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). In this lengths are correlated with egg load in Plodia (Gage study, superparasitism is unlikely to occur but it has to 1998, Reed 1998), representing a potential delayed effect be assumed that if it does it has no effect on the results. of competition since growth and reproduction are As parasitism events occur independently at different influenced by resource acquisition during the larval points in time, each parasitoid introduction treatment stages in this and many insects (Benson 1973). Addi- (i.e. days 1Á/14) is considered separately in the analyses. tionally, adult parasitoid numbers from each treatment Differences between the replicates and their interactions were recorded. explained little of the variation in survival and were non- significant (ANOVA block F1,63 /0.12, p/0.72, all interactions p/0.39).

Response variables and statistical analysis Size and development time Host survival Leg size data were analysed with a general linear model The effect of the timing of parasitoid introduction on (ANOVA). Differences in the time to emergence of host survival was determined by a general linear model moths were analyzed with an accelerated failure time (ANOVA) of the arcsine square root transformation of survival model (Fox 2001) using a Weibull distribution. the survival data. Additionally, the effect of parasitised This distribution best fit the censored and normalized larvae density, which is an estimate of the strength of deviance residuals from our model (Harrell 2003). We competition with parasitized hosts, on the survival of the modelled emergence time as a function of the timing of healthy larvae was examined by plotting the total parasitoid introduction, the strength of the parasitoid emergence of parasitoids from each cohort against introduction (strength/the number of successful para- proportional survival of healthy larvae to adult moths sitoid attacks) and the sex of the adults. Initial model after each 6-hour bout of parasitism. This is calculated assessment indicated that males consistently mature after first correcting for background mortality (Table 1). earlier than females (pB/0.0001) and that there was no

Data were arcsine transformed for analysis and the interaction between treatment and sex (p/0.585), so we means and standard deviations were back transformed examined each sex separately. All the data from all the for graphical presentation. treatments were pooled for the failure time model such In order to account for encapsulation, when the host that each adult moth emergence was an individual event immune system encloses and kills a developing para- in the model and this took account of differences sitoid egg or larvae, and its potential effect on the between replicates. surviving larva, the effect of the number of emerging For all analyses, post-hoc multiple comparisons were parasitoids was also analysed after weighting by an conducted using the best.fast method that determines approximate encapsulation rate of 5% (Reed et al. 1996, the smallest critical value by choosing from various S. M. Sait unpubl.). However, as Plodia encapsulates methods and minimises type II error by simultaneously

Table 1. Estimates of background survival of different instars of parasitised and healthy larvae. The survival of both parasitised and healthy larvae when put in competitive environments is also given. Rates refer to either mean values or ranges. In these estimates, sample size refers to the number of replicates with the number of larvae in each replicate given in brackets.

Vital rate Instar Rate (%) Sample size Reference

30 99 Background mortality of healthy larvae 4 0 97 Sait et al. 1994a 50 93 3 6 148 Sait et al. 1995 Background mortality of parasitised larvae 5 9 53 Harvey et al. 1995 5 9 52 S. M. Sait, unpubl. Background mortality of parasitised larvae attacked once 5 5 33 S. M. Sait, unpubl.

Survival of parasitised larvae under competition 2Á/560Á/85 7 (80) Begon et al. 1995 3Á/566Á/86 9 (10,20,40) Cameron, T.C, unpubl.

Survival of healthy larvae under competition 3Á/5 70 9 (40) Cameron, T.C, unpubl.

622 OIKOS 110:3 (2005) running the procedure for all treatments versus the regression of p/0.05). In these particular treatments control. All analyses and models were run in S-plus there was little variation in the strength of attack statistical software (Version 6.1.2 student ed. for MS between the replicates, which resulted in a clumping of Windows, # 2002 Insightful Corp. Seattle WA). the data. Weighting the survival data for known encapsulation rates makes no difference to the outcome of competition (results not shown), which supports our prediction that hosts that have successfully encapsulated Results the parasitoid compete at the same level as healthy hosts. Effects of parasitism and competition on survival of healthy host larvae Effects of parasitism and competition on pattern of Overall, earlier parasitoid introduction, which leads to adult emergence longer periods of competition between parasitised and healthy larvae, results in a significant reduction in Since the qualitative effects of the treatments on both survival of healthy moth larvae compared to the control sexes were similar we have only provided detailed where healthy larvae were reared alone (Fig. 1, ANOVA, analyses of the effects of timing and strength of F8,18 /8.91, pB/0.0001). Parasitoid introduction on days introduction on female development. A breakdown of 12 and 14, which results in shorter periods (1Á/3 days) of these results for both sexes is provided online. competition with parasitised larvae, were the only Increased periods of exposure to parasitised conspe- treatments where there was no significant reduction in cifics following earlier introduction (e.g. comparing the survival of healthy larvae. introduction on day 1 against controls, pB/0.001) results Increased strength of exposure to competition with in an increase in development time (1Á/4 days delay, parasitised hosts also significantly reduces the survival Fig. 3 aÁ/c) whereas parasitoid introduction on days 12 of the healthy unparasitised larvae (Fig. 2, ANOVA, and 14, at the end of the period of competition, results in F28,18 /6.06, pB/0.001). Additionally, there was a sig- a significant decrease (2 days, pB/0.01 and pB/0.01 nificant interaction between the time of parasitoid respectively, Fig. 3 aÁ/c) compared to the controls. introduction and the strength of competition with Across all introduction treatments, increased strength parasitised hosts (ANOVA, F26,18 /3.46, pB/0.005); of exposure (parasitised larvae density) results in a earlier introduction coupled with higher numbers of reduction in time to emergence (approximately 3 days, parasitised larvae leads to a greater reduction in survival pB/0.01, Fig. 3 dÁ/f). of remaining healthy larvae. The negative relationship is consistent across all treatments (Fig. 2), but not always statistically signifi- Effects of parasitism and competition on healthy cant (parasitoid introduction on days 4 and 6 results in a adult size 0.8 There were differences in leg size measurements between

0.7 the sexes; males were smaller at eclosion (males 1.729/

e / a 0.13 mm; females 1.8990.15 mm, students t-test: v r

a 0.6 l t1, 387 / /7.881, pB/0.0001), but there were also no y h

t / l significant treatment-sex interactions (ANOVA, F1,834 a 0.5 e

h 0.264, p/0.60) and the data for each sex was analysed f o

l 0.4 separately. a v i v

r In general, larger adult moths of either sex emerged u

s 0.3

l from boxes invaded by a parasitoid (Fig. 4a, only a n o

i females shown as graphically similar to males, ANOVA: t 0.2 r

o / / / p females F8,271 5.54, pB0.0001, males F8,38 4.68, o r

P 0.1 pB/0.0001). The effect was only significant in later periods of introduction (treatments on days 12 and 0 014121086421 14, post hoc mca, Sidak method), when competition Day of introduction of adult parasitoid between healthy and parasitised larvae is most limited, but also when competition between healthy hosts alone Fig. 1. Proportional survival (9/sd) of healthy larvae with increasing periods of exposure to competition with parasitised has been most prolonged. larvae. A greater period of exposure relates to an earlier adult Increased strength of exposure results in significant parasitoid introduction (day of attack). A period of 14 days changes in the average size of healthy larvae in the exposure is when the day of parasitism was day 1. Values cohorts relative to the control treatments (Fig. 4b only signiﬁcantly different (pB/0.05, Dunnet method) from the control, no exposure to parasitoids, are denoted by . females shown as males graphically similar, ANOVA

OIKOS 110:3 (2005) 623 1.0 Fig. 2. The proportional survival of healthy larvae against the

e density of parasitised larvae a

v (strength of introduction). Each r 0.8 10 a l regression line, denoted by a Range of survival y 1

h number, corresponds to the day

t for controls l 2

a of parasitoid introduction. The e

h 0.6 ﬁgure caption describes the f

o summary statistics for each l 12 a

v regression. i

v 4 r 1, p<0.007 r2=0.62 u 0.4 s 2, p<0.003 r2=0.68 l

a 6 4, p=0.49 n o

i 6, p=0.93 t r

o 8 8, p=0.08 r2=0.28

p 0.2 10, p=0.047 r2=0.37 o r 12, p=0.037 r2=0.40 P 14 14, p=0.002 r2=0.72

0.0 010203040 Density of parasitised larvae

females F24,364 /3.81, PB/0.001, males F25,376 /3.33, larval density (second order polynomial y/1.8853/ 2 PB/0.001). It would appear, however, that the direction 0.0089/x/ /0.0004/x ,F2,409 /8.63, p/0.002). of the effects on size changes with increasing parasitized Fig. 4b suggests that there may be a threshold (para- 0 0 0 . . . (a) (b) (c) 1 1 1 8 8 8 . . . 0 0 0 6 6 6 . . 0 6 . 1 6 6 0 1 0 0 1 4 8 8 0 8 14 10 2 4 10 2 4 4 . . 2 . 4 10 0 0

12 0 Emergence Emergence Emergence 0 14 4 2 2 2 12 . . . 0 0 0 14 12 0 0 0 . . . 0 0 0 25 26 27 28 29 30 25 26 27 28 29 30 25 26 27 28 29 30 Days post start Days post start Days post start Adjusted to: str2=1 Adjusted to: str2=3 Adjusted to: str2=5 0 0 0 . . (d) . (e) (f) 1 1 1 8 8 8 . . . 0 0 0 6 6 6 . . 1 . 1 0 0 3 3 0 1 4 2 4 2 2 4 4 4 . . . 5 5 3 0 0 0 Emergence Emergence Emergence 4 2 2 2 . . . 0 0 0 5 0 0 0 . . . 0 0 0 25 26 27 28 29 30 25 26 27 28 29 30 25 26 27 28 29 30 Days post start Dayspost start Days post start Adjusted to: treat=1 Adjusted to: treat=6 Adjusted to: treat=14

Fig. 3. Chart (aÁ/c) show the survival model outputs for the effects of the timing of introduction of the adult parasitoid on the proportion of Plodia not emerged (Y-axis) over time (X-axis). The analysis is adjusted for increasing density of parasitised larvae from (a) low (str/1) (b) medium (str/3) (c) high (str/5). The solid dark line represents the control treatment where no parasitoid invaded. Charts (dÁ/f) shows the survival model outputs for the effects of exposure to increasing density of parasitised larvae (1/0Á/ 7, 2/8Á/14, 3/15Á/21, 4/22Á/29, 5/30/) independent of the period of exposure. The analysis is adjusted for (d) short (treat/1) (e) medium (treat/6) (f) long (treat/14) periods of exposure. Compare plots at 0.5 on Y-axis where 50% of moths have emerged.

624 OIKOS 110:3 (2005) (a)2.2 relative to the survivorship that results from competition bbbaa a aaa between healthy larvae alone. Furthermore, these effects 2.1 are additive, so that mortality of healthy larvae is higher e a v r under longer periods of competition with greater den- a l y

h 2 t sities of parasitised conspecifics. l a e

h There are a number of possible mechanisms driving g n i

v 1.9 i the results we obtained for the interaction between v r u

s healthy Plodia larvae and Venturia-parasitised larvae: f o )

s 1.8 (i) parasitised larvae inflict more fatal injuries on r e t

e competitors; (ii) parasitised larvae behave differently m i l l i from healthy larvae; (iii) parasitism results in decreased m 1.7 ( e z

i resource requirements of the host larvae. We will discuss s g

e each of these possibilities in turn.

L 1.6

1.5 0 14 12 10 8 6 4 2 1 Day of introduction of adult parasitoid (i) Are parasitised Plodia more aggressive? Larval Pyralidae fight and inflict injury on competitors (b) 2.4 with their mandibles and injuries may result in infection and/or death (Corbet 1971). It has been shown that 2.2 parasitised Plodia larvae are more likely to be injured or cannibalised than their healthy counterparts if larvae are 2.0 kept with no food (Reed et al. 1996), though any amount m

m of food provision negated this observation. Parasitised e z

i 1.8

s larvae of the cranberry fruitworm Acrobasis vaccinii g

e Riley (Lepidoptera: Pyralidae) were also less able to L 1.6 defend a territory than healthy larvae (Sisterson and Averill 2003). So, it is unlikely that parasitised larvae are 1.4 more aggressive. Considering that Venturia selectively parasitise the 1.2 largest larvae (Sait et al. 1995, 1997), it is well 010203040documented that larger Plodia larvae are stronger, Density of parasitised larvae more aggressive competitors and asymmetric competi-

Fig. 4. (a) Mean leg size in millimeters (9/ sd) as a function of tion is important in driving the population dynamics the day of parasitoid introduction. A greater period of exposure observed in closed experimental populations (Sait et al. relates to an earlier adult parasitoid introduction (day of attack). A period of 14 days exposure is when the day of 1994, Bjørnstad et al. 1998, Briggs et al. 2000, Wearing parasitism was day 1. The same letter indicates treatments that et al. 2004a, 2004b). Parasitised larvae may then be were not signiﬁcantly different from each other. (b) The competitively dominant in fighting bouts over healthy relationship between leg size of surviving healthy moths and larvae due to their larger size, rather than their infective the density of parasitised larvae. All data presented are for female moths only as males show similar results. See text for state. However, as the greatest reduction in healthy larval equation. survival followed early parasitoid introduction, when hosts are small and there is little variation in host size, sitised larvae at densities of 10Á/12) where the effects of and parasitism reduces host body size compared to increasing numbers of parasitised conspecifics at low healthy larvae (Harvey et al. 1994), we do not feel that densities leads to larger adults, but at high densities leads selection of larger larvae by the searching adult para- to smaller adults. sitoid is an important mechanism in these experiments.

(ii) Do parasitised larvae behave differently? Discussion Contestants often display a signal to deter or acknowl- Intuitively we might expect that parasitised hosts would edge a competitor in order to prevent an actual bout exert a weaker competitive effect on healthy, unparasi- taking place (Parker 1974). In Plodia, larvae regurgitate tised hosts. In this study we have found the opposite fluid from their mandibular glands on meeting a effect. An increase in either the period or strength of conspecific, after which the two competitors withdraw competitions with parasitised conspecific larvae can (Corbet 1971). Overcrowding stimulates the excess decrease the survival of the remaining healthy larvae production of mandibular fluids which is thought to

OIKOS 110:3 (2005) 625 induce dispersal behaviour (Corbet 1971, Mudd and entirely parasitised larvae than from entirely healthy Corbet 1973, Mossadegh 1980). This behaviour could be larval populations. considered as interference competition as they disrupt Contrary to this are the findings of a similar series of the time available to the larvae for feeding. experiments with Drosophila melanogaster and the It is unknown whether parasitism of Plodia by parasitoid Asobara tabida (Hymenoptera: Braconidae) Venturia results in a different response of parasitised (Kraaijeveld and Godfray 1997, Tien et al. 2001). hosts to mandibular fluids, but if parasitised larvae were Parasitised larvae were found to have reduced back- behaving according to different density-dependent func- ground survival rates compared to healthy larvae and tions and requirements, they may have a competitive their competitive abilities were compromised (Tien et al. advantage over healthy hosts by avoiding competitors 2001). This was due to the costs involved in the hosts and suffering less interference competition. immune response to a parasitoid egg. In our system Parasitised hosts often appear to behave differently Plodia is not a strong encapsulator of Venturia eggs from their healthy counterparts (Fritz 1982). Whether (approximately 0Á/10% depending on instar attacked) this is due to manipulation of the host by the juvenile and Venturia will passively avoid the immune response of parasitoid is still open to debate (Godfray 1994). its host (Kinuthia et al. 1999, Beck et al. 2000). Similarly, However, it is clear that some parasitised hosts, parasitised cranberry fruitworm Acrobasis vaccinii Riley although likely to perish due to infection, suffer (Lepidoptera: Pyralidae) were found to give up their reduced rates of other mortality factors in the interim resource, a single cranberry, more readily under strong period between infection and death. There are docu- direct contest competition (Sisterson and Averill 2003). mented cases of reduced mortality, or reduced prob- In this situation the resource that is challenged is both a ability of further attack of insect larvae following initial territory and a food source and it is therefore difficult to attack by a parasitoid (Stamp 1981, Brodeur and compare to our system. McNeil 1992). Competition for resources is not cited If reduced resource consumption due to reduced as a possible selection pressure for the evolution of host requirements is the mechanism driving reduced suscept- behaviour modification. However, other selective pres- ibility to competition of parasitised larvae, we must ask sures, such as reduced activity or dispersal or conspecific why it is not releasing healthy larvae from competition? This is because a greater number of both adult moths patch avoidance, may have the same effect of increasing and parasitoids develop compared with the number of access to resources. While it is intuitive that larvae may developing moths in the parasitoid-free populations, behave differently following parasitism, it is not clear which reflects the number of individuals that survive that it could generate the survival patterns observed competition. The overall resource use is greater and the here. competitive environment is increased when parasitoids are present (Takahashi 1973, Bernstein et al. 2002, Lane and Mills 2003, T. C. Cameron unpubl.). This hypothesis is not unlike that of the R* theorem (Tilman 1982); in (iii) Do parasitised hosts require fewer resources? our case parasitism reduces the minimum requirement of Harvey et al. (1994, 1995) observed that hosts that were parasitised hosts, allowing them to survive periods of strong competition at the expense of healthy host parasitised when small and subject to long periods of survival. We predict that this pattern of hostÁ/parasitoid parasitism, were significantly smaller and had reduced interaction will be observed more broadly when the level growth rates than their healthy unparasitised conspeci- of host competition, host survival and development is fics. This result has been confirmed in other pyralid dependent on meeting stage thresholds that are governed moths (Harvey and Vet 1997). Thus, Venturia success- by food intake, when larval parasitoid survival is high fully develops and emerges from hosts that are often and when parasitoid resource requirements for successful smaller than healthy Plodia larvae. This suggests that, development are less than that of its host. although the parasitoid does not commence destructive feeding until the host has reached a threshold size, Venturia’s minimum requirements for development are less than that of its host (approximately 50Á/70%). Such a difference in requirements may render parasitised Patterns of size and date at emergence larvae less susceptible to competition-derived mortality The introduction of parasitised competitors resulted in when resources are scarce. This was suggested by an increase in size of surviving adult moths. Survivors, Bernstein et al. (2002) who compared the outcome of then, gain from enemy introduction as larger body size competition on host survivorship between either healthy can confer benefits to the individual (e.g. mate access or Ephestia kuehniella (Zeller) alone or exclusively between fecundity, Gage 1998). However, increases in moth size those parasitised by Venturia. There were a greater are reduced when the exposure to parasitised conspeci- number of insects emerging from high densities of fics is for a longer period, emphasising that the potential

626 OIKOS 110:3 (2005) benefits following survival from parasitoid attack can be Additional information can be found at: countered by prolonged periods of competition with http://www.fbs.leeds.ac.uk/People/staffprofile.php?staff/ parasitised competitors. bgytcc Late parasitoid introduction, which results in significantly larger moths that develop faster than Acknowledgements Á/ The authors would like to thank Andrew Beckerman for help with the survival model, Kris Kirby, Phil controls, demonstrates an important point. Despite Graham, Rebecca Shackleton, Paul Challender and Katherine much of the resource depletion having already occurred, White for technical assistance. This study is supported by a large larvae that escape parasitism during late parasitoid NERC studentship awarded to TCC and was in part supported by NERC grant NER/A/S/2000/00341 to PR and SMS. introduction benefit over larvae in the control experiments. The decrease in development time is likely to occur due to a relaxation of interference competition for safe pupation sites i.e. cannibalism free space for References vulnerable pupae. A possible explanation for this is that large final instar larvae parasitised by Venturia are Arbogast, R. T. and Mullen, M. A. 1978. Spatial distribution of entering the pre-pupal stage more quickly than a similar eggs by ovipositing Indian meal moths, Plodia interunctella (Hu¨bner) (Lepidoptera: Pyralidae). Á/ Res. Popul. Ecol. 19: sized healthy larva, a potential mechanism of risk 148Á/154. avoidance from cannibalising larvae (J. Whittingham Astrom, M., Lundberg, P. and Lundberg, S. 1996. Population dynamics with sequential density-dependencies. / Oikos 75: and S. M. Sait, unpubl.). Á 174Á/181. The effects of parasitised larvae competitor density on Beck, M., Theopold, U. and Schmidt, O. 2000. Evidence for healthy larval development are non-linear as was found serine protease inhibitor activity in the ovarian calyx fluid of in E. keuhniella (Lane and Mills 2003). Overall, surviv- the endoparasitoid Venturia canescens. Á/ J. Insect Physiol. 46: 1275Á/1283. ing healthy larvae that took longer to develop were Begon, M., Sait, S. M. and Thompson, D. J. 1995. Persistence of smaller as adults, contrary to what might be expected a parasitoid-host system-refuges and generation cycles. Á/ Proc. R. Soc. Lond. Ser. B Biol. Sci. 260: 131Á/137. from traditional life history theory. When faced with a Benson, J. F. 1973. The biology of Lepidoptera infesting stored competitive environment at earlier stages of develop- products, with special reference to population dynamics. ment, an individual can avoid the lethal effects of Á/ Biol. Rev. 48: 1Á/26. Bernstein, C., Heizmann, A. and Desouhant, E. 2002. Intras- competition through delaying growth (Day and Rowe pecific competition between healthy and parasitised hosts in 2002). There are costs involved in this tradeoff and they a hostÁ/parasitoid system: consequences for life-history arise during later stages of competition, where resource traits. Á/ Ecol. Entomol. 27: 415Á/423. Bjørnstad, O. N., Begon, M., Stenseth, N. C. et al. 1998. quality and quantity has been reduced. Delaying growth Population dynamics of the Indian meal moth: demographic to increase survival results in smaller sized adults, which stochasticity and delayed regulatory mechanisms. Á/ J. Anim. in turn results in a reduced reproductive potential, as in Ecol. 67: 110Á/126. Boots, M. and Norman, R. 2000. Sublethal infection and the female Plodia, size is correlated with egg load (Gage population dynamics of hostÁ/microparasite interactions. 1998). This is evidence of a delayed density-dependent Á/ J. Anim. Ecol. 69: 517Á/524. response. Boots, M., Greenman, J., Ross, D. et al. 2003. The population dynamical implications of covert infections in host /micro- The results presented here are relevant to the Á parasite interactions. Á/ J. Anim. Ecol. 72: 1064Á/1072. understanding of parasitoidÁ/host systems where com- Briggs, C. J. and Latto, J. 1996. The window of vulnerability and petition between hosts is important, and perhaps its effect on relative parasitoid abundance. Á/ Ecol. Entomol. 21: 128Á/140. of particular interest to infestations of larvae in stored Briggs, C. J., Sait, S. M., Begon, M. et al. 2000. What causes products as the outbreaks are often patchily distributed, generation cycles in populations of stored-product moths? competition within a patch is strong (Arbogast and Á/ J. Anim. Ecol. 69: 352Á/366. Brodeur, J. and McNeil, J. N. 1992. Host behavior modification Mullen 1978), and the aim of biocontrol release is by the endoparasitoid Aphidius nigripes Á/ a strategy to for parasitism rates to be high. Koinobiont parasitoids reduce hyperparasitism. Á/ Ecol. Entomol. 17: 97Á/104. may be useful biological control agents not only because Cameron, T. C. and Benton, T. G. 2004. Stage structured harvesting and its effects: an empirical investigation using of direct mortality caused by killing the host, but if soil mites. Á/ J. Anim. Ecol. 73: 996Á/1006. the larvae they parasitise are also less susceptible Chase, J. M., Abrams, P. A., Grover, J. P. et al. 2002. The to competition they can also suppress pest populations interaction between predation and competition: a review and synthesis. Á/ Ecol. Lett. 5: 302Á/315. through density-dependent additive mortality. Indeed, Corbet, S. A. 1971. Mandibular gland secretion of larvae of the pest management and general ecological models flour moth, Anagasta kuehniella contains an epideictic predict that reduced susceptibility to competition of pheromone and elicits oviposition movements in a hyme- nopteran parasite. Á/ Nature 232: 481. parasitised hosts can benefit control through introducing Day, T. and Rowe, L. 2002. Developmental thresholds and the stability in the enemyÁ/victim dynamics (Spataro evolution of reaction norms for age and size at life-history and Bernstein 2004). There has been little exploration transitions. Á/ Am. Nat. 159: 338Á/350. Fox, G. A. 2001. Failure time analysis. Á/ In: Gurevitch, S. M. S. of how influential or widespread these effects may be in J. (ed.), Design and analysis of ecological experiments. nature. Oxford Univ. Press.

OIKOS 110:3 (2005) 627 Fritz, R. S. 1982. Selection for host modification by insect studied by a simulation model. Á/ J. Anim. Ecol. 47: 159Á/ parasitoids. Á/ Evolution 36: 283Á/288. 171. Gage, M. J. G. 1998. Influences of sex, size, and symmetry on Parker, G. A. 1974. Assesment strategy and the evolution of ejaculate expenditure in a moth. Á/ Behav. Ecol. 9: 592Á/597. animal conflicts. Á/ J. Theor. Biol. 47: 223Á/243. Godfray, H. C. J. 1994. Parasitoids: behavioural and evolu- Poulin, R. 1999. The functional importance of parasites in tionary ecology. Á/ Princeton Univ. Press. animal communities: many roles at many levels? Á/ Int. J. Godfray, H. C. J., Hassell, M. P. and Holt, R. D. 1994. The Parasitol. 29: 903Á/914. population-dynamic consequences of phenological asyn- Reed, D. J. 1998. Larval competition and cannibalism in the chrony between parasitoids and their hosts. Á/ J. Anim. Indian meal moth Plodia interpunctella. Á/ School of Biol. Ecol. 63: 1Á/10. Sci., Univ. of Liverpool. Graham, I. M. and Lambin, X. 2002. The impact of weasel Reed, D. J., Begon, M. and Thompson, D. J. 1996. Differential predation on cyclic field-vole survival: the specialist predator cannibalism and population dynamics in a host-parasitoid hypothesis contradicted. Á/ J. Anim. Ecol. 71: 946Á/956. system. Á/ Oecologia 105: 189Á/193. Haeselbarth, E. 1979. Zur Parasitierung der Puppen der Sait, S. M., Begon, M. and Thompson, D. J. 1994. The effects of Forleule (Panolis flammea) [Schiff.]) und Heidelbeerspanner a sublethal baculovirus infection in the Indian meal moth, (Boarmia bistortana) [Goeze]) in bayerischen Kiefern- Plodia interpunctella. Á/ J. Anim. Ecol. 63: 541Á/550. wa¨ldern. Á/ Z. Angew. Entomol. 87: 186Á/202, 311Á/322. Sait, S. M., Andreev, R. A., Begon, M. et al. 1995. Venturia Harrell, F. 2003. Overview of the Design library. http:// canescens parasitizing Plodia interpunctella Á/ Host vulner- biostat.mc.vanderbilt.edu/s/Design/html/Overview.html ability a matter of degree. Á/ Ecol. Entomol. 20: 199Á/201. Harvey, J. A. and Vet, L. E. M. 1997. Venturia canescens Sait, S. M., Begon, M., Thompson, D. J. et al. 1997. Factors parasitizing Galleria mellonella and Anagasta kuehniella: affecting host selection in an insect host-parasitoid interac- differing suitability of two hosts with highly variable growth tion. Á/ Ecol. Entomol. 22: 225Á/230. potential. Á/ Entomol. Exp. Appl. 84: 93Á/100. Sait, S. M., Liu, W. C., Thompson, D. J. et al. 2000. Invasion Harvey, J. A., Harvey, I. F. and Thompson, D. J. 1994. Flexible sequence affects predator-prey dynamics in a multi-species larval growth allows use of a range of host sizes by a interaction. Á/ Nature 405: 448Á/450. parasitoid wasp. Á/ Ecology 75: 1420Á/1428. Salt, G. 1970. The cellular defence reactions of insects. Harvey, J. A., Harvey, I. F. and Thompson, D. J. 1995. The Á/ Cambridge Univ. Press. effect of host nutrition on growth and development of the Sisterson, M. S. and Averill, A. L. 2003. Interactions between parasitoid wasp Venturia canescens. Á/ Entomol. Exp. Appl. parasitized and unparasitized conspecifics: parasitoids mod- 75: 213Á/220. ulate competitive dynamics. Á/ Oecologia 135: 362Á/371. Huffaker, C. B. and Matsumoto, B. M. 1982. Group versus Spataro, T. and Bernstein, C. 2004. Combined effects of individual functional responses of Venturia (Nemeritis) intraspecific competition and parasitoid attacks on the canescens (Grav). Á/ Res. Popul. Ecol. 24: 250Á/269. dynamics of a host population: a stage-structured model. Jonzen, N. and Lundberg, P. 1999. Temporally structured Á/ Oikos 105: 148Á/158. density-dependence and population management. Á/ Ann. Stamp, N. E. 1981. Behavior of parasitized aposematic cater- Zool. Fenn. 36: 39Á/44. Kinuthia, W., Li, D. M., Schmidt, O. and Theopold, U. 1999. Is pillars-advantageous to the parasitoid or the host. Á/ Am. the surface of endoparasitic wasp eggs and larvae covered by Nat. 118: 715Á/725. Takahashi, F. 1973. An experimental study on the suppression a limited coagulation reaction? Á/ J. Insect Physiol. 45: 501Á/ 506. and regulation of the population of Cadra cautella (Walker) Kokko, H. 2001. Optimal and suboptimal use of compensatory (Lepidoptera; Pyralidae) by the action of a parasite wasp, responses to harvesting: timing of hunting as an example. Nemeritus canescens Gravenhorst (Hymenoptera; Ichneu- monidae). Á/ Memoirs of the college of agriculture Kyoto Á/ Wildl. Biol. 7: 141Á/150. Kraaijeveld, A. R. and Godfray, H. C. J. 1997. Tradeoff University 104: 1Á/12. between parasitoid resistance and larval competitive ability Tang, S. Y. and Chen, L. S. 2004. The effect of seasonal / in Drosophila melanogaster. Á/ Nature 389: 278Á/280. harvesting on stage-structured population models. Á J. Kusch, J., Czubatinski, L., Wegmann, S. et al. 2002. Competi- Math. Biol. 48: 357Á/374. tive advantages of Caedibacter infected paramecia. Á/ Protist Tien, N. S. H., Boyle, D., Kraaijeveld, A. R. et al. 2001. 153: 47Á/58. Competitive ability of parasitized Drosophila larvae. Á/ Evol. Lane, S. D. and Mills, N. J. 2003. Intraspecific competition and Ecol. Res. 3: 747Á/757. density dependence in an Ephestia kuehniella Á/ Venturia Tilman, D. 1982. Resource competition and community struc- canescens laboratory system. Á/ Oikos 101: 578Á/590. ture. Á/ Princetown. Mossadegh, M. S. 1980. Inter- and Intra-specific effects of the van Nouhuys, S. and Lei, G. C. 2004. Parasitoid-host metapo- mandibular gland secretion of larvae of the Indian-meal pulation dynamics: the causes and consequences of pheno- moth, Plodia interpunctella. Á/ Physiol. Entomol. 5: 165Á/ logical asynchrony. Á/ J. Anim. Ecol. 73: 526Á/535. 173. Wearing, H. J., Sait, S. M., Cameron, T. C. et al. 2004a. Stage Mudd, A. and Corbet, S. A. 1973. Mandibular gland secretion structured competition and the cyclic dynamics of hostÁ/ of larvae of the stored product pests Anagasta kuehiniella, parasitoid populations. Á/ J. Anim. Ecol. 73: 706Á/722. Ephestia cautella, Plodia interpunctella and Ephestia elute- Wearing, H. J., Sait, S. M., Cameron, T. C. et al. 2004b. The lla. Á/ Entomol. Exp. Appl. 16: 291Á/293. dynamical consequences of developmental variability and Mu¨nster-Swensden, M. and Nachman, G. 1978. Asynchrony in demographic stochasticity for hostÁ/parasitoid interactions. insect hostÁ/parasite interaction and its effect on stability, Á/ Am. Nat. 164: 543Á/558.

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