On the Chemical Disguise of a Physogastric Termitophilous Rove Beetle

Cassiano Sousa Rosa, Paulo Fellipe Cristaldo, Daniela Faria Florencio, Alessandra Marins, Eraldo R Lima, Og DeSouza

Abstract


Inter-specific symbiotic links are often reinforced by morphological, physiological, or behavioural trait modification undergone by the associated species. In some cases, such as in physogastric termitophile staphylinids, such modifications do facilitate the social interaction. Here we inspect chemical traits of the physogastric staphylinid Corotoca melantho (Insecta: Coleoptera) and its termite host Constrictotermes cyphergaster (Insecta: Blattodea: Isoptera), aiming to verify whether staphylinids resemble their host. First, we compared CHC profiles of hosts and guests within and among termitaria, to gather evidence on the origin of such profiles in guests. Then, we examined nitrogen and carbon isotopic signatures of these cohabitants to inspect whether chemical disguise is achieved by predation of host workers by staphylinids. Beetles presented CHC more similar to the CHC of their cohabiting termites than to (i) their conspecifics and (ii) termites from another nest, thereby favouring the hypothesis on CHC acquisition by guests. Isotopic signatures revealed that such similarities could not be majorly determined by share nutrition between these cohabitants. In general, our results evidenced that chemical disguise in termitophiles may function as a strategy for social integration in morphological mimics.

Keywords


cohabitation; Constrictotermes cyphergaster; Corotoca melantho; symbiosis

Full Text:

PDF

References


Akino, T. K., Knapp, J. J., Thomas, J. A. & Elmes, G. W. (1999). Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proceedings of the Royal Society of London - Series B, 266, 1419–1426. doi:10.1098/rspb.1999.0796

Blomquist, G. J. & Bagneres, A.-G. (2010). Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Cambridge, UK, Cambridge University Press, 492p.

Carlson, D. A., Bernier, U. R. & Sutton, B. D. (1998). Elution patterns from capillary GC for methyl-branched alkanes. Journal of Chemical Ecology, 24:11, 1845–1865. doi:10.1023/A:1022311701355

Costa-Lima, A. M. (1952). Insetos do Brasil - Tomo 07. Escola Nacional de Agronomia, 372p.

Costa, C. & Vanin, S. A. (2010). Coleoptera larval fauna associated with termite nests (Isoptera) with emphasis on the “Bioluminescent termite nests” from Central Brazil. Psyche, 2010, 1–13. doi:http://dx.doi.org/10.1155/2010/723947

Cristaldo, P. F., Rosa, C. S., Florencio, D. F., Marins, A. & DeSouza, O. (2012). Termitarim volume as a determinant of invasion by obligatory termitophiles and inquilines in the nests of Constrictotermes cyphergaster (Termitidae: Nasutitermitinae). Insectes Sociaux, 59:4, 541–548. doi:10.1007/s00040-012-0249-3

Cunha, H. F., Costa, D. A., Santo, K. D., Silva, L. O. & Brandão, D. (2003). Relationship between Constrictotermes cyphergaster and inquiline termites in the Cerrado (Isoptera : Termitidae). Sociobiology, 42:3, 761–770.

Cunha, H. F., Lima, J. S., Souza, L. F. de, Santos, L. G. A. dos & Nabout, J. C. (2015). No morphometric distinction between the host Constrictotermes cyphergaster (Silvestri) (Isoptera: Termitidae, Nasutitermitinae) and its obligatory termitophile Corotoca melantho Schiødte (Coleoptera: Staphylinidae). Sociobiology, 62:1, 65–69. doi:http://dx.doi.org/10.13102/sociobiology.v62i1.65-69

DeNiro, M. J. & Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42:5, 495-506. doi:10.1016/0016-7037(78)90199-0

DeSouza, O., Araújo, A. P. A., Florencio, D. F., Rosa, C. S., Marins, A., Costa, D. A., Cristaldo, P. F. (2016). Allometric Scaling of Patrolling Rate and Nest Volume in Constrictotermes cyphergaster Termites: Hints on the Settlement of Inquilines. PloS one, 11:1, e0147594. doi:10.1371/journal.pone.0147594

Dool, H. van Den & Dec. Kratz, P. (1963). A generalization of the retention index system including linear temperature programmed gas—liquid partition chromatography. Journal of Chromatography A, 11, 463–471. doi:http://dx.doi.org/10.1016/S0021-9673(01)80947-X

Eggers, T. & Jones, T. H. (2000). You are what you eat. . . or are you? Trends in Ecology & Evolution, 15:7, 265–266. doi:http://dx.doi.org/10.1016/S0169-5347(00)01877-2

Elgar, M. A. & Allan, R. A. (2004). Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften, 91:3, 143–147. doi: 10.1007/s00114-004-0507-y

Elgar, M. A. & Allan, R. A. (2006). Chemical mimicry of the ant Oecophylla smaragdina by the myrmecophilous spider Cosmophasis bitaeniata: Is it colony-specific? Journal of Ethology, 24:3, 239–246. doi:10.1007/s10164-005-0188-9

Elmes, G. W., Barr, B., Thomas, J. A. & Clarke, R. T. (1999). Extreme host specificity by Microdon mutabilis (Diptera : Syrphidae), a social parasite of ants. Proceedings Of The Royal Society Of London Series B-Biological Sciences, 266:1418, 447–453.

Florencio, D. F., Marins, A., Rosa, C. S., Cristaldo P. F. Araújo, A. P. A., Silva, I. R. & DeSouza, O. (2013). Diet segregation between cohabitating builder and inquiline termite species. Plos One, 8:6, e66535. doi:10.1371/journal.pone.0066535

Florencio, D. F., Rosa, C. S., Marins, A., Cristaldo, P. F., Araujo, A. P., Silva, I. R. & DeSouza, O. (2011). How to preserve termite samples in the field for carbon and nitrogen stable isotopes studies? Rapid Communications in Mass Spectrometry, 25:1, 243–246. DOI: 10.1002/rcm.4820

Grassé, P. P. (1986). Termitophiles et termitophilie. In Termitologie (pp. 235–367). Foundation Singer-Polygnac.

Guillem, R. M., Drijfhout, F. & Martin, S. J. (2014). Chemical deception among ant social parasites. Current Zoology, 60:1, 62–75.

Haverty, M. l., Thorne, B. L. & Nelson, L. (1996). Hydrocarbons of Nasutitermes acajutlae and comparison of methodologies for sampling cuticular hydrocarbons of caribbean termites for taxonomic and ecological studies. Journal of Chemical Ecology, 22:11, 2081–2109. doi:10.1007/BF02040096.

Howard, R. W., McDaniel, C. A. & Blomquist, G. J. (1980). Chemical mimicry as an integrating mechanisms: cuticular hydrocarbons of a termitophile and its host. Science, 210:4468, 431–433. doi:10.1126/science.210.4468.431

Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: Siber–stable isotope bayesian ellipses in R. Journal of Animal Ecology, 80:3, 595–602. doi:10.1111/j.1365-2656.2011.01806.x

Kanao, T., Eldredge, K. & Maruyama, M. (2016). A defensive body plan was pre-adaptive for termitophily in the rove beetle tribe Termitohospitini (Staphylinidae: Aleocharinae). bioRxiv. doi:doi: 10.1101/083881

Kather, R., Drijfhout, F. P. & Martin, S. J. (2015). Evidence for colony-specific differences in chemical mimicry in the parasitic mite Varroa destructor. Chemoecology, 25:4, 215–222. doi:http://dx.doi.org/10.1007/s00049-015-0191-8

Kistner, D. H. (1979). Social and evolutionary significance of social insect symbionts. In H. R. Hermann (Ed.), Social Insects (Vol. I, pp. 339–413). New York, Academic Press.

Kistner, D. H. (1982). The social Insect’s bestiary. In Social Insects (Vol. III, pp. 1–244). Academic Press.

Kneip, C., Lockhart, P., Voß, C. & Maier, U. G. (2007). Nitrogen fixation in eukaryotes–new models for symbiosis. BMC Evolutionary Biology, 7:55, 1–12. doi:10.1186/1471-2148-7-55

Lenoir, A., Hefetz, A., Simon, T. & Soroker, V. (2001). Comparative dynamics of gestalt odour formation in two ant species Camponotus fellah and Aphaenogaster senilis (Hymenoptera: Formicidae). Physiological Entomology, 26, 275–283.

Liang, D. & Silverman, J. (2000). “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften, 87:9, 412–416.

Marten, A., Kaib, M. & Brandl, R. (2009). Cuticular Hydrocarbon Phenotypes Do not Indicate Cryptic Species in Fungus-Growing Termites (Isoptera: Macrotermitinae). Journal Of Chemical Ecology, 35:5, 572–579. doi:10.1007/s10886-009-9626-4

Mathews, A. G. A. (1977). Studies on Termites from the Mato Grosso State, Brazil. (A. B. De Ciências, Ed.). Rio de Janeiro, RJ, 267p.

Moura, F. M. S., Vasconcellos, A., Araújo, V. F. P. & Bandeira, A. G. (2006). Feeding habit of Constrictotermes cyphergaster (Isoptera, Termitidae) in an area of caatinga, Northeast Brazil. Sociobiology, 48:2, 1–6.

Muscatine, L. & Porter, J. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience, 27:7, 454–460. doi:10.2307/1297526

Nash, D. R. & Boomsma, J. J. (2008). Communication between hosts and social parasites. In P. D’Ettorre & D. P. Hughes (Eds.), Sociobiology of communication: an interdisciplinary perspective (pp. 55–79). Oxford.

Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Wagner, H. (2015). vegan: Community Ecology Package. Retrieved from http://cran.r-project.org/package=vegan

Oystaeyen, A. Van, Zweden, J. S. van, Huyghe, H., Drijfhout, F., Bonckaert, W. & Wenseleers, T. (2015). Chemical Strategies of the Beetle Metoecus Paradoxus, Social Parasite of the Wasp Vespula vulgaris. Journal of Chemical Ecology, 41:12, 1137–1147. doi:10.1007/s10886-015-0652-0

Parker, J. (2016). Myrmecophily in beetles (Coleoptera): evolutionary

patterns and biological mechanisms. Myrmecological News, 22, 65–108.

Parnell, A. C., Inger, R., Bearhop, S. & Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS ONE, 5:3, e9672. doi:https://doi.org/10.1371/journal.pone.0009672

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83:3, 703–718. doi:http://dx.doi.org/10.1890/0012-

(2002)083[0703:USITET]2.0.CO;2

Proffit, M., Birgersson, G., Bengtsson, M., Reis-Jr, R., Witzgall, P. & Lima, E. (2011). Attraction and oviposition of Tuta absoluta females in response to tomato leaf volatiles. Journal of Chemical Ecology, 37:6, 565–574. doi:10.1007/s10886-011-9961-0

R Development Core Team. (2015). R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing.

Rettenmeyer, C. W. (1970). Insect Mimicry. Annual Review of Entomology, 15, 43–74. doi:https://doi.org/10.1146/annurev.en.15.010170.000355

Sands, W. A. & Lamb, R. W. (1975). Systematic position of Kaudernitermes gen. n. (Isoptera-Termitidae, Nasutitermitinae) and its relevance to host relationships of termitophilous staphylinid beetles. Journal of Entomology Series B - Taxonomy & Systematics, 44, 189–200.

Schönrogge, K., Napper, E. K. V, Birkett, M. A., Woodcock, C. M., Pickett, J. A. & Thomas, J. A. (2008). Host recognition by the specialist hoverfly Microdon mutabilis, a social parasite of the ant Formica lemani. Journal of Chemical Ecology, 34:2, 168–178. doi:10.1007/s10886-007-9417-8

Seevers, C. H. (1957). A monograph on the termitophilous Staphylinidae (Coleoptera). Fieldiana Zoology, 40, 1–334.

Tayassu, I., Abe, T., Eggleton, P. & Bignell, D.-E. (1997). Nitrogen and carbon isotope ratios in termites: an indicator of trophic habit along the gradient fromwood-feeding to soil-feeding. Ecol. Entomol., 22:3, 343–351. doi:10.1046/j.1365-2311.1997.00070.x

Thompson, J. N. (1999). The evolution of species interactions. Science, 284:5423, 2116–2118. doi:10.1126/science.284.5423.2116

Vasconcellos, A., Araújo, V. F. P., Moura, F. M. S. & Bandeira, A. G. (2007). Biomass and population structure of Constrictotermes cyphergaster (Silvestri) (Isoptera: termitidae) in the dry forest of caatinga, northeastern Brazil. Neotropical Entomology, 36:5, 693–698. doi:http://dx.doi.org/10.1590/S1519-566X2007000500009

Visser, S. N. De, Freymann, B. P. & Schnyder, H. (2008). Trophic interactions among invertebrates in termitaria in the African savanna: a stable isotope approach. Ecological Entomology, 33:6, 758–764. doi:10.1111/j.1365-2311.2008.01029.x

Von-Beeren, C., Pohl, S. & Witte, V. (2012). On the Use of Adaptive Resemblance Terms in Chemical Ecology. Psyche, 2012:ID 635761, 1–7. doi:10.1155/2012/635761

Wheeler, W. M. (1918). A study of some ant larvae, with a consideration of the origin and meaning of the social habit among insects. Proceedings of the American Philosophical Society, 57:4, 293–343. Retrieved from http://www.jstor.org/stable/983940

Yamamoto, S., Maruyama, M. & Parker, J. (2016). Evidence for social parasitism of early insect societies by Cretaceous rove beetles. Nature Communications, 7, 13658. doi:10.1038/ncomms13658




DOI: http://dx.doi.org/10.13102/sociobiology.v65i1.1942

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2016: 0.699