Behavior and Extra-Oral Digestion of the Wasp Sclerodermus guani (Hymenoptera: Bethylidae) Parasitizing

Volume 6, Issue 2, April 2021     |     PP. 13-44      |     PDF (669 K)    |     Pub. Date: May 17, 2021
DOI: 10.54647/biology18144    112 Downloads     2820 Views  

Author(s)

Lai Yanxue, Forest Pest Control and Quarantine Station of Ningbo City, Ningbo 315000, China

Abstract
For many decades, the parasitic behavior of wasp Sclerodermus guani (Hymenoptera: Bethylidae), a typical generalist gregarious ectoparasitoid, was described as paralyzing the hosts by stinging with venom for egg-laying, and then their offspring larvae after hatching feed on hosts’ hemolymph for the development until emergence. However, this paper reported a new mechanism of the wasp to parasitize the host borer Monochamus alternatus (Coleoptera: Cerambycidae). Observation on their parasitic behavior and their offspring growth discovered that the wasp needs 6 steps to complete its parasitic process, i.e. host-biting and-fighting, host-subduing and-nursing, host-liquefying and-feeding, wasps’ berried and oviposition, larval sucking and developing, cocooning and wasps’ emerging. Host-biting and host-liquefying are the key steps which would evolve an amazing array of mechanisms to create a liquid nutrient reservoir inside the borer body cavity for the parasitoid larvae’s sucking and developing. This mechanism suggests that S.guani is a species of ectoparasitoid wasp, with the characteristic of extra-oral digestion; the nature of subduing is to fully liquefy the borer internal material and help their offspring smoothly sucking the liquid nutrient from the host for development.

Keywords
Sclerodermus guani, Bethylidae, Monochamus alternatus, Cerambycidae Parasitize, Extra-oral Digestion, Suck, Berried, Fecundity

Cite this paper
Lai Yanxue, Behavior and Extra-Oral Digestion of the Wasp Sclerodermus guani (Hymenoptera: Bethylidae) Parasitizing , SCIREA Journal of Biology. Volume 6, Issue 2, April 2021 | PP. 13-44. 10.54647/biology18144

References

[ 1 ] Askew RR, Shaw MR. 1979. Mortality factors affecting the leaf-mining stages of Phyllonorycter (Lepidoptera: Gracillariidae) on oak and birch. 2. Biology of the parasite species. Zoological Journal of the Linnean Seciety. 67:51-64.
[ 2 ] Anthony J. Kurian C. 1960. Studies on the habits and life history of Perisierola nephantidis Muesebeck. Indian Coconut Journal, 13, 145-53.
[ 3 ] Balfour-Browne F. 1922. On the life-history of Melittobia acasta Walker; a chalcid parasite of bees and wasps. Parasitology. 14:349-370.
[ 4 ] Baptist BA. 1941. The morphology and physiology of the salivary glands of Hemiptera-Heteroptera. Q.J.Microscop.Sci. 83:91-139.
[ 5 ] Bartlett BR. 1964. Patterns in the host-feeding of adult Hymenoptera. Annals of the Entomological Society of America. 57:344-350.
[ 6 ] Beckage NE, Nesbit DJ, Nielsen BD, Spence KD, Barman MAE. 1989. Alteration of hemolymph polypeptides in Manduca sexta larvae parasitized by Cotesia congregata: a two-dimensional electrophoretic analysis and comparison with major bacteriainduced proteins. Archives of Insect Biochemistry and Physiology 10, 29–45.
[ 7 ] Beckage NE. 1985. Endocrine interactions between endoparasitic insects and their hosts. Annu.Rev. Entomol. 30:371-413
[ 8 ] Beckage NE and Gelman DB. 2004. Wasp parasitoid disruption of Host development: Implications fro new biologically based strategis for insect control. Annu. Rev. Entomol. 49:299-330.
[ 9 ] Beard RL, 1971. Production and use of venom by Bracon brevicornis (Wesm.). In Toxins of Animal and Plant Origin. Vol. 1 (eds A. de Vries and E. Kockva), Gordon and Breach, New York. pp.181一190
[ 10 ] Blass S, Ruthmann A, 1989. Fine structure of the accessory glands of the female genital tract of the ichneumonid Pimpla turionellae ( Insecta，Hymenoptera). Zoomorphology. 108( 6) :367 -377．
[ 11 ] Bocchino FJ, Sullivan DJ. 1981. Effects of venoms from two aphid hyperparasitoids, Asaphes lucens and Dendrocerus carpenteri (Hymenoptera:Pteromalidae and Megaspilidea), on larvae of Aphidius smithi (Hymenoptera:Aphidiidae). Canadian Entomologist. 113:887-889.
[ 12 ] Bridewell JC. 1919. Some notes on Hawaiian and other Bethylidae [Hymenoptera] with descriptions of ncw species. Proc. Of Hawaii Entomol. Soc., 4, 21-38.
[ 13 ] Bridges A, Owen M. 1984. The morphology of the honey bee venom gland and reservoir. Journal of Morphology. 181( 1): 69-81.
[ 14 ] Buschinger A, Bonger A. 1969. Zur extraintestinalen Verdauung des Ameisenlowen (Euroleon nostras Fourcr.,Myrmeleontidae). Z.Vgl. Physiol. 62:205-213.
[ 15 ] Burgess E. 1883. The structure of the mouth in the larva of Dytiscus. Proc. Boston Soc. Nat. Hist. 21:223-228.
[ 16 ] Casale A. 1991. Some notes on the parental and parasocial behaviour of Sclerodermas domesticus Latreille (Hymenoptera Bethylidae). Ehtology Ecology & Evolution, 3:sup1, 34-38.
[ 17 ] Chen MR, Song SH, Zhang LQ, Zhang E, Li QH, Yang L. 1996. Indirect control of pine wood nematode by releasing Scleroderma Guani. Chinese Joumal of Biological Control. 12(2): 52—54. ( In Chinese with English summary).
[ 18 ] Cheeseman MT, Gillott C. 1987. Organization of protein digestion in Calosoma calidum (Coleoptera: Carabidae). J. Insect Physiol. 33:1-18.
[ 19 ] Cheng SC, Yu JY, Zhu XE, Wu YK, Huang HY, Ding ZG. 2007. Prarasitism of Scleroderma guani on the larva of Monochamus alternatus in the xylem of Pinus massoniana in lab and in the field. Forest Pest and Diseas. 26(6):9—12. ( In Chinese with English summary)
[ 20 ] Cherian MC, Israel P. 1942. Goniozus indicus Ash., a new natural enemy of the sugarcane white moth borer (Sciroophaga rhodoproctalis). J. Bombay Nat. Hist. Soc.. 43: 488-493.
[ 21 ] Cohen AY. 1990. Feeding adaptations of some predatory hemiptera. Ann. Entomol.Soc.Am.83:1215-1223.
[ 22 ] Cohen AY. 1993. Organization of digestion and preliminary characterization of salivary trypsin-like enxymes in a predaceous heteropteran, Zelus renardii. J. Insect Physiol. 39:823-829.
[ 23 ] Cohen AY. 1995. Extra~oral digestion in predaceous Arthopods. Annual Review of Entomology. 40:85-103.
[ 24 ] Cohen AY. 1998. Solid~to~Liquid Feeding: The Inside(s) Story of Extra~Oral Digestion in Predaceous Arthopoda. American Entomologist. 44:103-116.
[ 25 ] Coudron TA, Kelly TJ, Puttler B. 1990. Developmental responses of Trichoplusia ni (Lepidoptera: Noctuidae) to parasitism by the ectoparasite Euplectrus plathypenae (Hymenoptera:Eulophidae). Arch. Insect Biochem. Physiol. 13:83-94.
[ 26 ] Coudron TA, Kelkly TJ. 1994. Premature production of late larval storage proteins in larvae of Trichoplusia ni parasitized by Euplectrus comstockii. Arch. Insect Biochem. Physiol. 26:97-109.
[ 27 ] Coudron TA, Brandt SL. 1996. characteristics of a developmental arrestant in the venom of the ectoparasitoid wasp Euplectrus comstockii, Toxicon. 34:1431-1441.
[ 28 ] Dahlman DL, Vinson SB. 1993. Teratocytes developmental and biochemical characteristics. In: Beckage NE, Thompson SN, Federici BA eds. Parasites and Pathogens of Insects. Vol. 1.New York: Academic Press. 145-165.
[ 29 ] Doury G, Bigot Y, Periquet G. 1997. Physiological and biochemical analysis of factors in the female venom gland and larval salivary secretions of the ectoparasitoid wasp Eupelmus orientalis. Journal of Insect Physiology. 43, 69–81.
[ 30 ] Down RE, Ford L, Mosson HJ, Fitches E, Gatehouse JA, Gatehouse AMR. 1999. Protease activity in the larval stage of the parasitoid wasp, Eulophus pennicornis (Nee) (Hymenoptera: Eulophidae): effect of protease inhibitors. Parasitology 119, 157–166.
[ 31 ] Damon A, Valle J. 2002. Comparison of two release techniques for the use of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), to control the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae) in Soconuseo, southeastern Mexico. Biological Control. 4(2):117-127.
[ 32 ] Edson KM, Vinson SB. 1979. A comparative morphology of the venom apparatus of female braconids ( Hymeopetera:raconidae). Canadian Entomology. 111: 1013-1024．
[ 33 ] Edson KM, Barlin MR, Vinson SB. 1982. Venom apparatus of braconid wasps: Comparative ultrastructure of reservoirs and gland filaments. Toxicon. 20 ( 3):553- 562.
[ 34 ] Fu¨hrer E, Willers D. 1986. The anal secretion of the endoparasitic larva Pimpla turionellae: sites of production and effects. Journal of Insect Physiology 32: 361–367.
[ 35 ] Gelman DB, Kelly TJ, Coudron TA. 1997. Mode of action of the venom of the ectoparasitic wasp, Euplectrus comstockii, in causing developmental arrest in the European corn borer, Ostrinia nubilalis. Inertebr. Neurosci. 3:231-238.
[ 36 ] Ghamari M, Hosseininaveh V, Darvishzadeh A. 2014. Carbohydrases in the digestive system of the spined soldier bug, Podisus maculiventris (say) (Hemiptera: Pentatomidae). Archives of Insect Biochemistry and Physiology. 85(4):195-215.
[ 37 ] Gnatzy W, Volknandt W. 2000. Venom gland of the digger wasp Liris niger: morphology, ultrastructure, age-related changes and biochemical aspects. Cell Tissue Research. 302( 2) : 271-284．
[ 38 ] Gopalapillai R, Kadono-Okuda K, Okuda T. 2005. Molecular cloning and analysis of a novel teratocyte-specific carboxylesterase from the parasitic wasp, Dinocampus coccinellae. Insect Biochemistry and Molecular Biology. 35: 1 171一1180.
[ 39 ] Gordh G, Móczár L. 1990. A catalog of the world Bethylidae (Hymenoptera: Aculeata). Memoirs of the American Entomological Institute. 46: 1–364
[ 40 ] Gordh G, Medved RE.1986. Biological notes on Goniozus pakmanus Gordh [Hymenoptera :Bethylidae], a parasite of Pink bollworm, Pectinophora gossypiella (Saunders) [Lepidoptera :Gelechiidae]. J. Kansas Entomol. Soc. 59: 723-733.
[ 41 ] Gordh, G. 1976. Goniozus gallicola Fouts, parasites of moth larvae with notes on other bethylids [Hymenoptera : BethylMae, Lepidoptera : Gelechiidae]. U.S.D.,4. Techn. Bull., 1542, 27 pp.
[ 42 ] Gordh G, Evans HE. 1976. A new species of Goniozus imported into California from Ethiopia for the biological control of Pink boilworm and some notes on the taxonomic status of Parasierola and Goniozus [Hymenoptera : Bethylidae]. Proc. Entomol. Soc. of Washington, 78: 479-489.
[ 43 ] Hawkins BA, Gordh G.1986.Bibliography of the word literature of the Bethylidae(Hymenoptera:bethyloidae). Insecta Mundi. 1: 261-283.
[ 44 ] Hawkins BA, Smith JWJ. 1986. Rhaconotus roslinensis (Hymenoptera:Braconidae), a candidate for biological control of stalkboring sugarcane pests (Lepidoptera: Pyralidae): development, life tables, and intraspecific competition. Annals of the Entomological Society of America 79: 905–911.
[ 45 ] Hong JI, Koh SH, Chung YJ, Shin SC, Kim GH, Choi KS. 2008. Biological characteristics of Sclerodermus harmandi (Hymenoptera: Bethylidae)parasitized on cerambycid. Korean Journal of Applied Entom logy. 47(2):133—139.
[ 46 ] Howard RW, Charlton M, Charlton RE. 1998. Host-finding, host- recognition, and host-acceptance behavior of Cephalonomia tarsalis (Humenoptera:Bethylidae). Ann. of Entomol.Sco. Am. 91(6):879-889.
[ 47 ] Jarjees E, Merritt DJ, Gordh G. 1998. Anatomy of the mouthparts and digestive tract during feeding in larvae of the parasitoid wasp Trichogramma australicum Girault (Hymenoptera:Trichogrammatidae). International Journal of Insect Morphology &Embryology. 27:103-110.
[ 48 ] Kishitani, U. 1961. Observations on the egg-laying habit of Goniozus japonicus Ashmead [Hymenoptera : Bethylidae]. Kontyo, 29, 175-179.
[ 49 ] Koch M,Bongers J. 1981. Nahrungserwerb des Ameisenlowen Euroleon nostras Fourcr. Neth.J. Zool. 31:713-728.
[ 50 ] Lanes GO, Azevedo CO. 2008. Phylogeny and taxonomy of Sclerodermini (Hymenoptera, Bethylidae, Epyrinae).Insect Syst Evol. 39: 55–86.
[ 51 ] Leius K. 1960. Attractiveness of different foods and flowers to the adults of some hymenopterous parasites. Canadian Entomologist. 92:369-376.
[ 52 ] Leius K.1961a. Influence of food on fecundity and longevity of adults of Itoplectis conquisitor (say) (Hymenoptera:Ichneumonidae). Canadian Entomologist. 92:771-780.
[ 53 ] Leius K.1961b. Influence of various food on fecundity and longevity of adults of Scambus buolianae (Htg.) (Hymenoptera:Ichneumonidae). Canadian Entomologist. 92:1079-1084.
[ 54 ] Nakamatsu Y, Fujii S, Tanaka T. 2002. Larvae of an endoparasitoid, Cotesia kariyai (Hymenoptera: Braconidea), feed on the host fat body directly in the second stadium with the help of teratocytes. Journal of Insect Physiology. 48: 1041一1052.
[ 55 ] Nakamatsu Y, Tanaka T. 2003b. Development of a gregarious ectoparasitoid, Euplectrus separatae (Hymenoptera: Eulophidae), that parasitizes Pseudaletia separata (Lepidoptera: Noctuidae). Arthropod Structure and Development. 32:329–336.
[ 56 ] Nakamatsu Y. Tanaka T. 2004. The function of trypsin-like enzyme in the saliva of Euplectrus separatae larvae. Journal of Insect Physiology.50:847–854.
[ 57 ] Qin Q, Gong H, Ding T. 2000. Two collagenases are secreted by teratocytes from Microplitis mediator (Hymenoptera: Braconidae) cultured in vitro. Journal of lnvertebrate Pathology. 76: 79-80.
[ 58 ] Ratcliffe NA, King PE, 1969. Morphological, ultrastructural, histochemical and electrophoretic studies on the venom system of Nasonia vitripennis walker ( Hymenoptera: Pteromalidae). Journal of Morphology. 127( 2):177 -204．
[ 59 ] Skinner WS, Dennis PA, Quistad GB. 1990. Partial characterization of toxins from Goniozus legnei( Hymenoptera:Bethylidae). Journal of Economic Entomology. 83( 3):733- 736．
[ 60 ] Strand MR, Quarles JM, Meola SM, Vinson SB. 1985. Cultivation of teratocytes of the egg parasitoid Telenomus heliothidis (Hymenoptera: Scelionidae). In Vitro Cellular and Developmental Biology. 21: 359-366.
[ 61 ] Strand MR, Meola SM, Vinson SB.1986. Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis. Journal of lnsect Physiology. 32: 389-402.
[ 62 ] Tang QY, Feng MG, 2007. DPS Data Processing System: Experimental Design, Statistical Analysis and Data Mining. 2nd ed. Science Press, Beijing. 75—128, 656-665. ( In Chinese with English summary).
[ 63 ] Thompson, S.N. 1980. Artificial culture techniques for rearing larvae of the chalcidoid parasite, Brachymeria intermedia (respiration, oxygen consumption, artificial rearing). Entomologia Experimentalis et Applicata 27, 133–143.
[ 64 ] Venkatrama, TV, Chacko MJ. 1961. Some factors influencing the efficiency of Goniozus marasmi, Kurian, a parasite of the maize and jowar leaf roller. Indian Acad. Sci. Proceed. 53:275-283.
[ 65 ] Vet LEM, Dicke M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141–172.
[ 66 ] Vet LEM, Groenewold AW, 1990. Semiochemicals and learning in parasitoids. J.Chem.Ecol. 16:3119–3135.
[ 67 ] Vinson SB, Mourad AK, Sebesta DK. 1994. Sources of possible host regulatory factors in Cardiochiles nigriceps (Hymenoptera: Braconidae). Archives of Insect Biochemistry and Physiology 26:197–210.
[ 68 ] Voukasoviteh MP. 1924. Sur la bioiogie de Goniozus claripennis Forst., parasite d' Oenophthira pilleriana S. hif. Bull. Soc. Hist. Nat. Toulouse, 52: 225-246.
[ 69 ] Wang GG, Zhou LH, Wang CX, Ma DJ, Lu B, 2004. Techniques of using Sderoderma guani against Monochamus alternatus. Forest Pest and Disease. 3:32—34. ( In Chinese with English summary).
[ 70 ] Wu ZX, Cohen AC, Nordlund DA.2000. Thefeeding behavior of Trchogramma brassicae: new evidence for selective ingestion of solid food. Entomologia Experimentalis et Applicata 96:1-8.
[ 71 ] Xiao GR, Wu J. 1983. A new species of Scleroderma (Hymenoptera, Bethylidae) from China. Scientia Silvae Sinicae. 8: 81—84. ( In Chinese with English summary).
[ 72 ] Yang ZQ. 2004. Advance in biocontrol researches of the important forest insect pests with natural enemies in China. Chinese Journal of Biological Control. 20(4):221—227. ( In Chinese with English summary).