Activity-density and spatial distribution of termites on a fine-scale in a tropical rainforest in Xishuangbanna, southwest China
Myo Thant, Xiaobing Lin, Anjana J. Atapattu, Min Cao, Shang-wen Xia, Shengjie Liu, Xiaodong Yang
Activity-density and spatial distribution of termites on a fine-scale in a tropical rainforest in Xishuangbanna, southwest China
● Strong associations among soil-wood feeders and fungus growers were observed.
● Weak associations between litter feeders and other feeders were observed.
● TPI and pH had effects on all feeding groups of termites.
● Plant biomass influenced soil-wood feeders and wood feeders.
● Litter mass influenced fungus growers, litter feeders, and soil feeders.
The community composition and activity-density of termites can influence nutrient cycling and other ecological functions. However, the spatial distribution and the activity-density of termites on a fine-scale in tropical forests are still unknown. We checked the spatial distribution patterns of the feeding groups and species of termites and their co-occurrence pattern in a 1-ha (100 m × 100 m) plot, and their correlation with the environmental factors. We used a standard protocol to collect termite assemblages and classified them into five feeding groups based on their preferred diet: fungus growers, litter feeders, soil feeders, soil-wood feeders, and wood feeders. We measured the environmental factors: soil pH, litter mass, aboveground plant biomass, and topographic position index (TPI). Soil-wood feeders showed the highest activity-density, followed by wood feeders, fungus growers, soil feeders, and litter feeders. Soil-wood feeders and fungus growers demonstated a strong correlation while litter feeders showed weak correlations with other feeding groups. Termite feeding groups and most of the termite species displayed a positive association with the high TPI and the low soil pH patches. Our results indicated that the examined environmental factors influenced the termite community assemblages and distribution patterns on a fine-scale in tropical rainforests.
Competition / Co-occurrence / Feeding groups / Fine-scale / Spatial distribution / Tropical rainforest
[1] |
Abe,T., Higashi,M., 2001. Isoptera. In: Levin, S.A., ed. Encyclopedia of Biodiversity. Elsevier, 408– 433.
|
[2] |
Atapattu,A.J., Xia,S.W., Cao,M., Zhang,W., Mishra,S., Yang,X., 2020. Can dominant canopy species leaf litter determine soil nutrient heterogeneity? A case study in a tropical rainforest in southwest China.. Journal of Soil Science and Plant Nutrition 20, 2479– 2489.
CrossRef
Google scholar
|
[3] |
Avitabile,S.C., Nimmo,D.G., Bennett,A.F., Clarke,M.F., 2015. Termites are resistant to the effects of fire at multiple spatial scales. PLoS One 10, 1– 18.
CrossRef
Google scholar
|
[4] |
Betz,O., Srisuka,W., Puthz,V., 2020. Elevational gradients of species richness, community structure, and niche occupation of tropical rove beetles (Coleoptera: Staphylinidae: Steninae) across mountain slopes in Northern Thailand. Evolutionary Ecology 34, 193– 216.
CrossRef
Google scholar
|
[5] |
Bignell,D.E., 2018. Wood-Feeding Termites. In:, Ulyshen, M.D., ed. Saproxylic Insects, Zoological Monographs 1. Springer, Heidelberg, pp. 339– 373.
|
[6] |
Bignell,D.E., Eggelton,P., 2000. Termites in Ecosystems. In: Abe, T., E.D., Bignell, Higashi, M., eds. Termites: Evolution, Sociality, Symbioses, Ecology. Springer Netherlands, Dordrecht, pp. 363– 387.
|
[7] |
Bourguignon,T., Drouet,T., Šobotník,J., Hanus,R., Roisin,Y., 2015. Influence of soil properties on soldierless termite distribution. PLoS One 10, e0135341.
CrossRef
Google scholar
|
[8] |
Cai,B.H., Huang,F.S., 1980. Termite of China. Sciences Press, Beijing, .
|
[9] |
Cancello,E.M., Silva,R.R., Vasconcellos,A., Reis,Y.T., Oliveira,L.M., 2014. Latitudinal variation in termite species richness and abundance along the Brazilian Atlantic forest hotspot. Biotropica 46, 441– 450.
CrossRef
Google scholar
|
[10] |
Cao,M., Zou,X., Warren,M., Zhu,H., 2006. Tropical forests of Xishuangbanna, China. Biotropica 38, 306– 309.
CrossRef
Google scholar
|
[11] |
Chave,J., Réjou-Méchain,M., Búrquez,A., Chidumayo,E., Colgan,M.S., Delitti,W.B.C., Duque,A., Eid,T., Fearnside,P.M., Goodman,R.C., Henry,M., Martínez-Yrízar,A., Mugasha,W.A., Muller-Landau,H.C., Mencuccini,M., Nelson,B.W., Ngomanda,A., Nogueira,E.M., Ortiz-Malavassi,E., Pélissier,R., Ploton,P., Ryan,C.M., Saldarriaga,J.G., Vieilledent,G., 2014. Improved allometric models to estimate the aboveground biomass of tropical trees. Global Change Biology 20, 3177– 3190.
CrossRef
Google scholar
|
[12] |
Chen,C., Zou,X., Wu,J., Zhu,X., Jiang,X., Zhang,W., Zeng,H., Liu,W., 2020. Accumulation and spatial homogeneity of nutrients within termite ( Odontotermes yunnanensis) mounds in the Xishuangbanna region, SW China . Catena 105057
|
[13] |
Cheng,S., Kirton,L.G., Panandam,J.M., Siraj,S.S., Ng,K.K.S., Tan,S.G., 2011. Evidence for a higher number of species of Odontotermes (isoptera) than currently known from peninsular Malaysia from mitochondrial DNA phylogenies. PLoS One 6, e20992.
CrossRef
Google scholar
|
[14] |
Chiu,C.I., Yeh,H.T., Li,P.L., Kuo,C.Y., Tsai,M.J., Li,H.F., 2018. Foraging phenology of the fungus-growing termite Odontotermes formosanus (Blattodea: Termitidae). Environmental Entomology 47, 1509– 1516.
CrossRef
Google scholar
|
[15] |
Colwell,R.K., Futuyma,D.J., 1971. On the measurement of niche breadth and overlap. Ecology 52, 567– 576.
CrossRef
Google scholar
|
[16] |
Dahlsjö,C.A.L., Parr,C.L., Malhi,Y., Meir,P., Eggleton,P., 2015. Describing termite assemblage structure in a Peruvian lowland tropical rain forest: a comparison of two alternative methods. Insectes Sociaux 62, 141– 150.
CrossRef
Google scholar
|
[17] |
Dahlsjö,C.A.L., Valladares Romero,C.S., Espinosa Iñiguez,C.I., 2020. Termite diversity in Ecuador: A comparison of two primary forest national parks. Journal of Insect Science 20, 4.
CrossRef
Google scholar
|
[18] |
Dambros,C.S., Morais,J.W., Azevedo,R.A., Gotelli,N.J., 2017. Isolation by distance, not rivers, control the distribution of termite species in the Amazonian rain forest. Ecography 40, 1242– 1250.
CrossRef
Google scholar
|
[19] |
Davies,A.B., Eggleton,P., van Rensburg,B.J., Parr,C.L., 2013. Assessing the relative efficiency of termite sampling methods along a rainfall gradient in African Savannas. Biotropica 45, 474– 479.
CrossRef
Google scholar
|
[20] |
De Souza,H.J., Delabie,J.H.C., 2018. Fine-scale spatial distribution of murundus structures in the semi-arid region of Brazil. Austral Ecology 43, 268– 279.
CrossRef
Google scholar
|
[21] |
Donovan,S.E., Eggleton,P., Bignell,D.E., 2001. Gut content analysis and a new feeding group classification of termites. Ecological Entomology 26, 356– 366.
CrossRef
Google scholar
|
[22] |
Donovan,S.E., Griffiths,G.J.K., Homathevi,R., Winder,L., 2007. The spatial pattern of soil-dwelling termites in primary and logged forest in Sabah, Malaysia. Ecological Entomology 32, 1– 10.
CrossRef
Google scholar
|
[23] |
Dosso,K., Konaté,S., Aidara,D., Linsenmair,K.E., 2010. Termite diversity and abundance across fire-induced habitat variability in a tropical moist savanna (lamto, central Côte d’Ivoire). Journal of Tropical Ecology 26, 323– 334.
CrossRef
Google scholar
|
[24] |
Dosso,K., Deligne,J., Yéo,K., Konaté,S., Linsenmair,K.E., 2013. Changes in the termite assemblage across a sequence of land-use systems in the rural area around Lamto Reserve in central Côte d’Ivoire. Journal of Insect Conservation 17, 1047– 1057.
CrossRef
Google scholar
|
[25] |
Dosso,K., Roisin,Y., Tiho,S., Konaté,S., Yéo,K., 2017. Short-term changes in the structure of termite assemblages associated with slash-and-burn agriculture in Côte d’Ivoire. Biotropica 49, 856– 861.
CrossRef
Google scholar
|
[26] |
Eggleton,P., Homathevi,R., Jeeva,D., Jones,D.T., Davies,R.G., Maryati,M., 1997. The species richness and composition of termites (Isoptera) in primary and regenerating lowland dipterocarp forest in Sabah, east Malaysia. Ecotropica (Bonn) 3, 119– 128.
|
[27] |
Eggleton,P., Tayasu,I., 2001. Feeding groups, lifetypes and the global ecology of termites. Ecological Research 16, 941– 960.
CrossRef
Google scholar
|
[28] |
Fajar,A., Himmi,S.K., Latif,A., Tarmadi,D., Kartika,T., Guswenrivo,I., Yusuf,S., Yoshimura,T., 2021. Termite assemblage and damage on tree trunks in fast-growing teak plantations of different age: A case study in West Java, Indonesia. Insects 12, 295.
CrossRef
Google scholar
|
[29] |
Gao,M., Qiao,Z., Hou,H., Jin,G., Wu,D., 2020. Factors that affect the assembly of ground-dwelling beetles at small scales in primary mixed broadleaved-Korean pine forests in north-east China. Soil Ecology Letters 2, 47– 60.
CrossRef
Google scholar
|
[30] |
Gathorne-Hardy,F., Syaukani,Eggleton, P., theGathorne-Hardy, 2001. The effects of altitude and rainfall on the composition of the termites (Isoptera) of the Leuser Ecosystem (Sumatra, Indonesia). Journal of Tropical Ecology 17, 379– 393.
CrossRef
Google scholar
|
[31] |
Grohmann,C., Oldeland,J., Stoyan,D., Linsenmair,K.E., 2010. Multi-scale pattern analysis of a mound-building termite species. Insectes Sociaux 57, 477– 486.
CrossRef
Google scholar
|
[32] |
Harit,A.K., Ramasamy,E.V., Babu,N., Rajasree,M.J., Monsy,P., Bottinelli,N., Cheik,S., Jouquet,P., 2021. Are wood-feeding and fungus-growing termites so different? Comparison of the organization and properties of Microcerotermes pakistanicus and Odontotermes obesus soil constructions in the Western Ghats, India. Insectes Sociaux 68, 207– 216.
CrossRef
Google scholar
|
[33] |
Hemachandra,I.I., Edirisinghe,J.P., Karunaratne,W.A.I.P., Gunatilleke,C.V.S., Fernando,R.H.S.S., 2014. Diversity and distribution of termite assemblages in montane forests in the Knuckles Region, Sri Lanka. International Journal of Tropical Insect Science 34, 41– 52.
CrossRef
Google scholar
|
[34] |
Hesselbarth,M., 2021. shar: An R package to analyze species-habitat associations using point pattern analysis. Journal of Open Source Software 6, 3811.
CrossRef
Google scholar
|
[35] |
Hojo,M., 2019. Distribution pattern of Termitomyces types symbiotic with the fungus-growing termite Odontotermes formosanus on Okinawa Island. Entomological Science 22, 398– 403.
CrossRef
Google scholar
|
[36] |
Hyodo,F., Tayasu,I., Inoue,T., Azuma,J.I., Kudo,T., Abe,T., 2003. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Functional Ecology 17, 186– 193.
CrossRef
Google scholar
|
[37] |
Illian,J., Penttinen,A., Stoyan,H., Stoyan,D., 2007. Statistical analysis and modelling of spatial point patterns, international statistical review. John Wiley & Sons, Ltd, Chichester.
|
[38] |
Jenness,J., 2006. Topographic Position Index (tpi_jen.avx) extension forArcView 3.x, v. 1.2. Jenness Enterprises. Available at: http://www.jennessent.com/arcview/tpi.htm
|
[39] |
Jiménez,J.J., Rossi,J.P., Lavelle,P., 2001. Spatial distribution of earthworms in acid-soil savannas of the eastern plains of Colombia. Applied Soil Ecology 17, 267– 278.
CrossRef
Google scholar
|
[40] |
Jiménez,J.J., Decaëns,T., Amézquita,E., Rao,I., Thomas,R.J., Lavelle,P., 2011. Short-range spatial variability of soil physico-chemical variables related to earthworm clustering in a neotropical gallery forest. Soil Biology & Biochemistry 43, 1071– 1080.
CrossRef
Google scholar
|
[41] |
Jones,D.T., Susilo,F.X., Bignell,D., Hardiwinoto,S., Gillison,A.N., Eggleton,P., 2003. Termite assemblage collapse along a land-use intensification gradient in lowland central Sumatra, Indonesia. Journal of Applied Ecology 40, 380– 391.
CrossRef
Google scholar
|
[42] |
Jouquet,P., Traoré,S., Choosai,C., Hartmann,C., Bignell,D., 2011. Influence of termites on ecosystem functioning. Ecosystem services provided by termites. European Journal of Soil Biology 47, 215– 222.
CrossRef
Google scholar
|
[43] |
Jouquet,P., Guilleux,N., Chintakunta,S., Mendez,M., Subramanian,S., Shanbhag,R.R., 2015. The influence of termites on soil sheeting properties varies depending on the materials on which they feed. European Journal of Soil Biology 69, 74– 78.
CrossRef
Google scholar
|
[44] |
Jouveau,S., Toïgo,M., Giffard,B., Castagneyrol,B., van Halder,I., Vétillard,F., Jactel,H., 2020. Carabid activity-density increases with forest vegetation diversity at different spatial scales. Insect Conservation and Diversity 13, 36– 46.
CrossRef
Google scholar
|
[45] |
Koné,N.A., Silué,K.S., Konaté,S., Linsenmair,K.E., 2018. Determinants of termite assemblages’ characteristics within natural habitats of a Sudano-Guinean savanna (Comoe national park, Côte d’Ivoire). Insects 9, 189.
CrossRef
Google scholar
|
[46] |
Korb,J., Foster,K.R., 2010. Ecological competition favours cooperation in termite societies. Ecology Letters 13, 754– 760.
CrossRef
Google scholar
|
[47] |
Li,J., Sang,M., Jiang,Y., Wei,J., Shen,Y., Huang,Q., Li,Y., Ni,J., 2021. Polyene-producing Streptomyces spp. from the fungus-growing termite Macrotermes barneyi exhibit high inhibitory activity against the antagonistic fungus Xylaria. Frontiers in Microbiology 12, 1– 15.
CrossRef
Google scholar
|
[48] |
Liu,S., Lin,X., Behm,J.E., Yuan,H., Stiblik,P., Šobotník,J., Gan,J., Xia,S.-W., Yang,X., 2019. Comparative responses of termite functional and taxonomic diversity to land-use change. Ecol. Entomol. 0– 9.
|
[49] |
Long,Y.H., Xie,L., Liu,N., Yan,X., Li,M.H., Fan,M.Z., Wang,Q., 2010. Comparison of gut-associated and nest-associated microbial communities of a fungus-growing termite (Odontotermes yunnanensis). Insect Science 17, 265– 276.
CrossRef
Google scholar
|
[50] |
Martins,R.F., Andrades,R., Nagaoka,S.M., Martins,A.S., Longo,L.L., Ferreira,J.S., Bastos,K.V., Joyeux,J.C., Santos,R.G., 2020. Niche partitioning between sea turtles in waters of a protected tropical island. Regional Studies in Marine Science 39, 101439.
CrossRef
Google scholar
|
[51] |
Mills,A.J., Milewski,A., Fey,M.V., Groengroeft,A., Petersen,A., 2009. Fungus culturing, nutrient mining and geophagy: A geochemical investigation of Macrotermes and Trinervitermes mounds in southern Africa . Journal of Zoology (London, England) 278, 24– 35
|
[52] |
Mills,A.J., Sirami,C., 2018. Nutrient enrichment of ecosystems by fungus-growing versus non-fungus-growing termites. Journal of Tropical Ecology 34, 385– 389.
CrossRef
Google scholar
|
[53] |
Miura,T., Matsumoto,T., 1997. Diet and nest material of the processional termite Hospitalitermes, and cohabitation of Termes (Isoptera, Termitidae) on Borneo Island. Insectes Sociaux 44, 267– 275.
CrossRef
Google scholar
|
[54] |
Mujinya,B.B., Adam,M., Mees,F., Bogaert,J., Vranken,I., Erens,H., Baert,G., Ngongo,M., Van Ranst,E., 2014. Spatial patterns and morphology of termite (Macrotermes falciger) mounds in the Upper Katanga, D. R. Congo. Catena 114, 97– 106.
CrossRef
Google scholar
|
[55] |
Niittynen,P., Heikkinen,R.K., Aalto,J., Guisan,A., Kemppinen,J., Luoto,M., 2020. Fine-scale tundra vegetation patterns are strongly related to winter thermal conditions. Nature Climate Change 10, 1143– 1148.
CrossRef
Google scholar
|
[56] |
Nunes,C.A., Quintino,A.V., Constantino,R., Negreiros,D., Reis Júnior,R., Fernandes,G.W., 2017. Patterns of taxonomic and functional diversity of termites along a tropical elevational gradient. Biotropica 49, 186– 194.
CrossRef
Google scholar
|
[57] |
Osborne,B.B., Soper,F.M., Nasto,M.K., Bru,D., Hwang,S., Machmuller,M.B., Lopez,M., Philippot,L., Sullivan,B.W., Asner,G.P., Cleveland,C.C., Townsend,A.R., Porder,S., 2021. Litter inputs drive patterns of soil nitrogen heterogeneity in a diverse tropical forest: Results from a litter manipulation experiment. Soil Biology & Biochemistry 158, 108247.
CrossRef
Google scholar
|
[58] |
Palin,O.F., Eggleton,P., Malhi,Y., Girardin,C.A.J., Rozas-Dávila,A., Parr,C.L., 2011. Termite diversity along an Amazon-Andes Elevation Gradient, Peru. Biotropica 43, 100– 107.
CrossRef
Google scholar
|
[59] |
Pebesma,E.J., 2004. Multivariable geostatistics in S: the gstat package. Computers & Geosciences 30, 683– 691.
CrossRef
Google scholar
|
[60] |
Perner,J., Schueler,S., 2004. Estimating the density of ground-dwelling arthropods with pitfall traps using a nested-cross array. Journal of Animal Ecology 73, 469– 477.
CrossRef
Google scholar
|
[61] |
Pratiknyo,H., Ahmed,I., Budiyanto,B.H., 2018. Diversity and abundance of termites along altitudinal gradient and slopes in Mount Slamet, Central Java, Indonesia. Biodiversitas (Surakarta) 19, 1649– 1658.
CrossRef
Google scholar
|
[62] |
Pratiknyo,H., Setyowati,E.A., theENDANG ARIYANI SETYOWATI, 2020. Short communication: The diversity of termites along the altitudinal gradient in a Karst Area of Southern Gombong, Central Java, Indonesia. Biodiversitas (Surakarta) 21, 1730– 1734.
CrossRef
Google scholar
|
[63] |
RCore Team, 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
|
[64] |
Scholtz,O., Knight,M.E., Eggleton,P., 2021. Spatial structure of rainforest termites: Two matched pioneering cross-continental case studies. Biotropica 53, 1178– 1190.
CrossRef
Google scholar
|
[65] |
Schyra,J., Gbenyedji,J.N.B.K., Korb,J., 2019. A comparison of termite assemblages from West African savannah and forest ecosystems using morphological and molecular markers. PLoS One 14, 1– 20.
CrossRef
Google scholar
|
[66] |
Shanbhag,R.R., Kabbaj,M., Sundararaj,R., Jouquet,P., 2017. Rainfall and soil properties influence termite mound abundance and height: A case study with Odontotermes obesus (Macrotermitinae) mounds in the Indian Western Ghats forests. Applied Soil Ecology 111, 33– 38.
CrossRef
Google scholar
|
[67] |
Slaytor, 2000. Energy metabolism in the termite and its gut microbiota. In: Termites: Evolution, Sociality, Symbioses, Ecology. Springer Netherlands, Dordrecht, pp. 307– 332.
|
[68] |
Šobotník,J., Dahlsjö,C.A.L., 2017. Isoptera. In: Reference Module in Life Sciences. Elsevier.
|
[69] |
SoilSurvey Staff, 2014. Keys to Soil Taxonomy. United States Department of Agriculture (USDA), Natural Resources Conservation Service, Washington, DC
|
[70] |
St. Clair,A.L., Dolezal,A.G., O’Neal,M.E., Toth,A.L., 2020. Pan traps for tracking honey bee activity-density: A case study in soybeans. Insects 11, 366.
CrossRef
Google scholar
|
[71] |
Sugimoto,A., Bignell,D.E., MacDonald,J.A., 2000. Global Impact of Termites on the Carbon Cycle and Atmospheric Trace Gases. In: Abe, T., E.D., Bignell, Higashi, M., eds. Termites: Evolution, Sociality, Symbioses, Ecology. Springer Netherlands, Dordrecht, 409–435.
|
[72] |
Syaukani,S., Thompson,G.J., Zettel,H., Pribadi,T., 2016. A new species of open-air processional column termite, Hospitalitermes nigriantennalis sp. n. (Termitidae), from Borneo . ZooKeys 554, 27– 36
|
[73] |
Thiele,H.-U., 1977. Carabid Beetles in Their Environments. Springer Heidelberg.
CrossRef
Google scholar
|
[74] |
Valckx,J., Cockx,L., Wauters,J., Van Meirvenne,M., Govers,G., Hermy,M., Muys,B., 2009. Within-field spatial distribution of earthworm populations related to species interactions and soil apparent electrical conductivity. Applied Soil Ecology 41, 315– 328.
CrossRef
Google scholar
|
[75] |
Vasconcellos,A., 2010. Biomass and abundance of termites in three remnant areas of Atlantic Forest in northeastern Brazil. Revista Brasileira de Entomologia 54, 455– 461.
CrossRef
Google scholar
|
[76] |
Vesala,R., Niskanen,T., Liimatainen,K., Boga,H., Pellikka,P., Rikkinen,J., 2017. Diversity of fungus-growing termites (Macrotermes) and their fungal symbionts (Termitomyces) in the semiarid Tsavo Ecosystem, Kenya. Biotropica 49, 402– 412.
CrossRef
Google scholar
|
[77] |
Wiegand,T., Moloney,K.A., 2013. Handbook of Spatial Point-Pattern Analysis in Ecology. Chapman and Hall/CRC.
|
[78] |
Wiens,J.A., 1989. Spatial Scaling in Ecology. Functional Ecology 3, 385.
CrossRef
Google scholar
|
[79] |
Xia,S.W., Chen,J., Schaefer,D., Detto,M., 2015. Scale-dependent soil macronutrient heterogeneity reveals effects of litterfall in a tropical rainforest. Plant and Soil 391, 51– 61.
CrossRef
Google scholar
|
[80] |
Yang,X., Chen,J., 2009. Plant litter quality influences the contribution of soil fauna to litter decomposition in humid tropical forests, southwestern China. Soil Biology & Biochemistry 41, 910– 918.
CrossRef
Google scholar
|
[81] |
Zaret,T.M., Rand,A.S., 1971. Competition in tropical stream fishes: Support for the competitive exclusion principle. Ecology 52, 336– 342.
CrossRef
Google scholar
|
[82] |
Zhang,J., Ma,K., 2013. spaa: An R package for computing species association and niche overlap. In: Chinese National Committee for Diversity, ed. Advances in Biodiversity Conservation and Research in China. China Meteorological Press, Beijing
|
[83] |
Zhang,L., Meng,L., Guo,C., Gao,M., Liu,D., Zhang,X., 2015. Spatial heterogeneity of soil mite community and its spatial relationship with environmental factors in Maoer Mountains. International Journal of Smart Home 9, 141– 148.
CrossRef
Google scholar
|
/
〈 | 〉 |