In insects, tritrophic interactions between plants, herbivores and their natural enemies are among the most studied multitrophic interactions (e.g. Turlings et al ., 1990; Vet and Dicke, 1992; Vet et al ., 1995; Lewis et al ., 1997). In this food chain, the first trophic level, represented by the plant, influences the herbivore (the second trophic level) by its quality and quantity as a food-source. On the third trophic level, natural enemies limit herbivore populations by mortality. However, interactions between herbivores and their host plants and between herbivores and their natural enemies can only be understood when considered all together within a tritrophic context (Price et al ., 1980). For instance, the first trophic level (plant) can also influence the efficiency of the third trophic level (natural enemy) by providing shelter, mediating host/prey accessibility and availability, providing host/prey finding cues, influencing host/prey suitability, and providing supplemental food sources for natural enemies (Cortesero et al ., 2000). Vice-versa, natural enemies may ‘help’ the plants, using the benefits named above, thus limiting the herbivore population more than would be otherwise possible.

To further understand fluctuations in predator or parasitoid populations and the level of herbivore suppression, not only tritrophic interactions have to be examined, but also the impact of higher-level natural enemies. Predatory and parasitic insects are attacked by their own suite of predators, parasitoids and pathogens (Rosenheim, 1998), which constitute the fourth trophic level. The impact of these higher trophic levels on natural enemies of herbivores has received relatively little attention. They may exert a significant negative effect on plant-fitness by removing parasitoids or predators of the herbivores (top-down regulation) (Luck et al ., 1981). But not only top-down effects are to be expected. It has been shown recently that bottom-up forces may also play a role in mediating interactions involving plants, herbivores, parasitoids and hyperparasitoids. Harvey et al . (2003) have demonstrated that qualitative differences in herbivore diet can differently affect the performance of interacting organisms across four trophic levels.

Like parasitoids, larvae of endophagous hyperparasitoids feed inside the host, whereas ectophagous species feed externally. Koinobiont hyperparasitoid species allow their host to continue development after oviposition, and idiobionts attack non-growing or non-feeding host stages and/orarrest the development of the host by paralysis of killing during oviposition (Sullivan, 1987).

Hyperparasitism has a wide taxonomic distribution among insects. However, none of the parasitoid families consists exclusively of hyperparasitoids, although within families hyperparasitism may follow phylogenetic lines (Brodeur, 2000). This suggests that hyperparasitism has evolved independently several times in different taxa (Gordh, 1981). Obligate hyperparasitism could have evolved in at least two ways: a) via facultative hyperparasitism as an opportunistic trade-off to use herbivore or parasitoid hosts, and/or if the hyperparasitic species frequently encounters already parasitised hosts; or b) by a host shift where a primary parasitoid of one host becomes a secondary parasitoid of another species. This host transfer is facilitated if the usual primary and new secondary hosts share physiological and/or ecological attributes (Sullivan and Völkl, 1999). One of the reasons why hyperparasitism may have evolved in a multitrophic context might be in order to avoid the sequestration of plant toxins in the host. Compared to the herbivore, the primary parasitoid may be a less toxic resource, especially after voiding the meconium (Vet, pers. comm).

Theoretically, if a large fraction of a parasitoid population is attacked by hyperparasitoids, an increase in the herbivore’s equilibrium density should be expected. If that fraction becomes large, the herbivore population may escape control by the primary parasitoid entirely (Luck et al ., 1981). Mathematical models have given variable results. The majority of models predict an increase of the herbivore density (May and Hassell, 1981; Briggs, 1993). On the other hand, Beddington and Hammond (1977) predicted that in a stable host - primary parasitoid - hyperparasitoid system, hyperparasitism weakens biological control, but when the system is unstable, the presence of a hyperparasitoid may dampen the oscillations and may enable a stable three-species equilibrium to be attained. This may benefit biological control, altering the system from one in which the pest exhibits periodic outbreaks to one of continuous sub-economic densities (Luck et al ., 1981). It is not known how realistic these models are because of a lack of information on the biology and behaviour of hyperparasitoids. It is often assumed that hyperparasitoids and primary parasitoids have similar life histories and information about primary parasitoids is extrapolated to the next trophic level.

In the literature, high levels of hyperparasitism have often been reported. In an agro-ecosystem, the mortality of parasitoids due to hyperparasitism can even reach 100% (Höller et al ., 1993). It is often assumed that as hyperparasitism increases, the greater the negative impact on herbivore control by primary parasitoids. Indeed, in several studies the low level of biological control by parasitoids has been repeatedly attributed to the high level of hyperparasitism (e.g. Burton and Starks, 1977; Bourchier and Nealis, 1992). However, in other cases, hyperparasitoids had little or no influence on biological control, even when the level of hyperparasitism was high (Farrell and Stufkens, 1990; Agricola and Fischer, 1991; van den Bosch et al ., 1979; (Walker and Cameron, 1981; Wilson and Swincer, 1984; Hughes et al ., 1987 cited in Mackauer and Völkl, 1993)). These differences have been explained based on the timing of hyperparasitoid attack during the season and synchronisation between primary parasitoid and hyperparasitoid. In conclusion, these studies have produced little definitive evidence regarding the impact of hyperparasitism on the regulating capacity of parasitoids in biological control. Luck et al . (1981) emphasised that percent mortality is not necessarily a good measure of a mortality’s importance without knowing the levels of other sources of mortality, and the interactions between different sources of mortality.

Finally, experimental investigations (Burton and Starks, 1977; Shi, 1986 cited in Rosenheim, 1998) Goergen and Neuenschwander, 1992) led to the conclusion that hyperparasitoids disrupt the short-term regulation of herbivore hosts by primary parasitoids. The longer-term, multi-generation experiments needed to test the prediction that hyperparasitoids stabilise the herbivore-parasitoid interaction have not been conducted (Rosenheim, 1998).

In addition to direct mortality, hyperparasitoids may have indirect effects on parasitoid populations. Höller et al . (1993) and Mackauer and Völkl (1993) state that hyperparasitoids can also influence biological control of herbivores indirectly by modifying the behaviour of primary parasitoids. It was demonstrated that when hyperparasitoids are present, primary parasitoid females could abandon patches of their herbivore host without having exploited the resource completely, to minimise the mortality risks of their progeny (Ayal and Green, 1993; Höller et al ., 1993, 1994; Mackauer and Völkl, 1993; Weisser et al ., 1994; Petersen, 2000). However, Völkl et al . (1995) found no evidence of an effect of adult hyperparasitoids on foraging behaviour or resource exploitation patterns of primary parasitoids within an aphid colony. Finally, hyperparasitoids might influence the herbivore. Boenish et al . (1997) and van Veen et al . (2001) demonstrated that the presence of females of different species of hyperparasitoids stimulated the reproduction of the aphids Sitobion avenae and Acyrthosiphon pisum , indicating some kind of communication between herbivores and hyperparasitoids. Increased reproduction of aphids in the presence of hyperparasitoids may be advantageous as their descendants will be less likely to be parasitised, especially if parasitoid wasps currently in the vicinity respond to incoming hyperparasitoids by dispersing away (van Veen et al ., 2001)

Regardless of the impact of a hyperparasitoid on a parasitoid population, a hyperparasitoid cannot affect biological control if biological control does not exist in the first place (Luck et al ., 1981). Therefore, the impact of primary parasitoids on herbivores in the absence of hyperparasitoids should be studied first. For example, Mackauer and Völkl (1993) suggested that the degree of aphid colony exploitation primarily results from the wasp’s foraging efficiency and oviposition decisions, instead of hyperparasitism. Furthermore, aestivation, a high mortality due to other factors than hyperparasitism (e.g intra-guild predation) and dispersal can also result in low levels of primary parasitoid abundance (Höller et al ., 1993).

In summary, our knowledge of the impact of hyperparasitism on primary parasitoid populations is limited and very fragmented. I agree with the conclusion of Rosenheim (1998), that limited experimental evidence supports the idea that hyperparasitism significantly disrupts the short-term regulation of herbivorous host populations by parasitoids, but critical multi-generation studies have yet to be conducted to assess the long-term effects. Moreover, accurate knowledge of the natural history of some important groups of hyperparasitoids is a prerequisite for improving our understanding of their origin, distinctive biological attributes, and role in community structure (Brodeur, 2000). However, major gaps exist in our knowledge of the mode of development (koinobiont or idiobiont), life-table characteristics, searching behaviour and competitive ability of hyperparasitoids.

In parasitoids, development mode (koinobiont or idiobiont) has been emphasized as a major potential determinant of life histories (for a review, see Godfray, 1994; Quicke, 1997; Mayhew and Blackburn, 1999; Strand, 2000; Harvey and Strand, 2002). The dichotomous hypothesis states that natural selection operates on the life history strategies of these two categories of parasitoids to magnify their differences (Godfray, 1994). Koinobiont endoparasitoids allow their host to continue development. Therefore they are able to attack small hosts that have less efficient defenses against parasitism. Moreover, younger hosts are generally more abundant than the later stages (Price, 1974). However, many koinobionts are able to attack hosts ranging in size from a fraction of that of the ovipositing female wasp to many times her size at oviposition (Harvey and Strand, 2002). In order to obtain sufficient resources to complete development in nutritonally suboptimal (=small) hosts, koinobionts may have to greatly reduce the rate of growth, resulting in an extended development time. Furthermore, because young hosts often suffer high mortality, the balanced mortality hypothesis predicts a high fecundity (Price, 1974). This high fecundity can be achieved by reducing egg size, which is possible because eggs are laid in the host haemolymph and therefore require less yolk as sufficient proteins for oogenesis are uptaken from the host. The eggs and larvae of endoparasitoids will also need to cope with the immune system of the host and engage in subtile synchronisation with the living host, which causes many endoparasitic species to have a relatively narrow host range. Idiobiont ectoparasitoids have an oposite set of life history traits. After parasitisation the development of the host is usually stopped, meaning that idiobionts must attack more mature stages of hosts that are larger. Therefore, the development time of idiobiont parasitoids is predicted to be generally less than that shown by koinobiont . Idiobiont ectoparasitoids that develop externally on their host require large, yolky eggs which tends to reduce fecundity. Furthermore, they do not have to cope with the immune system of the host, so that many species have comparatively large host ranges. Due to the innumerbale trade-offs and relationhipss between life history parameters, the above descriptions are only an impression of how development mode is observed to influence life history, and many causal relationships between parameters remain to be studied. However, observations on the life history data of 474 parasitoid Hymenoptera support the dichotomous hypothesis (Mayhew and Blackburn, 1999).

Although the same dichotomy (idiobiont – koinobiont) is also found in hyperparasitoids, it is not known if this is correlated to the same sets of life history traits as found in primary parasitoids. Because hyperparasitism evolved from parasitism (Gordh, 1981) and based on the many similarities between primary and secondary parasitoids, I predict that:

1. Similar to primary parasitoids, the life history parameters of hyperparasitoids are determined by development mode following the predictions of the dichotomous hypothesis.

Life history parameters are also influenced by the profitability of the host, for example the nutritional quality. Most aphid hyperparasitoid species attack either a host in the living aphid before mummification or in the aphid mummy. For them, the profitability of the host may vary between different parasitoid host species. In the case of S. aphidivorus however, a female can attack both parasitoid larvae in live aphids and parasitoid (pre-)pupae in aphid mummies, two very different stages of the same host species. It is unknown if these two host stages differ in profitability for the offspring of S. aphidivorus , but females seem to have a preference for the mummy host (Kanuck and Sullivan, 1992). Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Therefore the following prediction was formulated:

2. Female S. aphidivorus have a preference for pupae of primary parasitoids within aphid mummies, because these are the most profitable hosts for offspring fitness.

Both parasitoids and hyperparasitoids have to search for hosts to reproduce. Most searching strategies involve the use of cues (for example chemical, visual or tactile cues). In parasitoids, it has been shown that females zoom in from long to short distance cues, thereby slowly confining their search area, shifting from long range cues to short range cues. Within this gradual transition, we usually observe a shift from indirect, often unreliable cues, such as plant cues, to more direct, reliable cues, such as contact chemicals directly derived from the host itself. The resulting intensified search of the restricted area where any cue is perceived enhances the chance of locating the host (Vet et al. , 2002). The use of cues varies according to the host-specificity of the parasitoid. There is a continuum from intense and specific use of cues in specialists, to the absence of cue use in extreme generalistic species (Vet and Dicke, 1992). To find their host, hyperparasitoids potentially have many cues at their disposal from all trophic levels. However, we have little insight in which cues are actually being used by hyperparasitoids. Alloxystine aphid hyperparasitoids have narrower host ranges than the Pteromalidae, Megaspilidae (Brodeur, 2000) or Encyrtidae (Hoffer and Stary, 1970). It is therefore expected that they will differ in host searching strategies:

3. The relatively host specific alloxystid hyperparasitoid species will use general cues associated with aphids and specific cues from primary parasitoid females and/or host plant volatiles associated with their plant – aphid - host system. Ecto-hyperparasitoids with a broader host range than koinobionts will depend less on specific cues, and use only general cues associated with aphids and aphid mummies on different plant – aphid – host systems. The species with the dual oviposition behaviour, S. aphidivorus , is predicted to resemble the ecto-hyperparasitoids because of its broad host range and its preference for mummies.

One of the cues that aphid hyperparasitoids may use in host searching is aphid honeydew (Budenberg, 1990; Grasswitz, 1998). The composition of honeydew can vary with various factors, among which are aphid species (Hendrix et al. , 1992; Völkl et al. , 1999; Fisher and Shingleton, 2001) and parasitism of the aphid by braconid wasps (Cloutier and Mackauer 1979, Cloutier 1986, Rahbé et al. , 2002). Therefore, honeydew could be a direct and reliable cue for hyperparasitoids if females have the capacity to discriminate between the different chemical compositions of honeydew. I predict that:

4. Foraging aphid hyperparasitoid females not only have the ability to detect honeydew but also show a preference for honeydew from aphid rather than non-aphid species and, more specifically, for honeydew from parasitised vs. unparasitised aphids.

Although life history and host searching behaviour have already been studied to some extent in a few hyperparasitoid species, much of this information is fragmented or anecdotal and most of the emphasis has been put on working out the complex biology of individual species (Hawkins, 1994). Species are difficult to compare because data on different species often originates from different herbivore-primary parasitoid systems which can vary in quality, suitability and potential cues for host location. Furthermore, hyperparasitoids show a large interspecific variation in development mode, host stage and host range. Due to these facts, no firm conclusions on life history and host location of hyperparasitoids can be drawn based on literature data.

Contrary to previous studies, I have chosen an interspecific comparative approach. Comparative evidence brings generality, suggests hypotheses and places inter-specific patterns into context (Stearns, 1992). I used four hyperparasitoid species from the principal families that contain aphid hyperparasitoids, and reared them on the same aphid-primary parasitoid system. This made it possible to directly compare the results of different species and to find general patterns of the influence of development mode, host stage and host range on life history traits and host location behaviour. I expect to find that:

5. There are differences in life history and host location behaviour between hyperparasitoid species due to differences in development mode, host stage or host range.

In addition, the results are compared to similar data on primary parasitoids. In contrast to hyperparasitoids, hymenopteran primary parasitoids have been studied extensively (e.g Godfray, 1994; Quicke, 1997). It is an intriguing question how much of the theory on primary parasitoids can be applied to hyperparasitoids. Although the degree of similarity between primary and secondary parasitoids is obvious because of their common evolutionary origins and life-history strategies, hyperparasitoids are likely to possess specific biological attributes enabling them to exploit resources from the third trophic level (Brodeur, 2000). It is therefore predicted that:

6. Hyperparasitoids have developed specific biological attributes enabling them to exploit resources from the third trophic level as compared to primary parasitoids.

Life history of aphid hyperparasitoids:

Host searching behaviour of aphid hyperparasitoids:

Chapter 3 aims to elucidate the dual oviposition behaviour of the encyrtid hyperparasitoid Syrphophagus aphidivorus . Female preference for either a parasitoid larva in the live aphid or a pupa in an aphid mummy is reinvestigated and correlated with the fitness of the offspring.

The host location behaviour in four species of aphid hyperparasitoids is studied in chapter 4. The influence of volatile and contact infochemicals from all trophic levels was tested in an olfactometer and while a female was searching on a plant, respectively. The influence of host stage, host range and mode of development are discussed and the results are compared to primary parasitoids.

In chapter 5, research is focussed on the role of one of the cues in chapter 3, honeydew, in host search of the four species of aphid hyperparasitoids. It is tested if female hyperparasitoids can distinguish between aphid and non-aphid honeydew, as only aphids may contain hosts. Furthermore it is tested if they can distinguish if honeydew comes from healthy unparasitised aphids, or from parasitised aphids hosting a suitable host. The response of the four species of hyperparasitoids is compared with respect to their respective biological attributes.

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