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The Parasitoid, Verticia Fasciventris Causes Morphological And The Parasitoid, Verticia fasciventris Causes Morphological and Behavioral Changes in Infected Soldiers of the Fungus-Growing Termite, Macrotermes carbonarius Author(s): Kok-Boon Neoh and Chow-Yang Lee Source: Journal of Insect Science, 11(21):1-11. 2011. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1673/031.011.0121 URL: http://www.bioone.org/doi/full/10.1673/031.011.0121 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. 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Journal of Insect Science: Vol. 11 | Article 21 Neoh and Lee The parasitoid, Verticia fasciventris causes morphological and behavioral changes in infected soldiers of the fungus-growing termite, Macrotermes carbonarius Kok-Boon Neoha* and Chow-Yang Leeb Urban Entomology Laboratory, Vector Control Research Unit, School of Biological Sciences, Universiti Sains Malaysia, Minden, Penang, 11800, Malaysia Abstract The larval parasitoid Verticia fasciventris Malloch (Diptera: Calliphoridae) develops in the head of soldiers of the fungus-growing termite Macrotermes carbonarius (Hagen) (Isoptera: Termitidae). Morphological and behavioral changes in the host were evaluated and the termite castes and stages that were parasitized were identified. The larval emergence process is also described and possible mechanisms for the parasitoid fly’s entry into the host body are discussed based on qualitative observations. Only a single larva per host was found. The mature larva pupated outside the host’s body by exiting between the abdominal cerci. Parasitized soldiers possess a short and square-shaped head capsule, a pair of notably short mandibles, and a pair of 18-segmented antennae. Although parasitized soldiers were statistically less aggressive than healthy soldiers (P < 0.05), they expressed varying levels of aggression. Both minor and major soldiers can be parasitized and based on evidence from presoldiers, parasitization may begin during the precursor stages of soldiers. However, the stage at which parasitism first occurs has not been determined. Keywords: aggression behavior, blowfly, Calliphoridae, parasitism Correspondence: a* [email protected], b [email protected], *Corresponding author Editor: Todd Shelly was editor of this paper. Received: 2 December 2009, Accepted: 11 February 2010 Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 11, Number 21 Cite this paper as: Neoh KB, Lee CY. 2011. The parasitoid, Verticia fasciventris causes morphological and behavioral changes in infected soldiers of the fungus-growing termite, Macrotermes carbonarius. Journal of Insect Science 11:21 available online: insectscience.org/11.21 Journal of Insect Science | www.insectscience.org 1 Journal of Insect Science: Vol. 11 | Article 21 Neoh and Lee Introduction major soldiers develop from fourth larval instars, and minor soldiers derive from third Interactions between immature parasitoids and larval instars, and both pass through the hosts often cause drastic changes in the host. presoldier stage (Neoh and Lee 2009a). Pre- These changes can affect both individual and soldiers are non-sclerotized and possess colony-level responses in social insects. soldier-like features (e.g. mandible, head Parasitism in termites leads to various costs capsule). M. carbonarius usually forages for for host colonies. For instance, infected food on open ground (Inoue et al. 2001). workers often have reduced fitness. This may Soldiers often stand in a line at both sides of alter foraging rates, which would result in less the foraging processional columns and defend energy (= food source) channeling to the the workers. (Sugio 1995). Because of this young swarmers, thereby decreasing a behavior, soldiers may be at risk of predation colony’s reproductive output (Fuller and and of parasitism. Jeyasingh 2004). In the Caribbean termite, Nasutitermes acajutlae, infected termites have Life histories are exceptionally diverse among higher predation risk by lizard predators blowflies (Oldroyd 1964). For example, (Fuller et al. 2003). Parasites also cause blowfly larvae that cause myiasis are of behavioral changes in hosts (O’Donnell medical importance (Askew 1971), whereas 1997). For example, Korb and Fuchs (2006) others are carrion feeders and protelean found that compared to non-infected colonies, parasites of vertebrates and invertebrates mite-infected drywood termites performed (Oldroyd 1964; Colyer and Hammond 1968). more feeding and resting rather than the The dipteran genus Verticia of the subfamily allogrooming and proctodeal trophallaxis that Bengaliinae is widely distributed in the Malay can prevent parasites being transmitted within Peninsula, Borneo, Singapore, and Thailand the host colony. Furthermore parasitism of (Tumrasvin et al. 1979; Kurahashi et al. termites, which are known to be ecosystem 1997). Verticia fasciventris Malloch (Diptera: engineers (Dangerfield et al. 1998), may have Calliphoridae) is a small-sized fly with a body a large impact on ecosystem processes length of 5.5 mm for males. The fly is (Thomas et al. 1999). brownish-yellow in color with three indistinct longitudinal stripes on the thorax (Tumrasvin Macrotermes carbonarius (Hagen) (Isoptera: et al. 1979). Little is known about the biology Termitidae) is an abundant fungus-culturing of this fly, but it is known to parasitize some termite species in Southeast Asia. It is found species of Macrotermes (Sze et al. 2008). mainly in Thailand, Cambodia, Vietnam, the Malay Peninsula, and Borneo (Roonwal Parasites have significant evolutionary effects 1970). M. carbonarius exhibits a forked on their hosts, especially on social behavior. developmental pathway, in which the Therefore, a better understanding of the developmental lines of workers and nymphs relationships between social insects and their split at the first molt. This species exhibits parasites is necessary to elucidate the adaptive size dimorphism in the soldier castes, with strategies of both hosts and parasites. In the head widths of 4.40 and 2.95 mm for the present study, we quantified the effects of the major and minor soldiers, respectively. The fly parasitoid V. fasciventris on both soldiers differentiate from the worker line: morphological and behavioral changes in the Journal of Insect Science | www.insectscience.org 2 Journal of Insect Science: Vol. 11 | Article 21 Neoh and Lee termite host M. carbonarius. We also and major and minor workers to ensure that examined the prevalence of parasitism in this the soldiers were fed. host and the process of fly larva emergence. Based on our qualitative observations, we Emergence of larval parasitoid from host discuss possible mechanisms whereby fly Host and larval parasitoid behavior before and parasitoid enters the termite host’s body. after emergence of the larval parasitoid were video recorded (Sony Digital Handycam 8, Materials and Methods www.sony.com). The larvae and adult flies that emerged were preserved in 70% alcohol Study area and slide mounted for species identification. The study was conducted at Penang Island, located on the northeastern coast of the Morphometric analysis Malaysian Peninsula, between January 2008 Random samples of infected and healthy and April 2009. Parasitized termite mounds soldiers were taken and preserved in 70% were surveyed at two locations: (1) Minden alcohol for morphometric analysis. Various Campus of Universiti Sains Malaysia (USM) parts of parasitized soldiers (Neoh and Lee (5º 21’ N and 100º 18’ E): the campus 2009a) were observed under an Olympus encompasses an area of approximately 100 ha, SZ61 stereo microscope with IC Imaging and the density of M. carbonarius mounds on Standard, version 2.1 (Olympus, the campus can exceed 3 mounds/ha; and (2) www.olympus.com), and measured by using Bayan Lepas (5º 17’N and 100º 15’E): about 3 Analysis® Image Processing Software (Soft km on each side of the road along Jalan Imaging System GmbH, www.soft- (Road) Tun Dr Awang. The sites were imaging.net). The following measurements of approximately 8 km apart. infected soldiers were taken: width of the head and pronotum at the widest point; length of Termite mounds were broken up by removing the head at the side base of the mandibles; their outer wall. Under the wall, the colony length of the antenna; and length of the third was exposed to reveal fungus combs and clay hind tibia. Discriminant analysis was pillars. The colonies were surveyed for the performed on the measurements to determine presence of parasitized soldiers as these which soldier castes were parasitized (using soldiers tended
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