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First published online July 17, 2009
Journal of Experimental Biology 212, 2386-2393 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.030668
Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus
Institut de Recherche sur la Biologie de l'Insecte, UMR 6035 CNRS–Université François Rabelais, Tours, France
* Author for correspondence (e-mail: claudio.lazzari{at}univ-tours.fr)
Accepted 7 May 2009
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Summary |
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Key words: motivation, orientation, feeding behaviour, Chagas disease
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Klowden, 1990;
Klowden and Briegel, 1994;
Klowden, 1995;
Takken et al., 2001).
Actually, if a first meal is sufficient to produce a batch of eggs, a
supplementary meal would not necessarily increase fecundity
(Lea et al., 1978;
Edman and Scott, 1987).
Concerning hemimetabolous insects, which are obligatory haematophagous
throughout all of their life stages, to our knowledge, no information is
presently available. Even when reproduction and ovarian activity may modulate
the feeding activity of females, this would not be the case in males and in
larvae, which are subjected to the same trade-off between feeding and avoiding
predation. To shed some light on this problem, we studied the response of
blood-sucking insects to host-associated cues and their motivation to feed as
a function of the time elapsed since the last meal. We have previously shown
that internal factors, such as circadian clocks and the moult cycle, affect
the responsiveness of these insects to host cues
(Bodin et al., 2008;
Bodin et al., 2009). By
analysing the effect of feeding, we expand the characterisation of the effects
of the physiological state on host-seeking and host-feeding behaviour. This
knowledge is relevant to achieve a better comprehension on how feeding
frequency is modulated in blood-sucking insects; a main factor affecting the
transmission of parasites.
As an experimental model, we chose Rhodnius prolixus, because in addition to fulfilling the conditions for the study (i.e. hemimetabolous development, and larvae, males and females are obligatory haematophagous), it is a classical model in insect physiology and one of the main vectors of Chagas disease in Central and South America. First, we studied the response of larvae and adult males and females to CO2 and heat, and their motivation to feed at different times after feeding and, in the case of the larvae, until their ecdysis. Second, we also analysed the effect of abdominal distension and the influence of haemolymph-borne factors on the behavioural responses to host-associated stimuli in these insects.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Fifth-instar larvae, adult males and females that had just
moulted were isolated in individual plastic containers and starved until the
tests. It has previously been shown that these insects hatch at the end of the
night (Ampleford and Steel,
1982). For our experiments, insects were collected in the morning
following ecdysis. They are recognisable by their characteristic pale-pink
colour. In order to avoid any eventual interference of reproduction, adults of
both sexes were kept virgin.
Bioassay protocols
Experiment 1: nutritional state and host-seeking behaviour
To investigate the potential modulation of the behavioural response of
R. prolixus to host signals after a blood meal, we tested the
behavioural response to CO2 and heat, as well as the motivation to
feed at different times after a blood meal. Insects were fed using an
artificial feeder (Lazzari and
Núñez, 1989) 15 days after their ecdysis, either to
the fifth instar or to adulthood, in order to assure that they were highly
motivated to feed (Bodin et al.,
2009). During the 24 h after feeding, the mass of the insects
varied rapidly because of the excretion of urine
(Maddrell, 1963;
Maddrell, 1964a;
Maddrell, 1964b). Insects were
weighted 24 h after feeding because insects are too sensitive to manipulation
to be weighed immediately after feeding. Insects that had not been fed at
repletion were discarded in order to constitute homogenous groups.
In the case of fifth-instar larvae, after a complete blood meal the
behavioural responses to CO2 and heat were tested each day during
eight consecutive days and on the 10th, 15th, 20th and 27th days. Fifth-instar
larvae moult to adults (imaginal ecdysis) around the 27th day
(Rabinovich et al., 1979). In
males and females, the behavioural responses to CO2 and heat after
a complete blood meal were tested every two days during 20 days. The responses
of the tested fed groups were compared with the control group; highly
motivated insects, which were starved for 15 days after ecdysis
(Bodin et al., 2009). Each
insect was tested only once (N=951).
All of the assays were conducted in a room maintained at 25±2°C,
40–60% RH, 500±100 p.p.m. of CO2 and under functional
darkness for the insects, i.e. under infrared illumination
(Reisenman et al., 1998). The
experiments were carried out during the first hours of the scotophase, because
triatomines display a peak of activity throughout this period corresponding to
the moment insects emerge from their refuges following host-emitted cues in
order to have a blood meal (Lazzari,
1992). Also, their attraction to CO2 is limited to this
temporal window (Barrozo et al.,
2004; Bodin et al.,
2008).
Experiment 2: abdominal distension and host-seeking behaviour
To assess the potential role of the abdominal distension on the
host-seeking modulation, we tested the response of fifth-instar larvae of
R. prolixus to CO2 and heat during three days after
feeding them with Ringer solution. As in the previous experiment, the insects
were fed using an artificial feeder 15 days after their ecdysis. The solution
used was Ringer Locke (for 1 l of solution: 9 g NaCl; 0.42 g KCl; 0.24 g
CaCl2 2H2O; 0.15 g NaHCO3; 1 g glucose and
distilled water to complete the volume). Just before feeding, adenosine
triphosphate (ATP) 10–3 mol l–1 was added to
the solution. R. prolixus does not normally gorge on saline solutions
unless they are supplemented with ATP or some other related compound
(Friend, 1965;
Friend and Smith, 1977;
Guerenstein and Núñez,
1994; Smith and Friend,
1982). These compounds are `phagostimulants' and are a cue used by
these insects to identify the presence of blood in the food source.
The rationale underlying this experiment was to test the effect of the
abdominal distension as opposed to that of blood nutritive elements (proteins,
lipids, etc.) in host-seeking behaviour and motivation to feed. In order to
estimate the volume of ingested solution, insects were weighted 24 h after
feeding and every experimental day afterwards. The mass of the insects was
compared with that of blood-fed insects to assure similar abdominal
distension. Insects insufficiently fed were discarded to ensure a homogenous
group of insects. The experiments were carried out during the first hours of
the insects' scotophase because their attraction to CO2 is limited
to this temporal window (Barrozo et al.,
2004; Bodin et al.,
2008). Each insect was tested only once and then discarded from
the experiments (N=95). We have chosen to feed the insects on saline
solution to induce abdominal distension rather than injecting the solution
into the cavity of the insects' body for the following reasons: (1) making the
insects feed by themselves represents a non-invasive, less deleterious manner
to distend the abdomen (Wintle and
Reinhardt, 2008), and (2) to get full distension; the abdomen of
triatomines needs to be `plasticised' (i.e. to change its mechanical
properties), a process triggered by stimuli associated to biting
(Ianowski et al., 1998).
Experiment 3: the role of haemolymph-borne factors
To explore the existence of humoral factors affecting the post-feeding
modulation of the host-seeking behaviour, we analysed the behavioural response
to CO2 and heat, as well as the motivation to feed in non-fed
fifth-instar larvae to which the haemolymph of fed donors was transferred. As
in the previous experiment, the non-fed insects were starved for 15 days so
that they would have a high motivation to feed
(Bodin et al., 2009). Two
groups of 15 fed donors were constituted, the first one composed of insects
fed one day (I1) and the second one composed of insects fed four days (I4)
before haemolymph extraction. The collection of haemolymph for these groups
was accomplished by securing the insects by their back over adhesive tape,
removing the legs and applying a slight pressure to the abdomen until a drop
of haemolymph extruded from the leg cuts. Collections were performed with a
graduated micro-capillary connected to a manual pump, under a stereomicroscope
(Leica MZ16, Wetzlar, Germany). Using the same apparatus, non-fed insects were
injected with 1µl of I1–haemolymph or I4–haemolymph, and
different groups of insects were tested for their response either at day 1
(t1), day 2 (t2) or day 3 (t3) after the injection. As previously stated, the
experiments were carried out during the first hours of the insects' scotophase
because their attraction to CO2 is limited to this temporal window
(Barrozo et al., 2004;
Bodin et al., 2008). Each
insect was tested only once and then discarded (N=143). Three control
experiments were conducted: (1) non-injected, non-fed insects (A group); (2)
non-fed insects injected with 1µl of saline solution (B group), and (3)
non-fed insects injected with 1µl of haemolymph obtained from non-fed
insects (C group).
The response to CO2
The behavioural response of R. prolixus to CO2 was
recorded in an open-loop design for translation, on a locomotion compensator,
and the walking paths of the insects were reconstructed and analysed in their
spatio–temporal components, as previously described by Barrozo and
Lazzari (Barrozo and Lazzari,
2004a). Before the beginning of each test, the insect remained in
still air on the locomotion compensator for 2 min to familiarise themselves
with the experimental situation, after which the air-streams (control and
stimulus) were presented during 3 min. The assays were monitored from the
outside of the experimental room by means of an infrared-sensitive camera
(Conrad, Lille, France) equipped with an array of infrared LEDs (emission 900
nm). This light illuminated the scene without being perceived by the insects
(Reisenman et al., 1998).
Because triatomines exhibit spontaneous anemotaxis to odourless air-streams
under these conditions (Barrozo et al.,
2003), a simultaneous-discrimination bioassay was conducted,
similar to that previously used by us
(Barrozo et al., 2004;
Barrozo and Lazzari, 2004a;
Barrozo and Lazzari, 2004b;
Bodin et al., 2008;
Bodin et al., 2009). Individual
insects were exposed to two opposite horizontal charcoal-filtered air-streams
(180 deg.): one bearing 1200 p.p.m. of CO2, over the environmental
concentration of 500±100 p.p.m., while the other was just clean
filtered air (control versus test). Thus, each insect could choose
either walking towards one of the two streams or exhibit a non-oriented
behaviour, i.e. to walk randomly. Both air-streams were blown over the insects
through glass tubes (0.6 cm inner diameter, 14 cm length) placed at 3 cm from
the insects at constant velocity (4.2 cm s–1), temperature
(25±2°C) and RH (40±5%). The production of CO2
was achieved as previously described by Barrozo and Lazzari
(Barrozo and Lazzari, 2004a).
To avoid eventual environmental biases, the position of the stimulus and the
control air-streams were changed randomly along the experiments.
The walking pathways described by the insects on the locomotion compensator
were analysed by means of circular statistics
(Zar, 1984;
Fisher, 1993). The mean
walking angle (
i) displayed by each insect along the
experimental time was computed and, subsequently, for every experimental
group, a mean angle (m) and the length of the resultant mean
vector (r) were calculated. The angle varied between 0 deg.
and 360 deg., and r varied between 0 and 1 (0 indicating a
non-defined mean direction and 1 indicating a straight path to a given
direction). The position of the stimulus-delivered current was conventionally
designated as 0 deg., and the control current as 180 deg. The V-test
(Zar, 1984) was conducted to
test if m was significantly different from the stimulus
direction (0 deg.). Additionally, for an easier visualisation of the data, an
orientation index (OI) was calculated by multiplying the cosine of the
m by r, as
cos(m)xr. This index fluctuates between 1 and
–1, indicating orientation directly towards or away from the stimulus
position, respectively. We also tested the pathways for eventual bimodal axial
directions (i.e. opposite directions versus uniformity) by means of
the Rao's Spacing test (Fisher,
1993).
Response to heat and feeding motivation
In order to study the impact of a blood meal on the behavioural response to
heat and the motivation to feed, we tested the ability of the insects to
respond to a thermal source, which also served as a feeder. We set up an
artificial feeder allowing us to independently observe 10 insects at a time
(Bodin et al., 2009). The
artificial feeder consisted of 10 1 ml Eppendorf® tubes whose rear ends
were cut and replaced by Parafilm® through which insects were able to
bite. The tubes contained 0.5 ml of sheep heparinised blood and were placed in
a taped aluminium block (35x5x1.3 cm) equipped with a flat
electric resistance. A thermostat kept the temperature of the blood at
33±1°C, which roughly corresponds to the temperature of the surface
of a host body. The aluminium block was isolated with a polystyrene foam
plate, which was pierced to make the tubes accessible. Thus, the lower side of
the polystyrene plate was at ambient temperature (25±2°C). The
insects were placed in plastic containers (11.7 cm height and 3 cm diameter),
the tops of which were covered with a fabric mesh, allowing the insects to
pierce the Parafilm® and feed from the blood. Each tube contained a piece
of filter paper that reached the top of the container, allowing the insects to
reach the feeder. Before the test began, each insect was allowed to habituate
for 2 min to the experimental situation without stimulation. After this time,
the artificial feeder was placed over the containers and the response of the
insects was recorded during 15 min. Three parameters were recorded: (a)
approaching (the bug climbed up approaching the feeder), (b) PER (proboscis
extension response), and (c) feeding (the bug increased noticeably its
abdominal volume).
Binary data (1=behaviour observed and 0=behaviour not observed) were
collected and a proportion of response (p) was calculated for each
behaviour. The standard deviation (s.d.) was calculated by the following
formula for binary data: s.d.=[p(1-p)]
.
When needed, a non-parametric Mann–Whitney U-test was performed
for comparing groups adjusting the value of in the case of multiple
comparisons.
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RESULTS |
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Fig. 2B represents the behavioural response of female R. prolixus to heat. As in the case of larvae, all of the insects that approached the thermal source extended their proboscis. Before feeding, we observed a high proportion of insects approaching the heat source and extending their proboscis (65±12.5%), and a notable proportion of insects that fed (60±9.6%). These proportions were statistically different from those observed in larvae (U=2.84, P<0.05 and U=–2.17, P<0.05, respectively, for the proportion of insects attracted (approaching and PER) and for insects that fed through the feeder). Then, after the blood meal and throughout the experimental period, there was a decrease in the proportion of insects that responded to heat. The proportion of insects approaching the heat source and displaying the PER never exceeded 30%. The maximal responses were observed between t6 and t10. Concerning feeding motivation, no insect was observed trying to feed from the artificial feeder during the experimental time.
Behavioural response to CO2 and heat in males
Fig. 1C represents the
response of male R. prolixus to CO2. As for larvae and
females, we observed a variation in the orientation response of the insects as
a function of the time elapsed since the blood meal. Males showed a strong
attraction response to CO2 before taking a blood meal
(V-test, P<0.05), displaying a preferred walking
direction to the stimulus. Contrary to what we had observed in larvae and
females, males showed no orientated response towards CO2, i.e.
neither attraction nor repulsion. The pathways of the insects were uniformly
distributed between 0 deg. and 360 deg. (V-test, n.s. in all cases),
i.e. they walked randomly on the sphere showing no orientation preference. The
comparison of the walking duration among all the different groups revealed, in
all cases, no significant differences, indicating that the activity on the
locomotion compensator was similar in all groups (ANOVA, n.s.). Rao's Spacing
test did not reveal axial orientation in any case, i.e. P>0.05,
n.s.
Fig. 2C represents the behavioural response of male R. prolixus to heat. All the insects that approached the thermal source extended their proboscis. Our results are similar to those obtained with females. Before feeding, we observed that most insects approached the heat source and extended their proboscis (62±10.2%), as well as an important proportion of insects that fed (59±9.3%). These proportions were statistically different from those observed in larvae [U=2.15, P<0.05 and U=–2.29, P<0.05, respectively, for the proportion of insects attracted (approaching and PER) and for insects that fed through the feeder] but not from females (Mann–Whitney, P>0.05 for all behaviours). After the blood meal, there was a decrease in the proportion of insects responding to heat. The proportion of insects approaching the heat source and displaying the PER never exceeded 20%. The maximal responses were observed between t8 and t16. As for females, we never observed insects trying to feed from the artificial feeder.
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Fig. 3A represents the response of fifth-instar larvae of R. prolixus to CO2 before and after feeding with saline solution. The results obtained before feeding correspond to those obtained in experiment 1 (see above). During the first three days after feeding, insects showed no orientation tendency towards the stimulus (V-test, P>0.05 in all cases). The comparison of the walking duration among all the different groups revealed, in all cases, no significant differences, indicating that the activity on the locomotion compensator was similar in all groups (ANOVA, n.s.). Rao's Spacing test did not reveal axial orientation in any case.
The behavioural response to heat after feeding with saline solution is represented in Fig. 3B. The results before feeding correspond to those obtained in the first experiment (see above). As with CO2, no response to heat was observed during the first three days after feeding with saline solution. Insects remained immobile in their containers.
Experiment 3: the role of haemolymph-borne factors
Fig. 4A represents the
behavioural response to CO2 of non-fed R. prolixus
fifth-instar larvae injected with haemolymph from fed fifth-instar insects.
Larvae were injected with haemolymph of insects fed the previous day (I1) or
four days before (I4) behavioural tests. The results of the control group A
(non-fed insects without injections) correspond to those obtained in
experiment 1. The two other control groups, B (non-fed insects injected with
saline solution) and C (non-fed insects injected with haemolymph from non-fed
insects), showed that insects displayed an orientation preference to the
stimulus after being injected (V-test, P<0.05 in all
cases), excluding any possible negative effect of the injections.
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Fig. 4B represents the behavioural response to heat of non-fed R. prolixus fifth-instar larvae injected with haemolymph from fed larvae. The results of the control A (before injections) are the same as those obtained in experiment 1 (see above). For the control B (non-fed insects injected with saline solution) and C (non-fed insects injected with haemolymph from non-fed insects), the three behavioural responses (approaching, PER and feeding) did not differ from animals in the control A (Mann–Whitney, n.s. in all cases). As explained before, data from the group I1 were obtained only for 1 day after injection (t1) and showed that the insects were not attracted to heat. Insects did not even move in their containers. Results obtained from the group I4 are very different, showing a progressive attraction response to heat was observed. Observations revealed that few insects responded to the heat stimulus 1 day after injection. These proportions of response increased during the following days (I4–t2 and I4–t3) to nearly reach the proportions of response of the control A. In I4–t1 and I4–t2, the proportions of insects that responded to heat and fed from the feeder were statistically different from those obtained from the control A (Mann–Whitney, P<0.05 in all cases). The proportions of response obtained in I4–t3 were not different from the control A (Mann–Whitney, n.s.). Our results also show that all the insects that approached the thermal source (the feeder) extended their proboscis.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Starved insects responded to CO2 and heat and fed, whereas fed
insects either remained indifferent or walked away from such stimuli and did
not feed. Interestingly, we found that the response to a host cue may be
attraction, indifference or, quite surprisingly, a significant repellence. As
far as we know, this is the first time that a repellent effect to a
host-associated cue has been demonstrated in a haematophagous insect. The
theory of spatial orientation mechanisms indicates that a same stimulus might
mediate orienting responses of opposite signs
(Jander, 1963). Our
experiments confirm the use of the same host-associated cue for both
approaching and avoiding a host.
Negative responses to CO2 became evident in R. prolixus
at different moments or `physiological contexts'. In larvae, repulsion
appeared about 72 h after feeding, lasting for about two days
(Fig. 1A, t3–t5) and also
close to the ecdysis (Fig. 1A),
i.e. at t20 and t27 postfeeding when most larvae of R. prolixus are
known to moult (Lent and Valderrama,
1977; Rabinovich et al.,
1979). In females, repulsion to CO2 appeared a little
later, between t6 and t10 (Fig.
1B), when their motivation to oviposit is maximal
(Davey, 1965). The fact that
males did not show repellence to CO2 seems to be consistent with
the fact that in females it could only be related to oviposition and not to
feeding as in larvae.
Concerning heat, only a reduction in the motivation of the insects to
approach a thermal source was observed. Even though our assay did not allow us
to verify repulsion (approach or not approach), we never observed any insect
on the upper part of the tube moving down. Larvae, males and females strongly
reduced both their responsiveness to heat and their motivation to feed
(Fig. 2). In all cases, the
response to heat completely disappeared right after the blood meal (i.e.
during the repulsion phase to CO2) and gradually recovered during
the following days. It should be noted that approaching and PER were
associated in 100% of the cases (i.e. every time the insects approached the
heat source, they extended their proboscis), evincing once more the crucial
role of heat for triggering biting in triatomines
(Flores and Lazzari, 1996).
Nevertheless, PER did not necessarily lead to feeding. In contrast to chemical
stimulation, which relies on anemotaxis, heat orientation take place in the
short range (Lazzari and
Núñez, 1989), and the PER is triggered by the close
proximity of a heat source (Wigglesworth
and Gillett, 1934; Flores and
Lazzari, 1996). Therefore, it is not surprising that insects
responded trying to bite (i.e. PER) a heat source when they were in contact or
almost in contact, even when their motivation to feed repressed them from
taking blood.
The physiological mechanisms
In order to explore the physiological basis of the state-dependency of
seeking a host and feeding in R. prolixus, we performed two further
experimental series. The first one was aimed at testing whether the
post-feeding behavioural changes were induced by the mechanical distension of
the abdomen or by the composition of the food. We therefore fed a group of
insects with saline solution enriched with phagostimulants. We observed a
strong reduction of both the response to CO2 and to heat
(Fig. 3). However, no repulsive
response to CO2 was observed; only a blood meal was able to induce
repellence but not saline, suggesting that negative orientation to
CO2 is triggered by one or more chemical components of the
blood.
We also tested whether the factors responsible for the modulation of the
response to host cues are transported by the haemolymph. Starved insects
injected with haemolymph from recently fed insects showed a reduced
responsiveness to both CO2 and heat
(Fig. 4), reproducing to some
extent the effect of a blood meal. The duration of this effect on the
receivers could not be measured because insects died within the following 48 h
after being injected. Neither change in the response nor death occurred when
the starved insects were injected with saline solution or haemolymph from
non-fed insects (Fig. 4). The
death of insects injected with haemolymph of recently fed insects can be due
to changes in the haemolymph associated with the process of feeding. In order
to handle blood meals that are several times heavier than their own mass,
these insects experience dramatic physiological modifications, including the
flow of a big amount of blood components and water through the crop wall to
the haemolymph. At the same time, diuretic hormones assure the rapid
elimination of a large amount of blood components during the first hours
following feeding (Maddrell,
1963). It is likely that injected animals received all of these
factors, including some toxic ones that could not be eliminated, because even
though diuretic hormones were also transferred, they do not suffice to induce
diuresis in starved insects (Gomez and
Balderrama, 1986).
In our final experiment we injected starved insects with haemolymph from donors fed four days before. This experiment allowed us to test two things. The first one was to test whether, during the period of repulsion to CO2, unknown factors in the haemolymph could induce this response in injected insects. The second was to test whether the lethal effect of haemolymph from recently fed insects persisted for several days. When tested for their response, the receivers of this haemolymph remained indifferent concerning both CO2 and heat (Fig. 4), and no significant repulsion was observed (Fig. 4B). Injected insects did not die after the injection and their response was followed for a long time, revealing a recovery of the response to heat and the persistence of the lack of response to CO2 for at least three days. These results show that the haemolymph-borne factors are responsible for the reduction of the insect's behavioural response and also that these factors persisted for several days and slowly lose their efficacy. The survival of the receiver insects supports the idea that what caused the death of receivers of haemolymph of recently fed insects was an unknown factor associated with the physiological changes occurring during or immediately after feeding.
The influence of the nutritional state on host-seeking behaviour in
haematophagous insects has been analysed in detail in mosquitoes and has been
particularly concerned with the interaction between the nutritive and the
reproductive states. In female mosquitoes, feeding triggers endocrine
processes controlling the ovarian function
(Klowden, 1997). After the
initiation of a gonotrophic cycle by a blood meal, host seeking is inhibited
until egg maturation or oviposition
(Klowden and Briegel, 1994).
The inhibition is the result of the interplay between a nervous and a humoral
mechanism. The distension of the abdomen stimulates abdominal mechanoreceptors
[`distension-induced inhibition' (Klowden
and Lea, 1979a)]. If the blood meal suffices to trigger egg
production, the humoral mechanism is activated [`oocyte-induced inhibition'
(Klowden and Lea, 1979b)],
where different organs are involved, such as the ovary, fat body and
neurosecretory cells. Concerning the physiological mechanism, it has been
shown in Aedes aegypti that the response of lactic acid olfactory
receptors is inhibited by humoral factors present in the haemolymph after
feeding (Brown et al., 1994).
It is worth comparing our present results revealed in R. prolixus
with those obtained in mosquitoes. In both cases, feeding reduces the insect
motivation to respond to host-associated cues, and humoral factors released
during or after feeding seem to be involved. Concerning the modulation of the
response, in contrast to our findings in triatomine bugs, no repulsion seems
to occur in mosquitoes. In mosquitoes, given that only females feed on blood
and that feeding influences the ovarian activity, it is difficult to
discriminate between the direct effect of feeding and that of ovarian
activation. This does not mean, however, that female reproduction would not
influence the response of insects, because as indicated above, females exhibit
a delayed repulsion to CO2 at the time when they are probably ready
to lay eggs. Nevertheless, in the case of larvae and males, we have been able
to evince the effect of feeding in the absence of other influences, with the
exception of larval ecdysis.
In conclusion, we have shown that the response of haematophagous insects to their host is modulated by their physiological state. Feeding, moult and oviposition (all three) seem to affect the response to both chemical and physical cues associated with vertebrate hosts. This modulation seems to be triggered by both the distension of the abdomen and chemical components of the blood meal. Only a blood meal is able to induce repulsion and could be directly or indirectly responsible for the release of haemolymph-borne factors, which can be transferred from an insect to another. Further work should reveal the exact origin and targets of these factors.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Ampleford, E. J. and Steel, C. G. H. (1982). Circadian control of ecdysis in Rhodnius prolixus (Hemiptera). J. Comp. Physiol. A 147,281 -286.[CrossRef]
Barrozo, R. B. and Lazzari, C. R. (2004a). The
response of the blood-sucking bug Triatoma infestans to carbon
dioxide and other host odours. Chem. Senses
29,319
-329.
Barrozo, R. B. and Lazzari, C. R. (2004b).
Orientation behaviour of the blood-sucking bug Triatoma infestans to
short-chain fatty acids: synergistic effect of L-lactic acid and carbon
dioxide. Chem. Senses
29,833
-841.
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