L. Wäckers* - 5 The Parasitoids’ Need for Sweets: Sugars in Mass Rearing and Biological Control

5 The Parasitoids’ Need for Sweets: Sugars in Mass Rearing and Biological Control

F. L. Wäckers*

Laboratory of Entomology, PO Box 8031, 6700 EH Wageningen, The Netherlands

Introduction

Due to their ability to regulate herbivore populations, parasitoids and predators play an important role both as biological control agents and as keystone species in natural ecosystems. Given this fact, it is not surprising that research interest has largely focused on how predators and parasitoids ﬁnd and interact with their herbivorous prey/host (Godfray, 1994; Dicke and Vet, 1998).

However, the majority of these principally carnivorous arthropods also use plant- derived foods as a source of nutrients. This

vegetarian side of the menu may include various plant substrates, such as nectar, food bodies, pollen and fruits, as well as foods indirectly derived from plants (e.g. honeydew, or pycnial ﬂuid of fungi). In some cases, predators may also feed on plant productive tissue, in which case they have to be classi- ﬁed as potential herbivores (Coll, 1996). The level at which predators or parasitoids depend on primary consumption varies.

Many predator species are facultative consumers of plant-derived food. This category includes predatory mites (Bakker and Klein, 1992), spiders (Ruhren and Handel, 1999),

*Present address: Netherlands Institute of Ecology, PO Box 40, 6666 ZG Heteren, The Netherlands.

Theory and Testing Procedures (ed. J.C. van Lenteren) 59

Abstract

It is generally accepted that most parasitoids and many predators require sugar sources, such as nectar or honeydew, to cover their energetic needs. Protocols for the mass rearing and release of these natural enemies often take these sugar requirements into account. Nevertheless, the choice of food sources and the methods of application are usually based on trial and error, due to the fact that basic information on food ecology of beneﬁcial insects is scarce. In this chapter, an overview is presented of the ﬁeld of parasitoid food ecology.

After discussing the various ways in which parasitoid ﬁtness can beneﬁt from sugar feeding, various natural sugar sources are compared in respect of their function in nature and their suitability as parasitoid nutrition.

Given the fact that the choice of the optimal food supplement depends on characteristics of both the food source and its consumer, either side of the equation is addressed. Sugar sources are compared in respect of their composition and the volume produced. Parasitoid characteristics addressed include taste perception, digestive efﬁciency and food-foraging behaviour. It is argued that the ﬁeld of food ecology can help in select- ing food supplements for use in parasitoid rearing as well as application in biological control.

predatory hemipterans (Bugg et al., 1991), predacious beetles (Larochell, 1990), lacewings (Limburg and Rosenheim, 2001) and predacious wasps (Beggs and Rees, 1999).

Feeding on pollen or nectar can enable these species to bridge periods of low prey availability (Limburg and Rosenheim, 2001). When combined with prey feeding, plant-derived foods can increase predator ﬁtness over prey feeding alone (van Baalen et al., 2001). A sec- ond category of natural enemies are obliga- tory consumers of plant-derived foods, at least during part of their life cycle. This category includes many ant species (Porter, 1989;

Tobin, 1994), syrphid ﬂies (Lunau and Wacht, 1994) and parasitoids (Jervis et al., 1996).

As the nutritional ecology of predators has been extensively covered elsewhere, the focus of this chapter will be on issues con- cerning feeding by adult parasitoids. I shall stress that sugar feeding represents an inte- gral part of parasitoid biology and that insight in this topic is essential to our under- standing of parasitoid ecology, as well as their efﬁcacy as biological control agents.

Nutritional Requirements of Parasitoids During their development from parasitic larvae to free-living adults, the dietary requirements of parasitoids take an equally marked turn. While parasitoid larvae are strictly carnivorous, virtually all adult parasitoids require carbohydrates as a source of energy (Jervis et al., 1996), especially for ﬂight (Hoferer et al., 2000).

While predators can often utilize both liquid and solid plant substrates (pollen, food bodies), by far the majority of parasitoids are restricted to feeding on sugar-rich solutions, such as nectar and honeydew. This group includes those species that emerge with a full complement of mature eggs (so-called preovigenic species), as well as species that continue to mature eggs during their adult life (synovigenic).

Some (usually synovigenic) parasitoid species retain a level of carnivory during their adult life, as they may feed on host haemolymph in addition to sugar feeding (Jervis and Kidd, 1986). Due to their different

nutritional composition, haemolymph and nectar or honeydew are only partly inter- changeable and they are believed to cover sep- arate requirements. Sugar-rich nectar or honeydew primarily provides for the parasitoid’s energetic needs. While these food sources usually contain low levels of amino acids, proteins and lipids, they might nevertheless contribute to physiological processes, such as egg maturation. Host haemolymph, on the other hand, is usually a relatively poor source of energy. In part, this can be explained by the fact that haemolymph in general contains relatively low levels of carbohydrates (Kimura et al., 1992). An additional limitation lies in the fact that trehalose as the main haemolymph sugar is rather poorly metabo- lized by parasitoids (Wäckers, 2001). Instead, haemolymph constitutes a primary source of protein for physiological processes, such as egg maturation (Rivero and Casas, 1999).

Those synovigenic species that do not engage in host feeding draw upon the protein and fat reserves transferred over from the larval stage.

Effects of Sugar Feeding on Parasitoid Fitness Parameters

Parasitoids emerge with a limited supply of energy. The nutrients transferred from the larval stage often cover no more than 48 h of the parasitoid’s energetic requirements. This period is extremely brief, considering the fact that these species usually have the potential to live for weeks when suitable food is available. Part of this brief period covered by larval food reserves cannot be used to search for hosts, as parasitoids often require a preoviposition period for the maturation of their eggs. The reproductive success in the remaining narrow time-window is further limited by lack of experience, resulting in an initially slow and inefﬁcient search (Turlings et al., 1993; Vet et al., 1995).

Sugar feeding can considerably increase the parasitoid’s lifespan. Taking the preoviposition period and experience into account, the effective impact will be even more signiﬁcant. This means that parasitoids that fail to replenish their energy reserves through sugar feeding will suffer severe ﬁt- 60 F.L. Wäckers

ness consequences. Carbohydrates can have a strong impact on several key ﬁtness parameters. Sugar feeding is indispensable to parasitoid survival, a factor applying to both females (Zoebelein, 1956; Syme, 1975; van Lenteren et al., 1987; Idoine and Ferro, 1988;

Wäckers, 2001) and males (Zoebelein, 1956;

Wäckers and Swaans, 1993). In the ideal world of the laboratory, sugar can increase parasitoid longevity up to 20-fold (Zoebelein, 1956; Syme, 1975; Idoine and Ferro, 1988; Wäckers and Swaans, 1993; Dyer and Landis, 1996).

Sugar feeding can also beneﬁt a parasitoid’s fecundity, either through a positive effect on the rate of egg maturation, through an increase in reproductive lifespan or both (Zoebelein, 1956; Hocking, 1966; Syme, 1975; Baggen and Gurr, 1998;

van Lenteren, 1999; Schmale et al., 2001).

Finally, the feeding status can affect the parasitoid’s propensity to seek out their herbivorous hosts. Telenga (1958) and van Emden (1962) found that parasitoids are more active in habitats in which flowers are in bloom than in nearby habitats without flowers. Wäckers (1994) and Takasu and Lewis (1995) demonstrated that sugar deprivation reduces host-searching effi- ciency, partly due to a general reduction in activity and partly due to a shift from host searching to food searching.

Each of the listed ﬁtness parameters translates directly into the number of herbivores that can be attacked. The availability of suitable plant-provided food sources conse- quently has a strong impact on parasitoid mass rearing, as well as on their efﬁcacy as biological control agents.

Choosing Food Supplements for Mass Rearing

The basic concept that parasitoid ﬁtness can be dramatically enhanced through the sim- ple provision of food supplements has been long engrained in parasitoid rearing. It is standard practice to provide adult insects with honey, honeydew, sugar water, fruits or other sugar sources. While the importance of food supplements is thus widely

acknowledged, often little attention is given to the actual choice of the food source. This choice may be based on issues like conve- nience (honey can be easily obtained, does not require preparation and does not spoil), methodology (parasitoids can get stuck in liquid food media, while they have trouble imbibing solid food sources) and economy (cost). Hardly ever is the choice actually based on what should be the central issue:

the question of which substrate is the optimal food for a given parasitoid.

This omission is hardly surprising in light of the fact that few comparative data exist in respect of the relative suitability of various food sources. The low priority given to this issue reﬂects the generally held conception that any sugar-rich liquid makes a suitable food supplement for parasitoids. In an attempt to correct this notion, I shall com- pare the main natural sugar sources in respect of their composition, and discuss the consequences for feeding parasitoids.

Potential Sugar Sources and Their Ecological Function

Most hymenopteran pollinators, ants and parasitoids share a dependency on sugars as their main source of energy. The ecological importance of these species, in combination with their dependency on carbohydrates, explains the fact that sugars play a central role in numerous types of mutualisms involving Hymenoptera. Sugar-feeding insects usually have a wide range of carbohydrate sources available, the most important being ﬂoral nectar, extraﬂoral nectar (EFN) and honeydew.

Floral nectar serves as a food reward in the mutualism between plants and their pollinators. Even though parasitoids in general are ineffective pollinators, they can freeload on this mutualism as they seek out ﬂowers and collect ﬂoral nectar (Kevan, 1973; Jervis et al., 1993). Due to the fact that many plants are pollinated by Hymenoptera (e.g. bee species), their nectar can be expected to cater to the taste and nutritional requirements of these species. As nectar requirements of hymenopteran parasitoids appear Food Ecology and Mass Rearing in Biocontrol 61

to be similar to those of honey-bees (Wäckers, 1999, 2001), the composition of ﬂoral nectar is probably suitable for hymenopteran parasitoids. Parasitoid species have been reported to feed on various types of ﬂoral nectar (Kevan, 1973;

Jervis et al., 1993; Idris and Graﬁus, 1995;

Baggen and Gurr, 1998).

Extrafloral nectaries include a wide range of nectar-excreting structures (Zimmerman, 1932). Extrafloral nectaries have been described in approximately 1000 species from 93 plant families (Koptur, 1992; Whitman, 1996). They occur on a range of plant parts, including stems, leaves, fruits and flowers. Extrafloral nectaries are distinguished from their floral counterparts by the fact that they are not involved in pollination. Instead, they are thought to serve a role in an entirely different type of mutualism, in which plants use nectar to recruit predators or parasitoids.

The latter return the favour by safeguard- ing plants against herbivory.

In a number of plant systems, it has been demonstrated that the presence of extraﬂoral nectar can translate into both reduced plant damage (O’Dowd and Catchpole, 1983;

Wagner, 1997) and increased plant reproductive ﬁtness (Rico-Gray and Thien, 1989;

Oliveira, 1997). The above-mentioned stud- ies have all focused on the role of EFN in plant–ant mutualisms. However, extraﬂoral nectaries are also frequented by a range of other carnivorous arthropods (Bugg et al., 1989; Koptur, 1994; Whitman, 1996). The provision of these food supplements may serve to enhance the effectiveness of plant–spider (Ruhren and Handel, 1999), plant–predatory wasp (Torres-Hernández et al., 2000) or plant–parasitoid interactions (Lingren and Lukefahr, 1977; Stapel et al., 1997).

Honeydew is a generic term for sugar-rich excretions of phloem-feeding Sternorrhyncha.

It is generally accepted that sap-feeding insects have to excrete carbohydrates to bring the high carbohydrate/amino acid ratio of the ingested phloem sap in balance with their nutritional requirements. Honeydew is an exception to the above-mentioned sugar sources, as it is a waste product, rather than having a primary function in mutualistic

interactions. However, depending on its composition, honeydew can be eagerly collected by ants (Stadler and Dixon, 1999; Völkl et al., 1999). The general tendency of ants to defend and protect sugar sources has resulted in mutualistic interaction between some honeydew producers and ants. In these instances, honeydew production has to some extent become an analogue to EFN.

Sugar-source Characteristics Nectar and honeydew contain various sugars, amino acids, lipids and other organic compounds in more or less aqueous solutions (Baker and Baker, 1982b; Kloft et al., 1985). The nutritional and energetic value of a particular nectar or honeydew is deter- mined by its volume, its composition and the component concentrations.

Volume

The volume of ﬂoral nectar excreted and its composition are primarily a plant characteristic. In addition, however, they may be affected by other factors, such as the age of the nectary, irradiance, temperature, soil conditions and water balance (Búrquez and Corbet, 1991) and state of pollination (Gori, 1983). The duration of nectar secretion is limited by the – often brief – ﬂowering time.

The often copious nectar volume secreted by extrafloral nectaries can exceed floral nectar production. This is in part due to high production levels, as well as to extended periods of production. As in floral nectar, the production of EFN is affected by abiotic factors (Bentley, 1977). In addition, plants can raise the secretion of nectar in response to two biotic mechanisms. Nectar production can be induced both by ant attendance (i.e. nectar removal) (Koptur, 1992; Heil et al., 2000) and herbivore feeding (Koptur, 1989; Wäckers and Wunderlin, 1999; Heil et al., 2001; Wäckers et al., 2001).

This sophisticated two-pronged mechanism allows plants to actively distribute their investments in a way that optimizes their defence.

62 F.L. Wäckers

In the case of honeydew, the volume produced and its composition depend on the sap-feeding species, as well as on plant parameters and environmental factors (Kloft et al., 1985). Sap feeders can actively increase the quantity of excreted honeydew when tended by ants (Takeda et al., 1982; Yao and Akimoto, 2001).

Sugar composition

Floral nectar, EFN and honeydew are principally sugar solutions. However, the sugar composition can vary in respect of both the types of saccharides and their relative proportions.

Floral nectar is generally dominated by the monosaccharides fructose and glucose

and the disaccharide sucrose (Baker and Baker, 1982b). The proportions of the three main sugars are rather constant within a species, but can show wide differences between ﬂowering species. Percival (1961) and Baker and Baker (1982b), for instance, showed that the sucrose/hexose ratios of ﬂowering plants can vary from less than 0.1 to more than 0.999. In addition to these main nectar sugars, nectar may contain low concentrations of other carbohydrates (Table 5.1).

EFN is typically dominated by sucrose and its hexose components glucose and fructose. These are also the three most com- mon sugars in EFN. Unlike the species- characteristic sugar ratio in ﬂoral nectar, however, the ratio of sucrose to hexose in the EFN of a given species can be much Food Ecology and Mass Rearing in Biocontrol 63

Table 5.1. Sugars reported to occur in ﬂoral nectar, extraﬂoral nectar and honeydew.

Reported to occur in References Monosaccharides

Glucose Various (extra)ﬂoral nectars Bentley, 1977

Honeydew Baker and Baker, 1983; Kloft et al., 1985 Fructose Various (extra)ﬂoral nectars Bentley, 1977; Baker and Baker, 1983

Honeydew Kloft et al., 1985

Galactose Extraﬂoral nectar Bory and Clair Maczulajtys, 1986; Olson and Nechols, 1995

Floral nectar Gottsberger et al., 1973

Honeydew Byrne and Miller, 1990

Mannose Traces in ﬂoral nectar and fruits Barnavon et al., 2000

Rhamnose Extraﬂoral nectar Bory and Clair Maczulajtys, 1986 Disaccharides

Sucrose Various (extra)ﬂoral nectars Bentley, 1977; Baker and Baker, 1983

Honeydew Kloft et al., 1985

Maltose Floral nectar Baker and Baker, 1983; Belmonte et al., 1994

Coccid honeydew Ewart and Metcalf, 1956

Melibiose Floral nectar Baker and Baker, 1983

Eucalyptus manna (plant exudate) Steinbauer, 1996

Trehalose Honeydew Kloft et al., 1985

Trehalulose Honeydew (whiteﬂy) Hendrix et al., 1992 Trisaccharides

Rafﬁnose Floral nectar Baker and Baker, 1983

Honeydew Byrne and Miller, 1990

Melezitose Primarily in honeydew Kloft et al., 1985; Hendrix et al., 1992 Some ﬂoral nectars Baker and Baker, 1983

Erlose Honeydew Kloft et al., 1985

Tetrasaccharide

Stachyose Floral nectar (orchids) Baker and Baker, 1983

Honeydew Byrne and Miller, 1990; Davis et al., 1993

more variable. In general, EFN composition shows relatively high levels of fructose and glucose (Tanowitz and Koehler, 1986;

Koptur, 1994). This can be explained by the exposed nature of most extraﬂoral nectaries, resulting in increased microbial breakdown of sucrose. In addition to the three main sugars, several other sugars may be present (Table 5.1). Besides carbohydrates, EFN may contain variable amounts of proteins, amino acids and lipids (Baker et al., 1978; Smith et al., 1990).

The particular amino acid composition can increase the attractiveness of EFN as a food source (Lanza et al., 1993).

Honeydew differs from ﬂoral nectar and EFN as it often contains substantial amounts of oligosaccharides (Kloft et al., 1985;

Hendrix et al., 1992). Even though the sugar composition of honeydew reﬂects the origi- nal composition of the phloem sap of the host plant, the sugar components and their relative quantities can be altered during the passage through the gut of the phloem feeder. On the one hand, phloem sugars such as sucrose and maltose are broken down by digestive enzymes, while, on the other hand, the sap feeders may also synthesize more complex sugars. The trisaccharides melezitose and erlose (fructomaltose), as well as the disaccharides trehalose and trehalulose, are examples of sugars that are synthesized through the action of gut enzymes on plant- derived sucrose (Mittler and Meikle, 1991;

Hendrix et al., 1992). The resulting sugar spectrum may range from honeydews that are almost entirely composed of the phloem sugar sucrose and its hexose components fructose and glucose to those honeydews that completely lack hexoses and are dominated by insect-synthesized oligosaccharides (Kloft et al., 1985; Hendrix et al., 1992; Völkl et al., 1999).

Sugar concentrations

Sugar concentration is an important factor determining the uptake of a sugar source. At low concentrations, gustatory perception might be impeded (Wäckers, 1999), whereas high sugar concentrations interfere with

sugar uptake (Wäckers, 2000). In ﬂoral nectar, sugar concentrations can already range from 5 to 75% at the time of nectar secretion (Dafni, 1992). Environmental conditions may further affect nectar concentrations, both indirectly, through their effects on the nectar- producing plant, and directly, through evaporation, hygroscopy or rain dilution.

Sugar concentrations of undiluted EFN range from 5 to more than 80% (Koptur, 1992; Wäckers et al., 2001). In general, EFN shows much more variation in respect of sugar concentrations than ﬂoral nectar from the same plant. When protected from rain, EFN tends to be more concentrated, probably due to the fact that its exposed nature increases evaporation.

The fact that honeydew is typically available as little droplets or as a thin film on the substrate means that it is even more sub- jected to evaporation. As a result, sugar concentrations are often at saturation. This is likely to be a limiting factor in honeydew uptake. This problem is accentuated by the specific tendency of the honeydew sugars raffinose and melezitose to crystallize rapidly (Wäckers, 2000).

Parasitoid Characteristics

Insects often show a tendency to visit sugar sources of a certain composition (Baker and Baker, 1982a). The sugar components are an important factor determining patterns of food utilization (Inouye and Waller, 1984;

Alm et al., 1990; Lanza et al., 1993; Josens et al., 1998; Völkl et al., 1999). We have seen that nectar and honeydew often vary widely in respect of their sugar composition. As a result, one frequently investigates an insect’s response to individual nectar or honeydew components at well-deﬁned concentrations, rather than studying a few arbi- trary examples out of the broad range of natural nectar or honeydew compositions.

In previous work, I have studied a range of sugars occurring in nectar and/or honeydew (listed in Table 5.1), as well as lactose.

These 14 sugars were compared in respect of their effect on parasitoid gustatory response and longevity.

64 F.L. Wäckers

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