© 2024. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.

247530

RESEARCH ARTICLE

Barometric pressure decrease induces density-dependent

changes in foraging behaviour in a parasitoid fly
Jean-Noë l Houchat, Marcela K. Castelo and José E. Crespo*

ABSTRACT Sujimoto et al., 2020; Azevedo et al., 2023), host fruit odour
Barometric pressure is an environmental factor involved in the recognition and oviposition (Leskey and Prokopy, 2003). For instance,
modulation of a variety of activities in insects. Generally, a drop in it has been seen in ants that increased wetness of loads tends to
barometric pressure precedes the arrival of weather conditions that can increase the probability of dropping a leaf fragment (Farji-Brener
affect insect activities and life expectancy. We simulated different et al., 2018).
scenarios of pressure drop in a modified hermetic chamber and studied Given their importance in food webs and as biological control
their influence on the host-seeking behaviour of the larvae of the robber agents, insect parasitoid foraging strategies have received a lot of
fly Mallophora ruficauda using air stationary olfactometers. In addition, attention, and a vast body of general literature is available (Wajnberg
we studied whether larval density modulates orientation to the host et al., 2008; de Rijk et al., 2013; Aartsma et al., 2019). Effects of
under the same scenarios of pressure drop. We found that motivation to abiotic conditions on parasitoid host-seeking behaviour have also
search for hosts is affected by the same slope of pressure drop in both been reported. In wasp parasitoids, females must locate host habitat,
low- and high-density larvae. However, larval density modulates the find hosts, evaluate their quality, and then accept or reject laying
onset of the responses to pressure decrease, as low-density larvae stop eggs on or in them (Godfray, 1994; Brodeur and Boivin, 2004).
searching for hosts more quickly than high-density larvae. This result Hence, the adults have been focus of several studies and it has been
reflects an avoidance strategy according to which low-density larvae shown that host-seeking behaviour is influenced by temperature
would have a reduced host range and higher risk of mortality and fewer (Amat et al., 2006), wind speed (Keller, 1990; Fink and Völkl,
chances to find a suitable host under adverse pressure conditions. Low- 1995; Weisser et al., 1997), rain (Weisser et al., 1997) and
density larvae, known to prefer healthy hosts, do not search for barometric pressure (Steinberg et al., 1992; Roitberg et al., 1993).
parasitized hosts under normal pressure conditions nor under a range For instance, it has been shown that when faced with conditions
of pressure drops, strongly suggesting that host selectivity is not related to the onset of a storm, wasps tend to superparasitize more
modulated by barometric pressure. This study paves the way to a better frequently or show reduced activity in wind tunnel experiments
understanding of the changes in crucial insect behaviours induced by (Steinberg et al., 1992; Roitberg et al., 1993).
weather conditions, and provides more knowledge about the risk factors In dipteran parasitoids, where oviposition occurs in the vicinity of
likely to affect insect survival in the context of foraging ecology. hosts, the first instar larvae are responsible for host location and
selection (Eggleton and Belshaw, 1992; Feener and Brown, 1997).
KEY WORDS: Robber fly, Mallophora ruficauda, Asilidae, Orientation However, in contrast to adults, the abiotic factors that modulate host-
mechanism, Host-seeking behaviour seeking behaviour in larvae have been less studied (Crespo and
Castelo, 2012). Furthermore, few studies show that environmental
INTRODUCTION factors such as temperature, barometric pressure and CO2 can
It is well established that environmental conditions have a modulating impact host orientation in larvae (Bernklau et al., 2004; Bodlah
effect on the activities of insects (Drake, 1994). Owing to their small et al., 2016; Haberyan, 2022).
size and the need to forage for food and mates in a constantly changing The robber fly Mallophora ruficauda (Diptera, Asilidae) is a
environment, their development, survival and reproductive success are common insect in the Pampas region of Argentina. The adults are a
particularly susceptible to changes in abiotic factors. Among these significant threat to honeybees, as they are key predators of foraging
factors, a variety of activities have been reported to be modulated by workers. As larvae, they parasitize white grubs of Scarabaeidae

Journal of Experimental Biology

changes in temperature, barometric pressure and wind. For instance, it beetles, especially Cyclocephala signaticollis (Castelo and Capurro,
has been shown that temperature influences flight initiation and 2000). In this species, there is a split host searching strategy between
locomotion (Gaylord et al., 2008; Chen and Seybold, 2014; Martini females and larvae. Females must find suitably high oviposition
et al., 2018). Studies have shown that barometric pressure and wind sites in grasslands, because oviposition height is crucial for optimal
influence not only flight initiation and locomotion (Fournier et al., larval dispersal and successful parasitism (Castelo et al., 2006).
2005; Chen and Seybold, 2014; Miao et al., 2021), but also mating Larvae dispersing from tall grasses are more likely to find a suitable
behaviour (Pellegrino et al., 2013) and reproduction (Adonyeva et al., host after dispersal (Castelo and Corley, 2004), as the probability of
2021). In addition, barometric pressure has been described as a finding a non-parasitized host increases (Castelo et al., 2006).
modulator of foraging for food resources (Polatto et al., 2014; Newborn larvae are dispersed by the wind, and after falling to the
ground, they burrow themselves, moult and search for a white grub
to parasitize (Castelo and Capurro, 2000; Crespo and Castelo, 2008)
*Author for correspondence ( jose.crespo@conicet.gov.ar) (Fig. 1A). Larvae orient themselves in the soil using chemical cues
produced in the posterior region of the intestine of the host
J.-N.H., 0000-0002-1469-3667; M.K.C., 0000-0001-7107-6078; J.E.C., 0000-
0002-0074-6924 C. signaticollis (Castelo and Lazzari, 2004; Crespo et al., 2011).
The chemical cues are produced in the fermentation chamber of the
Received 21 February 2024; Accepted 6 August 2024 white grub and are thought to be by-products of the activity of

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

A Life cycle of Mallophora ruficauda B Rearing in laboratory conditions

Oviposition on tall
Egg clutch 25qC
grasses

×100 ×500

Adult predator of
bees and other Collection Hatching
insects

1st instar
larva

Moulting

×100 ×500

Selective Non-selective

Host-seeking
2nd instar larva

Host
Host orientation
on
orientati

Pupa Collection
Parasitism on
white grubs

Host Healthy Parasitized

Journal of Experimental Biology

Fig. 1. Experimental design. (A) Life cycle of Mallophora ruficauda. The green patch indicates the host-seeking part of the cycle studied in the present
study. (B) Methodology of rearing of M. ruficauda larvae and hosts. Briefly, M. ruficauda egg clutches and Scarabaeidae white grubs (Cyclocephala
signaticollis) were collected, and neonate M. ruficauda larvae were maintained in two different conditions of preparasitism competition (low and high density)
determining host selectivity towards optimal (healthy) and suboptimal ( parasitized) hosts.

symbiont microorganisms, as treatment with antibiotics abolishes Effects of population density on life-history traits have been
larval host orientation (Groba and Castelo, 2012; Groba and largely documented (Than et al., 2020). In a broad sense, low
Castelo, 2016; Castelo and Crespo, 2022). It has been also shown density is a term used to define individuals or small groups of
that larvae can detect already parasitized hosts, avoid them and individuals living in an area, and high density defines larger groups
orient towards healthy non-parasitized third instar C. signaticollis for the same area. Often, exposure to a given density level during
(Crespo and Castelo, 2009). Because dispersal is exerted by an larval life is a factor modulating a variety of traits not only in larvae,
abiotic factor such as the wind, spatial heterogeneity in larval but also in adults. For instance, beneficial effects of high density are
distribution arises as a result of different levels of wind speed. reported in larvae of the fruit fly Bactrocera tryoni, which aggregate
Hence, conspecific density is an important ecological factor that and improve individual growth (Morimoto et al., 2018). In the case
modulates behavioural decisions. of M. ruficauda, larval density has been shown to influence the

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

selectivity for hosts. Indeed, M. ruficauda larvae grown in low- consisted of flasks with 500 larvae in 100 ml of potting soil
density conditions have a clear preference for healthy non (high-density group). This treatment induces non-selective larvae
parasitized third instars of C. signaticollis and can detect already that are more likely to orient towards suboptimal hosts (Crespo et al.,
parasitized hosts, then avoid them (Crespo and Castelo, 2009). 2015; Martínez et al., 2017) (Fig. 1B).
Nevertheless, larvae grown with a higher number of conspecifics Healthy and singly parasitized C. signaticollis host larvae were
during first and second larval stages are more prone to parasitize collected by digging in the soil at a depth of 25 cm at the same
poor quality hosts such as already parasitized grubs or other instars grasslands where egg clutches of the parasitoid were found
(Crespo et al., 2015; Martínez et al., 2017). Lower selectivity in (Fig. 1B). They were identified to species level in the laboratory
high-density larvae is interpreted as a response to the increased using a taxonomic key (Alvarado, 1980) and kept at 25°C in
preparasitism competition for hosts, reflecting a trade-off between individual black tubes filled with potting soil. They were fed with
their risk of mortality if they do not find a host to parasitize, and their fresh carrot pieces once a week. Only third-instar larvae were used in
chances to win against conspecifics in a superparasitized host or the experiments.
survive parasitizing any poor-quality host (Crespo et al., 2015;
Martínez et al., 2017). Thus, population density modulates host- Experimental design
seeking behaviour in M. ruficauda larvae. Experimental device
Regarding the influence of environmental conditions on host- To study the influence of barometric pressure decrease on the host-
seeking behaviour, in previous work, larvae of M. ruficauda seeking behaviour of larvae, we modified an SB type acrylic
exhibited a correlation between changes in host orientation and vacuum desiccator (Sanplatec Corp., Japan). This chamber has
natural variations in barometric pressure (Crespo and Castelo, internal dimensions of 20×20×19.5 cm with a lid fitted with a
2012). This work showed that selective larvae did not orient to host silicone gasket to ensure that the sealed chamber is completely
odours in olfactometry assays when barometric pressure decreased hermetic. The lid also has a valve with a nozzle and a vacuum gauge
at a higher rate than expected in normal conditions. Although this measuring system. The chamber was modified to be fully controlled
result indicated that larvae of M. ruficauda are influenced by by the low cost and easy to use Arduino technology, which has
barometric pressure, it was only a correlational study and only the already been used in the laboratory to develop other experimental
response to host odours was tested. devices. We used an Arduino UNO with a BMP085 pressure sensor
In the present work, we investigated whether changes in the (Bosch) to take measurements of the barometric pressure. A vacuum
magnitude and duration of a decrease in barometric pressure hinders pump (DvrII, DOSIVAC, Argentina) was connected to the
the orientation to the host in M. ruficauda larvae. In particular, we chamber’s valve system through a tube and controlled by the
studied whether larvae raised under different larval density Arduino through a solid-state relay (Fig. 2).
conditions exhibited a differential host orientation behaviour
when exposed to different scenarios of barometric pressure. Barometric pressure patterns
Finally, we studied whether orientation to parasitized hosts was To test for the effects of the duration and magnitude of the barometric
affected in larvae under high larval density under conditions of a pressure decrease on the larval orientation mechanism during host
high decrease of barometric pressure. location, we exposed the larvae to different scenarios (Fig. 3). These
scenarios were combinations of a fixed duration and a fixed
MATERIALS AND METHODS magnitude of pressure decrease from normal initial pressure values
Ethical note (at least 1010 hPa). In each scenario, the pressure decrease could be
No licences or permits were required for this research. During progressive for 1 h, or direct, and the magnitude could be set up at
experiments, the larvae and hosts were not harmed. After the 12 hPa (moderate decrease) or 24 hPa (strong decrease). In normal
experiments, both larvae and hosts were raised until reaching the conditions, no pressure decrease was applied, but the pressure was
adult stage, and then released. maintained at its initial value. As an intermediate condition between
1 h and direct pressure decreases, durations of 30 min were also fixed
Insects for 12 hPa scenarios. The normal initial pressure value was chosen
Egg clutches of Mallophora ruficauda Wiedemann 1828 were because it is the normal mean barometric pressure value in the zone
collected from dry standing grasses near apiaries in different of the experiments. These data were obtained from a nearby weather
localities of the province of Buenos Aires (Mercedes 34°37′S, 59° station (Fig. S1). In turn, the moderate and strong decrease values

Journal of Experimental Biology

27′W, Luján 34°35′S, 59′4′W, Olivera 34°37′S, 59°12′W), were chosen after analyzing the barometric pressure drops before the
Argentina, during the summers of 2021–2022 and 2022–2023 onset of rains (for an example, see Fig. S2).
and kept in the laboratory in individual tubes. After hatching, larvae
were separated in flasks with 100 ml of potting soil (humidity 45– Behavioural experiments
55%) and kept in boxes in complete darkness at 25±1°C until used All behavioural experiments were performed in complete darkness
in the experiments. Each flask was filled with larvae from different between 08:00 and 17:00 h at 25±1°C room temperature and an
clutches to eliminate possible effects of egg clutch. As the larval average relative humidity of 65±5%. Also, experiments were carried
rearing density has previously been shown to modulate larval host- out only when barometric pressure had been steady at normal values
seeking behaviour (Crespo et al., 2015; Martínez et al., 2017), we (≥1010 hPa) for at least 24 h prior to the beginning of the
raised larvae under different densities that simulated low and high experiments. The olfactometry device consisted of a plastic box that
intensity of preparasitism intraspecific competition. The low- contained two experimental arenas, i.e. two dual election air-
intensity level of preparasitism competition treatment consisted of stationary olfactometers, each divided in three equal rectangular
placing 100 larvae per flask with 100 ml of potting soil (low-density zones (Crespo and Castelo, 2012) (Fig. 2). For each experimental
group). This treatment results in selective larvae with preference for arena, a live host (C. signaticollis larva) was placed in one lateral
healthy third instar larva of C. signaticollis. On the contrary, the zone as stimulus (S), while the other lateral zone remained empty
high-intensity level of preparasitism competition treatment and served as control (C). For each experiment, a second instar larva

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

‘’ Pressure, temperature, time, date Fig. 2. Experimental device used

SD 1018,25.91,11:53:54,21/03/2022 in this study. A vacuum desiccator
card 1017,25.94,11:54:07,21/03/2022 was modified to be controlled by an
1012,26.00,11:55:07,21/03/2022 Arduino UNO. A vacuum pump was
1013,26.10,11:56:41,21/03/2022
controlled to generate the different
1013,26.12,11:57:21,21/03/2022
ARDUINO 1013,26.14,11:58:14,21/03/2022 patterns of barometric pressure
1013,26.16,11:59:10,21/03/2022 decrease. Barometric pressure
1013,26.17,12:00:17,21/03/2022 inside the chamber was saved on
‘’ an SD card. (1) Representation of
each of the four experimental
4 arenas used per trial. The inset
3 shows a diagram of the two dual-
choice olfactometers used in the
experimental arenas. (2) Vacuum
desiccator. (3) BMP085 sensor to
monitor barometric pressure inside
the chamber. (4) Arduino UNO used
2 for sensing and controlling the
vacuum pump. (5) Vacuum pump
used to generate the barometric
pressure decrease.

5 1

Stimulus Non-decision Control

? ?

Cyclocephala Mallophora
signaticollis ruficauda

? ?

of M. ruficauda was placed in the centre of the middle zone. After competition regime and larvae raised under a high-intensity
1 h in the dark, its position in the arena was registered. Three preparasitism competition regime. This experiment aimed to study

Journal of Experimental Biology

responses were possible: (1) the larva could orient to the host (S) if the effect of barometric pressure decrease on the orientation
the larva was found in the zone where the host was placed, (2) the response on larvae with different selectivity thresholds. The second
larva could orient to the control (C) if the larva was found in the series of experiments aimed to study the effect of the decrease in
opposite empty zone, or (3) the response was classed as undecided barometric pressure on the response of selective larvae to hosts of
(ND) if the larva remained in the central zone. The lateral zones different quality. For this, we compared the orientation response to
were separated from the central zone by plastic grids, which healthy third instar hosts and singly parasitized third instar hosts.
prevented host escape from the S zone but allowed host-seeking
larvae to move along the entire box. Between trials, the olfactometer Statistical analysis
was cleaned with non-ionic detergent and water to remove any In order to study the effects of barometric pressure on the orientation
possible odour. In each trial, up to four olfactometers were placed in mechanism, we analysed two behaviours. First, we analysed larvae
the pressure chamber, i.e. eight larvae. Each treatment was repeated that were found either on the stimulus side (S) or the control side
until the number of larvae that left the release zone (S or C) or the (C). Larvae with this behaviour were considered as showing a
number of undecided larvae (ND) reached at least 30. directed response towards or against the stimulus. We also analysed
Two experimental series were performed. In the first series, the the case where larvae were found in the centre of the arena, the no
orientation response to healthy third instar hosts was evaluated decision zone (ND). These larvae were considered as performing
between larvae raised under a low-intensity preparasitism non-directional movements.

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

A Control B 1 | 12 hPa C 1 | 24 hPa

Pi Pi Pi

–12 hPa –12 hPa –12 hPa

–24 hPa –24 hPa –24 hPa

0 0.5 1 0 0.5 1 0 0.5 1

Time (h) Time (h) Time (h)

Density Host quality N Density Host quality N Density Host quality N

Healthy 47 Healthy 39 Healthy 61
Low Low Low
Parasitized 57 Parasitized 47 Parasitized 55
High Healthy 39 High Healthy 40 High Healthy 47

D E F
30 min | 12 hPa Direct | 12 hPa Direct | 24 hPa

Pi Pi Pi

–12 hPa –12 hPa –12 hPa

–24 hPa –24 hPa –24 hPa

0 0.5 1 0 0.5 1 0 0.5 1

Time (h) Time (h) Time (h)

Density Host quality N Density Host quality N Density Host quality N

Healthy 47 Healthy 62 Healthy 59
Low Low Low
Parasitized 46 Parasitized 43 Parasitized 48
High Healthy 46 High Healthy 63 High Healthy 39
Fig. 3. Patterns of barometric pressure decrease applied to study the effect of the duration and magnitude of the decrease on the orientation
mechanism of M. ruficauda larvae under two levels of density (i.e. intensity of preparasitism competition) and host quality. (A) Control (no pressure
decrease applied). (B) Decrease of 12 hPa for 1 h. (C) Decrease of 24 hPa for 1 h. (D) Decrease of 12 hPa for 30 min. (E) Direct decrease of 12 hPa.
(F) Direct decrease of 24 hPa. White areas represent time windows during which experiments are carried out. Orange lines show the time course of each
pressure change applied in the experimental device. Pi, initial pressure (≥1010 hPa). N, number of replicates for each treatment.

Journal of Experimental Biology

The probability of larvae to orient to the host was analysed with a the same flask were used. For each treatment, between five and
generalised linear mixed model (GLMM) with logit link function seven flasks were used. Every time the parasitoid larvae oriented to
and binomial distribution. The logit link function ensures fitted a host was counted as a success, noted with a 1, otherwise, a 0 was
values between 0 and 1, and the binomial distribution is typically registered. Hence, this model included both fixed factors with their
used for probability data. As predictors, we used the combination of interaction ( pattern of pressure decrease and intensity of
duration and magnitude conditions [fixed categorical predictor with preparasitism competition) and one random factor. Larvae that did
six levels: (1) control, (2) 1 h | 12 hPa, (3) 1 h | 24 hPa, (4) 30 min | not exhibit directed movement and remained in the centre of the
12 hPa, (5) direct | 12 hPa, and (6) direct | 24 hPa], and the intensity arena (ND) were excluded from this analysis.
of preparasitism intraspecific competition [categorical with two In order to study the effect of the decrease in barometric pressure
levels: (1) high and (2) low]. To incorporate the dependency among on the motivation of larvae to initiate exploratory movements, we
observations of the same olfactometry device (recall each performed a similar model as before but now the larvae that
olfactometer consisted of two arenas), we used the olfactometer as remained in the middle zone of the arena were noted with a 1, and 0
a random factor. This random factor accounted for the different if larvae were found either on the stimulus or on the control zone.
flasks used for each experiment because in every trial, larvae from The model was constructed with the same predictors as before.

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

Second, to test how barometric pressure decrease modulate the centre of the olfactometer (Table 2). Interestingly, selective larvae
response of selective larvae to hosts of different quality, we analysed showed a marginal probability to remain in the middle zone when
the response by means of another GLMM. In this case, fixed factors barometric pressure decreased 12 hPa for 30 min (the confidence
were the conditions of barometric pressure decrease (categorical interval marginally includes a 0.5 probability; Table 2). However,
with the same levels as in the first model) and host quality for a decrease of 24 hPa in 1 h, a high probability to remain in the
[categorical with two levels: (1) healthy and (2) parasitised], and as middle zone was found (Table 2). In turn, non-selective larvae
a random factor we included the olfactometer. Note that a showed a high probability of remaining in the middle zone under a
suboptimal host consisted of a third instar C. signaticollis larva 1-h 24 hPa decrease and a direct 12 hPa decrease. Hence, motivation
previously parasitised by one M. ruficauda larva. Finally, the same to undertake host searching was affected by the same slope
analysis as before was used to study the effects of the different (Table 2). In other words, selective larvae, given their very reduced
scenarios of pressure decrease on the probability of selective larvae host range, would stop searching for white grubs as soon as or very
to initiate exploratory movements. This final model included the quickly after the pressure drop began because the probability of
same fixed factors as before, but larvae that remained in the middle finding healthy hosts is low compared with the risk of mortality
zone were coded a 1 and larvae that were found either on the (Fig. 4A), whereas non-selective larvae have more chances to
stimulus or the control zone were coded with a 0. parasitize hosts because of a wider host range that would keep them
All analyses were performed using R v3.6.3 ‘Holding the searching for hosts until an upper limit is reached (Fig. 4B).
Windsock’ software (https://www.r-project.org/). The packages
glmmTMB (Brooks et al., 2017) and nlme (https://CRAN.R-project. Effects of a pressure decrease on orientation to suboptimal
org/package=nlme) were used to fit the models. For testing model hosts (host selectivity)
assumptions, we used the package DHARMa (https://CRAN.R- We found that larvae orient randomly to the parasitized host when
project.org/package=DHARMa). Graphs were made using the exposed to a barometric decrease of 12 hPa in 1 h (Table 3). In turn,
package ggplot2 (https://CRAN.R-project.org/package=ggplot2). larvae orient randomly to the healthy host when exposed to a
Tukey contrasts were performed with the emmeans function of the barometric decrease of 12 hPa in 30 min (Table 3). These results
package emmeans (https://CRAN.R-project.org/package=emmeans). show that larvae have similar behaviours but respond to slightly
different conditions. The other condition that showed a random
RESULTS orientation behaviour to parasitized hosts was when larvae were
Effects of a pressure decrease on host-seeking behaviour exposed to a direct decrease of 24 hPa (Table 3).
under different levels of larval density Also, higher probabilities of remaining in the middle zone under
Larvae reared at low density (selective) oriented to hosts under every condition were found (Table 4). Conditions where barometric
control conditions of barometric pressure, i.e. in the absence of pressure decreased in time (i.e not a direct decrease) did not
pressure drop (Table 1). Host orientation was high in all the substantially increase the probability of larvae remaining in the
conditions except for the 12 hPa decrease in 30 min, where larvae middle zone compared with the control (Table 4). However, larvae
have a random probability of finding a host. However, as evidenced exposed to a direct decrease in barometric pressure of 24 hPa
by the odds ratio value, the chances of host orientation occurring showed an increased probability of remaining in the middle zone. In
were not significantly lower compared with control conditions, so fact, this condition induced a 2-fold increase in the probability of
this result should be interpreted carefully (Table 1). A similar remaining in the release zone compared with the control (Table 4).
situation was found for high-density reared larvae (non-selective),
where host orientation was found in almost every treatment except DISCUSSION
for the 1-h 24 hPa decrease, where larvae have a random probability The present study aimed to investigate how decreases in barometric
of finding a host. In addition, the odds ratio against the control was pressure influence host-seeking behaviour in larvae of the parasitoid
similar, indicating that the effect is not so strong (Table 1). M. ruficauda. The decrease in barometric pressure is a typical
Regarding the tendency to leave the release zone, most selective condition prior to the onset of a storm. Indeed, fast decreases in
and non-selective larvae showed a low probability to remain in the barometric pressure are usually preceded by big storms in natural

Table 1. Summary of the results of the probability of host orientation in Mallophora ruficauda under different conditions of preparasitism

Journal of Experimental Biology

competition
Larval density Pressure pattern NR Pr(S) (LCI, UCI) OR (LCI, UCI) P-value
Low Control 35 0.861 (0.696, 0.944)* – –
1 h – 12 hPa 30 0.772 (0.578, 0.893)* 0.55 (0.11, 2.83) 0.776
0.5 h – 12 hPa 30 0.677 (0.480, 0.827) 0.34 (0.07, 1.64) 0.288
1 h – 24 hPa 34 0.766 (0.583, 0.885)* 0.53 (0.11, 2.63) 0.734
Direct – 12 hPa 55 0.733 (0.585, 0.842)* 0.44 (0.10, 1.89) 0.469
Direct – 24 hPa 38 0.688 (0.511, 0.824)* 0.36 (0.08, 1.62) 0.297
High Control 31 0.748 (0.555, 0.875)* – –
1 h – 12 hPa 31 0.711 (0.517, 0.850)* 0.83 (0.20, 3.56) 0.985
0.5 h – 12 hPa 33 0.851 (0.677, 0.940)* 1.93 (0.38, 9.71) 0.719
1 h – 24 hPa 15 0.654 (0.381, 0.853) 0.64 (0.11, 3.68) 0.908
Direct – 12 hPa 35 0.850 (0.675, 0.939)* 1.91 (0.38, 9.63) 0.729
Direct – 24 hPa 32 0.789 (0.604, 0.901)* 1.26 (0.28, 5.70) 0.975
NR, number of larvae actively deploying locomotory movements. Pr(S), estimated probability to orient to hosts. *Indication of significant orientation to hosts against
a random search. OR, odds ratio between the treatment and the control. LCI and UCI, respective lower and upper confidence intervals for the estimated probability
and the odds ratio. A treatment was significantly different from the control when P<0.05.

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

Table 2. Summary of the results of the probability of undertaking host searching in M. ruficauda larvae raised under different intensities of
preparasitism competition
Larval density Pressure pattern NND Pr (ND) (LCI, UCI) OR (LCI, UCI) P-value
Low Control 12 0.255 (0.151, 0.398)* – –
1 h – 12 hPa 9 0.231 (0.125, 0.387)* 0.88 (0.24, 3.14) 0.991
0.5 h – 12 hPa 17 0.362 (0.238, 0.507) 1.66 (0.53, 5.17) 0.666
1 h – 24 hPa 27 0.443 (0.324, 0.568) 2.32 (0.80, 6.73) 0.177
Direct – 12 hPa 7 0.113 (0.055, 0.218)* 0.37 (0.10, 1.39) 0.213
Direct – 24 hPa 21 0.356 (0.245, 0.485)* 1.61 (0.54, 4.79) 0.670
High Control 8 0.205 (0.106, 0.360)* – –
1 h – 12 hPa 9 0.225 (0.121, 0.379)* 1.13 (0.28, 4.49) 0.995
0.5 h – 12 hPa 13 0.283 (0.172, 0.428)* 1.53 (0.42, 5.59) 0.832
1 h – 24 hPa 32 0.681 (0.536, 0.798)* 8.27 (2.31, 29.59) <0.001*
Direct – 12 hPa 28 0.459 (0.339, 0.584) 3.29 (0.99, 10.84) 0.051
Direct – 24 hPa 7 0.179 (0.088, 0.331)* 0.85 (0.20, 3.62) 0.989
NND, number of larvae staying in the release zone. *Indication of significant orientation to hosts against a random search. Pr(ND), estimated probability of non-
decision. OR, odds ratio between the treatment and the control. LCI and UCI: respective lower and upper confidence intervals for the estimated probability and the
odds ratio. A treatment was significantly different from the control when P<0.05.

weather. We studied the effects of the magnitude and the duration of a examined the effect of changing barometric pressure on host
pressure decrease on the non-directed responses and directed orientation odours (Crespo and Castelo, 2012). However, there are
responses to host chemical cues in selective and non-selective substantial differences between both studies. In the present study, we
larvae. Additionally, we explored whether the pressure decreases managed to control precisely the barometric pressure differences,
modulated host selectivity by selective larvae. In a previous study, we whereas in the previous study, only correlational patterns were
analysed. Also, we studied the effect of both selective and non-
selective larvae on orientation to both healthy and parasitised hosts.
Low larval density
A And finally, the present study shows robust responses because we
Pi studied the response to whole live hosts instead of host odours.
Optimal conditions From a physiological point of view, the effects of weather
Adverse conditions conditions on the orientation of insects to odorant cues are associated
–12 hPa Avoidance
with their ability to locate these cues in the environment, as may be
the case of the plum curculio Conotrachelus nenuphar, which stops
Unperceived
discriminating fruit odours in olfactometry experiments when
Pressure change barometric pressure decreases (Leskey and Prokopy, 2003).
–24 hPa
Therefore, the effects of a pressure decrease on host orientation in
M. ruficauda larvae likely occur through the sensilla previously
0 0.5 1
identified on maxillary palps and responsible for responding to host
Time (h)
chemical cues (Crespo et al., 2011; Pueyrredon et al., 2017).
B High larval density However, none of the scenarios of pressure decrease that were
applied affected M. ruficauda orientation to the host in a significant
Pi way. The reduced activity was due to a lack of motivation to
undertake host-searching rather than an inability of larvae to find
white grubs. Indeed, under scenarios affecting host-seeking
–12 hPa behaviour, most larvae remained in the centre of the olfactometer,
but a main proportion of individuals searching for hosts found them.
Both selective and non-selective larvae stopped searching for white

Journal of Experimental Biology

–24 hPa grubs under a 1-h 24 hPa decrease of pressure, whereas they sought
hosts under a 1-h 12 hPa decrease, strongly suggesting the existence
0 0.5 1 of an intermediate slope of pressure decrease affecting motivation
Time (h) independently of preparasitism competition. Selective larvae
stopped searching for hosts more quickly, before the pressure drop
Fig. 4. Effects of barometric pressure decrease on M. ruficauda host
reached 12 hPa, whereas non-selective larvae were affected before
seeking behaviour under different conditions of preparasitism
competition. (A) Effects on selective larvae (larvae experiencing low levels
the drop reached 24 hPa. It is unknown whether the time passed since
of competition owing to a low number of conspecifics). (B) Effects on non- the beginning of the pressure decrease is the only factor setting these
selective larvae. Grey areas represent time windows before and after respective limits or whether the magnitude of the drop has to be
experiments. White areas represent optimal conditions of barometric considered. Nevertheless, this agrees with a previous estimation of a
pressure making larvae strongly likely to search for hosts. Yellow areas very small threshold of pressure drop above which selective larvae
represent adverse pressure conditions increasing the risk for survival and host-seeking behaviour was affected (Crespo and Castelo, 2012).
parasitism success. Dashed yellow areas mark an avoidance strategy,
where larvae stop undertaking host searching. Orange lines show the time
Thus, we show that preparasitism competition modulates the onset of
course of each pressure change applied in the experimental device. Blue larval response to pressure decrease.
areas represent a hypothetical physiological limit in the ability to perceive For many adult insects, drops in barometric pressure reflect
pressure decrease. Pi, initial pressure (≥1010 hPa). arriving bad weather conditions such as a storm that can kill them.

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

Table 3. Summary of the results of the probability of selective M. ruficauda larvae to orient to healthy and parasitized hosts
Host quality Pressure pattern NR Pr(S) (LCI , UCI) OR (LCI , UCI) P-value
Healthy Control 35 0.859 (0.696, 0.942)* – –
1 h – 12 hPa 30 0.770 (0.580, 0.890)* 0.55 (0.11, 2.83) 0.778
0.5 h – 12 hPa 30 0.674 (0.481, 0.822) 0.34 (0.07, 1.63) 0.285
1 h – 24 hPa 34 0.766 (0.588, 0.883)* 0.54 (0.11, 2.65) 0.745
Direct – 12 hPa 55 0.730 (0.588, 0.837)* 0.44 (0.10, 1.88) 0.468
Direct – 24 hPa 38 0.689 (0.516, 0.821)* 0.36 (0.08, 1.64) 0.307
Parasitized Control 35 0.898 (0.722, 0.968)* – –
1 h – 12 hPa 31 0.674 (0.483, 0.821) 0.23 (0.04, 1.46) 0.173
0.5 h – 12 hPa 31 0.805 (0.621, 0.912)* 0.47 (0.07, 3.22) 0.738
1 h – 24 hPa 31 0.811 (0.630, 0.916)* 0.49 (0.07, 3.34) 0.767
Direct – 12 hPa 34 0.771 (0.594, 0.886)* 0.38 (0.06, 2.43) 0.537
Direct – 24 hPa 15 0.521 (0.276, 0.757) 0.12 (0.02, 0.95) 0.041*
NR, number of larvae actively deploying locomotory movements. Pr(S), estimated probability to orient to hosts. *Indication of significant orientation to hosts against
a random search. OR, odds ratio between the treatment and the control. LCI and UCI, respective lower and upper confidence intervals for the estimated probability
and the odds ratio. A treatment was significantly different from the control when P<0.05.

Perceiving these pressure drops triggers behaviours associated with because of differences in their host range. This could indicate that
avoidance strategies. For instance, field experiments suggest that a M. ruficauda larvae evolved behavioural avoidance strategies based
decrease in barometric pressure inhibits flight in the parasitoid wasp on the perception of a transient decrease in barometric pressure.
Cotesia glomerata, and reduces its mortality risk (Vosteen et al., For instance, Sujimoto et al. (2020) showed that worker ants
2020). Leptopilina heterotoma wasps superparasitize more often change their foraging behaviour and exit the nest more frequently in
after a drop in barometric pressure, which is associated with reduced response to drops in barometric pressure. Physiologically, it is
life expectancy (Roitberg et al., 1993). This type of behaviour can conceivable that, when facing temporary adverse pressure
be interpreted as risk-prone behaviour caused by a decrease in the conditions, host chemical cues are perceived by M. ruficauda
expected reproductive success owing to reduced expected survival larvae but processed in a different way by their central system,
(Wajnberg et al., 2008). Hence, in M. ruficauda larvae, switching resulting in unresponsiveness of larvae to host odours. For instance,
between taxis and kinesis in response to pressure decrease also Barrozo et al. (2010) showed that in newly mated males of the moth
could be an avoidance strategy, as their small size could Agrotis ipsilon, the female sex pheromone processed by central
significantly affect parasitism success and survival while foraging neurons has an inhibitory effect on attraction when the reproductive
for hosts in bad weather conditions. The results that we obtained glands are empty, which allows them to save energy. This energy
applying non-direct decreases are in accordance with this savings can be allocated to host searching when optimal pressure
hypothesis. On the one hand, host searching occurred in absence conditions return. We hypothesize that the perception of pressure
of pressure decrease and even under a very slow decrease of drops by M. ruficauda larvae is associated with the presence of
pressure. In these conditions, the risk for survival is minimal specific anatomical structures. For instance, the antennae of other
compared with the chances to find and parasitize hosts, which insects such as the cockroach Periplaneta americana and the stick
would explain that most larvae sought for hosts. On the other hand, insect Caurausius morosus exhibit hygroreceptive sensilla that also
higher slopes of pressure decrease may indicate significantly respond to changes in air pressure, although the responses to
adverse conditions that can increase the risk of mortality. Under pressure were lower than to humidity changes (Tichy and Kallina,
these conditions, larvae would adopt a strategic behavioural 2010). To date, pressure-sensitive structures remain to be identified
response modulated by the preparasitism competition they were not only in second-instar larvae, but also in insects in general. Also,
exposed to. In fact, selective larvae seem to be more affected by it is possible that larvae, because of their soft and flexible cuticles,
decrease in barometric pressure than non-selective larvae, probably show these adaptive responses (Azevedo et al., 2023). In this

Journal of Experimental Biology

Table 4. Summary of the results of the probability of selective M. ruficauda larvae to undertake searching for healthy and parasitized hosts
Host quality Pressure pattern NND Pr(ND) (LCI , UCI) OR (LCI , UCI) P-value
Healthy Control 12 0.255 (0.151, 0.398)* – –
1 h – 12 hPa 9 0.231 (0.125, 0.387)* 0.88 (0.24, 3.14) 0.991
0.5 h – 12 hPa 17 0.362 (0.238, 0.507) 1.65 (0.53, 5.17) 0.666
1 h – 24 hPa 27 0.443 (0.324, 0.568) 2.31 (0.80, 6.72) 0.177
Direct – 12 hPa 7 0.113 (0.055, 0.218)* 0.37 (0.10, 1.39) 0.213
Direct – 24 hPa 21 0.356 (0.245, 0.485)* 1.61 (0.54, 4.78) 0.669
Parasitized Control 22 0.420 (0.292, 0.559) – –
1 h – 12 hPa 16 0.340 (0.220, 0.485)* 0.71 (0.25, 2.06) 0.840
0.5 h – 12 hPa 15 0.326 (0.207, 0.473)* 0.67 (0.23, 1.96) 0.765
1 h – 24 hPa 24 0.436 (0.312, 0.569) 1.07 (0.39, 2.90) 0.997
Direct – 12 hPa 9 0.209 (0.113, 0.356)* 0.37 (0.11, 1.20) 0.130
Direct – 24 hPa 33 0.688 (0.544, 0.802)* 3.04 (1.04, 8.84) 0.038*
NND, number of larvae staying in the release zone. Pr(ND), estimated probability of non-decision. *Indication of significant orientation to hosts against a random
search. OR, odds ratio between the treatment and the control. LCI and UCI, respective lower and upper confidence intervals for the estimated probability and the
odds ratio. A treatment was significantly different from the control when P<0.05.

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RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

context, larvae may not be perceiving extreme pressure drops, Adonyeva, N. V., Menshanov, P. N. and Gruntenko, N. (2021). A link between
atmospheric pressure and fertility of drosophila laboratory strains. Insects 12, 947.
eliciting a host-seeking behaviour similar to that evoked under doi:10.3390/insects12100947
favourable pressure conditions. Consequently, in the face of a direct Alvarado, L. (1980). Sistemá tica y bionomı́a de los estados inmaduros de
decrease, the influence of other parameters cannot be ignored. coleó pteros Scarabaeidae que habitan en el suelo. PhD thesis, Universidad
In the present study, we investigated whether a decrease in Nacional de La Plata, La Plata, Argentina.
Amat, I., Castelo, M., Desouhant, E. and Bernstein, C. (2006). The influence of
barometric pressure impacted selectivity for hosts in M. ruficauda temperature and host availability on the host exploitation strategies of sexual and
selective larvae. Effects of abiotic factors on host preference are asexual parasitic wasps of the same species. Oecologia 148, 153-161. doi:10.
described in other insects, such as foraging females of the aphid 1007/s00442-005-0332-9
Azevedo, K. E. X., Magalhaes, ̃ D. M., de Andrade Moral, R. and Bento, J. M. S.
parasitoid Aphidius ervi, which attack low-quality hosts more (2023). Weathering the hunt: the role of barometric pressure in predator insects’
frequently at high temperatures that they associate with a reduced foraging behaviour. Ecol. Evol. 13, e10416. doi:10.1002/ece3.10416
life expectancy and a low reproductive success (Moiroux et al., Barrozo, R. B., Gadenne, C. and Anton, S. (2010). Switching attraction to
2015). Therefore, we might infer that drops in barometric pressure inhibition: mating-induced reversed role of sex pheromone in an insect. J. Exp.
Biol. 213, 2933-2939. doi:10.1242/jeb.043430
would make M. ruficauda selective larvae search for suboptimal Bernklau, E. J., Fromm, E. A. and Bjostad, L. B. (2004). Disruption of host location
hosts more readily, as their chances to find and parasitize optimal of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon
hosts are low. As expected, high levels of unwillingness to dioxide. J. Econ. Entomol. 97, 330-339. doi:10.1093/jee/97.2.330
Bodlah, M. A., Zhu, A.-X. and Liu, X.-D. (2016). Host choice, settling and folding
undertake host searching were observed in larvae in the absence leaf behaviors of the larval rice leaf folder under heat stress. Bull. Entomol. Res.
of a pressure decrease, as demonstrated by larvae showing high 106, 809-817. doi:10.1017/S0007485316000584
probabilities of remaining in the middle zone of the arena in all non- Brodeur, J. and Boivin, G. (2004). Functional ecology of immature parasitoids.
Annu. Rev. Entomol. 49, 27-49. doi:10.1146/annurev.ento.49.061703.153618
direct pressure decrease scenarios. Thus, barometric pressure may Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W.,
be acting as an environmental cue that influences locomotor Nielsen, A., Skaug, H. J., Mä chler, M. and Bolker, B. M. (2017). glmmTMB
response and may not be a factor modulating host selectivity in M. balances speed and flexibility among packages for zero-inflated generalized
ruficauda. linear mixed modeling. R. J. 9, 378-400. doi:10.32614/rj-2017-066
Castelo, M. K. and Capurro, A. F. (2000). Especificidad y denso-dependencia
In conclusion, our study shows that barometric pressure is an inversa en parasitoides con oviposició n fuera del hospedador: el caso de
important abiotic factor that modulates host seeking behaviour in Mallophora ruficauda (Diptera: Asilidae) en la pampa argentina. Ecol. Austral 10,
underground larvae. Hence, barometric pressure could act as an 89-101.
Castelo, M. K. and Corley, J. C. (2004). Oviposition behavior in the robber fly
important indicator of environmental conditions in the soil where Mallaphora ruficauda (Diptera: Asilidae). Ann. Entomol. Soc. Am. 97, 1050-1054.
changes in light or temperature are not very noticeable. Also, our doi:10.1603/0013-8746(2004)097[1050:OBITRF]2.0.CO;2
results contribute to predicting the incidence of parasitism of M. Castelo, M. K. and Crespo, J. E. (2022). Microorganismal cues involved in host-
ruficauda. In rainy summers, less parasitism should be expected than location in Asilidae parasitoids. Biology (Basel) 11, 129. doi:10.3390/
biology11010129
in dry summers. Hence, an important prediction derived from this Castelo, M. K. and Lazzari, C. R. (2004). Host-seeking behavior in larvae of the
work is that rainy years should be followed by a decreased abundance robber fly Mallophora ruficauda (Diptera: Asilidae). J. Insect Physiol. 50, 331-336.
of adults in the next season. It would be interesting to test this doi:10.1016/j.jinsphys.2004.02.002
Castelo, M. K., Ney-Nifle, M., Corley, J. C. and Bernstein, C. (2006). Oviposition
hypothesis through a nation-wide survey of the presence of adult height increases parasitism success by the robber fly Mallophora ruficauda
M. ruficauda in different areas associated with rainy conditions. (Diptera: Asilidae). Behav. Ecol. Sociobiol. 61, 231-243.
Chen, Y. and Seybold, S. J. (2014). Crepuscular flight activity of an invasive insect
Acknowledgements governed by interacting abiotic factors. PLoS ONE 9, e105945. doi:10.1371/
We thank many of the bee farmers, especially Carlos Schwindt, for their help and journal.pone.0105945
Crespo, J. E. and Castelo, M. K. (2012). Barometric pressure influences host-
willingness to let us work in their fields.
orientation behavior in the larva of a dipteran ectoparasitoid. J. Insect Physiol. 58,
1562-1567. doi:10.1016/j.jinsphys.2012.09.010
Competing interests Crespo, J. E. and Castelo, M. K. (2009). Insights to host discrimination and host
The authors declare no competing or financial interests. acceptance behaviour in a parasitoid (Diptera: Asilidae): implications for fitness.
J. Insect Physiol. 55, 1072-1078. doi:10.1016/j.jinsphys.2009.08.002
Author contributions Crespo, J. E. and Castelo, M. K. (2008). The ontogeny of host-seeking behaviour in
a parasitoid dipteran. J. Insect Physiol. 54, 842-847. doi:10.1016/j.jinsphys.2008.
Conceptualization: M.K.C., J.E.C.; Methodology: J.E.C.; Software: J.E.C.; Formal
03.002
analysis: J.E.C.; Investigation: J.-N.H.; Resources: M.K.C.; Data curation: J.-N.H.;
Crespo, J. E., Lazzari, C. R. and Castelo, M. K. (2011). Orientation mechanisms
Writing - original draft: J.-N.H.; Writing - review & editing: J.-N.H., M.K.C., J.E.C.;
and sensory organs involved in host location in a dipteran parasitoid larva.
Supervision: M.K.C., J.E.C.; Project administration: M.K.C.; Funding acquisition: J. Insect Physiol. 57, 191-196. doi:10.1016/j.jinsphys.2010.11.010

Journal of Experimental Biology

M.K.C., J.E.C. Crespo, J. E., Martı́nez, G. A. and Castelo, M. K. (2015). Exposure to competitors
influences parasitism decisions in ectoparasitoid fly larvae. Anim. Behav. 100,
Funding 38-43. doi:10.1016/j.anbehav.2014.11.005
This work was supported by the Consejo Nacional de Investigaciones Cientı́ficas y de Rijk, M., Dicke, M. and Poelman, E. H. (2013). Foraging behaviour by
Té cnicas (grant PIP 2021-2023 no. 11220200101939CO to J.E.C.), the University of parasitoids in multiherbivore communities. Anim. Behav. 85, 1517-1528. doi:10.
Buenos Aires, Argentina (grant UBACyT 2020 no. 20020190100059BA to M.K.C.), 1016/j.anbehav.2013.03.034
and the Agencia Nacional de Promoció n de la Investigació n, el Desarrollo Drake, V. (1994). The influence of weather and climate on agriculturally important
Tecnoló gico y la Innovació n - FONCyT (grant PICT 2019 no. 2019-I-A-00975 to insects: an Australian perspective. Aust. J. Agric. Res. 45, 487-509.
M.K.C.). Eggleton, P. and Belshaw, R. (1992). Insect parasitoids: an evolutionary overview.
Philos. Trans. Biol. Sci. 337, 1-20.
Farji-Brener, A. G., Dalton, M. C., Balza, U., Courtis, A., Lemus-Domı́nguez, I.,
Data availability Ferná ndez-Hilario, R. and Cá ceres-Levi, D. (2018). Working in the rain? Why
All data can be found in the Harvard Dataverse repository at https://doi.org/10.7910/ leaf-cutting ants stop foraging when it’s raining. Insectes Soc. 65, 233-239. doi:10.
DVN/CQM6HR. 1007/s00040-018-0605-z
Feener, D. H. J. and Brown, B. V. (1997). Diptera as parasitoids. Annu. Rev.
References Entomol. 42, 73-97. doi:10.1146/annurev.ento.42.1.73
Aartsma, Y., Cusumano, A., Ferná ndez de Bobadilla, M., Rusman, Q., Vosteen, Fink, U. and Vö lkl, W. (1995). The effect of abiotic factors on foraging and
I. and Poelman, E. H. (2019). Understanding insect foraging in complex habitats oviposition success of the aphid parasitoid, Aphidius rosae. Oecologia 103,
by comparing trophic levels: insights from specialist host-parasitoid- 371-378. doi:10.1007/BF00328627
hyperparasitoid systems. Curr. Opin. Insect Sci. 32, 54-60. doi:10.1016/j.cois. Fournier, F., Pelletier, D., Vigneault, C., Goyette, B. and Boivin, G. (2005). Effect
2018.11.001 of barometric pressure on flight initiation by Trichogramma pretiosum and

9
RESEARCH ARTICLE Journal of Experimental Biology (2024) 227, jeb247530. doi:10.1242/jeb.247530

Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Environ. Morimoto, J., Nguyen, B., Tabrizi, S. T., Ponton, F. and Taylor, P. (2018). Social
Entomol. 34, 1534-1540. doi:10.1603/0046-225X-34.6.1534 and nutritional factors shape larval aggregation, foraging, and body mass in a
Gaylord, M. L., Williams, K. K., Hofstetter, R. W., McMillin, J. D., Degomez, T. E. polyphagous fly. Sci. Rep. 8, 14750. doi:10.1038/s41598-018-32930-0
and Wagner, M. R. (2008). Influence of temperature on spring flight initiation for Pellegrino, A. C., Peñaflor, M. F. G. V., Nardi, C., Bezner-Kerr, W., Guglielmo,
southwestern ponderosa pine bark beetles (Coleoptera: Curculionidae, C. G., Bento, J. M. S. and McNeil, J. N. (2013). Weather forecasting by insects:
Scolytinae). Environ. Entomol. 37, 57-69. doi:10.1603/0046-225x(2008)37[57: modified sexual behaviour in response to atmospheric pressure changes. PLoS
iotosf ]2.0.co;2 ONE 8, e75004. doi:10.1371/journal.pone.0075004
Godfray, H. C.J. (1994). Parasitoids: Behavioral and Evolutionary Ecology. Polatto, L. P., Chaud-Netto, J. and Alves-Junior, V. V. (2014). Influence of abiotic
Princeton University Press. factors and floral resource availability on daily foraging activity of bees. J. Insect
Groba, H. F. and Castelo, M. K. (2016). Host gut microorganisms’ cues mediate Behav. 27, 593-612. doi:10.1007/s10905-014-9452-6
orientation behaviour in the larva of the parasitoid Mallophora ruficauda. Bull. Pueyrredon, J. M., Crespo, J. E. and Castelo, M. K. (2017). Functional sensorial
Entomol. Res. 106, 81-90. doi:10.1017/S0007485315000838 complementation during host orientation in an Asilidae parasitoid larva. Bull.
Groba, H. F. and Castelo, M. K. (2012). Chemical interaction between the larva of a Entomol. Res. 107, 668-675. doi:10.1017/S0007485317000189
dipteran parasitoid and its coleopteran host: a case of exploitation of the Roitberg, B. D., Sircom, J., Roitberg, C. A., van Alphen, J. J. M. and Mangel, M.
communication system during the searching behaviour? Bull. Entomol. Res. 102, (1993). Life expectancy and reproduction. Nature 364, 108-108. doi:10.1038/
315-323. doi:10.1017/S0007485311000691 364108a0
Haberyan, K. A. (2022). Observations on the fall movements of Isabella moth larvae Steinberg, S., Dicke, M., Vet, L. E. M. and Wanningen, R. (1992). Response of the
braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals:
(Lepidoptera: Erebidae: Arctiinae) in Northwest Missouri. Am. Midl. Nat. 188,
effects of bioassay set-up, parasitoid age and experience and barometric flux.
244-249. doi:10.1674/0003-0031-188.2.244
Entomol. Exp. Appl. 63, 163-175. doi:10.1111/j.1570-7458.1992.tb01571.x
Keller, M. A. (1990). Responses of the parasitoid Cotesia rubecula to its host Pieris
Sujimoto, F. R., Costa, C. M., Zitelli, C. H. L. and Bento, J. M. S. (2020). Foraging
rapae in a flight tunnel. Entomol. Exp. Appl. 57, 243-249. doi:10.1111/j.1570-
activity of leaf-cutter ants is affected by barometric pressure. Ethology 126,
7458.1990.tb01436.x
290-296. doi:10.1111/eth.12967
Leskey, C. T. and Prokopy, J. R. (2003). Influence of barometric pressure on odor
Than, A. T., Ponton, F. and Morimoto, J. (2020). Integrative developmental
discrimination and oviposition by adult plum curculios (Coleoptera:
ecology: a review of density-dependent effects on life-history traits and host-
Curculionidae). EJE 100, 517-520. microbe interactions in non-social holometabolous insects. Evol. Ecol. 34,
Martı́nez, G. A., Castelo, M. K. and Crespo, J. E. (2017). Behavioural plasticity 659-680. doi:10.1007/s10682-020-10073-x
induced by intraspecific competition in host orientation in a parasitoid. Ecol. Tichy, H. and Kallina, W. (2010). Insect hygroreceptor responses to continuous
Entomol. 42, 484-491. doi:10.1111/een.12407 changes in humidity and air pressure. J. Neurophysiol. 103, 3274-3286. doi:10.
Martini, X., Rivera, M., Hoyte, A., Sé tamou, M. and Stelinski, L. (2018). Effects of 1152/jn.01043.2009
wind, temperature, and barometric pressure on Asian citrus psyllid (Hemiptera: Vosteen, I., Bianchi, F. J. J. A. and Poelman, E. H. (2020). Adverse weather
Liviidae) flight behavior. J. Econ. Entomol. 111, 2570-2577. doi:10.1093/jee/ conditions impede odor-guided foraging of parasitoids and reduce their host-
toy241 finding success. Agric. Ecosyst. Environ. 301, 107066. doi:10.1016/j.agee.2020.
Miao, J., Guo, P., Li, H., Wei, C., Liu, Q., Gong, Z., Duan, Y., Li, T., Jiang, Y., Feng, 107066
H. et al. (2021). Low barometric pressure enhances tethered-flight performance Wajnberg, E., Bernstein, C. and van Alphen, J. (2008). Behavioural Ecology of
and reproductive of the oriental armyworm, Mythimna separata (Lepidoptera: Insect Parasitoids: from Theoretical Approaches to Field Applications. John Wiley
Noctuidae). J. Econ. Entomol. 114, 620-626. doi:10.1093/jee/toaa291 & Sons.
Moiroux, J., Boivin, G. and Brodeur, J. (2015). Temperature influences host instar Weisser, W. W., Volkl, W. and Hassell, M. P. (1997). The importance of adverse
selection in an aphid parasitoid: support for the relative fitness rule. Biol. J. Linn. weather conditions for behaviour and population ecology of an aphid parasitoid.
Soc. 115, 792-801. doi:10.1111/bij.12545 J. Anim. Ecol. 66, 386-400. doi:10.2307/5984

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