Appl. Entomol. Zool. 40 (2): 309–316 (2005) http://odokon.ac.affrc.go.jp/

Comparing and contrasting life history and development strategies in the pupal hyperparasitoids Lysibia nana and agilis (: )

Jeffrey A. HARVEY* and Leontien M. A. WITJES Netherlands Institute of Ecology (NIOO-KNAW), Department of Multitrophic Interactions, Centre for Terrestrial Ecology; Boterhoeksestraat 48, 6666 ZG Heteren, The Netherlands (Received 12 November 2004; Accepted 3 February 2005)

Abstract Since the concept of the ‘niche’ was proposed by Hutchinson almost 50 years ago, many researchers have investigated factors that enable species within ‘guilds’ (i.e., species that exploit a common resource and are likely to compete with one another) to co-exist and to persist. Here, development, host utilization, and life-history characteristics are com- pared in two species of solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis, attacking pre-pupae of their primary parasitoid host, . More than 80% of the host cocoons presented to L. nana successfully pro- duced adult hyperparasitoids compared with only about 20% for G. agilis. Adult hyperparasitoid body mass increased with host mass, but there was little difference in the mean overall body mass of either species. However, egg-to-adult development time for L. nana was significantly less than that for G. agilis. When provided with unlimited food (honey solution), G. agilis had a lifespan that was almost twice that of L. nana. However, dissections of the ovaries of adult wasps at death revealed that L. nana usually had accumulated more than 20 mature eggs, whereas G. agilis was effec- tively sterile. We suggest that several eco-physiological factors, as well as differing degrees of specialization amongst the guild of secondary hyperparasitoids attacking C. glomerata cocoons, enable them to successfully co-exist in nature.

Key words: Competition; Cotesia glomerata; guild; hyperparasitoid; niche

experienced by hosts that feed in exposed or con- INTRODUCTION cealed locations, resulting in trade-offs between fit- Life-history strategies in parasitoids are often ness functions such as development time and adult based on a long period of co-evolution between the size (Harvey and Strand, 2002). Furthermore, vari- parasitoid and its host(s). Compared with most ations in the abundance and mortality risks of dif- predators, which attack many different ferent host stages are reflected in the form and kinds of prey, interactions between parasitoids and structure of adult female parasitoid morphology their hosts are usually highly intimate (van Alphen and reproductive biology in ways that optimize and Visser, 1990; Godfray, 1994). For this reason, fecundity and survival (Price, 1972). parasitoids exhibit a suite of developmental, physi- However, there are bound to be exceptions to ological, and morphological traits that are often these examples because such ‘laws’ in nature, even strongly correlated with the eco-physiological between species exploiting a common resource, are characteristics of their hosts (Price, 1972; Vinson rarely absolute. Amongst parasitoid complexes and Iwantsch, 1980; Jervis and Kidd, 1986; God- within defined ‘guilds’ [i.e., groups of species that fray, 1994; Strand and Pech, 1995; Quicke, 1997; exploit the same host stage and are thus liable to Harvey and Strand, 2002). For example, develop- compete with one another (Root, 1967)], there may mental strategies of many koinobiont parasitoids be considerable variation in the expression of cer- (i.e., parasitoids that attack hosts that continue tain traits. For instance, Price (1970, 1972) found feeding and growing after parasitism) appear to be that six species of idiobiont parasitoids (i.e., para- adaptive responses to differential mortality risks sitoids that attack non-growing or paralyzed hosts)

*E-mail: [email protected] DOI: 10.1303/aez.2005.309

309 310 J. A. HARVEY and L. M. A. WITJES successfully co-exist on cocoons of the Jack Pine (Hymenoptera: Ichneumonidae) is an asexually Sawfly (Neodiprion swaineii) in the boreal forests reproducing facultative hyperparasitoid that is also of eastern Canada. He attributed the ability of these potentially a primary parasitoid of many other parasitoids to co-exist on several possible factors, hosts in nature. In addition to parasitoid cocoons, including inter-specific differences in the oviposi- Gelis species are known to parasitize such evolu- tor length of female parasitoids and on subtle tionarily divergent hosts as moth pupae and even forms of niche partitioning based on differing spider egg sacs (Bezant, 1956; Schwarz and Bori- responses (and preferences) of the parasitoids to a ani, 1994; van Baarlen et al., 1996). range of microclimatic conditions occupied by the The main aims of this study are (a) to determine host. if the specialist hyperparasitoid exploits host Another important factor that enables parasitoids resources differently and more effectively (in terms within guilds to persist over time, but which is of fitness correlates) than the generalist hyperpara- often overlooked or under-emphasized, is the de- sitoid, and (b) to compare life-history and morpho- gree of host specialization they exhibit. Many para- logical characteristics of the two species to see if sitoids, and in particular idiobionts, possess broad they differ in ways that enable them to co-exist host ranges, and will readily attack other suitable under natural conditions by further reducing com- hosts that are available (Godfray, 1994; Mayhew petition. Lastly, we discuss the role of other envi- and Blackburn, 1999). The studies by Price (1970, ronmental and biological factors that may influence 1972) also reported that all but one of the six the local distribution of secondary hyperparasitoids cocoon parasitoids of N. swaineii are facultative of C. glomerata in the field. hyperparasitoids; this suggests that all were also generalists. The ability to attack other hosts within MATERIALS AND METHODS a habitat acts to diffuse competition by enabling the parasitoids to reduce niche overlap (Hutchin- . Hosts and parasitoids were reared at son, 1959). On the other hand, parasitoids that are 252°C under a 16L : 8D regime. Cultures of C. specialized (i.e., attack one or only a few host glomerata and P. brassicae were obtained from in- species in nature) probably exhibit phenotypic sects maintained for many years at Wageningen traits that more closely reflect strong co-evolution University (WUR), The Netherlands, and which with the preferred host than is the case for general- were originally collected from agricultural fields in ists that might attack many other unrelated hosts in the vicinity of WUR. All P. brassicae larvae used nature. Thus, we might expect more specialized in these experiments had been maintained on Bras- parasitoids to be (a) better competitors for their sica oleracea var. Cyrus (i.e., brussel sprouts) at preferred hosts than generalists, and (b) to exploit a WUR. given amount of host resources more effectively in In these experiments, P. brassicae larvae were terms of survival, adult size, and development maintained on Sinapis arvensis plants that origi- time. nated from the seeds of plants growing along a This study compares and contrasts development road near the Institute of Ecology at Driel, The and life-history characteristics in two species of Netherlands. It was decided to use S. arvensis as all solitary, secondary idiobiont hyperparasitoids that of the species in this study are known to be directly attack fully cocooned pre-pupae of the same pri- or indirectly associated with it under natural condi- mary parasitoid host. Cotesia glomerata L. (Hy- tions (Harvey, personal observations). Moreover, menoptera: ) is a gregarious koinobiont S. arvensis is a wild crucifer that has not been arti- primary parasitoid that attacks young larvae of ficially selected via domestication and, like its white butterflies, including the large cabbage but- close relatives including Brassica nigra, it contains terfly Pieris brassicae L. (Lepidoptera: Pieridae). higher levels of secondary plant compounds (glu- Lysibia nana Gravenorst (Hymenoptera: Ichneu- cosinolates) than cultivated species such as B. oler- monidae) is an sexually reproducing obligate hy- acea (Harvey et al., 2004; Harvey et al., unpub- perparasitoid that only attacks closely related pri- lished). mary hosts in the braconid subfamily Microgastri- Cotesia glomerata were reared according to the nae, including C. glomerata. Gelis agilis Fabricius protocol described by Harvey (2000). Adult female Comparing Hyperparasitoid Development 311 wasps oviposit 10–40 eggs into the first (L1) to larvae to parasitoids at the end of a brush in plastic third (L3) instars of P. brassicae. During their de- vials. Parasitism was verified by allowing wasps to velopment, parasitoid larvae feed primarily on host sting hosts for at least 5 s, which represents the ap- hemolymph and egress from the host caterpillar late proximate threshold between host acceptance and during its final instar. After egression, wasp larvae rejection in this species (Harvey, 2000). Parasitized immediately spin cocoons on the host plant adja- caterpillars were immediately placed in large rear- cent to the host, which perishes within a few days. ing cages (1 m60 cm60 cm) containing four S. Lysibia nana was originally obtained from co- arvensis plants. These were refreshed every 3 d, or coons of C. glomerata recovered from the leaves of earlier if required. B. oleracea growing in a garden plot adjacent to Whether they are parasitized or not, mature (L5) the Institute of Ecology, Heteren, The Netherlands. larvae of P. brassicae begin to initiate metamor- Although it is a little studied species, L. nana has phosis 24–48 h before pupation or larval parasitoid been successfully reared from the pupae of C. egression. The larvae were collected from the glomerata, C. marginiventris, C. congregata and plants in rearing cages and placed individually into Microplitis tristis in the laboratory (Harvey, unpub- Petri dishes (10-cm dia.) with excised leaves of lished observations). S. arvensis. Upon parasitoid egression, separate Gelis agilis was also originally obtained from broods of C. glomerata cocoons were collected, cocoons of C. glomerata placed into the field adja- and separated carefully using a pair of forceps and cent to the institute. Little is known about its biol- a caecum. Cocoons of C. glomerata within broods ogy and ecology (see van Nouhuys and Hanski, were then numbered and weighed individually on a 2000). Like many ectoparasitic idiobionts, adult fe- Mettler-Toledo MT5 Electrobalance with an accu- males of L. nana and G. agilis perforate the host racy of 1 mg. The numbered cocoons were then cocoon with their ovipositor and inject perma- placed in two rows of five in labelled Petri dishes nently paralysing venom into the pre-pupa or pupa. (for L. nana) or a single row of seven (for G. Following envenomation, the wasp lays a single agilis) and attached to the plate surface using a tiny egg on the moribund host. After the parasitoid egg drop of honey. A single adult female hyperpara- hatches, the larva perforates the host cuticle with sitoid was then given access to each group of co- its mandibles and imbibes the hemolymph. How- coons (10 for L. nana or 7 for G. agilis) for 24 h. ever, as it grows it begins attacking other tissues Preliminary experiments revealed that G. agilis sig- indiscriminately and eventually consumes the nificantly parasitized fewer cocoons over 24 h than entire host, pupating within the cocoon of C. glom- L. nana, explaining the difference in cocoon access erata. In culture, L. nana and G. agilis were main- for each species. To prevent pseudo-replication, tained exclusively on 1–2 day-old pupae of C. each of the data points for host mass, development glomerata. Male and female parasitoids were kept time, and adult hyperparasitoid mass are based on in large (20-cm dia.) Petri dishes at 10°C (e.g., a means obtained on these parameters for each hy- temperature that greatly extends their longevity). perparasitoid female. In order to generate cultures of L. nana, After 24 h, hyperparasitoids were returned to the 200–300 C. glomerata cocoons were periodically culture and the cocoons were placed individually placed in rearing cages with approximately 50 in labelled plastic vials. Upon eclosion, newly wasps at 25°C for 24 h. Following parasitism, co- emerged adults of L. nana and G. agilis were nar- coons of C. glomerata were placed in large Petri cotized using CO2 and weighed on the Mettler mi- dishes until parasitoid emergence. The protocol for crobalance. In the case of L. nana, offspring sex G. agilis was similar, except that the hyperpara- was also determined. The fate of parasitized co- sitoids were allowed to host-feed on a small num- coons was measured by recording the following ber (50) of C. glomerata pupae for 24 h for 3–4 d over the course of the experiment: (1) Emerged prior to being presented with other cocoons for adult hyperparasitoid, (2) emerged adult C. glomer- oviposition. ata, and (3) dead host (i.e., in which neither an Experimental protocol. The larvae of P. brassi- adult hyperparasitoid nor an adult C. glomerata cae were parasitized by the females of C. glomer- emerged successfully). Egg-to-adult development ata in the first instar (L1) by presenting individual times, in days, of both hyperparasitoid species 312 J. A. HARVEY and L. M. A. WITJES were also recorded. After their wet mass was deter- mined, a total of 34 newly emerged female wasps (17 of each hyperparasitoid species) were individu- ally placed in Petri dishes (10-cm dia.) and given access to several small drops of honey. A small ball of cotton wool soaked in water was also added to ensure that the honey remained partly in solution (and accessible to the wasps, which cannot imbibe desiccated honey with their mouthparts). Honey and water were refreshed on a daily basis, and adult longevity (in days) was recorded upon death. The wasps were then dissected in 70% alcohol on a glass slide using two pairs of forceps and a cae- cum, with the number of mature (ovulated) eggs in their ovaries counted. The relationship between adult size and longevity was also determined.

RESULTS The effect of hyperparasitoid species on the fate of parasitized cocoons was highly significant (c 2136.04, p0.0001). More than 80% of the C. glomerata cocoons presented to L. nana produced adult hyperparasitoids, whereas in G. agilis only about 20% of the available cocoons were para- sitized (Fig. 1). In contrast, more cocoons pre- sented to G. agilis died without producing either a hyperparasitoid or a parasitoid as compared with L. nana. Host cocoon mass did not vary significantly with treatment (species or offspring sex in L. nana (F2,51 0.23, p 0.796)). In all cases, hyperpara-

Fig. 2. Developmental interactions between Cotesia glomerata, Lysibia nana, and Gelis agilis. (a) Mean mass (mg) of Cotesia glomerata pre-pupae parasitized by male and fe- male L. nana and female G. agilis, (b) Mean adult mass (mg), Fig. 1. Percentage fate of Cotesia glomerata pre-pupae and (c) Egg-to-adult development time (in days) of male and parasitized by Lysibia nana and Gelis agilis. Dark bar female L. nana and female G. agilis emerging from C. glomer- Emerged adult C. glomerata; Light barDead cocoon (neither ata cocoons. Line bars represent standard error of the mean. a parasitoid nor a hyperparasitoid emerged successfully); Bars with the same letter are not significantly different Hatched barSuccessfully emerged adult hyperparasitoid. (p0.05, Tukey’s HSD test). Sample sizes: L. nana male25, Sample sizes: L. nana250, G. agilis140. female14; G. agilis15. Comparing Hyperparasitoid Development 313 sitoid cocoons weighed an average of approxi- G. agilis had a lifespan that was almost twice as mately 2.90 mg (Fig. 2a). Hyperparasitoid mass long as the L. nana (64 versus 37 d; Fig. 4a). There also did not vary significantly with treatment was, however, no correlation between body size (F2,51 0.01, p 0.995). In fact, there was a striking and longevity in L. nana (F1,15 0.902, p 0.05) or similarity in the mass of male and female L. nana G. agilis (F1,14 0.10, p 0.05), although in the for- when compared to that of G. agilis. Typically, all mer species there was actually a weak trend for hyperparasitoids weighed approximately 1.10 mg smaller wasps to live longer than larger wasps. (Fig. 2b). In contrast, development time varied sig- Egg loads in the female L. nana at death were only nificantly with treatment (F2,51 31.46, p 0.0001). significantly higher than those in G. agilis There was a slight, albeit insignificant difference in (F1,32 170.11, p 0.0001); whereas, while the development time between L. nana males and fe- ovaries of all L. nana wasps contained several to males. However, development time for G. agilis many mature eggs, those of the G. agilis had none, was an average of over 30 h longer than that for L. except for one female with a single egg (Fig. 4b). nana females, and almost 48 h longer than that for L. nana males (Fig. 2c). Adult body size of the L. nana males (F1,23 185.859, p 0.0001) and females (F1,12 54.672, p0.0001), as well as of the G. agilis fe- males (F1,13 19.121, p 0.001), varied signifi- cantly with host size. Host cocoons that were heav- ier at parasitism produced larger adult hyperpara- sitoids than smaller cocoons (Fig. 3). However, the relationship was stronger for L. nana than for G. agilis, based on the higher R2 value obtained for re- gressions of the slopes in the former species. For the longevity experiment, there was no sig- nificant difference in the mean adult body masses of the female L. nana and G. agilis at eclosion (F1,32 1.48, p 0.232). However, G. agilis wasps had a significantly longer lifespan than L. nana wasps (F1,32 40.05, p 0.0001). In the laboratory,

Fig. 3. Relationship between the cocoon mass (in mg) of Cotesia glomerata and emerging adult male and female mass Fig. 4. (a) Mean longevity (in days) and (b) egg load at in Lysibia nana and female Gelis agilis. L. nana male wasps death of adult female Lysibia nana and Gelis agilis provided (open circles, dashed line): y0.379x0.007, R20.89; L. ad libitum with honey. Line bars represent standard error of nana female wasps (open triangles, dotted line): y0.464x the mean. Bars with the same letter are not singificantly differ- 0.206, R20.82; G. agilis female wasps (closed circles, solid ent (p0.05, Tukey’s HSD test). Sample sizes: L. nana17, G. line): y0.449x0.167, R20.60. Sample sizes are as in Fig. 2. agilis16. 314 J. A. HARVEY and L. M. A. WITJES

nectar). The wasps used in this study were derived DISCUSSION from individuals occurring in a mown field that The results of this investigation reveal that pat- had climbed plastic pots containing wild Brassica terns of host usage and offspring development dif- nigra plants. Once on the plants, they dispersed fer substantially between the generalist hyperpara- and attacked C. glomerata cocoons that had been sitoid, G. agilis, and the more specialized L. nana. lightly glued to the surface of single mid-level A significantly higher percentage of host cocoons leaves on each plant (see also, Stamp, 1981). In presented to L. nana were successfully parasitized contrast, L. nana is winged and actively forages for to eclosion as compared to G. agilis. In the latter hosts while in flight (personal observations). Ac- species, the vast majority of cocoons perished cording to Price (1972), the loss of wings in taxa without yielding either an adult parasitoid or hy- such as Gelis and other pupal (hyper) parasitoids is perparasitoid. Moreover, egg-to-adult development an efficiency measure, allowing the parasitoids to time in G. agilis was significantly longer than that utilize the thoracic cavity for body fat (i.e., used for both male and female L. nana. However, there for maintenance), whereas in winged species it is was a striking similarity in the body sizes of both taken up primarily by wing musculature. This may hyperparasitoid species across a wide range of host account for the longer lifespan of G. agilis, as com- sizes at parasitism. pared to L. nana. Profound differences were also recorded for Gelis agilis appeared to kill most hosts through a other life-history and reproductive characteristics process of destructive host-feeding behavior (Jervis of the two hyperparasitoids. When provided with a and Kidd, 1986), whereby the female wasp pierced constant source of adult nutrition (honey solution), the pre-pupal integument with her ovipositor and G. agilis females lived almost twice as long as L. allowed the host hemolymph to ooze from the nana females. Furthermore, dissections of the wound through the cocoon silk. The parasitoid then wasp ovaries shortly after death revealed that most fed orally on the hemolymph, which contains pro- of the L. nana had accumulated more than 20 ma- teins that are mobilized for the production of ger- ture eggs, whereas G. agilis wasps were effectively minal tissues (eggs) and sugars, such as trehalose sterile. Iwata (1960) also reported that, amongst and sucrose, that slow the metabolic use of body studied ichneumonid parasitoids, Gelis spp. often fat that is mobilized for somatic tissues (mainte- have the lowest egg loads and fewest number of nance) (Jervis and Kidd, 1986; Ellers et al., 1998; ovarioles. Ueno, 1999; Giron et al., 2002). In contrast, L. In the field, L. nana is probably quite specialised nana does not host-feed, but instead relies entirely in attacking cocoons of gregarious parasitoids like on resources obtained during larval feeding that are C. glomerata, which are aggregated in clusters carried over to the adult stage for egg production (typically 15–40 cocoons per cluster). Under labo- (Ellers and Jervis, 2003). Additional resources uti- ratory conditions, female L. nana have been ob- lized for maintenance are obtained by feeding on served to parasitise an entire cluster of C. glomer- carbohydrate sources such as nectar (Wäckers, ata cocoons in succession (Harvey et al., unpub- 2001). The high rate of host mortality in the G. ag- lished). In contrast, G. agilis is an opportunist that ilis–C. glomerata interaction was almost certainly will likely parasitise a range of suitable hosts, some due to the destructive host-feeding behavior by the of which occur singly. Thus, the potentially large adult female parasitoid (Jervis and Kidd, 1986). differences in reproductive output between L. nana Similarly, Flanders (1953) found that the encyrtid and G. agilis could be due to differing selection parasitoid Metaphycus helvolus frequently kills pressures on egg production in the two species more than 80% of its scale hosts due to destructive based on variable host encounter rates. host-feeding. There is also considerable variation in the Both hyperparasitoid species produce large, expression of behavioral and morphological traits yolky ‘anhydropic’ eggs that contain a full comple- of the two species. Gelis agilis is wingless and ment of proteins that are a pre-requisite for the exhibits ant-like behavior while foraging on the completion of oogenesis (Flanders, 1950; Jervis ground. However, it readily climbs plants in search and Kidd, 1986). Because L. nana does not host- of suitable hosts or sources of adult nutrition (e.g., feed, it is likely that the costs of initiating and sus- Comparing Hyperparasitoid Development 315 taining egg production are higher in this species trade-off based on the nature of the interaction be- than they are in G. agilis, which acquires extra tween both organisms. Because G. agilis is proba- resources for oogenesis exogenously, through host- bly able to attack many hosts in nature, it is far less feeding or predation. In addition, a number of para- dependent on finding the cocoons of C. glomerata sitoids, including both host-feeding and non-host- (or related species) than is L. nana. feeding species, are also known to ‘resorb’ egg Although considered by some workers to be out- nutrients for maintenance when deprived of suit- dated terminology, the use of ‘r’ and ‘K’ selective able hosts (Flanders, 1953; Gauthier and Monge, strategies appropriately describes the differences in 1999; Jervis et al., 2001). The lack of eggs found the selected life-history traits of L. nana and G. ag- in the ovaries of G. agilis wasps could be due to ilis (Pianka, 1970; Stearns, 1976). Species display- egg resorption, or else the wasps are ‘anautoge- ing typical ‘r’ characteristics have a high egg pro- nous’ and must host-feed to initiate oogenesis duction, a short-life span, and an efficient dispersal (Jervis and Kidd, 1986). capability, whereas ‘K’ selected species have a low Gelis agilis and L. nana exhibited remarkable fecundity, a longer life span and limited dispersal efficiency in converting host tissues into hyperpar- ability. In comparison with parasitoids occupying asitoid tissues. In L. nana, a previous study re- other guilds, in particular parasitoids attacking nu- ported that parasitoids emerging from host cocoons merous early larval stages, both hyperparasitoid of a given mass at parasitism grew up to 98% of species probably exhibit ‘K’ characteristics; how- the size of the C. glomerata adults that had been ever, when compared within the cocoon hyperpara- allowed to develop in cocoons of a comparable size sitoid guild, L. nana appears to be much more (Harvey et al., submitted). This must represent one indicative of an ‘r’ selected species than G. agilis. of the most efficient transfers of resources between It is possible that each suite of traits in both species different trophic levels in the kingdom, and is more favorable under a given set of environmen- is probably attributable to several factors. Para- tal conditions, thus enabling both species to co- sitoids exploit a highly nutritious but finite re- exist (Price, 1970). source and have been selected to optimize efficient Cotesia glomerata pre-pupae and pupae are at- use of this resource. Moreover, since parasitoid lar- tacked by at least five species of secondary hyper- vae are effectively sessile, the costs of metabolic parasitoids in western Europe (unpublished obser- activity are greatly reduced as compared to actively vations). So far, we have recovered three solitary foraging predators (Slansky, 1986). It is also now ichneumonids (L. nana, G. agilis and Acrolyta known that parasitoid venoms, besides having a nens) and two gregarious pteromalids (Baryscapus paralytic effect on the host, may also increase the galactopus, and one unidentified species) from the accessibility and even quality of host resources cocoons of C. glomerata in the field. Interestingly, as food for parasitoid progeny (Nakamatsu and there appears to be some evidence of niche differ- Tanaka, 2003, 2004). Finally, most secondary hy- entiation amongst these hyperparasitoids that is perparasitoids do not construct their own cocoons, based on the structure of the surrounding plant but instead pupate within a cocoon that has been community on which P. brassicae and C. glomerata prepared by their host. Although the cost of silk interact, as well as on the secondary chemistry of production in parasitoids has not, as far as we the plant in determining the presence or absence of know, been quantified, it is likely to be high be- a given hyperparasitoid species in the community cause silk contains a number of proteins that might (Harvey et al., 2003, 2004). Further experiments be used in other metabolic functions. that are currently underway in both areas will A similarity in body size, coupled with differ- hopefully enhance our understanding of the various ences in development time between the two hyper- eco-physiological factors that enable guilds con- parasitoids, suggests that the former parameter is taining many species to co-exist and persist. more important for fitness in both species (see also a discussion by Harvey and Strand, 2002). Alterna- ACKNOWLEDGEMENTS tively, it could reflect either differences in the The authors wish to thank Leo Koopman and André Gid- degree of specialization (and hence adaptation) to ding of Wageningen University for a constant supply of herbi- the host (C. glomerata) or reveal a secondary vores and parasitoids, and Wim van der Putten, Rieta Gols, 316 J. A. HARVEY and L. M. A. WITJES and Roxina Soler for their comments on an earlier draft of the Mayhew, P. J. and T. M. 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