Limited survival strategy in starving subterranean termite colonies
Termites feed on a carbon-rich but nitrogen-poor diet and evolved efficient nitrogen conservation strategies. It was previously suggested that during time of low access to resources (i.e., starvation), subterranean termites (Rhinotermitidae) colonies would adopt an energy conservation strategy by cannibalizing soldiers, a dependent caste. However, such hypothesis was tested with relatively small groups of foragers, which may not have reflected how resources are reallocated in whole colonies when food (carbon) is scarce. The current study subjected 2-year-old colonies (≈ 3000 termites with all castes and instars) to starvation, in order to reexamine if cannibalism is part of an active energy conservation strategy. Within 12 days of starvation, eggs and larvae were all cannibalized, followed by young workers. Soldiers then died marginally faster than old workers. By 22 days, cannibalism was no longer observed, and the king and queen were among the last individuals to die. Termites that engaged in the process of ecdysis with no energetic resources, failed to molt, died in the process, and the subsequent cannibalism was a passive mortality-driven process. Therefore, cannibalism was primarily the result of the inherent termite behavior for recycling nitrogen resources. The hemimetabolous developmental pathway, the difference of timing in the molting cycle of termite instars and the relatively rapid exhaustion of soldiers, indirectly determined the sequence of starvation-induced mortality and subsequent cannibalism. Although termites have evolved efficient nitrogen conservation strategies, they have not evolved an efficient carbon conservation strategy, which is essentially limited to keeping the primary reproductives alive as long as possible.
KeywordsLarval instar Resource limitation Starvation Coptotermes Colony level
Thanks to Zachary Kaplan, Ronald Pepin, Reynaldo Moscat and Alvin Puzio for technical assistance, Aaron Mullins, Nan-Yao Su and two anonymous reviewers for providing constructive comments on early versions of this manuscript. This study was supported in part by a grant from USDA-ARS under the Grant agreement no. 58-6435-8-276, by NSF-DEB Grant agreement no. 1754083, and by a research opportunity fund of the University of Florida under the Grant agreement no. 00094648.
- Buchli HR (1958) Recherche sur la fondation et le développement des nouvelles colonies chez le ermite lucifuge (Reticulitermes lucifugus (Rossi)). Physol Comp Oecol 2:145–160Google Scholar
- Chong A, Yap HH, Chong NL Lee CY (2002) Effects of starvation on nutrient distribution in the Pharaoh ant, Monomorium pharaonis (L.) (Hymonoptera: Formicidae) workers and various larval stages. In: Jones SC, Zhai J, Robinson WH (eds) Proceedings of the 4th international conference on urban pests. Pocahontas Press, Blacksburg, Virginia, pp 121–128Google Scholar
- Fox J, Weisberg S (2011) Cox proportional-hazards regression for survival data in R, second edition. https://socialsciences.mcmaster.ca/jfox/Books/Companion-2E/appendix/Appendix-Cox-Regression.pdf. Accessed Jun 2019
- Gulmahamad H (2002) Survival strategy of a western drywood termite colony, Incisitermes minor, (Isoptera: Kalotermitidae) established in a limited food source. Sociobiol 40:595–604Google Scholar
- Higa SY (1981) Flight, colony foundation and development of the gonads of the primary reproductives of the Formosans subterranean termites, Coptotermes formosanus Shiraki. Ph.D. dissertation, University of Hawaii, HonoluluGoogle Scholar
- Hunt JH, Nalepa CA (1994) Nourishment and evolution in insect societies. Westview Press, Boulder, p 449Google Scholar
- Nakajima S, Shimizu K, Nakajima Y (1963) Analytical studies on the vitality of colonies of the Formosan termite. Coptotermes formosanus, II. Seasonal fluctuations on the external characters of the workers, the ratio of caste-number and carbon dioxide in the nest of a colony. Miyazaki Univ Fac Agric Bull 9:222–227Google Scholar
- Nalepa CA (1994) Nourishment and the origin of termite eusociality. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, pp 57–104Google Scholar
- R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vianna, p 2018Google Scholar
- Shimizu K (1962) Analytical studies on the vitality of colonies of the Formosan subterranean termite, Coptotermes formosanus Shiraki. I. Analysis of the strength and vitality. Miyazaki Univ Fac Agric Bull 8:108–110Google Scholar
- Song D, Hu XP, Su NY (2006) Survivorship, cannibalism, body weight loss, necrophagy, and entombment in laboratory groups of the Formosan subterranean termite, Coptotermes formosanus under starvation (Isoptera: Rhinotermitidae). Sociobiology 47:27–39Google Scholar