[Termite Control] Home is Where the Heart is

The eastern subterranean termite, Reticulitermes flavipes (Kollar), is a wood-eating structural pest responsible for a large proportion of the billions of dollars Americans spend each year on termite infestation prevention and damage repair. R. flavipes colonies, which can contain thousands of members, are made up of several specialized castes, or categories, of individuals.
Kings and queens are solely responsible for reproduction. If either of them die, some of their offspring can develop into secondary or replacement reproductives. This reproductive flexibility allows the colony to survive after the loss of its parents. Soldiers defend their nestmates from other termites and predatory ants but are unable to feed themselves. Larvae and eggs, collectively called brood, are the immature members of the colony. Workers or foragers form the vast majority of the colony, feeding and grooming all the other castes, foraging for resources and maintaining the nest and galleries.

COLONY CHARACTERISTICS. R. flavipes colonies are essentially nomadic, living in underground galleries excavated near or in the wood they feed on. Typically a colony will utilize more than one resource at a time, feeding at sites spread across several square meters. The classic interpretation of this pattern of feeding at multiple, physically separated sites follows a “central foraging” model in which activity centers around a resource-rich hub containing the king and queen and their brood. In this scenario, workers leave the main nest, gather food at outlying resources and retrace their steps back to the central nest. Workers then redeploy back to the outlying feeding sites at random; thus, a colony’s entire population regularly cycles through all of its feeding locations (Orians and Pearson 1979, Su, et al. 1984).
Field research has suggested that this model is flawed, and that in fact termite workers exhibit feeding site fidelity or tenacity, eating preferentially in one location rather than remixing uniformly across the foraging territory (Su, et al. 1993, Forschler and Townsend 1996, Evans, et al. 1998, 1999). A fuller understanding of R. flavipes’ exploitation of their multiple feeding resources is valuable in its own right, but may also impact pesticide delivery strategies; slow-acting, nonrepellent termiticides depend on the interaction between exposed and naive nestmates.
We built foraging networks in the lab to examine how 13 R. flavipes colonies exploited multiple, physically separated feeding sites. We monitored travel within the networks regularly and fully censused the colonies after 18 months to answer the following questions: Would workers circulate throughout the network or feed preferentially in one site? How would the different castes distribute themselves across the network? Were the reproductives and the brood housed together in the central resource?

THE EXPERIMENTS. The feeding networks were constructed with three clear plastic canisters linked together with 3.5-meter sections of flexible plastic tubing; a whole system measured almost 7 meters from end to end. Although the center canister of each network was larger than the two side ones, all three were filled with equal amounts of moist wood. The connecting tubes were loosely filled with sand to simulate active worker tunneling during the search for new resources. Wood and moisture were replenished as needed.
We placed entire, eight-year-old lab colonies (averaging 7,000-plus individuals) in the center chamber of each feeding network and allowed them to forage for three years.  Nine of the colonies contained their original kings and queens (the primary reproductives), while four contained primary kings and at least one replacement or secondary reproductive female which had developed after the queen died. At the experiment’s midpoint, the networks were temporarily dismantled and all of the termites were counted. This gave us a snapshot of each colony’s distribution within the networks and the relative positions of the reproductives and their brood. 
Monitoring individual termites throughout the networks was impossible; however, we were able to track travel patterns across the networks using mark-recapture, an indispensable tool for mapping foraging territories in the field. Workers were collected from both side chambers and were fed paper that had been dyed either red or blue. This dye remained visible in the termites’ bodies for up to 30 days (Figure 2). We returned the dyed termites to their original containers and recollected from both side chambers and the central hub after either 7, 14 or 30 days. By comparing the ratio of red and blue termites collected from all three feeding sites, we were able to evaluate the movement patterns. (See chart on page 66.) For example, if the same proportions of dyed workers were recovered in each of the three resources, it suggested that termites redistributed evenly throughout the network. Alternatively, if marked termites were recaptured disproportionately, then workers apparently failed to redistribute uniformly.

RESULTS. Analysis of our recapture data showed that even 30 days after marked termites were returned to the chamber where they had first been collected, they were significantly more likely to be recovered from that same resource than from either of the other two available feeding chambers.  We emphasize that this preference was not absolute; marked workers were recovered from all three chambers, but workers did not remix fully with their nestmates in the other chambers. 
The census showed that kings and queens (or secondary female reproductives) were found side by side in all but one colony.  In that one exception (a colony with four secondary females), the king and two female neotenics were located in the central chamber and the other two neotenic females were positioned together in a side chamber.  Reproductives never shared the same cavity within the wood as their brood, and in seven of the 13 colonies they were in an entirely separate chamber of the network. The eggs and larvae were largely kept together in a brood gallery excavated within the wood.  On average, 81 percent of larvae and 96 percent of eggs were found here. The resource chambers that contained these brood clutches also housed just over half of the colonies’ workers who were presumably there to care for the young.   
Our results cast doubt on the classic assumption that R. flavipes colonies always maintain central nesting chambers containing brood and reproductives. The glimpses of colony life offered by our direct census indicate that the kings and queens were mobile throughout the three-year time period. Eighteen months after introduction into the foraging networks, 69 percent of royal pairs were found outside the original, central chamber, and they were no more likely to be found in the same resource as their brood than would occur randomly. When networks were dismantled 18 months later, all but one pair were found in a different location. These observations did not capture the frequency of reproductive relocation, but suggest that despite the absence of obvious distress (such as predation, resource depletion or environmental changes) they were itinerant.
The combination of workers preferentially feeding in specific locations and the fact that kings, queens and brood were not together a significant portion of the time, nor were they found in the central chamber of a three-chamber feeding arena with any regularity suggests that, at least under certain conditions, R. flavipes can establish a decentralized, dynamic network rather than a classic central-place foraging system.  Such a dispersed foraging model seems particularly well suited to Reticulitermes, given the genus’ exploitation of fallen timber, which is a spatially patchy, unpredictable and exhaustible food resource. 
Several slow-acting, nonrepellent termiticides are on the market. When these treatments fail to eliminate an infestation, feeding site fidelity and the subsequent failure of termiticide-exposed foragers to fully circulate throughout the colony may be contributing factors.
To fulfill their colony control potential, these products depend on two elements of random remixing: i) exposed workers are constantly replaced at a treated site by naive nestmates; ii) toxicant is transferred from initially exposed foragers to their remote nestmates via grooming, trophallaxis and cannibalism (Bayer 2004; BASF 2005; Dow AgroSciences 2005; McNally, et al. 2005). The aforementioned feeding tenacity results demonstrate that although foragers may travel from one end of the multi-resource network to another within a seven-day period, they are significantly more likely to be found within their original resource for at least a month. Given that fipronil mortality was nearly 100 percent after only 72 hours (Ibrahim, et al. 2003) and that workers can experience impaired mobility within minutes of exposure to imidacloprid (Thorne and Breisch 2001), many of the potential termiticide carriers might be dead or incapacitated before they have the chance to leave the site of exposure and contact distant nestmates. When these treatments fail to eliminate an infestation, feeding site fidelity and the subsequent failure of termiticide-exposed foragers to fully circulate throughout the colony may be contributing factors.

The authors thank N.L. Breisch, L.W. Douglass and A. Black for assistance with data collection and analysis. This study was conducted in partial fulfillment of a doctoral degree at the University of Maryland-College Park. Financial support was provided by the Gahan Family Fellowship and the Jeffery P. LaFage Graduate Student Research Award.

Catherine Long, Ph.D., is an entomologist at American Pest Management, Takoma Park, Md. Dr. Barbara Thorne is an entomology professor at the University of Maryland-College Park.
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