VENOMOUS SALIVA OF NON-HAEMATOPHAGOUS REDUVIID BUGS (HETEROPTERA: REDUVIIDAE): A REVIEW
Authors/Creators
- 1. P.G & Research Department of Advanced Zoology & Biotechnology, Loyola College, Chennai-600034
Description
ABSTRACT
While reduviids are a modestly well characterized group of insects, especially the blood sucking triatominae due to the medical implications of the Chagas disease, which is mainly transmitted by the infected bugs whose excrement contains Trypanosoma cruzi that enters the body through bruises or cuts in the skin of humans, their non-haematophagus counterparts are a forgotten lot and have not been thoroughly investigated. The venom in the saliva of the non-haematophagus reduviids has come into the spotlight in the last couple of decades due to the voracious predatory lifestyle that enable them to be used as biological control agents in subduing pests. But the biochemistry of reduviid venom, its action and subsequent effect on the prey, toxicity, enzymes, peptides present in the venom and their significance, the role of extra oral digestion facilitated by the venom for its predatory lifestyle have not been given much consideration. This review aims to summarize the existing body of literature regarding the venomous saliva of non-haematophagous reduviid bugs for the first time.
REFERENCES
- Ambrose, D.P. (1999). Assassin bugs. New Delhi, India: Oxford and IBH Publ. Co. Pvt. Ltd.
- Ambrose, D.P. (2004). The status of biosystematics of Indian Reduviidae (Hemiptera: Heteroptera). In: Perspectives on biosystematics and biodiversity. Rajmohana, K., Sudheer, K., Girish, P., Kumar, Santhosh, S., (Eds.). Harvest Media Services, Calicut, 441-459.
- Ambrose, D.P. and Kumaraswami, N.S. (1990). Functional response of the reduviid predator Rhinocoris marginatus Fabr. on the cotton stainer Dysdercus cingulatus Fabr. Journal of Biological Control. 4(1): 22-24.
- Ambrose, D.P. and Maran, S.P.M. (1999). Quantification of protein content and paralytic potential of saliva of fed and prey deprived reduviid Acanthapsis pedestris Stal. (Heteroptera: Reduviidae: Reduviinae). Indian Journal of Environmental Science. 3(1): 11-16.
- Amino, R., Martins, R.M., Procopio, J., Hirata, I.Y., Juliano, M.A. and Schenkman, S. (2002). Trialysin, a Novel Pore-forming Protein from Saliva of Hematophagous Insects Activated by Limited Proteolysis. The Journal of Biological Chemistry. 277(8): 6207-6213.
- Anand, G.B., Rizwana, F.A. and Prakash, S. (2010). Ecofriendly technology for the management of Brinjal pest using reduviids. International Journal on Applied Bioengineering. 4(2):15-18.
- Andersen, J.F., Francischetti, I.M.B., Jesus, G., Valenzuela, Schuck, P. and Ribeiro, J.M.C. (2003). Inhibition of Hemostasis by a High Affinity Biogenic Amine-binding Protein from the Saliva of a Blood-feeding Insect. J. Biol. Chem. 278: 4611-4617.
- Baptist, B.A. (1941). The morphology and physiology of the salivary glands of Hemiptera-Heteroptera. Quart. J. Micros. Sci. 83: 91-139.
- Cheeseman, M.T. and Gillott, C. (1987). Organization of protein digestion in Calosoma calidum (Coleoptera: Carabidae). J. Insect Physiol. 33:1-8.
- Claver, M.A., Muthu, M.S.A., Ravichandran, B. and Ambrose, D.P. (2004). Behaviour, prey preference and functional response of Coranus spiniscutis Reuter, a potential predator of tomato insect pests. Pest Management in Horticultural Ecosystems. 10:19-27.
- Claver, M.A., Ramasubbu, G., Ravichandran, B. and Ambrose, D.P. (2002). Searching behaviour and functional response of Rhynocoris longifrons (Stål) (Heteroptera: Reduviidae), a key predator of pod sucking bug, Clavigralla gibbosa Spinola. Entomon. 27:339-346.
- Claver, M.A., Ravichandran, B., Khan, M.M. and Ambrose, D.P. (2003). Impact of cypermethrin on the functional response, predatory and mating behaviour of a non-target potential biological control agent Acanthaspis pedestris (Stål) (Het., Reduviidae). Journal of Applied Entomology. 127:18-22.
- Cobben, R.H. (1978). Evolutionary trends in Heteroptera: mouthparts, structure and feeding strategies. Mede, part 2.
- Cohen, A.C. (1984). Food consumption, food utilization and metabolic rates of Geocoris punctipes (Het.: Lygaeidae) fed Heliothis virescens (Lep.: Noctuidae) eggs. Entamophaga. 29: 361-367.
- Cohen, A.C. (1989). Ingestion and food consumption efficiency in a predacious hemipteran. Ann. Entomol. Soc. Am. 82:495-499.
- Cohen, A.C. (1990). Feeding adaptations of some predateous hemiptera. Ann. Entomol. Soc. Am. 83(6):1215-1223.
- Cohen, A.C. (1993). Organization of digestion and preliminary characterization of salivary trypsin like enzymes in a predaceous heteropteran, Zelus renardii. J. Insect Physiol. 39: 823-829.
- Cohen, A.C. (1998). Biochemical and morphological dynamics and predatory feeding habits in terrestrial heteroptera. In Predatory Feeding Habits in Terrestrial Heteroptera, J.R. Ruberson and M. Coll. (Ed.) Thomas say pubs., Phoenix, Arizona. 21-32.
- Edwards, J.S. (1960). Spitting as a defensive mechanism in a predatory reduviid. In Proceeding of International Congress of Entomology, Vienna. 259-263.
- Edwards, J.S. (1961). The action and composition of the saliva of an assassin bug Platymeris rhadamanthus Gaerst. (Hemiptera, Reduviidae). J. Exp. Biology. 38: 61-77.
- Edwards, J.S. (1962). Observations on the development and predatory habit of two reduviid heteroptera, Rhinocoris carmelita Stäl and Platymeris rhadamanthus Gerst. In Proceedings of the Royal Entomological Society of London. Series A, General Entomology. 3(7): 89–98.
- Evangelin, G., Bertrand, H., Muthupandi, M. and John William. (2012). Bioefficacy of Rhynocoris kumarii on the hemipteran pests of cotton (abstract). In Proceedings of the National conference on Climate change – a challenge to sustainable development, Andhra Pradesh, India, BEITR 22, 23.
- Foelix, R.F. (1982). Biology of Spiders. Cambridge, MA: Harvard Univ. Press.
- Forero, D., Choe, D.H. and Weirauch, C. (2011). Resin Gathering in Neotropical Resin Bugs (Insecta: Hemiptera: Reduviidae): Functional and Comparative Morphology. Journal of Morphology. 272: 204–229.
- George, P.J.E. and Ambrose, D.P. (2001). Polymorphic adaptive insecticidal resistance in Rhynocoris marginatus (Fabr.) (Het., Reduviidae) a non-target biocontrol agent. Journal of Applied Entomology. 125(4): 207-209.
- Gerardo, C., Salumi, A., Akahane, T.W., Yoshihisa, K. and Tomni, W. (2001). Novel peptides from assassin bugs (Hemiptera: Reduviidae): isolation, chemical and biological characterization. FEBS Lett. 499: 256-261.
- Gilmour, D. (1961). The biochemistry of insects. New York, Academic.
- Goodchild, A.J.P. (1955). Some observations on growth and egg production of the blood-sucking reduviids, Rhodnius proxilus and Triatoma infestans. In Proceedings of the Royal Entomological Society of London. 30(10-12): 137–144.
- Goodchild, A.J.P. (1966). Evolution of the alimentary canal in the hemiptera. Biol. Rev. 41: 97-140.
- Grundy, P.R. (2007). Utilizing the assassin bug, Pristhesancus plagipennis (Hemiptera: Reduviidae), as a biological control agent within an integrated pest management programme for Helicoverpa spp. (Lepidoptera: Noctuidae) and Creontiades spp. (Hemiptera: Miridae) in cotton. Bull Entomol Res. 97(3): 281-90.
- Guerenstein, P.G. and Guerin, P.M. (2001). Olfactory and behavioural responses of the blood-sucking bug Triatoma infestans to odours of vertebrate hosts. The Journal of Experimental Biology. 204: 585–597.
- Haridass, E.T. (1978). Biological and ethological studies on some South Indian Reduviids (Hemiptera:Reduviidae). Ph.D. thesis. University of Madras, India.
- Haridass, E.T. (1985). Feeding and ovipositional behavior in some reduviids (Insecta- Heteroptera). In Proc. Indian Acad. Sci. (Animal. Sci.) 94:239-247.
- Haridass, E.T. and Ananthakrishnan, T.N. (1980). Models for the predatory behavior of some reduviids from Southern India (Insecta-Heteroptera-Reduviidae). In Proc. Indian Acad. Sci. (Animal. Sci.). 89: 387-402.
- Haridass, E.T. and Ananthakrishnan, T.N. (1981). Functional morphology of the salivary system in some Reduviidae (Insecta-Heteroptera). In Proc. Indian Acad. Sci. (Animal. Sci.). 90(2): 145-160.
- Hespenheide, H.A. (1973). Ecological inferences from morphological data. Rev. Sys. Ecol. 4:213-299.
- Hilty, J.E. (2013). Insect Visitors of Illinois Wildflowers. (illinoiswildflowers.info, version 03).
- Hwang, W.S. and Weirauch, C. (2012). Evolutionary History of Assassin Bugs (Insecta: Hemiptera: Reduviidae): Insights from Divergence Dating and Ancestral State Reconstruction. PLoS ONE. 7 (9): (e45523. doi:10.1371/journal.pone.0045523).
- Imamura, T., Murata, M. and Miyanoshita, A. (2008). Biological Aspects and Predatory Abilities of Hemipterans Attacking Stored-Product Insects. Japan Agricultural Research Quarterly. 42(1):1-6.
- Jacobson, E. (1911). Biological notes on the hemipteron Ptilocerus ochraceus. Tijdschrift voor Entomologie. 54:175–179.
- Kaspari, M. (1990). Prey preparation and determinants of handling time. Anim. Behav. 40: 118-126.
- Lakkundi, N.H. (1989). Assessment Of Reduviids For Their Predation And Possibilities Of Their Utilization In Biological Control. Ph.D. thesis, IARI, Division of Entomology, New Delhi.
- Law, J.H., Dunn, P.E. and Kramer, K.J. (1977). Insect proteases and peptidases. Adv. Enzymol. 45: 389-425.
- Lent, H. and Wygodzinsky, P. (1979). Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bul Am Mus Nat Histo. 163:123-520.
- Louis, D. (1974). Biology of Reduviidae of Cocoa farms in Ghana American midi. Nature 91:68-89.
- Lucas, J.R. (1985). Partial prey consumption by antlion larvae. Anim. Behav. 33:945-958.
- Maldonado, J. (1990). Systemic catalouge of the Reduviidae of the world (Insecta: Heteroptera). Carribean. Special edition, university of Puerto Rico, Mayaguez, J. Sci. 694.
- Maran, P.M. (2000). Chosen reduviid predators-prey interaction: nutritional and pheromonal chemical ecology (Insecta:Heteroptera: Reduviidae). Ph.D. thesis. Manonmanium Sundaranar University, Department of Zoology, India.
- McMahan, E.A. (1983a). Adaptations, feeding preferences, and biometrics of a termite-baiting assassin bug (Hemiptera, Reduviidae). Annals of the Entomological Society of America. 76:483–486.
- McMahan, E.A. (1983b). Bugs angle for termites. Natural History. 92: 40-47.
- Miles, M.A., Souza de, A.A. and Povoa, M. (1981). Chagas disease in the Amazon basin. III. Ecotopes of ten triatomine bug species (Hemiptera: Reduviidae) from the vicinity of Belém, Pará State, Brazil. J Med Entomol. 18: 266-278.
- Miles, P.W. (1972). The saliva of Hemiptera. Adv. Insect Physiol. 9:183-256.
- Miller, N.C.E. (1953). Notes on the biology of the Reduviidae of Southern Rhodesia. Trans Zool Soc London. 27: 541–672.
- Mommsen, T.P. (1978). Digestive enzymes of a spider (Tegenaria atricia Koch), Digestion of proteins. Comp. Biochem. Physiol. 60(A): 371-375.
- Morrison, N.M. (1989). Gel electrophoretic studies with reference to functional morphology of the salivary glands of Acanthaspis pedestris Stal. (Insecta: Heteroptera: Reduviidae). In Proc. Indian Acad. Sci. Anim. Sci. 98:167-73.
- Nagarajan, K. and Ambrose, D.P. (2013). Chemically Mediated Prey-Approaching Behaviour of the Reduviid Predator Rhynocoris fuscipes (Fabricius) (Insecta: Heteroptera: Reduviidae) by Y-arm Olfactometer. Pakistan Journal of Biological Sciences. 16: 1363-1367.
- Nentwig, W. and Wissel, C. (1986). A comparison of prey lengths among spiders. Oecologica. 68: 595-600.
- Noeske-Jungblut, C., Kratzschmar, J., Haendler, B., Alagon, A., Possani, L., Verhallen, P., Donner, P. and Schleuning, W.D. (1994). An Inhibitor of Collagen-induced Platelet Aggregation from the Saliva of Triatoma pallidipennis. The Journal of Biological Chemistry. 269(7): 5050-5053.
- Olivera, B.M., Rivier, J., Scott, J.K., Hillyard, D.R. and Cruz, L.J. (1991). Conotoxins. The Journal of Biological Chemistry. 266(33):22067-22070.
- Patterson, J. (1999). A Morphometric Investigation of the Relationships between Triatoma rubrofasciata (Hemiptera: Reduviidae: Triatominae), Old World Triatoma and Representatives of the New World Species. Ph.D. thesis, LSHTM, London.
- Rastogi, S.C. (1962). The salivary enzymes of some phytophagous and predaceous heteropterans. Sci. Cult. 28:479-480.
- Rees, A.R. and Offord, R.E. (1969). Studies on the protease and other enzymes from venom of Lethocerus cordofanus. Nature. 221:665-667.
- Rocha, L. and Redaelli, L.R. (2004). Functional response of Cosmoclopius nigroannulatus (Hem.: Reduviidae) to different densities of Spartocera dentiventris (Hem.: Coreidae) nymphae. Braz. J. Biol. 64(2):309-316.
- Ryckman, R.E. (1951). Recent observations of cannibalism in Triatoma (Hemiptera: Reduviidae). J Parasitol. 37: 433-434.
- Sahayaraj, K. (1994). Capturing success by reduviid predators Rhinocoris kumarii and Rhinocoris marginatus on different age groups of Spodoptera litura, a polyphagous pest (Heteroptera: Reduviidae). J. Ecobiol. 6(3): 221-224.
- Sahayaraj, K. (2013). Threrapeutic biomolecules of venomous arthropods (abstract). Proc. Bioavailability and Bioequivalence: Pharmaceutical R&D Summit, Beijing, China.
- Sahayaraj, K. and Vinothkanna, A. (2011). Insecticidal activity of venomous saliva from Rhynocoris fuscipes (Reduviidae) against Spodoptera litura and Helicoverpa armigera by microinjection and oral administration. The Journal of Venomous Animals and Toxins including Tropical Diseases. 17(4): 486-490.
- Sahayaraj, K., Borgio, J.F., Muthukumar, S. and Anandh G.P. (2006). Antibacterial activity of Rhynocoris marginatus (fab.) and Catamirus brevipennis (serville) (hemiptera: reduviidae) venoms against human pathogens. J. Venom. Anim. Toxins incl. Trop. Dis. 12(3): 487-496.
- Sahayaraj, K., Kumara Sankaralinkam, S. and Balasubramaniam, R. (2007). Prey influence on the salivary gland and gut enzymes qualitative profile of Rhynocoris marginatus (Fab.) and Catamirus brevipennis (Serville) (Heteropetera: Reduviidae). Journal of Entomology. 4(4):331-336.
- Sahayaraj, K., Muthukumar, S. and Anandh, G.P. (2006). Evaluation of milking and electric shock methods for venom collection from hunter reduviids. Entomon. 31(1): 65-68.
- Sahayaraj, K., Muthukumar, S. and Rivers, D. (2013). Biochemical and electrophoretic analyses of saliva from the predatory reduviid species Rhynocoris marginatus (Fab.). Acta Biochimica Polonica. 60(1): 91-97.
- Sandoval, C.M., Joya, M.I., Gutierez, R. and Angullo, V.M. (2000). Cleptohaematophagy of the triatomine bug Belminus herreri. Med Vet Entomol. 14: 100-101.
- Schaefer, C.W. (1988). Reduviidae (Hemiptera: Heteroptera) as agents of biological control. In Bicovas, K.S. Ananthasubramanian, P. Venkatesan and S. Sivaraman (Ed.), Loyola College, Madras. 27-33.
- Schmidt, J.O. (1982). Biochemistry of insect venoms. Annu. Rev. Entomol. 27:239-268.
- Schofield, C.J. (1994). Triatominae - Biology & Control. West Sussex, UK: Eurocommunica Publications;
- Schofield, C.J. (2000). Trypanosoma cruzi - The Vector-parasite Paradox. Mem. Inst. Oswaldo Cruz, Rio de Janeiro. 95(4): 535-544.
- Smith, D.S. and Wigglesworth, V.B. (1959). Collagen in the perilemma of insect nerve. Nature. 183: 127.
- Soley, F.G., Jackson, R.R. and Taylor, P.W. (2011). Biology of Stenolemus giraffa (Hemiptera: Reduviidae), a web invading, araneophagic assassin bug from Australia. New Zealand Journal of Zoology. 38: 297–316.
- Southwood, T.R.E. (1955). The morphology of the salivary glands of terrestrial Heteroptera (Geocorisae) and its bearing on classification. Tijdschr., Entomol. 98:77-84.
- Stanic, M. (1956). Allergenic properties of venom hyper-sensitiveness in man and animals. In Venoms, Edited by Buckley, E.E. & Proges, N. Washington.
- Swingle, H.S. (1925). Digestive enzymes of an insect. The Ohio Journal of Science. 25(5): 209-218.
- Teo, S.K. and Cheah, J.S. (1973). Severe reaction to the bite of the triatomine bug (Triatoma rubrofasciata) in Singapore. J Trop Med Hyg. 76: 161-162.
- Vennison, S.J. and Ambrose, D.P. (1992). Biology, Behaviour and Biocontrol Efficiency of a Reduviid Predator, Sycanus reclinatus Dohrn (Heteroptera: Reduviidae) from Southern India. Mitteilungen aus dem Museum für Naturkunde in Berlin, Zoologisches Museum und Institut für Spezielle Zoologie (Berlin). 68 (1):143–156.
- Weirauch, C. and Cassis, G. (2006). Attracting ants: the trichome in Ptilocnemus lemur (Heteroptera: Reduviidae) and novel glandular area on the sternum. J. Ny Entomol. Soc. 114: 28-37.
- Wigglesworth, V.B. (1943). The fate of haemoglobin in Rhodnius prolixus (Hemiptera) and other blood-sucking arthropods. In Proceedings of the Royal Entomological Society of London B. 131(865): 313-339.
- Wigglesworth, V.B. (1957). The use of osmium in the fixation and staining of insects. In Proc. Roy. Soc. B. 147:185-199.
- Wignall, A.E. and Taylor, P.W. (2011). Assassin bug uses aggressive mimicry to lure spider prey. In Proceedings of the Royal Society B-Biological Sciences. 278:1427–1433 (doi: 10.1098/rspb.2010.2060).
- Zerachia, T., Bergmann, F. and Shulov, A. (1973). Pharmacological activities of the venom of the predaceous bug Holotrichius innessi (Heteroptera: Reduviidae). Anim. Plant toxins. 143-146.
- Zhang, G. and Weirauch, C. (2011). Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). Acta Zoologica (doi: 10.1111/j.1463-6395.2011.00522.x).