Table Of ContentISSN 0373-5680 Rev. Soc. Entomol. Argent. 66 (3-4): 197-203, 2007 197
Locomotor activity of Cycloneda sanguinea
(Coleoptera: Coccinellidae) exposed to volatile
semiochemicals and to direct contact with the odour
source
HEIT, Guillermo E.*, Pedro SARDOY*, Graciela R. COHEN** and
Graciela MAREGGIANI*
*Cátedra Zoología Agrícola, Facultad de Agronomía, Universidad de Buenos Aires.
Avda. San Martín 4453. (1417) Buenos Aires, Argentina; e-mail: [email protected],
[email protected]
**Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias
Exactas y Naturales, Universidad de Buenos Aires. Pabellon 2, Ciudad Universitaria.
(C1428EHA) Buenos Aires, Argentina; e-mail: [email protected]
Actividad locomotriz de Cycloneda sanguinea (Coleoptera:
Coccinellidae) expuesta a semioquímicos volátiles y al
contacto directo con la fuente de olor
(cid:132)(cid:132)(cid:132)(cid:132)(cid:132) RESUMEN. Cycloneda sanguinea (Linnaeus) (Coleoptera:
Coccinellidae) es un predador polífago oportunista y cuando su menú
está dominado por áfidos, es esperable un comportamiento complejo de
forrajeo. Un movimiento activo, caracterizado por alta actividad
locomotriz, juega un rol importante en la búsqueda de esta presa. En
este trabajo se analizó el comportamiento de adultos de C. sanguinea
expuestos a los semioquímicos volátiles, emitidos por sustratos de
Capsicum annuum Linnaeus (Solanaceae) sanos o infestados con Myzus
persicae (Sulzer) (Hemiptera: Aphididae), o simplemente puestos en
contacto directo con esos sustratos. Los tratamientos evaluados fueron:
A) hojas de pimiento infestadas con alta densidad de áfidos, B) hojas de
pimiento infestadas con baja densidad de áfidos, C) hojas de pimiento
sanas y D) control. La actividad locomotriz no difirió significativamente
entre los distintos tratamientos cuando C. sanguinea se expuso solamente
a los volátiles. En cambio, cuando los coccinélidos se pusieron en contacto
directo con los sustratos evaluados, se encontraron diferencias
significativas entre los tratamientos. Estos resultados preliminares
indicarían que la sola presencia de un estímulo de olor, no sería suficiente
para modular un patrón locomotor diferente en C. sanguinea.
PALABRAS CLAVE. Comportamiento de forrajeo. Capsicum annuum.
Cycloneda sanguinea. Myzus persicae. Actómetro.
(cid:132)(cid:132)(cid:132)(cid:132)(cid:132) ABSTRACT. Cycloneda sanguinea (Linnaeus) (Coleoptera:
Coccinellidae) is an opportunistic polyphagous predator and when aphids
dominate its menu, a complex foraging behaviour can be expected. An
active movement characterized by a high locomotor activity plays an
important role in the search of this prey. The behaviour of C. sanguinea
adults exposed to volatile semiochemicals emitted by Capsicum annuum
Recibido: 29-V-2007; aceptado: 26-IX-2007
198 Rev. Soc. Entomol. Argent. 66 (3-4): 197-203, 2007
Linnaeus (Solanaceae) substrates, healthy or infested with Myzus persicae
(Sulzer) (Hemiptera: Aphididae), or in direct contact with these substrates
was here analyzed. The treatments evaluated were: A) high aphid-infested
pepper leaves, B) low aphid-infested pepper leaves, C) healthy pepper
leaves and D) control. Locomotor activity was not significantly different
among treatments when C. sanguinea was exposed only to the volatiles.
However, when adults were placed in direct contact with the evaluated
substrates, statistically significant differences were found among
treatments. These preliminary results could indicate that the sole presence
of an olfactory stimulus could not be sufficient to modulate a different
locomotor pattern in C. sanguinea.
KEY WORDS. Foraging behaviour. Capsicum annuum. Cycloneda
sanguinea. Myzus persicae. Actometer.
INTRODUCTION circumscribed search, passing over long
straight paths quickly and making just a few
Food sources are distributed along the stops (Ferren & Dixon, 1993; Carter et al.,
environment, both in time and space. To 1984; Bond, 1980). In this way, they
forage successfully, predators and parasitoids minimize the waste of time on unprofitable
must face a trade-off between the most proper areas, avoiding unnecessary energy
moments to look for their food and the expenditure (Gendron & Staddon, 1983). ACS
amount of resources present in a certain foraging behaviour would match to some
volume of space. extent the distribution of resources in a
Coccinellids are opportunistic continuous patchy environment.
polyphagous predators, but their essential Some authors consider that coccinellids
food requirements are very specific (Soares look randomly for their preys and can detect
et al., 2004). In Argentina, Cycloneda them only when direct contact is achieved
sanguinea (Linnaeus) (Coleoptera: (Ferran et al., 1994). This foraging behaviour
Coccinellidae) is considered an important has great advantage when the prey lives
aphids predator, but its impact in biological gregariously, such as aphids. Perhaps this is
control is very variable, particularly due to the reason why coccinellid ovipositions are
its polyphagy. When aphids dominate their mostly located in aphid-infested places or
menu, a complex foraging behaviour near them (Nakamuta, 1982), favoring
representative of a huge range of generalist successful prey foraging when ladybirds
predators, can be expected (Dicke, 1999; larvae hatch. On the other hand, newly
Ninkovic et al., 2001). emerged adult coccinellids must look for new
According to the Area Concentrated patches, because usually all the preys around
Search (ACS) behaviour model, if predators them have been consumed during juvenile
such as coccinellids detect their preys, which development (Obata, 1986).
are usually distributed in patches throughout Other authors (Dicke, 1999; Al Abassi et
the environment, after feeding, they will al., 2000; Ninkovic et al., 2001; Acar et al.,
explore the prey-patch intensely (Wiens, 2001) propose that a wide diversity of
1976). They will do this in order to delimit a generalist predators such as ladybirds use
concentrated area to search for more different semiochemicals or infochemicals
resources. This area will be slowly swept emitted by plants and insects to mediate in a
following sinuous ways and making series of key processes during foraging
numerous stops in order to raise the behaviour.
probability of finding more preys. On the An active movement of predators,
other hand, if predators do not find preys, characterized by a high locomotor activity,
they will undertake a more extensive or less plays an important role in the search for preys
HEIT, G. et al. Locomotor activity of Cycloneda sanguinea 199
(Bell, 1990). However, little research on the squares (1.5 cm side) of a squared grid crossed
effect of volatile semiochemicals in by the insect during its movement for 60
coccinellid locomotor activity has been done. seconds (Tourniaire et al., 1999). Data were
The aim of the present investigation was analyzed with three way ANOVA and Tukey
to evaluate the locomotor activity of the multiple comparison test (α=0.05). Square
predator C. sanguinea, exposed to volatile root transformations were used to fulfil the
semiochemicals emitted by Capsicum assumptions of the test (Sokal & Rohlf, 1995;
annuum Linnaeus (Solanaceae) plants, Zar, 1999). Data were analyzed using InfoStat
healthy or infested with Myzus persicae program.
(Hemiptera: Aphididae), or in direct contact
with these materials.
Two experimental series were done:
MATERIAL AND METHODS
First series: exposure to volatile
Rearing of predator and prey. Culture of semiochemicals. Locomotor activity of
plant-host Cycloneda sanguinea was evaluated with an
actometer (modified from Manrique et al.,
Adults of Cycloneda sanguinea, collected 2006). In each test, a male or a female of C.
in the campus of FAUBA (Facultad de sanguinea, chosen randomly from a
Agronomía, Universidad de Buenos Aires), randomized sample of 24 h starved
were reared in the laboratory. Ladybirds were individuals, was put in the experimental
fed on nymphs and adults of the aphid M. arena. The actometer (Fig. 1) consisted of an
persicae (Hemiptera: Aphididae). Every two acrylic cylindrical box 12 cm diameter,
days, C. sanguinea eggs were collected and composed by two horizontal compartments
put in a Petri dish until larval emergence. of the same height (2 cm), separated by a wire
Neonate larvae from each cohort were reared mesh to allow the diffusion of odour stimulus
separately in glass flasks closed with gauze. to avoid direct contact between the insect and
The adults obtained were used for the the volatiles source. The upper compartment,
bioassays. the arena, where the insects were placed, had
Myzus persicae colonies were multiplied a removable and transparent cover on the top,
in the laboratory on pepper plants, Capsicum with a squared grid drawn on its surface. The
annuum CV. California Wonder, cultivated in lower compartment, the diffusion volatile
350 cc polyethylene pots. C. annuum was chamber, was connected by means of a
selected as plant host due to its economic perforated plate in the centre of its floor, to a
importance as horticultural crop and to its stimulus delivery chamber, where the odour
high susceptibility to M. persicae sources were placed. After the introduction
colonization. Predators, prey and host were of the insect into the arena, 4 minutes
maintained in standardized conditions (24º acclimations were spent until the initiation
C ± 2º C, 65 ± 10% RH, photoperiod: 16:8 h of the experiment, to allow the uniform
light-darkness). diffusion of the volatile chemicals.
The volatile sources evaluated were: A)
Bioassays high aphid-infested pepper leaves (80 aphids/
replica) on filter paper, infested with Myzus
Standardized conditions were used for the persicae for one month before the
bioassays (24ºC±2ºC, 65±10% RH and light experiments, B) low aphid-infested pepper
60 watts). Every test was performed in the leaves (20 aphids/replica) on filter paper,
morning (9-12 h) and in the evening (13-16 infested with M. persicae for one week before
h). Cycloneda sanguinea individuals from the the experiments, C) healthy pepper leaves on
same cohort, which were food deprived for filter paper, and D) control: clean filter paper.
24 hours, were tested. The behavioural Nine independent replicates resulting
response, evaluated as the locomotor activity, from the combination of sex, moment of the
was estimated according to the number of day (morning and afternoon) and volatiles
200 Rev. Soc. Entomol. Argent. 66 (3-4): 197-203, 2007
Fig. 1. Actometer scheme. Lateral view shows the disposition and dimensions of the compartments.
Upper view shows the removable and transparent cover with a squared grid drawn on its surface, a
wire mesh as the arena’s floor, and below this, the connection of the diffusion volatile chamber with the
stimulus delivery chamber by means of a plate with holes, which allowed the diffusion of volatiles to
the arena.
source were made for each treatment. The substrates, its locomotor activity was not
experimental unit consisted of a male or a significantly different among treatments
female of Cycloneda sanguinea. (F =1.366, p=0.257). No differences
3,113,0.05
Second series: Direct contact of predator were found between the mean locomotor
with the odour source. The experimental activity in either female or male adults of this
arena consisted of a Petri dish, 9 cm diameter, predator measured during the morning and
with a squared grid drawn in the upper cover. afternoon (F =3.683, p=0.058) (Fig. 2).
1,113,0.05
In each test, a male or a female of Cycloneda However, when adults of the coccinellid
sanguinea, chosen randomly from a were placed in direct contact with the
randomized sample of 24 h starved evaluated substrates, statistically significant
individuals, was put in the experimental differences were found among treatments
arena, which allowed the contact with the (F =73,62, p<0,0001) and between both
3,112,0.05
substrate evaluated. moments of the day (F =9.54,
1,112,0.05
Treatments evaluated were the same as in p=0.0025) (Fig. 3).
the first series, but in this case the aphids were The mean locomotor activity of
removed from the infested leaves with a Cycloneda sanguinea measured in contact
brush, to avoid fortuitous stops of predators with pepper leaves, with either high or low
to eat, which could affect the locomotor density of infestation by Myzus persicae, was
activity. Eight independent replicates resulting significantly lower than that recorded in
from the same combinations as in the first contact with uninfested pepper leaves or
series of experiments were performed. In the clean filter paper. Furthermore, C. sanguinea
second series, the experimental unit consisted was significantly more active on filter paper
of a male or a female of Cycloneda sanguinea, than on healthy pepper leaves (p<0.05).
as well. In both experimental series, 3 gr of On the other hand, the mean locomotor
pepper leaves were used as the odour source activity non discriminating among treatments
for each bioassay. neither between sexes resulted statistically
lower (p=0.0025) in the morning
RESULTS (mean=3.87;S.E.=0.24) than in the afternoon
(mean=4.44; S.E.=0.19).
When Cycloneda sanguinea was exposed No significant differences between sexes
only to the volatiles of the evaluated were observed neither during the volatile-
HEIT, G. et al. Locomotor activity of Cycloneda sanguinea 201
Fig. 2. Locomotor activity of Cycloneda sanguinea adults (male and female), exposed to several substrate
volatiles, evaluated during morning or afternoon hours. Locomotor activity was estimated according to
the number of squares crossed by the insect during 60 seconds. Substrates: A) High-infested pepper
leaves, B) Low-infested pepper leaves, C) Healthy pepper leaves, D) Control. Mean locomotor activity
and standard error are shown.
Fig. 3. Locomotor activity of Cycloneda sanguinea adults (male and female), in contact with several
substrates, evaluated during morning or afternoon hours. Locomotor activity was estimated according
to the number of squares crossed by the insect during 60 seconds. Substrates: A) High-infested pepper
leaves (aphids removed), B) Low-infested pepper leaves (aphids removed), C) Healthy pepper leaves,
D) Control. Mean locomotor activity and standard error are shown.
only-exposure series of bioassays different visual and olfactory cues for
(F =0.0004, p=0.983) nor during those orientation (Nakamuta, 1980; Ferren &
1,113,0.05
of direct contact with the odour source Dixon, 1993; Lambin et al., 1996). Olfactory
(F =1.025, p=0.313). cues such as volatile semiochemicals emitted
1,112,0.05
by the aphids, the host or their interaction
DISCUSSION are chemical messages essential for survival
of these species.
Coccinellids are important natural Some authors (Dicke, 1999; Al Abassi et
enemies of aphids and have often been used al., 2000; Ninkovic et al., 2001; Acar et al.,
as a tool for biological control of several 2001; Heit et al., 2005) consider that
plagues (Obrycki & Kring, 1998). These coccinellids would be able to use olfactory
predators are constantly monitoring the and/ or visual cues to optimise their foraging
environment in search for food by means of behaviour. In this case, a specific stimulus
202 Rev. Soc. Entomol. Argent. 66 (3-4): 197-203, 2007
linked to the presence of the prey or pepper exposed to volatiles and measured during the
leaves could trigger a distinctive locomotor morning and afternoon is very close to the
activity pattern in the predator, although there limit of significance (α=0.05), which suggests
may not be any contact with the aphids or that additional replicates should be added in
the host plant. However, according to our order to obtain more conclusive results.
results (Fig. 3), once Cycloneda sanguinea Instead, this activity in males and females put
was in contact with a patch-prey on pepper on direct contact with the substrates was
leaves infested with Myzus persicae significantly higher during the afternoon than
(regardless of prey density), it followed a during the morning hours (p=0.0025). These
behaviour similar to the one described by the results agree with Elliott et al (2000), who
Area Concentrated Search model (ACS) and found that searching activity of Hippodamia
moved slowly scanning exhaustively the area convergens Guerin-Meneville, Hippodamia
around. These results agree with those of tredecimpunctata tibialis (Say), and
Ferran et al. (1994), who pointed out that Coleomegilla maculata (De Geer)
coccinellids could only detect their preys (Coleoptera: Coccinellidae) adults is
when they become in contact with them. On influenced positively as time of day and
the other hand, when C. sanguinea did not temperature increase in spring cereal fields.
detect a feeding resource, i.e. in contact with The above mentioned could point out to
uninfested pepper leaves or clean filter paper the presence of a rhythm in the foraging
(control), it moved significantly faster, activity of Cycloneda sanguinea (Mishra &
monitoring very superficially the area devoid Omkar, 2004). Foraging behaviour is one of
of food. the main adaptive functions which allow
These results could have also been predator insects to find their preys. To be
affected by the presence of honeydew, a successful, the search for food must be done
sugar-rich sticky substance released by aphids when and where the preys are more
as they feed, which could act as an additional available. In this sense, volatile
patch cue in a similar way as other sugars semiochemicals and/or tactile cues from
that are phagostimulants for phytophagous phytosuccivorous preys, the host plant or their
insects do (Mitchell & Gregory, 1979; interaction, must be necessary. The increase
Mitchell & Harrison 1984; Blaney et al., of the locomotor activity in the afternoon
1990; Nagnan-Le Meillour et al., 2000). It suggests an adaptive behavioural response of
has been reported that honeydew could this predator.
influence the behaviour of syrphids. The prey searching behaviour did not
Budenberg & Powell (1992) point out that differ between sexes in both experimental
females of Episyrphus balteatus (De Geer) series during morning and afternoon.
(Diptera: Syrphidae) landed more frequently Probably, foraging in this predator is the main
on ears contaminated with honeydew than diurnal activity in both sexes. Later, in the
on clean ears, suggesting a response to evening or night, foraging would stop and
honeydew volatiles. Additional experiments sexual activities would start, and then, male
could be useful to evaluate the effect of and female locomotor activity could differ.
honeydew on foraging activities of Cycloneda Mishra and Omkar (2004) observed that the
sanguinea adults. major foraging activity and field presence
Our results indicate that the sole presence levels of Propylea dissecta (Mulsant)
of an olfactory stimulus could not be sufficient (Coleoptera: Coccinellidae) occur in the
to modulate a different locomotor pattern in photophase while peaks of rhythm of mating,
Cycloneda sanguinea. Perhaps the lack of oviposition, hatching and moult occur in
response to volatiles could be due to a short scotophase, then supposing that the
acclimation time to the odour sources (4 min). concentration of life events other than
New assays with longer acclimation periods foraging in the same moments could be a
would be useful. survival strategy of evolutionary significance.
The p value 0.058 for the mean locomotor
activity of Cycloneda sanguinea (both sexes)
HEIT, G. et al. Locomotor activity of Cycloneda sanguinea 203
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