termite species but differ in relative species abundance between castes. We investigated protist communities from four castes of Reticulitermes flavipes (Kollar), Reticulitermes virginicus (Banks), and Reticulitermes hageni Banks. We used a standardized counting technique and found termite workers and early stage nymphs had the largest population of protists, followed by soldiers and alates. R. flavipes workers averaged 59,000 flagellates compared with 21,000 in R. hageni and 14,000 in R. virginicus. We recorded two new genera, Microjoenia Grassi and Monocercomonas Grassi, from R. virginicus. We identified eight protist species from R. hageni, whereas only four have been previously noted. This is the first report of Dinenympha fimbriata Kirby, Holomastigotes elongatum Grassi, Monocercomonas Grassi, Pyrsonympha minor Powell, Spirotrichonympha flagellata (Grassi), and Trichonympha agilis Leidy from R. hageni. Across all termite species, we found that workers, nymphs, and soldiers had similar relative protist species abundances, with alates being different. The results also demonstrated the utility of using the relative abundance of indicator protist species to identify these three subterranean termite species. The presence of Dinenympha gracilis can be used to distinguish R. flavipes from R. virginicus and R. hageni. R. virginicus has a greater abundance of T. agilis, compared with the other two termite species. The relative abundance of D. fimbriata and Pyrsonympha from R. hageni is greater than those found in both R. flavipes and R. virginicus.

Received: January 30, 2004; Accepted: July 21, 2004



References

Azuma, J., K. Kanai, K. Okamura, K. Nishimoto, and M. Takahashi. Studies on digestive system of termites III. Digestibility of xylan by termite Reticulitermes speratus (Kolbe). Wood Res 1993. 79:4151.
Boykin, M. S., L. Stockert, H. E. Jr, Buhse, and H. E. Smith-Somerville. Trichomitus trypanoides (Trichomonadida) from the termite Reticulitermes flavipes II. Fine structure and identification of the cloned flagellate. Trans. Am. Microsc. Soc 1986. 105:223238. CrossRef
Brown, V. E. On the morphology of Spirotrichonympha with a description of two new species from Reticulitermes hageni Banks. Archiv. für. Protistenkunde 1930. 70:517530.
Brown, V. E. Hypermastigote flagellates from the termite Reticulitermes: Torquenympha octoplus gen. nov., sp. nov., and two new species of Microjoenia. Univ. of Cal. Publ. Zool 1930. 36:6780.
Brown, G. V. E. The morphology of Spironympha, with a description of a new species from Reticulitermes hesperus Banks. J. Morph. Physiol 1931. 51:291307.
Buchli, H. R. L ‘Òrigine des castes et les potentialities ontogéniques des termites Européens du genre Reticulitermes Holmgren. Ann. des Sc. Nat. Zool 1958. 11:263429.
Cleveland, L. R. The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol. Bull 1924. 46:178227. CrossRef
Cleveland, L. R. The feeding habit of termite castes and its relation to their intestinal flagellates. Biol. Bull 1925. 48:295306.
Cleveland, L. R. The effects of oxygenation and starvation on the symbiosis between the termite, Termopsis, and its intestinal flagellates. Biol. Bull 1925. 48:309326. CrossRef
Cleveland, L. R. Toxicity of oxygen for protozoa in vivo and vitro Animals defaunated without injury. Biol. Bull 1925. 48:455468.
Cleveland, L. R. Further investigations and experiments on the symbiosis between termites and their intestinal protozoa. Biol. Bull 1928. 54:231237.
Collins, M. S. Taxonomic problems with termites of North America, Canada through Panama. Sociobiol 1988. 14:207210.
Cook, T. J. Community structure and assemblage interaction among the symbiotic flagellates of subterranean termites in the genus Reticulitermes (Holmgren). Ph.D. dissertation. 1996. Texas A&M University College Station, TX.
Cook, T. C. and R. E. Gold. Organization of the symbiotic flagellate community in three castes of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 1998. 31:2539. CSA
Cook, T. C. and R. E. Gold. Symbiotic hindgut flagellate communities of the subterranean termites Reticulitermes virginicus and Reticulitermes flavipes in Texas (Isoptera: Rhinotermitidiae). Sociobiology 1999. 34:533543.
Cook, T. C. and R. E. Gold. Effects of different cellulose sources on the structure of the hindgut flagellate community in Reticulitermes virginicus (Isoptera: Rhinotermitidae). Sociobiology 2000. 35:119130.
Dropkin, V. H. The ecology of the termite gut. Ph.D. dissertation. 1944. University of Chicago Chicago, IL.
Dubosq, O. and P. P. Grassé. Notes sur les protistes parasites des termites de France. I. Trichomonas trypanoïdes n. sp. Comptes Rendus des Sciences de la Société de Biologie et de ses Filiales 1924. 90:547550.
Dubosq, O. and P. P. Grassé. Notes sur les protistes parasites des termites de France. V. Les Spirotrichonympha et leur evolution. Archive de Zoologie Experiméntale et Générale. Note et. Rev 1928. 67:159178.
Forschler, B. T. and M. L. Townsend. Mortality of eastern subterranean termites (Isoptera: Rhinotermitidae) exposed to four soils treated with termiticides. J. Econ. Entomol 1996. 89:678681. CSA
Grassé, P. P. and C. Noirot. La transmission des flagelles symbiotiques et les aliments des termites. Bull. Biol. Fr. Belg 1945. 79:273292.
Grassi, B. Dei protozoi parassiti e specialmente di quelli che sono nell ‘uomo. Gazz. Med. Ital. Lombard 1879. 39:445448.
Grassi, B. Conclusioni d’una memoria sulla societa dei Termitid. Rend. R. Accad. Lincei 1892. 1:3336.
Grassi, B. Flagellati viventi nei Termiti. Mem. R. Acad. Lincei 1917. 12:331394.
Grassi, B. and Sandias. Constituzione e sviluppo della società dei Termitidi. Appendice I. Protozoa parasiti dei termitidi. Atti. Acad. Gioenia. Sci. Nat. Catania 1893. 7:4559.
Grosovsky, B. D. and L. Margulis. Termite microbial communities. R. G. Burns J. H. Slater Experimental microbial ecology 1982. 519-532. Blackwell Scientific Oxford, United Kingdom.
Haverty, M. I., B. T. Forschler, and L. J. Nelson. An assessment of the taxonomy of Reticulitermes (Isoptera: Rhinotermitidae) from the Southeastern United States based on cuticular hydrocarbons. Sociobiology 1996. 28:287318. CSA
Honigberg, B. M. Evolutionary and systematic relationships in the flagellate order Trichomonadida Kirby. J. Protozool 1963. 10:2063. PubMed
Honigberg, B. M. Protozoa associated with termites and their role in digestion. K. Krishna F. M. Weesner Biology of termites vol. II 1970. 1-36. Academic New York.
Hostettler, N. C., D. W. Hall, and R. H. Scheffrahn. Intracolony morphometric variation and labral shape in Florida Reticulitermes (Isoptera: Rhinotermitidae) soldiers significance for identification. Fla. Entomol 1995. 78:119129. CrossRef, CSA
Howard, R. W. Effects of methoprene on laboratory colonies of Reticulitermes flavipes (Kollar) (ISOPTERA: Rhinotermitidae). J. Ga. Entomol. Soc 1984. 19:290298.
Howard, R. and M. I. Haverty. Reproductives in mature colonies of Reticulitermes flavipes (Kollar) abundance, sex-ratio, and association with soldiers. Environ. Entomol 1980. 9:459460.
Howard, R. and M. I. Haverty. Seasonal variation in caste proportions of field colonies of Reticulitermes flavipes (Kollar). Environ. Entomol 1981. 10:546549. CSA
Hungate, R. E. Quantitative analysis on the cellulose fermentation by termite protozoa. Ann. Entomol. Soc. Am 1943. 36:730739.
Kirby, H. Morphology and mitosis of Dinenympha fimbriata sp. nov. Univ. Calif. Publ. Zool 1924. 26:199220.
Kirby, H. Host-parasite relations in the distribution of protozoa in termites. Univ. Calif. Publ. Zool 1937. 41:189212.
Koidzumi, M. Studies on the trichonymphids parasitic in the termites of Japan I (in Japanese). Annual Report of the Institute of Science, Government of Formosa 1916. 5:5583.
Koidzumi, M. Studies on the Trichonymphids parasitic in the termites of Japan II (in Japanese). Annual Report of the Institute of Science, Government of Formosa 1917. 6:93175.
Koidzumi, M. Studies on the intestinal protozoa found in the termites in Japan. Parasitology 1921. 13:235309.
Kudo, R. R. Protozoology. 5th ed.. 1997. Charles C Thomas Publisher Springfield, IL.
La Fage, J. P. and W. L. Nutting. Nutrient dynamics of termites. M. V. Brian Production ecology of ants and termites 1978. 165-232. Cambridge University Press Cambridge United Kingdom.
Lai, P. Y., M. Tamashiro, and J. K. Fuji. Abundance and distribution of the three species of symbiotic protozoa in the hindgut of Coptotermes formosanus (Isoptera: Rhinotermitidae). Proc. Haw. Entomol. Soc 1983. 24:271276. CSA
Leidy, J. On intestinal parasites of Termes flavipes. Proc. Acad. Nat. Sci. Phila 1877. 29:146149.
Leidy, J. Parasites of the termites. J. Acad. Nat. Sci. Phila 1881. 8:425450.
Lewis, J. L. Examination of protist communities in three species of Reticulitermes subterranean termites (Isoptera: Rhinotermitidae). 2003. M.S. thesis. University of Georgia Athens.
Lewis, J. L. and B. T. Forschler. Nitrogen-sparged media extends lifespan of symbiotic protists found in subterranean termites (Isoptera: Rhinotermitidae) providing more time for microscopic examination. Environ. Entomol 2004. 33:11451150. Abstract
Mannesmann, R. Untersuchungen über den einfluβ der temperature aug die darm-symbionten von termiten und über die regulatorischen mechanismen bei der symbiose. Z. Ang. Zool 1969. 56:385440.
Mannesmann, R. Vergleichende untersuchungen über den einfluβ der temperatur auf die darmsymbionten von termiten und über die regulatorischen mechanismen bei der symbiose. Part. II. Z. Ang. Zool 1970. 57:167.
Mannesmann, R. Relationship between different wood species as a termite food source and the reproduction of termite symbionts. Z. Ang. Entomol 1972. 72:116128.
Mannesmann, R. Qualitative und quantitative untersuchung der darmfaunen mehrerer populationen von Reticulitermes (Isop., Rhinotermitidae). Z. Ang. Entomol 1974. 76:8697.
Mauldin, J. K., F. L. Carter, and N. M. Rich. Protozoan populations of Reticulitermes flavipes (Kollar) exposed to heartwood blocks of 21 American species. Material Organismen 1981. 16:1528.
Mauldin, J. K., R. V. Smythe, and C. C. Baxter. Cellulose catabolism and lipid synthesis by the subterranean termite, Coptotermes formosanus. Insect Biochem 1972. 2:209217. CrossRef
McMahan, E. Feeding relationships and radioisotope techniques. K. Krishna Biology of termites vol. I 1969. 387-406. Academic New York.
Noirot, C. and C. Noirot-Timothee. The digestive system. K. Krishna Biology of termites vol. I 1969. 49-88. Academic New York.
Polizzi, J. M. and B. T. Forschler. Intra- and Interspecific agonism in Reticulitermes flavipes (Kollar) and R. virginicus (Banks) and effects of arena and group size in laboratory assays. Insectes Soc 1998. 45:4349. CrossRef, CSA
Powell, W. N. On the morphology of Pyrsonympha with a description of three new species from Reticulitermes hesperus Banks. Univ. Calif. Publ. Zool 1928. 31:179200.
Scheffrahn, R. H. and N-Y. Su. Keys to soldier and winged adult termites (Isoptera) of Florida. Fla. Entomol 1994. 77:460474. CrossRef, CSA
Smythe, R. V. Feeding and survival at constant tempteratures by normally and abnormally faunated Reticulitermes virginicus. Ann. Entomol. Soc. Am 1972. 65:756757.
Smythe, R. V. and J. K. Mauldin. Soldier differentiation, survival, and wood consumption by normally and abnormally faunated workers of the Formosan termite, Coptotermes formosanus. Ann. Entomol. Soc. Am 1972. 65:10011004.
StatSoft, Inc Statistica for Windows (Computer program manual). 2001. StatSoft, Inc. Tulsa, OK.
Steel, R. G. D. and J. H. Torrie. Principles and procedures of statistics. 1960. McGraw Hill New York.
To, L. P., L. Margulis, D. Chase, and W. L. Nutting. The symbiotic microbial community of the Sonoran desert termite Pterotermes occidentis. BioSystems 1980. 13:109137.
Trager, W. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol. Bull 1934. 66:182190. CrossRef
Yamin, M. A. Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi & Foà reported from lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology 1979. 4:3119.
Yoshimura, T., J. Azuma, K. Tsunoda, and M. Takahashi. Changes of wood-attacking of the lower termite, Coptotermes formosanus Shiraki in defaunation-refaunation process of the intestinal protozoa. Material und Organismen 1993. 28:153164.
Yoshimura, T., J. Azuma, K. Tsunoda, and M. Takahashi. Cellulose metabolism of the symbiotic protozoa in termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) III. Mokuzai Gakkaishi 1993. 39:13221326.
Yoshimura, T., T. Fujino, T. Itoh, K. Tsunoda, and M. Takahashi. Ingestion and decomposition of wood and cellulose by the protozoa in the hindgut of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) as evidenced by polarizing and transmission electron microscopy. Holzforschung 1996. 50:99104.

Fig. 1. (a–k) Light microscopy of protist species from R. flavipes. (a) P. vertens. (b) P. major. (c) S. flagellata. (d) T. agilis. (e) T. trypanoides. (f) S. kofoidi. (g) D. fimbriata. (h) D. gracilis. (i) Monocercomonas sp. (j) H. elongatum. (k) M. fallax. Scale bar, 10 μm (photographs taken using a Leica microscope at 400× magnification, and images acquired using an AxioCam digital camera)

Fig. 2. (a–h) Light microscopy of protist species from R. virginicus. (a) H. elongatum. (b) P. minor. (c) D. fimbriata. (d) S. flagellata. (e) T. agilis. (f) Microjoenia sp. (g) S. kofoidi. (h) Monocercomonas sp. Scale bar, 10 μm (photographs taken using a Leica microscope at 400× magnification, and images acquired using an AxioCam digital camera)

Fig. 3. (a–h) Light microscopy of protist species from R. hageni. (a) P. minor. (b) T. agilis. (c) S. kofoidi. (d) H. elongatum. (e) D. fimbriata. (f) Monocercomonas sp. (g) Spirotrichonympha flagellata (h) M. pyriformis. Scale bar, 10 μm (photographs taken using a Leica microscope at 400× magnification, and images acquired using an AxioCam digital camera)

Fig. 4. Mean (±SD) total protist population from four castes of R. flavipes, R. virginicus, and R. hageni. Means followed by the same letter do not differ significantly from each other within termite species at P < 0.05; Duncan’s multiple range test

table

Table 1. Termite species, collection locale, date (in 2003), and number of replicates per sample for comparison of protists by termite caste

table

Table 2. Protist species from R. flavipes, R. virginicus, and R. hageni reported in the literature and those found in the present study

table

Table 3. Relative species abundance (±SD) by protist species between castes of R. flavipes

table

Table 4. Relative species abundance (±SD) by protist species between castes of R. virginicus

table

Table 5. Relative species abundance (±SD) by protist species between castes of R. hageni

table

Table 6. Relative protist species relative abundance (±SD) from the worker caste in three species of Reticulitermes

Cited by

C.J. Peterson, P.D. Gerard, T.L. Wagner. (2007) Charring does not affect wood infestation by subterranean termites. Entomologia Experimentalis et Applicata 0:0, 071120225250003-???
Online publication date: 20-Dec-2007.
CrossRef
click this button to close

Article Views

click this button to open

Citing Articles

 
BioOne is the product of innovative collaboration between scientific societies, libraries, academe and the private sector.
 
21 Dupont Circle NW, Suite 800, Washington, DC 20036 • Phone 202.296.2296 • Fax 202.872.0884
 
Copyright © 2009 BioOne All rights reserved