Isoptera: Rhinotermitidae - PubAg - USDA

HOUSEHOLD AND STRUCTURAL INSECTS

Foraging Populations and Distances of the Desert Subterranean Termite, Heterotermes aureus (Isoptera: Rhinotermitidae), Associated with Structures in Southern Arizona PAUL B. BAKER1

AND

MICHAEL I. HAVERTY2

J. Econ. Entomol. 100(4): 1381Ð1390 (2007)

ABSTRACT MarkÐreleaseÐrecapture studies were conducted on foraging populations of Heterotermes aureus (Snyder) (Isoptera: Rhinotermitidae) associated with three structures in Tucson, AZ. Foraging population estimates ranged from 64,913 to 307,284 termites by using the Lincoln Index and from 75,501 to 313,251 termites using the weighted mean model. The maximum distance between monitors ranged from 26 to 65 m, with minimum total foraging distance ranging between 297 and 2,427 m. Characterizations of the cuticular hydrocarbons of foraging groups were qualitatively identical. Quantitative similarities within sites and differences among sites suggested that each site was occupied by a single colony during the sampling period. The colony at each site had a proportion of soldiers (0.135, 0.069, and 0.040) that was signiÞcantly different from the colonies at each of the other sites. From this study, we question the assumption of equal mixing of marked H. aureus foragers throughout the occupied collars around structures. KEY WORDS colony density, colony size, cuticular hydrocarbons, markÐreleaseÐrecapture, soldier proportions

Subterranean termites have signiÞcant economic impact worldwide. In the United States, subterranean termites cost consumers at least US$1.5 billion (Su and Scheffrahn 1990). Species of Reticulitermes, Coptotermes formosanus Shiraki, and Heterotermes aureus (Snyder), are among the most economically important pests of structures in the mainland United States (Su and Scheffrahn 1990, Baker and Bellamy 2006), yet there are relatively few studies of colony demographics or foraging characteristics. With the development of long-lasting dyes for marking foragers (Su et al. 1991) or ßuorescent paint markers (Forschler 1994), markÐrecapture and markÐreleaseÐrecapture methods have been used extensively to study and monitor subterranean termites worldwide, but not without controversy (Thorne et al. 1996, Evans et al. 1998). However, despite drawbacks, including wide variations in the estimated number of termites, BaroniUrbani et al. (1978) suggested this technique represents at least a practical approach for estimating social insect population sizes. In Arizona, H. aureus is the most economically important termite pest of structures. Control by destruc1 Corresponding author: Department of Entomology, University of Arizona, Tucson, AZ 85720 (e-mail: [email protected]). 2 Chemical Ecology of Forest Insects, PaciÞc Southwest Research Station, U.S. Department of AgricultureÐForest Service, P.O. Box 245, Berkeley, CA 94701; and Division of Organisms and the Environment, Department of Environmental Science, Policy, and Management, College of Natural Resources, 137 Mulford Hall 3114, University of California, Berkeley, CA 94720.

tion of foraging populations requires knowledge of foraging biology. However, our ability to understand the population and foraging dynamics of H. aureus is restricted by its cryptic nature. Direct and indirect methods of sampling H. aureus in undeveloped, native environments have produced asymmetrical results ranging from 23,000 to 300,000 individuals per colony on the same site near Tucson, AZ (Haverty et al. 1975, Haverty and Nutting 1975, Jones 1990b). We report here estimates of the foraging populations and foraging distances, as well as soldier proportions, of colonies of H. aureus associated with structures in three different locations in Tucson, AZ. We used a markÐreleaseÐrecapture protocol similar to that used to assist the development of baits for control of subterranean termites (Su and Scheffrahn 1994, Getty et al. 2000) and characterizations of cuticular hydrocarbons (Haverty et al. 1996) and soldier proportions to associate foraging groups within a colony. An understanding of the magnitude of the foraging distances and populations is key to effective deployment of baits for protection of structures in urban settings, as well as understanding the role H. aureus plays in natural systems. Materials and Methods Sites. Three structures located in Tucson, AZ, with active infestations of H. aureus were chosen for this study. None of the structures had received a termiticide application in the previous 5 yr. Site 1 is the

0022-0493/07/1381Ð1390$04.00/0 䉷 2007 Entomological Society of America

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Vol. 100, no. 4

Fig. 1. Diagram of collar deployment at site 1, the University of ArizonaÕs Environmental Research Laboratory (Tucson, AZ).

University of ArizonaÕs Environmental Research Laboratory located near the Tucson International Airport. This 70 m2, split-level structure, with a half basement, is made of slump block walls (Fig. 1). Site 2 is called the Shrimp House, and it is located on the West Agricultural Campus of the University of Arizona (Tucson, AZ). This concrete block structure covers 139.4 m2, and it was built 3.2 m below the soil surface with ⬇0.7 m above ground (Fig. 2). Site 3, the Olson residence, is a 337-m2 home with a standard ßoating slab, and it is constructed of slump blocks (Fig. 3). Colonies, Population Estimates, and Foraging Distances. Size and dispersion of foraging populations were estimated with markÐreleaseÐrecapture studies. Monitoring stations (collars) were placed at 3.3-m intervals around each structure. Collars consisted of 15.8-cm-long by 15.8-cm-diameter polyvinyl chloride pipe forced 2 mm into the ground. Within each collar we placed a 10- by 120-cm section of rolled cardboard (B ßute, SF Roll Corp., Tucson Container Corp., Tucson, AZ). A piece of 2.5-by 1.5- by 10-cm ash (Fraxinus sp.) was positioned in the center, and cardboard was wrapped around the wood and held in place with a rubber band. Once the rolled cardboard was placed inside the collar, a 16- by 16- by 1.5-cm concrete brick

paver was placed on top. Approximately 5 mo after the establishment of the collars, a tripleÐmarkÐrecapture program (Su et al. 1993) was used to delimit colonies and estimate the foraging populations and distances. In addition, Sentricon monitoring stations (Dow Agrosciences LLC, Indianapolis, IN) were placed equidistance or 3.3 m between collars, but they were used only for evaluating foraging distances when occupied by marked termites. Sentricon Termite Colony Elimination System is a Dow AgoSciences product developed for the commercial termite market for use by pest management professionals. Termites were captured, marked, released, and recaptured over a period of Þve consecutive weeks in the late summerÐfall 2000. The number of workers and soldiers was determined by direct counts of individuals. One collar with at least 200 termites was selected and force-fed Þlter paper (Whatman no. 1, Whatman, Maidstone, United Kingdom) with 0.1% (wt:wt) Nile Blue A (Sigma-Aldrich, St. Louis, MO) (Su et al. 1993, Forschler and Townsend 1996) in an 85-mm petri dish in complete darkness at 25⬚C for 7 d. After 7 d, blue termites were counted, and they were returned to the monitoring collar from which they had been collected (Su et al. 1993).

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BAKER AND HAVERTY: FORAGING POPULATIONS OF THE DESERT SUBTERRANEAN TERMITE

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Fig. 2. Diagram of collar deployment at site 2, the Shrimp House, West Agricultural Campus, University of Arizona (Tucson, AZ).

Collections were made every 7 d after the release of the marked termites, for 21 d. Termites were collected from all collars and brought back to the laboratory for sorting and counting. Termites found within a collar that contained marked termites at any time within the 21-d sampling period were considered nestmates. All foraging nestmates within these collars were fed dyed Þlter paper for another 7 d and released back into their corresponding location. The weighted mean model (WMM) was used to estimate termite foraging populations by counting the numbers of marked and unmarked termites collected and the number of marked termites released at each cycle (Begon 1979, Haverty et al. 2000). As a comparison, population estimates based on the Lincoln Index (LI) (Bailey 1951) were made using the Þrst markÐreleaseÐrecapture cycle. For the purposes of this article, we considered a colony to be foraging groups of H. aureus sharing interconnected galleries (Su and Scheffrahn 1996). Our deÞnition assumes that these foragers also are associated with other conspeciÞcs involved in cooperative rearing of offspring (Wilson 1971). The maximum foraging distance between collars used by a colony was determined by measuring (or calculating) the linear distance between the two connecting collars that are furthest apart. The minimum total foraging distance potentially traveled by members of a colony was computed as the sum of the linear dis-

tances between all possible pairs of collars occupied by the colony. These measurements assume foraging galleries between collars for sites 1 and 2 were along solid structure guidelines, such as block walls, whereas at site 3 it was calculated based on a straight line, and thus is a conservative estimate. Relationship of Foraging Groups by Quantification of Cuticular Hydrocarbon Mixtures. Termites were gathered from individual monitoring collars to characterize the cuticular hydrocarbons of each foraging group. Our hypothesis was that foraging groups from the same colony would have cuticular hydrocarbon mixtures that were quantitatively similar and that were quantitatively different from foraging groups that belonged to a different colony. To validate this methodology, we compared the cuticular hydrocarbon mixtures of foraging groups from the three sites, because we were certain that the sites shared no colonies in common. Termite samples were collected 2 or 6 mo after the markÐreleaseÐrecapture cycle, and they were brought to the laboratory at the University of Arizona, where the termites were separated from cardboard and any other debris. Samples of 50 Ð200 foragers (pseudergates or workers) were placed in separate vials, frozen, and then dried (Haverty et al. 1996). Once the termites were completely dry, specimens were placed in separate, labeled, tightly capped 20-ml scintillation

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Fig. 3. Diagram of collar deployment at site 3, the Olson residence (Tucson, AZ).

vials (Wheaton ScientiÞc, Millville, NJ), and they were shipped overnight to the USDAÐForest Service laboratory in Albany, CA. The hydrocarbons from each termite sample were extracted, characterized, and quantiÞed in the same manner as reported in Haverty et al. (1996). In the text, we use shorthand nomenclature to identify individual hydrocarbons or mixtures of hydrocarbons. This shorthand uses a descriptor for the location of methyl groups (X-me); the total number of carbons (CXX) in the hydrocarbon component, excluding the methyl branch(es); and the number of double bonds after a colon (CXX:Y). Thus, heptacosane becomes n-C27; 9-methylheptacosane becomes 9-meC27; 11,19-dimethylnonacosane becomes 11,19-dimeC29; and nonacosadiene becomes C29:2. Gas chromatographic-mass spectrometric peak areas were converted to percentages of the total hydrocarbon fraction. We tested the relationship among the foraging groups and sites by using cluster analysis of the cuticular hydrocarbon mixtures. The presence of coeluting compounds precluded exact quantiÞcation of many individual hydrocarbons; therefore, we used the percentage of each peak as the response variable. The Euclidean distance for the 12 foraging groups from the three sites was calculated using all hydrocarbons (R Development Core Team 2004).

Relationship of Foraging Groups by Examining Soldier Proportions. Numbers of soldier and worker termites in each collection were used to calculate the proportion of the total represented by soldiers. The statistical signiÞcance of the Þxed effects (sites 1, 2, and 3), sampling period (Þrst, second, or third sample), and group (collars with dyed termites or collars without dyed termites) were tested using the generalized linear mixed model at ␣ ⫽ 0.05 (SAS Institute 2002). Regression analyses using foraging groups from collars with and without dyed termites were conducted to test the slopes (i.e., soldier proportions) among sites and among foraging groups from collars with or without dyed termites at each site. Statistical signiÞcance between and/or among slopes was determined by constructing 95% conÞdence limits.

Results and Discussion Mark–Release–Recapture Studies. Both H. aureus and Gnathamitermes perplexus (Banks) (Termitidae) foragers were collected in collars at all three sites; however, the two species never occupied the same collar at the same time. In addition, G. perplexus foragers represented ⬍1.4% of the foraging termites collected at any site. They were easily distinguished from

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Summary of foragers released and recaptured for each of three cycles of mark–release–recapture at three sites in Tucson, AZ

Site

No. collars

No. collars with foragers

No. collars with marked foragers

Marked foragers releaseda

First recaptureb

Second recaptureb

Third recaptureb

1 2 3

16 39 30

7 23 16

7 8 10

782 ⫹ 4,170 371 ⫹ 1,422 273 ⫹ 3,000

4,498 (30) 3,290 (9) 13,557 (12)

1,325 (9) 3,584 (2) 7,959 (4)

49 (8) 654 (5) 2,419 (27)

a b

Number of marked foragers initially released ⫹ no. of foragers subsequently released. Total number of termites recovered with the number of marked termites in parentheses.

H. aureus and thus they were not included in any of the results. During this study, we collected and marked 11,230 H. aureus foragers in total, and we released 89.2% of them (10,018) back into their original collars. The return of the marked foragers was very low (Table 1). Because of the small return of marked foragers (ⱕ11 with a mean of 2.12 per occupied collar) in the collars, we decided to estimate the population two different ways: 1) include only the monitoring collars with marked termites assuming the other collars were occupied by a different colony or colonies, and 2) include all collars at the site as one colony assuming the collars without marked foragers did not receive them simply because of the small return of marked individuals (Table 1; Appendices 1Ð3). Site 1. Marked termites were initially released into collar 9; additional marked foragers were released 2 wk later into collars 8 Ð12 and 16 (Fig. 1; Appendix 1). One week after the release of marked termites, six of the seven collars that were occupied during the 3-wk sampling period had marked termites in them. The following week, six of the seven collars were occupied, but only three contained marked termites. During the third week, only two collars were occupied, but both collars had marked termites in them. Only one collar (16) furthest from the release point was consistently occupied and contained marked termites all 3 wk. All occupied collars at this site had marked termites at least once during the 3-wk sampling period. Nine collars were never occupied. Overall recapture rate of marked foragers was 47 of 4,952 released for a return of 0.94% (Table 1). Foraging populations were estimated to be 118,030 by the LI and 100,410 by the WMM (Table 2). Termites were collected from Sentricon stations; however, we did not include them in the estimates of Table 2. Population estimates based on Lincoln Index and weighted mean model and foraging distances for H. aureus colonies at three sites in Tucson, AZ

Site

Lincoln Index

Site 1 Site 2 Site 3

118,030 64,913 226,272

Site 1 Site 2 Site 3

118,030 98,797 307,284

Weighted mean model

Max distance (m)

Min total foraging distance (m)

Only collars with marked foragers 110,410 26 297 75,501 62 1,193 252,205 35 880 All collars with foragers 110,410 26 297 175,596 66 2,427 313,251 35 1,130

foraging populations because of the very small numbers collected (less than Þve). Nonetheless, marked foragers were found in Sentricon stations 1 and 8, and they were included in the calculation of foraging distances (Fig. 1; Table 2). The maximum foraging distance of 26 m and minimum of total foraging distance of 297 m (Table 2) were based on all collars and the two Sentricon stations that contained marked termites during at least one sampling period (Table 2; Appendix 1). Site 2. Marked foragers were initially released into collar 19; additional marked foragers were released 2 wk later into collars 20 and 37 (Fig. 2; Appendix 2). No termites, marked or unmarked, were ever recovered from the initial release point. One week after the release of marked termites only Þve of the 14 occupied collars had marked termites in them. The next week, none of the four collars originally occupied by marked foragers contained marked termites; only one collar (27) contained marked foragers. During the third week, only three collars (12, 17, and 23) contained marked termites. None of the collars was consistently occupied over the 3-wk sampling period. Of the 23 occupied collars, only eight ever contained marked termites (Table 1). Sixteen of the total 39 collars were never occupied at this site during the 3-wk sampling period. Because not all of the occupied collars contained marked foragers during this sampling period, we would infer that site 2, Shrimp House, was “infested” by at least two colonies, if we were to assume random foraging among the collars and uniform mixing of the marked termites (Su et al. 1984). However, Jones (1990a) inferred that mixing of marked foragers of H. aureus might not be uniform in a natural setting; thus, the assumption that marked H. aureus foragers would mix uniformly around structures is also doubtful. Because the return of marked foragers was so low, we hesitate to assume uniform mixing of marked foragers among the collars. Therefore, it is not unreasonable to assume that all of the occupied collars were used by only one colony. Only 16 marked foragers were recovered of 1,793 released, for a return of 0.89% (Table 1). If we were to consider only the collars with marked foragers, estimated foraging population was 64,913 by the LI and 75,501 by the WMM, with a maximum foraging distance of 62 m and a minimum total foraging distance of 1,193 m (Table 2). However, if we were to include all of the collars with termites in them, the foraging population estimate would be 98,797 by the LI and 175,596 by the WMM, with a maximum distance be-

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tween monitoring collars of 66 m and a minimum total foraging distance of 2,427 m (Table 2). Site 3. Marked foragers were initially released into collar 19; additional marked termites were released 2 wk later into collars 15, 18, 20, and 21 (Fig. 3; Appendix 3). No termites, marked or unmarked, were ever recovered from the initial release point. One week after the release of marked termites only four of the 14 occupied collars contained marked termites in them. The next week, none of the four collars originally occupied by marked foragers contained marked individuals. Moreover, two of the four stations were unoccupied. However, 10 previously occupied collars, in addition to one previously unoccupied collar, contained foragers; only three contained marked foragers. During the third week after release of marked termites, only nine collars were occupied; six contained marked termites. Only four of the collars were consistently occupied over the 3-wk sampling period. All but one of the occupied collars were occupied at least twice. Of the 16 collars occupied by foragers, only 10 ever contained marked termites (Table 1; Appendix 3). Because not all of the occupied collars were visited by marked foragers during the 3-wk sampling period, we would infer that the site 3 was “infested” by at least two colonies, if we were to assume random foraging and uniform mixing of the marked termites (Su et al. 1984). However, as with the site 2, the return of marked termites was so low, we hesitate to make an emphatic inference about the number of colonies. Only 43 marked foragers were recovered of 3,273 released for a return of 1.31% (Table 1). If we were to consider only the collars with marked foragers the estimated foraging population was 226,272 by the LI, and 252,205 by the WMM, with a maximum foraging distance of 35 m and a minimum total foraging distance of 880 m (Table 2). Based on the number of marked foragers recovered, it is not unreasonable to assume that we should include all of the collars. Thus, the foraging population estimate would be 307,284 by the LI and 313,251 by the WMM, with a maximum distance between monitoring collars of 35 m and a minimum total foraging distance of 1,130 m (Table 2). Colonies per Structure Inferred from Characterization of Cuticular Hydrocarbons. We sampled 12 foraging groups of H. aureus, three groups from site 1, Þve groups from site 2, and four groups from the site 3, albeit 2Ð 6 mo after population sampling. The cuticular hydrocarbon mixture of H. aureus is composed of n-alkanes, dienes, 2/4-, 3-, 5-, and internally branched monomethyl alkanes, and various internally branched dimethylalkanes, and 5,19-dimeC27. The most abundant components were 9-meC27, 9-meC29 and 11,19-dimeC29. All 12 samples were qualitatively identical, i.e., all samples had the same hydrocarbons. There were quantitative differences in the cuticular hydrocarbon mixtures among the various collars that we sampled. Cuticular hydrocarbon mixtures were more similar among collars from the same site than among those from different sites, with one exception: site 1, collar 7 (Fig. 4). Thus, all of the site 2 samples were more

Vol. 100, no. 4

Fig. 4. Dendrogram from cluster analysis based on Euclidian distance of hydrocarbons extracted from 12 foraging groups collected from sites 1, 2, and 3.

similar to one another than they were to those from site 1 or site 3. The same is true for sites 1 and 3. We collected cuticular hydrocarbon samples from collars that were not previously occupied by marked foragers during the markÐreleaseÐrecapture sampling, primarily because termites were present when we sampled 2 or 6 mo later. Because of the similarity of the cuticular hydrocarbon mixtures of these to the others from the same site that were occupied during the 3-wk sampling period, we are conÞdent that they are from the same colonies. However, the cuticular hydrocarbons of the foragers collected in collar 7 from site 1 6 mo after population sampling was completed are so different from the others at the same site that we concluded that two colonies, rather than one, “infested” site 1. This is the Þrst attempt to use the quantities of cuticular hydrocarabons to connect or associate foraging groups of the same species from the same general area. Our results are very encouraging. Our inference would be stronger if corroborated with agonistic bioassays and microsatellite analyses. These latter two tests were not part of the original protocol. These results do, however, have positive implications for estimating colony populations and foraging distance. Colonies per Structure Inferred from Proportion of Soldiers. Only the site Þxed effect resulted in a statistically signiÞcant difference (F2,71 ⫽ 5.82; P ⬍ 0.005) in proportion of soldiers. Thus, each site had a proportion of soldiers that was statistically signiÞcant from each of the others; sampling period and presence or absence of marked termites did not affect soldier proportions. The mean proportion of soldiers at the site 1 was 0.135 (SE ⫽ 0.038), whereas samples at sites 2 and 3 had mean proportions of 0.069 (SE ⫽ 0.009) and 0.040 (SE ⫽ 0.009), respectively. At site 1, the correlation between number of soldiers and the total number of foragers was highly signiÞcant (r2 ⫽ 0.88, P ⬍ 0.005; n ⫽ 14). Because all collars sampled contained marked termites during at

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least one sampling period, we did not compare the regression of collars with and without marked foragers at this site. At site 2, the correlation between the number of soldiers and the total number of foragers was highly signiÞcant (r2 ⫽ 0.86, P ⬍ 0.005; n ⫽ 34). At this site, the regression of foraging groups with dyed termites was not statistically different from that of foraging groups without dyed termites (Y ⫽ 4.19 ⫹ 0.052X, r2 ⫽ 0.93, P ⬍ 0.005 [n ⫽ 13] versus Y ⫽ 1.51 ⫹ 0.050X, r2 ⫽ 0.78, P ⬍ 0.005 [n ⫽ 21]). Therefore, we feel it is reasonable to assume that the foragers in all of the collars at this site were from the same colony, because the soldier proportions are so similar between the two groups and the return of dyed termites was low, such that dyed termites might not have found their way to all collars sampled. At site 3, the correlation between the number of soldiers and the total number of foragers was highly signiÞcant (r2 ⫽ 0.64, P ⬍ 0.005; n ⫽ 34). At this site, the regression of foraging groups with dyed termites was not statistically different from that of foraging groups without dyed termites (Y ⫽ 7.16 ⫹ 0.022X, r2 ⫽ 0.61, P ⬍ 0.005 [n ⫽ 22[ versus Y ⫽ 3.51 ⫹ 0.026X, r2 ⫽ 0.80, P ⬍ 0.005 [n ⫽ 12]). As with site 2, we feel it is reasonable to assume that the foragers in all monitoring collars were from the same colony for the same reasons. This is a signiÞcant deviation from the hypothesis presented by Haverty (1977) that each termite species has a Þxed proportion of soldiers. Conditions at each site, whether biological or physical, resulted in different proportions of soldiers, as well as soldier proportions higher than those previously reported for H. aureus (Nutting et al. 1973; Haverty and Nutting 1975). However, signiÞcant differences in soldier proportions among colonies of the same species should be expected. Haverty (1979) and Haverty and Howard (1981) demonstrated that soldier development in orphaned groups of workers of the rhinotermitid species C. formosanus and Reticulitermes flavipes (Kollar) was signiÞcantly different among colonies within each of these species. Oster and Wilson (1978) theorized that caste ratios should be ßexible in mature colonies to accommodate environmental variations. However, at the time of their publication, they had not seen a systematic study relating soldier/worker ratios to nest structure or features of the environment. Thus, we conclude that it is likely that all collars sampled at each site contained foragers from the same colony. The reason(s) for the signiÞcant differences in soldier proportions among sites is unknown. At site 1, all termites collected in the collars during the 3-wk sampling period were, without question, from a single colony, because each collar that contained termites contained dyed termites at one time or another. At both sites 2 and 3, it is possible that more than one colony was present, because not all of the collars that were visited by foragers contained dyed termites (Table 1). However, the evidence from characterization of the cuticular hydrocarbons and soldier proportions strongly suggest that each site was occu-

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pied by only one colony each. Regardless, we reported population estimates and foraging distances for sites 2 and 3 by using both assumptions (Table 2). Our population estimates of H. aureus for the three sites, based on the LI and the WMM, seem to fall within the ranges reported by Haverty and Nutting (1975) and Jones (1990b), despite the presence of the structures. All of the previous estimates of H. aureus Þeld populations and foraging territories (Haverty and Nutting 1975; Jones and Nutting, 1989; Jones 1990a,b) were made under native desert conditions. In comparison with other estimates of subterranean termite foraging populations in North America, our data, and those of others (Jones 1990b), support an equivalent range in numbers of termites/colony from 5,000 to 500,000 foragers of Reticuliterms spp. (Forschler and Townsend 1996, Haverty et al. 2000). However, colonies of the Formosan subterannean termite, C. formosanus, can range from 1 to 6 million (Su and Scheffrahn 1988, Grace et al. 1996). Of the 10,018 termites that were dyed blue, only 106 were recaptured from all three sites for a 1.06% return. This is considerably lower that the 2.49% reported by Jones (1990b) under native desert conditions using Sudan Red, whereas Forschler and Townsend (1996), Thorne et al. (1996), and Haverty et al. (2000) had returns of 6.15, 6.67, and 5.39%, respectively, for Reticuliterms spp. Sornnuwat et al. (1996) reported 1.83% return of marked termites from a foraging populations of Coptotermes gestroi Wasmann in an urban area, a proportion more reßective of our results. Haverty et al. (1974) reported H. aureus foraging moderately high in late summer and early fall responding to the increase in rain and favorable soil temperatures during this period. In general, we collected the greatest number of foragers during the Þrst collection, with the third collection substantially lower. However the third collection gave the highest percentage of marked termites. Continual disturbance probably caused this decrease in the number of foragers captured. Maximum foraging distance for the three sites ranged from 26 to 62 m, and it is likely a consequence of the greatest distance of the collars. Minimum total foraging distances between sites varied widely from 297 to 2,427 m. Thus, the size of the occupied structure and the number of occupied collars greatly affects this metric. The greater distances traveled by H. aureus foragers at the site 2 were based on a 3.2-m-deep basement and our assumption that the termites traveled along the physical guides of the slump block wall, not in a straight line from collar to collar. Whereas at site 3, we assumed a straight line between collars because of a ßoating slab only 10 cm in depth. Estimates of foraging populations of subterranean termites are commonly made worldwide by using markÐreleaseÐrecapture techniques. There is, however, considerable debate and controversy over the accuracy, validity, and usefulness of these estimates (Baroni-Urbani et al. 1978, Thorne et al. 1996, Evans et al. 1998). We made our estimates of foraging populations of H. aureus with knowledge and appreciation of both sides of the argument and in-

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cluded our raw data (Appendices 1Ð3) so that others can draw their own conclusions. QuantiÞcation of foraging distances, range, area or territory also can also debated. The concept of foraging range seems to be a more appropriate descriptor of where termites are working than an arbitrary foraging territory (Thorne 1998). Constructing a polygon around the collars or monitoring stations occupied or used by a colony includes a great deal of real estate that the termites are not necessarily using or defending. In our study, we have chosen to use the metric minimum total foraging distance proposed by Haverty et al. (2000) as a variance of foraging range. This is the distance potentially traveled by members of a colony, and it was computed as the sum of the linear distances between all possible pairs of collars occupied and defended by a colony. We know that the tunneling galleries do not follow straight lines, at the same depth in the soil, between collars or other food sources. Rather these galleries are a vast network of interconnected tunnels and chambers within the soil, at various depths, and they avoid various obstacles, interspersed among food sources. We recognize that the density of collars could affect this parameter. Furthermore, it would be naieve to state that all pairs of collars are connected with their own separate tunnel; some collars could be connected in series that would make the total foraging distance smaller. Nonetheless, minimum total foraging distance provides an additional metric for a more complete picture of overall colony size for comparing colonies of the same, or different, species of termites, and it does not include an area or volume of soil that termites do not use. The results of this study continue to support the concept that estimates of foraging populations based on markÐreleaseÐrecapture are somewhat controversial (Thorne et al. 1996, Evans et al. 1998); we did not Þnd evidence that marked foragers mix equally among foraging sites (collars) occupied by the same colony. However, we feel that markÐreleaseÐrecapture does retain a practical use for estimating foraging populations of subterranean termites (Baroni-Urbani et al. 1978, Su and Scheffrahn 1996, Tsunoda et al. 1998). Still foraging population estimates of H. aureus seem to be similar whether around structures or in native, undisturbed deserts. Maximum foraging distance is probably a function of the size of the foraging “territory” or “area,” whereas the minimum total foraging distances are strongly affected by the number of foraging sites (in our case collars); the more available sites or the greater their density, the minimum total foraging distance will be larger. Although, it is still unclear whether the structures affect the dispersion of foraging sites and can make the total foraging distances larger because the structure itself can exclude a signiÞcant portion of the territory (in all three dimensions), but it does provide guides (and gaps) for foraging galleries.

Vol. 100, no. 4 Acknowledgments

We thank Ruben Marchosky for technical assistance with the data; L. J. Nelson for technical assistance characterizing the cuticular hydrocarbons of H. aureus; J. A. Baldwin for assistance with the cluster and regression analyses; and M. K. Rust, B. T. Forschler, C. Schal, and three anonymous reviewers for helpful reviews of an earlier draft of this manuscript. This research was made possible, in part, by donations from Dow AgroSciences.

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in cuticular hydrocarbons of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). J. Chem. Ecol. 22: 1813Ð1843. 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. Jones, S. C. 1990a. Delineation of Heterotermes aureus (Isoptera: Rhinotermitidae) foraging territories in a Sonoran Desert grassland. Environ. Entomol. 19: 1047Ð1054. Jones, S. C. 1990b. Colony size of the desert subterranean termite Heterotermes aureus (Isoptera: Rhinotermitidae). Southwest. Nat. 35: 285Ð291. Jones, S. C., and W. L. Nutting. 1989. Foraging ecology of subterranean termites in the Sonoran Desert, pp. 79 Ð106. In J. O. Schimdt [ed.], Interactions among plants and animals in the western deserts. University of New Mexico Press, Albuquerque, NM. Nutting, W. L., M. I. Haverty, and J. P. La Fage. 1973. Foraging behavior of two species of subterranean termites in the Sonoran Desert of Arizona, pp. 298 Ð301. In Proceedings, 7th International Congress of the International Union for the Study of Social Insects, 10 Ð15 September 1973, London, United Kingdom. Birkha¨user, Basel, Switzerland. Oster, G. F., and E. O. Wilson. 1978. Caste and ecology in the social insects. Princeton University Press, Princeton, NJ. R Development Core Team. 2004. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org). SAS Institute. 2002. SAS/STAT 2002Ð2003. Software, version 9.1.3 of the SAS System for Windows. SAS Institute, Cary, NC. Sornnuwat, Y., K. Tsunoda, T. Yoshimura, M. Takahashi, and C. Vongkaluang. 1996. Foraging populations of Coptotermes gestroi (Isoptera: Rhinotermitidae) in an urban area. J. Econ. Entomol. 89: 1485Ð1490. Su, N.-Y., and R. H. Scheffrahn. 1988. Foraging population and territory of the Formosan subterranean termite

Appendix 1. Termites collected for each of three dates at site 1, the Environmental Research Laboratory Collara 8 9 10 11 12 15 16 Totals

18 Aug. 2000b 243 (4) 18 (1) 467 (3) 675 (10) 300 (1) 2,825 (11) 4,498 (30)

25 Aug. 2000b

1 Sept. 2000b

219 (0) 51 (5) 265 (0) 47 (0) 157 (3) 586 (1) 1,325 (9)

16 (4) 33 (4) 49 (8)

On 11 August 2000, 782 marked termites were released into collar 9. On 25 August 2000, 4170 marked termites were released into collars 8 Ð12 and 16. a Collars 1Ð7, 13, and 14 were never occupied by foragers. b Total number of termites recovered with the number of marked termites in parentheses.

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(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. Su, N.-Y., and R. H. Scheffrahn. 1994. Field evaluation of hexaßumuron bait for population suppression of subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 87: 389 Ð397. Su, N.-Y., and R. H. Scheffrahn. 1996. A review of the evaluation criteria for bait-toxicant efÞcacy against Þeld colonies of subterranean termites (Isoptera). Sociobiology 28: 521Ð530. Su, N.-Y., P. M. Ban, and R. H. Scheffrahn. 1991. Evaluation of twelve dye markers for population studies of the eastern and Formosan subterranean termites (Isoptera: Rhinotermitidae). Sociobiology 19: 349 Ð362. Su, N.-Y., P. M. Ban, and R. H. Scheffrahn. 1993. Foraging populations and territories of the eastern subterranean termite (Isoptera: Rhinotermitidae) in southeastern Florida. Environ. Entomol. 22: 1113Ð1117. Su, N.-Y., M. Tamashiro, J. Yates, and M. I. Haverty. 1984. Foraging behavior of the Formosan subterranean termite (Isoptera: Rhinotermitidae). Environ. Entomol. 13: 1466 Ð 1470. Thorne, B. L. 1998. Biology of subterranean termites in the genus Reticulitermes. Part I, pp. 1Ð30. In NPCA research report on subterranean termites. National Pest Control Association, Dunn Loring, VA. Thorne, B. L., E. Russek-Cohen, B. T. Forschler, N. L. Breisch, and J.F.A. Traniello. 1996. Evaluation of markÐ releaseÐrecapture methods for estimating forager population size of subterranean termite (Isoptera: Rhinotermitidae) colonies. Environ. Entomol. 25: 938 Ð951. Tsunoda, K., H. Matsuoka, and T. Yoshimura. 1998. Colony elimination of Reticulitermes speratus (Isoptera: Rhinotermitidae) by bait application and the effect of foraging territory. J. Econ. Entomol. 91: 1383Ð1386. Wilson, E. O. 1971. The insect societies. The Belknap Press of Harvard University Press, Cambridge, MA. Received 22 September 2006; accepted 27 April 2007.

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Appendix 2. Termites collected for each of three dates at Site 2, the Shrimp House

Appendix 3. Termites collected for each of three dates at site 3, the Olson residence

Collara

21 Sept. 2000b

Collara

200 (0) 18 (0)

1 5 7 10 11 15 16 17 18 20 21 25 27 28 29 30 Totals

7 8 9 11 12 13 14 16 17 18 19 20 22 23 24 25 26 27 29 30 33 35 37 Total

7 Sept. 2000b

14 Sept. 2000b

240 (0) 21 (1)

26 (0) 94 (3) 56 (0) 159 (0) 27 (3) 64 (2) 544 (2) 81 (0)

105 (0) 0 (0) 34 (0) 40 (0) 789 (0) 230 (0)

306 (0) 86 (0) 125 (0) 172 (0) 1,398 (1) 3,290 (9)

18 (1)

25 (0) 124 (0) 233 (2) 876 (0) 1,066 (0) 62 (0) 3,584 (2)

87 (1) 1 (0)

127 (0) 83 (0)

654 (5)

On 31 August 2000, 371 marked termites were released into collar 19. On 14 September 2000, 1422 marked termites were released into collars 20 and 37. a Collars 1Ð 6, 10, 15, 16, 21, 28, 31Ð32, 34, and 38 Ð39 were never occupied by foragers. b Total number of termites recovered with the number of marked termites in parentheses.

25 Sept. 2000b 988 (0) 3,827 (0) 1,703 (0) 455 (0) 1,411 (1) 1,027 (0) 77 (0) 266 (4) 1,595 (6) 578 (1) 534 (0) 107 (0) 828 (0) 111 (0) 13,507 (12)

2 Oct. 2000b 645 (0) 1,389 (0) 405 (1) 651 (2) 1,010 (0) 1,116 (0) 285 (0) 281 (0)

9 Oct. 2000b 226 (0) 318 (0) 216 (2) 265 (4)

15 (5) 477 (0) 27 (7) 289 (7) 453 (0) 1,267 (1) 7,979 (4)

43 (0) 1,020 (2) 2,419 (27)

On 18 September 2000, 273 marked termites were released into collar 19. On 2 October 2000, 3,000 marked termites were released into collars 15, 18, 20, and 21. a Collars 2Ð 4, 6, 8 Ð9, 12Ð14, 22Ð24, and 26 were never occupied by foragers. b Total number of termites recovered with the number of marked termites in parentheses.