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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Biological Control 55 (2010) 63–71 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Laboratory evaluation of aggregation, direct mutual interference, and functional response characteristics of Pseudacteon tricuspis Borgmeier (Diptera: Phoridae) Donald C. Henne *, Seth J. Johnson Department of Entomology, 404 Life Sciences Building, Louisiana State University Agricultural Center, Baton Rouge, LA 70803, USA article info abstract Article history: Studies of parasitoid behavior yield information on behavioral strategies, and are crucial tests of theoret- Received 19 November 2009 ical models. The studies reported here provided insights into behavioral and functional responses of the Accepted 2 July 2010 red imported fire ant (Solenopsis invicta Buren) parasitoid, Pseudacteon tricuspis (Borgmeier) that were Available online 8 July 2010 previously unknown. Laboratory studies were performed to quantify aggregative responses of P. tricuspis adults to variable host ant densities, determine effect of direct mutual interference between multiple ovi- Keywords: positing P. tricuspis females confined with host S. invicta, elucidate the effect of confining one or two addi- Parasitoid behavior tional males with premated females on progeny sex ratios, and determine the form of the functional Oviposition response of individual ovipositing P. tricuspis. Consistent with theory and field observations, P. tricuspis Searching efficiency tended to aggregate at host patches containing greater numbers of ants. Some evidence of direct mutual interference was found, as per capita oviposition success declined when more than one female was con- fined and weak, but significant, reductions in searching efficiency were found when more than two P. tric- uspis females are simultaneously ovipositing. The presence of one or two males did not appear to affect ovipositional efficiency of solitary premated females, but normally male–biased sex ratios of progeny trended toward a 1:1 ratio when the number of males was increased from zero to two. None of the linear parameters in the logistic models were significantly different from zero suggesting that P. tricuspis had constant, type 1, attack rates regardless of host density, at least under our laboratory experimental design. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction spatially heterogeneous (Hassell and May, 1973; Chesson and Murdoch, 1986; Godfray and Pacala, 1992). Small and/or sparsely The study of host–parasitoid interactions has produced a wealth distributed host populations escape parasitism spatially and/or of theory. Ever since the development of simple theoretical models temporally in refugia because they are at low risk to parasitism. by Thompson (1924) and Nicholson (1933), a proliferation of re- Conversely, in a continuous time framework density-dependent search has shown that many interacting factors determine how host mortality theoretically destabilizes the interaction (Murdoch many hosts a female parasitoid can successfully parasitize. These and Stewart-Oaten, 1989). However, other factors are also impor- factors include host density, parasitoid density and the spatial dis- tant when parasitoids aggregate that can stabilize host–parasitoid tribution and density of hosts (Hassell and May, 1973; Beddington, interactions. 1975; Cook and Hubbard, 1977). The study of insect pests and their Hassell and Varley (1969) and Hassell and May (1973) recog- biological control have benefited from these theoretical insights, as nized the importance of behavioral interactions between multiple there is considerable interest in establishing the mechanisms by searching conspecifics that encounter one another, also known as which parasitoids control host densities (Stiling, 1987). direct mutual interference. Multiple simultaneously ovipositing fe- One prediction of optimal foraging theory is that parasitoids males may engage in aggressive interactions with conspecifics, should aggregate in higher density host patches in a density- resulting in delayed searching and more time wasted (Visser and dependent way to achieve maximal oviposition rates (Charnov, Driessen, 1991; Visser et al., 1999; Hassell, 2000), thereby leading 1976; Cook and Hubbard, 1977). This has long been suggested as to declining rates of host parasitism as parasitoid density increases an important stabilizing factor allowing for the persistence of dis- (Free et al., 1977). These interactions present unique problems for crete time host–parasitoid interactions, because parasitism risk is individual parasitoids when faced with optimal foraging decisions (Maynard Smith, 1974), such as maximizing host parasitism rates. The resulting contribution of these interactions, if sufficiently * Corresponding author. Present address: Texas AgriLife Research, 2301 Exper- iment Station Road, Bushland, TX 79012, USA. Fax: +1 806 534 5829. strong, can lead to the long-term stability of host–parasitoid inter- E-mail address: [email protected] (D.C. Henne). actions (Hassell, 2000). 1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2010.07.001 Author's personal copy 64 D.C. Henne, S.J. Johnson / Biological Control 55 (2010) 63–71 Studies of insect predation rates at variable host densities led to (3) elucidate the effect of confining 1 or 2 additional males with al- the derivation of the well-known type I, II and III functional response ready mated females on progeny production and sex ratios, and (4) curves (Holling, 1966). Solomon (1949) defined the functional re- determine the form of the functional response of individual ovipos- sponse as the density-dependent rate of attack of a single natural en- iting P. tricuspis to varying host densities. emy to changes in the number of hosts available. In other words, the functional response describes the relationship between the per capi- 2. Materials and methods ta predation (parasitization) rate of a predator (parasitoid) and prey density (Holling, 1959, 1961, 1966), and is a fundamental basis of all Monogyne S. invicta colonies were collected at the Louisiana Agri- 0 trophic (consumer–victim) interactions (Mills and Lacan, 2004). The cultural Experiment Station in St. Gabriel, Louisiana (30° 16 N, 91° 0 three types of functional responses were derived according to the 05 W). As of 2006, expanding populations of P. tricuspis in Louisiana relative shape of the curve. The type I functional response character- had not yet reached this location. Colonies were separated from soil izes arthropod predators (and parasitoids) that search for hosts ran- in the laboratory by the drip flotation method (Banks et al., 1981). domly in a patch and attack at an increasingly linear rate to a Ants from each colony were then sieved to yield host ants that were maximum level, at which point attack rates become independent within the preferred size class for P. tricuspis females (approximately of increasing prey density (a combination of density-dependent 1 mm head width (see Morrison et al., 1997)). and density-independent responses (Chong and Oetting, 2006; Para- Laboratory trials were performed using a large enclosed Plexi- Ò julee et al., 2006)). The type II functional response, or ‘disk’ equation, glas cage (120 cm  60 cm  60 cm) that was illuminated by an describes the predation rate as a non-linear function of prey density. overhead flicker-free fluorescent lamp (Hi-Lume Electronic Fluo- As host density increases, the number of hosts that can be attacked in rescent Dimmer Ballast, 0.70 amps, serial #4LZ22, by Lutron Corp., a fixed period of time hyperbolically reaches an asymptote, at which Coopersburg, PA) and heated by a 75 W infrared lamp. Plaster point the predator is spending all its time handling prey (Holling, blocks saturated with water were placed on the middle and cor- 1961; Parajulee et al., 2006). However, as host density increases ners of the cage floor to provide humidity. Trials were conducted the proportion of hosts parasitized by a type II parasitoid decreases when temperatures inside the cage were approximately 26–28 °C exponentially (inverse density dependence) (Chong and Oetting, and had 80–90% RH. At least 200–300 newly emerged P. tricuspis 2006; Parajulee et al., 2006). The type III functional response applies were released inside the cage prior to the trials. To minimize var- when the number of prey killed sigmoidally reaches an asymptote, iance in performance of P. tricuspis, only flies less than 1 day-old where prey killed increases in proportion up to an inflection point were used. While many S. invicta colonies were used, to reduce var- and then decreases in proportion (Parajulee et al., 2006). Therefore, iation individual trials used ants from the same colony. Except functional responses

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