Chem. Senses 28: 231-236,
2003
© Oxford University Press 2003
Associative Learning of Complex Odours in Parasitoid Host Location
1 Institut für Biologie, Freie Universität Berlin, Haderslebener Str. 9, D-12163 Berlin, Germany, 2 NIOO CTE, PO Box 40, 6666 ZG Heteren, The Netherlands 3 USDA-ARS-IBPMRL, PO Box 748, Tifton, GA 31793, USA
Correspondence to be sent to: Torsten Meiners, Angewandte Zoologie/Oekologie der Tiere, Haderslebener Str. 9, D-12163 Berlin, Germany. e-mail: meito{at}zedat.fu-berlin.de
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Abstract |
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In this paper we address the question how hymenopteran parasitoids deal with complex odour bouquets, using Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) as a model. We examined the capacity of Microplitis croceipes to respond to individual compounds in flight chamber experiments after conditioning parasitoids with a mixture consisting of 2-octanone, methyl jasmonate and ß-caryophyllene. Parasitoids were given a choice between single compounds from the training mixture and ß-ocimene as an unrewarded alternative. When compared with control individuals lacking experience with the odour mixture, parasitoids trained to the odour blend showed an increased preference for 2-octanone and ß-caryophyllene, but not for methyl jasmonate. However, when trained with methyl jasmonate alone, parasitoids were able to respond to this compound. This demonstrates that parasitoids can learn to respond to individual compounds following experience with an odour mixture. However, for certain compounds of a mixture, learning can be blocked by other mixture components. Further experiments in which parasitoids were conditioned and challenged with two compound mixes confirmed that the olfactory background can affect recognition of individual compounds.
Key words: background odour, complex blends, insect learning, mixture recognition, plant volatiles
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Volatile semiochemicals play a key role in the host location process of parasitoids [reviewed by Vinson (Vinson, 1991
)] and in their foraging for sugar sources
(Wäckers, 1994). Host
searching parasitoids respond especially to semiochemicals released by
herbivore-infested plants. They can use a range of host- or plant-derived
volatiles during host location (Rutledge,
1996; Turlings and Benrey,
1998). In many plants, over 100 volatile plant components have
been identified (Visser, 1979;
Etiévant et al.,
1984; Borg-Karlson and
Tengö, 1986; Knudsen
et al., 1993; Blight
et al., 1997). The quality and quantity of these blends
can fluctuate according to abiotic conditions
(Robacker et al.,
1982), inherent factors such as phenology
(Hedin, 1976), or external
biotic factors such as type, quantity and time of herbivore plant damage
(Turlings et al.,
1998), and even oviposition
(Hilker et al.,
2002). Therefore natural odours encountered by parasitoids in
their natural environment are both complex and variable mixtures.
Associative learning allows parasitoids to focus on the most reliable cues
(Vet et al., 1990;
De Jong and Kaiser, 1991;
Papaj and Lewis, 1993). It has
also been shown that parasitoids can learn a wide range of volatiles,
including ecologically relevant (Vet and
Groenwold, 1990; Kester and
Barbosa, 1991) as well as novel odours
(Lewis and Takasu, 1990).
Despite the broad range of studies on parasitoid learning, there are very
few studies that examined the perception of defined blends in parasitoids
(Fukushima et al.,
2002). Studies on parasitoid learning have typically trained
parasitoids to essential oils or pure chemicals. However, the parasitoid
Leptopilina heterotoma was shown to learn to respond to single
C6-compounds in a complex background of yeast odour
(Vet and Groenwold, 1990;
Vet et al.,
1998).
To study the learning mechanisms that are required for the identification
of defined blends we used the braconid wasp Microplitis croceipes, as
a model system. Microplitis has been successfully used for the study
of various learning paradigms (Lewis and
Takasu, 1990; Wäckers
et al., 2002) and we have recently started to survey the
effect of molecular structure of volatiles on its olfactory discrimination
(Meiners et al.,
2002). Furthermore, the larvae of its noctuid host species,
Helicoverpa and Helitothis, are polyphagous
(Fitt, 1989) and the
parasitoid is challenged during host location with a multitude of blends with
different components.
The odours selected for training and testing the wasps were 2-octanone,
ß-caryophyllene and methyl jasmonate. ß-Ocimene was used as an
untrained control odour in subsequent dual choice tests. All compounds, with
the exception of 2-octanone, are plant volatiles that play an important role
in plant defence and could signal parasitoids the presence of wounded plants
(McCall et al., 1993;
Takabayashi et al.,
1994; Turlings et
al., 1998). Thus, these compounds may reflect odours that are
important within the host-searching realm of M. croceipes. 2-Octanone
is a ketone known from cheese odour and serves as an attractant for cheese
mites (Yoshizawa et al.,
1970). This volatile was chosen, as it has no known ecological
function for M. croceipes.
The parasitoids were trained and challenged with either a single component or blends of two and three components. These experiments, albeit with a limited number of compounds, are a crucial first step in understanding how odour learning takes place under more natural situations, in which biologically relevant odours occur in blends and against a background of additional olfactory stimuli.
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Materials and methods |
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Insects
Heliothis zea was reared as described by Burton
(1969) at 28°C,
50–70% relative humidity (RH), and a 16 h light: 8 h dark photoperiod.
Microplitis croceipes was reared on H. zea larvae according
to the method of Lewis and Burton (Lewis
and Burton, 1970). The parasitoid females were held with males,
water and a honey supply in 30 x 30 x 20 cm acrylic cages.
Three-day-old mated females without oviposition experience were used in the
experiments.
Flight chamber
The flight chamber used in the experiments was similar to the one described
previously (Drost et al.,
1988). All flight responses were tested at 25°C, 50% RH, a
wind speed of 70 cm/s and a light intensity of 2000 lux.
Conditioning
Female M. croceipes were allowed to contact fresh frass (
20
mg) of artificial diet-fed H. zea larvae offered on a filter paper (9
cm in diameter) for a period of 30 s. Antennal contact with host frass serves
as the unconditioned stimulus for M. croceipes in associative
learning of volatiles (Lewis and
Tumlinson, 1988). To condition female parasitoids to a novel
odour, 1 µl of the given solution was applied on 0.5 x 0.5 cm filter
paper, which was subsequently placed in a glass pipette. While the female
parasitoids were contacting the frass, they were concurrently exposed to the
volatiles emitted from the odour source. For this purpose the odour was blown
over their antennae through the odour laden pipette at a rate of 40 ml/min. As
a control parasitoids were trained to clean air only using a pipette with a
blank piece of filter paper. Clean air (and not the solvent) was used as
control odour during training since it could not be excluded that the
parasitoids are able to learn to respond to the solvent itself.
Chemicals
The following chemicals were used as training odours: (i) a mixture of
2-octanone, ß-caryophyllene and methyl jasmonate (ternary odour mixture);
(ii) a mixture of ß-caryophyllene and methyl jasmonate (binary mixture);
and (iii) methyl jasmonate alone. ß-Ocimene was used as unconditioned
control odour during testing. Compounds were used as 5% (vol/vol) solutions in
hexane–paraffin. All tested compounds were purchased from Sigma (St
Louis, MO). They were at least 95% pure except for ß-ocimene, which
consisted of isomers (70% (E)- and 30%
(Z)-ß-ocimene).
Testing
Fifteen minutes after conditioning, the female wasps were introduced into a flight chamber using a 7.6 ml shell vial at a position 80 cm downwind of two odour sources. The two odours were presented on strips of filter paper (1 x 2 cm) on which 1 µl of the respective solution had been placed. Both filter papers were attached to a glass pipette placed vertically on a stand and spaced 12 cm apart.
Each wasp was given three attempts to complete an oriented flight by landing on one of the odour sources. Uncompleted flights were recorded as well. Females that did not make a choice after three trials or that did not take off after 5 min were recorded as ‘no choice’.
Parasitoids trained to the ternary odour mixture were offered a choice between the ternary blend and ß-ocimene (both diluted to 5% with hexane–paraffin). Next, individual females trained to the odour blend were given the choice between each single compound of the conditioned ternary odour mixture and the unconditioned odour (ß-ocimene). The response of the wasps to methyl jasmonate and ß-ocimene was investigated in a dual choice test after the parasitoids had been trained to methyl jasmonate alone. A control group that had been trained with frass in the presence of pure air was also tested in each of the above experiments.
Finally the preference of females trained to the binary mixture, the ternary mixture or control females (trained to pure air) was tested when given a choice between the binary mixture and the mixture of the three compounds.
For each different treatment in the wind tunnel experiments five females were tested every day for 5 days (a total of 25 females for each treatment). The range of non-responders during the test period of 13 days was 10–40%. On average, 30% of the wasps did not respond.
Differences in the total number of wasps that completed a flight to one
odour alternative within each two-choice experiment were analysed by
2 statistics. Whenever the difference was found to be
significant, we concluded that a preference for the more frequent visited
odour exists. Differences between the wasps' responses to the two odour
sources over two different treatments were also compared by 2
statistics. Whenever the difference was found to be significant, we concluded
that learning had occurred.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Learning of single components in a mixture
Parasitoids trained to control air showed a non-significant preference towards the mixture of 2-octanone, ß-caryophyllene and methyl jasmonate when it was pitted against the untrained odour ß-ocimene in the flight chamber. Following experience with the ternary mixture, more parasitoids completed their flight and landed significantly more often on the filter paper treated with the mixture than on the control filter paper (Figure 1). However, no learning occurred after parasitoids had been trained with the ternary odour mixture.
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Parasitoids trained to control air tended to have a non-significant innate preference for the plant odour ß-ocimene over 2-octanone (Figure 2a). They showed no difference in their flight response to the plant odours ß-ocimene and ß-caryophyllene (Figure 2b) or ß-ocimene and methyl jasmonate (Figure 2c) in dual choice tests.
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Female M. croceipes trained to the ternary mixture successfully learned to respond to 2-octanone (Figure 2a) and also to caryophyllene (Figure 2b) when these compounds were pitted against the untrained ß-ocimene. In contrast, the female wasps experienced with the mixture did not prefer methyl jasmonate to the control odour (Figure 2c). However, when they were trained to methyl jasmonate alone they successfully responded to that compound (Figure 3).
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Learning of complex odours
Females of M. croceipes trained to air showed no preference for the binary mixture of methyl jasmonate and caryophyllene lacking 2-octanone or the ternary odour blend in dual choice tests (Figure 4). This confirms the lack of an innate preference for 2-octanone (Figure 2a). Also females trained to the two components methyl jasmonate and caryophyllene alone did not discriminate between the binary mixture and the ternary odour blend (Figure 4). When 2-octanone was used together with the other two components to train the parasitoids, the wasps showed a non-significant tendency to prefer this previously experienced blend over the blend of methyl jasmonate and caryophyllene. Despite this apparent tendency, no learning occurred after training the wasps with the two- and three compound mixes.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Learning of single components in a mixture
Our results show that M. croceipes are able to learn to respond to
single compounds within odour blends. The wasp appears to prefer
ß-caryophyllene and 2-octanone over the untrained stimulus ß-ocimene
after experiencing the ternary mixture. Such a learning process was not found
in the case of methyl jasmonate. However, wasps conditioned to methyl
jasmonate alone did show a significant increased preference for this compound
over ß-ocimene. This indicates that the two other compounds affected the
learning of methyl jasmonate during training. Volatility differences could
have influenced the learning abilities of M. croceipes. However,
Laloi et al. (Laloi et
al., 1999) showed that concentration differences of
conditioned stimuli from 10 ng to 1 µg had no relevant effect on the
learning of blends in honey bees. Furthermore, Park et al.
(Park et al., 2001)
showed in electroantennogram studies that the antenna of M. croceipes
is more sensitive to less volatile compounds (e.g. methyl jasmonate,
ß-caryophyllene) than to more volatile compounds (e.g. ß-ocimene).
Thus a lower volatility might be compensated by a higher sensitivity.
Our results are consistent with studies of mixtures of chemical stimuli
that demonstrate interactions between the odours perceived in mixes in a broad
array of animals (Schiet and Cain,
1990; Akers and Getz,
1993; Laska and Hudson,
1993; Patterson et
al., 1993; Derby et
al., 1996; Smith
1998). Sensory receptors for non-pheromonal odorants can respond
to many compounds and exhibit complex interactions in response to compounds in
mixtures (Ache, 1989;
Atema et al., 1989).
Mixture suppression is a common result in recordings of sensory cell responses
to pure compounds and to mixtures (Ache,
1989; Akers and Getz,
1993) and might explain that interactions in some mixtures are
stronger than in others.
Consistent with the data obtained from mixture recognition studies in honey
bees (Pham-Delégue et al.,
1993; Wadhams et al.,
1994; Laloi et al.,
2000), our wind tunnel studies confirm a hierarchy within the
components of a mixture, with some components eliciting mixture recognition
better than others. Laloi et al.
(Laloi et al., 1999)
found that individual honey bees differed in their learning ability. Good
learners perceived a hierarchy among the components of a mixture, with some
compounds being more representative of the conditioning mixture than
others.
Learning of complex odours
Wasps trained to air only, to the binary mixture of methyl jasmonate and
ß-caryophyllene, and to the ternary mixture containing additionally
2-octanone did not prefer one of the odour mixes in the flight chamber
(Figure 4). This indicates that
wasps trained to the binary mixture treated 2-octanone as a neutral background
odour. Although females of M. croceipes conditioned to the ternary
mixture responded to 2-octanone when offered alone (see above), they did not
prefer this compound in the background of the two other trained compounds.
Laloi et al. (Laloi et
al., 2000) found a similar result in honey bees, which
recognized components from a blend in no-choice tests, though they were less
active in choice tests with free-flying bees. Furthermore, they showed that
the discrimination of the individual compounds of six component mixtures in
honey bees is affected by the other components of the mixture. It is believed
that a small number of key compounds account for a major part of the
behavioural activity of the total mixture in honey bees
(Blight et al., 1997).
Smith and Cobey (Smith and Cobey,
1994) compared response levels in honey bee proboscis extension
with binary mixtures using citral, geraniol, hexanal and 1-hexanol. Three out
of four binary mixtures caused no significant difference in response levels to
mixtures compared with responses to the components. However, after
conditioning to a hexanal/1-hexanol mixture the response level to 1-hexanol
was significantly lower than to hexanal and the mixture.
In many cases it might be favourable for a parasitoid to generalize very
similar odours and not to invest too much time or sensory–physiological
effort to differentiate between several odours that might be promising
indicators of hosts in natural environments. Vet et al.
(Vet et al., 1998)
found that Leptopilinia heterotoma can adjust its degree of
discrimination between similar odours (e.g. apple varieties) according to the
profitability of the information in terms of host encounters that is connected
with the odour. Coupling a rewarding experience with one odour and an
unrewarding experience with the other odour allowed the parasitoids to
differentiate between the odours. A further developed training process might
help to enhance the accuracy of conditioning and testing of M.
croceipes. Further detailed studies are required to investigate the
possible correlations between the initial level of activity of compounds and
their significance in mixture recognition, as well as the interactions between
compounds.
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Acknowledgments |
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We thank Dawn Olson and Keiji Takasu for productive discussions in the lab and Thoris Green for rearing the parasitoids. Two anonymous reviewers and Kirst King-Jones provided very helpful comments on an earlier version of the manuscript.
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Accepted February 14, 2003
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