- Email: [email protected]
Behavioral variation among tunnelers in the Formosan subterranean termite
Journal of Asia-Pacific Entomology 13 (2010) 45–49
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j a p e
Behavioral variation among tunnelers in the Formosan subterranean termite Paul Bardunias ⁎, Nan-Yao Su, Rou-Ling Yang Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, 3205 College Avenue, Fort Lauderdale, FL 33314, USA
a r t i c l e
i n f o
Article history: Received 27 July 2009 Revised 30 October 2009 Accepted 4 November 2009 Keywords: Key individual Excavation Tunnel Division of labor Coptotermes formosanus
a b s t r a c t Division of labor is a common feature of insect societies and has been theorized to account for much of their success. Asymmetries in the work of individuals, whose aggregate labor results in the completion of a task, can lead to the emergence of key individuals that dominate or govern the task. Coptotermes formosanus Shiraki excavate in a series of alternating workers whose efforts combine not only to elongate tunnels, but also to guide the direction of propagation. When groups of 100 termites were presented with a single tunnel, only ∼ 16% of termites entered. Of those that entered, the level of excavation was not uniform, with 20.6% of termites responsible for over half of the total excavation. These termites, a small percentage of the total available workforce, act as key individuals, producing the majority of labor and possibly guiding the efforts of others. An examination of the excavation patterns of individuals shows that some individuals excavate sporadically, but at a very high rate (number of excavation events per time). By focusing their effort over a short period, these highly active individuals may influence the orientation of a tunnel and the formation of branches to a degree out of proportion to the total amount of digging they engage in. © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2009 Published by Elsevier B.V. All rights reserved.
The benefit of task specialization and division of labor was perhaps best described by Xenophon, a student of Socrates, in one of the earliest descriptions of the process, “…he who devotes himself to a very highly specialized line of work is bound to do it in the best possible manner.” Division of labor is a major factor in the success of social insects, thought to increase the efficiency of the large workforces of colonies (Oster and Wilson, 1978). Often this division of labor is reflected in worker polymorphism or temporal polyethism, but a more fluid system of task specialization among less specialized individuals is seen as well (Robinson, 1992). Most studies emphasized the differences between task-groups, while minimizing or ignoring variation within them (Robson and Traniello, 1999). Groups may not be uniform in their task performance, and many individuals that could partake in tasks appear to do no work (Herbers, 1983; Evans, 2006; Dornhaus et al., 2008). Conversely, elite individuals (Hölldobler and Wilson, 1990) or key individuals (Robson and Traniello, 1999) perform a disproportionate amount of labor. Robson and Traniello (1999) proposed three types of key individuals: catalysts, performers, and organizers. Performers are simply individuals who are highly active and account for a disproportionate amount of labor on any task. Catalysts stimulate others to activity through their actions, and organizers serve to initiate labor and maintain group cohesion throughout the task. The presence of key individuals results in their
⁎ Corresponding author. E-mail address: paulmb@ufl.edu (P. Bardunias).
behavioral idiosyncrasies being over-represented in the final work product. One task that termites carry out as groups is the excavation of tunnels. Coptotermes formosanus Shiraki excavate tunnels by combining their efforts as members of a group which removes soil from the tunnel in rotation (Bardunias and Su, 2009a, 2010). Recently, Yang et al. (2009) demonstrated that termites in excavation groups that were introduced to experimental arenas did not perform equal amounts of work. Understanding how termites apportion the total work on a task among individuals is important to our understanding of the evolution of division of labor (Robson and Traniello, 1999). Alternatively, if our goal is to understand the mechanics of tunnel excavation, then the manner in which individuals combine their efforts over a limited time-frame, their place and frequency of occurrence in the rotation of excavators is more important than the overall duration of labor. In situations where a key individual is responsible for choosing a prey item (Robson and Traniello, 1998) or a new nest site (Möglich and Hölldobler, 1975), the ability for a single key individual's actions to shape the outcome of task is obvious. Termites in a tunneling-group alternate their labor at a digging site, each individual working as part of a rotation of individuals who work in series (Bardunias and Su, 2009a, 2010). This will tend to dampen the influence of any single termite's idiosyncratic behavior. For example, termites tunnel along internally generated vectors and tunnel headings reflect a consensus of the orientation vectors of the working group (Bardunias and Su, 2009a). The reliance on multiple individuals to work together to generate tunnel headings may act to mitigate individual errors in path
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2009 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.aspen.2009.11.002
46
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
integration through the “many wrongs principle” (Walraff, 1978, Simons, 2004). The orientation vectors on individuals may drift away from their initial movement vector, but they will not all err in the same direction or by the same magnitude. Thus, if many individuals work in union, the resulting vector is more likely to correspond to the original vector. If key individuals dominate excavation, then the homogenizing effect of sampling the orientation vectors of many excavators is reduced. Termites are also known to respond to depressions in tunnel walls by excavating at the site (Lee et al., 2008; Bardunias and Su, 2009b). Repeated excavation by an individual at a preferred site along the tunnel wall may be enough to stimulate others to dig there as well, leading to branch formation. In order to characterize the workforce that is responsible for tunnel excavation we re-examined the asymmetry in excavation shown by Yang et al. (2009) by counting the actual occurrence of excavation events rather than the time on task. We sought to determine if all termites with access to a tunnel opening take the first step in tunneling by entering the tunnel. Of those termites that did enter the tunnel, we determined if they shared equally in the excavation process. Most importantly, we gauged the potential for any single excavator's behavior to disproportionately shape the resultant tunnel's form or heading by determining if termites excavate at a uniform rate (excavation/time).
between a pair of plastic spacers forming a tunnel 2 cm directly away from the introduction point, then the spacers forced the termites to turn 90° and travel another 2 cm (Fig. 1c). Termites respond to this forced turn by excavating a curved tunnel (Fig. 1d) in the opposite direction when they were free of the spacers and allowed to tunnel freely once more (Bardunias and Su, 2009a). A curved tunnel allows the maximum length of tunnel to fit into a video frame and the termites to be filmed at maximum magnification. Upon debouching from this guided channel, termites then tunneled freely. Once the tunnel tip advanced beyond the guided channel, tunneling activity was recorded at room temperature (26 °C) and room lighting for 1 h with a video camcorder (Sony DVHandycam, Tokyo, Japan) mounted above the arena. Entering the tunnel
Methods
The first step in an individual termite's joining the group of excavators in an existing tunnel is simply entering the tunnel from the introduction chamber. In each trial the identity of every termite entering the tunnel over the 1 h period was recorded. The average of the percentages of termites entering the tunnel among trials was determined. The number of termites entering the tunnel in ten trials was compared with the expectation that all 90 potential excavators would enter the tunnel in each trial via chi-square analysis at α = 0.05 (SAS Institute, 1985).
Study subjects
Excavation
Individuals of C. formosanus were collected from two field colonies in Broward County, FL, by using the methodology of Su and Scheffrahn (1986). They were stored at 27 ± 2 °C in plastic boxes with thin, moist wood chips. Ten groups, five from each colony, of 100 termites, made up of 90 potential excavators of at least 3rd instar and 10 soldiers, were created for 10 experimental trials. All 100 termites were individually marked with a unique one- and two-dot color scheme of 12 colors of enamel paint (Testor Corp., Rockford, IL) on their dorsal abdomen. Horizontal arenas consisted of two sheets of transparent Plexiglas (24 by 24 cm2), with four Plexiglas spacers (2 × 24 by 4 by 0.2 cm3, and 2 × 20 by 4 by 0.2 cm3) between the outer margins. Sifted sand (150– 500 μm sieves, Play Sand Bonsal, Miami, FL) was moistened with deionized water ≈ 7% by weight. A 15 ml cryogenic vial (Nalge Nunc International, Rochester, NY) was used as an introduction chamber (Fig. 1a, 3 cm diameter by 4 cm height). This was connected to the arena via a 6 cm, 3 mm diameter, tunnel bored through a Plexiglas coupling (Fig. 1b). Termites were initially constrained to excavate
The contribution of each termite that entered a tunnel to the total labor that went into tunnel excavation was determined. Over the 1 h experimental period, all of the excavation events performed by each termite in a trial were tallied. In order to determine if all termites contributed equally to the tunnel excavation, the number of excavation events performed by each individual within a trial was compared to the mean number of excavations performed by all termites within that trial via chi-square analysis at α = 0.05 (SAS Institute 1985). The proportion of the tunnel excavation performed by each participant within a trial was calculated by dividing the number of excavation events performed by the individual by the total number of excavation in the trial. The result was converted to a percentage and these were binned in 5% intervals from 0% to 35%. The mean percentage of individuals whose contribution to overall excavation of the tunnel in their trial fell into each of these 5% intervals was compared via Kruskal–Wallis test (SAS Institute 1985). Significant differences among the mean percentages of individuals whose proportion of excavation fell within each of the binned intervals from 0% to 35% were separated by a Dunn's post-hoc test at an adjusted α of 0.001 (0.05/42). Temporal pattern of excavation
Fig. 1. The experimental arenas consisted of sifted sand between two sheets of transparent Plexiglas (24 by 24 cm2). (a) 15 ml cryogenic vial was used as an introduction chamber. (b) A 4 cm, 3 mm diameter Plexiglas coupling connected the introduction chamber to the arena. (c) Termites were initially constrained to excavate between a pair of plastic spacers forming a tunnel 3 cm directly away from the introduction point, then the spacers forced the termites to turn 90° and travel another 3 cm. (d) The forced turn results in the excavation of a curved tunnel.
To examine the temporal pattern of an individual's excavation we plotted each individual termite's excavation over the total time of the trial. Even if termites contributed an equal number of excavation events over the course of the trial, the rate (number of excavations/ time) at which they work may be different. The time of the initiation of excavation was recorded when a termite initiated excavation by grasping sand with its maxilla. The number of excavation events that occurred within a 1 min period was recorded over the 1 h duration of the trial for each excavator in the 10 trials. Plotting the number of excavation events carried out by each individual in a trial results in a graph that is too cluttered to be easily understood. For the sake of clarity, we plotted the excavation for 1 min intervals from 0 to 60 min of only the top excavators in each trial: the minimum number of individuals whose labor accounted for at least 50% of the total
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
47
excavation. In addition, because there could be long periods of inactivity, we calculated a rate of excavation for these top excavators as the number of excavation events occurring in any 1 min period in which they performed an excavation. By examining the pattern of every individual's excavation each trial we determined if termites ever performed an uninterrupted series of excavation events rather than excavating in alternation with other termites. Results Entering the tunnel Not all of the 90 potential excavators with access to the tunnel entered it. The number of potential excavators that entered over the 1 h period of recording ranged among trials from 21 to 9, with an average of 14.5 ± 3.7 (mean ± SD). That is a mean percentage of 15.7 ± 4% of all potential excavators entering the tunnels, which differed significantly from the expectation that all termites would enter the tunnel (χ2 = 634.71, df = 9, P b 0.0001). Excavation The termites entering the tunnel did not contribute equally to the excavation of the tunnel (Table 1). In each trial some individuals performed at a much higher level than did others, their efforts ranging from 0 to 56 excavation events in any trial during the 1 h period. The percentage of individuals whose labor fell into each of the 5% excavation intervals from 0% to 35% within their trial was significantly different according to a Kruskal–Wallis test (χ2 = 45.276, df = 6, P b 0.0001). The mean percentages of termites in the 5%, 10%, 15%, and 20% excavation intervals were all significantly different from the other intervals (Fig. 2), but the 25% excavation interval did not differ significantly from the 30%, or the 30% from the 35%. Few termites (5.5%) entered the tunnel, yet failed to excavate any soil. Of those termites that entered the tunnel, 57.9% performed 5% or less and 84.8% performed 15% or less of the excavation in their tunnels. The effort of top excavators in any tunnel still accounted for less than a third of the total tunnel excavation. Small groups of individuals, 3 ± 0.9 (mean ± SD), in each tunnel whose aggregate excavation accounted for at least 50% of the total work on that tunnel represented 20.6% of all of the termites which entered tunnels. This drops to only 3.3% of the total number of termites if we include the majority that never entered the tunnels. Temporal pattern of excavation The number of excavation events in each 1 min interval, from 0 to 60 min, for each of the top excavators in a trial is plotted for all ten
Table 1 A comparison of the number of excavation events performed by each of the termites that entered a tunnel within a trial compared with the mean number of excavation events for all termites in that trial. Trial
n
Mean ± SE
1 2 3 4 5 6 7 8 9 10
21 13 18 17 10 13 9 17 13 14
6.714 ± 1.313a 9.846 ± 2.991a 7.556 ± 1.873a 10.529 ± 2.749a 17.5 ± 6.32a 12.307 ± 3.663a 12.444 ± 3.44a 12.764 ± 3.804a 11.153 ± 4.102a 12.857 ± 4.192a
a Means that are significantly different at α = 0.05 (chi-square analysis, SAS Institute 1985).
Fig. 2. The percentage of total tunnel excavation in trials, binned in 5% increments, and the mean percentage of termites (± SE) whose relative excavation effort falls within each. Bars bearing different letters are significantly different at α = 0.001 (Kruskal– Wallis test; Dunn's post-hoc test).
trials in Fig. 3. The temporal pattern of excavation for highly active individuals varied between individuals. Some termites excavated steadily over time (Fig. 3I, b and c), while others excavated in short bursts of activity followed by an extended absence from the tunnel (Fig. 3I, a). The mean rate (number of excavations/time) of excavation for the 876 excavation events that were recorded in any minute during the 10 trials was 1.3 ± 0.8 excavation events (mean ± SD) varying from a minimum mean of 1 event in any minute where excavation occurred (Fig. 3A, a) to a mean of 3.4 ± 2.1 per minute (Fig. 3I, a). The maximum number of excavation events in any minute was 7, one every 8.57 s. Looking at all of the excavation events carried out by all workers in a trial shows that at a high excavation rate (number of excavations/time) an individual may perform a series of uninterrupted excavations, whereas when the excavation rate is as low as once per minute, excavation always occurred as a part of a group of termites alternating their digging among them.
Discussion Tunnel excavation in termites is a group effort, but not all individuals contribute equally to the creation of tunnels. Without knowledge of the full repertoire of behaviors that can be conducted by termites in the introduction chamber, we cannot know if they were simply not motivated to enter the tunnel to excavate or if instead they were performing another task. Even among termites that did enter the tunnel excavation was not uniform, with a small minority of termites responsible for most of the excavation. The few termites that dominated excavation in each trial may be considered key individuals, but defining their role in the organization of labor within the three categories (organizer, catalyst, and performer) defined by Robson and Traniello (1999) will require further research. They clearly performed the task of excavation at high rate relative to the other termites. In this way they are similar to “performers” because, within the period of their peak excavation, they are carrying out the majority of excavation. Their presence could be inhibiting other excavators by physically blocking access to the tunnel end, but, through their rapid excavation, they may be acting as “catalysts,” leading others to greater effort. Similarities between the group excavation process in termites and ants (Chen, 1937, but see Sudd, 1972) suggest that this may occur. Future studies should include the removal of these highly active individuals to determine if the overall rate of excavation decreases in their absence, as it would
48
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
Fig. 3. Excavation schedules over the 1 h experimental period for the top excavators, defined as the minimum number whose labor accounted for at least 50% of total excavation. Each point represents the number of excavation events occurring within a 1 min period. The symbols for each line correspond to individuals a through e, assigned in no particular order.
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
were they true “performers,” or if the excavation effort of other termites decreases in their absence, indicating a catalytic function. An intriguing possibility is that the highly active excavators are also acting in an organizational capacity akin to the “organizers” of Robson and Traniello (1999). The sporadic excavation at a high rate (number of excavations/time) seen for some termite excavators reflects a breakdown in the rotation system that results in the efforts of the key individuals dominating the course and shape of the tunnel over the short period of their labor. Because of the fidelity of termites in following the tunnel to its tip to excavate (Bardunias and Su, 2009a) and the ability of small irregularities in tunnel wall profile to release excavation behavior (Bardunias and Su, 2010), rapid excavation over a short period by a termite oriented along an idiosyncratic vector can change the course of tunnels away from the previous consensus direction or induce branching which may be followed by subsequent excavators long after the termite has left the tunnel. This excavation would display an organizing effect out of proportion with their contribution to the total excavation effort of the group of termites digging in rotation. The breakdown of the rotation system at first seems maladaptive, but the sinuosity that will emerge in tunnel heading as they drift around a specific vector due to idiosyncratic excavation and subsequent corrections may be adaptive. Such tunnels may cover a broader search area than tunnels that are straighter and more faithful to a vector heading. Imprecision may lead to a more efficient spread of search area in a manner similar to the imprecision in honeybee dances (Weidenmüller and Seeley, 1999). The ability of key individuals to alter tunnel heading or branch in a given direction may also enable tunnels to respond to environmental stimuli, such as moisture (Su and Puche, 2003) or olfactory gradients (Su, 2005) more rapidly because if an individual exists with a low threshold for detection, it can of itself facilitate a change. It remains to be determined why so few termites were excavating the tunnel at any given time. The queuing described by Bardunias and Su (2009a, 2010) by termites awaiting access to excavate at the tunnel tip implies a role of interference between individuals in organizing labor. Because excavation is focused at the tips of elongating tunnels, the width of tunnels at the tip and the number of tunnel tips may be more important in determining the size of the excavation force than the total number of available termites outside of the tunnel. Surplus termites would have no access to tunnel tips and would be relegated to excavating along the tunnel walls after a period of delay (Bardunias and Su, 2010). Acknowledgments We thank R. Pepin and P. Ban, (University of Florida) and S. Koi and E. Helmick for technical assistance. This research was supported
49
by the Florida Agricultural Experiment Station and a grant from USDA-ARS under the grant 58-6435-8-276. References Bardunias, P.M., Su, N.-Y., 2009a. Dead reckoning in tunnel propagation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 102, 158–165. Bardunias, P.M., Su, N.-Y., 2009b. Opposing headings of excavating and depositing termites facilitate branch formation in the Formosan subterranean termite. Anim. Behav. 78, 755–759. Bardunias, P.M., Su, N.-Y., 2010. Queue size determines the width of tunnels in the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Insect Behav. (In Press). Chen, S.C., 1937. Social modification of the activity of ants in nest building. Physiol. Zool. 10, 420–436. Dornhaus, A., Holley, J.-A., Pook, V.G., Worswick, G., Franks, N.R., 2008. Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis. Behav. Ecol. Sociobiol. 63, 43–51. Evans, T.A., 2006. Foraging and building in subterranean termites: task switchers or reserve labourers? Insect. Soc. 53, 56–64. Herbers, J.M., 1983. Social organization in Leptothorax ants: within and between species patterns. Psyche 90, 361–386. Hölldobler, B., Wilson, E.O., 1990. The Ants. Harvard University Press, Cambridge, MA. Lee, S.-H., Bardunias, P., Su, N.-Y., Yang, R.L., 2008. Behavioral response of termites to tunnel surface irregularity. Behav. Processes 78, 397–400. Möglich, M., Hölldobler, B., 1975. Communication and orientation during foraging and emigration in the ant Formica fusca. J. Comp. Physiol. 101, 275–288. Oster, G.F., Wilson, E.O., 1978. Caste and Ecology in the Social Insects. Princeton University Press, Princeton, NJ. Robinson, G.E., 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665. Robson, S.K., Traniello, J.F.A., 1998. Resource assessment, recruitment behavior and the organization of cooperative prey retrieval in the ant Formica shaufussi. J. Insect Behav. 11, 1–22. Robson, S.K., Traniello, J.F.A., 1999. Key individuals and the organisation of labor in ants, pp. 239–259. In: Detrain, C., Deneubourg, J.L., Pasteels, J.M. (Eds.), Information Processing in Social Insects. Birkhäuser, Basel. Institute, SAS, 1985. SAS/STAT Guide for Personal Computers, version 6 ed. SAS Institute, Cary, NC. Simons, A.M., 2004. Many wrongs: the advantage of group navigation. Trends Ecol. Evol. 19, 453–455. Su, N.-Y., 2005. Directional change in tunneling of subterranean termites (Isoptera: Rhinotermitidae) in response to decayed wood attractants. J. Econ. Ent. 98, 471–475. Su, N.-Y., Puche, H., 2003. Tunneling activity of subterranean termites (Isoptera: Rhinotermitidae) in sand with moisture gradients. J. Econ. Ent. 96, 88–93. Su, N.-Y., Scheffrahn, R.H., 1986. A method to access, trap, and monitor field populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 12, 299–304. Sudd, J.H., 1972. The absences of social enhancement of digging in pairs of ants (Formica lemani Bondroit). Anim. Behav. 20, 813–819. Walraff, H.G., 1978. Social interrelations involved in migratory orientation of birds: possible contribution of field studies. Oikos 30, 401–404. Wiedenmüller, A., Seeley, T.D., 1999. Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation? Behav. Ecol. Sociobiol. 46, 190–199. Xenophon, 1914. Cyropaedia. In: Miller, W. (Ed.), Loeb Classic Library. Harvard University Press, Cambridge, MA. Yang, R.-L., Su, N.-Y., Bardunias, P.M., 2009. Individual task load in tunnel excavation by the Formosan subterranean termite Coptotermes formosanus (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 102, 906–910.
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j a p e
Behavioral variation among tunnelers in the Formosan subterranean termite Paul Bardunias ⁎, Nan-Yao Su, Rou-Ling Yang Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, 3205 College Avenue, Fort Lauderdale, FL 33314, USA
a r t i c l e
i n f o
Article history: Received 27 July 2009 Revised 30 October 2009 Accepted 4 November 2009 Keywords: Key individual Excavation Tunnel Division of labor Coptotermes formosanus
a b s t r a c t Division of labor is a common feature of insect societies and has been theorized to account for much of their success. Asymmetries in the work of individuals, whose aggregate labor results in the completion of a task, can lead to the emergence of key individuals that dominate or govern the task. Coptotermes formosanus Shiraki excavate in a series of alternating workers whose efforts combine not only to elongate tunnels, but also to guide the direction of propagation. When groups of 100 termites were presented with a single tunnel, only ∼ 16% of termites entered. Of those that entered, the level of excavation was not uniform, with 20.6% of termites responsible for over half of the total excavation. These termites, a small percentage of the total available workforce, act as key individuals, producing the majority of labor and possibly guiding the efforts of others. An examination of the excavation patterns of individuals shows that some individuals excavate sporadically, but at a very high rate (number of excavation events per time). By focusing their effort over a short period, these highly active individuals may influence the orientation of a tunnel and the formation of branches to a degree out of proportion to the total amount of digging they engage in. © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2009 Published by Elsevier B.V. All rights reserved.
The benefit of task specialization and division of labor was perhaps best described by Xenophon, a student of Socrates, in one of the earliest descriptions of the process, “…he who devotes himself to a very highly specialized line of work is bound to do it in the best possible manner.” Division of labor is a major factor in the success of social insects, thought to increase the efficiency of the large workforces of colonies (Oster and Wilson, 1978). Often this division of labor is reflected in worker polymorphism or temporal polyethism, but a more fluid system of task specialization among less specialized individuals is seen as well (Robinson, 1992). Most studies emphasized the differences between task-groups, while minimizing or ignoring variation within them (Robson and Traniello, 1999). Groups may not be uniform in their task performance, and many individuals that could partake in tasks appear to do no work (Herbers, 1983; Evans, 2006; Dornhaus et al., 2008). Conversely, elite individuals (Hölldobler and Wilson, 1990) or key individuals (Robson and Traniello, 1999) perform a disproportionate amount of labor. Robson and Traniello (1999) proposed three types of key individuals: catalysts, performers, and organizers. Performers are simply individuals who are highly active and account for a disproportionate amount of labor on any task. Catalysts stimulate others to activity through their actions, and organizers serve to initiate labor and maintain group cohesion throughout the task. The presence of key individuals results in their
⁎ Corresponding author. E-mail address: paulmb@ufl.edu (P. Bardunias).
behavioral idiosyncrasies being over-represented in the final work product. One task that termites carry out as groups is the excavation of tunnels. Coptotermes formosanus Shiraki excavate tunnels by combining their efforts as members of a group which removes soil from the tunnel in rotation (Bardunias and Su, 2009a, 2010). Recently, Yang et al. (2009) demonstrated that termites in excavation groups that were introduced to experimental arenas did not perform equal amounts of work. Understanding how termites apportion the total work on a task among individuals is important to our understanding of the evolution of division of labor (Robson and Traniello, 1999). Alternatively, if our goal is to understand the mechanics of tunnel excavation, then the manner in which individuals combine their efforts over a limited time-frame, their place and frequency of occurrence in the rotation of excavators is more important than the overall duration of labor. In situations where a key individual is responsible for choosing a prey item (Robson and Traniello, 1998) or a new nest site (Möglich and Hölldobler, 1975), the ability for a single key individual's actions to shape the outcome of task is obvious. Termites in a tunneling-group alternate their labor at a digging site, each individual working as part of a rotation of individuals who work in series (Bardunias and Su, 2009a, 2010). This will tend to dampen the influence of any single termite's idiosyncratic behavior. For example, termites tunnel along internally generated vectors and tunnel headings reflect a consensus of the orientation vectors of the working group (Bardunias and Su, 2009a). The reliance on multiple individuals to work together to generate tunnel headings may act to mitigate individual errors in path
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2009 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.aspen.2009.11.002
46
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
integration through the “many wrongs principle” (Walraff, 1978, Simons, 2004). The orientation vectors on individuals may drift away from their initial movement vector, but they will not all err in the same direction or by the same magnitude. Thus, if many individuals work in union, the resulting vector is more likely to correspond to the original vector. If key individuals dominate excavation, then the homogenizing effect of sampling the orientation vectors of many excavators is reduced. Termites are also known to respond to depressions in tunnel walls by excavating at the site (Lee et al., 2008; Bardunias and Su, 2009b). Repeated excavation by an individual at a preferred site along the tunnel wall may be enough to stimulate others to dig there as well, leading to branch formation. In order to characterize the workforce that is responsible for tunnel excavation we re-examined the asymmetry in excavation shown by Yang et al. (2009) by counting the actual occurrence of excavation events rather than the time on task. We sought to determine if all termites with access to a tunnel opening take the first step in tunneling by entering the tunnel. Of those termites that did enter the tunnel, we determined if they shared equally in the excavation process. Most importantly, we gauged the potential for any single excavator's behavior to disproportionately shape the resultant tunnel's form or heading by determining if termites excavate at a uniform rate (excavation/time).
between a pair of plastic spacers forming a tunnel 2 cm directly away from the introduction point, then the spacers forced the termites to turn 90° and travel another 2 cm (Fig. 1c). Termites respond to this forced turn by excavating a curved tunnel (Fig. 1d) in the opposite direction when they were free of the spacers and allowed to tunnel freely once more (Bardunias and Su, 2009a). A curved tunnel allows the maximum length of tunnel to fit into a video frame and the termites to be filmed at maximum magnification. Upon debouching from this guided channel, termites then tunneled freely. Once the tunnel tip advanced beyond the guided channel, tunneling activity was recorded at room temperature (26 °C) and room lighting for 1 h with a video camcorder (Sony DVHandycam, Tokyo, Japan) mounted above the arena. Entering the tunnel
Methods
The first step in an individual termite's joining the group of excavators in an existing tunnel is simply entering the tunnel from the introduction chamber. In each trial the identity of every termite entering the tunnel over the 1 h period was recorded. The average of the percentages of termites entering the tunnel among trials was determined. The number of termites entering the tunnel in ten trials was compared with the expectation that all 90 potential excavators would enter the tunnel in each trial via chi-square analysis at α = 0.05 (SAS Institute, 1985).
Study subjects
Excavation
Individuals of C. formosanus were collected from two field colonies in Broward County, FL, by using the methodology of Su and Scheffrahn (1986). They were stored at 27 ± 2 °C in plastic boxes with thin, moist wood chips. Ten groups, five from each colony, of 100 termites, made up of 90 potential excavators of at least 3rd instar and 10 soldiers, were created for 10 experimental trials. All 100 termites were individually marked with a unique one- and two-dot color scheme of 12 colors of enamel paint (Testor Corp., Rockford, IL) on their dorsal abdomen. Horizontal arenas consisted of two sheets of transparent Plexiglas (24 by 24 cm2), with four Plexiglas spacers (2 × 24 by 4 by 0.2 cm3, and 2 × 20 by 4 by 0.2 cm3) between the outer margins. Sifted sand (150– 500 μm sieves, Play Sand Bonsal, Miami, FL) was moistened with deionized water ≈ 7% by weight. A 15 ml cryogenic vial (Nalge Nunc International, Rochester, NY) was used as an introduction chamber (Fig. 1a, 3 cm diameter by 4 cm height). This was connected to the arena via a 6 cm, 3 mm diameter, tunnel bored through a Plexiglas coupling (Fig. 1b). Termites were initially constrained to excavate
The contribution of each termite that entered a tunnel to the total labor that went into tunnel excavation was determined. Over the 1 h experimental period, all of the excavation events performed by each termite in a trial were tallied. In order to determine if all termites contributed equally to the tunnel excavation, the number of excavation events performed by each individual within a trial was compared to the mean number of excavations performed by all termites within that trial via chi-square analysis at α = 0.05 (SAS Institute 1985). The proportion of the tunnel excavation performed by each participant within a trial was calculated by dividing the number of excavation events performed by the individual by the total number of excavation in the trial. The result was converted to a percentage and these were binned in 5% intervals from 0% to 35%. The mean percentage of individuals whose contribution to overall excavation of the tunnel in their trial fell into each of these 5% intervals was compared via Kruskal–Wallis test (SAS Institute 1985). Significant differences among the mean percentages of individuals whose proportion of excavation fell within each of the binned intervals from 0% to 35% were separated by a Dunn's post-hoc test at an adjusted α of 0.001 (0.05/42). Temporal pattern of excavation
Fig. 1. The experimental arenas consisted of sifted sand between two sheets of transparent Plexiglas (24 by 24 cm2). (a) 15 ml cryogenic vial was used as an introduction chamber. (b) A 4 cm, 3 mm diameter Plexiglas coupling connected the introduction chamber to the arena. (c) Termites were initially constrained to excavate between a pair of plastic spacers forming a tunnel 3 cm directly away from the introduction point, then the spacers forced the termites to turn 90° and travel another 3 cm. (d) The forced turn results in the excavation of a curved tunnel.
To examine the temporal pattern of an individual's excavation we plotted each individual termite's excavation over the total time of the trial. Even if termites contributed an equal number of excavation events over the course of the trial, the rate (number of excavations/ time) at which they work may be different. The time of the initiation of excavation was recorded when a termite initiated excavation by grasping sand with its maxilla. The number of excavation events that occurred within a 1 min period was recorded over the 1 h duration of the trial for each excavator in the 10 trials. Plotting the number of excavation events carried out by each individual in a trial results in a graph that is too cluttered to be easily understood. For the sake of clarity, we plotted the excavation for 1 min intervals from 0 to 60 min of only the top excavators in each trial: the minimum number of individuals whose labor accounted for at least 50% of the total
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
47
excavation. In addition, because there could be long periods of inactivity, we calculated a rate of excavation for these top excavators as the number of excavation events occurring in any 1 min period in which they performed an excavation. By examining the pattern of every individual's excavation each trial we determined if termites ever performed an uninterrupted series of excavation events rather than excavating in alternation with other termites. Results Entering the tunnel Not all of the 90 potential excavators with access to the tunnel entered it. The number of potential excavators that entered over the 1 h period of recording ranged among trials from 21 to 9, with an average of 14.5 ± 3.7 (mean ± SD). That is a mean percentage of 15.7 ± 4% of all potential excavators entering the tunnels, which differed significantly from the expectation that all termites would enter the tunnel (χ2 = 634.71, df = 9, P b 0.0001). Excavation The termites entering the tunnel did not contribute equally to the excavation of the tunnel (Table 1). In each trial some individuals performed at a much higher level than did others, their efforts ranging from 0 to 56 excavation events in any trial during the 1 h period. The percentage of individuals whose labor fell into each of the 5% excavation intervals from 0% to 35% within their trial was significantly different according to a Kruskal–Wallis test (χ2 = 45.276, df = 6, P b 0.0001). The mean percentages of termites in the 5%, 10%, 15%, and 20% excavation intervals were all significantly different from the other intervals (Fig. 2), but the 25% excavation interval did not differ significantly from the 30%, or the 30% from the 35%. Few termites (5.5%) entered the tunnel, yet failed to excavate any soil. Of those termites that entered the tunnel, 57.9% performed 5% or less and 84.8% performed 15% or less of the excavation in their tunnels. The effort of top excavators in any tunnel still accounted for less than a third of the total tunnel excavation. Small groups of individuals, 3 ± 0.9 (mean ± SD), in each tunnel whose aggregate excavation accounted for at least 50% of the total work on that tunnel represented 20.6% of all of the termites which entered tunnels. This drops to only 3.3% of the total number of termites if we include the majority that never entered the tunnels. Temporal pattern of excavation The number of excavation events in each 1 min interval, from 0 to 60 min, for each of the top excavators in a trial is plotted for all ten
Table 1 A comparison of the number of excavation events performed by each of the termites that entered a tunnel within a trial compared with the mean number of excavation events for all termites in that trial. Trial
n
Mean ± SE
1 2 3 4 5 6 7 8 9 10
21 13 18 17 10 13 9 17 13 14
6.714 ± 1.313a 9.846 ± 2.991a 7.556 ± 1.873a 10.529 ± 2.749a 17.5 ± 6.32a 12.307 ± 3.663a 12.444 ± 3.44a 12.764 ± 3.804a 11.153 ± 4.102a 12.857 ± 4.192a
a Means that are significantly different at α = 0.05 (chi-square analysis, SAS Institute 1985).
Fig. 2. The percentage of total tunnel excavation in trials, binned in 5% increments, and the mean percentage of termites (± SE) whose relative excavation effort falls within each. Bars bearing different letters are significantly different at α = 0.001 (Kruskal– Wallis test; Dunn's post-hoc test).
trials in Fig. 3. The temporal pattern of excavation for highly active individuals varied between individuals. Some termites excavated steadily over time (Fig. 3I, b and c), while others excavated in short bursts of activity followed by an extended absence from the tunnel (Fig. 3I, a). The mean rate (number of excavations/time) of excavation for the 876 excavation events that were recorded in any minute during the 10 trials was 1.3 ± 0.8 excavation events (mean ± SD) varying from a minimum mean of 1 event in any minute where excavation occurred (Fig. 3A, a) to a mean of 3.4 ± 2.1 per minute (Fig. 3I, a). The maximum number of excavation events in any minute was 7, one every 8.57 s. Looking at all of the excavation events carried out by all workers in a trial shows that at a high excavation rate (number of excavations/time) an individual may perform a series of uninterrupted excavations, whereas when the excavation rate is as low as once per minute, excavation always occurred as a part of a group of termites alternating their digging among them.
Discussion Tunnel excavation in termites is a group effort, but not all individuals contribute equally to the creation of tunnels. Without knowledge of the full repertoire of behaviors that can be conducted by termites in the introduction chamber, we cannot know if they were simply not motivated to enter the tunnel to excavate or if instead they were performing another task. Even among termites that did enter the tunnel excavation was not uniform, with a small minority of termites responsible for most of the excavation. The few termites that dominated excavation in each trial may be considered key individuals, but defining their role in the organization of labor within the three categories (organizer, catalyst, and performer) defined by Robson and Traniello (1999) will require further research. They clearly performed the task of excavation at high rate relative to the other termites. In this way they are similar to “performers” because, within the period of their peak excavation, they are carrying out the majority of excavation. Their presence could be inhibiting other excavators by physically blocking access to the tunnel end, but, through their rapid excavation, they may be acting as “catalysts,” leading others to greater effort. Similarities between the group excavation process in termites and ants (Chen, 1937, but see Sudd, 1972) suggest that this may occur. Future studies should include the removal of these highly active individuals to determine if the overall rate of excavation decreases in their absence, as it would
48
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
Fig. 3. Excavation schedules over the 1 h experimental period for the top excavators, defined as the minimum number whose labor accounted for at least 50% of total excavation. Each point represents the number of excavation events occurring within a 1 min period. The symbols for each line correspond to individuals a through e, assigned in no particular order.
P. Bardunias et al. / Journal of Asia-Pacific Entomology 13 (2010) 45–49
were they true “performers,” or if the excavation effort of other termites decreases in their absence, indicating a catalytic function. An intriguing possibility is that the highly active excavators are also acting in an organizational capacity akin to the “organizers” of Robson and Traniello (1999). The sporadic excavation at a high rate (number of excavations/time) seen for some termite excavators reflects a breakdown in the rotation system that results in the efforts of the key individuals dominating the course and shape of the tunnel over the short period of their labor. Because of the fidelity of termites in following the tunnel to its tip to excavate (Bardunias and Su, 2009a) and the ability of small irregularities in tunnel wall profile to release excavation behavior (Bardunias and Su, 2010), rapid excavation over a short period by a termite oriented along an idiosyncratic vector can change the course of tunnels away from the previous consensus direction or induce branching which may be followed by subsequent excavators long after the termite has left the tunnel. This excavation would display an organizing effect out of proportion with their contribution to the total excavation effort of the group of termites digging in rotation. The breakdown of the rotation system at first seems maladaptive, but the sinuosity that will emerge in tunnel heading as they drift around a specific vector due to idiosyncratic excavation and subsequent corrections may be adaptive. Such tunnels may cover a broader search area than tunnels that are straighter and more faithful to a vector heading. Imprecision may lead to a more efficient spread of search area in a manner similar to the imprecision in honeybee dances (Weidenmüller and Seeley, 1999). The ability of key individuals to alter tunnel heading or branch in a given direction may also enable tunnels to respond to environmental stimuli, such as moisture (Su and Puche, 2003) or olfactory gradients (Su, 2005) more rapidly because if an individual exists with a low threshold for detection, it can of itself facilitate a change. It remains to be determined why so few termites were excavating the tunnel at any given time. The queuing described by Bardunias and Su (2009a, 2010) by termites awaiting access to excavate at the tunnel tip implies a role of interference between individuals in organizing labor. Because excavation is focused at the tips of elongating tunnels, the width of tunnels at the tip and the number of tunnel tips may be more important in determining the size of the excavation force than the total number of available termites outside of the tunnel. Surplus termites would have no access to tunnel tips and would be relegated to excavating along the tunnel walls after a period of delay (Bardunias and Su, 2010). Acknowledgments We thank R. Pepin and P. Ban, (University of Florida) and S. Koi and E. Helmick for technical assistance. This research was supported
49
by the Florida Agricultural Experiment Station and a grant from USDA-ARS under the grant 58-6435-8-276. References Bardunias, P.M., Su, N.-Y., 2009a. Dead reckoning in tunnel propagation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 102, 158–165. Bardunias, P.M., Su, N.-Y., 2009b. Opposing headings of excavating and depositing termites facilitate branch formation in the Formosan subterranean termite. Anim. Behav. 78, 755–759. Bardunias, P.M., Su, N.-Y., 2010. Queue size determines the width of tunnels in the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Insect Behav. (In Press). Chen, S.C., 1937. Social modification of the activity of ants in nest building. Physiol. Zool. 10, 420–436. Dornhaus, A., Holley, J.-A., Pook, V.G., Worswick, G., Franks, N.R., 2008. Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis. Behav. Ecol. Sociobiol. 63, 43–51. Evans, T.A., 2006. Foraging and building in subterranean termites: task switchers or reserve labourers? Insect. Soc. 53, 56–64. Herbers, J.M., 1983. Social organization in Leptothorax ants: within and between species patterns. Psyche 90, 361–386. Hölldobler, B., Wilson, E.O., 1990. The Ants. Harvard University Press, Cambridge, MA. Lee, S.-H., Bardunias, P., Su, N.-Y., Yang, R.L., 2008. Behavioral response of termites to tunnel surface irregularity. Behav. Processes 78, 397–400. Möglich, M., Hölldobler, B., 1975. Communication and orientation during foraging and emigration in the ant Formica fusca. J. Comp. Physiol. 101, 275–288. Oster, G.F., Wilson, E.O., 1978. Caste and Ecology in the Social Insects. Princeton University Press, Princeton, NJ. Robinson, G.E., 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665. Robson, S.K., Traniello, J.F.A., 1998. Resource assessment, recruitment behavior and the organization of cooperative prey retrieval in the ant Formica shaufussi. J. Insect Behav. 11, 1–22. Robson, S.K., Traniello, J.F.A., 1999. Key individuals and the organisation of labor in ants, pp. 239–259. In: Detrain, C., Deneubourg, J.L., Pasteels, J.M. (Eds.), Information Processing in Social Insects. Birkhäuser, Basel. Institute, SAS, 1985. SAS/STAT Guide for Personal Computers, version 6 ed. SAS Institute, Cary, NC. Simons, A.M., 2004. Many wrongs: the advantage of group navigation. Trends Ecol. Evol. 19, 453–455. Su, N.-Y., 2005. Directional change in tunneling of subterranean termites (Isoptera: Rhinotermitidae) in response to decayed wood attractants. J. Econ. Ent. 98, 471–475. Su, N.-Y., Puche, H., 2003. Tunneling activity of subterranean termites (Isoptera: Rhinotermitidae) in sand with moisture gradients. J. Econ. Ent. 96, 88–93. Su, N.-Y., Scheffrahn, R.H., 1986. A method to access, trap, and monitor field populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 12, 299–304. Sudd, J.H., 1972. The absences of social enhancement of digging in pairs of ants (Formica lemani Bondroit). Anim. Behav. 20, 813–819. Walraff, H.G., 1978. Social interrelations involved in migratory orientation of birds: possible contribution of field studies. Oikos 30, 401–404. Wiedenmüller, A., Seeley, T.D., 1999. Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation? Behav. Ecol. Sociobiol. 46, 190–199. Xenophon, 1914. Cyropaedia. In: Miller, W. (Ed.), Loeb Classic Library. Harvard University Press, Cambridge, MA. Yang, R.-L., Su, N.-Y., Bardunias, P.M., 2009. Individual task load in tunnel excavation by the Formosan subterranean termite Coptotermes formosanus (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 102, 906–910.