SEARCH

SEARCH BY CITATION

Keywords:

  • kairomones;
  • synomones;
  • natural enemies;
  • parasitoid;
  • predator;
  • innate;
  • learning;
  • trophic levels;
  • chemical ecology

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

For the location of hosts and prey, insect carnivores (i.e., parasitoids or predators) often use infochemical cues that may originate from the host/prey itself but also from the food of the host/prey, a food plant, or another feeding substrate. These cues can be either specific for certain host/prey complexes or generally present in various complexes, and the reaction of the carnivores to these cues is either innate or learned. According to the concept on dietary specialization and infochemical use in natural enemies, the origin and specificity of the infochemical cues used and the innateness of the behavioural response are dependent on the degree of dietary specialization of the carnivore and its host/prey species. This concept has been widely adopted and has been frequently cited since its publication. Only few studies, however, have been explicitly designed to test predictions of the concept. Thus, more than 10 years after publication and despite of its broad acceptance, the general validity of the concept is still unclear. Using data from about 140 research papers on 95 species of parasitoids and predators, the present literature study comparatively scrutinises predictions from the concept.

 In accordance with the concept, learning to react to infochemicals and the use of general host and host plant cues was more often found in generalists than in specialists. In addition, more specialists were using specific infochemicals than generalists. In contrast to the concept, however, there was no significant difference between specialists and generalists in the proportion of carnivore species that use infochemicals during foraging and also extreme generalists are using infochemical cues for foraging. Likewise, an innate reaction to infochemicals was found in both specialists and generalists. Several reasons why infochemical use, including an innate reaction to infochemicals, is adaptive in generalist carnivores are discussed . We conclude that the concept has been a useful paradigm in advancing the chemical ecology of arthropod carnivores, but needs to be modified: the use of infochemicals is expected in all arthropod carnivores, regardless of dietary specialization.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

During foraging, insect carnivores (i.e., parasitoids or predators) often use infochemical cues for the location of hosts and prey. These cues may originate directly from the host/prey or from their products such as faeces, silk, or exuviae. In addition, they may be emitted from the food plants of the hosts/prey or from other feeding substrates. Thus, carnivores orient to cues from the whole host/prey complex consisting of the host/prey insect plus its food. These infochemical cues might be either specific for certain host/prey complexes or they might be generally present in various complexes and the reaction to the cues may be either innate or may be associatively learned after a host/prey encounter in their presence. Hence, the infochemicals used by carnivores can be categorized according to their origin, their specificity, and the innateness of response they elicit.

In 1992, Vet & Dicke formulated the concept of dietary specialization and infochemical use in natural enemies. According to this concept, the origin and the specificity of infochemicals used by a carnivore and the innateness of the reaction is expected to depend on the dietary specialization of the carnivore and its host/prey species. With over 330 citations since 1992 (ISI-Web of Science) this concept has been often cited in studies on chemical foraging cues, especially of parasitoids, to put results in perspective. Only a few studies, however, have been explicitly designed to test predictions of the concept (Steidle & van Loon, 2002). Thus, more than 10 years after publication and despite of its broad acceptance, the general validity of the concept is still unclear.

The concept of dietary specialization and infochemical use in natural enemies

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

For their concept, Vet & Dicke (1992) outlined different categories of host/prey complexes by combining the degree of dietary specialization and the trophic level at which this specialization is expressed. Carnivores might be specialists or generalists, but also their host/prey species can either be specialists or generalists on their host plants or feeding substrates. Thus, carnivores can be considered specialists or generalists at the host/prey level and the host plant/feeding substrate level. Accordingly, Vet & Dicke (1992) distinguish between the following four groups (Figure 1):

image

Figure 1. Groups of tritrophic host/prey complexes with different dietary specialization. After Vet & Dicke (1992).

Download figure to PowerPoint

Group A: Specialists at host/prey and host plant/feeding substrate levels.

Group B: Generalists at host/prey level and specialists at the host plant/feeding substrate level.

Group C: Specialists at the host/prey level and generalists at the host plant/feeding substrate level.

Group D: Generalists at the host/prey and the host plant/feeding substrate levels.

These categories represent extremes and the authors acknowledge that many intermediates will exist. Several predictions are made for the carnivores in these groups with respect to the origin and the specificity of the infochemicals used and the innateness of the elicited response (Table 1). In the highly specialized group A, an innate response to infochemicals from the host/prey as well as from the host plant/feeding substrate is predicted. These carnivores should not need learning to react to foraging cues. In group B, carnivores should innately react to infochemicals that are general for all host/prey species and to infochemicals from the host plant/feeding substrate. The reaction to infochemicals specific for certain host/prey species should be learned. In group C, an innate reaction to host/prey kairomones and to general cues from host plant/feeding substrate is expected, as well as a learned reaction to specific infochemicals from the host plant/feeding substrate. Finally, in group D the variety of potential host/prey species and host plants/feeding substrates is assumed to be associated with a great diversity of infochemicals causing physiological constraints on the sensory processing of the carnivore. Furthermore, for extremely generalist carnivores, random search might be more adaptive than focusing on certain cues. Thus, Vet & Dicke (1992) assume that under these circumstances no infochemicals should be used at all. To test the concept in the present study, the detailed predictions made above and depicted in Figure 1 and Table 1 are summarized as follows:

Table 1.  The quality (origin, specificity, innateness) of infochemical foraging cues used by arthropod carnivores with different dietary specialization in a tritrophic context according to Vet & Dicke (1992)
GroupsAaBCD
  • a

    A–D refer to groups from Figure 1.

  • b

    Abbreviations: H/P = host/prey; HP = host plant; FS = feeding substrate; S = specific cues; G = general cues; I = reaction to cues innate; L = reaction to cues learned.

OriginH/PbHP/FSH/PH/PHP/FSH/PHP/FSHP/FS
SpecificitySSGSSSGS
Innate learnedIIILIIIL
  • 1
    No infochemical use in extreme generalists.
  • 2
    Specialists should use specific cues and generalists should use general cues.
  • 3
    Innate use of infochemicals should occur in specialists but not in generalists.
  • 4
    Learning of infochemicals is expected in generalist carnivores and not in specialists.

Database

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

To examine the validity of the four predictions made above, data from approximately 140 research papers on the infochemical use of 95 species of insect parasitoids and predators have been analysed (Tables 2–4). To allocate carnivores to the four groups mentioned above, their degree of specialization was assessed according to the definition used for herbivores (Bernays & Chapman, 1994). On the host/prey level, carnivores were considered generalists when they feed on host/prey species from different taxonomic families and specialists when they feed on host/prey species from one family only. On the level of the host plant/feeding substrate, they were regarded generalists when their host/prey species feed on plants from different families or on feeding substrates as different as decaying plant material and carrion, and specialists when their host/prey species feed on plants from one family only or on similar feeding substrates. Such relatively difficult to categorize feeding substrates almost exclusively play a role in Drosophila-parasitoids, of which nine species are included in this study. Infochemicals were categorized according to the following criteria:

Table 2.  Number of carnivores with different diet breadth that are reacting to cues specific or general for their host/prey complexes
 Groups with different dietary breadth
ACDPa
  • a

    Level of significance (2 × 3 χ2-test).

  • b

    Note that some species react to specific cues from different sources, therefore percentage values in the lower part of the table do not sum up to 100%.

  • c

    Data with different lower case letters within one row are significantly different at P ≤ 0.05 (Bonferroni corrected 2 × 2 χ2-test).

Species studied [n]283829 
Species reacting to16b abc25a9b0.016
 specific cues(57%)(66%)(31%) 
Species reacting to111560.206
 specific host/prey cues(39%)(39%)(21%) 
Species reacting to6ab10a1b0.045
 specific host plant/ feeding substrate cues(21%)(26%)(3%) 
Species reacting to0a3a7b0.001
 general cues(0%)(8%)(24%) 
Table 3.  Number of carnivores with different diet breadth that innately use infochemicals from different origin
 Groups with different dietary breadth
ACDPa
  • a

    Level of significance (2 × 3 χ2-test).

  • b

    Note that some species innately react to cues from different sources, therefore percentage values in the lower part of the table do not sum up to 100%.

  • c

    Percentage from species with innate reaction.

Species studied283820 
Species with28b34160.059
 innate reaction(100%)(89%)(80%) 
Reaction to cues from:
 host/prey1828130.664
(64%)c(82%)(81%) 
 host plant/ feeding substrate 122070.417
(39%)(59%)(44%) 
 host/prey complex2410.744
(7%)(12%)(6%) 
Table 4.  Number of carnivores with different diet breadth that are learning to react to infochemicals from different origin
 Groups with different dietary breadth
ACDPa
  • a

    Level of significance (2 × 3 χ2-test).

  • b

    Data with different lower case letters within this row are significantly different at P ≤ 0.05 (Bonferroni corrected 2 ≤ 0.05 (Bonferroni corrected 2 × 2 χ2-test).

Species studied [n]283820 
Species with learned reaction4ab20b11b0.005
(18%)(53%)(55%) 

Origin from host/prey or host plant/feeding substrate

Infochemicals from host/prey originate from host/prey products such as faeces, silk, etc., or directly from the host/prey, e.g., cuticular compounds. Infochemicals from the host plant/feeding substrate are released from undamaged plants, herbivore damaged plants, and feeding substrate, with and without hosts.

General or specific infochemicals

Infochemicals were considered as general when they are present in different, non-related host/prey complexes. To demonstrate this, the identification of infochemicals in several host/prey complexes is required. A reaction to specific infochemicals was assumed when it was demonstrated that carnivores were able to differentiate between the respective odour source and a comparable one (e.g., when carnivores preferred a host-odour over non-host odours) or when the infochemicals have been identified and it is reasonable to assume that they only occur in a certain host/prey complex (or several, related host/prey complexes). This was the case mostly in species-specific pheromones.

Innate or learned response

Based on the definition by Vet et al. (1990) an innate response was assumed for holometabolous carnivores when insects were naive, i.e., had no experience with the host/prey or plant/feeding substrate apart from experience gained during development within and eclosion from the host. For hemimetabolous carnivores (e.g., Heteroptera), an innate response was assumed for insects that also during development never had contact with the prey or the host plant. A response to infochemicals was considered as learned when it only was observed in experienced insects after encounters with hosts/prey or host plants/feeding substrates, mostly including oviposition or feeding events, but was absent in naive insects.

With the exception of group D, only those studies were included where the experience of the examined carnivore was considered. In group D, nine more species were added where infochemical use has been demonstrated regardless of experience, in order to examine the frequency of infochemical use in extreme generalists. Altogether, studies on 28 species belonging to group A (Table 5), 38 to group C (Table 6), 29 to group D (Table 7), and only two to group B were taken into account. The lack of data for group B probably reflects the rare occurrence of systems belonging to this group rather than an underrepresentation in experimental studies. In a study of insect carnivores from Canadian forests by Lill et al. (2002), almost no parasitoids belonging to this group have been found. Group B, therefore, will not be further considered in this study.

Table 5.  Infochemical use by natural enemies from group A as found in the literature
Natural enemyHaPHPFSHPCOrigin of cuesReference
  • a

    Abbreviations: H = host; P = prey; HP = host plant; FS = feeding substrate; S = specific cues; G = general cues; i = reaction to cues innate; l = reaction to cues learned; s = specific cues.

Apanteles carpatusi    Substrate–host complexTakács et al. (1997)
Apoangyrus lopezi  i (s)  Healthy and host infested plantSouissi (1999); Souissi & Le Rü (1999); Souissi et al. (1998)
Aprostocetus hagenowiii (s)    Host ootheca (i), host faeces (i)Suiter et al. (1996)
Asobara rufescens  i, l  Decaying plant material (i), fermenting fruit (l)Vet & van Opzeeland (1984); Vet et al. (1984)
Chrysonotomyia ruforumi (s)    Host sex pheromone (i)Hilker et al. (2000)
Coeloides bostrichorum  i (s)  Host infested plant (i)Pettersson et al. (2001)
Cotesia rubeculai i lHost faeces, host infested plant (i), plant–host complex (l)Agelopoulos & Keller (1994); Geervliet et al. (1998); Kaiser & Cardé (1992)
Dahlbominus fuscipennisi    Host cocoon (i)Rostas et al. (1997)
Diadromus pulchellusi (s)    Host faeces (i), host cocoon (i)Auger et al. (1989)
Dipriocampe diprionii (s)    Host sex pheromone (i)Hilker et al. (2000)
Eupelmus vuilettii   lHost larvae (i), host pupae (i), host faeces (i), host plant (seed pods), plant-host complex (l)Cortesero et al. (1993), (1995)
Halticoptera laevigatai (s)    Host marking pheromone (i)Hoffmeister & Gienapp (1999)
Halticoptera rosaei (s)    Host marking pheromone (i)Hoffmeister, pers. comm.
Kleidotoma dolichocera   i Decaying plant material (i)Vet (1985)
Leptopilina clavipes   I Mushroom (i)Vet (1983)
Lemophagus pulcheri, l I  Host larva (i), larval shield (i),Schaffner & Müller (2001)
      host oral secretion (l), 
      infested HP (i) 
Orgilus lepidusI    Host faeces (i)Hendry et al. (1973)
Oomyzus gallerucaei (s) i (s)  Host faeces (i), host eggs (i)Meiners et al. (2000); Meiners, pers. comm.
Pherbellia cinerella i   Fresh prey faeces (i)Coupland et al. (1996)
Parasysrphus nigritarsisi (s)    Host defensive secretion (i)Köpf et al. (1997)
Roptrocerus xylophagorum  i (s)  Host infested plant (i)Pettersson (2001)
Roptrocerus mirus  i (s)  Pettersson (2001)
Rhopalicus tutela  i (s)  Pettersson (2001)
Teleonomus busseolaei (s)    Host sex pheromone (i)Colazza et al. (1997)
Trichogramma sibiricumi (s)    Host sex pheromone (i)McGregor & Henderson (1998)
Trybliographa rapae    iPlant–host complex (i)Brown & Anderson (1999)
Uscana lariophagai i  Host females (i), eggs (i), host plant (seeds) (i)van Huis et al. (1994)
Venturia canescensi (s)    Host mandibular secretion (i), faeces (i), l?Mudd & Corbet (1982); Nemoto et al. (1987); Arthur (1971)
Table 6.  Infochemical use by natural enemies from group C as found in the literature
Natural enemyHaPHPFSHPCOrigin of cuesReference
  • a

    Abbreviations: H = host; P = prey; HP = host plant; FS = feeding substrate; S = specific cues; G = general cues; i = reaction to cues innate; l = reaction to cues learned; s = specific cues; g = general cues.

  • b

    Learning occurs also towards artificial odour.

Anagrus nigriventris  i, l i (s)Sugar beet (i), potatoe (l)Honda & Walker (1996)
Anicetus beneficusi (s)    Host (i)Takabayashi & Takahashi (1985)
Apanteles melanoscelusi    Host exuviae (i)Weseloh (1974)
Aphaereta minuta   i Meat, yeastVet (1985)
Aphelinus abdominalis  l (s)   Mölck et al. (1999)
Aphelinus flavusI i (s)  Host (i), host honeydew (i), plant cues (i)Wickremasinghe & van Emden (1992)
Aphidius colemani  l (s) lPlant host complex (l), plant (l)Grasswitz (1998)
Aphidius eadyii (s)    Host pheromone (i)Glinwood et al. (1999a)
Aphidius ervii i (s), l lHost (i), host honeydew (i), host pheromone (i), uninfested plant (i, l), herbivore infested plant (i, l)Du et al. (1996); Glinwood et al. (1999b); Du et al. (1997); Wickremasinghe & van Emden (1992); Guerrieri et al. (1993)
Aphidius rophalosiphii i (s)  Host (i), host honeydew (i), plant (i)Wickremasinghe & van Emden (1992)
Aphytis melinusl l  Host (l), host plant (l),Morgan & Hare (1998)
Aphytis yanonensisi (s)    Host scalesTakahashi et al. (1990)
Aphidius uzbekistanicusi, l l lAlarm pheromone (i), cornicle secretion (i), herbivore infested plant (l), plant host complex (l)Micha & Wyss (1996); Micha (1995)
Ascogaster reticulatusi l  Egg-mass (i), host scales (i), plant (l)Kainoh & Tamaki (1982); Kainoh & Tatsuki (1988); Honda et al. (1998)
Asobara tabidal (s)  i, l Aggregation pheromone (l), fermenting yeast (i), decaying plants (l)Hedlund et al. (1996); Vet et al. (1984); Vet & Opzeeland (1984); Vet (1985b)
Campoletis sonorensis  i i (s), lMechanically damaged plant (i)McAuslane et al. (1991a), (1991b)
Cotesia glomeratai (s) i i, lHost (i), damaged host plant (i), host plant, plant–host complex (i, l)Takabayashi et al. (1998); Benrey et al. (1997); Geervliet et al. (1998), Mattiacci & Dicke (1995)
Cotesia kariyaii i (s), l (g)  Host (i), host infested plant (i, l)Takabayashi & Takahashi (1989);
       Takabayashi et al. (1998);
       Fukushima et al. (2002)
Cotesia plutellaei (s) i (g), l  Host pheromone (i), host faeces (i), host plant cues (i, l), damaged and herbivore infested plants (i, l)Reddy et al. (2002); Potting et al. (1999)
Diachasmimorpha tryonii i  Host (i), host substrate (i)Duan & Messing (2000)
Diachasmimorphai i iHost substrate (i), uninfested and infested host substrate (i)Duan & Messing (2000); Messing & Jang (1992); Jang et al. (2000); Eben et al. (2000)
Diaeretiella rapae  l lHost plant, host plantReed et al. (1995);
      complexSheehan & Shelton (1989)
Dinocampus coccinellae i (s)   Host defensive compounds (i)Al Abassi et al. (2000)
Encarsia formosai i  Host pupal case (i)Guerrieri et al. (1997)
Episyrphus balteatusi (s)    Host, host extract, honeydewBudenberg & Powell (1992);
       Bargen et al. (1998)
Gelis festinansi (s) i  Host silk (i), plant cues (i)van Baarlen et al. (1996)
Glyptapanteles flavicollisi (s) i  Host, host faeces, healthy and host damaged plantHavill & Raffa (2000)
Leptopilina boulardii (s)  i (s), lb Host (i), fruits (l), yeast (i)Couty et al. (1999); De Jong & Kaiser (1991); Hedlund et al. (1996); Vet (1985a)
Leptopilina heterotomai (s, l)  i, l (s)lHost (i, l), yeast (i), host aggregation pheromone (i)Dicke et al. (1984); Hedlund et al. (1996); Vet & Schoonman (1988); Vet & Papaj (1992); Wiskerke et al. (1993); Vet (1985b)
Lysiphlebus fabarumi i (s)  Host (i), honeydew (i), plant (i)Wickremasinghe & van Emden (1992)
Lysiphlebus testaceipesi (s) l lHost cornicle secretion (i), host plant (l), plant–host complex (l)Micha & Wyss (1996); Grasswitz & Paine (1992)
Macrocentrus grandii  i (s), l  Host plant (i, l),Grasswitz & Paine (1993a), (1993b); Udayagiri & Jones (1992a), (1992b), (1993)
Metasyrphus corollaei    Host (aphids)Shonouda et al. (1998)
Microplitis croceipesi i, l (g)  Host faeces (i), host infested plant (i), artifically damaged host plant (i), plant cues (l)Cortesero et al. (1997); Eller et al. (1988a), (1988b), (1992); McCall et al. (1993); Whitman & Eller (1990)
Oomyzus galerucivorusi (s) l  Host faeces (i), host eggs (i), host plant (l)Meiners et al. (1997)
Opius dissitus    i, lPlant–host complex (i, l)Petitt et al. (1992)
Praon volucrei (s)    Host pheromone (i)Glinwood et al. (1999b)
Trissolcus basalisi    Host (i)Colazza et al. (1999)
Table 7.  Infochemical use by generalist natural enemies from group D as found in the literature
Natural enemyHaPHPFSHPCOrigin of cuesReference
  • a

    Abbreviations; H = host; P = prey; HP = host plant; FS = feeding substrate; S = specific cues; G = general cues; i = reaction to cues innate; l = reaction to cues learned; s = specific cues; g = general cues; × = presumably learned response.

Amblyseius cucumerisi (s)    Alarm pheromone (i)Teerling et al. (1993)
Anthocoris nemorum  i (s) lTomato (i), plant–host complex (l)Dwumfour (1992)
Anthocoris nemoralis  l  Host infested plant (l), MeSa (l), E,E-α-farnesene (l)Drukker et al. (2000)
Ascogaster quadridentatal    Host egg (l)DeLury et al. (1999)
Brachymeria intermediai, l    Host pupae (i), vanilla odour (l)Drost & Cardé (1992); Kerguelen & Cardé (1996)
Bracon mellitori (g), l    Faeces (l, i)Vinson (1976), (1977); Henson et al. (1977)
Chrysoperla carneai (s) i (g)   Reddy et al. (2002)
Coccinella septempunctatai (g)    E-(β)-farneseneAl Abassi et al. (2000)
Cotesia congregata  l  Host plantKester & Barbosa (1991)
Cotesia marginiventrisi i lHost infested plant, plant–host complex Cortesero et al. (1997); Turlings et al. (1989)
Exeristes roborator     Artificial cues (l)Wardle & Borden (1989)
Habrobracon hebetori    Host faecesParra et al. (1996), Shonouda & Nasr (1998)
Harmonia axyridisi i  Aphids, leafsObata (1986)
Lariophagus distinguendusi (g, s) i, l  Host faeces (g), host pheromone (i), host infested seedsSteidle & Schöller (1997); Steidle et al. (2001); Steidle et al. (2003)
Orius tristicolor    i (s)Host complex (i)VanLaerhoven et al. (2000)
Pimpla turionellaei    Host cuesSandlan (1980)
Pholetesor bicolor  i  Squalene from host infested plant (i)Dutton et al. (2000)
Trichogramma chilonisi (s) i (g)  Host pheromone (i), host faeces volatile isothiocyanate (i), GLVs (i), sorghum volatiles (i)Reddy et al. (2002); Romeis et al. (1997)
Trichogramma brassicaei (g), l    Host sex pheromone, host egg extract and hydrocarbons, ethylpalmitate, palmitic acid from host egg extract (i), host cues (l)Renou et al. (1989), (1992); Kaiser et al. (1989)
Trichogramma evanescensl, i (s)    M. brassicae-sexpheromone (i); sexpheromone compound (Z, E)- 9,12-tetra-decenylacetate (l)Noldus et al. (1991); Schöller & Prozell (2002)
Cataglyphis fortis     InfochemicalsWolf & Wehner (2000)
Chiracanthium mildeix    Trimedlure, Ceratitis capitata-malesKaspi (2000)
Geocoris pallens  x  Prey infested Nicotiana plantKessler & Baldwin (2001)
Harpalus rufipes     E-(β)-farneseneKielty et al. (1996)
Myrmica rubras    Faecal shield from Cassida spec.Müller & Hilker (1999)
Nebria brevicollisx    Collembola (prey)Kielty et al. (1996)
Podisus maculiventris  x (g)  GLV, linalool, nonanal, MeSaDickens (1999)
Pterostíchus melanariusx (g) x  E-(β)-farnesene, aphids, Collembola, cabbage, wheat, clover Tréfás et al. (2001); Kielty et al. (1996)
Vespula germanicas    C. capitata-pheromoneHendrichs et al. (1994)

Using literature data for testing hypotheses is a critical issue, for instance, scientists tend to publish only positive data. To justify this approach, our reasoning is given below. From all studies available on the infochemical use of carnivore species, only a part was suitable to be included into this comparative review. Many studies had to be discarded, for instance because no attention was paid to the experience of the tested carnivores. We assume that the carnivore species examined in the selected studies are representative for carnivores of their respective groups (A, C, or D). Furthermore, we assume that the proportion of species for which a certain trait, for example, has been studied is equal in all groups. Then, the frequency of a trait found (and published) within the selected studies of this group should be representative for the proportion of this trait within the whole group. Consequently, if the frequency of a specific trait is equal in all groups, the proportion of species for which this trait has been demonstrated should be similar. If, however, a specific trait was found more often in the selected studies of one group, this demonstrates that this trait is more frequent in this group. The frequency of the different traits in the three groups was statistically analysed using 2 × 3 and 2 × 2 Chi-squared tables. Thereby, the number of species for which a trait has been demonstrated was compared to the number of remaining species from this group.

Testing the concept

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

No infochemical use in extreme generalists

Whereas the orientation to infochemical cues from host/prey complexes is an adaptive strategy for carnivores with a restricted diet breadth, a number of theoretical considerations suggest infochemical use is much less likely in extreme generalists from group D. First, generalists need to invest less time in searching particular host and prey species than specialists, therefore the use of infochemicals in order to reduce searching time is less important. Furthermore, when host/prey species are randomly or regularly distributed, random search might be more adaptive than to rely on a diverse array of infochemicals. Finally, many different host/prey complexes will represent a great diversity of specific cues. Sensory perception and processing of such a wide array of compounds will be subject to physiological constraints.

In contrast to the prediction, however, infochemical use was found in 29 carnivore species from group D (Table 7). These include not only species with a relatively narrow host range where the conditions mentioned might not (yet) be very pronounced, but also extreme generalists like ants, carabid beetles, spiders, coccinellids, and predatory bugs. This indicates that the use of infochemicals for foraging is an adaptive strategy regardless of dietary specialization and that physiological constraints on sensory processing in generalists might be less severe than supposed. Honeybees, which are generalist foragers of flowers from many families, can perceive numerous chemical cues (e.g., Laloi et al., 1999; Laska & Galizia, 2001), demonstrating that insects are capable of dealing with a large variety of chemicals. The ‘neural constraints’ hypothesis proposed for herbivores, however, assumes that physiological constraints on processing of a variety of infochemical cues would result in the evolution of specialized host range (Bernays, 1998). One reason for the use of infochemicals in generalist carnivores could be that most host/prey species probably have an aggregated instead of a random or regular distribution, because patchiness is the most common pattern of distribution for organisms in general (Begon et al., 1996). This makes random search less adaptive and favours directed search strategies. Consequently, in many cases the use of infochemicals should be more adaptive than the use of other cues. Chemical cues are more persistently released than sound and, as compared to optical cues, they are more traceable over larger distances and when host/prey species are hidden. In addition to these general advantages, several other reasons might explain the use of infochemicals for particular generalist species.

In some cases, general cues indicating the presence of various, non-related host/prey complexes might be much more common than assumed. At least seven of the 29 generalists from Table 7 have been shown to react to plant volatiles. When subject to feeding damage, plants change their pattern of volatile emission. The amount of green leaf volatiles, a group of C6 alcohols, acetates, aldehydes, and ketones, is increased upon damage, as is the release of certain mono- and sesquiterpenoids e.g., farnesene and linalool (Rutledge, 1996; Dicke & Vet, 1999; Kessler & Baldwin, 2001; van Loon & Dicke, 2001). Green leaf volatiles constitute a well-detectable signal, representing a group of general chemicals that indicate the presence of actively feeding potential prey (Dickens, 1999).

  • For several carnivores these innate responses could be the ‘ghost of monophagy’, i.e., behavioural relicts from monophagous ancestors of the extant species, which evolved into generalists, as discussed for the generalist parasitoid Lariophagus distinguendus by Steidle et al. (2003). Note that this would indicate the evolution of generalists out of specialists in contrast to the common assumption that specialization would be an evolutionary dead end (Termonia et al., 2001).

  • Certain species might in fact be specialized on certain prey/host complexes and only occasionally attack other host/prey species. These marginal hosts would cause them to be categorized as generalists. For these species the innate use of host/prey-specific cues would not be unexpected.

  • As discussed in more detail below, some species might consist of different, sometimes even sympatric, subpopulations, which are specialized on different hosts or prey species.

  • Finally, for a species like the polyphagous ant Cataglyphis fortis living in desert habitats almost completely devoid of odours, the reaction to any chemical cue might be a very efficient way to locate food sources.

Specialists should use specific cues and generalists should use general cues

Specialist carnivores focus on single or a few host/prey species, therefore only they should react to infochemical cues that are specific for their host/prey complex. Generalists, on the other hand, are assumed to make use of general cues, released by all their different host/prey complexes. This prediction is most difficult to scrutinize, because it requires the identification of the cues. Specific cues are relatively easy to identify in those cases where species-specific pheromones are used as kairomones. The use of general cues, however, not only requires identification but also extensive comparative studies between host/prey complexes. In accordance with the concept, literature data indicate a lower frequency of making use of specific cues from group A and C to group D, with a significant difference between C and D (Table 2). Although the use of general cues was only demonstrated in a few cases, it occurs significantly more often in group D than in groups A and C, supporting the hypothesis that general cues are mostly used by generalists.

Innate use of infochemicals should occur in specialists but not in generalists

The innate use of infochemicals by carnivores during foraging is predicted to occur when these chemicals reliably indicate the presence of host or prey species between and within carnivore generations (Stephens, 1993). This is the case for carnivores from group A that are specialized on the level of the host/prey species and the host plants/feeding substrates. Thus, a congenitally fixed response to cues from both levels is expected for these species. The reliance on innate use should be less pronounced with increasing diet breadth, because the spatiotemporal occurrence of specific infochemicals is expected to be less predictable and the diversity of infochemicals might cause physiological constraints on sensory processing that prevent congenitally fixed reactions to these cues. Data from the literature do not support these predictions. An innate reaction to infochemical cues from host plant/feeding substrate and the whole host/prey complex was found in many cases in the generalist groups C and D, respectively. The percentage of species that are innately reacting to infochemicals is only slightly and not significantly decreasing from 100% in group A to 80% in group D (Table 3).

The reason for this difference between predictions and observations could lay in the fact that the use of infochemical cues seems to be superior over random search as indicated above. Thus, freshly emerged naive generalist carnivores may need a basic set of cues to which they respond innately in order to prevent exclusive reliance on random search during their first foraging activities. In addition, some of the explanations given above for the infochemical use in generalists might also apply here. Physiological constraints might be less severe then assumed or species might have evolved from monophagous ancestors. Furthermore, some species in the generalist groups C and D might in fact consist of complexes of different populations or strains, each specialized on certain herbivores feeding on certain host plants. This scenario was discussed to explain the innate reaction to specific cues in the aphid parasitoid A. ervi (Guerrieri et al., 1993), which was included in category C. Finally, for some species the reaction to these cues might have not been innate as assumed. Carnivores could have learned to react to these cues during larval stage or during emergence from their hosts (van Emden et al., 1996). According to the definition for naive insects used in our study (see above), reactions that have been learned by larvae or during emergence of adults are considered innate. So far, however, memory transfer from larval to adult stage has not been demonstrated in insect carnivores (van Emden et al., 1996).

Another prediction, stating that the relative importance of innately recognized cues from both lower trophic levels depends on the dietary breadth of the top level, cannot be tested because too few cases of group B are documented. Between the other three groups, the proportion of species innately using infochemicals from the host/prey, the host plant/feeding substrate, and the whole host/prey complex is not statistically different.

Learning of infochemicals is expected in generalist carnivores and not in specialists

Learning to react to infochemicals associated with the presence of host or prey species is considered an adaptive strategy especially for those carnivores living in an environment where availability of host/prey species and their host plants/feeding substrate is subject to temporal variability. Thus, learning behaviour is expected in generalist carnivores confronted with variable availability of host/prey species within and between generations, whereas this would have little adaptive value in specialists. This prediction is confirmed by literature data. Learning has been demonstrated for only a few species from group A, but for almost half of the species from groups C and D (Table 4). Most species from groups A and C are parasitoids. We believe that this significant difference reflects the natural situation and is not caused by preferences of researchers for species from group C, because learning behaviour is a much studied subject in parasitoid biology.

Interestingly, in group C, most carnivores learned to react to cues originating from the plant/feeding substrate but only four learned to react to host/prey cues. This is in agreement with the fact that species from group C are specialists on the host/prey level and generalists on the level of the plant/feeding substrate. It is unclear, however, whether this reflects a natural phenomenon or is caused by more intense research on the learning of plant/feeding substrate cues as compared to host/prey cues.

Modification of the concept based on the available literature

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

Results from the present literature study confirm some predictions of the concept of dietary specialization as articulated by Vet & Dicke (1992), and fail to support others. In accordance with the concept, the use of general host and host plant cues and learning to react to infochemicals was found more frequently in generalists than in specialists. In addition, specialist species were found to use specific cues more frequently than generalist species. In contrast to the concept, however, specific infochemical cues are used by quite a number of generalists and there was no difference between specialists and generalists in the frequency of an innate response to these cues. Moreover, extreme generalists were shown to use infochemical cues for foraging. Thus, according to the current literature the use of infochemicals during foraging behaviour, including an innate reaction to infochemicals, seems to be adaptive for carnivores in general, regardless of dietary specialization. Potential explanations are discussed above. Consequently, we suggest rephrasing the predictions made above for groups A, C, and D as follows (Figure 2):

image

Figure 2. Modification of the concept of dietary specialization and infochemical use in carnivores according to the present literature. The width of the bars below each carnivore-system represents the importance of the respective trait for the tritrophic system.

Download figure to PowerPoint

  • 1
    All carnivores use infochemicals for foraging regardless of dietary specialization.
  • 2
    Specialists more frequently use specific cues and generalists more frequently use general cues.
  • 3
    The innate use of infochemicals occurs in all carnivores regardless of specialization.
  • 4
    Learning of infochemicals for foragimg occurs frequently in generalist carnivores and rarely in specialists.

A graphical representation of these statements is given in Figure 2, depicting a smooth continuum from specialists to generalists rather than the existence of distinct categories.

Prospects

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References

Almost no studies have been devoted to carnivores belonging to group B. Evidently, future studies of this group would allow for a comparative assessment of the relative importance of innate and specific cues from host/prey or host plant/feeding substrate in all carnivore groups. Furthermore, for a more rigorous evaluation of the concept more information is needed on the following aspects: (1) the frequency of occurrence of learning behaviour of generalist predators, (2) relative importance of cues from different trophic levels, (3) the population structure of generalist carnivores (especially the possible occurrence of more specialized subpopulations or subspecies), and (4) the specificity or generality of infochemical cues employed by carnivores (Dicke, 1999). As has been argued by Vet & Dicke (1992), the assessment of the precise host or prey range of carnivores is liable to inherent uncertainties, posing constraints on studying aspect (3). Here we employed definitions of specialism and generalism for carnivores that are accepted in the literature on herbivores to enable the distinction of four categories. Concerning aspect (4), rigorous testing strongly depends on efforts in analytical chemistry. Demonstration that an infochemical is specific to a particular plant or herbivore species is mostly accepted when the infochemical is not found in closely related plant or herbivore species, although it cannot be excluded that it occurs in unrelated species. Research into aspects (1) and (2) is relatively straightforward and particularly studies on generalist predators might provide us with new insights.

Infochemicals play an important role in the interactions between organisms, therefore a full understanding of infochemical use by carnivores is expected to contribute to a better knowledge of the evolution and functioning of ecological food webs. Furthermore, this information can be crucial for the use of natural enemies in biological control. When exotic parasitoids and predators are considered for introduction in classical biological control measures, host range studies are required to ensure that only pest species are affected and to exclude impact on non-target organisms (e.g., Simberloff & Stiling, 1996; Boettner et al., 2000). It is mostly impossible, however, to study whether all potential non-target organisms are accepted as hosts or prey. Alternatively, studies on the infochemical use of the respective natural enemy species might be used for risk assessment. Attack of non-target organisms is less likely if natural enemies are innately using infochemicals that are specific for the host/prey complex of the pest organism and if learning of infochemicals is absent. As demonstrated in this study these conditions are met by specialists and not by generalists. This is in line with the postulation that generalist natural enemies should not be used in classical biological control (e.g., Nechols et al., 1992).

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. The concept of dietary specialization and infochemical use in natural enemies
  5. Database
  6. Testing the concept
  7. Modification of the concept based on the available literature
  8. Prospects
  9. References
  • Agelopoulos NG & Keller MA (1994) Plant–natural enemy association in the tritrophic system, Cotesia rubecula-Pieris rapae– Brassicaceae (Cruciferae). I. Sources of infochemicals. Journal of Chemical Ecology 20: 17251734.
  • Al-Abassi S, Birkett MA, Petterson J, Pickett JA, Wadhams LJ & Woodcock CM (2000) Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. Journal of Chemical Ecology 26: 17651771.
  • Arthur AP (1971) Associative learning by Nemeritis canescens (Hymenoptera: Ichneumonidae). Canadian Entomologist 103: 11371141.
  • Auger J, Lecomte C, Paris J & Thibout E (1989) Identification of leek-moth and diamondback-moth frass volatiles that stimulate parasitoid, Diadromus pulchellus. Journal of Chemical Ecology 15: 13911398.
  • Van Baarlen P, Topping CJ & Sunderland KD (1996) Host location by Gelis festinans, an eggsac parasitoid of the linyphiid spider Erigone atra. Entomologia Experimentalis et Applicata 81: 155163.
  • Bargen H, Saudhof K & Poehling HM (1998) Prey finding by larvae and adult females of Episyrphus balteatus. Entomologia Experimentalis et Applicata 87: 245254.
  • Begon ME, Harper JL & Townsend CR (1996) Ecology, 3rd edn. Blackwell Publishing, Oxford.
  • Benrey B, Denno RF & Kaiser L (1997) The influence of plant species on attraction and host acceptance in Cotesia glomerata (Hymenoptera: Braconidae). Journal of Insect Behavior 10: 619630.
  • Bernays EA (1998) The value of being a resource specialist: Behavioral support for a neural hypothesis. American Naturalist 151: 451464.
  • Bernays EA & Chapman RF (1994) Host-Plant Selection by Phytophagous Insects. Chapman & Hall, New York.
  • Boettner GH, Elkinton JS & Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conservation Biology 14: 17981806.
  • Brown PE & Anderson M (1999) Factors affecting ovipositor probing in Trybliographa rapae, a parasitoid of the cabbage root fly. Entomologia Experimentalis et Applicata 93: 217225.
  • Budenberg WJ & Powell W (1992) The role of honeydew as an ovipositional stimulant for two species of syrphids. Entomologia Experimentalis et Applicata 64: 5761.
  • Colazza S, Rosi MC & Clemente A (1997) Response of egg parasitoid Telenomus busseolae to sex pheromone of Sesamia nonagrioides. Journal of Chemical Ecology 23: 24372444.
  • Colazza S, Salerno G & Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biological Control 16: 310317.
  • Cortesero AM, De Moraes CM, Stapel JO, Tumlinson JH & Lewis WJ (1997) Comparisons and contrasts in host-foraging strategies of two larval parasitoids with different degrees of host specificity. Journal of Chemical Ecology 23: 15891606.
  • Cortesero AM, Monge JP & Huignard J (1995) Influence of two successive learning processes on the response of Eupelmus Vuilleti Crw (Hymenoptera: Eupelmidae) to volatile stimuli from hosts and host plants. Journal of Insect Behavior 8: 751762.
  • Cortesero AM, Monge JP & Huignard J (1993) Response of the parasitoid Eupelmus vuilleti to the odours of the phytophagous host and its host plant in an olfactometer. Entomologia Experimentalis et Applicata 69: 109116.
  • Coupland JB (1996) Influence of snail feces and mucus on oviposition and larval behavior of Pherbellia cinerella (Diptera: Sciomyzidae). Journal of Chemical Ecology 22: 183189.
  • Couty A, Kaiser L, Huet D & Pham Delegue MH (1999) The attractiveness of different odour sources from the fruit–host complex on Leptopilina boulardi, a larval parasitoid of frugivorous Drosophila spp. Physiological Entomology 24: 7682.
  • De Jong R & Kaiser L (1991) Odor learning by Leptopilina boulardi, a specialist parasitoid (Hymenoptera: Eucoilidae). Journal of Insect Behavior 4: 743750.
  • DeLury NC, Gries R, Gries G, Judd GJR & Khaskin G (1999) Moth scale-derived kairomones used by egg-larval parasitoid Ascogaster quadridentata to locate eggs of its host, Cydia pomonella. Journal of Chemical Ecology 25: 24192431.
  • Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomologia Experimentalis et Applicata 91: 131142.
  • Dicke M, Van Lenteren JC, Boskamp GJF & Van Dongen LE (1984) Chemical stimuli in host-habitat location by Leptopilina heteroma (Thomson) (Hymenoptera: Eucoilidae), a parasite of Drosophila. Journal of Chemical Ecology 10: 695712.
  • Dicke M & Vet LEM (1999) Plant–carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore. Herbivores: Between Plants and Predators (ed. by HOlff, VKBrown & RHDrent), pp. 483520. Blackwell Science, Oxford.
  • Dickens JC (1999) Predator–prey interactions: olfactory adaptations of generalist and specialist predators. Agricultural and Forest Entomology 1: 4754.
  • Drost YC & Cardé RT (1992) Host switching in Brachymeria intermedia (Hymenoptera: Chalcididae), a pupal endoparasitoid of Lymantria dispar (Lepidoptera: Lymantriidae). Environmental Entomology 21: 760766.
  • Drukker B, Bruin J & Sabelis MW (2000) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiological Entomology 25: 260265.
  • Du YJ, Poppy GM & Powell W (1996) Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. Journal of Chemical Ecology 22: 15911605.
  • Du YJ, Poppy GM, Powell W & Wadhams LJ (1997) Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). Journal of Insect Behavior 10: 509522.
  • Duan JJ & Messing RH (2000) Effects of host substrate and vibration cues on ovipositor-probing behavior in two larval parasitoids of tephritid fruit flies. Journal of Insect Behavior 13: 175186.
  • Dutton A, Mattiacci L & Dorn S (2000) Plant-derived semiochemicals as contact host location stimuli for a parasitoid of leafminers. Journal of Chemical Ecology 26: 22592273.
  • Dwumfour EF (1992) Volatile substances evoking orientation in the predatory substances evoking orientation in the predatory flowerbug Anthocoris-nemorum (Heteroptera, Anthocoridae). Bulletin of Entomological Research 82: 465469.
  • Eben A, Benrey B, Sivinski J & Aluja M (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 29: 8794.
  • Eller FJ, Tumlinson JH & Lewis WJ (1988a) Beneficial arthropod behavior mediated by airborne semiochemicals: source of volatiles mediating the host-location flight behavior of Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), a parasitoid of Heliothis zea (Boddie) (Lepidoptera: Noctuidae). Environmental Entomology 17: 745753.
  • Eller FJ, Tumlinson JH & Lewis WJ (1988b) Beneficial arthropod behavior mediated by airborne semiochemicals. II. Olfactometric studies of host location by the parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). Journal of Chemical Ecology 14: 425434.
  • Eller FJ, Tumlinson JH & Lewis WJ (1992) Effect of host diet and pre-flight experience on the flight responses of Microplitis croceipes (Cresson). Physiological Entomology 17: 235240.
  • Van Emden HF, Sponagl B, Wagner E, Baker T, Ganguly S & Douloumpaka S (1996) Hopkins’‘host selection principle’, another nail in its coffin. Physiological Entomology 21: 325328.
  • Fukushima J, Kainoh Y, Honda H & Takabayashi J (2002) Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. Journal of Chemical Ecology 28: 579586.
  • Geervliet JBF, Vreugdenhil AI, Dicke M & Vet LEM (1998) Learning to discriminate between infochemicals from different plant–host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomologia Experimentalis et Applicata 86: 241252.
  • Glinwood RT, Du YJ & Powell W (1999a) Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi. Entomologia Experimentalis et Applicata 92: 227232.
  • Glinwood RT, Du YJ, Smiley DWM & Powell W (1999b) Comparative responses of parasitoids to synthetic and plant-extracted nepetalactone component of aphid sex pheromones. Journal of Chemical Ecology 25: 14811488.
  • Grasswitz TR (1998) Effect of adult experience on the host-location behavior of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Biological Control 12: 177181.
  • Grasswitz TR & Paine TD (1992) Kairomonal effect of an aphid cornicle secretion on Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphididae). Journal of Insect Behavior 5: 447457.
  • Grasswitz TR & Paine TD (1993a) Effect of experience on in-flight orientation to host-associated cues in the generalist parasitoid Lysiphlebus testaceipes. Entomologia Experimentalis et Applicata 68: 219229.
  • Grasswitz TR & Paine TD (1993b) Influence of physiological-state and experience on the responsiveness of Lysiphlebus testaceipes (Cresson) (Hymenoptera, Aphidiidae) to aphid honeydew and to host plants. Journal of Insect Behavior 6: 511528.
  • Guerrieri E (1997) Flight behaviour of Encarsia formosa in response to plant and host stimuli. Entomologia Experimentalis et Applicata 82: 129133.
  • Guerrieri E, Pennacchio F & Tremblay E (1993) Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. European Journal of Entomology 90: 415421.
  • Havill NP & Raffa KF (2000) Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions. Ecological Entomology 25: 171179.
  • Hedlund K, Vet LEM & Dicke M (1996) Generalist and specialist parasitoid strategies of using odours of adult drosophilid flies when searching for larval hosts. Oikos 77: 390398.
  • Hendrichs J, Katsoyannos BI, Wornoayporn V & Hendrichs MA (1994) Odour-mediated foraging by yellowjacket wasps (Hymenoptera: Vespidae): predation on leks of pheromone-calling mediterranean fruit fly males (Diptera: Tephritidae). Oecologia 99: 8894.
  • Hendry LB, Greany PD & Gill RJ (1973) Kairomone mediated host-finding behavior in the parasitic wasp Orgilus lepidus. Entomologia Experimentalis et Applicata 16: 471477.
  • Henson RD, Vinson SB & Barfield CS (1977) Ovipositional behaviour of Bracon mellitor Say, a parasitoid of the boll weevil (Anthonomus grandis Boheman). III. Isolation and identification of natural releasers of ovipositor probing. Journal of Chemical Ecology 3: 151158.
  • Hilker M, Blaske V, Kobs C & Dippel C (2000) Kairomonal effects of sawfly sex pheromones on egg parasitoids. Journal of Chemical Ecology 26: 25912601.
  • Hoffmeister TS & Gienapp P (1999) Exploitation of the host's chemical communication in a parasitoid searching for concealed host larvae. Ethology 105: 223232.
  • Honda T, Kainoh Y & Honda H (1998) Enhancement of learned response to plant chemicals by the egg–larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Applied Entomology and Zoology 33: 271276.
  • Honda JY & Walker GP (1996) Olfactory response of Anagrus nigriventris (Hym. Mymaridae): effects of host plant chemical cues mediated by rearing and oviposition experience. Entomophaga 41: 313.
  • Van Huis A, Schütte C, Cools MH, Fanget P, Van Der Hoek H & Piquet SP (1994) The role of semiochemicals in host location by Uscana lariophaga, egg parasitoid of Callosobruchus maculatus. Proceedings of the 6th International Working Conference on Stored-Product Protection (ed. by EHighley), pp. 11581164. CAB International, Montpellier/Canberra.
  • Jang EB, Messing RH, Klungness LM & Carvalho LA (2000) Flight tunnel responses of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) to olfactory and visual stimuli. Journal of Insect Behavior 13: 525538.
  • Kainoh Y & Tamaki Y (1982) Searching behavior and oviposition of the egg-larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Applied Entomology and Zoology 17: 194206.
  • Kainoh Y & Tatsuki S (1988) Host egg kairomones essential for egg–larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). 1. Internal and external kairomones. Journal of Chemical Ecology 14: 14751484.
  • Kaiser L & Cardé RT (1992) In-flight orientation to volatiles from the plant–host complex in Cotesia rubecula (Hym. Braconidae): increased sensitivity through olfactory experience. Physiological Entomology 17: 6267.
  • Kaiser L, Pham Delegue MH, Bakchine E & Masson C (1989) Olfactory responses of Trichogramma maidis Pint et Voeg – Effects of chemical cues and behavioral plasticity. Journal of Insect Behavior 2: 701712.
  • Kaspi R (2000) Attraction of female Chiracanthium mildei (Araneae: Clubionidae) to olfactory cues from male Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae). Biocontrology 45: 463468.
  • Kerguelen V & Cardé RT (1996) Reinforcement mechanisms of olfactory conditioning during parasitization by the parasitoid Brachymeria intermedia (Hymenoptera: Chalcididae). Journal of Insect Behavior 9: 947960.
  • Kessler A & Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 21412144.
  • Kester KM & Barbosa P (1991) Postemergence learning in the insect parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae). Journal of Insect Behavior 4: 727742.
  • Kielty JP, Allen Williams LJ, Underwood N & Eastwood EA (1996) Behavioral responses of three species of ground beetle (Coleoptera: Carabidae) to olfactory cues associated with prey and habitat. Journal of Insect Behavior 9: 237250.
  • Kopf A, Rank NE, Roininen H & Tahvanainen J (1997) Defensive larval secretions of leaf beetles attract a specialist predator Parasyrphus nigritarsis. Ecological Entomology 22: 176183.
  • Laloi D, Roger B, Blight MM, Wadhams LJ & Pham-Delegue MH (1999) Individual learning ability and complex odor recognition in the honey bee, Apis mellifera L. Journal of Insect Behavior 12: 585597.
  • Laska M & Galizia CG (2001) Enantioselectivity of odor perception in honeybees (Apis mellifera carnica). Behavioral Neuroscience 115: 632639.
  • Lill JT, Marquis RJ & Ricklefs RE (2002) Host plants influence parasitism of forest caterpillars. Nature 417: 170173.
  • Van Loon JJA & Dicke M (2001) Sensory ecology of arthropods utilizing plant infochemicals. Ecology of Sensing (ed. by FGBarth & ASchmid), pp. 253270. Springer Verlag, Berlin.
  • Mattiacci L & Dicke M (1995) The parasitoid Cotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its host Pieris brassicae, on the basis of contact cues from frass, silk, and herbivore-damaged leaf tissue. Journal of Insect Behavior 8: 485498.
  • McAuslane HJ, Vinson SB & Williams HJ (1991a) Influence of adult experience on host microhabitat location by the generalist parasitoid, Campoletis sonorensis (Hymenoptera: Ichneumonidae). Journal of Insect Behavior 4: 101113.
  • McAuslane HJ, Vinson SB & Williams HJ (1991b) Stimuli influencing host microhabitat location in the parasitoid Campoletis sonorensis. Entomologia Experimentalis et Applicata 58: 267277.
  • McCall PJ, Turlings TCJ, Lewis WJ & Tumlinson JH (1993) Role of plant volatiles in host location by the specialist parasitoid Microplitis croceipes Cresson (Braconidae: Hymenoptera). Journal of Insect Behavior 6: 625639.
  • McGregor R & Henderson D (1998) The influence of oviposition experience on response to host pheromone in Trichogramma sibiricum (Hymenoptera: Trichogrammatidae). Journal of Insect Behavior 11: 621632.
  • Meiners T, Kopf A, Stein C & Hilker M (1997) Chemical signals mediating interactions between Galeruca tanaceti L. (Coleoptera, Chrysomelidae) and its egg parasitoid Oomyzus galerucivorus (Hedqvits) (Hymenoptera, Eulophidae). Journal of Insect Behavior 10: 523539.
  • Meiners T, Westerhaus C & Hilker M (2000) Specificity of chemical cues used by a specialist egg parasitoid during host location. Entomologia Experimentalis et Applicata 95: 151159.
  • Messing RH & Jang EB (1992) Response of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to host-fruit stimuli. Environmental Entomology 21: 11891195.
  • Micha SG (1995) Die Bedeutung von Semiochemikalien im tritrophischen System aus Hafer (Avena sativa), Große Getreideblattlaus (Sitobion avenae) und Blattlausparasitoid (Aphidius uzbekistanikus). PhD-thesis, Christian-Albrechts Universität, Kiel.
  • Micha SG & Wyss U (1996) Aphid alarm pheromone (E)-beta-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7: 132139.
  • Mölck G, Micha SG & Wyss U (1999) Attraction to odour of infested plants and learning behaviour in the aphid parasitoid Aphelinus abdominalis. Zeitschrift Fur Pflanzenkrankheiten und Pflanzenschutz 106: 557567.
  • Morgan David JW & Hare JD (1998) Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited. Entomologia Experimentalis et Applicata 88: 235245.
  • Mudd A & Corbet SA (1982) Response of the ichneumonid parasite Nemeritis canescens to kairomones from the flour moth, Ephestia kuehniella. Journal of Chemical Ecology 8: 843850.
  • Müller C & Hilker M (1999) Unexpected reactions of a generalist predator towards defensive devices of cassidine larvae (Coleoptera, Chrysomelidae). Oecologia 118: 166172.
  • Nechols JR, Kauffman WC & Schaefer PW (1992) Significance of host specificity in classical biological control. Selection Criteria and Ecological Consequences of Importing Natural Enemies (ed. by W CKauffman & JRNechols), pp. 4152. Thomas Say Symposia Proceedings Series, Entomological Society of America, Landham, MD, USA.
  • Nemoto T, Shibuya M, Kuwahara Y & Suzuki T (1987) New 2-acylcyclohexane-1,3-diones: kairomone components against a parasitic wasp, Venturia canescens, from feces of the almond moth, Cadra cautella, and the Indian meal moth, Plodia interpunctella. Agricultural Biology and Chemistry 51: 18051810.
  • Noldus LP, Potting RPJ & Barendregt HE (1991) Moth sex pheromone adsorption to leaf surface: bridge in time for chemical spies. Physiological Entomology 16: 329344.
  • Obata S (1986) Mechanisms of prey finding in the aphidophagous ladybird beetle, Harmonia-axyridis[Coleoptera, Coccinellidae]. Entomophaga 31: 303311.
  • Parra JRP, Vinson SB, Gomes SM & Consoli FL (1996) Flight response of Habrobracon hebetor (Say) (Hymenoptera: Braconidae) in a wind tunnel to volatiles associated with infestations of Ephestia kuehniella ZELLER (Lepidoptera: Pyralidae). Biological Control 6: 143150.
  • Pettersson EM (2001) Volatile attractants for three Pteromalid parasitoids attacking concealed spruce bark beetles. Chemoecology 11: 8995.
  • Pettersson EM, Birgersson G & Witzgall P (2001) Synthetic attractants for the bark beetle parasitoid Coeloides bostrichorum Giraud (Hymenoptera: Braconidae). Naturwissenschaften 88: 8891.
  • Petitt FL, Turlings TCJ & Wolf SP (1992) Adult experience modifies attraction of the leafminer parasitoid Opius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals. Journal of Insect Behavior 5: 623634.
  • Potting RPJ, Poppy GM & Schuler TH (1999) The role of volatiles from cruciferous plants and pre-flight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae. Entomologia Experimentalis et Applicata 93: 8795.
  • Reddy GVP, Holopainen JK & Guerrero A (2002) Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. Journal of Chemical Ecology 28: 131143.
  • Reed HC, Tan SH, Haapanen K, Killmon M, Reed DK & Elliott NC (1995) Olfactory responses of the parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) to odor of plants, aphids, and plant–aphid complexes. Journal of Chemical Ecology 21: 407418.
  • Renou M, Hawlitzky N, Berthier A, Malosse C & Ramiandrasoa F (1989) Evidence of a kairomonal activity from eggs of the European corn borer on females of Trichogramma maidis. Entomophaga 34: 569580.
  • Renou M, Nagnan P, Berthier A & Durier C (1992) Identification of compounds from the eggs of Ostrinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae. Entomologia Experimentalis et Applicata 63: 291303.
  • Romeis J, Shanower TG & Zebitz CPW (1997) Volatile plant infochemicals mediate plant preference of Trichogramma chilonis. Journal of Chemical Ecology 23: 24552465.
  • Rostas M, Dippel C & Hilker M (1997) Chemical and physical signals mediating the parasitization of cocoons of the European spruce sawfly Gilpinia hercyniae by the wasp Dahlbominus fuscipennis Zett. Mitteilungen Deutsche Gesellschaft für Allgemeine und Angewandte Entomologie 11: 537540.
  • Rutledge CE (1996) A survey of identified kairomones and synomones used by insect parasitoids to locate and accept their hosts. Chemoecology 7: 121131.
  • Sandlan K (1980) Host location by Coccygonimus turionellae (Hymenoptera: Ichneumonidae). Entomologia Experimentalis et Applicata 27: 233245.
  • Schaffner U & Müller C (2001) Exploitation of the fecal shield of the lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae), by the specialist parasitoid Lemophagus pulcher (Hymenoptera: Ichneumonidae). Journal of Insect Behavior 14: 739757.
  • Scholler M & Prozell S (2002) Response of Trichogramma evanescens to the main sex pheromone component of Ephestia spp. and Plodia interpunctella, (Z,E)-9,12-tetra-decadenyl acetate (ZETA). Journal of Stored Products Research 38: 177184.
  • Sheehan W & Shelton AM (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae). Journal of Insect Behavior 2: 743759.
  • Shonouda ML, Bombosch S, Shalaby AM & Osman SI (1998) Biological and chemical characterization of a kairomone excreted by the bean aphids, Aphis fabae Scop. (Hom., Aphididae), and its effect on the predator Metasyrphus corollae Fabr. II. Behavioural response of the predator M. corollae to the aphid kairomone. Journal of Applied Entomology 122: 2528.
  • Shonouda ML, Bombosch S, Shalaby AM & Osman SI (1998) Biological and chemical characterization of a kairomone excreted by the bean aphids, Aphis fabae Scop. (Hom., Aphididae) and its effect on the predator Metasyrphus corollae Fabr. I. Isolation, identification and bioassay of aphid-kairomone. Journal of Applied Entomology 122: 1524.
  • Shonouda ML & Nasr FN (1998) Impact of larval-extract (kairomone) of Ephestia kuehniella Zell. (Lep., Pyralidae), on the behaviour of the parasitoid Bracon hebetor Say. (Hym., Braconidae). Journal of Applied Entomology 122: 3335.
  • Simberloff D & Stiling P (1996) How risky is biological control? Ecology 77: 19651974.
  • Souissi R (1999) The influence of the host plant of the cassava mealybug Phenacoccus manihoti on the plant and host preferences of its parasitoid Apoanagyrus lopezi. Biological Control 15: 6470.
  • Souissi Ra & Le Ru B (1999) Behavioural responses of the endoparasitoid Apoanagyrus lopezi to odours of the host and host's cassava plants. Entomologia Experimentalis et Applicata 90: 215220.
  • Souissi Ra, Nenon JP & Le Ru B (1998) Tritrophic interactions between host plants, the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Hom., Pseudococcidae) and its parasitoid Apoanagyrus lopezi De Santis (Hym., Encyrtidae). Journal of Applied Entomology 122: 561564.
  • Steidle JLM, Lanka J, Müller C & Ruther J (2001) The use of general infochemicals in a generalist parasitoid. Oikos 95: 7886.
  • Steidle JLM & Schöller M (1997) Olfactory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Journal of Insect Behavior 10: 331342.
  • Steidle JLM, Steppuhn A & Ruther J (2003) Specific foraging kairomones used by a generalist parasitoid. Journal of Chemical Ecology 29: 131143.
  • Steidle JLM & Van Loon JJA, (2002) Chemoecology of parasitoid and predator oviposition behaviour. Chemoecology of Insect Eggs and Egg Deposition (ed. by MHilker & TMeiners), pp. 291317. Blackwell Publishers, London.
  • Stephens DW (1993) Learning and behavioural ecology: Incomplete information and environmental predictability. Insect Learning (ed. by DRPapaj & ACLewis), pp. 195218. Chapman & Hall, New York.
  • Suiter DR, Carlson DA, Patterson RS & Koehler PG (1996) Host-location kairomone from Periplaneta americana (L.) for parasitoid Aprostocetus hagenowii (Ratzeburg). Journal of Chemical Ecology 22: 637651.
  • Takabayashi J, Sato Y, Horikoshi M, Yamaoka R, Yano S, Ohsaki N & Dicke M (1998) Plant effects on parasitoid foraging: differences between two tritrophic systems. Biological Control 11: 97103.
  • Takabayashi J & Takahashi S (1985) Host selection behavior of Anicetus beneficus Ishii et Yasumatsu (Hymenoptera: Encyrtidae). III. Presence of ovipositional stimulants in the scale wax of the genus Ceroplastes. Applied Entomology and Zoology 20: 173178.
  • Takabayashi J & Takahashi S (1989) Effects of host fecal pellet and synthetic kairomone on host-searching and post-oviposition behaviour of Apanteles kariyai, a parasitoid of Pseudaletia separata. Entomologia Experimentalis et Applicata 52: 221227.
  • Takacs S, Gries G & Gries R (1997) Semiochemical-mediated location of host habitat by Apanteles carpatus (Say) (Hymenoptera: Braconidae), a parasitoid of clothes moth larvae. Journal of Chemical Ecology 23: 459472.
  • Takahashi S, Hajika M, Takabayashi J & Fukui M (1990) Oviposition stimulants in the coccoid cuticular waxes of Aphytis yanonensis De Bach & Rosen. Journal of Chemical Ecology 16: 16571665.
  • Teerling CR, Gillespie DR & Borden JH (1993) Utilization of western flower thrips alarm pheromone as a prey-finding kairomone by predators. Canadian Entomologist 125: 431437.
  • Termonia A, Hsiao TH, Pasteels JM & Milinkovitch MC (2001) Feeding specialization and host derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end. Proceedings of the National Academy of Sciences 98: 39093914.
  • Tréfás H, Canning H, McKinlay RG, Armstrong G & Bujáki G (2001) Preliminary experiments on the olfactory responses of Pterostichus melanarius Illiger (Coleoptera: Carabidae) to intact plants. Agricultural and Forest Entomology 3: 7176.
  • Turlings TCJ, Tumlinson JH, Lewis WJ & Vet LEM (1989) Beneficial arthropod behaviour mediated by airborne semiochemicals. VIII. Learning of host-related odors induced by a brief contact experience with host by-products in Cotesia marginiventris (Cresson), a generalist larval parasitoid. Journal of Insect Behavior 2: 217225.
  • Udayagiri S & Jones RL (1992a) Flight behavior of Macrocentrus grandii Goidanich (Hymenoptera: Braconidae), a specialist parasitoid of European corn borer (Lepidoptera: Pyralidae): factors influencing response to corn volatiles. Environmental Entomology 21: 14481456.
  • Udayagiri S & Jones RL (1992b) Role of plant odor in parasitism of European corn borer by braconid specialist parasitoid Macrocentrus grandii Goidanich: isolation and characterization of plant synomones eliciting parasitoid flight response. Journal of Chemical Ecology 18: 18411855.
  • Udayagiri S & Jones RL (1993) Variation in flight response of the specialist parasitoid Macrocentrus grandii Goidanich to odours from food plants of its European corn borer host. Entomologia Experimentalis et Applicata 69: 183193.
  • VanLaerhoven S, Gillespie DR & McGregor RR (2000) Leaf damage and prey type determine search effort in Orius tristicolor. Entomologia Experimentalis et Applicata 97: 167174.
  • Vet LEM (1983) Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym, Eucoilidae), a parasitoid of fungivorous Drosophila– the influence of conditioning. Netherlands Journal of Zoology 33: 225248.
  • Vet LEM (1985) Olfactory microhabitat location in some Eucoilid and Alysiine species (Hymenoptera), larval parasitoids of Diptera. Netherlands Journal of Zoology 35: 720730.
  • Vet LEM (1985) Response to kairomones by some Alysiine and Eucoilid parasitoid species (Hymenoptera). Netherlands Journal of Zoology 35: 486496.
  • Vet LEM & Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37: 141172.
  • Vet LEM, Janse C, Van Achterberg C & Van Alphen JJM (1984) Microhabitat location and niche segregation in two sibling species of drosophilid parasitoids: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae). Oecologia 61: 182188.
  • Vet LEM, Lewis WJ, Papaj DR & Van Lenteren JC, (1990) A variable-response model for parasitoid foraging behavior. Journal of Insect Behavior 3: 471490.
  • Vet LEM & Papaj DR (1992) Effect of experience on parasitoid movement in odour plumes. Physiological Entomology 17: 9096.
  • Vet LEM & Schoonman G (1988) The influence of previous foraging experience on microhabitat acceptance in Leptopilina heterotoma. Journal of Insect Behavior 1: 387392.
  • Vet LEM & Van Opzeeland K (1984) The influence of conditioning on olfactory microhabitat and host location in Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae) larval parasitoids of Drosophilidae. Oecologia 63: 171177.
  • Vinson SB, Barfield CS & Henson RD (1977) Oviposition behaviour of Bracon mellitor, a parasitoid of the boll weevil (Anthonomus grandis). II. Associative learning. Physiological Entomology 2: 157164.
  • Vinson SB, Henson RD & Barfield CS (1976) Ovipositional behavior of Bracon mellitor Say (Hymenoptera: Braconidae), a parasitoid of boll weevil (Anthonomus grandis Boh.). I. Isolation and identification of a synthetic releaser of ovipositor probing. Journal of Chemical Ecology 2: 431440.
  • Wardle AR & Borden JH (1989) Learning of an olfactory stimulus associated with host microhabitat by Exeristes roborator. Entomologia Experimentalis et Applicata 52: 271279.
  • Weseloh RM (1974) Host recognition by the gypsy moth larval parasitoid, Apanteles melanoscelus. Annals of the Entomological Society of America 67: 583587.
  • Whitman DW & Eller FJ (1990) Parasitic wasps orient to green leaf volatiles. Chemoecology 1: 6975.
  • Wickremasinghe MGV & Van Emden HF (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from host plants of their aphid prey. Physiological Entomology 17: 297304.
  • Wiskerke JSC, Dicke M & Vet LEM (1993) Larval parasitoid uses aggregation pheromone of adult hosts in foraging behaviour: a solution to the reliability-detectability problem. Oecologia 93: 145148.
  • Wolf H & Wehner R (2000) Pinpointing food sources: Olfactory and anemotactic orientation in desert ants, Cataglyphis fortis. Journal of Experimental Biology 203: 857868.