Chem. Senses 27: 811-816,
2002
© Oxford University Press 2002
The Effect of Molecular Structure on Olfactory Discrimination by the Parasitoid Microplitis croceipes
1 Institut für Biologie, Freie Universität Berlin, Haderslebener Str. 9, D-12163 Berlin, Germany 2 NIOO CTO, 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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Flight chamber experiments were conducted to examine the capacity of the larval parasitoid Microplitis croceipes (Hymenoptera: Braconidae) to learn to distinguish between structurally related aliphatic alcohols differing in the carbon chain-length and the position of the functional group, and between an alcohol and the respective aldehyde. The parasitoid's ability to discriminate between the components depended on the chain-length of the alcohol to which they had been conditioned. Discrimination improved with increasing difference in carbon chain-length, e.g. the parasitoids made clear distinction between 1-hexanol and 1-octanol. Microplitis croceipes could also distinguish different isomers of six-carbon alcohols on the basis of the position of the alcoholic group as well as between 1-hexanol and 1-hexanal. The learning abilities of M. croceipes correspond to the specificity of antennal odour receptors towards aliphatic alcohols and aldehydes in previous electrophysiological studies of M. croceipes and other insects. Differences in perception or processing of single compounds might reflect differences of their ecological relevance.
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Introduction |
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Parasitoids use odours as they forage for sugar sources, or to locate insect hosts for the purpose of oviposition. Searching behaviour often involves upwind flight toward odours emitted by the resource. In the case of food foraging, these can be flower volatiles (Wäckers, 1994
), while
during host-search parasitoids may employ volatiles from the host itself, its
faeces, host-associated microorganisms, or the plants on which the host lives
(Vinson, 1991). A limited
number of odours evoke innate flight responses in inexperienced parasitoids
(Wäckers, 1994).
Parasitoids can usually extend their array of foraging cues by learning
(Vet and Dicke, 1992). It has
been shown that parasitoids can learn to respond to new compounds by
associating them with either a food reward
(Lewis and Takasu, 1990) or
the host (Papaj and Lewis,
1993). Associative learning of host-associated information may
occur during adult emergence, when the egressing parasitoid is exposed to the
remnants of its host (Herard et
al., 1988; Caubet and
Jaisson, 1991; Cortesero and
Monge, 1994). Alternatively, parasitoids may associate chemical,
as well as visual information experienced during host encounters
(Lewis and Tumlinson, 1988;
Turlings et al.,
1989; Wäckers and Lewis,
1994; Vet et al.,
1995).
Despite the broad range of studies on parasitoid learning, little is known
about the specificity of the learned response, i.e. the ability of parasitoids
to distinguish between conditioned and unconditioned stimuli of similar
molecular structure (Vet et al.,
1998). Plants emit numerous volatiles, featuring various
functional groups and ranging in structure from short, straight carbon chains
to complex multi-ring sesquiterpenes
(Visser, 1979;
Knudsen, et al.,
1993). Relevant odour sources might be characterized by subtle
differences in volatile chemistry, e.g. volatile plant alcohols and aldehydes
varying only in their chain-length or active group. Thus, a high level of
odour learning specificity can be critical to the success of parasitoid
search.
We chose Microplitis croceipes for our experiments as this species
has served as a model of parasitoid learning paradigms. Microplitis
croceipes is a parasitoid of Helicoverpa and Heliothis
spp., whose larvae feed on >100 plant species from different plant families
(Fitt, 1989).
Six-carbon alcohols and aldehydes play an important role as `green leaf
volatiles' in the orientation of phytophagous insects to their host plants and
of predatory insects and parasitoids to their predatory hosts
(Loughrin et al.,
1994; Turlings et
al., 1998). To examine whether females of M.
croceipes are able to discriminate between similar alcohols and
aldehydes, we trained females to a single compound and subsequently challenged
them to discriminate between the conditioned compound and an alternative. The
alternatives were: (i) alcohols with a different chain-length; (ii) alcohols
with the same chain-length, but with the active chemical group at a different
position; and (iii) alcohols and aldehydes with the same chain-length, but
different active group. The parasitoid's reaction was tested with dual-choice
tests in flight chamber bioassays.
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Materials and methods |
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Insects
Heliothis zea was reared as described previously
(Burton, 1969) at 28°C,
50-70% relative humidity (RH) and a 16L:8D photoperiod. Microplitis
croceipes was reared on H. zea larvae according to a previously
published method (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 that described in
an earlier study (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
Females of M. croceipes were allowed to contact fresh frass
(
20 mg) of artificial-diet-fed H. zea larvae provided 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, 0.5 µl of the compound was applied to a 0.5 x 0.5 cm filter
paper which was subsequently placed in a glass pipette. While 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.
Odour compounds
All tested compounds were purchased from Sigma (St Louis, MO). One group of parasitoids was trained to 1-hexanol, while another group was trained to an odour alternative. This alternative was one of a range of saturated primary alcohols (C4—C10), for chain-length discrimination, 2-hexanol or 3-hexanol (differing with regard to the position of the functional group), or 1-hexanal (differing with regard to the type of functional group). As the last three compounds have a similar vapour pressure compared to 1-hexanol, it can be assumed that parasitoids were exposed to comparable numbers of molecules during conditioning and testing.
Testing
Fifteen minutes after conditioning, parasitoids were introduced into the
flight chamber using a 2 dram shell at a position 80 cm downwind of the
conditioned odour and an unconditioned alternative. The two odours were
presented on strips of filter paper (1 x 2 cm) on each of which 0.5
µl of the respective compound had been placed. Both filter papers were
attached to a glass pipette placed vertically on a stand and spaced 12 cm
apart. Each insect 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'. All experiments were
conducted with 30 different females, 15 of which had been conditioned to each
of the odour alternatives. Exceptional to this were experiments with 1-hexanol
and 1-hexanal, which were conducted with a total of 40 parasitoids. In order
to avoid possible diurnal variation in response, data were collected daily
from several insects in each of the different combinations. Differences in
choice were tested by 
2 statistics.
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Results |
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Discrimination relative to differences in chain-length
The parasitoids did not learn to discriminate between 1-hexanol and its direct neighbours 1-pentanol and 1-heptanol (Figure 1). However, at a difference in chain-length of two carbon atoms, the parasitoids were more successful, as they showed a tendency to distinguish between 1-butanol and 1-hexanol, and made a clear distinction between the trained and the untrained alcohol 1-octanol versus 1-hexanol. Success of discrimination dropped strongly when 1-hexanol was pitted against 1-nonanol or 1-decanol. None of the parasitoids trained to 1-hexanol landed at the filter papers treated with 1-nonanol or 1-decanol. Training the parasitoids to 1-nonanol or 1-decanol yielded very few complete flights in the test.
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Discrimination based on position of functional group
Following experience with 1-hexanol, 2-hexanol, or 3-hexanol, parasitoids also proved to distinguish effectively between volatiles on the basis of the position of their functional group. Parasitoids trained to 1-hexanol made 50 and 70% of their landings on this odour source when pitted against 2-hexanol and 3-hexanol, respectively. Parasitoids trained to 2-hexanol or 3-hexanol, on the other hand, exclusively flew to the trained component and ignored 1-hexanol (Figure 2).
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Discrimination based on type of functional group
Parasitoids were successful in learning to discriminate between 1-hexanol and 1-hexanal (Figure 3). All but one of the landings by parasitoids that had been trained to 1-hexanol were on the 1-hexanol-treated filter paper target. This clear-cut choice differs significantly from the equal distribution by parasitoids trained to 1-hexanal (Figure 3).
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Discussion |
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In this study, the learning and discrimination abilities of parasitoids were investigated by comparing their responses to 1-hexanol and structurally similar compounds. In conditioned honey bees and sphinx moths, the magnitude of the response to an unconditioned odour depends on the structural similarity between the conditioned and the novel odour compound (Smith and Menzel, 1989a
,b;
Getz and Smith, 1990;
Daly et al.,
2001). Discrimination based on differences in chain-length
The results of this study show that parasitoids possess a well-developed
ability to discriminate between aliphatic alcohols. Furthermore, we have shown
that the ability of M. croceipes to learn to differentiate between
alcohols depends on difference in chain-length. A difference of at least two
C-units appears to be required for successful discrimination in our
experiments. Such a negative correlation between discrimination performance
and structural similarity in terms of differences of carbon chain-length was
also found in humans for aliphatic alcohols, aldehydes, carboxylic acids,
aliphatic ketones and acetic esters (Laska and Teubner,
1998,
1999;
Laska and Hübener, 2001).
It has been shown (Li et al.,
1992) that electrophysiological responses of antennal odour
receptors in M. croceipes are maximal for the green leaf volatile
1-hexanol and decline as the carbon chain-length increases or decreases. Also,
several other insects show a relationship between the electro-antennogram
(EAG) amplitude and carbon-chain-length. Other researchers
(Schofield et al.,
1995), working with primary aliphatic alcohols, found that EAGs of
the stable fly Stomoxys calcitrans increased with carbon chain-length
to 1-octanol. Adult boll weevils (Anthonomus grandis) showed a
maximal response to the C6 and C7 molecules of aliphatic alcohols and
aliphatic aldehydes (Dickens,
1984). In the Mediterranean fruit fly (Ceratitis
capitata), EAG responses were highest in response to stimulation by C7
aliphatic alcohols, aliphatic aldehydes and aliphatic acids, and C5 in the
case of aliphatic acetates (Light et
al., 1988). These EAG hierarchies lead to three
interpretations: (i) a group of receptors has a higher affinity for a molecule
with a certain chain-length; (ii) there are more receptors for a specific
molecule; (iii) EAGs for a specific chemical summate in such a way that the
recorded potential is greater for that chemical. Although EAGs indicate which
chemicals an insect can smell, no conclusions about the insect's behaviour
towards those chemicals can be drawn from these recordings. Behavioural
studies are necessary to identify the biological function of a compound and
learning bioassays can give information as to whether behavioural responses to
certain compounds can change with experience.
None of the M. croceipes females that were trained to 1-hexanol
landed at the filter papers treated with 1-nonanol or 1-decanol. Also, hardly
any parasitoids trained to 1-nonanol and 1-decanol completed any flights,
indicating that the parasitoids cannot learn to respond to 1-nonanol and
1-decanol. However, the antennae of M. croceipes and M.
demolitor respond to 1-nonanol and 1-decanol to a comparable degree as to
1-butanol or 1-pentanol (Ramachandran and
Norris, 1991; Li et
al., 1992). Since data from single cell recordings are
lacking in M. croceipes, it cannot, as yet, be determined whether our
results indicate differences in higher-order processing of incoming peripheral
information or in the perception of these primary C-9 and C-10 alcohols.
Discrimination based on position of functional group
Asymmetric responses were obtained from M. croceipes trained to 1-hexanol, 2-hexanol, or 3-hexanol. While parasitoids trained to 1-hexanol also landed on targets treated with the other alcohol, they clearly distinguished between the alcohols when trained to 2-hexanol or 3-hexanol. (For a discussion of asymmetric responses see below.)
Gustavsson et al. (Gustavsson
et al., 1995) showed that analogues of a turnip moth sex
pheromone elicited different electrophysiological single-cell activities based
on the position of an oxygen atom replacing a methylene group. They concluded
from molecular mechanics that the bioactive conformation is responsible for
this effect. The position of the functional groups of different plant
volatiles had significant effects on the magnitudes of the EAG responses of
the cherry fruit fly Rhagoletis cerasi
(Raptopoulos et al.,
1995).
Discrimination of the functional group
Microplitis croceipes showed asymmetric flight responses in the discrimination of learned aldehydes and alcohols. While 1-hexanol trained parasitoids clearly preferred this alcohol to the aldehyde, parasitoids trained to 1-hexanal showed no difference in their response. This indicates that the parasitoids have an innate preference for the alcohol. Even though conditioning with 1-hexanal did not reverse this preference, it did result in a significant shift in the parasitoid's response towards the aldehyde.
Vet et al. (Vet et
al., 1998) showed that the parasitoid Leptolinia
heterotoma can differentiate between C6 compounds with different
functional groups. The parasitoids preferred cis-3-hexen-1-ol to
1-hexanol and 1-hexanal when they were trained to cis-3-hexen-1-ol.
But they generalized to 1-hexanal when the learned cis-3-hexen-1-ol
was not present.
In honey bees, conditioning experiments with alcohols and aldehydes showed
that alcohols elicited stronger learned responses than their corresponding
aldehydes (Smith and Menzel,
1989b; Smith,
1991). Honey bees conditioned to mixtures of an aliphatic aldehyde
and an alcohol showed asymmetric response patterns in proboscis extension
(Smith and Cobey, 1994). The
response to the aldehyde was much stronger than to the alcohol. The response
to the alcohol was much lower when the bee was trained with the alcohol and
the aldehyde than when the bee was trained to the same alcohol in the
background of another odorant. Honey bee studies of blocking show that
behavioural acquisition in response to one component can be hindered or
blocked by pre-training with the other component
(Smith and Cobey, 1994).
Greater antennal responsiveness to leaf alcohols than to their aldehyde
analogues has been found for the Colorado potato beetle and the boll weevil
(Visser, 1979;
Dickens, 1984), suggesting that
differences in the receptor population might explain the higher salience of
1-hexanol. However, others (Hartlieb
et al., 1999) showed that some odours were more salient
than others in the moth Spodoptera littoralis, despite the fact that
fewer receptors were present for the salient odour. The authors concluded that
the differences in salience might be due to differences in the central nervous
system or central processing.
It is not known why some insects perceive certain compounds better than
others, but there is evidence that differences in the receptor populations
cause this phenomenon. Carbon chain-length, degree of saturation and type and
position of functional groups all have a significant effect on the magnitude
of EAG response in insects from different orders
(Dickens, 1984;
Light et al., 1988;
Cork, 1994;
Raptopoulos et al.,
1995; Schofield et
al., 1995). On the olfactory receptor level, other
researchers (Liljefors et al.,
1984,
1985,
1987;
Bengtson et al., 1990)
have shown a close relationship between the molecular structure and the
response of the olfactory receptor for sex pheromone components. Single
sensillum studies on plant-odour-detecting neurons suggest that most of these
neurons are narrowly rather than broadly tuned and respond only to one or two
closely related compounds (Barata et al.,
2000,
2002,
Rostelien et al.,
2000), thus providing a basis for sensitive odour discrimination
(Todd and Baker, 1999).
However, although there is a potential for discrimination at the receptor
level, the role of central information processing is also important. It has
been shown (Stopfer et al.,
1997) that discrimination of similar compounds (1-hexanol and
1-octanol) depends on central events (neural synchronization).
The findings of the present study provide evidence of a well-developed
discrimination ability for aliphatic compounds in the parasitoid M.
croceipes. Carbon chain-length and type and position of functional groups
all have significant effects on parasitoid learning and discrimination of
odours in the context of host finding. The differences in perception and/or
processing might reflect the different ecological relevance of the single
compounds for M. croceipes. Six-carbon alcohols and aldehydes play an
important role as `green leaf volatiles' in the orientation of phytophagous
insects to their host plants and of predatory insects and parasitoids to their
prey (Loughrin et al.,
1994; Turlings et
al., 1998). Parasitoids and predators of herbivores might
have learning predispositions for certain plant components that are emitted
during herbivore feeding (Vet et
al., 1990; Steidle and
van Loon, 2002). Interference of trained compounds with those
volatiles might lead to the asymmetric learning effects described above.
Other work (Takasu and Lewis,
1996) on M. croceipes showed that increasing the number
of odour experiences increases the accuracy of choosing the experienced odour.
Others (Vet et al.,
1998) found that parasitoids can differentiate better between
similar odours if they have associated a rewarding experience with one odour
and an unrewarding experience with the alternative. Thus, future studies with
a more developed training process and additional electrophysiological
investigations can help further to explore and explain the
discrimination-learning abilities in insect parasitoids.
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Acknowledgments |
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We thank Dawn Olson and Keiji Takasu for fruitful discussions in the laboratory and Thoris Green for rearing the parasitoids. Two anonymous reviewers provided very helpful comments on an earlier version of this manuscript.
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Accepted August 29, 2002
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