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Effect of Gland Extracts on Digging and Residing Preferences of Red Imported fire Ant Workers (Hymenoptera: Formicidae)

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Effect of Gland Extracts on Digging and Residing Preferences of Red Imported fire Ant Workers (Hymenoptera: Formicidae) Insect Science (2013) 20, 456–466, DOI 10.1111/j.1744-7917.2012.01553.x ORIGINAL ARTICLE Effect of gland extracts on digging and residing preferences of red imported fire ant workers (Hymenoptera: Formicidae) Jian Chen and Guangmei Zhang USDA-ARS, National Biological Control Laboratory, Biological Control of Pests Research Unit, Stoneville, MS 38776, USA Abstract There is evidence that ant-derived chemical stimuli are involved in regulat- ing the digging behavior in Solenopsis invicta Buren. However, the source gland(s) and chemistry of such stimuli have never been revealed. In this study, extracts of mandibular, Dufour’s, postpharyngeal, and poison glands were evaluated for their effect on ant digging and residing preferences of S. invicta workers from three colonies. In the intracolonial bioassays, workers showed significant digging preferences to mandibular gland extracts in 2 of 3 colonies and significant residing preferences in 1 of 3 colonies; significant digging preferences to Dufour’sgland extracts in 1 of 3 colonies and significant residing preferences in 2 of 3 colonies. No digging and residing preferences were found for postpharyngeal and poison gland extracts. In intercolonial bioassays, significant digging and residing prefer- ences were found for mandibular gland extracts in 3 of 6 colony combinations. Significant digging preferences to Dufour’s gland extracts were found in 4 of 6 colony combinations and significant residing preferences in all 6 colony combinations. For postpharyngeal gland extracts, significant digging preferences were found only in 1 of 6 colonial combinations and no significant residing preferences were found. For poison gland extracts, no signif- icant digging preferences were found; significant residing preferences were found in 1 of 6 colony combinations. However, a significant residing deterrence (negative residing preference index) was found for 2 of 6 colony combinations. Statistical analyses using data pooled from all colonies showed that mandibular and Dufour’s gland extracts caused sig- nificant digging and residing preferences in both intracolonial and intercolonial bioassays but not postpharyngeal and poison gland extracts. By analyzing the data pooled from the same three colonies used for gland extract bioassays, it was found that, in no cases, workers showed significant digging and residing preferences to 2-ethyl-3,6-dimethylpyrazine, an alarm pheromone component from mandibular gland. Key words digging preference, Dufour’s gland, mandibular gland, poison gland, postpharyngeal gland, residing preference Introduction mass migration, in which they have to expose themselves to the open air. S. invicta construct earthen nests and for- Red imported fire ants, Solenopsis invicta Buren pre- aging tunnels which not only reduces the risk of an ant fer staying in a concealed environment except for a few colony being desiccated and predated, but also provides a critical events such as foraging, nuptial swarming, and unique structure for its optimum development (Tschinkel, 2006). Digging is a fundamental behavior in construction and maintenance of both nest and subterranean forag- Correspondence: Jian Chen, USDA-ARS, National Biolog- ing tunnels, which has been found to be precisely regu- ical Control Laboratory, Biological Control of Pests Research lated in ant colonies. For example, mound (aboveground Unit, Stoneville, MS 38776, USA. Tel: +1662 686 3066; fax: part of the nest) volume is directly proportional to the +1662 686 5281; email: [email protected] colony total weight in S. invicta (Tschinkel, 2006). Such a 456 Published 2012. This article is a U.S. Government work and is in the public domain in the USA. Ant digging and residing preferences 457 well-defined relationship between colony size and nest et al., 1981), and Atta laevigata (Smith)(Salzemann volume has also been found in other ant species et al., 1992); trunk route markers in Pogonomyrmex bar- (Tschinkel, 1987, 1999, 2004; Mikheyev & Tschinkel, batus (Latreille), P. rugosus Emery, and P. maricopa 2004), indicating that ants are able to adjust the volume Wheeler (Holldobler¨ et al., 2004). Dufour’s gland se- of their living space through the digging and constructing cretion is also used in the establishment of hierarchies behavior. In addition to nest and tunnel construction, dig- within colonies of Leptothorax gredleri Mayr (Heinze ging is also a critical component in ant rescue behavior et al., 1998) and during nest usurpation by the slave-maker (Nowbahari et al., 2009). ant, Rossomyrmex minuchae Tinaut (Ruano et al., 2005). Most, if not all, activities of an ant colony such as for- Parallel to its great functional diversity, the Dufour’sgland aging, mating, defense, offense, immigration, nestmate has a very complex chemistry (Morgan, 2008). However, recognition, and care of brood and eggs are mediated by whether the Dufour’s gland secretion affects the digging chemical signals (Vander Meer & Alonso, 1998; Jackson behavior has not been investigated. & Ratnieks, 2006; Smith et al., 2009). In addition to re- The poison gland is the main source of ant defen- leaser pheromones such as alarm and trail pheromones, sive/offensive compounds. However, in many ant species, which cause immediate alterations in the behaviors of the it also has other functions. The venom gland was identi- recipients, queens also use primer pheromones to trig- fied as a source of trail pheromones in a number of ant ger a change of developmental events in a colony, such species (Evershed & Morgan, 1983; Morgan & Ollett, as suppression of production of sexuals (Vargo, 1998) 1987; Janssen et al., 1995; Attygalle et al., 1998; Maile and change of conspecific aggressiveness (Vander Meer et al., 2000; Leclercq et al., 2001). In S. invicta, piperidine & Alonso, 2002). There is evidence that chemical stimuli alkaloids occur in the poison gland of workers and queens are also involved in regulating digging behavior in several (Brand et al., 1972; Blum et al., 1992) and piperideine ant species such as Conomyrma pyramica (Roger) (Blum alkaloids in workers only (Chen & Fadamiro, 2009; Chen & Warter, 1966), Formica yessensis Forel (Imamura, et al., 2009a, 2010). Although they are key attractants to 1982), Lasius niger (Linnaeus) (Rasse & Deneubourg, the phorid fly, Pseudacteon tricuspis Borgmeier, an intro- 2001), Pogonomyrmex badius (Latreille) (Wilson, 1958), duced fire ant parasitoid (Chen et al., 2009b), no data have P.occidentalis (Cresson) (Spangler, 1968), and S. invicta shown they have any pheromonal functions. The queen (Hubbard, 1974). However, the chemical nature of those recognition pheromones were found in the poison gland stimuli has been identified only for a few species such of the mated queens (Rocca et al., 1983). No information as 2-heptanone in C. pyramica (Blum & Warter, 1966), is available about the effect of venom gland secretion on 4-methyl-3-heptanone in P.badius (McGurk et al., 1966; the digging behavior of S. invicta. Wilson, 1958), and carbon dioxide in S. geminata (Fabri- The chemistry of postpharyngeal glands is well stud- cius) (Hangartner, 1969). ied for some ant species (Vinson et al., 1980; Bagneres` The mandibular gland was often identified as a source & Morgan, 1991; Oldham et al., 1999; Attygalle et al., of alarm pheromones (Morgan, 2008; Holldobler¨ & 2006). Phillips and Vinson (1980) described the mor- Wilson, 1990). In P.badius, the chemical releaser of dig- phology of postpharyngeal gland of S. invicta and found ging behavior is from the mandibular gland, which also that it was most highly developed in the queen. Post- elicits alarm behavior. The presumed source of digging pharyngeal glands often contain the same compounds pheromones in F. yessensis is also the mandibular gland as those on the cuticle (Bagneres` & Morgan, 1991; (Imamura, 1982). Alkylpyrazines are commonly found in Tschinkel, 2006). For example, the postpharyngeal gland mandibular glands of many ant species (Morgan et al., of S. invicta contains long-chain hydrocarbons, which are 1999). Recently, 2-ethyl-3,6-dimethylpyrazine was iden- also found on the cuticle (Cabrera et al., 2004). Vinson tified as an alarm pheromone from mandibular gland in et al. (1980) found that the function of the postpharyngeal S. invicta (Vander Meer et al., 2010). However, whether gland also included the absorption of free fatty acids and those alkylpyrazines were involved in regulating digging triglycerides. Postpharyngeal gland secretion functions as behavior is unknown. a modifier of aggressive behavior in the myrmicine ant, The Dufour’sgland has very versatile functions. It is the Manica rubida Latreille (Hefetz et al., 1996). In S. invicta, source of both releaser and orientator of trail following the role of cuticular hydrocarbons in colony recognition behavior in S. invicta (Wilson, 1959) and Gnamptogenys was first manifested by a study on a myrmecophilus bee- striatula Mayr (Blatrix et al., 2002); territorial markers tle, Myrmecophodius excavaticollis (Blanchard). It was in Myrmica rubra (Linnaeus), M. ruginodis Nylander, M. found that the acquisition of host hydrocarbons was as- sabuleti Meinert, M. scabrinodis Nylander (Cammaerts sociated with the acceptance of this beetle into S. invicta Published 2012. This article is a U.S. Government work and is in the public domain in the USA., 20, 456–466 458 J. Chen & G. Zhang colonies (Vander Meer & Wojcik, 1982). The effect of postpharyngeal gland secretion on the digging behavior has never been investigated. In this study,
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