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King Saud University Saudi Journal of Biological Sciences

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ORIGINAL ARTICLE Superparasitism in glomerata does not benefit the host plant by reduction of herbivory caused by brassicae

Fazil Hasan *, M. Shafiq Ansari

Department of Plant Protection, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh 202002, India

Received 4 October 2010; revised 25 October 2010; accepted 6 November 2010 Available online 16 November 2010

KEYWORDS Abstract Superparasitism occurs in L. (: ), a gregarious Cotesia glomerata; endoparasitoid of Pieris spp. (Lepidoptera: Pieridae). The responses of L. larvae to Pieris brassicae; superparasitism were examined in order to elucidate the ecological significance of this behaviour. Superparasitism; Models of tritrophic interactions often imply that attraction of herbivore natural enemies by the plant Food consumption; constitutes a defence. attack on herbivores is assumed to result in a reduction in herbivory Plant fitness survivorship; and or an increase in plant fitness. Coupled with the active involvement of the plant in producing sig- Oviposition; nals, this can be seen as an indirect mediation of wound induced defence. The results show that super- Larval growth parasitism of P. brassicae by the parasitoid C. glomerata reduced survivorship but increased food consumption and weight growth in P. brassicae larvae. The duration of host larval development was found prolonged as the number of oviposition increased and superparasitized larvae (three to five time parasitized) grew slower than unparasitized larvae or larvae parasitized one or two times. ª 2010 King Saud University. Production and hosting by Elsevier B.V. All rights reserved.

1. Introduction cific females results in superparasitism (Gu et al., 2003; Dorn and Beckage, 2007; Hasan and Ansari, 2010a,b). Superparasit- The deposition of a clutch of eggs (or a single egg) by a female ism can have consequences on offspring fitness by causing or parasitoid in a host already parasitized by itself or by conspe- enhancing intraspecific competition of within a host (van Alphen and Visser, 1990). Many parasitoids are at- * Corresponding author. Tel.: +91 9259167918. tracted most by plants currently under herbivore attack. E-mail address: [email protected] (F. Hasan). This response is mediated by volatiles produced by the action of the host feeding on the plant (Dicke and Sabelis, 1989). 1319-562X ª 2010 King Saud University. Production and hosting by Many studies of plant–herbivore–parasitoid systems have as- Elsevier B.V. All rights reserved. sumed that the attraction of the parasitoid and the increase in parasitism rates benefit the plant, either in terms of in- Peer review under responsibility of King Saud University. doi:10.1016/j.sjbs.2010.11.002 creased fitness or of a reduction in herbivore damage. Forag- ing parasitoids face a dilemma, termed the ‘reliability/ detectability’ problem by Vet et al. (1991) in that host stimuli Production and hosting by Elsevier are the hardest to detect but the most reliable; the opposite being true for plant volatiles. Parasitoids have possible 66 F. Hasan, M.S. Ansari strategies to circumvent this dilemma. The most successfully by C. glomerata may contain brood sizes up to 62 individuals and commonly utilized cues are chemicals produced by the (Gu et al., 2003). Superparasitized P. brassicae hosts that re- plant only in response to insect attack (Vet et al., 1991; Vet ceived up to five ovipostion bouts provide further insights into and Dicke, 1992). Early interpretations of how induced re- the tritrophic dynamics (Gu et al., 2003). Other studies suggest sponses could benefit plants indirectly emphasized the possibil- that female wasps of C. glomerata are able to distinguish be- ity that prolonged herbivore development could increase tween unparasitized and parasitized hosts, probably by detec- exposure to natural enemies (Price et al., 1980; Schultz, tion of internal cues during ovipositor insertion (le Masurier, 1983). Although this seems likely, few studies have actually 1990; Bauer et al., 1998; Fatouros et al., 2005). On the other documented such impacts (Bergelson and Lawton, 1988; hand, multiple attacks on the same host larva by C. glomerata Haggstrom and Larsson, 1995; Benrey and Denno, 1997; Ben- have been observed in laboratory studies (Ikawa and Okabe, rey, 1997). Moreover, other studies have emphasized the 1984, 1985), and superparasitism is known to occur in the field attractiveness of induced plant allelochemicals to parasitoids (van Driesche, 1988). and predators (Vet and Dicke, 1992; Agrawal, 1999). Host This work seeks to clarify whether parasitism of P. brassi- habitat location by parasitoids is greatly enhanced by info- cae by C. glomerata reduces leaf consumption at different in- chemicals released by plants following herbivore feeding (Tur- stars of the herbivore. Any reduction of herbivory may be lings et al., 1991; Dicke et al., 1993; Rose et al., 1998). The seen as a plant benefit. Leaf consumption may also be influ- composition and timing of these volatile emissions suggest enced by herbivore growth rate, so data were collected on an active role in plant defence and a coevolutionary relation- the growth of parasitized and unparasitized larvae. ship between plants and parasitoids (Mattiacci et al., 1994; Turlings et al., 1995; Pere and Tumlinson, 1997; Vinson, 1998). It is possible that the involvement of the third trophic 2. Materials and methods level in plant–herbivore interactions is an evolved response by the plant. This is a suggestion put forward by many authors 2.1. Experimental (Dicke and Sabelis, 1989; Godfray, 1994; Turlings et al., 1995) hence the term ‘synonome’, an infochemical (Dicke and Sabel- The parasitoids collected from the field population in 2009 is, 1988) of mutual benefit to the plant and to the natural en- were used to establish a laboratory colony. Ten pairs of newly emy. Such use of the third trophic level to defend plant tissues emergent wasps were introduced into an insect cage may be called the ‘bodyguard hypothesis’ (Dicke and Sabelis, (35 · 35 · 35 cm) and fed with water and honey. After 3 days, 1989). However, the summoning of a parasitoid cannot be as- 30 second-instar P. brassicae larvae feeding on a cabbage plant sumed always to be beneficial to the plant (Price et al., 1980); Brassica oleracea var. capitata were placed in the cage. Follow- advantages must be demonstrated in terms of a reduction in ing 24-h exposure to parasitoids, host larvae were removed and herbivory or a fitness benefit. reared in a new cage. This process of parasitism was repeated Pieris brassicae L. is a serious pest of cruciferous crops the following day. Cultures were maintained in an insectary at (Hasan and Ansari, 2010b), particularly cabbage and related 25 ± 1 C, 60% RH, under an LD 16:8 h photoperiod. Para- varieties throughout India and North-West Europe (Fetwell, sitoid cocoon clusters were collected 3 days after pupation. 1982). Its major enemy in the field is Cotesia glomerata L. On emergence, male and female wasps were reared together (Fetwell, 1982), a gregarious koinobiont endoparasitoid. This and fed on 10% honey soaked in cotton swab. The same envi- lays its eggs in the first/second instar of its host, and the para- ronmental conditions were used in the following experiments sitoid larvae egress from the host halfway through its fifth in- unless stated otherwise. star (Laing and Levin, 1982). Host larvae parasitized by koinobiont species continue to grow and develop, but larval 2.2. Effect of superparasitism on the duration of host larval endoparasitoids can alter the growth and development of their development hosts to meet their own nutritional requirements (Gauld, 1988). Some studies have indicated that parasitism by C. glom- 2.2.1. Laboratory manipulated experiments erata can induce physiological alterations in the host (Gu et al., 2003). In response to parasitism by gregarious par- Duration of larval development in respect to different numbers asitoids, many host species consume more food due to en- of ovipositions was noticed. Parasitism was manipulated to ob- hanced digestibility (Parker and Pinnell, 1973; Sato et al., tain one, two, three, four, and five successive ovipositions on a 1986; Schopf and Steinberger, 1997; Nakamatsu et al., 2001) host larva (Gu et al., 2003). The following procedure was used and grew faster than unparasitized larvae (Rahman, 1970; to parasitize hosts. One first and second-instar P. brassicae lar- Slansky, 1978; Coleman et al., 1999), although their general va was placed on a piece of previously host-infested cabbage efficacy of energy utilization does not change (Gu et al., leaf, which was then introduced into a glass tube (4 · 2 cm) 2003) but such effects depend on the number of parasitoids that held a 3-day-old female wasp. For single oviposition, present (Harvey, 2000). This regulation of food intake and lar- the larva was removed from the tube immediately after com- val growth by the host to stabilize food supply for the develop- pletion of the first oviposition. In the case of superparasitism, ing parasitoid larvae appears to be fine-tuned to the host the same parasitized host larva was exposed to a new wasp species involved (Alleyne and Beckage, 1997; Harvey, 2000). each time until the required number of ovipositions was Further studies have demonstrated that the effect of parasitism obtained. on the growth and development of hosts depends on the num- Twenty-five first instars larvae (for each experiment) with dif- ber of ovipositions in a host body (Cloutier and Mackauer, ferent numbers of ovipositions (parasitized) and unparasitized 1980; Alleyne and Beckage, 1997; Harvey, 2000; Gu et al., (control) larvae were kept singly in 25 Petri plates of 10 cm diam- 2003 ). P. brassicae parasitized by a single oviposition bout eter, and each Petri plate was designated as replicate. The data Superparasitism in Cotesia glomerata does not benefit the host plant by reduction of herbivory 67 obtained in this experiment were subjected to non-parametric 3. Results Kruskal–Wallis one way analysis of variance. 3.1. Effect of superparasitism on the duration of host larval 2.2.2. Field collected parasitized larval development development Fifty parasitized larvae of P. brassicae were collected randomly from the field of cabbage. These larvae were purely unknown 3.1.1. Laboratory manipulated experiments from how many number of times they were parasitized. These There was a significant difference in the duration of instars be- larvae were kept separately in 50 Petri plates of 10 cm diameter tween larvae parasitized one time, two times, three times, four in the same environmental condition as mentioned above. times and five times (K = 118.51, d.f. =5,P < 0.001). As the Comparisons were made between parasitized and unparasit- number of ovipositions increased, larvae spending more time ized larval duration on the basis of Student’s t-test. in all instars and they grew slow (Fig. 1). Larvae with multiple These larvae were reared until the egression of parasitoid’s ovipositions spend more time in fifth instar since it was at this cocoon (from parasitized larvae) or the formation of host pupa stage that the parasitoid larvae egresses from the host (Fig. 1). (of unparasitized larvae or control) to determine the duration The total mean time of larvae parasitized five times was of whole development. 22.32 days with a median of 23 days. When comparing with control the mean time was 13.56 days with a median of 2.3. Effect of superparasitism on the food consumption and 13 days. growth of host larvae 3.1.2. Field collected parasitized larval development This experiment also involved five different numbers of oviposi- There is a significant difference between parasitized and unpar- tion on a host, with 30 individual host larvae for each number of asitized larval development (t = 35.25, d.f. = 99, P < 0.001). ovipositions. The same procedure of parasitism as used in the Field collected parasitized larvae took more time of above experiment was employed. The parasitized host larvae 23.50 days, and after this period the egression of parasitoids were reared singly in plastic boxes (19 · 9 · 8 cm) and fed with cabbage leaves removed from B. oleracea L. var. capitata plants bearing eight leaves. The cabbage plants were grown in a green- house at 16–26 C and LD 16:8 h photoperiod with a light illu- mination of 50,000 lux. At intervals of initially 3 days then 2 days, the host larvae were given fresh cabbage leaves while the remaining leaf parts were removed. For determination of the leaf area consumed by a host larva, each fresh leaf and the remaining part were photocopied onto transparencies. Leaf area was measured using a leaf area meter based on light transmission detection. To estimate the factor of leaf shrinkage following re- moval from plants, during each feeding period four fresh leaves were photocopied and kept under the same environmental condi- tions as the leaves that were used to feed host larvae. After 2 days, these leaves were photocopied again. A shrinkage factor was determined and used to correct calculations of leaf area consumed during a given feeding period. Meanwhile, five 1-cm2 leaf discs were weighed to determine their fresh weight, and the mean value Figure 1 Mean duration of instar of P. brassicae larvae related was used to convert leaf area into weight. Larval growth was mea- to different numbers of ovipositions by C. glomerata (X1v to sured by weighing live host larvae on an electronic balance. X5v = first oviposition to five ovipositions). To estimate the efficiency of food utilization by P. brassicae larvae subjected to different numbers of oviposition, three Waldbauer indices (Waldbauer, 1968) were calculated: The consumption index (CI) = F/[(BA)T], where F = fresh weight of food consumed, BA = arithmetic mean of fresh body weight during a feeding period [BA = (Bfinal + Bstart)/2], and T = the feeding period in days. The relative growth rate (GR) = G/ [(BA)T], where G = fresh weight gain of the larva during a feeding period. The efficiency of conversion of ingested food to body mass = (dry weight gained/dry weight of food ingested) · 100. The dry weight of both cabbage leaves and host larvae was estimated by drying samples in an oven (50 C) to a constant weight. The food consumption and body weight of hosts in rela- tion to days after parasitisation were analyzed using a general linear model with repeated measures using the language pro- gram R Development Core Team R2.10.1 unless stated other- wise. A Kruskal–Wallis test was applied to determine the Figure 2 Mean duration of field collected parasitized and significance of differences in each of the three Waldbauer indices. unparasitized larvae of P. brassicae. 68 F. Hasan, M.S. Ansari started (Fig. 2). However, unparasitized larvae grow faster significant (a general linear model with repeated measures, than parasitized ones and the rate of development was re- F = 11.67, d.f. = 5, 115, P < 0.001). The effect of superpara- corded as 13.38 days. After the completion of this mean period sitism on the increase of body weight in hosts was also signif- pupation of unparasitized larvae takes place. icant (F = 10.56, d.f. = 4, 15, P < 0.001). The data showed clearly that the body weight achieved before parasitoid egres- 3.2. Effects of superparasitism on the food consumption and sion in the host larvae subjected to multiple ovipositions was growth of host larvae significantly greater compared with those parasitized once (P < 0.001). After 22 days of development under the given experimental conditions, the first parasitoid larvae egressed. Food consump- 4. Discussion tion increased exponentially with the host larval age during the first 14–16 days after parasitization, then decreased (Fig. 3A). This study demonstrated the occurrence of superparasitism in The age-related differences in food consumption were signifi- C. glomerata through both field surveys of a natural popula- cant (a general linear model with repeated measures, F = tion and manipulative experiments on a laboratory popula- 18.97, d.f. = 5, 115, P < 0.001). The food consumption of tion, though this behaviour had been known from previous parasitized hosts also varied significantly with the number of anecdotal evidence (van Driesche, 1988; Tagawa, 1992, ovipositions on them (F = 16.85, d.f. = 4, 15, P < 0.001). 2000). The behavioural, functional response of host larvae to On the other hand, neither the consumption index, which indi- superparasitism might have a net beneficial effect on parasitoid cates the rate of intake relative to body weight during a given nutrition, thereby alleviating the negative effect of competition feeding period, nor the relative growth rate or the efficiency of in the host to some extent. Apparently, superparasitism altered conversion of ingested food to body mass changed significantly food consumption of host larvae. The consumed amount of with the number of ovipositions by parasitoids (Table 1). The cabbage leaves and weight growth during the development of body weight of parasitized host larvae increased with age, and superparasitized P. brassicae larvae were greater and faster also varied with the number of ovipositions on them (Fig. 3B). in comparison with singly parasitized hosts, although their The age-related changes in the body weight of host larvae were general efficiency of energy utilization did not change (Gu

Figure 3 (A) Food consumption and (B) growth in body weight of P. brassicae larvae subjected to different numbers of ovipositions by C. glomerata under laboratory conditions. Superparasitism in Cotesia glomerata does not benefit the host plant by reduction of herbivory 69

Table 1 Waldbauer’s indices of P. brassicae larvae subjected to different numbers of ovipositions by C. glomerata. Mean values (±SD) are presented for consumption index (CI: g consumed gÀ1 body weight dayÀ1), relative growth rate (GR: g gained gÀ1 body weight dayÀ1), and the efficiency of conversion of ingested food to body mass (ECI: g dry weight gained gÀ1 dry food consumed · 100). Index Control Number of ovipositions Kruskal–Wallis test 12345HP CI 1.157 ± 0.010 1.157 ± 0.005 1.083 ± 0.005 1.063 ± 0.003 0.947 ± 0.043 1.30 ± 0.06 10.53 0.06 GR 1.432 ± 0.006 1.137 ± 0.002 0.142 ± 0.005 0.146 ± 0.009 0.146 ± 0.001 0.144 ± 0.003 8.958 0.11 ECI (%) 25.66 ± 2.08 26.66 ± 2.08 28.68 ± 1.52 26.00 ± 1.00 27.66 ± 2.51 25 ± 1.00 6.799 0.23

et al., 2003)(Table 1), as in the tobacco hornworm Manduca to the plant in terms of reduction of herbivory, instead of this, sexta parasitized by (Alleyne and Beckage, the system shows a later increase in rates of leaf consumption. 1997). Moreover, the final weight gained by the parasitized Four possible hypotheses are suggested; these have implica- host larvae was correlated with the number of parasitoid lar- tions for successful pest control on cabbage by natural vae present in the host body (Harvey, 2000). enemies. The results of the leaf consumption analysis would tend to Firstly the plant used is an agricultural cultivar, having negate the assumption that in cabbage, parasitism of P. brass- been selected for market characteristics, possibly altering other icae by C. glomerata is an aspect of the defensive ecology of the aspects of its biology, including any defensive attributes of the plant (Steinberg et al., 1993; Mattiacci et al., 1994, 1995). plant. The response of the system has almost certainly evolved Parasitism did not reduce the final weight of P. brassicae feed- under different conditions and so cannot be considered typical ing on cabbage; in fact their weight was significantly higher of the current situation (Noldus, 1989). Data from similar than unparasitized larvae during the latter half of their devel- experiments on the wild strain of B. oleracea would help to opment. The greater maximal weight and rate of growth of the clarify this, but if correct it may clarify how selective breeding parasitized larvae can be ascribed to the number of parasitoid may inadvertently increase the plants’ susceptibility to pests. larvae present in their tissues, a situation also shown by Secondly, that this system is truly tritrophic; in an arms-race Karowe and Schoonhoven (1992). The presence of endoparasi- (Ehrlich and Raven, 1964) context, the system has arrived at toids could lead to greater leaf consumption rate because of a point where the plant is losing. In a natural system, given the greater nutritional demands of the high numbers of para- a longer period of time another process may restore the bal- sitoid larvae extracting nutrients from haemolymph (Parker ance; this is unlikely to happen in a crop plant. A third possi- and Pinnell, 1973). The elevated growth of larvae parasitized bility is that the plant is operating a long-term strategy. Wild by C. glomerata may be due to greater energy and nitrogen B. oleracea is a biennial plant (Mitchell and Richards, 1979), consumption by the host–parasitoid complex (Junnikala, so by attracting parasitoids to the site of feeding herbivores, 1966; Slansky and Feeny, 1977; Slansky, 1978). It is probable the plant may locally reduce the population of herbivores in that hosts which successfully encapsulate their parasitoid subsequent herbivore generations, thus reducing the possibility attackers have growth rates and hence leaf consumption rates of attack in the next growing season. The final hypothesis, are broadly similar to those of control larvae, since their nitro- which may be considered the null hypothesis, is that there is gen and energy requirements will be similar. Encapsulation oc- no active plant involvement. The parasitoid has adapted to uti- curs very early on in the development of the host larvae (Laing lize an effective signal released as a by-product of its host’s and Levin, 1982). If attraction of parasitoids is to be defensive feeding. If this is the case, then the paradox described above to the plant there must be a reduction in consumption, but disappears. Elevated growth rates by parasitized larvae may there is no evidence of reduced consumption by parasitized lar- have nothing to do with the plant. Instead this could be an vae on the plant. The rate of leaf consumption is in fact higher, evolutionary strategy by the parasitoid to reduce hyperparasit- although there is no significant difference in total area con- ism (Godfray, 1994, 1995) if true this emphasizes that results sumed over the duration of the experiment. The results of this suggesting attraction of parasitoids to plant volatiles must be work confirm previous results of studies in and interpreted cautiously when considering their application. P. brassicae (Rahman, 1970; Parker and Pinnell, 1973; Gu As it is well known from the previous studies, the response et al., 2003). Parasitized larvae would be expected to consume to superparasitism by parasitoids, a number of host species more leaf material at a later stage in host development, since grew faster than unparasitized larvae (Gu et al., 2003). But the eggs of C. glomerata in P. brassicae do not start to develop in the present study the results shows that parasitized host lar- until the third instar (Fetwell, 1982; Laing and Levin, 1982). vae grew slower than unparasitized larvae. So, as far as the Parasitism of P. brassicae may be deleterious to the plant subject of duration of parasitized larval development is con- and so potentially reduces crop yields in that many crucifers cerned still there is an ambiguity and further work is required can outgrow herbivory (Chew, 1988), but if parasitism results to clarify this ambiguity. in increased consumption rates then this may not be possible. The results presented herein show that the defensive role of So here is a paradox, first noted by Price et al. (1980). C. glom- insect herbivore-induced chemicals that attract parasitoids erata is preferentially attracted to feeding by its host on the cannot be assumed, any more than that of induced chemicals plant compared with all other stimuli (Steinberg et al., 1993; which affect herbivores directly. This work also indicates that Mattiacci et al., 1994, 1995). Yet there appears to be no benefit in systems constrained by artificial selection, such as cabbage, 70 F. Hasan, M.S. Ansari natural enemies cannot always be relied on to provide efficient Godfray, H.C.J., 1995. Communication between the first and third crop protection, since the process of selection may interfere trophic levels: an analysis using signaling theory. Oikos 72, 367– with the plants’ natural mechanisms of insect resistance. 374. Gu, H., Wang, Q., Dorn, S., 2003. Superparasitism in Cotesia glomerata: response of hosts and consequences for parasitoids. Acknowledgement Ecol. Entomol. 28, 422–431. 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