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Synchronization of alate emergence among colonies and dispersal strategy in the Ryukyu dry-wood termite Neotermes sugioi (Isoptera: Kalotermitidae)

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Abstract

The synchronized dispersal of colonies is an important strategy among social insects in terms of both successful mating and the avoidance of inbreeding. Although several studies have focused on these processes in the most common termite species characterized by pulsed dispersal, only a few studies have reported on termite species characterized by continuous dispersal. Here, we describe the phenology and biological characters of the dispersal flight of Neotermes sugioi, a dry-wood termite native to the Ryukyus Islands of Japan, using five colonies isolated under semi-field conditions over a period of 183 days. We obtained evidence for the synchronicity of alate emergence among colonies of N. sugioi based on observations of synchronous patterns on the major flight and non-flight days, which showed positive correlations in alate emergence between all colony pairs. However, due to the occurrence of months with small correlation coefficients, and inconsistent alate emergence peaks among colonies on a single day, N. sugioi showed less synchronization than subterranean termites characterized by pulsed dispersal flights. Environmental conditions of temperatures and humidities greater than 22 °C and 70% were found to be necessary for high flight activity during both high and low flight seasons. In all colonies, the sex ratio of emerging alates during the observation period was significantly biased toward males. Given that adjustment of synchronous and asynchronous alate release among neighboring colonies could reduce the risk of sibling pair mating and inbreeding, the characteristic alate emergence in N. sugioi may indirectly minimize the potential for inbreeding.

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References

  • Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 125–148

    Google Scholar 

  • Aguilera-Olivares D, Flores-Prado L, Véliz D, Niemeyer HM (2015) Mechanisms of inbreeding avoidance in the one-piece drywood termite Neotermes chilensis. Insectes Soc 62:237–245

    Article  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  CAS  PubMed  Google Scholar 

  • Cheng WJ, Zheng XL, Wang P, Zhou LL, Si SY, Wang XP (2016) Male-biased capture in light traps in Spodoptera exigua (Lepidoptera: Noctuidae): results from the studies of reproductive activities. J Insect Behav 29:368–378

    Article  Google Scholar 

  • Chouvenc T, Scheffrahn RH, Mullins AJ, Su NY (2017) Flight phenology of two Coptotermes species (Isoptera: Rhinotermitidae) in southeastern Florida. J Econ Entomol 110:1693–1704

    Article  PubMed  Google Scholar 

  • Connétable S, Robert A, Bordereau C (2012) Dispersal flight and colony development in the fungus-growing termites Pseudacanthotermes spiniger and P. militaris. Insectes Soc 59:269–277

    Article  Google Scholar 

  • Costa-Leonardo AM, Barsotti RC (1998) Swarming and incipient colonies of Coptotermes havilandi (Isoptera, Rhinotermitidae). Sociobiology 31:131–142

    Google Scholar 

  • Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270

    Article  PubMed  Google Scholar 

  • Henderson G, Delaplane KS (1994) Formosan subterranean termite swarming behavior and alate sex-ratio (Isoptera: Rhinotermitidae). Insect Soc 41:19–28

    Article  Google Scholar 

  • Huang ZY, Qian X, Zhong JH, Xia CG, Hu J (2007) Progress of biological studies on primary reproductives in Cryptotermes domesticus (Isopterra: Kalotermitidae). Sociobiology 50:599–605

    Google Scholar 

  • Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140

    Article  CAS  PubMed  Google Scholar 

  • Ioannou CC, Tosh CR, Neville L, Krause J (2008) The confusion effect—from neural networks to reduced predation risk. Behav Ecol 19:126–130. https://doi.org/10.1093/beheco/arm109

    Article  Google Scholar 

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Sys 2:465–492

    Article  Google Scholar 

  • Japan Meteorological Agency (2019) https://www.jma.go.jp/jma/index.html. Accessed 4 Nov 2019

  • Jones SC, La Fage JP, Howard RW (1988) Isopteran sex ratios: phylogenetic trends. Sociobiology 14:89–118

    Google Scholar 

  • Katoh H, Matsumoto T, Miura T (2007) Alate differentiation and compound-eye development in the dry-wood termite Neotermes koshunensis (Isoptera, Kalotermitidae). Insect Sociaux 54:11–19

    Article  Google Scholar 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447

    Article  Google Scholar 

  • Korb J, Lenz M (2004) Reproductive decision-making in the termite, Cryptotermes secundus (Kalotermitidae), under variable food conditions. Behav Ecol 15:390–395

    Article  Google Scholar 

  • Kusaka A, Matsuura K (2017) Allee effect in termite colony formation: influence of alate density and flight timing on pairing success and survivorship. Insectes Soc 65(1):17–24

    Article  Google Scholar 

  • Lepage M, Darlington JPEC (2000) Population dynamics of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 333–361

    Chapter  Google Scholar 

  • Maki K, Abe T (1986) Proportion of soldiers in the colonies of a dry wood termite, Neotermes koshunensis (Kalotermitidae, Isoptera). Physiol Ecol Jpn 23:109–117

    Google Scholar 

  • Milinski M (1984) A predator's costs of overcoming the confusion-effect of swarming prey. Anim Behav 32:1157–1162

    Article  Google Scholar 

  • Miller RC (1922) The significance of the gregarious habit. Ecology 3:122–126

    Article  Google Scholar 

  • Minnick DR (1973) The Flight and Courtship Behavior of the Drywood Termite Cryptotermes brevis. Environ Entomol 2:587–591. https://doi.org/10.1093/ee/2.4.587

    Article  Google Scholar 

  • Miyaguni Y, Sugio K, Tsuji K (2012) Refinement of methods for sexing instars and caste members in Neotermes koshunensis (Isoptera, Kalotermitidae). Sociobiology 59:65–68

    Google Scholar 

  • Miyaguni Y, Sugio K, Tsuji K (2013) The unusual neotenic system of the Asian Dry Wood Termite, Neotermes koshunensis (Isoptera: Kalotermitidae). Sociobiology 60:1217–1222

    Article  Google Scholar 

  • Miyatake T (2011) Insect quality control: synchronized sex, mating system, and biological rhythm. Appl Entomol Zool 46:3–14

    Article  Google Scholar 

  • Mizumoto N, Fuchikawa T, Matsuura K (2017) Pairing strategy after today's failure: unpaired termites synchronize mate search using photic cycles. Popul Ecol 59(3):205–211

    Article  Google Scholar 

  • Nalepa CA, Miller LR, Lenz M (2001) Flight characteristics of Mastotermes darwiniensis (Isoptera, Mastotermitidae). Insect Soc 48:144–148

    Article  Google Scholar 

  • Neoh KB, Lee CY (2009a) Flight activity and flight phenology of the Asian subterranean termite, Coptotermes gestroi (Blattodea: Rhinotermitidae). Sociobiology 54:521–530

    Google Scholar 

  • Neoh KB, Lee CY (2009b) Flight activity of two sympatric termite species, Macrotermes gilvus and Macrotermes carbonarius (Termitidae: Macrotermitinae). Environ Entomol 38:1697–1706

    Article  PubMed  Google Scholar 

  • Nutting WL (1966) Colonizing flights and associated activities of termites. The desert damp-wood termite Pararicotermes simplicicornis (Kalotermididae). Psyche 73:131–149

    Article  Google Scholar 

  • Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press, New York, pp 233–282

    Chapter  Google Scholar 

  • Olson RS, Hintze A, Dyer FC, Knoester DB, Adami C (2013) Predator confusion is sufficient to evolve swarming behaviour. J R Soc Interface 10:20130305. https://doi.org/10.1098/rsif.2013.0305

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 95–119

    Chapter  Google Scholar 

  • Sugio K, Miyaguni Y, Tayasu I (2018a) Characteristics of dispersal flight and disperser production in an Asian dry-wood termite, Neotermes koshunensis (Isoptera, Kalotermitidae). Insectes Soc 65:323–330

    Article  Google Scholar 

  • Sugio K, Miyaguni Y, Yoshimura T (2018b) Damage and ecological characteristics of termite Neotermes koshunensis on Taiwan cherry tree Cerasus campanulata in Okinawa Island. J Asia-Pacific Entomol 21:1424–1429

    Article  Google Scholar 

  • Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus and Robertson, North Ryde

    Google Scholar 

  • Wang C, Powell JE, Liu Y (2002) A literature review of the biology and ecology of Coptotermes formosanus (Isoptera: Rhinotermitidae) in China. Sociobiology 40:343–364

    Google Scholar 

  • West S (2009) Sex allocation. Princeton University Press, New Jersey

    Book  Google Scholar 

  • Wilkinson W (1962) Dispersal of alates and establishment of new colonies in Cryptotermes havilandi (Sjöstedt) (Isoptera, Kalotermitidae). Bull Entomol Res 53:265–286

    Article  Google Scholar 

  • Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517

    Article  Google Scholar 

  • Yashiro T, Takematsu Y, Ogawa N, Matsuura K (2019) Taxonomic assessment of the termite genus Neotermes (Isoptera: Kalotermitidae) in the Ryukyu-Taiwan Island arc, with description of a new species. Zootaxa 4604:549–561

    Article  Google Scholar 

Download references

Acknowledgements

We thank K. Kobayashi (Kyoto University) for helpful advice and discussion. We also thank A. Renzetti (University of the Ryukyus) for correcting the English in our manuscript, and the anonymous referees for their constructive comments.

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Authors and Affiliations

  1. Graduate School of Education, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    K. Sugio

  2. Global Education Institute, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    Y. Miyaguni

  3. Research Institute for Sustainable Humanosphere, Kyoto University, Uji, Kyoto, 611-0011, Japan

    T. Yoshimura

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  1. K. Sugio
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  2. Y. Miyaguni
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  3. T. Yoshimura
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Correspondence to K. Sugio.

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Sugio, K., Miyaguni, Y. & Yoshimura, T. Synchronization of alate emergence among colonies and dispersal strategy in the Ryukyu dry-wood termite Neotermes sugioi (Isoptera: Kalotermitidae). Insect. Soc. 67, 309–316 (2020). https://doi.org/10.1007/s00040-020-00766-5

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  • DOI: https://doi.org/10.1007/s00040-020-00766-5

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