Source: UNIVERSITY OF FLORIDA submitted to NRP
BIOLOGY AND CONTROL OF SUBTERRANEAN TERMITES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
1004023
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Aug 14, 2014
Project End Date
Aug 10, 2019
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIVERSITY OF FLORIDA
G022 MCCARTY HALL
GAINESVILLE,FL 32611
Performing Department
Ft. Lauderdale Research and Education Center
Non Technical Summary
This project will examine the newly discovered hybridized population of two most destructive termite pest species for their damaging potential and their ability to inhabit other areas. We will explore the biological control options against termites, and develop novel control measures that are more effective and safer to the environment and human health.
Animal Health Component
34%
Research Effort Categories
Basic
33%
Applied
34%
Developmental
33%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
72106501130100%
Knowledge Area
721 - Insects and Other Pests Affecting Humans;

Subject Of Investigation
0650 - Wood and wood products;

Field Of Science
1130 - Entomology and acarology;
Goals / Objectives
1. To study the biology of economically important subterranean termites, and the interaction of previously allopatric invasive species co-existing in introduced areas2. To study termite-microbes interaction in colony defensive mechanism with the aim to explore the potential for biological control of subterranean termites3. To develop noble methods for more efficient baiting technologies against subterranean termites4. To explore the sustainable population management of subterranean termites in area-wide programs
Project Methods
Objective 1Light traps will be placed in areas known to be infested with both C. formosanus and C. gestroi during their swarming seasons to collect alates. Their species will be identified and incipient colonies will be established for each species and the hybrid combinations using the methods of Higa (1981). Temperature data of the past 20 years will be used to test our hypothesis that the extreme fluctuation in recent years may have triggered the extended swarming seasons of both species. Incipient colonies will be transferred to progressively larger containers as they grow. A few individuals will be sampled from healthy two- or three-year old hybrid colonies for DNA analysis (micro-satellite markers) to confirm the hybridization. Population size, caste composition, and biomass will be surveyed bi-annually for each colony, and morphological characteristics of hybrids will be examined for comparisons with both species. Wood-consumption rates and growth rates will be compared. To investigate the presence of viable hybrid populations in the field, special attention will be given to alates with in-between or mixed morphological characteristics of both species. Suspicious individuals will be subjected to DNA analysis for confirmation. Similar searches will be extended to field colonies of Coptotermes species for potential hybrid populations. In collaboration with H.-F. Li of National Chongshin University, similar field search for hybrid populations will be extended to southern Taiwan where these two termite species have co-existed for much longer than Florida. Hybrid alates will be mated with each other to examine if these two species are capable of inter-breeding to produce viable progenies, and hence should be considered sub-species to each other.Objective 2A malt-agar enriched with chloroamphenicol will be used to isolate fungi of genus Leucocoprinus from termite carton nest to investigate the suitability of the termite nest environment for the growth of potential beneficial fungi. One-year old incipient colonies will be provided with a choice of food source: sound wood, decomposed wood with Leucocoprinus, and decomposed wood with a brown rot fungus (Gloeophyllum trabeum), to determine if termites prefer a fungus that is known to be domesticated by other social insects. In addition, selected incipient colonies will be exclusively fed with one of the food sources and the growth of incipient colonies will be monitored for 2 years to determine if the access to Leucocoprinus influences the colony ability to grow successfully. The nitrogen fixation ability of the colony will be determined by elemental analysis, with the source of food as a factor. Finally, using soils with different organic matter content, we will determine if the termite carton nest is favorable for the growth of Leucocoprinus.In order to determine if the symbiosis described in Chouvenc et al (2013) is the result of vertical or horizontal transmission, we will establish two experiments. First, two field colonies of C. formosanus will be monitored in ground stations. The carton nest will be obtain from these stations, and samples from the soil surrounding the ground station will also be obtained at 1 m and 3 m away from the station. Both types of samples will be subjected to microbial screening to promote the growth of Streptomyces. Pure isolates of all bacterial colonies will be stored and processed for sequencing of their 16S RNA gene. The genetic diversity of Streptomyces isolates from the termite carton nest will be compared with the one from the surrounding soils using a phylogenetic analysis. The results will indicate if termites are recruiting beneficial strains of Streptomyces from their surrounding soil, and "farm" them in their carton nest in order to obtain antibiotic protection against pathogens. Second, we will test if the termites inherit the beneficial Streptomyces strains from their parent. We will identify a field colony of C. formosanus that possess alates during the swarming season. The carton nest will be sampled, along with the microbial load of the alates. Incipient colonies will be established in sterile conditions using a modified version of the rearing units described by Higa (1981). The Streptomyces diversity will be established from the original nest material, from the alates, and from 6-months incipient colonies established from alates from the same original colony, by plating serial dilution of the samples on termite fecal agar. Obtained isolates will be analyzed by sequencing their 16S RNA gene, and the profile of the Streptomyces community from the three types of samples will be compared to determine if, alates recruit the beneficial Streptomyces strain from their original nest, carry it with them, and inoculate it in their foundation. Both experiments will determine how termites interact with their symbionts and if this mutualism is an open system, with potential symbiotic turnover, as a combination of both vertical and horizontal transfer.Objective 3A liquid bait comprising a feed medium impregnated with an active ingredient (AI) at a desired concentration and a liquid carrier will be formulated for injection into voids created by termite tunneling or feeding, or into natural voids (such as internal wall cracks or tree hollows) where termites will likely enter. The AI concentration has to be slow-acting and non-repellent even following dehydration of the formulation. The liquid bait formulation of the invention has a viscosity that allows it to be injectable by using a syringe or a caulking gun. For a commercial prototype, a feed medium of 90% α-cellulose and 10% wood flour decayed with G. trabeum and impregnated with hexaflumuron at 0.5% (AI wt/wt) will be prepared for testing. The liquid bait formulation will contain nine parts of the impregnated feeding medium mixed with one part of 1% methylcel solution to yield 10% dry weight feeding medium in 1% methylcel solution. The prototype liquid baits will be tested in laboratory arenas with simulated termite galleries in wood by using data from our termite tunneling study (Su et al. 2004). Termites of both Coptotermes and Reticulitermes species will be placed in the arenas before the liquid baits are injected into one portion of the simulated galleries. Termite mortalities will recorded at 4, 6, and 8 weeks for comparison with untreated control. Following the laboratory results, field trials will be conducted against colonies of Coptotermes and Reticulitermes species by using the protocol similar to previous field studies with baits (Su 1994, Su et al. 1995, 1997).Objective 4Sentricon HD, a commercial bait product based on the concept of durable baits described by Su (2007) and an UF patent (US7,169,403 B2), have been applied in the Armstrong Park since 2009. After the intense feeding of Sentricon HD in 2009-2011, termite activities have declined substantially, and since 2013, almost no termites have been detected. The results validated the hypothesis that durable baits can be placed in soil to intercept and eliminate invading and/or emerging termite populations before causing substantial damage to structures. The baiting with Sentricon HD probably eliminated several C. formosanus colonies near the borders of the Park, and thus the probability of re-invasion by neighboring colonies may have been reduced. The next phase of this area-wide project is to remove all Sentricon HDs from the site and to observe (by using IG monitoring stations) how long it may take for a re-invasion to occur. This is done in anticipation that some homeowners may stop using baits when termites are no longer found in the stations over an extended period.

Progress 10/01/17 to 09/30/18

Outputs
Target Audience:Pest control management industry, homeowners, manufacturers and research community Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?"Potential of area-wide management program for subterranean termites," Cook Pest Control, Birmingham, AL. Jan. 15-16, 2018 "Conceptualization of termite baiting system and development of Sentricon," Dow AgSci., Davie, FL, May 3, 2018. "Sciences behind termite baiting system," Sentricon Partnership meeting, Davie, FL, Sep. 25, 2018 "Termite lesson of a lifetime: From population sampling techniques to population management technologies," University of Kentukey Pest Control Short Course, Lexington, KY, Nov. 5-7, 2018 "Target species," Fumigation School, Ft. Lauderdale, FL, Nov. 16, 2018 How have the results been disseminated to communities of interest?Lee, S.-B, T. Chouvenc, and N.-Y. Su. 2018. Individual foraging behavior of the Formosan subterranean termite. Annual Mtng. Florida Entomol. Sco. St. Augustin, FL, Jul. 22-25. Status: Co-author. Tong, R., and N.-Y. Su. 2018. Addition of exuviae to young Coptotermes gestroi (Wasmann) colonies increases biomass gained in a nitrogen-poor environment. Annual Mtng. Florida Entomol. Sco. St. Augustin, FL, Jul. 22-25. Status: Co-author. Patel, J., T. Chouvenc, and N.-Y. Su. 2018. Colony growth and wood consumption rates of the two invasive Coptotermes species and their hybrids over a four-year period. Annual Mtng. Florida Entomol. Sco. St. Augustin, FL, Jul. 22-25. Status: Co-author. Velenovsky, J., T. Chouvenc, F. Martini, G. H. Gile, and N.-Y. Su. 2018. Quantitative changes in symbiotic parabasalids within Coptotermes gestroi (Wasmann) (Insecta: Blattodea: Rhinotermitidae) kings and queens during incipient colony development. Annual Mtng. Florida Entomol. Sco. St. Augustin, FL, Jul. 22-25. Status: Co-author. Su, N.-Y. 2018. Formosan subterranean termite in Florida and its control. Annual Mtng. Florida Entomol. Sco. St. Augustin, FL, Jul. 22-25. Status: Invited speaker. Patel, J, T. Chouvenc, and N.-Y. Su. 2018. Colony growth and wood consumption rates of incipient colonies of two invasiveCoptotermesspecies and their hybrids. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. Tong, R., and N.-Y. Su. 2018. Addition of exuviae to incipientCoptotermes gestroi (Wasmann) colonies increases biomass gained in a nitrogen-poor environment. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. Lee, S.-B., D. Aguilera-Olivares, A. Mullins, T. Chouvenc, and N.-Y. Su. 2018. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. Velenovsky, J., F. Martini, T. Chouvenc, G. H. Gile, and N.-Y. Su. 2018. Coptotermes gestroi (Wasmann) and Coptotermes formosanus Shiraki (Blattodea: Rhinotermitidae) hybrids harbor an integrated protozoan community composed of protozoa from both parental communities. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. Mullins, A., and N.-Y. Su. 2018. Nitrogen fixation across termite lineages and diets. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. Su, N.-Y., and Am. Mullins. 2018. Masking feeding deterrence of bait toxicants with phagostimulants. Nitrogen fixation across termite lineages and diets. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Speaker. Patel, J, T. Chouvenc, and N.-Y. Su. 2018. Soldier morphology in hybrid termites of the two invasive Coptotermes species. Annual Mtng. Entomol. Soc. America, Vancouver, Canada, Nov. 11-14. Status: Co-author. What do you plan to do during the next reporting period to accomplish the goals?Development of commercial prototype fluid baits and their field testing. Laboratory testing of ecdysteroids as bait toxicants to reduce colony elimination time. To study the biology of C. formosanus x C. gestroi hybrid populations. To examine the nitrogen economy of termite colonies.

Impacts
What was accomplished under these goals? Studies on the molting behavior of termites under the influence of chitin synthesis inhibitors (CSIs) showed that CSI-affected workers return to the central nest and died in the vicinity of reproductives and eggs. The aversion to the dead and decaying workers caused reproductives and brood to leave the original central nest site in a colony and refuge at newer sites every few days in response to newly dead workers near them. Hence the reproductives continued to move to new sites but only to be surrounded by dead termites, and the cycle repeats itself until the entire colony is killed. The results led the formulation of the hypothesis that molt-accelerating compounds such as ecdysteroids may cause the similar death chase as in CSI-affected colonies and may be used in baits to kill a termite colony. A laboratory study showed that termites exposed to the ecdysteroid, 20-hydroxyecdyson (20E) exhibited symptoms of hyperecdysonism before the onset of death, and times required for 20E to fully express its effects were 10-13 days. Because the lethal time of a CSI is equivalent to the molting time of termites, i.e. 45 days, as a bait toxicant 20E may reduce the colony elimination time. Field trains were conducted in which fluid baits were injected through drill holes behind infested wood surface and bypassed the difficulties for installing above-ground (AG) bait stations on uneven surface or at tight corners. All baited colonies were eliminated. Because a large quantity of fluid baits could be applied at once, termite control professionals may be able to avoid revisiting the site to add more baits. The absence of unsightly AG station in a house will also make fluid baits more acceptable to homeowners than AG baits. Currently, local applications of liquid termiticides are common practices because termite control professionals are often urged by homeowners to take remedial actions when termites are found in a house, but such treatments only drive termites away from the active loci without affecting the termite colony(s). Remedial treatments with fluid baits would result in immediate bait consumption and shorten colony elimination time with or without the use of in-ground baiting systems. Introduction of fluid baits will add another tool to the termite control industry and will make it more plausible for the homeowners to accept baiting technology.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kakkar, G., and N.-Y. Su 2018. Molting drives mortality in foraging populations of Formosan subterranean termites (Isoptera: Rhinotermitidae) baited with a chitin synthesis inhibitor, noviflumuron. Pest Management Sci. 74: 219224. DOI 10.1002/ps.4699 Kakkar, G., W. Osbrink, and N.-Y. Su. 2018. Molting site fidelity accounts for colony elimination of the Formosan subterranean termites (Isoptera: Rhinotermitidae) by chitin synthesis inhibitor baits. Sci. Reports, 8:1259. DOI:10.1038/s41598-018-19603-8 Mullins, A., and N.-Y. Su. 2018. Parental nitrogen transfer and apparent absence of N2 fixation during colony foundation in Coptotermes formosanus Shiraki. Insects, 9: 37. DOI: http://dx.doi.org/10.3390 Su, N.-Y., B. Yokum, A. J. Mullins, E. Bordes, C. Cotonne, and C. Riegel. 2018. Field evaluations of fluid baits against colonies of the Formosan subterranean termite (Blattodea: Rhinotermitidae). J. Econ. Entomol. 111: 18061812. DOI: https://doi.org/10.1093/jee/toy153 Carnohan, L. and N.-Y. Su. 2018. Mortality time trends of three subterranean termite species when exposed to 20-hydroxyecdysone, alone and in combination with noviflumuron. J. Econ. Entomol. 111: 23122316. doi: 10.1093/jee/toy186 Foley, J. R. IV, T. Chouvenc, R. M. Giblin-Davis, N.-Y. Su, and N. Kanzaki. 2018. Phoresy and within-colony transmission of nematodes associated with alates of subterranean termites (Isoptera: Rhinotermitidae). Environ. Entomol. 47: 1107-1116 Chouvenc, T., H.-F. Li, and N.-Y. Su. 2018. Connecting termite researchers from around the world at ICE 2016. American Entomologists. 64: 152-154 Chouvenc, T., M. L. Elliott, J. `obotn�k, C. A. Efstathion, and N.-Y. Su. 2018. The termite fecal nest: A framework for the opportunistic acquisition of beneficial soil Streptomyces (Actinomycetales: Streptomycetaceae). Environ. Entomol. 47: 1431-1439. https://doi.org/10.1093/ee/nvy152


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Pest control management industry, manufacturers, and research community Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?Research results were disseminated by 10 papers presented as follow: Su, N.-Y., W. Osbrink, G. Kakkar, A. Mullins, and T. Chouvenc. 2017. Foraging distance and caste composition of incipient colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in laboratory extended arenas. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Presenting author. Lee, S.-B, T. Chouvenc, and N.-Y. Su. 2017. A comparison of movement activity among two Coptotermes species and their hybrids. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Foley, J., T. Chouvenc, R. Giblin-Davis, and N.-Y. Su. 2017. Phoresy and within-colony transmission of nematodes associated with alates of subterranean termites (Isoptera: Rhinotermitidae). Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Carnohan, L., N.-Y. Su, and S. Gezan. 2017. Evaluation of the 20-hydroxyecdysone deterrence threshold for C. formosanus, C. gestroi, and R. flavipes with comparison to noviflumuron. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Velenovsky, J., T. Chouvenc, G. Gile, and N.-Y. Su. 2017. Identification of protozoa in Coptotermes gestroi (Wasmann) (Blattodea: Rhinotermitidae) and quantitative changes in protozoan density within kings and queens during colony development. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Mullins, A., and N.-Y. Su. 2017. Nitrogen sources for the Formosan subterranean termite. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Chouvenc, T., and N.-Y. Su. 2017. "That baby ain't that cute": Developmental instability in young termite colonies. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Mullins, A., and N.-Y. Su. 2017. Nitrogen inventories and nitrogenase expression rates of a drywood and a subterranean termite. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Patel, J., T. Chouvenc, and N.-Y. Su. 2017. Comparison of temperature dependent survivorship and wood consumption rate among two subterranean termite species (Isoptera: Rhinotermitidae: Coptotermes) and their hybrid. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. Mullins, A., and N.-Y. Su. 2017. Nitrogen fixation in different termite lineages and diets. Annual Mtng. Entomol. Soc. America, Denver, CO, Nov. 5-8. Status: Co-author. What do you plan to do during the next reporting period to accomplish the goals?Explore the potentials of ecdysonsteroids as bait toxicants that my reduce time requited to eliminate termite colonies. Examine the possibility of C. formosanus x C. gestroi hybrid populations in the urban South Florida. Determine the biological characteristics of the hybrid population, including their colony growth rate, wood consumption rate, temperature tolerance and preference, and insecticide susceptibility.

Impacts
What was accomplished under these goals? As C. formosanus colonies mature, older individuals move out of nest to forage for food more frequently than younger workers, and only 15-20% of colony population engaged in foraging activity. The rest of the younger individuals stay near the main nest and engaged in other activities such as feeding and caring of broods and nest maintenance. This finding implies that, if a house is treated with CSI baits, foragers that consumed baits are unaffected until they molt, but since younger termites molt more often than older individuals, the younger instars die first, leaving the colony with older termites that eventually die when they molt. The finding illustrates the dynamics of lethal process of CSIs in baited colonies and will offer further clues to improve baiting technologies. Spatial assessment of molting in C. formosanus workers showed that molting individuals were found exclusively in the central nest, which suggested that speeding up the time for mortality induced by molting will not result in an inhibitory cascade of dead termites around the bait stations. Thus, speeding up the elimination of a C. formosanus colony using molt-accelerating compounds will not lead to secondary repellency. Laboratory evaluation study showed hyperecdysonism-generated mortality of C. formosanus and R. flavipes when exposed to ecdysone and 20-hydroxyecdysone (20E). Both ecdysteroids induced ecdysis, hence will not lead to secondary repellency, but their lethal time of 12 days is shorter than that of a CSI (45 d), thus the baiting time should be reduced bymore than a month when they are incorporated in termite baits. Since the observation of simultaneous flights by two invasive termite species, C. formosanus and C. gestroi in 2013, interspecific mating were confirmed in the laboratory, but it remains unclear if the hybrid populations are present in the field. Genetic genotyping and cuticular hydrocarbons profile techniques were developed to identify field hybrid populations and to determine if South Florida has become the hybrid zone of these two most economically important termite pests in the world.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Du, H., T. Chouvenc, W. L. A. Osbrink, and N.-Y. Su. 2017. Heterogeneous distribution of castes/instars and behaviors in the nest of Coptotermes formosanus Shiraki. Insect. Soc. 64: 103-112. DOI: http://dx.doi.org/10.1007/s00040-016-0520-0 Du, H., T. Chouvenc, and N.-Y. Su. 2017. Development of age polyethism with colony maturity in Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ. Entomol. 46: 311-318. doi: 10.1093/ee/nvw162 Su, N.-Y., T. Chouvenc, and H.-F. Li. 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects. doi:10.3390/insects8010014 Bernard, S., W. Osbrink, and N.-Y. Su. 2017. Response of the Formosan subterranean termite to neighboring con-specific populations after baiting with noviflumuron. 110: 575583. doi: 10.1093/jee/tow317 Su, N.-Y., W. Osbrink, G. Kakkar, A. Mullins, and T. Chouvenc. 2017. Foraging distance and population size of juvenile colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in laboratory extended arenas. J. Econ. Entomol. 110: 1728-1735. doi: 10.1093/jee/tox153 Su, N.-Y., and E. J. Monteagudo. 2017. Hyperecdysonism in the Formosan subterranean termite and eastern subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 110: 1736-1739. doi: 10.1093/jee/tox178 Chouvenc T., R.H. Scheffrahn, A. J. Mullins and N.-Y. Su. 2017. Flight phenology of two Coptotermes species (Isoptera: Rhinotermitidae) in southeastern Florida. J. Econ. Entomol. 110: 1693-1704. doi: 10.1093/jee/tox136 Chouvenc T., M. Basille, and N.-Y. Su. 2017. Role of accelerated developmental pathway and limited nurturing capacity on soldier developmental instability in subterranean termite incipient colonies. Insect. Soc. 64: 477-483. DOI: 10.1007/s00040-017-0566-7 Chouvenc, T., S. Osorio, S. Chakrabarti, E. E. Helmick, H.-F. Li, and N.-Y. Su. 2017. Assessment of genetic markers for the determination of Coptotermes formosanus � Coptotermes gestroi hybrids. Florida Entomol. 100: 657-659. DOI: 10.1653/024.100.0325 Chouvenc, T., and N.-Y. Su. 2017. Testing the role of predominant cuticular hydrocarbons on intercolonial agonism in two subterranean termite species (Coptotermes) and their hybrids. Insect. Soc. 64: 347-355. DOI: 10.1007/s00040-017-0552-0 Chouvenc, T., and Su N-Y. 2017. Irreversible transfer of brood care duties and insights on the burden of caregiving in incipient subterranean termite colonies. Ecological Entomology. 42: 777-784. DOI: 10.1111/een.12443 Zukowski, J. G, and N.-Y. Su. 2017. Survival of termites (Order: Isoptera) exposed to different levels of relative humidity (RH) and water availability and their RH preferences. Florida Entomol. 100: 532-538. DOI: 10.1653/024.100.0307 Kakkar, G., W. Osbrink, A. Mullins, and N.-Y. Su. 2017. Molting site fidelity in workers of Formosan subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 110: 25122517. doi: 10.1093/jee/tox246 Chouvenc, T., and N.-Y. Su. 2017. Subterranean termites feeding on CSI baits for a short duration still results in colony elimination. J. Econ. Entomol. 110: 2534-2538. doi: 10.1093/jee/tox282 Mevers, E, T. Chouvenc, N.-Y. Su, and J. Clardy. 2017. Chemical interaction among termite-associated microbes. J. Chem. Eco. 43:1078-1085. https://doi.org/10.1007/s10886-017-0900-6
  • Type: Book Chapters Status: Published Year Published: 2017 Citation: Cottone, C.B. and N.-Y. Su. 2017. Survival of Formosan subterranean termite colonies during periods of flooding. In P. Dhang [ed.], pp. 65-79. Climate Change: Effects on Urban Pests. CAB International, Boston, MA.


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:Research community, termite control industry and product manufacturers, and homeowners. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?Research results were disseminated by 10 papers presented by my team as follow: Su, N.Y. 2016. Science and innovation in academia. Florida University Board of Governor meeting. March 26, Pensacola, FL. Status: Presenting author. Su, N.-Y. 2016. A lasting impact of a mentor, in science and in person. A symposium honoring Professor Minoru Tamashiro's contribution to entomology: His legacy and academic genes. Annual Mtng. Pacific Branch Entomol. Soc. America, April 3-6, Honolulu, HI. Status: Symposium organizer and presenting author. Li, H.-F., and N.-Y. Su. 2016. Formosan subterranean termite and Taiwanese: A hundred-year journey of seeking the truth and solution. A symposium honoring Professor Minoru Tamashiro's contribution to entomology: His legacy and academic genes. Annual Mtng. Pacific Branch Entomol. Soc. America, April 3-6, Honolulu, HI. Status: Author. Su, N.-Y. 2016. From population sampling techniques to population management technologies for subterranean termites: A scientific account for the development of Sentricon Termite Colony Elimination System. Sentricon authorized operator annual meeting. April 4, Honolulu, HI. Status: Presenting author. Su, N.-Y. 2016. The rise and fall of the Formosan subterranean termite colonies in Louis Armstrong Park, New Orleans, LA. 1999 - 2014. A seminar for Terminix and DowAgroSci. July 26-27, Memphis, TN. Su, N.-Y. 2016. Insects in Japanese tradition and culture. Symposium: Insects and the global human experience. XXV Int'l. Congress of Entomol. Sep. 25-30. Orlando, FL. Status: Presenting author. Chouvenc, T., and N.-Y. Su. 2016. Hybridization between two termite invaders, Coptotermes formosanus and C. gestroi: Opportunities for gene flow between species. Symposium: Invasive termite species: Where are they from, where are they now, and where will they be? XXV Int'l. Congress of Entomol. Sep. 25-30. Orlando, FL. Status: Symposium organizer and author. Bernard, S., and N.-Y. Su. 2016. Laboratory response of the eastern subterranean termite, Reticulitermes flavipes, to neighboring populaitons of the Formosan subterranean termite, Coptotermes formosanus, baited with noviflumuron. XXV Int'l. Congress of Entomol. Sep. 25-30. Orlando, FL. Status: Author. Carnohan, L., and N.-Y. Su. 2016. The Asian subterranean termite, Coptotermes gestroi, baited with insect growth regulators in extended foraging arenas. XXV Int'l. Congress of Entomol. Sep. 25-30. Orlando, FL. Status: Author. Foley, J., and N.-Y. Su. 2016. Vertical transfer of nematodes associated with alates of Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae). XXV Int'l. Congress of Entomol. Sep. 25-30. Orlando, FL. Status: Author. What do you plan to do during the next reporting period to accomplish the goals?Continue on-going research and attend professional meetings

Impacts
What was accomplished under these goals? Temperature preferences of four subterranean termite species, C. gestroi, C. formosanus, R. virginicus, and R. flavipes, and effects of temperature on their survivorship and wood-consumption rate were studied. The result showed that Reticulitermes spp. preferred significantly lower temperatures than Coptotermes spp. R. flavipes survived at 10 °C but not at 35 °C. whereas C. gestroi did not survive at 10 °C, but the wood-consumption rate at 35 °C was significantly higher than those of other temperatures. The results account for the geographic distributions of the four termite species, including the co-existence of C. formosanus and C. gestroi in metropolitan southeastern Florida. Termite records from 1990 to 2015 suggest that the ranges of the distribution of these two invasive species have increased exponentially during this time frame, which raises concerns about potential structural damage in this urbanized area that includes 6 million residents. We argue that the subterranean termite problem in metropolitan southeastern Florida is still in its early phase of invasion, and we predict that the distribution and structural infestations by Coptotermes will continue to increase in the years to come, with an estimated 50% of all structures in southeastern Florida at risk by 2040. Durable baits, Recruit HD were installed in 45 Sentricon stations between September 2010 and July 2014 in the 32-acre Armstrong Park, New Orleans. After eliminating all detectable termite colonies in the Park, six to 12 months elapsed before new activity was detected. Newly invading termite colonies were usually found near the Park border or were smaller colonies that originated from recently paired alates. After colony elimination, Recruit HD baits were left in the stations to intercept newly invading colonies of subterranean termites, leading to their elimination, and multiple cycles of such interception and elimination events were recorded. Because the presence of Recruit HD baits continues to eliminate incoming colonies with little effort in maintaining and resupplying baits in the target areas, the bait system offers an economically sustainable option for managing subterranean termite populations in a large area. The 32-acre Armstrong Park is a manageable size to carry out an area-wide (AW) project. If the number of such AW projects is gradually increased over time in selected metro areas of New Orleans, we predict that we may be able to turn the tide against the ever increasing populations of C. formosanus in the entire city. Recognition of the incidence of molting in worker termites is challenging because of their successive stationary molt, asynchronous molting among individuals, cryptic behavior, a soft and poorly sclerotized cuticle, and they immediately consume the shed exuvia of nestmates. A method was developed to quantify the degree of sclerotization of the mouthparts in newly molted workers of C. formosanus, and was used to determine if an individual has molted within a 36-h time frame. Using this method, molt frequency of C. formosanus workers was determined so as to provide insights into potential methods of reducing the time to eliminate a CSI-baited colony. The results from a time lapse study on foraging population of workers showed that on average there is a 44-d intermolt period for second-instar workers molting to third instar and 45 d for third-instar workers molting to fourth instar. Information from this study suggests that time to molt is an important component of total time for eliminating colonies treated with CSI baits and reduction in time lapse between two consecutive molts may reduce the time required for colony elimination.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Cao, R., and N.-Y. Su. 2016. Temperature preferences of four subterranean termite species (Isoptera: Rhinotermitidae) and temperature-dependent survivorship and wood-consumption rate. Ann. Entomol. Soc. Am. 109: 64-71. DOI: http://dx.doi.org/10.1093/aesa/sav095
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kakkar, G., T. Chouvenc, and N.-Y. Su. 2016. Postecdysis sclerotization of mouthparts of the Formosan subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 109: 792-799. DOI: 10.1093/jee/tov394
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Su, N.-Y., E. Guidry, A. J. Mullins, and C. Cotonne. 2016. Reinvasion dynamics of subterranean termites (Isoptera: Rhinotermitidae) following the elimination of all detectable colonies in a large area. J. Econ. Entomol. 109: 809-814. DOI: 10.1093/jee/tow018
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Su, N.-Y., E. Guidry, and C. Cotonne. 2016. Sustainable management of subterranean termite populations (Isoptera: Rhinotermitidae) in Armstrong Park, New Orleans, with durable baits. J. Econ. Entomol. 109: 1326-1332. DOI: 10.1093/jee/tow051
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Chouvenc, T., R. H. Scheffrahn, and N.-Y. Su. 2016. Establishment and spread of two invasive subterranean termite species (C. formosanus and C. gestroi; Isoptera; Rhinotermitidae) in metropolitan southeastern Florida (1990-2015). Florida Entomol. 99: 187-191.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Scheffrahn, R. H., H. H. Hochmair, F. Tonini, J. K?e?ek, N.-Y. Su, P. Fitzgerald, K. Hendricken, J. A. Chase, J. Mangold and J. Olynik. 2016. Proliferation of the invasive termite Coptotermes gestroi (Isoptera: Rhinotermitidae) on Grand Cayman and overall termite diversity on the Cayman Islands. Florida Entomol. 99: 496-504. DOI: http://dx.doi.org/10.1653/024.099.0323
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Du, H., T. Chouvenc, W. L. A. Osbrink, and N.-Y. Su. 2016. Social interactions in the central nest of Coptotermes formosanus juvenile colonies. Insect. Soc. DOI: http://dx.doi.org/10.1007/s00040-016-0464-4
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kakkar, G., T. Chouvenc, W. Osbrink, and N.-Y. Su. 2016. Temporal assessment of molting in workers of Formosan subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 109: 2175-2181. http://doi: 10.1093/jee/tow180


Progress 10/01/14 to 09/30/15

Outputs
Target Audience:National and internation research comminity in termitology, termite control industry, and foregin government agencies in charge of termite management. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?Research results were dissminated by 12 papers presented by team in three meeting as follow: Su, N-Y. 2015. When the Formosan and Asia subterranean termite meet. Annual Mtng. Southeastern Branch Entomol. Soc. America, Biloxi, MS, March 15-18. Status: Author. Carnohan, L., and N.-Y. Su. 2015. Comparative effects of 20-hydroxyecdysone and noviflumuron against the Formosan subterranean termite. Annual Mtng. Southeastern Branch Entomol. Soc. America, Biloxi, MS, March 15-18. Status: Co-author. Kakkar, G., and N.-Y. Su. 2015. Efficacy of slow acting chitin synthesis inhibitor baits onCoptotermes formosanus(Isoptera: Rhinotermitdae) in linearforaging arenas. Annual Mtng. Southeastern Branch Entomol. Soc. America, Biloxi, MS, March 15-18. Status: Co-author. Su, N.-Y., E. Guidry, and C. Cottone. 2015. The Rise and Fall of Formosan Subterranean Termite Colonies in Louis Armstrong Park, New Orleans, 2004 - 2014. Annual Mtng. FL Entomol. Soc., Ft. Myer, FL, Aug. 2-5. Status: Author Su, N.-Y., B. P. Yokum, E. Bordes, C. Cottone, and C. Riegel. 2015. Field trials of fluid baits for remedial control of the Formosan subterranean termite. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Author Bernard, S., and N.-Y. Su. 2015. Laboratory response of the eastern subterranean termite, Reticulitermes flavipes,to neighboring populations of the Formosan subterranean termite,Coptotermes formosanus,baited with noviflumuron. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Mullins, A., and N.-Y. Su. 2015. Nitrogen fixation in Cryptocercus punctulatus Scudder (Blattodea: Cryptocercidae) and lower termites (Isoptera: Kalotermitidae, Rhinotermidae). Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Carnohan, L., N.-Y. Su, and S. Gezan. 2015.The dose-independent lethal time of 20-hydroxyedysone ingested by Formosan subterranean termites. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Du, H., W. Osbrink, and N.-Y. Su. 2015. Primary elements of age polyethism in workers from the central nest of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Chouvenc, T., and N.-Y. Su. 2015. From foundation to death: Differential caste investment during the life of a termite colony. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Kakkar, G., and N.-Y. Su. 2015. Spatial distribution of mortality of CoptotermesformosanusShiraki (Isoptera: Rhinotermitidae)exposed to chitin synthesis inhibitor or metabolic inhibitor in extended foraging arenas. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author Chouvenc, T., E. Helmick, and N.-Y. Su. 2015. Hybridization of two termite invaders: Causes and consequences. Annual Mtng. Entomol. Soc. America, Minneapolis, MN, November 15 - 18. Status: Co-author. What do you plan to do during the next reporting period to accomplish the goals?To present research results in nantional and international professional meetings

Impacts
What was accomplished under these goals? The Formosan subterranean termites (Coptotermes formosanus) and Asian subterranean termites (C. gestroi) are both ecologically successful and are the two most economically important termite pests in the world. Both species have spread throughout many areas of the world due to human activity; however, their distributions overlap in only three narrow areas because of distinct ecological requirements. In south Florida, where C. formosanus and C. gestroi are both invasive, the dispersal flight seasons of both species overlapped for the first time on record in 2013 and 2014. Pairings of heterospecific individuals were readily observed in the field and C. gestroi males preferentially engaged in mating behavior with C. formosanus females rather than females from their own species. In the laboratory, heterospecific and conspecific pairings had an equal colony establishment rate, but heterospecific incipient colonies had twice the growth rate of conspecific incipient colonies, suggesting a potential case of hybrid vigor. As all prezygotic barriers were lifted between the two species in the field, the apparent absence of post-zygotic barriers in the laboratory raises the possibility for introgressive hybridization in south Florida. While laboratory observations remain to be confirmed in the field, and the alate hybrid fertility is currently unknown, our results raise a tangible concern about the hybridization of two major destructive pest species. Such hybridization would likely be associated with a new economic impact. C. formosanus is particularly known for its tendency to establish populations in nonendemic areas via maritime vessels as well as human-aided transport of infested materials. The natural spread of this species after new introductions occurs in part by dispersal flights originating from mature colonies. Dispersal flight activity is also the primary variable for the evaluation of area-wide management programs. Data collected by mark-recapture of C. formosanus alates over 12 individual evenings of dispersal flights in the New Orleans French Quarter indicated that for one selected flight dispersal location, which was not affected by a high density of trap locations nearby, alates flew on average 621 m from their parent colony. A new record of a 1,300-m dispersal flight was recorded. Spatial analysis showed that neither wind nor light affected the direction of flight, which may be attributed to scarce light and wind measurements in the study region. A fluid-bait, comprised of α-cellulose and fine-ground phagostimulants (Summon Preferred Food Source) impregnated with 0.5% hexaflumuron (AI wt/wt) and mixed with 1% methylcel solution to yield 10% dry weight, was injected into simulated foraging galleries of C. formosanus and the eastern subterranean termite, Reticulitermes virginicus (Banks) for a laboratory efficacy evaluation. Six wks after the injection, mortalities for both species exceeded 90%, and all termites died by the 8th wk. The fluid-bait can be applied internally through a small drill hole in a tight spot with any surface contour and may bypass many problems associated with the AG system that has to be installed externally on the walls or wood surface. When injected into an active gallery of termites in a structure, a tree or in soil, the fluid baits may be fed immediately by termites to achieve the colony elimination. Following the elimination of all detectable termite colonies in the 32-acre Louis Armstrong Park in New Orleans, LA in 2002 - 2003, termite activity was monitored by using 808 Sentricon stations equipped with Electronic Sensing and Monitoring system. Between January 2004 and July 2005, termites were found in 8 - 11 stations. In August 2005, the Park was flooded by Hurricane Katrina, but termites remained active. Post-Katrina termite activity levels of 16 - 21 stations were recorded throughout 2006, and in October 2007 the activity drastically increased to 43 stations. This rapid increase of termite activity continued into 2008, and a total of 94 stations harbored termite activities by July 2008. Termite activity peaked at 109 stations in September 2008 then leveled down to 64 stations in March 2009. Termite activity in the Park between 2004 and 2009 was described by a Sigmoid model with a carrying capacity of 76 stations, and a Sigmoid mid-point of 1,202 d. In April 2009, a total of 14 colonies of C. formosanus and one colony of R. flavipes were delineated by using microsatellite genotyping and mark-recapture protocol. Of the 15 colonies, eight near the Park border probably originated from existing colonies from outside, and seven C. formosanus colonies found inside the Park were probably initiated by alate pairs. Our results showed that, if surrounded by high population pressure of termites and no control measures are applied, an area cleared of termite populations by baits can be completely re-populated by termites from outside in 53 mon.

Publications

  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., M. Basille, and N.-Y. Su. 2015. The production of soldiers and the maintenance of caste proportions delay the growth of termite incipient colonies. Insect. Soc. 62: 2329 (DOI 10.1007/s00040-014-0369-z)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Su, N.-Y. 2015. A fluid-bait for remedial control of subterranean termites. J. Econ. Entomol. 108: 274-276 (DOI: 10.1093/jee/tou039)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Su, N.-Y. 2015. Current state of the Florida Entomological Society  2014 FES presidential address. Florida Entomol. 98: 815-817
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Mullins, A. J., M. Messenger, H. H. Hochmair, F. Tonini, N.-Y. Su, and C. Riegel. 2015. Dispersal flights of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 108: 702-719 (DOI: 10.1093/jee/tov022)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., E. E. Helmick, and N.-Y. Su. 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS ONE 10: e0120745 (doi:10.1371/journal.pone.0120745)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Li, H.-F., Y.-C. Lan, I. Fujisaki, N. Kanzaki, H.-J. Lee, and N.-Y. Su. 2015. Termite assemblage pattern and niche partitioning in a tropical forest ecosystem. Environ. Entomol. (doi: 10.1093/ee/nvv038)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., A. J. Mullins, and N.-Y. Su. 2015. Territorial status-quo between the big-headed any (Hymenoptera: Formicida) and the Formosan subterranean termite (Isoptera: Rhinotermitidae). Florida Entomol. 98: 157-161.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Cottone, C. B., N.-Y. Su, R. H. Scheffrahn, and C. Riegel. 2015. Survivorship of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in a hypoxic environment. Sociobiology 62: 76-81 (DOI: 10.13102/sociobiology.v62i1.76-81)
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Scheffrahn, R. H., T. F. Carrijo, J. Krecek, N.-Y. Su, A. L. Szalanski, J. W. Austin, and J. Mangold. 2015. A single endemic and three exotic species of the termite genus Coptotermes (Isoptera: Rhinotermitidae) in the New World. Arthropod Systematics and Phylogyny, 73: 333-348.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., and N.-Y. Su. 2015. How do entomologists consume and produce their sciences? American Entomol. 61: 252-257
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., H.-F. Li, J. Austin, C. Bordereau, T., Bourguignon, S. L. Cameron, E. M. Cancello, R. Constantino, A. Costa-Leonardo, P. Eggleton, T. A. Evans, B. Forschler, J. K. Grace, C. Husseneder, J. Crecek, C.Y. Lee, T. Lee, N. Lo, M. Messenger, A. Mullins, A. Robert, Y. Roisin, R. H. Scheffrahn, D. Sillam-Dusses, J. Sobotnik, A. Szalanski, Y. Takematsu, E. L. Vargo, A. Yamada, T. Yoshimura, and N.-Y. Su. 2015. Revisiting Coptotermes (Isoptera: Rhinotermitidae): a global taxonomic road map for species validity and distribution of an economically important subterranean termite genus. Systematic Entomol. DOI: 10.1111/syen.12157
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Cao, R., and N.-Y. Su. 2015. Temperature Preferences of Four Subterranean Termite Species (Isoptera: Rhinotermitidae) and Temperature-Dependent Survivorship and Wood-Consumption Rate. Ann. Entomol. Soc. Am. DOI: http://dx.doi.org/10.1093/aesa/sav095
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chouvenc, T., A. J. Mullins, and N.-Y. Su. 2015. Rare production of nymphs in an Asian subterranean termite (Isoptera: Rhinotermitidae) incipient colony. Florida Entomol. 98: 972-973.


Progress 08/14/14 to 09/30/14

Outputs
Target Audience: Termite control industry and research community Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Presented at the national conference of the Entomological Society of America What do you plan to do during the next reporting period to accomplish the goals? Cotinue the objectives 1-4.

Impacts
What was accomplished under these goals? 1. Collected and initiated hydrid incipient colonies of two invasive species, C. formosanus and C. gestroi 2. Identified some of the chemcials produced by bacterias with anti-fungal properties 3. Field tested fluid bait formulaiotn 4. Coninue to monitor the large area control efforts in a field site in New Orleans

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Bujang, N. S., N. A. Harrison, and N.-Y. Su. 2014. Molecular cloning of five beta-glucosidases from four species of higher termites. Ann. Entomol. Soc. Am. 107: 251-256 (DOI: http://dx.doi.org/10.1603/AN13012) Bujang, N. S., N. A. Harrison, and N.-Y. Su. 2014. A phylogenetic study of endo-beta-1,4-glucanase in higher termites. Insectes Sociaux 61: 29-40 (http://dx.doi.org/10.1007/s00040-013-0321-7) Cao, R., and N.-Y. Su. 2014. Tunneling and food transportation activity of four subterranean termite species (Isoptera: Rhinotermitidae) at various temperatures. Ann. Entomol. Soc. Am. 107: 696-701 (http://www.bioone.org/doi/full/10.1603/AN13181) Xing, L., T. Chouvenc, and N.-Y. Su. 2014. Behavioral and histological changes in the Formosan subterranean termite (Isoptera: Rhinotermitidae) induced by the chitin synthesis inhibitor noviflumuron. J. Econ. Entomol. 107: 741-747 (http://www.bioone.org/doi/full/10.1603/EC13254) Chouvenc, T., and N.-Y. Su. 2014. Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insectes Sociaux 61: 171182 (http://dx.doi.org/10.1007/s00040-014-0343-9) Su, N.-Y. 2014. Asian Americans in entomology, and the future of science and engineering workforce in the United States. American Entomol. 60: 147-149 Su, N.-Y. 2014. Tokoyo no Kami, a caterpillar worshiped by a cargo cult in ancient Japan. American Entomol. 60: 182-188 Chouvenc, T., M. Basille, H.-F. Li, and N.-Y. Su. 2014. Developmental instability in incipient colonies of social insects. PloS one 9: e113949 (DOI: 10.1371/journal.pone.0113949)