Comparison of Symbiotic Flagellate Faunae Between Termites and a Wood-Feeding Cockroach of the Genus Cryptocercus
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Microbes Environ. Vol. 19, No. 3, 215–220, 2004 http://wwwsoc.nii.ac.jp/jsme2/ Comparison of Symbiotic Flagellate Faunae between Termites and a Wood-Feeding Cockroach of the Genus Cryptocercus OSAMU KITADE1* 1 Natural History Laboratory, Faculty of Science, Ibaraki University, Mito, Ibaraki 310–8512, Japan (Received May 22, 2004—Acccepetd July 1, 2004) Termites of most isopteran families and wood-feeding cockroaches of the genus Cryptocercus usually harbor more than one symbiotic flagellate species in their hindgut. To evaluate the similarity of their symbiont faunae, data on symbiont composition at a generic level were examined by cluster analysis and type III quantification method. In both analyses, the symbiont composition recorded from host insects belonging to the same families or monophyletic family groups tended to be similar. This tendency was particularly remarkable in the clade Kalo- termitidae and the clade Rhinotermitidae plus Serritermitidae. Two basal host groups, the Cryptocercidae and the Mastotermitidae, exhibited very different symbiont compositions. These findings suggested that the symbiont faunae mainly reflect the host’s phylogenetic relationships. Within the Rhinotermitid hosts, the genus Reticuliter- mes showed a unique symbiont fauna although it is not a basal taxon in the Rhinotermitidae. Horizontal transfers of symbiotic protists might explain such anomalistic fauna. Key words: cluster analysis, community, cospeciation, Oxymonadea, Parabasalea, protist, type III quantification method Termites (Isoptera) are the most ecologically important era Rhinotermes, Parrhinotermes, Termitogeton16) to 26 in wood-feeding animals because of their huge biomass in the the wood-feeding cockroach Cryptocercus28). The composi- tropics and their large contribution to carbon cycling in ter- tion of symbiont species is usually a host species, which restrial ecosystems. Lower termites, representing six of the may be relevant to the mode of symbiont transmission. That seven families in the Isoptera, have a symbiotic protist com- is, the symbionts are transmitted between host individuals in munity in their hindgut9,10). These symbionts belong to basal a colony by way of proctodeal trophallaxis, and consequent- eukaryotic taxa, flagellate orders of the phylum Axostylata: ly a newly founded host colony should succeed the Trichomonadida, Hypermastigida (class Parabasalea) and symbiont faunae of the mother nests of its king and queen. Oxymonadida (class Oxymonadea)7). Recently, Lo et al.18) Because the host-symbiont relationship is obligatorily suggested that the cockroach order Blattodea is not mono- mutualistic, the protist faunae should reflect the phylogenet- phyletic, but a cockroach genus, Cryptocercus (Cryptocer- ic relationships of the hosts. Some authors have discussed cidae), is a sister group of the termite order Isoptera. Spe- infection patterns of particular symbiont taxa in connection cies of Cryptocercus are all wood-feeding and possess with phylogenetic relationships of host termites9,14,15). protist symbionts of the same orders as those of termites4). However, these arguments were not convincing due to the Cellulases produced by the symbionts are essential for limited amount of available data. In this study, I present the the host termites to digest wood-fibers10) and the symbionts results of a composition of symbiotic protist fauna between are dependent on their hosts for food supply and anaerobic most termite genera and the wood feeding cockroach genus habitats. The number of symbiont species in a host’s hind- Cryptocercus. gut varies among host taxa, such as from one in termite gen- Materials and Methods * Corresponding author; E-mail: [email protected], Tel: 81–29–228–8375, Fax: 81–29–228–8404 The data on the symbiont composition were taken mainly 216 KITADE Table 1. Number of symbiotic flagellate genera found in each host genus Host taxa No. symbiont genera No. host species examined* T** H** O** Total Order BLATTODEA Family Cryptocercidae Genus 1. Cryptocercus 4 (9) 0 11 6 17 Order ISOPTERA Family Mastotermitidae Genus 2. Mastotermes 1 (1) 2 2 0 4 Family Kalotermitidae Genus 3. Cryptotermes 15 (45) 14 0 3 17 4. Epicalotermes 5 (6) 2 1 0 3 5. Bifiditermes 7 (13) 4 1 1 6 6. Proneotermes 1 (2) 2 1 1 4 7. Allotermes 3 (3) 3 1 0 4 8. Marginitermes 1 (2) 2 1 1 4 9. Incisitermes 15 (27) 12 2 1 15 10. Pterotermes 1 (1) 1 1 1 3 11. Postelectrotermes 11 (15) 5 4 2 11 12. Neotermes 26 (109) 14 4 1 19 13. Rugitermes 5 (13) 5 1 1 7 14. Kalotermes 10 (18) 6 2 3 11 15. Paraneotermes 1 (1) 5 4 1 10 16. Gryptotermes 29 (120) 9 1 3 13 17. Calcaritermes 6 (13) 6 0 2 8 Family Hodotermitidae Genus 18. Anacanthotermes 7 (10) 6 7 1 14 19. Microhodotermes 2 (3) 2 2 1 4 20. Hodotermes 1 (2) 2 3 0 5 Family Termopsidae Genus 21. Archotermopsis 1 (1) 3 4 1 8 22. Hodotermopsis 1 (1) 2 8 2 12 23. Zootermopsis 3 (3) 3 1 1 5 24. Porotermes 3 (3) 3 4 1 8 25. Stolotermes 7 (7) 2 5 0 7 Family Rhinotermitidae Genus 26. Psammotermes 2 (7) 0 4 0 4 27. Reticulitermes 22 (75) 4 6 2 12 28. Heterotermes 10 (38) 3 5 0 8 29. Coptotermes 14 (71) 3 3 0 6 30. Prorhinotermes 3 (18) 0 4 0 4 31. Termitogeton 1 (3) 0 1 0 1 32. Schedorhinotermes 5 (32) 3 5 0 8 33. Rhinotermes 3 (4) 0 1 0 1 34. Dolichorhinotermes 1 (5) 1 1 0 2 35. Parrhinotermes 4 (9) 0 1 0 1 Family Serritermitidae Genus 36. Glossotermes 1 (1) 1 2 0 3 37. Serritermes 1 (1) 1 2 0 3 *: Number of known host species (data from Kambhampati and Eggleton13)) in each genus is also shown in brackets. **: T, Order Trichomo- nadida; H, Order Hypermastigida; O, Order Oxymonadida. Flagellate Faunae of Termites 217 from Yamin28), but also from taxonomic/ecological 1,16,20,21,22) papers . Symbiont data for the following host spe- Results cies were obtained by direct observation: Hodotermopsis Cluster Analysis based on the similarities of symbiont sjoestedti, Porotermes planiceps (Termopsidae); Micro- composition hodotermes viator (Hodotermitidae); Glyptotermes satsum- ensis, G. fuscus, G. nakajimai (Kalotermitidae); Serriter- The analysis using r as similarity (Figure 1) divided host mes serrifer, Glossotermes oculatus (Serritermitidae); genera into six clusters (I–VI) at a distance level of 0.1, and Rhinotermes marginalis, R. hispidus, Dolichorhinotermes the genera in clusters IV and V each into subclusters (IVa, sp. (Rhinotermitidae); and Cryptocercus kyebangensis IVb, Va, Vb) at a similarity level of 0.2. The result general- (Cryptocercidae). I followed Kambhampati and Eggleton13) ly coincided with the current classification of the host gen- for the classification of host insects except for the familial era at the family level. Fourteen out of the 15 genera in the assignment of the Glossotermes to the Serritermitidae2). The Kalotermitidae and four of the five genera in the Termop- family Termitidae lack symbiotic protists, and were not in- sidae formed exclusive clusters (III and V, respectively). cluded in the analyses. As the species level taxonomy of Nine out of the ten genera in the Rhinotermitidae also both hosts and symbiotic protists is still poorly conducted, formed an exclusive cluster, VI, together with two genera in the data were combined at the generic level for both hosts and symbionts. Host genera for which less than three sym- biont species have been recorded were not included in the data set, except for four Rhinotermitid genera for which I directly examined more than one colony. For the protist tax- onomy I followed Yamin28), but treated Spirotrichonympha, Spironympha, Pyrsonympha and Dinenympha as indepen- dent genera as in Grassé6) (Table 1). Cluster analyses of the host genera using the unweighted pair group method using arithmetic averages (UPGMA)23) were made based on similarities either in the symbiont com- position or in geographic distribution. For the symbiont composition, I calculated two similarity indices based on the presence/absence (1/0) data of each symbiont genus: the correlation coefficient (r) and Jaccard’s coefficient11). To quantify the similarity in biogeographical affiliation, I calculated the correlation coefficient between the host gen- era based on a matrix representing the presence/absence (1/ 0) data of each host genus in each biogeographical region. For the system of biogeographical regions, I followed Kam- bhampati and Eggleton13) in which the world was divided into the following nine regions: Nearctic, West Palearctic, East Palearctic, Neotropical, Afrotropical, Malagasy, Oriental, Papuan, and Australian regions. Calculation of the similarity indices and clustering was conducted with the STATISTICA (StatSoft Inc., Tulsa, OK) and the R 4.0d63) program packages. Type III quantification method8) was also used to analyze the similarity patterns of the symbiont composition using the “Let’sStat! Pro” package (provided by M. Kitamura). Fig. 1. Results of UPGMA clustering of host genera based on the The presence/absence data of symbiont genera were treated similarity of symbiont composition using the correlation coeffi- as “category (1/0) data” and directly subjected to an analy- cient (r) as a similarity index. Symbols and numerals (see Table 1) indicate host families and genera, respectively. Capital letters sis without assigning dummy variables to “absence”. (A–E) indicate the result of grouping of host genera based on the similarity of biogeographical affiliation (see Figure 3). 218 KITADE Fig. 2. Results of UPGMA clustering of host genera based on the Fig. 3. Results of UPGMA clustering of host genera based on the similarity of symbiont composition using the Jaccard’s coeffi- similarity of biogeographical distribution using the correlation cient as a similarity index. Symbols and numerals (see Table 1) coefficient (r) as a similarity index. Symbols and numerals (see indicate host families and genera, respectively. Capital letters (A– Table 1) indicate host families and genera, respectively.