TY - JOUR
AU - Zhou, Xuguo
AB - Abstract Corpse management is essential for social animals to maintain colony health. In the eastern subterranean termite, Reticulitermes flavipes, workers carry out undertaking behaviors to mitigate the risks associated with the dead. In this study, we hypothesized that termites would respond differently to the corpses from different castes based on their postmortem chemical signatures. To test this hypothesis, we 1) documented the behavioral responses of the workers toward corpses from different castes, and 2) profile the chemical signatures of these corpses. Corpses from all castes were retrieved inside the nests and cannibalized when they were decomposed <64 h, regardless of the presence or absence of the cues that we refer to as early death cues (3-octanol and 3-octanone). However, after 64 h, all corpses except for soldiers were buried on site by R. flavipes workers. The late death cues (oleic acid) were cumulative over time among castes but accumulated more slowly and at lower levels in soldiers. The differential release of 3-octanol and 3-octanone between workers/soldiers and nymphs could be explained by either qualitative or quantitative differences in signaling the death between imaginal and neuter developmental pathways. In summary, the efficient and selective recognition of the dead and the fine-tuning of subsequent undertaking responses observed in R. flavipes are aspects of corpse management, which can minimize the potential risks associated with different castes and maximize the colony fitness. Death is frequently encountered by animals, and represents a potential pathogenic risk (Liu et al. 2019), which typically induces avoidance behaviors by living conspecifics in both vertebrates (Pinel et al. 1981, Carr et al. 1981, Montoya et al. 1981, Prounis and Shields 2013, Stroud et al. 2014) and invertebrates (Yao et al. 2009, Candia-Zulbarán et al. 2015, Aksenov et al. 2017, Kierat et al. 2017). This is particularly true in eusocial insects, in which corpse management is essential to coping with the risks associated with the dead due to their enclosed nesting structures (Wilson et al. 1958, Sun and Zhou 2013, Shelton 2014) and high population densities (Su et al. 1993, Hölldobler and Wilson 2009). Necrophoric behavior, i.e., removal of dead colony members, has been observed in Hymenoptera (Wilson et al. 1958, Visscher 1983, López-Riquelme et al. 2013, McAfee et al. 2018). Whereas in termites, cannibalism is primarily conducted to recycle nutrients, such as nitrogen (Sun et al. 2018, 2020; Chouvenc 2020), whereas defense against pathogens, such as burial behavior, is a secondary benefit (Nalepa 1994). When there is battle or competition, decayed corpses would result from walling-off of intrusion points, where termites were killed, and subsequently rediscovered only while the tunnels are reopened (Li et al. 2010, Lima and Costa-Leonardo 2012, Bernard et al. 2017). As the corpses accumulate and continue to decompose, cannibalism becomes inefficient, and burial behavior would then follow (Strack 1998, Myles 2002, Chouvenc and Su 2012, Davis et al. 2018, Sun et al. 2018). Recognition of death is the critical first step for social animals to elicit undertaking behavior. Death recognition in eusocial insects primarily relies on chemical cues. The involvement of nonolfactory cues, such as tactile, auditory, thermal, or visual cues, is largely unknown, with the exception of a synergistic effect of tactile cues and a chemical death cue, oleic acid, on burial behavior in a subterranean termite, Reticulitermes virginicus (Banks, Blattodea: Rhinotermitidae) (Ulyshen and Shelton 2012). Currently, there are two major hypotheses underlying chemical cue-based death recognition: 1) the increased death cue hypothesis, suggesting that the accumulation of death-related chemicals elicits undertaking behavior (Wilson et al. 1958, Sun and Zhou 2013, Sun et al. 2018), and 2) the diminished vital sign hypothesis, proposing that the decrease of chemical cues associated with life immediately upon death mediates undertaking behavior (Choe et al. 2009). Since the discovery that the postmortem release of fatty acids stimulates corpse removal in ants (Wilson et al. 1958), fatty acid death cues have not only been documented in social insects but also widely reported to be repellents across other arthropod taxa (Haskins and Haskins 1974, Howard and Tschinkel 1976, Yao et al. 2009, Chouvenc et al. 2012, Ulyshen and Shelton 2012, Diez et al. 2013, McAfee et al. 2018). In comparison to the well-documented chemical releaser of undertaking behaviors in fatty acids, the diminished vital sign has only been identified in one ant species, the Argentine ant, Linepithema humile (Mayr, Hymenoptera: Formicidae) (Choe et al. 2009). Recently, a third hypothesis has been proposed in the eastern subterranean termite, Reticulitermes flavipes (Kollar, Blattodea: Rhinotermitidae), in which the interplays between the early and late death cues trigger a behavioral switch from cannibalism to burial in R. flavipes to balance pathogenic risks and nutritional rewards associated with corpses (Sun et al. 2017). Specifically, the combination of fatty acids, phenol, and indole are considered as late death cues due to their gradual accumulation after death (Chouvenc et al. 2012, Sun et al. 2013), whereas, 3-octanone and 3-octanol, which are released immediately upon death, peak at 0.5 h, diminish at 8-h postmortem, and elicit the retrieval of conspecific corpses from the testing arena to the holding chamber within 0.5 h after death (Sun et al. 2013), are categorized as the early death cues (Sun et al. 2017). In a natural termite colony, how and how often could the colony members encounter dead conspecifics from different castes? In eusocial animals, individuals follow different developmental trajectories and specialize in certain roles (Hölldobler and Wilson 2009). The developmental pathway in Reticulitermes can be divided into an imaginal (winged) and a neuter (wingless) lines (Lainé and Wright 2003). After initial embryonic and larval stages, R. flavipes follow either the imaginal line to develop into nymphs or the neuter line to molt into workers. Both primary reproductives, i.e., kings and queens, and secondary reproductives, nymphoids, are derived from nymphs. When undertakers encounter a dead termite, it is most likely a worker, not only because of their sheer dominance in numbers (Howard and Haverty 1981) but also risks associated with their allocated tasks (Bignell et al. 2010). Howard and Haverty (1981) surveyed the caste composition of R. flavipes in infested wood logs, in which workers were the most abundant caste (84%), followed by larvae (8.7%), nymphs (5%), soldiers (2.1%), presoldiers (0.1%), and neotenic reproductive (0.1%). Castes involved in risky tasks could be the most frequent source of day-to-day mortality. For example, workers handle a wide range of the tasks, including foraging, feeding, brood care, and nest maintenance/colony hygiene (Bignell et al. 2010), nymphs can develop into reproductives (Noirot and Pasteels 1987), and soldiers serve a defensive role to fend off competitors or predators (Yanagihara et al. 2018, Mitaka and Matsuura 2020). Given that foragers, i.e., older workers, are exposed to the outside world beyond the protective nesting structures (Sakagami and Fukuda 1968, Darlington 1991, Schmid-Hempel and Schmid-Hempel 1993, Du et al. 2016), and soldiers involve direct physical combat with competitors or predators, worker and soldier are the most risk-taking castes. In this study, our goal is to study how termites cope with the corpses derived from these different castes. Our overarching hypothesis is that R. flavipes workers would respond differently to the corpses from different castes based on their postmortem chemical signatures. To test this hypothesis, we carried out the following objectives: 1) documented the behavioral responses toward corpses from workers, soldiers, and two types of immature reproductives (nymphs with short- or long-wing buds) across a range of postmortem times; and 2) profiled the chemical signatures of these corpses. Materials and Methods Reticulitermes flavipes Colony Maintenance Reticulitermes flavipes colonies were collected between May and October 2018. The colonies were collected from two separated sites at Red River Gorge within the Daniel Boone National Forest (R-I: 37°47′38″ N 83°35′55″ W and R-II: 37°47′20″ N 83°35′42″ W) and one site at the Arboretum State Botanical Garden of Kentucky, which is located on the campus of the University of Kentucky (A: 38°00′54″ N 84°30′28″ W). Termite traps were made from cardboard rolls (diameter = 8.5 cm, height = 15.2 cm, wrapped by a rubber band) and placed under rotten fallen wood trunks. All traps were at least 200 m away from each other (Fig. 1A). Samples were collected every week, and traps were replaced after each collection. Termites were extracted from collected cardboard rolls, then placed in a Petri dish (diameter = 14.5 cm, height = 2.0 cm) with dampened unbleached paper towels as a food source, where they were held for 2 wk. After that, termites were transferred to a cuboid plastic shoebox and provisioned with moistened wood mulch and pine woodblocks. Termites collected from the same sites (the same rotten trunk) continuously throughout the season were considered as the same colony and kept in the same shoebox. Reticulitermes flavipes colonies were maintained in an incubator with L:D = 0:24 at 27 ± 1°C, and 89–99% RH. Before behavioral and chemical analysis, castes were identified based on morphological traits following Lainé and Wright (2003). Specifically, workers are wingless individuals lacking compound eyes with a pronotum that is trapezoidal in shape. Soldiers are individuals with elongated defensive mandibles, while their thoraxes and abdomens are similar to those of workers. Nymphs can be subdivided into those with short wing buds (SWBN), and those with long wing buds (LWBN) (Fig. 1C). In the laboratory, field-collected colonies were placed in a black PVC bucket for caste identification and separation (Fig. 1A). Fig. 1. Open in new tabDownload slide Termite collection, caste identification, and experimental setup. (A) Termite field collection. Left image: a termite trap was placed in a collection site. Right image: termites were extracted from the cardboard traps and were temporarily placed into a black PVC bucket for caste identification and measurement. Photo credit: Jizhe Shi. (B) A schematic drawing shows experimental setup of the undertaking behavioral assay. (C) Termite castes included in this study. Scale bar: 1 mm. Photo credit: Li Tian. Fig. 1. Open in new tabDownload slide Termite collection, caste identification, and experimental setup. (A) Termite field collection. Left image: a termite trap was placed in a collection site. Right image: termites were extracted from the cardboard traps and were temporarily placed into a black PVC bucket for caste identification and measurement. Photo credit: Jizhe Shi. (B) A schematic drawing shows experimental setup of the undertaking behavioral assay. (C) Termite castes included in this study. Scale bar: 1 mm. Photo credit: Li Tian. Behavioral Responses Toward Corpses From Different Castes The undertaking behavioral response toward termite corpses from workers, soldiers, short wing-bud nymph (SWBN), and long wing-bud nymph (LWBN) was tested in three R. flavipes colonies with eight replications for each colony (Fig. 1B). A Petri dish (diameter = 5.5 cm, height = 1.5 cm), the living chamber, was connected to a smaller dish (diameter = 3.5 cm, height = 1.5 cm), the testing arena, using a plastic tube (inner diameter = 0.7 cm, length = 3.5 cm). An entry port (diameter = 0.5 cm) was drilled onto the lid of the testing arena to introduce the corpses. Unbleached paper towel discs were lined at the bottom of each Petri dish and treated with 200 µl of distilled water, to serve as the food source. One gram of moistened sand (15% water by weight) was put into the living chamber as burial materials. In total, 29 workers and 1 soldier were placed in the living chamber. Termites were acclimated to the dishes for 3 d before the assay. Reticulitermes flavipes workers and soldiers were killed by freezing in a −80°C freezer for 1 min, whereas nymphs required 3 min. The corpses were thawed at room temperature in covered Petri dishes for 5 min, then maintained in the same conditions as the previous colony rearing condition for a series of postmortem times (0, 1, 16, 32, and 64 h) before the behavioral assay. The corpse was placed in the testing arena at the start of the behavioral assay. Only one corpse from the same colony was introduced each time. Undertaking behavior was recorded with a video camcorder (Canon VIXIA HF G10, Canon Inc., Tokyo, Japan) for 24 h. Several different behavioral parameters were recorded. The corpse was documented as retrieved if it was moved to the living chamber. The duration from the introduction of the corpse to first contact by workers was documented as the first detection time. The duration from the introduction of the corpse to its retrieval to the living chamber was recorded as the retrieval time. The duration of retrieval, however, was defined as the difference between the first detection time and the retrieval time. Burial (depositing sand on the corpse) and wall-off (using sand to block the entrance to the testing arena) behavior were documented if observed in the 64-h postmortem corpses. Chemical Profile of Corpses From Different Castes To profile the chemical signatures of corpses from different castes, we used an Agilent Technologies 6890N gas chromatograph (GC) in splitless mode with a DB-5 capillary column (30 m × 0.25 mm × 0.25 µm; Agilent Technologies, Santa Clara, CA). Helium was used as the carrier gas (1.0 ml/min). The starting temperature of the column, 40°C, was held for 2 min before being raised to 320°C at a rate of 10°C/min. The temperature of the injection port was 280°C. Mass spectra were obtained with an Agilent Technologies 5975 mass spectrometer (MS). The National Institute of Standards and Technology/National Institutes of Health/Environmental Protection Agency Mass Spectral Library was used as the basis for compound identification along with retention time from gas chromatography. Termite corpses of workers, soldiers, SWBN, and LWBN with a series of postmortem time (0, 0.5, 1, 2, 4, 6, 8, 16, 32, 64 h) were collected as samples. In total, 15 individuals were put into a 2-ml glass vial sealed with an aluminum crimp cap with a prefitted septum (Thermo Fisher Scientific, Waltham, MA). Volatiles were collected from the headspace of corpses with a 100-µm polydimethylsiloxane solid-phase microextraction (SPME) fiber (Sigma–Aldrich, St. Louis, MO). The needle of the fiber holder was injected into the vial and the fiber was extended inside without contacting the termite samples, and left there for 15 min for volatile collection. After this step, the fiber was retracted and then manually injected into the inlet port of the GC for 1 min. Quantification of compounds previously detected via SPME was conducted through hexane extraction of corpses. Discriminating ions and retention times were used to quantify the volatiles since the peak area was small and sometimes buried in contaminants. The peak area of the 99 and 101 ions was identified as indicators of 3-octanone and 3-octanol, respectively. Fifteen corpses were used for each sample and were first submerged in 200-µl hexane (glass-distilled, Thermo Fisher Scientific, with 10 ng/µl n-nonadecane as internal standard) for 10 min. In total, 50 µl of the solution was transferred to a conical bottom glass vial sealed with the same aluminum cap. Two µl of solution was injected into the GC for analysis. In total, eight replications for each type of corpse were generated from three R. flavipes colonies. Though termites release a blend of fatty acids with phenol and indole as late death cues, burial behavior can be triggered by oleic acid alone (Sun et al. 2017). As such, we used the quantity of oleic acid from the corpses as an indicator of fatty acid abundance in late death cue analysis. Samples of 10 individuals were extracted using 300 µl of glass distilled hexane with 10 ng/µl n-nonadecane as the internal standard for 10 min. About 200 ml of BF3-methanol (10%, w/w) was added to the solution for 10 min at 60 °C. The methyl ester derivative of the fatty acid was identified and quantified by GC-MS. Termite corpses from workers, soldiers, SWBNs, and LWBNs at 16-, 32-, and 64-h postmortem were subjected to analysis. Data Analysis Statistical analysis was performed using SAS software, Version 9.4 (SAS Institute, Cary, NC). Before the analysis of variance (ANOVA), the first detection time was log-transformed (log(x + 1)), the quantities of 3-octanone and 3-octanol were log-transformed as log(x) to fit the assumptions of parametric tests. The first detection time and the duration of retrieval were analyzed by two-way ANOVA with postmortem time, caste, and the interaction between the two as factors, while significance across different castes was analyzed using Tukey’s HSD all-pair wise comparisons test. Two-way ANOVA was also used to compare the release of death cues with postmortem time, caste, and the interaction between them as factors. At each postmortem time point, we conducted one-way ANOVA to compare the average quantity of death cues across different castes. After conducting ANOVA, the normality of residuals was assessed visually by the normal quantile plots. Results Behavioral Responses Toward Corpses From Different Castes Corpses of all castes with less than 64-h postmortem time were retrieved from the testing arena to the living chamber and then cannibalized by workers. After a termite worker detected the corpse, they began to drag the corpse using their mandibles and eventually brought the corpse back to the living chamber (Fig. 2A). There was a significant effect of caste on the first detection time (ANOVA: F(3, 382) = 7.48, P < 0.001). It took workers a significantly longer time to locate LWBN corpses than worker and soldier corpses (Tukey’s HSD all-pair-wise comparisons test; LWBN vs worker/soldier: P < 0.001; SWBN vs worker/soldier/LWBN and worker vs soldier: P > 0.05) (Fig. 2B). There was no effect of postmortem time and the interaction between postmortem time and caste on the first detection time (ANOVA; postmortem time: F(3,382) = 1.75, P = 0.16; interaction: F(9,382) = 1.30, P = 0.24). Fig. 2. Open in new tabDownload slide Behavioral responses to corpses with less than 64 h postmortem time from different castes. (A) Schematic drawings define the detection and retrieval time. Top drawing: the first worker detected the corpse. Bottom drawing: the corpse was retrieved when it was fully dragged into the connecting tube. (B) The first detection time of the introduced corpse (Mean + SEM, n = 24). (C) The duration of corpse retrieval (Mean + SEM, n = 24). Data were pooled from three colonies with eight replications for each colony. Means between groups denoted with the same letter were not significantly different (Tukey’s HSD all-pairwise comparisons test, P > 0.05). Corpses were introduced at a series of postmortem times, including 0, 1, 16, and 32 h. Fig. 2. Open in new tabDownload slide Behavioral responses to corpses with less than 64 h postmortem time from different castes. (A) Schematic drawings define the detection and retrieval time. Top drawing: the first worker detected the corpse. Bottom drawing: the corpse was retrieved when it was fully dragged into the connecting tube. (B) The first detection time of the introduced corpse (Mean + SEM, n = 24). (C) The duration of corpse retrieval (Mean + SEM, n = 24). Data were pooled from three colonies with eight replications for each colony. Means between groups denoted with the same letter were not significantly different (Tukey’s HSD all-pairwise comparisons test, P > 0.05). Corpses were introduced at a series of postmortem times, including 0, 1, 16, and 32 h. There was a significant effect of caste of corpse on duration of retrieval (ANOVA: F(3, 372) = 4.06, P < 0.01). It took a significantly longer time for workers to retrieve SWBN corpses than those of the other three castes (Tukey’s HSD all-pair-wise comparisons test; for SWBN vs worker/soldier: P < 0.05; for SWBN vs worker/soldier/LWBN, and worker vs soldier: P > 0.05). Postmortem time did not affect the duration of retrieval (ANOVA: F(3, 372) = 1.17, P = 0.32). There was an interaction between the postmortem time and caste (ANOVA: F(9, 372) = 2.38, P = 0.01; Fig. 2C). If a worker or nymph corpse was introduced 64-h postmortem, nestmates tended to bury the corpse on site using sand, feces, paper fiber, and/or any other materials they could find when they encountered the corpse. However, when a soldier corpse was introduced, in addition to burial behavior, termite workers exhibited wall-off behavior (using sand to block the entrance to the testing arena) or moved the corpse to the living chamber and then buried it (Fig. 3A and B). Fig. 3. Open in new tabDownload slide Behavioral responses to corpses with 64 h postmortem time from different castes. (A) Schematic drawings depict three different undertaking behaviors when termites encounter corpses from different castes. Drawings from top to bottom represent burial, wall-off, and move, then burial, respectively. (B) Behavioral responses to corpses from each caste. Stacked bars indicate the percentages of behavioral responses depicted in A. Data were pooled from three colonies with eight replications for each colony. Fig. 3. Open in new tabDownload slide Behavioral responses to corpses with 64 h postmortem time from different castes. (A) Schematic drawings depict three different undertaking behaviors when termites encounter corpses from different castes. Drawings from top to bottom represent burial, wall-off, and move, then burial, respectively. (B) Behavioral responses to corpses from each caste. Stacked bars indicate the percentages of behavioral responses depicted in A. Data were pooled from three colonies with eight replications for each colony. Chemical Signature of Corpses From Different Castes 3-Octanone and 3-octanol were detected in both worker and soldier corpses. These two volatile compounds, however, were absent or below detection limit in both types of nymph corpses. 3-Octanone reached the peak after 0.5-h postmortem for both worker and soldier corpses, whereas 3-octanol reached the peak right after death in soldier corpses but after 1-h postmortem in worker corpses. These two volatiles gradually decreased after the peak and became undetectable after 32 h. There were significant effects on the quantities in both volatiles, in castes (ANOVA; 3-octanone: F(3, 959) = 385.05, P < 0.0001; 3-octanol: F(3, 959) = 199.74, P < 0.0001), postmortem time (ANOVA; 3-octanone: F(9, 959) = 136.30, P < 0.0001; 3-octanol: F(9, 959) = 65.37, P < 0.0001) and their interaction (ANOVA; 3-octanone: F(27, 959) = 53.69, P < 0.0001; 3-octanol: F(27, 959) = 28.70, P < 0.0001). Worker corpses usually released significantly more 3-octanone than those of soldiers before 16 h (ANOVA; 0 h: F(24, 47) = 6.53, P = 0.014; 0.5 h: F(24, 47) = 37.47, P < 0.0001; 1 h: F(24, 47) = 22.00, P < 0.0001; 4 h: F(24, 47) = 8.26, P < 0.01; 8 h: F(24, 47) = 4.50, P < 0.05); and released more 3-octanol than soldiers between 0.5- and 16-h postmortem time (ANOVA; 0.5 h: F(24, 47) = 7.15, P = 0.01; 1 h: F(24, 47) = 39.25, P < 0.0001; 2 h: F(24, 47) = 12.73, P < 0.001; 4 h: F(24, 47) = 9.72, P < 0.01; 8 h: F(24, 47) = 6.54, P < 0.05; 16 h: F(24, 47) = 6.05, P < 0.05; Fig. 4A and B). Fig. 4. Open in new tabDownload slide Temporal profiles of the early and late death cues associated with R. flavipes corpses from different castes. A-D show the dynamic changes of the early (A: 3-octanone; B: 3-octanol) and late (C: indole; D: phenol) death cues among different castes. Quantities were determined by hexane extraction (Mean + SEM, n = 24). Data were pooled from three colonies with eight replications for each colony. Asterisks above the grouped bars denote significant difference (ANOVA): *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, NS: not significant. Fig. 4. Open in new tabDownload slide Temporal profiles of the early and late death cues associated with R. flavipes corpses from different castes. A-D show the dynamic changes of the early (A: 3-octanone; B: 3-octanol) and late (C: indole; D: phenol) death cues among different castes. Quantities were determined by hexane extraction (Mean + SEM, n = 24). Data were pooled from three colonies with eight replications for each colony. Asterisks above the grouped bars denote significant difference (ANOVA): *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, NS: not significant. Indole and phenol were released by all castes 16-h postmortem. There were significant effects on the quantities in both indole and phenol, among castes (ANOVA; indole: F(3, 959) = 122.16, P < 0.0001; phenol: F(3, 959) = 62.33, P < 0.0001), postmortem time (ANOVA; indole: F(9, 959) = 7735.48, P < 0.0001; phenol: F(9, 959) = 2975.67, P < 0.0001) and their interaction (ANOVA; indole: F(27, 959) = 114.20, P < 0.0001; phenol: F(27, 959) = 58.03, P < 0.0001). The accumulation of indole and phenol were different across castes after 16 h (ANOVA; indole: F(24, 95) = 5.18, P < 0.01; phenol: F(24, 95) = 5.12, P < 0.01), 32 h (ANOVA; indole: F(24, 95) = 11.30, P < 0.0001; phenol: F(24, 95) = 3.54, P < 0.05), 64 h (ANOVA; indole: F(24, 95) = 117.69, P < 0.0001; phenol: F(24, 95) = 64.03, P < 0.0001; Fig. 4C and D). Oleic acid accumulated as the corpse decayed in all four castes. The accumulation of oleic acid in soldier corpses was lower than in the other three castes across multiple postmortem times (ANOVA; caste: F(3, 143) = 20.77, P < 0.0001; postmortem time: F(3, 143) = 297.50, P < 0.0001; their interaction: F(3, 143) = 13.15, P < 0.0001). Significant differences of the oleic acid accumulation across castes showed in 16 h (ANOVA; F(9, 35) = 5.53, P < 0.01), 32 h (ANOVA; F(9, 35) = 8.41, P < 0.001), and 64 h (ANOVA; F(9, 35) = 15.40, P < 0.0001), but not in live termites (ANOVA; F(9, 35) = 0.069, P > 0.05) (Fig. 5). There was no colony effect on both early and late death cues (ANOVA; 3-octanone: F(2, 959) = 0.14, P = 0.87; 3-octanol: F(2, 959) = 0.15, P = 0.86; indole: F(2, 959) = 0.02, P = 0.98; phenol: F(2, 959) = 0.07, P = 0.93; oleic acid: F(2, 143)=0.03, P = 0.97). Fig. 5. Open in new tabDownload slide Temporal dynamics of oleic acid on R. flavipes corpses from different castes. Quantities were determined by hexane extraction in different castes (Mean + SEM, n = 9). Data were pooled from three colonies with three replications for each colony. Asterisks above the grouped bars denote significant difference (ANOVA): *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, NS: not significant. Fig. 5. Open in new tabDownload slide Temporal dynamics of oleic acid on R. flavipes corpses from different castes. Quantities were determined by hexane extraction in different castes (Mean + SEM, n = 9). Data were pooled from three colonies with three replications for each colony. Asterisks above the grouped bars denote significant difference (ANOVA): *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, NS: not significant. Discussion Corpses From Different Castes Elicit Differential Undertaking Responses The ability to recognize dead nestmates and respond to them properly is extremely important for social animals, particularly in the subterranean termites due to their high population density in an enclosed nesting environment. It is extremely challenging to quantify the natural turnover rate in eusocial insects, especially in the cryptic subterranean termites. Darlington (1991) documented the turnover in the field populations of a mound-building, fungus-growing termite, Macrotermes michaelseni (Sjöstedt, Blattodea: Rhinotermitidae). A daily production rate of 1.4% was estimated based on a pooled dataset from 22 mature nests over a span of seven years in Kenya, in which a total of 18,076 adults was produced on a daily basis from a mature M. michaelseni population containing 2,771,671 juvenile and 1,280,895 adult sterile termites (~4.1 million individuals per colony without the foraging populations outside the nest, n = 22, Darlington 1991). Assuming that the population size of a mature colony is stable, we anticipate a similar daily death rate for M. michaelseni. In the case of R. flavipes, the most widely distributed termite species in North America (Austin et al. 2005), as many as five million individuals might be included in a single colony, covering over 2,000 m2 of foraging territory (Su et al. 1993). Although the colony size and caste composition are substantially different between the two species, a R. flavipes colony could, in theory, contains up to 70,000 nest mate corpses per day based on the 1.4% daily death rate in M. michaelseni. Encountering the dead is common and often in social insects, which makes corpse management a necessity (Sun and Zhou 2013). The purpose of corpse management is not only to provide a level of social immunity by limiting/eliminating the potential pathogenic risks associated with corpses (Cremer et al. 2007, Thorne 1991), but also to recycle nutrients (e.g., nitrogen) and possibly symbionts by cannibalizing dead conspecifics (Sun et al. 2017). In contrast to the eusocial Hymenoptera, for which removal is the primary means of corpse management (Wilson et al. 1958, Visscher 1983, McAfee et al. 2018), termite undertaking responses shift from cannibalism to burial depending on the dynamic change of early and late death cues (Sun et al. 2017). In this study, corpses of all castes were carried inside the nest and cannibalized when the postmortem time was <64 h. Cannibalism of freshly dead conspecifics has been reported in various termite species as a primary strategy to manage the corpse in order to recycle the nutrients (Rosengaus and Traniello 2001; Neoh et al. 2012; Chouvenc and Su 2012; Sun et al. 2017, 2018, 2020; Chouvenc 2020). Given that wood is notorious for its imbalance of carbon: nitrogen ratio (ranging from 75:1 to 247:1), consumption of freshly dead individuals would provide an important nitrogen resource for wood-feeding termites (Hungate 1941, Sun et al. 2017). Theoretically, cannibalism on freshly dead conspecifics would also benefit termites by recycling gut symbionts that help them digest lignocellulose (Thorne 1990). Cannibalism of dead individuals in early stages of decomposition also protects the colony from pathogens associated with the corpse with the help of the antimicrobial properties of termite saliva and guts contents (Rosengaus and Traniello 2001, Chouvenc et al. 2009). Besides managing the corpses, termite has also been observed to cannibalize terminally ill nestmates as a collective hygienic behavior (Davis et al. 2018), attack and consume the wounded reproductives as a policing behavior (Sun et al. 2020), and recycle other live individuals as emergency food sources during a severe colony condition, such as starvation (Su and Lafage 1986). When left to decompose further, the corpse would become too depleted of nutrients or risky to be recycled. Burial and associated behaviors then occur to block the decayed corpse from the rest of the healthy nestmates so as to protect the colony from the risks associated with corpses. In our results, burial behavior was consistently observed in highly decayed corpses regardless of castes. Additional behaviors, such as walling-off and movement of the corpse before burial were observed for 50% of soldier corpses. Under natural conditions, such circumstances could result from battle and competition, and dead soldiers would be generated from such agonism serving as an indicator of the potential threat. Walling-off of intrusion points results in these individuals being killed and left for decaying outside the colony, and may be rediscovered later. In Coptotermes (Wasmann, Blattodea: Rhinotermitidae) termites, when two inter- or intraspecific colonies aggressively encounter one another, tunnel blockages are constructed (Li et al. 2010, Lima and Costa-Leonardo 2012, Bernard et al. 2017). Similarly, an intricate undertaking response was documented in the Asian subterranean termite, Coptotermes gestroi (Wasmann, Blattodea: Rhinotermitidae), in which soldiers that had been dead for over 24 h were buried, while freshly killed soldiers were buried, cannibalized (partially or fully), or ignored, demonstrating behavioral plasticity toward soldier corpses (da Silva et al. 2019). In addition, tunneling C. gestroi workers avoided areas containing dead soldiers from both conspecific and competitors (Lima and Costa-Leonardo 2012). Such ‘walling-off’ behavior could potentially reduce the risk of subsequent aggression. Chemical Signatures Are Quantitatively and/or Qualitatively Different Among Corpses From Different Castes Postmortem chemical profiles showed that the early death cues, 3-octanone and 3-octanol, in worker corpses were significantly higher than in soldier corpses, while they were undetectable in SWBN and LWBN corpses. In comparison, the late death cues, specifically oleic acid, were ubiquitously detected; however, these chemicals accumulated significantly slower in soldier corpses than other castes. The differential release of the early death cues between workers/soldiers and nymphs might be due to either quantitative or qualitative differences. Quantitatively, our detection method might not be sensitive enough to identify the trace-amount of 3-octanol and 3-octanone in nymph corpses. Qualitatively, there might be intrinsic differences in the biosynthesis of these two volatiles between imaginal and neuter developmental pathways. In addition, nymphs might use cues (e.g., tactile) other than chemicals to signaling death (Ulyshen and Shelton 2012). Such differences are the result of different chemical composition, physiology, biochemistry, etc., among castes. Such differences in the early death cues lead to subtle changes in undertaking responses. Although freshly killed corpses were always cannibalized, it took longer for R. flavipes to locate and recycle nymph corpses lacking 3-octanone and 3-octanol. The early death cues help workers from the living chamber locate the corpses (Sun et al. 2017). However, the fact that nymph corpses were eventually cannibalized suggests the involvement of other sensory cues. Tactile cues have been suggested to synergize with oleic acid to elicit burial behavior in R. virginicus (Ulyshen and Shelton 2012). In comparison to castes in the imaginal line (nymphs), castes in the neuter line (workers and soldiers) carry out tasks with higher risks, including disease and predation (Cremer et al. 2007). Analogous to ‘immune privilege’ documented in the germline or nerve cells in the central nervous system (Janeway et al. 1999, Cremer et al. 2007), reproductives in eusocial insects are expected to be subject to special protection. Nymphs, a reproductive-in-making caste, should share the social ‘immune privilege’ with other castes within the imaginal line. In contrast, considered ‘somatic’ and disposable according to the ‘disposable soma’ theory (Kirkwood 1987), the worker caste, especially for foragers (older workers), is more expendable. Consequently, the turnover rate should be lower in castes in the imaginal line (nymphs) compared with those in the neuter line (workers and soldiers). As such, a well-synchronized signaling system involving both early and late death cues allows R. flavipes to locate and respond to the corpses from the most risk-taking castes, i.e., workers and soldiers, quickly and efficiently (Sun et al. 2017). Meanwhile, the difference of accumulation in late death cues between the corpses of soldier and other castes could be proximately explained by 1) a delayed decomposition process, in which the accumulation of fatty acids was significantly slower in soldier corpses than in other castes; and 2) the mix of defensive secretions in the postmortem chemicals in soldier corpses. Autolytic catabolism and bacterial hydrolysis of triglycerides contribute to the accumulation of fatty acids in dead bodies (Blum et al. 1970). With substantial modifications in body plan, morphology and chemistry in soldiers, such as enlarged head capsules and mandibles and defensive chemicals stored in the frontal gland (Noirot and Pasteels 1987), the decomposition processes and postmortem chemical profiles of soldiers are, understandably, different from those in workers. In addition, defensive secretions by soldiers protect the colony from intruders and pathogenic attacks (Prestwich 1979, 1984; Zalkow et al. 1981). In a congeneric species, R. speratus (Kolbe, Blattodea: Rhinotermitidae), a soldier-specific volatile, (−)-β-elemene, exhibited fungistatic activity against entomopathogenic fungi (Mitaka et al. 2017). Fuller (2007) demonstrated that soldier secretions in Nasutitermes acajutlae (Holmgren, Blattodea: Termitidae) inhibited the growth of fungi on freshly killed soldier corpses, suggesting a slower decomposition process in soldier corpses. The possible causes of death in termites vary under natural conditions. In this study, we used a freeze–thaw method to generate termite corpses and examine their volatiles. Although freezing to death does exist in nature (personal observation), this method has been suggested to improve the detection of volatile compounds in several insect species, including R. flavipes (Chen 2017). Although we never observe any visible leaking of body fluid, i.e., hemolymph, from the corpses during the undertaking bioassay, ice crystals that are formed during the freeze–thaw cycle can cause cell membranes to rupture due to an imbalance in osmotic pressure. In a parallel study, however, death-related volatile compounds, including 3-octanol and 3-octanone, were ubiquitously detected in R. flavipes workers dead from biotic (competition and disease) and abiotic (freezing, heat, desiccation, and insecticides) factors (unpublished data). That being said, how freezing affects the undertaking process, is a question warrants further investigation. Summary and Perspectives Caste, division of labor, and well-orchestrated communication are key characteristics defining superorganisms. The assembly of superorganisms follows a series of algorithms, including developmental, behavioral, and genetic rules (Hölldobler and Wilson 2009). The differential undertaking responses to corpses from different castes follow behavioral algorithms, in which the selection of behavioral responses differs between castes. In termites, cannibalism of freshly killed corpses benefits the colony by recycling nutrients, and potential gut symbionts and by preventing pathogens development that would occur if corpses were left unattended. Furthermore, burial and walling-off behavior can be used to separate highly decomposed corpses from the colony to prevent further disease transmission and avoid further contact with predators or competitors. Such differential responses are achieved in an autonomous, decentralized way (Pratt et al. 2002, Werfel et al. 2014) following the behavioral algorithms/rules (Hölldobler and Wilson 2009). Castes are created following the developmental algorithm, a series of sequential decision-making events guiding the growth of colony members to reach their respective developmental endpoints (Hölldobler and Wilson 2009). In R. flavipes, at the first decision point of postembryonic development, the second instar larvae follow either the imaginal line to advance into nymphs (reproductives), or the neuter line to progress into workers and soldiers (nonreproductives). Death in the imaginal line is costly to the colony due to their all-important reproductive outputs, which warrants social ‘immune privilege’. Given that nymphs are typically nest-bound, risks associated with their allocated tasks and their turnover rate should be low. Indeed, the early death cues were absent or undetectable in nymphs. For the neuter line, however, the ‘somatic’ worker caste is disposable and replaceable. Workers carry out almost all tasks within the colony except reproduction. The downside with riskier tasks, such as foraging and undertaking, is the higher turnover rate in termite workers. Consequently, equipped with a battery of early and late death cues, termites are able to manage corpses from the numerically dominant worker caste in a timely and efficient manner to maximize colony fitness. Acknowledgments We are are grateful to the editors and anonymous reviewers for their constructive criticisms and comments to improve the manuscript. This project was supported by a Hatch fund (Accession Number: 1004654; Project Number: KY008071) from the USDA National Institute of Food and Agriculture to XGZ, and seed grants (Y852981G03 and Y952824103) from the State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Science to XGZ and CZ. In addition, JZS was supported by a 4-yr Chinese Scholarships Council (CSC) Stipend Fellowship. The granting agencies have no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author contribution JZS, KFH, and XGZ: conceived and designed the experiments; JZS and undergraduate researchers CZ and SRH: laboratory experiments; JZS: analyzed the data; JZS: drafted the manuscript; AM, KFH, QS, and XGZ: revised the manuscript. All authors read and approved the final manuscript. Conflict of Interests The authors declare no conflict of interest. Data Accessibility The original data used in this article are available upon request. References Cited Aksenov , V. , and C. D. Rollo. 2017 . Necromone death cues and risk avoidance by the cricket Acheta domesticus: effects of sex and duration of exposure . J. Insect. Behav . 30 : 259 – 272 . Google Scholar Crossref Search ADS WorldCat Austin , J. W. , A. L. Szalanski, R. H. Scheffrahn, and M. T. Messenger. 2005 . Genetic variation of Reticulitermes flavipes (Isoptera: Rhinotermitidae) in North America applying the mitochondrial rRNA 16S gene . Ann. Entomol. Soc. Am . 98 : 980 – 988 . Google Scholar Crossref Search ADS WorldCat Bernard , S. , W. Osbrink, and N. Y. Su. 2017 . Response of the formosan subterranean termite to neighboring con-specific populations after baiting with noviflumuron . J. Econ. Entomol . 110 : 575 – 583 . Google Scholar Crossref Search ADS PubMed WorldCat Bignell , D. E. , Y. Roisin, and N. Lo. 2010 . Biology of termites: a modern synthesis, Springer Science & Business Media , Dordrecht, the Netherlands . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Blum , M. S. , W. Kerr, and H. Fales. 1970 . The chemical basis of insect sociality, pp. 61 – 94 . In M. Beroza (eds.), Chemicals controlling insect behavior, Academic Press , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Candia-Zulbarán , R. I. , P. Briones-Fourzán, E. Lozano-Alvarez, C. Barradas-Ortiz, and F. Negrete-Soto. 2015 . Caribbean spiny lobsters equally avoid dead and clinically PaV1-infected conspecifics. ICES . J. Mar. Sci . 72 : i164 – i169 . Google Scholar OpenURL Placeholder Text WorldCat Carr , W. J. , M. R. Landauer, and R. Sonsino. 1981 . Responses by rats to odors from living versus dead conspecifics . Behav. Neural Biol . 31 : 67 – 72 . Google Scholar Crossref Search ADS PubMed WorldCat Chen , J . 2017 . Freeze–thaw sample preparation method improves detection of volatile compounds in insects using headspace solid-phase microextraction . Anal. Chem . 89 : 8366 – 8371 . Google Scholar Crossref Search ADS PubMed WorldCat Choe , D. H. , J. G. Millar, and M. K. Rust. 2009 . Chemical signals associated with life inhibit necrophoresis in Argentine ants . Proc. Natl. Acad. Sci. U. S. A . 106 : 8251 – 8255 . Google Scholar Crossref Search ADS PubMed WorldCat Chouvenc , T . 2020 . Limited survival strategy in starving subterranean termite colonies . Insectes Soc . 67 : 71 – 82 . Google Scholar Crossref Search ADS WorldCat Chouvenc , T. , and N. Y. Su. 2012 . When subterranean termites challenge the rules of fungal epizootics . PLoS One . 7 : e34484 . Google Scholar Crossref Search ADS PubMed WorldCat Chouvenc , T. , A. Robert, E. Sémon, and C. Bordereau. 2012 . Burial behaviour by dealates of the termite Pseudacanthotermes spiniger (Termitidae, Macrotermitinae) induced by chemical signals from termite corpses . Insectes Soc . 59 : 119 – 125 . Google Scholar Crossref Search ADS WorldCat Chouvenc , T. , N. Y. Su, and A. Robert. 2009 . Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes . J. Invertebr. Pathol . 101 : 130 – 136 . Google Scholar Crossref Search ADS PubMed WorldCat Cremer , S. , S. A. Armitage, and P. Schmid-Hempel. 2007 . Social immunity . Curr. Biol . 17 : R693 – R702 . Google Scholar Crossref Search ADS PubMed WorldCat Darlington , J . 1991 . Turnover in the populations within mature nests of the termite Macrotermes michaelseni in Kenya . Insectes Soc . 38 : 251 – 262 . Google Scholar Crossref Search ADS WorldCat Davis , H. E. , S. Meconcelli, R. Radek, and D. P. McMahon. 2018 . Termites shape their collective behavioural response based on stage of infection . Sci. Rep . 8 : 1 – 10 . Google Scholar Crossref Search ADS PubMed WorldCat Diez , L. , L. Moquet, and C. Detrain. 2013 . Post-mortem changes in chemical profile and their influence on corpse removal in ants . J. Chem. Ecol . 39 : 1424 – 1432 . Google Scholar Crossref Search ADS PubMed WorldCat Du , H. , T. Chouvenc, W. Osbrink, and N.-Y. Su. 2016 . Social interactions in the central nest of Coptotermes formosanus juvenile colonies . Insectes Soc . 63 : 279 – 290 . Google Scholar Crossref Search ADS WorldCat Fuller , C. A. 2007 . Fungistatic activity of freshly killed termite, Nasutitermes acajutlae, soldiers in the Caribbean . J. Insect Sci . 7 : 14 . Google Scholar Crossref Search ADS WorldCat Haskins , C. P. , and E. F. Haskins. 1974 . Notes on necrophoric behavior in the archaic ant Myrmecia vindex (Formicidae: Myrmeciinae) . Psyche . 81 : 258 – 267 . Google Scholar Crossref Search ADS WorldCat Hölldobler , B. , and E. O. Wilson. 2009 . The construction of a superorganism, pp. 3 – 10 . In B. Hölldobler, and E. O. Wilson (eds.), The superorganism: the beauty, elegance, and strangeness of insect societies , WW Norton & Company , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Howard , D. F. , and W. R. Tschinkel. 1976 . Aspects of necrophoric behavior in the red imported fire ant, Solenopsis invicta . Behaviour . 56 : 157 – 178 . Google Scholar Crossref Search ADS WorldCat Howard , R. , and M. I. Haverty. 1981 . Seasonal variation in caste proportions of field colonies of Reticulitermes flavipes (Kollar) . Environ. Entomol . 10 : 546 – 549 . Google Scholar Crossref Search ADS WorldCat Hungate , R . 1941 . Experiments on the nitrogen economy of termites . Ann. Entomol. Soc. Am . 34 : 467 – 489 . Google Scholar Crossref Search ADS WorldCat Janeway , C. A. , J. D. Capra, P. Travers, and M. Walport. 1999 . Immunobiology: the immune system in health and disease . Garland Publishing, New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Kierat , J. , M. Filipiak, H. Szentgyörgyi, and M. Woyciechowski. 2017 . Predation cues in solitary bee nests . J. Insect Behav . 30 : 385 – 393 . Google Scholar Crossref Search ADS PubMed WorldCat Kirkwood , T. B. 1987 . Immortality of the germ-line versus disposability of the soma, pp. 209 – 218 . In T. B. Kirkwood (eds.), Evolution of longevity in animals . Springer , Berlin, Germany . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Lainé , L. V. , and D. Wright. 2003 . The life cycle of Reticulitermes spp.(Isoptera: Rhinotermitidae): what do we know? B. Entomol. Res . 93 : 267 – 278 . Google Scholar Crossref Search ADS WorldCat Li , H. F. , R. L. Yang, and N. Y. Su. 2010 . Interspecific competition and territory defense mechanisms of Coptotermes formosanus and Coptotermes gestroi (Isoptera: Rhinotermitidae) . Environ. Entomol . 39 : 1601 – 1607 . Google Scholar Crossref Search ADS PubMed WorldCat Lima , J. T. , and A. M. Costa-Leonardo. 2012 . Tunnelling behaviour of the Asian subterranean termite in heterogeneous soils: presence of cues in the foraging area . Anim. Behav . 83 : 1269 – 1278 . Google Scholar Crossref Search ADS WorldCat Liu , L. , X.-Y. Zhao, Q. B. Tang, C. L. Lei, and Q. Y. Huang. 2019 . The mechanisms of social immunity against fungal infections in eusocial insects . Toxins 11 : 244 . Google Scholar Crossref Search ADS WorldCat López-Riquelme , G. O. , and M. L. Fanjul-Moles. 2013 . The funeral ways of social insects: social strategies for corpse disposal . Trends Entomol . 9 : 71 – 129 . Google Scholar OpenURL Placeholder Text WorldCat McAfee , A. , A. Chapman, I. Iovinella, Y. Gallagher-Kurtzke, T. F. Collins, H. Higo, L. L. Madilao, P. Pelosi, and L. J. Foster. 2018 . A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.) . Sci. Rep . 8 : 5719 . Google Scholar Crossref Search ADS PubMed WorldCat Mitaka , Y. , and K. Matsuura. 2020 . Age-dependent increase in soldier pheromone of the termite Reticulitermes speratus . J. Chem. Ecol . 46 : 483 – 489 . Google Scholar Crossref Search ADS PubMed WorldCat Mitaka , Y. , N. Mori, and K. Matsuura. 2017 . Multi-functional roles of a soldier-specific volatile as a worker arrestant, primer pheromone and an antimicrobial agent in a termite . Proc. R. Soc. B . 284 : 20171134 . Google Scholar Crossref Search ADS WorldCat Montoya , C. P. , R. J. Sutherland, and I. Q. Whishaw. 1981 . Cadaverine and burying in the laboratory rat . Bull. Psychon. Soc . 18 : 118 – 120 . Google Scholar Crossref Search ADS WorldCat Myles , T. G. 2002 . Laboratory studies on the transmission of Metarhizium anisopliae in the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae), with a method for applying appropriate doses of conidia to trapped termites for release . Sociobiology 40 : 277 – 280 . Google Scholar OpenURL Placeholder Text WorldCat Nalepa , C. A . 1994 . Nourishment and the origin of termite eusociality, pp. 57 – 104 . In J. H. Hunt and Nalepa, C. A. (eds), Nourishment and evolution in insect societies Westview Press , Boulder, CO . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Neoh , K. B. , B. K. Yeap, K. Tsunoda, T. Yoshimura, and C. Y. Lee. 2012 . Do termites avoid carcasses? Behavioral responses depend on the nature of the carcasses . PLoS One . 7 : e36375 . Google Scholar Crossref Search ADS PubMed WorldCat Noirot , C. , and J. Pasteels. 1987 . Ontogenetic development and evolution of the worker caste in termites . Experientia 43 : 851 – 860 . Google Scholar Crossref Search ADS WorldCat Pinel , J. P. , B. B. Gorzalka, and F. Ladak. 1981 . Cadaverine and putrescine initiate the burial of dead conspecifics by rats . Physiol. Behav . 27 : 819 – 824 . Google Scholar Crossref Search ADS PubMed WorldCat Pratt , S. C. , E. B. Mallon, D. J. Sumpter, and N. R. Franks. 2002 . Quorum sensing, recruitment, and collective decision-making during colony emigration by the ant Leptothorax albipennis . Behav. Ecol. Sociobiol . 52 : 117 – 127 . Google Scholar Crossref Search ADS WorldCat Prestwich , G. D. 1979 . Chemical defense by termite soldiers . J. Chem. Ecol . 5 : 459 – 480 . Google Scholar Crossref Search ADS WorldCat Prestwich , G. D. 1984 . Defense mechanisms of termites . Annu. Rev. Entomol . 29 : 201 – 232 . Google Scholar Crossref Search ADS WorldCat Prounis , G. S. , and W. M. Shields. 2013 . Necrophobic behavior in small mammals . Behav. Processes . 94 : 41 – 44 . Google Scholar Crossref Search ADS PubMed WorldCat Rosengaus , R. B. , and J. F. Traniello. 2001 . Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis . Behav. Ecol. Sociobiol . 50 : 546 – 556 . Google Scholar Crossref Search ADS WorldCat Sakagami , S. F. , and H. Fukuda. 1968 . Life tables for worker honeybees . Popul. Ecol . 10 : 127 – 139 . Google Scholar Crossref Search ADS WorldCat Schmid-Hempel , P. , and R. Schmid-Hempel. 1993 . Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects . Behav. Ecol. Sociobiol . 33 : 319 – 327 . Google Scholar Crossref Search ADS WorldCat Shelton , T . 2014 . Distance of the repellency of dead Reticulitermes flavipes (Isoptera: Rhinotermitidae) nestmates . J. Entomol. Sci . 49 : 221 – 227 . Google Scholar Crossref Search ADS WorldCat da Silva , L. H. B. , I. Haifig, and A. M. Costa-Leonardo. 2019 . Facing death: How does the subterranean termite Coptotermes gestroi (Isoptera: Rhinotermitidae) deal with corpses? Zoology (Jena) . 137 : 125712 . Google Scholar Crossref Search ADS PubMed WorldCat Strack , B. H. 1998 . The role of social behaviour of Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae) in defence against the fungal pathogen Metarhizium anisopliae (Metschikoff) Sorokin (Deuteromycotina: Hyphomycetes) . Master of Science in Forestry thesis, University of Toronto, Ontario, Canada . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Stroud , E. M. , C. P. O’Connell, P. H. Rice, N. H. Snow, B. B. Barnes, M. R. Elshaer, and J. E. Hanson. 2014 . Chemical shark repellent: Myth or fact? The effect of a shark necromone on shark feeding behavior . Ocean Coast. Manag . 97 : 50 – 57 . Google Scholar Crossref Search ADS WorldCat Su , N.-Y. , and J. P. LaFage. 1986 . Effects of starvation on survival and maintenance of soldier proportion in laboratory groups of the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae) . Ann. Entomol. Soc. Am. 79 : 312 – 316 . Google Scholar Crossref Search ADS WorldCat 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 : 1113 – 1117 . Google Scholar Crossref Search ADS WorldCat Sun , Q. , and X. Zhou. 2013 . Corpse management in social insects . Int. J. Biol. Sci . 9 : 313 – 321 . Google Scholar Crossref Search ADS PubMed WorldCat Sun , Q. , J. D. Hampton, A. Merchant, K. F. Haynes, and X. Zhou. 2020 . Cooperative policing behaviour regulates reproductive division of labour in a termite . Proc. Biol. Sci . 287 : 20200780 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Sun , Q. , K. F. Haynes, and X. Zhou. 2013 . Differential undertaking response of a lower termite to congeneric and conspecific corpses . Sci. Rep . 3 : 1 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Sun , Q. , K. F. Haynes, and X. Zhou. 2017 . Dynamic changes in death cues modulate risks and rewards of corpse management in a social insect . Funct. Ecol . 31 : 697 – 706 . Google Scholar Crossref Search ADS WorldCat Sun , Q. , K. F. Haynes, and X. Zhou. 2018 . Managing the risks and rewards of death in eusocial insects . Philos. T. R. Soc. B . 373 : 20170258 . Google Scholar Crossref Search ADS WorldCat Thorne , B . 1991 . A review of intracolony, intraspecific, and interspecific agonism in termites . Sociobiology 19 : 115 – 145 . Google Scholar OpenURL Placeholder Text WorldCat Thorne , B. L. 1990 . A case for ancestral transfer of symbionts between cockroaches and termites . Proc. Biol. Sci . 241 : 37 – 41 . Google Scholar Crossref Search ADS PubMed WorldCat Ulyshen , M. D. , and T. G. Shelton. 2012 . Evidence of cue synergism in termite corpse response behavior . Naturwissenschaften . 99 : 89 – 93 . Google Scholar Crossref Search ADS PubMed WorldCat Visscher , P. K. 1983 . The honey bee way of death: necrophoric behaviour in Apis mellifera colonies . Anim. Behav . 31 : 1070 – 1076 . Google Scholar Crossref Search ADS WorldCat Werfel , J. , K. Petersen, and R. Nagpal. 2014 . Designing collective behavior in a termite-inspired robot construction team . Science . 343 : 754 – 758 . Google Scholar Crossref Search ADS PubMed WorldCat Wilson , E. O. , N. I. Durlach, and L. M. Roth. 1958 . Chemical releasers of necrophoric behavior in ants . Psyche . 65 : 108 – 114 . Google Scholar Crossref Search ADS WorldCat Yanagihara , S. , W. Suehiro, Y. Mitaka, and K. Matsuura. 2018 . Age-based soldier polyethism: old termite soldiers take more risks than young soldiers . Biol. Lett . 14 : 20180025 . Google Scholar Crossref Search ADS PubMed WorldCat Yao , M. , J. Rosenfeld, S. Attridge, S. Sidhu, V. Aksenov, and C. Rollo. 2009 . The ancient chemistry of avoiding risks of predation and disease . Evol. Biol . 36 : 267 – 281 . Google Scholar Crossref Search ADS WorldCat Zalkow , L. H. , R. W. Howard, L. T. Gelbaum, M. M. Gordon, H. M. Deutsch, and M. S. Blum. 1981 . Chemical ecology of Reticulitermes flavipes (Kollar) and R. virginicus (Banks) (Rhinotermitidae) . J. Chem. Ecol. 7 : 717 – 731 . Google Scholar Crossref Search ADS PubMed WorldCat © The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Managing Corpses From Different Castes in the Eastern Subterranean Termite
JF - Annals of the Entomological Society of America
DO - 10.1093/aesa/saaa060
DA - 2021-01-27
UR - https://www.deepdyve.com/lp/oxford-university-press/managing-corpses-from-different-castes-in-the-eastern-subterranean-vtZP3u4uGC
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -