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A Koinobiont Parasitoid Mediates Competition and Generates Additive Mortality in Healthy Host Populations

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A Koinobiont Parasitoid Mediates Competition and Generates Additive Mortality in Healthy Host Populations OIKOS 110: 620Á/628, 2005 A koinobiont parasitoid mediates competition and generates additive mortality in healthy host populations Tom C. Cameron, Helen J. Wearing, Pejman Rohani and Steven M. Sait Cameron, T. C., Wearing, H. J., Rohani, P. and Sait, S. M. 2005. A koinobiont parasitoid mediates competition and generates additive mortality in healthy host populations. Á/ Oikos 110: 620Á/628. Insects are subject to attack from a range of natural enemies. Many natural enemies, such as parasitoids, do not immediately, or ever, kill their victims but they are nevertheless important in structuring biological communities. The lag that often occurs between attack and host death results in mixed populations of healthy and parasitised hosts. However, little is understood about how the effects of parasitism during this lag period affect the competitive ability of parasitised hosts and how this, in turn, affects the survival and dynamics of the surviving healthy host populations. Here we investigate the impact of the timing of introduction, and the strength of that introduction, of a parasitoid natural enemy Venturia canescens (Gravenhorst) on the outcome of intraspecific competition between larvae of the Indian meal moth, Plodia interpunctella (Hu¨bner). In contrast to healthy hosts alone, we find reduced survival of healthy larvae with increasing periods of exposure to greater numbers of parasitised conspecifics. This represents indirect mortality of the host, which is in addition to that imposed by parasitism itself. Furthermore, longer periods of exposure to parasitised larvae resulted in an increase in development time of healthy individuals and they were larger when they emerged as adults. These results are relevant to both insectÁ/parasitoid and insectÁ/pathogen systems where there is a lag in host death following infection or attack. T. C. Cameron and S. M. Sait, School of Biology, Univ. of Leeds, Leeds, UK, LS2 9JT ([email protected]). Á/ H. J. Wearing and P. Rohani, Institute of Ecology, Univ.of Georgia, Athens, GA 30602, USA. HJW also at: Dept of Zoology, Univ. of Cambridge, Downing Street, Cambridge, UK. In many animal populations mortality events are stage- approach omits the influence of the timing of a mortality dependent, such as larval competition for limited event relative to other life history events such as resource resources or egg predation, and the timing of mortality consumption, dispersal and reproduction. Additionally, in an animal’s life cycle can be an important factor in the above approaches often only consider natural terms of its impact on survival and reproductive rates, enemies that kill their victim immediately. Many natural the vital rates by which a population compensates for enemies do not immediately or ever kill their victims, but losses. Previous empirical studies of compensation they are nevertheless important in structuring biological by resource populations in response to mortality communities through differentially altering vital rates have considered direct mortality or killing power of (Poulin 1999). natural enemies through manipulating enemy densities Koinobiont parasitoids, an example of such a natural (Huffaker and Matsumoto 1982, Graham and Lambin enemy, inject their hosts with an egg (or a clutch of eggs), 2002, Lane and Mills 2003) or artificially imposed stage- whereupon hatching the juvenile permits the host to live dependent mortality (Cameron and Benton 2004). This until some later stage (Haeselbarth 1979). The length of Accepted 10 February 2005 Copyright # OIKOS 2005 ISSN 0030-1299 620 OIKOS 110:3 (2005) this delay, or lag, in host death is often determined by the how large it is (Harvey et al. 1994) and it prefers to age or size of the host when it is parasitised and by the attack larger instar larvae (Sait et al. 1997), although all cue from the host to the juvenile parasitoid that the host instars except the smallest 1st instar larvae can support contains sufficient resources for the parasitoid to parasitoid development. complete its development (Godfray 1994). Attack by Previous investigations with this natural enemy have parasitoids with this life history strategy will generate a shown that greater numbers of adult Venturia attacking mixed host population that comprises both healthy and cohorts of healthy larvae result in an increased total parasitised hosts, thereby leading to competitive inter- number of hosts attacked, but reduced per capita success actions between them. Any changes in behaviour, for each parasitoid (Huffaker and Matsumoto 1982, physiology or growth of the parasitised host before the Lane and Mills 2003). Additionally, changes in the onset of destructive feeding by the parasitoid larvae are competitive nature of the host environment from re- akin to sublethal effects, which are better known in source limitation to enemy free space has been demon- hostÁ/pathogen systems (Sait et al. 1994, Boots and strated (i.e. competition for access to a physical refuge, Norman 2000, Boots et al. 2003). The period over which Begon et al. 1995, Lane and Mills 2003). Uniquely we these effects can influence competitive dynamics in the consider the additional indirect effects of parasitised host population would be determined by the time of competitors in an experimental community. introduction of the parasitoid natural enemy relative to the period of competition in the host life history, usually the duration of the larval stage. Recent work in numerous systems has begun to demonstrate the im- Methods portance of infected competitors in enemyÁ/victim Plodia have been reared as an out-bred colony at Leeds dynamics and in the structuring of ecological commu- for three years following transfer from the University of nities (e.g. bacterial communities, Kusch et al. 2002; Liverpool where they were cultured under identical lepidopteran pest communities, Bernstein et al. 2002; conditions for ten years. Eggs were collected daily from natural lepidopteran populations, Sisterson and Averill Plodia reared on bran diet (broad bran 800 g, honey 2003). However, few studies have focused on how 200 ml, glycerol 200 ml, yeast 160 g, preservatives 12 g) competition for resources between parasitised and to start cultures of uniform age (Begon et al. 1995, Sait healthy individuals may influence the feedback between et al. 2000). Venturia were from a thelytokous laboratory interacting parasitoid and host populations. population reared on Plodia for over a decade. The In this paper we investigate how the timing of parasitoids were maintained in a constant environment introduction of a common natural enemy may alter the of 289/28C during development and 229/28C post competitive dynamics within a population with limited emergence. Only parasitoids between 2Á/4 days post resources. Such a question is timely given the progress emergence were used in the experiment. Host stock made in understanding the role of predation and populations and the experiments were maintained at parasitism in mediating density-dependent competition 279/28C and LD cycle of 16:8 h. within populations and between species (Chase et al. Forty early third instar larvae (13 days old) were 2002). An emerging body of empirical and theoretical selected randomly from the stock cultures and placed in evidence has highlighted the importance of the timing of a clear plastic box (dimensions 73/73/73 mm, Azpak, mortality events, including enemy introduction, to the Loughborough) containing 2.2 g of bran diet. This outcome of dynamics within age-structured populations represented 50% of the diet required for all 40 larvae (parasitism, Mu¨nster-Swensden and Nachman 1978, to pupate successfully (Reed 1998), but did not provide a Godfray et al. 1994, Briggs and Latto 1996, van physical refuge from parasitism (Begon et al. 1995). On Nouhuys and Lei 2004; commercial harvesting, Astrom day 1 of the experiment (one day after the larvae were et al. 1996, Jonzen and Lundberg 1999, Tang and Chen put in the box) a single 2Á/4 day old parasitoid was added 2004; hunting, Kokko 2001). to the box and allowed to search for and parasitise hosts We manipulate the time over which host larvae for a fixed period of 6 h before being removed. A pilot parasitised by a parasitoid, Venturia canescens (Grave- study demonstrated that a 6 h period of attack from a nhorst) (hereafter Venturia), compete within cohorts of single parasitoid gave rise to populations of both healthy healthy larvae of the Indian meal moth, Plodia inter- and parasitised host larvae (349/28 sd successful attacks/ punctella (Hu¨bner) (hereafter Plodia). Venturia is a 100 hosts). This process was subsequently repeated in solitary koinobiont endoparasitoid of Pyralidae larvae separate boxes on days 2, 4, 6, 8, 10, 12 and 14, which such as Plodia. Wasps lay a single egg inside a larva that, resulted in decreasing periods of competition between as described above, hatches and delays development parasitised and unparasitised hosts. Our final treatment until the final instar of the larva (Harvey et al. 1994). (day 14) was determined by a pilot study that showed The parasitoid takes about 20Á/25 days to develop that this was approximately when host pupation oc- depending on temperature, which instar it attacked and curred. In this treatment parasitised and unparasitised OIKOS 110:3 (2005) 621 larvae compete for the shortest period of time. Each of Venturia eggs soon after parasitism (Salt 1970), there is the eight parasitism treatments plus a control, in which likely to be a negligible effect on subsequent host no parasitoid was added, was replicated nine times. development and we assume that in our experiment The boxes were monitored daily and the survival of those hosts that encapsulate the parasitoid will develop moths and their development times were recorded. Adult and have the same competitive ability as healthy hosts. moths were sexed and placed in labelled tubes and frozen Larval mortality, resulting from injury during parasitoid for later leg measurements (right mid femur). Leg attack, is negligible in 3rd to 5th instars (Table 1).
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