HOUSEHOLD AND STRUCTURAL INSECTS
Influence of Environmental Factors on Activity Patterns of Incisitermes minor (Isoptera: Kalotermitidae) in Naturally Infested Logs VERNARD R. LEWIS,1 SHAWN LEIGHTON, ROBIN TABUCHI, JAMES A. BALDWIN,2 AND MICHAEL I. HAVERTY Division of Organisms and the Environment, Department of Environmental Science, Policy, and Management, College of Natural Resources, University of California/Berkeley, 1301 South 46th Street, Building 478, Richmond, CA 94804 Ð 4698
J. Econ. Entomol. 106(1): 338Ð346 (2013); DOI: http://dx.doi.org/10.1603/EC12050
ABSTRACT Acoustic emission (AE) activity patterns were measured from seven loquat [Eriobotrya japonica (Thunb.) Lindl.] logs, Þve containing live western drywood termite [Incisitermes minor (Hagen)] infestations, and two without an active drywood termite infestation. AE activity, as well as temperature, were monitored every 3 min under unrestricted ambient conditions in a small wooden building, under unrestricted ambient conditions but in constant darkness, or in a temperaturecontrolled cabined under constant darkness. Logs with active drywood termite infestations displayed similar diurnal cycles of AE activity that closely followed temperature with a peak of AE activity late in the afternoon (1700 Ð1800 hours). When light was excluded from the building, a circadian pattern continued and apparently was driven by temperature. When the seven logs were kept at a relatively constant temperature (!23 " 0.9#C) and constant darkness, the pattern of activity was closely correlated with temperature, even with minimal changes in temperature. Temperature is the primary driver of activity of these drywood termites, but the effects are different when temperature is increasing or decreasing. At constant temperature, AE activity was highly correlated with the number of termites in the logs. The possible implications of these Þndings on our understanding of drywood termite biology and how this information may affect inspections and posttreatment evaluations are discussed. KEY WORDS acoustic emissions, drywood termites, feeding periodicity, temperature effects
Much of the success achieved by termites in becoming dominant terrestrial organisms has been attributed to their ability to exploit the rhythmic pattern of the appearance and disappearance of cellulose resources deÞned by the environmental parameters of temperature, humidity, precipitation, and biotic factors such as limb- and tree-killing insects. Daily patterns in biology have been coined circadian rhythms and are common across many phyla of plants, microbes, and animals (Beck 1968, Schotland and Sehgal 2001). Circadian (meaning approximately daily) cycles can be endogenous and set by photoperiod, or cycles of light and dark, within the day. Circadian cycles of insect activity may also be simply driven by exogenous factors such as temperature, humidity, and light intensity (Beck 1968). Once the exogenous cue is removed or altered, the circadian nature of the cycle disappears. These circadian cycles can be nested within the seasonal cycle. Hebrant (1970) discovered an endogenous circadian rhythm in oxygen consumption in freshly collected whole colonies of the termite Cubitermes exCorresponding author, e-mail:
[email protected]. PaciÞc Southwest Research Station, USDA Forest Service, P.O. Box 245, Berkeley, CA 94701. 1 2
iguus Mathot that were maintained at a constant 30#C for 3 d. He observed two maxima, one in the evening and one in the morning, and two minima, the Þrst at midnight and the second, more expressed, in the early afternoon. He ascribed this variation in oxygen consumption to the periods of activity of the mound during the day. Relative humidity and temperature seemed to be the main factors driving this activity, as light did not act as a direct stimulus to C. exiguus. It is important to understand that this circadian cycle (rhythm) was sustained even though the phase-setting stimuli (or Zeitgebers), temperature and relative humidity, were no longer inßuential. For subterranean termites, their foraging habits have been well studied especially for desert, Mediterranean, and temperate climates (Haverty et al. 1974, 1975, 1999, 2000; La Fage et al. 1976; Esenther 1980; Su and Scheffrahn 1988; Grace et al. 1989; Jones 1990; French 1991; Haagsma and Rust 1995; Forschler and Townsend 1996; Baker and Haverty 2007). Using various topical and in-ground monitors, temperature probes, and measures of precipitation, foraging and wood consumption were found to be highly rhythmic seasonally and closely followed changes in temperature and were modiÞed by rainfall or increases in soil
0022-0493/13/0338Ð0346$04.00/0 ! 2013 Entomological Society of America
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moisture (Haverty et al. 1974, 1999; La Fage et al. 1976). Haverty and Nutting (1974) investigated the inßuence of temperature on feeding of the termite Paraneotermes simplicicornis (Banks) and the termite Heterotermes aureus (Snyder). They found that wood consumption, measured as milligrams of wood consumed per hour per gram dry weight of termite, from 16 to 36#C is described by a polynomial equation of the form a $ bX % cX2. Feeding was highest for P. simplicicornis at 28#C and highest for H. aureus at 32#C. Because drywood termites (family Kalotermitidae) are single piece nesters and can live deep in wood, there are few reports of seasonal or daily cycles of feeding or foraging behavior. Seasonal activity patterns of drywood termites are very important for their detection and treatment. A common seasonal activity for drywood termites is swarming. In California, the western drywood termite Incisitermes minor (Hagen), swarms during the day, starting in summer and continuing into fall (Ebeling 1978). Feeding and foraging are important drywood termite activities; however, little is known about when they occur or what drives them. The cryptic behavior of drywood termites inside wood hinders studies that explore their normal feeding and foraging behavior. Acoustic emission (AE) technology has been used to detect the presence of drywood and dampwood termites in wood (Lewis and Lemaster 1991, Lemaster et al. 1997) and recently has been used to explore seasonal and daily patterns foraging and feeding activity of I. minor (Lewis et al. 2011). Lemaster et al. (1997) found no periodicity in feeding of I. minor in a 24-h day. However, the investigation only ran for 1 wk and was conducted under constant temperature conditions. Indrayani et al. (2006) also used AE technology to monitor I. minor feeding when affected by different laboratory temperatures and relative humidity; however, they did not report diurnal or seasonal AE activity. Using AE monitoring during an investigation of local chemical treatments in a Þeld study in southern California, activity of I. minor infestations in untreated locations of structures declined during winter months (V. Lewis, unpublished data). Because this Þeld study involved only four posttreatment inspection dates, it was not possible to make deÞnitive statements on seasonal foraging of drywood termites. Little research has been conducted on the movement patterns of drywood termites. Currently, only the speed of locomotion of I. minor (1.4 cm/s) in response to temperature and light is known (Cabrera and Rust 1994, 1996, 2000). Rust et al. (1979) inferred movement of the drywood termite Incisitermes fruticavus Rust from studies that measured daily changes in temperature inside galleries for the Jojoba shrub, Simmondsia chinensis (Link); however, the daily or seasonality of movement of drywood termites within structures in California remains poorly understood. Lewis et al. (2011) investigated activity of colonies of I. minor with acoustic emission (AE) technology in naturally infested logs. Activity, whether it was feed-
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ing, excavation, or movement, was monitored for 11 mo under ambient conditions in a small wooden structure. AE, temperature, and humidity data were measured in 3-min increments. Termite activity was greater during the warmer summer months compared with the cooler winter months. Termites in all logs displayed a similar daily cycle of activity, peaking in the late afternoon. Seasonal and daily ßuctuations in termite activity were signiÞcantly associated with temperature, whereas humidity had a less noticeable effect on termite activity. The purpose of this study was to investigate the nature of the circadian cycle of activity in I. minor: the role or inßuence of temperature and light on patterns of feeding and foraging as measured by vibrational activity in naturally infested wood. By knowing when drywood termites are most active and whether physical features of their environment affect their activity, inspections and posttreatment evaluations of remedial treatments could be greatly improved. Materials and Methods Selection and Preparation of Naturally Infested Wood. Logs from a large loquat tree [Eriobotrya japonica (Thunb.) Lindl.] were collected during the summer of 2007 from Granada Hills, CA, and brought to our laboratory. The logs were similar in size and revealed visual signs of drywood termite activity. To verify that candidate logs had an active drywood termite infestation, three 1-min recordings of AE activity were taken from the center of the log (Lewis et al. 2004) by using a hand-held device (Tracker, Dunegan Engineering, Midland, TX). Five logs averaging !300 AE counts/min were randomly selected for use in these experiments. Two additional logs were randomly selected as controls. The control logs were put into an oven (Isotemp model 655 F; Fisher, Pittsburgh, PA) at 105#C for 24 h to kill all termites within the logs (Lewis et al. 2011). Multichannel AE Monitoring Equipment. All seven logs had a subsurface sensor installed into their long center by drilling a 2.4-mm-diameter hole and inserting the sensor probe 1.2 cm deep into wood. All log and sensor assignments were randomly chosen. A 3-mlong cable from each of the seven sensors was connected to a port in an AE Smart Device (Dunegan 2005) and dedicated computer (Dell Corporation, Austin, TX) that stored all of the data. All logs were placed onto a small wooden table, and the AE Smart Device, dedicated computer, and backup power supply were placed on a wooden desk near the table (Fig. 1). To prevent ants [Argentine ants, Linpethemia humilie (Mayr)] from attacking the termites in the logs on the table, the legs of the table were placed into small plastic saucers (15 cm in diameter by 3 cm deep) containing a 1-cm-deep band of motor oil (SAE 30; Ace Hardware Corporation, Oak Brook, IL). Additional ant prevention measures included applying a 15-cm-long band of petroleum jelly (Longs Drugs, Walnut Creek, CA) to the cable end leading into the main AE Smart Device controller box. The entire
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Fig. 1. Seven logs from a large loquat tree [Eriobotrya japonica (Thunb.) Lindl.] used for the study. The logs were similar in maximum diameter, length, and age. The seven small white boxes seen in the center of the photograph are AE Smart Max-modules and are used in conjunction with software to control the random order of sensor selection for AE activity during data collection.
system was visited at least weekly to check on the operating status. Infested Logs and AE Equipment Storage. All logs, AE, and temperature equipment were stored in a
small, wooden, 50-yr-old building at the University of California Richmond Field Station, Richmond, CA. The building was 8.2 by 4.9 m (40.2 m2), one story in height, and had a slab foundation. The construction
Fig. 2. Plots of AE ring down counts over time under constant darkness from 19 August 2009 to 25 August 2009 for Þve sensors that contain live colonies of I. minor. The smooth line is a running average of the AE ring down counts for 30 min before until 30 min after the data points.
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Fig. 3. Plots of AE ring down counts under constant darkness as a function of temperature in Þve I. minor-infested logs and two uninfested logs. The temperature values are “jittered” so that they do not land exactly on top of each other. All sensors associated with infested logs show a positive relationship with temperature. Each data point represents 3-min recordings taken at least two times/h/d/sensor over 7 d.
type was double wall with Douglas-Þr [Pseudotsuga menziesii (Mirbel) Franco V.] studs, redwood interior walls, and ceiling paneling. The exterior was plywood siding. The building had Þve windows for natural light. Three windows were on the northeast side (91.4 by 60.9 cm in size) and two on the southeast side of the building (121.9 by 111.8 cm and 122 by 91.4 cm in size). There was no air conditioning or heating in the building; environmental conditions were strictly ambient and unrestricted. The roof was tar and shingle and was in good condition. To minimize human trafÞc into the building, a sign up log was created requesting the date, time, name of individuals, and afÞxed to the exterior door of the building before entry. A warning sign was posted on the door to notiÞed individuals before entering that a vibration-sensitive research project was being conducted. Response Variables, Data Summaries, and Analyses. All data were downloaded onto a high capacity (256 MB), portable storage device (Kingston Data Traveler, Fountain Valley, CA) for long-term storage and future analysis. Twenty 3-min recordings were randomly taken among the seven sensors for each 60-min period during the study. No sensor was used more than three times or less than two times during a 60-min period, and the order of the readings were randomized. In addition, air temperature (Omega Engineering, Stamford, CT) was re-
corded for each 3-min AE recording and saved to an electronic spread sheet (Excel Corporation, Lubbock, TX). A backup battery power supply (Back-ups; APC Corporate, W. Kingston, RI) was installed in the event of unexpected power outages. The entire AE system as described above was run for 11 mo (15 June 2008 Ð15 May 2009). Lewis et al. (2011) reported results and conclusions from that 11-mo study. The same seven logs were used for additional experiments to determine whether circadian activity cycles were endogenously or exogenously controlled. Throughout the various studies the variables measured were AE ring down counts and air temperature. AE ring down counts were proxies for feeding and other activity of the termites and constituted the response variables of interest. AE Activity Under Constant Darkness. To ascertain whether cyclical activity patterns were endogenous circadian rhythms affected by photoperiod, the windows were covered with black plastic sheeting to exclude external light. Recordings under conditions of total darkness were made from 18 August 2009 to 25 August 2009. For each sensor, including those in the control logs, the individual 3-min readings were used for the 7-d period from 19 August 2009 until 25 August 2009 for display purposes. The resulting smooth line is composed of a running average of the AE ring down
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Fig. 4. Histogram of temperature taken every 3 min from 24 November 2009 until 26 January 2010 in a controlled temperature cabinet.
counts for 30 min before until 30 min after individual data points. The effect of temperature on AE ring down counts was displayed for each sensor. AE Activity Under Constant Temperature. To determine whether cyclical activity patterns would continue “to be manifested as circadian rhythms even in the absence of an entraining photoperiod or thermoperiod” (Beck 1968), the seven logs were placed in a constant-temperature cabinet (Precision Low Tem-
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perature Incubator, model 815; 677 mm by 1,448 by 508 mm, 566 liter capacity; Geneva ScientiÞc LLC, Fontana, WI) that also excluded light. Recordings under constant temperature conditions were made from 24 November 2009 until 26 January 2010. The constanttemperature cabinet had a small opening on the top side that allowed for all wiring for AE and temperature recording equipment to pass into the interior. AE activity and temperature were recorded within the cabinet as they were under the unrestricted and constant darkness conditions. For each sensor, including those in the control logs, the individual 3-min readings were used for the 63-d period. The effect of temperature on AE ring down counts was displayed for each sensor. Effect of Termite Numbers on AE Ring Down Counts. At the conclusion of experimentation, the number of surviving termites in each caste was counted after dissection of all seven logs by using a mallet and wood chisel from 15 June 2010 until 23 June 2010. The mean AE ring down count resulting form the constant temperature experiment was used as the dependent variable and regressed against the total number of termites (R Development Core Team 2004). Data were transformed to the natural log by using the following model: ln (AE ring down count) & a $ b * ln (number of termites remaining) $ error to make the normality and constant variances of the residuals more readily apparent.
Fig. 5. Three-min AE ring down counts from 24 November 2009 until 26 January 2010, for Þve sensors (1Ð5) in I. minor-infested logs and two sensors (6Ð7) in uninfested logs under constant temperature conditions.
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Fig. 6. The mean daily AE ring down count (black line) from Þve sensors (1Ð5) in I. minor-infested logs (1Ð5) and two sensors (6Ð7) in uninfested logs under constant temperature conditions. The mean has been smoothed with a loess (nonparametric regression) smoother. The gray line is the smoothed mean temperature proÞle across all observations. (Online Þgure in color.)
Results and Discussion Lewis et al. (2011) reported that seasonal activity, in terms of AE ring down counts, displayed a pattern of increasing and decreasing values each day, primarily associated with daily changes in temperature. AE activity was, in general, highest during the warmer late spring, summer, and early fall months (late AprilÐmidOctober) and lowest during the late fall through early spring (mid-OctoberÐmid-April). An increase in daytime temperature, or a sudden heat wave, even in January and February of 2009, resulted in a burst of increased AE activity (Lewis et al. 2011). Furthermore, Lewis et al. (2011) found that within an average 24-h day, AE activity displayed a nonlinear pattern of activity. This pattern was sinusoidal in shape and was lowest during the morning (!1,000), increased in the afternoon, and peaked in late afternoon (between 1,600 and 1,800), then declined until midmorning clearly following the temperature pattern. AE Activity Under Constant Darkness. To measure the inßuence of photoperiod on daily activity, we excluded light from the building. AE activity remained cyclical with apparent daily cycles of feeding activity (Fig. 2). Ambient temperature during this 1-wk period only varied from 22.5 to 26.5#C. The AE ring down counts for the Þve sensors in infested logs showed a positive relationship with temperature, whereas activity in the uninfested logs was at least 10' lower than
that in the infested logs, served as an indication of background AE activity, and was not positively associated with temperature (Fig. 3). AE Activity Under Constant Temperature. Temperature was regulated such that it was targeted for 23#C, but did rise to 26.7#C on a few occasions. A histogram of the temperatures that were taken at approximately 3-min intervals showed that 92.6% of the time the temperature ranged from 22.8 to 24.4#C) (Fig. 4). This temperature regime resulted in AE ring down counts (Fig. 5) that were quantitatively very similar to those observed under the constant darkness conditions (Fig. 2). We found that even with the much smaller variation in temperature, there is a consistent and delayed pattern in the mean AE ring down counts over an average 24-h period. When the mean AE ring down count has been smoothed with a nonparametric regression, the activity in I. minor-infested logs (sensors 1Ð5) displayed a pattern that is very similar to that of the temperature curve over the same period, whereas the sensors in the uninfested logs did not (Fig. 6). We Þnd this to be remarkable given that the swing in mean temperature is generally (2.2#C and is very similar to the patterns for each sensor over the much longer period (Lewis et al. 2011). Effect of Termite Numbers on AE Ring Down Counts. When we were certain that we had completed all experimentation by using the Þve I. minor-infested
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Table 1. Number of I. minor (Hagen) individuals of various castes dissected from five infested and two uninfested loquat )Eriobotrya japonica (Thunb.) Lindl.* logs after completion of all experiments No. of live termites Log no.
Date of dissection
Nymphs, workers, and pseudergates
Soldiers
Queen
King
Total
1 2 3 4 5 6 7
6/22/10 6/17/10 6/15/10 6/23/10 6/21/10 6/15/10 6/15/10
1,700 3,114 252 600 1,995 0 0
51 25 3 11 53 0 0
1 1 0 0 1 0 0
1 0 0 0 1 1 1
1,753 3,140 255 611 2,050 1 1
logs, we dissected these Þve logs, as well as the uninfested logs, and counted all live individuals by caste (Table 1). The single alate found in each of the untreated logs was because of natural swarming activity from some of the logs in the test building. We regressed the line (ln) of the mean AE ring down counts from the constant temperature experiment (the most recent experiment before log dissection) for all seven logs against the ln of the total number of individuals remaining. A highly signiÞcant relationship was found (r2 & 0.92) between the I. minor population and AE activity (Fig. 7). There are few reports of diurnal or seasonal AE activity data for I. minor. Using 100 I. minor workers contained in an artiÞcially infested wooden block held at constant temperature and humidity, Lemaster et al. (1997) reported AE events results from a single sensor during a 7-d test. There was no statistically signiÞcant cycling or periodicity found in AE activity. The plot of AE activity appeared ßat and hovered between the values of 100 and 200 events per hour. No ring down count data were reported. The maximum AE event results reported by Lemaster et al. (1997) compared favorably with the maximum events reported for the current study, although we report here only AE ring down count data. Indrayani et al. (2006) conducted a second AE activity study. For this laboratory study I. minor workers (10) also were used in small wooden
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blocks to test the affects of varying temperature and humidity. The tests were of short duration, only 12 h. This study reported that the optimum temperature for peak AE activity was 30#C. In the most extensive measurement to date of the relationship of drywood termite activity, as represented by AE activity, Lewis et al. (2011) demonstrated that AE ring down counts increased with temperature, even during warm days during seasonally cold months (November of 2008 to February of 2009). Furthermore, Þeld observations reported to the senior author (V.R.L., unpublished data) over the years included complaints of seeing drywood termite pellets in December from a large condominium site in Marina del Rey, CA. Before this study, those pellets were assumed to be background noise with little concern about when they are expelled from infested wood during colder winter months. However, with our new Þndings, perhaps warming of the interiors of apartments and residences during the winter months simulated drywood termite feeding activity. There is considerable variance in the size and number of I. minor dissected and reported in the literature from naturally infested logs and structural wood; counts ranged up to 9,200 (Harvey 1934, Nutting 1970, Scheffrahn et al. 1993, Lewis and Haverty 1996, Lewis and Power 2004, Lewis et al. 2005). Obviously, larger colonies produce greater AE activity (Fig. 7). Also it is evident that when drywood termites are allowed to search and forage for wood naturally under ambient conditions, their activity follows a cyclical pattern common to many terrestrial animals and this pattern is largely governed by temperature and is not an endogenous circadian rhythm. Two drywood termite species, I. minor and Cryptotermes brevis (Walker), are responsible for a majority of the damage caused by drywood termites in the United States (Light 1934, Su and Scheffrahn 1990, Grace 2009). The economic cost of control and repair of damage is second only to that of subterranean termites (Su and Scheffrahn 1990). Knowledge on optimal times for drywood termite foraging could be important to termite inspections. Traditional inspections
Fig. 7. Mean AE ring down counts resulting from the constant temperature experiment correlated with the total number of I. minor dissected from each of the Þve infested logs. Data were transformed to the natural log.
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are visual and based on visual searches for damaged wood or pellets. The results from this study suggest searches for pellets and active drywood termite infestations could be enhance by heating the wood to at least 25#C before inspection to simulate foraging and feeding, even in winter, and using AE technology to delimit infestations. Calibration of AE recordings for temperature and the numbers of termites could beneÞt determinations of the location(s) and extent of a drywood termite infestation. Acknowledgments We thank H. Dunegan and J. Farrow for their technical assistance in designing and customizing the AE Smart device and related hardware to accommodate our research needs. We also thank G. Briseno for developing the software for the automated collection of AE and temperature data into electronic spreadsheets. We extend sincere thanks to the Leighton family who provided us with the infested logs used to collect the drywood termite pellets. This research was made possible, in part, by contract 084-2856-5 to V.R.L. by the California Structural Pest Control Board, Department of Pesticide Regulation (formerly the Department of Consumer Affairs), Sacramento, CA.
References Cited Baker, P. B., and M. I. Haverty. 2007. Foraging populations and distances of the desert subterranean termite, Heterotermes aureus (Isoptera: Rhinotermitidae), associated with structures in southern Arizona. J. Econ. Entomol. 100: 1381Ð1390. Beck, S. D. 1968. Insect photoperiodism. Academic, New York and London, United Kingdom. Cabrera, B. J., and M. K. Rust. 1994. The effect of temperature and relative humidity on the survival and wood consumption of the western drywood termite, Incisitermes minor (Isoptera: Kalotermitidae). Sociobiology 24: 95Ð113. Cabrera, B. J., and M. K. Rust. 1996. Behavioral responses to light and thermal gradients by the western drywood termite (Isoptera: Kalotermitidae). Environ. Entomol. 25: 436 Ð 445. Cabrera, B. J., and M. K. Rust. 2000. Behavioral responses to heat in artiÞcial galleries by the western drywood termite (Isoptera: Kalotermitidae). J. Agric. Urban Entomol. 17: 157Ð171. Dunegan, H. L. 2005. Detection of movement of termites in wood by acoustic emission techniques, US Patent 6,883,375 B2, 14 pp. Assignee: H. L. Dunegan, Laguna Niguel, CA. Ebeling, W. 1978. Urban entomology. University of California Press, Berkeley, CA. Esenther, G. R. 1980. Estimating the size of subterranean termite colonies by a release-recapture technique, pp. 1Ð5. In Proceedings, 11th Annual Meeting of the International Research Group on Wood Preservation, 5Ð9 May 1980, Raleigh, NC (IRG Document No. IRG/WP/1112). IRG Secretariat, Stockholm, Sweden. Forschler, B. T., and M. L. Townsend. 1996. Mark-releaserecapture estimates for Reticulitermes spp. (Isoptera: Rhinotermitidae) colony foraging populations from Georgia, U.S.A. Environ. Entomol. 25: 952Ð962. French, J.R.J. 1991. Baits and foraging behavior of Australian species of Coptotermes. Sociobiology 19: 171Ð186. Grace, J. K. 2009. What can fecal pellets tell us about cryptic drywood termites (Isoptera: Kalotermitidae)? pp. 1Ð12.
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In Proceedings, 40th Annual Meeting of the International Research Group on Wood Protection, 24 Ð28 May 2009, Beijing, China (IRG Document No. IRG/WP/20407). IRG Secretariat, Stockholm, Sweden. Grace, J. K., A. Abdallay, and K. R. Farr. 1989. Eastern subterranean termite (Isoptera: Rhinotermitidae) foraging territories and populations in Toronto. Can. Entomol. 121: 551Ð556. Haagsma, K. A., and M. K. Rust. 1995. Colony size estimates, foraging trends, and physiological characteristics of the western subterranean termite (Isoptera: Rhinotermitidae). Environ. Entomol. 24: 1520 Ð1528. Harvey, P. A. 1934. Life history of Kalotermes minor, pp. 208Ð 224. In C. A. Kofoid, S. F. Light, A. C. Horner, M. Randall, W. B. Herms, and E. E. Bowe (eds.), Termites and termite control. University of California Press, Berkeley, CA. Haverty, M. I., and W. L. Nutting. 1974. Natural woodconsumption rates and survival of a dry-wood and a subterranean termite at constant temperatures. Ann. Entomol. Soc. Am. 67: 153Ð157. Haverty, M. I., J. P. La Fage, and W. L. Nutting. 1974. Seasonal activity and environmental control of foraging of the subterranean termite, Heterotermes aureus (Snyder), in a desert grassland. Life Sci. 15: 1091Ð1101. Haverty, M. I., W. L. Nutting, and J. P. La Fage. 1975. Density of colonies and spatial distribution of foraging territories of the desert subterranean termite, Heterotermes aureus (Snyder). Environ. Entomol. 4: 105Ð109. Haverty, M. I., G. M. Getty, K. A. Copren, and V. R. Lewis. 1999. Seasonal foraging and feeding behavior of Reticulitermes spp. (Isoptera: Rhinotermitidae) in a wildland and a residential location in northern California. Environ. Entomol. 28: 1077Ð1084. Haverty, M. I., G. M. Getty, K. A. Copren, and V. R. Lewis. 2000. Size and dispersion of colonies of Reticulitermes (Isoptera: Rhinotermitidae) in a wildland and a residential location in northern California. Environ. Entomol. 29: 241Ð249. Hebrant, F. 1970. Circadian rhythm of respiratory metabolism in whole colonies of the termite, Cubitermes exiguus. J. Insect Physiol. 16: 1229 Ð1235. Indrayani, Y., T. Yoshimura, Y. Yanase, Y. Fujii, and Y. Imamura. 2006. Evaluation of the temperature and relative humidity preferences of the western dry-wood termite Incisitermes minor (Hagen) using acoustic emission (AE) monitoring. J. Wood Sci. 52: 1Ð 4. Jones, S. C. 1990. Delineation of Heterotermes aureus (Isoptera: Rhinotermitidae) foraging territories in a Sonoran desert grassland. Environ. Entomol. 19: 1047Ð1054. La Fage, J. P., M. I. Haverty, and W. L. Nutting. 1976. Environmental factors correlated with the foraging behavior of a desert subterranean termite, Gnathamitermes perplexus (Banks) (Isoptera: Termitidae). Sociobiology 2: 155Ð169. Lemaster, R. L., F. C. Beall, and V. R. Lewis. 1997. Detection of termites with acoustic emission. For. Prod. J. 47: 75Ð79. Lewis, V. R., and M. I. Haverty. 1996. Evaluation of six techniques for control of the western drywood termite (Isoptera: Kalotermitidae) in structures. J. Econ. Entomol. 89: 922Ð934. Lewis, V. R., and R. L. Lemaster. 1991. The potential of using acoustical emission to detect termites within wood, pp. 34 Ð37. In M. I. Haverty and W. W. Wilcox (technical coordinators), Proceedings, symposium on current research on wood-destroying organisms and future prospects for protecting wood in use. U.S. Dep. Agric. Forest Service Gen. Tech. Rep. PSW-128. Lewis, V. R., and A. B. Power. 2004. Thiamethoxam trial update. Pest Control Technol. 9: 74, 76, 78, and 80 Ð 81.
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Lewis, V. R., A. B. Power, and M. I. Haverty. 2004. Surface and subsurface sensor performance in acoustically detecting the western drywood termite in naturally infested boards. For. Prod. J. 54: 57Ð 62. Lewis, V. R., A. B. Power, and G. M. Getty. 2005. Field evaluation of Thiamethoxam 2SC for the management of the western drywood termite (Isoptera: Kalotermitidae), pp. 331Ð336. In: C. Y. Lee and W. H. Robinson (eds.), Proceedings of the 5th International Conference on Urban Pests, 10 Ð13 July 2005, Suntec, Singapore. Perniagaan PhÕng@P & Y Desing, Network, Malaysia. Lewis, V., S. Leighton, R. Tabuchi, and M. Haverty. 2011. Seasonal and daily patterns in activity of the western drywood termite, Incisitermes minor (Hagen). Insects 2: 555Ð563. Light, S. F. 1934. The distribution and biology of the common dry-wood termite, Kalotermes minor, pp. 201Ð207. In C. A. Kofoid, S. F. Light, A. C. Horner, M. Randall, W. B. Herms, and E. E. Bowe (eds.), Termites and termite control. University of California Press, Berkeley, CA. Nutting, W. L. 1970. Composition and size of some termite colonies in Arizona and Mexico. Ann. Entomol. Soc. Am. 63: 1105Ð1110. R Development Core Team. 2004. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http:/www.R-project.org).
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Rust, M. E., D. A. Reierson, and R. H. Scheffrahn. 1979. Comparative habits, host utilization and xeric adaptations of the southwestern drywood termites, Incisitermes fruticavus Rust and Incisitermes minor (Hagen) (Isoptera: Kalotermitidae). Sociobiology 4: 239 Ð255. Scheffrahn, R. H., W. P. Robbins, P. Busey, N.-Y. Su, and R. K. Mueller. 1993. Evaluation of a novel, hand-held, acoustic emissions detector to monitor termites (Isoptera: Kalotermitidae, Rhinotermitidae) in wood. J. Econ. Entomol. 86: 1720 Ð1729. Schotland, P., and A. Sehgal. 2001. Molecular control of Drosophila circadian rhythms, pp. 15Ð30. In D. L. Denlinger, J. M. Giebultowicz, and D. S. Saunders (eds.), Insect timing: circadian rhythmicity to seasonality. Elsevier, Amsterdam, the Netherlands. Su, N.-Y., and R. H. Scheffrahn. 1988. Foraging population and territory of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in an urban environment. Sociobiology 14: 353Ð359. Su, N.-Y., and R. H. Scheffrahn. 1990. Economically important termites in the United States and their control. Sociobiology 17: 77Ð94. Received 1 February 2012; accepted 6 December 2012.
