Behavioral and Morphological Changes in Soldiers of Macrotermes gilvus (Termitidae: Macrotermitinae) Parasitized by Misotermes mindeni (Diptera: Phoridae)

ABSTRACT Misotermes mindeni Disney and Neoh is a solitary endoparasitoid of Macrotermes gilvus (Hagen) (Termitidae: Macrotermitinae), exclusively parasitizing the head of major soldiers. In this study, behavioral and morphological changes in the parasitized termite host were evaluated. We also observed the larval parasitoid emerging from the host. We found that parasitism mainly occurred in termite mounds overgrown with grass and mounds that had been broken up previously for other experiments. The parasitized soldiers showed a significantly lower level of interspecific aggressiveness compared with healthy soldiers (P < 0.05). Parasitized soldiers also changed in habitat preference to one isolated chamber of the nest. This might be an adaptive strategy that facilitates parasitoid dispersal, provides protection to parasitoids, and reduces the risk of parasitism to host colony. An abnormally rounded head capsule and remarkably short mandibles are characteristics of a parasitized soldier. The older larval fly stages were found only in major soldiers. We suggest that parasitization may first start in fourth or even earlier larval termite instars. The fly larva develops in the termite soldier's head capsule and pupates inside the host's body.

[1]  Chow‐Yang Lee,et al.  The Parasitoid, Verticia fasciventris Causes Morphological and Behavioral Changes in Infected Soldiers of the Fungus-Growing Termite, Macrotermes carbonarius , 2011, Journal of insect science.

[2]  Chow‐Yang Lee,et al.  Developmental Stages and Castes of Two Sympatric Subterranean Termites Macrotermes gilvus and Macrotermes carbonarius (Blattodea: Termitidae) , 2009 .

[3]  R. Disney,et al.  A new species of scuttle fly (Diptera: Phoridae) parasitizing a termite (Isoptera: Termitidae) in Malaysia. , 2009 .

[4]  T. Pape,et al.  The first blow fly parasitoid takes a head start in its termite host (Diptera: Calliphoridae, Bengaliinae; Isoptera: Macrotermitidae) , 2008 .

[5]  U. Maschwitz,et al.  Studies on European Ant Decapitating Flies (Diptera: Phoridae): I. Releasers and Phenology of Parasitism of Pseudacteon formicarum , 2008 .

[6]  S. N. Thompson,et al.  Parasitism of an insect Manduca sexta L. alters feeding behaviour and nutrient utilization to influence developmental success of a parasitoid , 2008, Journal of Comparative Physiology B.

[7]  R. Kfir,et al.  Diadegma mollipla parasitizing Plutella xylostella: host instar preference and suitability , 2007 .

[8]  M. Lenz,et al.  Challenges to subterranean termite management of multi-genera faunas in southeast Asia and Australia , 2007 .

[9]  D. Wood,et al.  TACHINIDAE: evolution, behavior, and ecology. , 2006, Annual review of entomology.

[10]  G. Boivin,et al.  Functional ecology of immature parasitoids. , 2001, Annual review of entomology.

[11]  M. Mackauer,et al.  Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models , 1991, Oecologia.

[12]  M. Rogers,et al.  Behavioral Changes in Japanese Beetle and Masked Chafer Grubs (Coleoptera: Scarabaeidae) After Parasitism by Tiphiid Wasps (Hymenoptera: Tiphiidae) , 2003 .

[13]  M. Bragança,et al.  Parasitism and biology of Myrmosicarius grandicornis (Diptera, Phoridae) in relationship to its host, the leaf-cutting ant Atta sexdens (Hymenoptera, Formicidae) , 2001, Insectes Sociaux.

[14]  L. Gilbert,et al.  Immature Development of Pseudacteon tricuspis (Diptera: Phoridae), an Endoparasitoid of the Red Imported Fire Ant (Hymenoptera: Formicidae) , 2001 .

[15]  M. Trabalon,et al.  Modification of morphological characters and cuticular compounds in worker ants Leptothorax nylanderi induced by endoparasites Anomotaenia brevis. , 2000, Journal of insect physiology.

[16]  J. Darlington,et al.  Alate termites (Isoptera: Termitidae) parasitized by a scuttle fly (Diptera: Phoridae) , 2000 .

[17]  P. Jmhasly,et al.  Intraspecific colony recognition in the termites Macrotermes subhyalinus and Macrotermes bellicosus (Isoptera, Termitidae) , 1999, Insectes Sociaux.

[18]  R. Disney,et al.  NEW SPECIES AND NEW HOST RECORDS OF PHORIDAE (DIPTERA) ASSOCIATED WITH TERMITES (ISOPTERA: TERMITIDAE) , 1997 .

[19]  D. Feener,et al.  Diptera as parasitoids. , 1997, Annual review of entomology.

[20]  D. Goulson Wipfelkrankheit: modification of host behaviour during baculoviral infection , 1997, Oecologia.

[21]  D. J. Thompson,et al.  Reciprocal influences and costs of parasitism on the development of Corcyra cephalonica and its endoparasitoid Venturia canescens , 1996 .

[22]  R. Disney Scuttle Flies: The Phoridae , 1994, Springer Netherlands.

[23]  R. Disney,et al.  Revision of the termitophilous Thaumatoxeninae (Diptera: Phoridae) , 1992 .

[24]  R. Belshaw,et al.  Insect parasitoids an evolutionary overview , 1992 .

[25]  J. McNeil,et al.  Host behaviour modification by the endoparasitoid Aphidius nigripes: a strategy to reduce hyperparasitism , 1992 .

[26]  B. Brown GENERIC REVISION OF PHORIDAE OF THE NEARCTIC REGION AND PHYLOGENETIC CLASSIFICATION OF PHORIDAE, SCIADOCERIDAE, AND IRONOMYIIDAE (DIPTERA: PHORIDEA) , 1992 .

[27]  R. Disney,et al.  Revision of the termite-parasitizing genus Dicranopteron (Diptera: Phoridae). , 1990 .

[28]  R. Cowie,et al.  Termite (Isoptera) damage and control in tropical forestry with special reference to Africa and Indo-Malaysia: a review , 1989 .

[29]  J. McNeil,et al.  Seasonal Microhabitat Selection by an Endoparasitoid Through Adaptive Modification of Host Behavior , 1989, Science.

[30]  R. Disney,et al.  Six new species of Oriental Phoridae from termite nests (Diptera; Isoptera; Termitidae & Rhinotermitidae) , 1989 .

[31]  J. McNeil,et al.  Biotic and abiotic factors involved in diapause induction of the parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae) , 1989 .

[32]  P. Ferrar A guide to the breeding habits and immature stages of Diptera Cyclorrhapha (Part 1: text; Part 2: figures). , 2015 .

[33]  R. Disney Two remarkable new species of scuttle‐fly (Diptera: Phoridae) that parasitize termites (Isoptera) in Sulawesi , 1986 .

[34]  R. Thapa Termites of Sabah. , 1982 .

[35]  N. Stamp Behavior of Parasitized Aposematic Caterpillars: Advantageous to the Parasitoid or the Host? , 1981, The American Naturalist.