NORMATIVAS A NIVEL NACIONAL

Attraction and arrestment behaviour

An appreciation of the stimuli and the responses involved in food and alternative host/prey location behaviour can be important in understanding how manipulation of natural enemy immigration and retention may be achieved (Tables 5.1 and 5.2). Attractant stimuli typically operate early in the searching sequence, eliciting orientation to areas that either contain or are likely to contain the hosts/prey/food. For many species, volatile chemicals are of primary impor- tance in attraction (Shahjahan 1974; Lewis and Takasu 1990; Cortesero et al. 2000; Fellowes et al. 2004), although visual stimuli may also play an important role (Wäckers 1994). Parasitoids may, like other flower-visitors, have odour or colour preferences in relation to the range of flowering plants they exploit (for protocols, see Dafni 1992, Wäckers 1994). Arrestant stimuli typically operate later in the searching sequence, eliciting a reduction in the distance or area covered per unit time by parasitoids moving within such areas (i.e. result in reduced emigration, so contributing to retention) (Waage 1978; Fellowes et al. 2004). For many species these stimuli are chemical and are detected upon contact (Waage 1978).

Key contributions to be made by behavioural work include establishing whether, and to what degree, the resource encourages immigration into the crop. Responses to olfactory stimuli can be evaluated using olfactometers of various kinds (static-air, airflow, i.e. Y-tube, four-arm Petersson) and wind-tunnels (Dafni 1992; Kielty et al. 1996; Takasu and Lewis 1996; Ballal and Singh 1999; Jang et al. 2000; Raymond et al. 2000; Le Ru and Makaya-Makosso 2001; Fellowes et al. 2004). Wind-tunnels have the greatest potential for approximating field conditions. Where a natural enemy has been shown to locate the resource by anemotaxis, spatial arrangements of crop plantings and other resources (e.g. nectar sources, artificial honeydew) can take account of wind direction, increase the probability of colonisation and thus maximise the number of preda- tors or parasitoid immigrants.

Attraction can also be studied under field conditions, and plants ranked according to their attractiveness, but investigators might find it difficult to control various significant confounding factors (Fellowes et al. 2004).

One of the aims of spraying a crop with an artificial honeydew or other substitute food is to increase immigration and/or reduce emigration (Butler and Ritchie 1971; Hagen et al. 1971, 1976; Carlson and Chiang 1973; Ben Saad and Bishop 1976; Nichols and Neel 1977; Hagley and Simpson 1981; Liber and Niccoli 1988; Evans and Swallow 1993; McEwen et al. 1993a; Mensah

1996, 1997; Evans and Richards 1997; Jacob and Evans 1998; Stephen and Browne 2000). Olfactometry and other behavioural techniques could prove very useful in comparing and optimising the attractant effects of honeydew mixtures (van Emden and Hagen 1976; Dean and Satasook 1983; McEwen et al. 1993b; Fellowes et al. 2004).

Once it has been shown that a parasitoid or predator can respond positively to the volatiles emanating from a plant or honeydew, the technique of coupled gas chromatography-mass spectrometry/electroantennography (coupled GC-MS/EAG) can be used to identify the specific chemicals that mediate attraction in the insects (Khan et al. 1997). Once the semiochemicals in a plant or other resource (e.g. natural honeydew) have been identified, known or potential resource-providing plant species, and artificial honeydew mixtures, can be screened, using GCMS, for their relative potential as attractors of natural enemies.

While a supplemental food (or source thereof) may be shown to be attractive, additional experiments should be conducted to determine whether the efficiency of food location is not significantly impeded under field conditions, as result of interference from odours emanating from other vegetation, including the pest-bearing crop. Odours from such sources may disrupt olfactory responses to food sources (Shahjahan and Streams 1973).

Natural honeydew is an arrestant, potentially contributing to population retention, for lacewings (McEwen et al. 1993b), coccinellids (Carter and Dixon 1984; van den Meiracker et al. 1990), syrphids (Budenberg and Powell 1992) and parasitoids (Ayal 1987; Budenberg 1990), and artificial honeydews are likely to have a similar effect, via the handling-time effect of feeding and/or through an effect on searching movements. Fellowes et al. (2004) provide guidance on designing experiments that can shed light on arrestment responses to artificial and natural honeydews. When planning manipulation using artificial honeydew sprays, consideration needs to be given to the possibility that too ‘powerful’ a formulation (in terms of arrestment), or a weak spatial association between spray deposits and host/prey patches, may confound the attempted manipulation by constraining the natural enemy’s searching efficiency.

Van Rijn et al. (2002) investigated how the spatial distribution of supplemental pollen influ- enced the biological control of thrips in greenhouses. The local supply of pollen on otherwise pollen-free cucumber plants increased the densities of the predatory mites and suppressed growth of the herbivore population despite thrips also feeding on the pollen. A parameterised predator–prey model revealed how a uniform supply of alternative food enhanced pest popula- tion growth rate and escape from predator control. Conversely, a spatially restricted food supply caused predators to aggregate; this deterred prey due to the increased predation risk and thus the predators monopolised the food. Whether the predators aggregate as a result of increased attraction, increased arrestment, or both is not known.

State-dependent behaviour

Parasitoid and predator behaviour is state-dependent, varying with the number of mature eggs present in the ovaries at a given time (Jervis and Kidd 1986; Heimpel and Collier 1996; Jervis et al. 1996; Heimpel et al. 1996; Heimpel and Rosenheim 1998) as well as with nutritional state (Sabelis 1992; Wäckers 1994; Heimpel and Rosenheim 1995; Heimpel and Collier 1996; Hickman et al. 2001). In parasitoids, for example, physiological state influences responsiveness to plant odours, the choice between food- and host-containing patches, responsiveness to contact chemicals, patch time allocation, oviposition rate and possibly flight activity (Wäckers 1994; Jervis et al. 1996; Sirot and Bernstein 1996; Lewis et al. 1998). Natural enemy behaviour is also influenced by experience (e.g. Lewis et al. 1990; Vet et al. 1995; Fellowes et al. 2004), and possibly also age (but see Heimpel and Rosenheim 1995).

Dispersal studies

Investigations of natural enemy movement – by which we mean immigration into and emigra- tion out of the crop (or the crop-associated habitat, e.g. in the case of some physical refugia) – are vital in studies of resource use in relation to habitat manipulation (Corbett 1998; MacLeod 1999) (Tables 5.1–3). While a natural or artificial resource may improve natural enemy survival, growth, development and reproduction, it does not necessarily guarantee that the resource, when placed in the vicinity of the crop, will be an effective source of immigrant parasitoids or predators. For example, incorporation of knotweed in alfalfa fields attracted more predators in the general area but did not cause an increase in predator densities in alfalfa, the economic crop (Bugg et al. 1987).

By the same token, an identified food source, natural or artificial, may be placed in or near to the crop, but the parasitoids or predators may not use the food. Proof is required that the natural enemies can travel between refuge and crop, between alternative host/prey and pest populations, or between food and pests, in sufficient numbers to improve pest suppression. Methods for monitoring parasitoid and predator movements are reviewed in Sunderland et al. (2004). Inexpensive techniques include marking coccinellids, carabids and other hard-bodied insects with paints (MacLeod 1999) and dusting smaller and soft-bodied insects such as parasitoids with fluorescent powder. However, fluorescent powder can be harmful to small-bodied parasitoids (Garcia-Salazar and Landis 1997). Other studies have involved labelling parasitoids with rubidium (Corbett and Rosenheim 1996) and immuno-markers (Hagler and Jackson 1998). One-way travel capability, between food source and crop, can also be assessed using the food materials themselves as markers: pollen grains located within the gut (e.g. see Wratten et al. 2003) or on the body surface, or signature sugars/dyes in nectar and honeydew present within the gut. Marking and tracking is reviewed by Lavandero et al. (ch. 7 this volume).

Theoretical studies can help predict whether adding beneficial vegetational structure for natural enemies of known dispersal powers will improve pest control. A simulation model by Corbett and Plant (1993) described the spatial distribution of natural enemies after the addition of strips of vegetation intersecting a field. Generally, if natural enemies used the vegetation before the crop germinated, the vegetation was a ‘source’ of natural enemies. Natural enemies would be available to exert pressure on pests once the crop germinated. However, if the vegetation and crop germinated simultaneously, the vegetation strip might serve as a ‘sink’ of natural enemies by reducing their activity in the economically important crop (see Mensah and Sequeira, ch. 12 this volume). Also, by incorporating the diffusion rate of the natural enemy, the model predicted the scale at which beneficial effects of the resource will be observed in the field. To what extent this model applies to real natural enemies is unclear, but with appropriate modification the model would be a useful basis for investigations aimed at assessing the importance of dispersal rate, coupled with plant phenology, in influencing outcome of manipulation programs.

Knowing the absolute distance a natural enemy can travel, and how this is affected by physio- logical state, is important. Evidence of commuting behaviour between refuge and crop (this would constitute migration, see Southwood 1962) or between food and crop (this would consti- tute foraging by the natural enemy within its trivial range, see Southwood 1977, 1978) should also be sought.

Body size can influence dispersal by natural enemies in two ways: directly, through its biome- chanical effect on flight performance (Dudley 2000) and indirectly through its effect on the size of the fat body which fuels both somatic maintenance and, in some insects, locomotion (Chapman 1998). Ellers et al. (1998) showed that in the parasitoid Asobara tabida (Braconidae), the greater the distance travelled from a central release point, the more the fat reserves were depleted. (The quantity of lipids in the fat body of individual insects can be measured using the ether extraction method of Ellers (1996) or the vanillin reaction (Olson et al. 2000).

Furthermore, larger females had larger fat reserves (see also Rivero and West 2002), and dispersed over greater distances than smaller females (Ellers et al. 1998). Note that a decline in fat reserves was recorded independently of female age (Ellers et al. 1998) (lipid reserves have been shown to decline with age in several parasitoid wasp species, see Jervis and Kidd 1986, Casas et al. 2003) carbohydrates, not fats, are used by Hymenoptera as a ‘flight fuel’ (Casas et al. 2003) and the same is likely to apply to the fuelling of ambulation. This points to egg production as the most likely cause of the fat body decline. At least as far as the body size–fat body effect was concerned, there is support for this: lifetime reproductive success (measured as the egg load of recaptured females plus the numbers of eggs they were estimated to have laid) increased with body size in A. tabida. Conservation biological control investigators should be mindful of the body size–dispersal distance relationship when planning a manipulation program: a nutrition- ally sub-optimal alternative host or prey species will produce smaller adult progeny (see Jervis et al. 2004) which will be inferior dispersers (see above).

Ellers et al’s (1998) study was of dispersal within A. tabida’s trivial range. Body size and fat body size have been measured in a migratory range context (migration to overwintering refugia) for Coccinella septempunctata (Zhou et al. 1995).

Last, the physical attributes of companion plants can significantly influence the number of predators dispersing to crop plants (Cottrell and Yeargan 1999).

Numerical responses

Supplemental foods

An increase in the numerical response (the rate of recruitment into the subsequent generation) of the natural enemy population is an important consideration where the pest is present in the crop for longer than the duration of one natural enemy generation. Van Rijn et al. (2002) point out that the effect of provision of supplemental foods on the natural enemy’s numerical response has nevertheless been ignored by some authors. The numerical response depends largely on three components: development rate, larval survival and the realised fecundity of females (Beddington et al. 1976; Hassell 1978). Food supplements have the potential to enhance some or all of these. For example, McEwen et al. (1993c, 1996) found diet-related variation in development and survival in the larvae of Chrysoperla carnea. Larvae given artificial honeydew, as opposed to water, were more likely both to complete development to the second larval moult (there are three larval instars) at low egg densities and to survive to adult eclosion. Pollen feeding increases development rate and survival to the adult stage in some phytoseiid mites (McMurtry and Scriven 1964; Osakabe 1988). Food supplements can enable immature predators to compensate for the energetic costs of maintenance metabolism (Beddington et al. 1976; Jervis et al. 2004) and achieve a higher adult weight (McEwen et al. 1993c), a higher egg load upon eclosion and a larger store of energy reserves for use in somatic maintenance.

Food provision may also affect female fecundity by altering the threshold prey density at which eggs are laid by anautogenous predators (Beddington et al. 1976; Jervis et al. 2004). Anautogenous insects cannot produce mature eggs without first ingesting a certain quantity of an appropriate food, due to insufficient resource carry-over from the larval stage. Anautogeny is found in Coccinellidae and Chrysopidae (Dixon 1959; Beddington et al. 1976; McEwen et al. 1996). Chrysoperla carnea displays plasticity in its dependence on food for initial egg produc- tion: it can be either anautogenous or, when given a non-prey food supplement during larval life, autogenous, capable of producing mature eggs before ingesting a meal as an adult (McEwen et al. 1996). If the food supplement contains adequate nutrients to allow initial egg production, then it should lower the prey density threshold for oviposition. Food provision can also increase age-specific and lifetime fecundity (Jervis et al. 2004).

Protocols for measuring the effects that natural and artificial supplementary foods have on the main components of the numerical response can be derived from van Lenteren et al. (1987), Idris and Grafius (1995), Gilbert and Jervis (1998), Crum et al. (1998), Evans (2000), Limburg and Rosenheim (2001) and Jervis et al. (2004). Negative correlations (indicative of physiological trade-offs) between key life-history variables can occur: supplemental food provision may increase one variable (e.g. fecundity) at the expense of another (e.g. egg size, which will influ- ence larval survival) (see Crum et al. 1998). Thus it is advisable to study a range of life-history variables to obtain insights into the potential benefits of supplemental or substitute food provi- sion (caution should be exercised in using any single life-history trait as a proxy measure of fitness, see the review by Roitberg et al. 2001).

Alternative foods may be investigated as potential substitutes for prey during periods when the latter are absent or very scarce, for example during the period following harvesting and reseeding/planting of the crop (see Crum et al. 1998 for protocols applied to predators). They may serve only as a stop-gap resource for some predator species (Gurr et al. 2004), enabling survival and a high search rate over a short time period (e.g. Limburg and Rosenheim 2001), whereas for others they may allow a significant amount of development, reproduction and survival to take place (Smith 1961, 1965; Kiman and Yeargan 1985; Cottrell and Yeargan 1998; Crum et al. 1998; van Rijn and Tanigoshi 1999). Provision of substitute foods may be more effective during some phases of the life-cycle than others (Crum et al. 1998).

Even when a supplement or substitute is found to be highly effective in promoting develop- ment, reproduction and survival, it still needs to be tested for its effect on the numerical response under field conditions. Obvious problems such as rainfall and humidity extremes aside, artificial resources can become ineffective due to bacterial or fungal contamination. Microorganisms may reduce the performance-enhancing value of the artificial food, and may even make the food repellent. For example, survival of adult Microplitis croceipes was greatly reduced when given honey-water that was contaminated with bacteria (Sikorowski et al. 1992).

Van Rijn et al. (2002) studied supplemental food effects under glasshouse conditions, remov- ing immigration and retention effects, and showed that pollen provision can greatly improve the control of thrips by predatory mites even though pollen was fed upon by the prey as well as by the predator. Improved control results from an increase in the predators’ numerical response to pollen and thrip density. The numerical response outweighs the negative effects of a reduction in the functional response (see above) and the accelerated population growth of the pest due to its feeding on pollen.

Provision of alternative hosts and prey

Among the range of possible population processes resulting from the provision of alternative hosts/prey are apparent competition and apparent mutualism (see Holt 1977). In the former case, the natural enemy increases in abundance (numerical response) on the alternative herbivore and, assuming the natural enemy readily transfers to the pest, the latter will decrease in the abundance – a result that is in line with the goal of pest management through habitat manipulation, although the precise level of the economic threshold would determine the degree to which the program has been successful. If, however, there is only a weak tendency for the natural enemy to transfer to the pest, and the alternative’s abundance remains sufficiently high, the parasitoids can become egg- depleted (the alternative host acting as a ‘sink’ for the parasitoids’ eggs, see Heimpel et al. 2003) or the predators can become satiated, so limiting the impact the enemy might have on the pest. (‘Apparent mutualism’ applies here because the pest indirectly benefits from the presence of the alternative herbivore species.) The pest is likely to suffer much less mortality than anticipated by the biological control practitioner so, depending on the precise level of the economic threshold,

the manipulation program may be a failure. Guidance on the design and interpretation of manip- ulation experiments for studying apparent competition and mutualism can be derived from Müller and Godfray (1997), Morris et al. (2001) and Heimpel et al. (2003).

Conclusions

Our purpose in writing this chapter was to outline how natural enemy life-history may affect the degree to which natural enemies may respond to habitat manipulation that is designed to improve biological control. The three habitat manipulations discussed are food supplementa- tion, provision of alternative hosts and provision of physical refugia. Clearly, a wide range of life-histories will mediate the effectiveness of these and other methods of conservation biologi- cal control. Designing habitat manipulation programs that best take advantage of natural enemy life-history traits should lead to more effective and predictable science of conservation biologi- cal control (Barbosa 1998; Pickett and Bugg 1998; Landis et al. 2000). Our approach can be summarised and illustrated by posing a series of questions for each of the manipulations discussed above. The effectiveness of supplementary food sources is centred on two broad questions (Table 5.1). First, does the natural enemy demonstrate a need for the supplemental food? Second, is the natural enemy likely to benefit from the supplemental food source? For the provision of alternative hosts or prey, questions focus on whether the resource is limiting for the natural enemy, and whether it will actually be used by the natural enemy in the field (Table 5.2). Finally, for the incorporation of physical refugia in the field, questions centre on the usefulness of diverse habitats and the ability of natural enemies to commute between the refugium and the pest habitat (Table 5.3). These are apparently simple questions, but as discussed in this chapter, each involves a suite of biological complexities. Accordingly, entomologists can, irrespective of their particular research specialism, make a valuable contribution to knowledge of the life- history traits that are potentially important in conservation biological control. Even evolution- ary biologists have a key role to play by discovering negative and positive correlations between life-history traits.

Acknowledgements

We are very grateful to two anonymous reviewers for their constructive comments on the