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Citation: Schifani, E.; Giannetti, D.;
Grasso, D.A. Predatory Abilities of
Two Mediterranean Ants on the Eggs
and Larvae of the Codling Moth
Cydia pomonella.Insects 2023,14, 97.
https://doi.org/10.3390/
insects14020097
Academic Editor: Kazuki Tsuji
Received: 25 December 2022
Revised: 13 January 2023
Accepted: 15 January 2023
Published: 17 January 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
insects
Communication
Predatory Abilities of Two Mediterranean Ants on the Eggs and
Larvae of the Codling Moth Cydia pomonella
Enrico Schifani * , Daniele Giannetti and Donato A. Grasso
Department of Chemistry, Life Sciences & Environmental Sustainability, University of Parma,
Parco Area delle Scienze, 11/a, 43124 Parma, Italy
*Correspondence: enrico.schifani@unipr.it
Simple Summary:
Ants are widespread across terrestrial ecosystems, including agroecosystems,
where they take part in several important processes. They often can act as predators of a wide
range of insect pests in agricultural fields, which should be considered by management programs,
and can sometimes be actively exploited to promote sustainable biological control strategies. In a
recent experiment conducted in Europe, pear trees visited by larger numbers of ants suffered fewer
attacks to their fruits by the codling moth, a small lepidopteran, which is a significant economic pest
worldwide, especially in apple, pear, and walnut orchards. However, the exact form of the interaction
between the ants and codling moths remained unclear. While ants were already known to prey upon
mature larvae or pupae in the soil, this new evidence suggested they could also control the eggs or
newly hatched larvae that had not yet attacked the fruits, which are the two stages whose removal
would directly prevent fruit damage. We conducted laboratory experiments to determine whether
two common European ants could prey upon these stages. Our results suggest that these ants are
effectively able to kill newly hatched larvae, while the eggs do not appear directly vulnerable to
predation. Further investigation under field conditions would be needed to assess whether ants may
also interfere with the oviposition by adult moths.
Abstract:
The predatory ability of ants (Hymenoptera, Formicidae) against insect pests can offer an
important service to agricultural activities and may sometimes be directly exploited in biological
control strategies. The codling moth Cydia pomonella (Lepidoptera, Tortricidae) is a major agricultural
pest of fruit orchards, whose biological control is complicated by the fact that the larvae spend most
of their life protected within the fruits they damage. In a recent experiment in Europe, pear trees in
which ant activity was artificially increased by the addition of sugary liquid dispensers (artificial
nectaries) suffered less damage caused by the larvae to their fruits. While some ants were already
known to prey upon the mature larvae or pupae of C. pomonella in the soil, prevention of fruit damage
would require predation upon eggs or newly hatched larvae, which have not yet excavated into the
fruits. We verified whether two different Mediterranean ants frequently observed in fruit orchards,
Crematogaster scutellaris and Tapinoma magnum, were able to prey upon C. pomonella eggs and larvae in
laboratory conditions. Our experiments demonstrated that both species similarly attacked and killed
young C. pomonella larvae. On the other hand, the eggs mostly attracted the attention of T. magnum
but were never damaged. Further field assessments are required to understand whether ants may
also interfere with oviposition by adults or whether larger ant species, although generally rarer in
orchards, may also prey upon eggs.
Keywords:
biological control; pest management; Formicidae; Tortricidae; Lepidoptera; Crematogaster
scutellaris;Tapinoma magnum
1. Introduction
Ants (Hymenoptera, Formicidae) are among the most successful insect groups, and
their widespread presence in terrestrial habitats has significant ecological
consequences [1,2]
.
Insects 2023,14, 97. https://doi.org/10.3390/insects14020097 https://www.mdpi.com/journal/insects
Insects 2023,14, 97 2 of 7
Their relationship with plants is of particular interest from both an evolutionary and an
applied perspective [
2
,
3
]. One of the most important services that ants may provide to
plants in these relationships is protection from a range of different herbivore insects that
ants may prey upon or at least displace [
4
,
5
]. In addition, ants in agriculture may also
play important roles in soil enrichment and bioturbation, as well as control of weeds
and certain plant pathogens [
6
–
8
]. Ants’ ability to protect certain honeydew insect pests
must be acknowledged; at the same time, their generalist predatory ability against several
phytophagous arthropods promotes their recognition as biological control agents across
different agricultural contexts [
4
,
5
,
9
]. This is especially well known in the tropics and
comparatively less studied in temperate regions [4].
The codling moth, Cydia pomonella (Linnaeus, 1758) (Lepidoptera, Tortricidae), is a key
polyphagous fruit pest whose economic relevance is particularly significant in apple, pear,
and walnut orchards [
10
–
12
]. Its control is complicated by the development of resistance
against pesticides and baculoviruses [
12
–
14
], while pesticide usage may disrupt the control
of secondary pests [
15
]. Biological control strategies normally focus on last instar larvae
that seek a shelter to pupate, on pupae, or on adults, using predators, parasitoids, and
viruses [
16
–
21
]. In addition, pheromones or the sterile insect technique can be used in
mating disruption strategies [
22
–
24
]. However, few biological control agents are known
to target eggs or younger larvae, which spend almost their entire life protected inside the
fruit they consume except for a short window after hatching (usually within 24 h), during
which they may travel for up to a few meters searching for some fruit to dig into [
10
,
25
].
Predatory heteropterans and earwigs are the only known predators of eggs [
26
–
28
], which
are very small (1–1.2 mm long), may be laid directly on the surface of fruits or on nearby
areas of the plants, and hatch in about 5–12 days [10,25].
Among the different generalist predators that may play a role in the control of C.
pomonella [
29
], ground-dwelling ants can prey upon last instar larvae and pupae [
18
]. More
recently, field data suggested that trees visited more intensively by ants may suffer less
damage to their fruits by the moths [30].
While this result suggested an effect of ants on the activity of C. pomonella before its lar-
vae dig into the fruits, it remained unclear whether ants affected the eggs and/or the newly
hatched larvae [
30
]. We aimed to test whether two Mediterranean ants that are common in
fruit orchards and agroecosystems, Crematogaster scutellaris (Olivier, 1792) and Tapinoma
magnum Mayr, 1861 [
31
,
32
], may act as predators of C. pomonella eggs and/or newly hatched
larvae by documenting their behavioral interactions in laboratory experiments.
2. Materials and Methods
All experiments were conducted during June 2022. Four days before the experiments,
fragments of C. scutellaris and T. magnum of at least 500 workers each [
33
] were taken
from Parma University Campus (northern Italy) and temporarily reared under laboratory
conditions (T: 25
±
1
◦
C, RH: 60
±
0.5%, photoperiod 12:12 L:D; honey provided as
food). Commercially available C. pomonella eggs were obtained from Andermatt Biocontrol
(Grossdietwil, Switzerland) and kept under the same laboratory conditions. Cydia pomonella
eggs and first-instar larvae (hatched in the previous 2–8 h) were used in the experiments
alongside ant workers randomly selected from the colony fragments.
In each trial, we introduced into a petri dish (
∅
= 9 cm) either an ant and a group
of 6 C. pomonella eggs laid on a 1 cm
×
1.5 cm paper or an ant and a single C. pomonella
larva. The C. pomonella eggs or larva were initially put at the center of the petri dish and
the ant was introduced one minute later. When the ant was introduced, the petri dish
was filmed for 10 min using a camera to record the behavioral interactions. Insects used
for an experimental trial were not reused in any following trial. A total of 12 trials were
conducted for each ant species to study its interaction with C. pomonella eggs (n = 24), while
15 trials were conducted to study the interaction of each ant species with C. pomonella larvae
(n = 30).
Insects 2023,14, 97 3 of 7
The videos were subsequently analyzed using the software, Solomon Coder 19.08.02,
to evaluate behavioral interactions. We recorded the following behaviors performed by the
ants towards the larvae:
(i)
Antennation: the ant touches the eggs/larva with its antennae while slowing or
stopping nearby.
(ii)
Mandible opening: the ant opens its mandibles in front of the eggs/larva without
biting.
(iii)
Biting: the ant bites the eggs/larva with its mandibles.
(iv) Chemical attack: the ant uses its chemical repellent to the eggs/larvae (this behavior is
performed by applying the venom topically, using the spatulate stinger in C. scutellaris
and by short distance spraying in T. magnum).
(v)
Transportation/feeding: the ant starts to feed on the eggs/larva or transport them
with its mandibles—this is considered as predation and/or as a proxy of food retrieval
to the nest.
(vi)
Walking over: the ant walks over eggs/larva.
The frequency of each behavior was recorded in each experimental trial. Biting and
transportation/feeding were always displayed together in our observations and were
therefore treated as a single behavior for the purpose of statistical analyses. Furthermore,
at the end of each trial, we inspected under a stereoscopic microscope whether the eggs
appeared damaged and whether the larvae were dead or injured.
We used a generalized linear model (GLM) followed by Tukey’s post hoc tests to ana-
lyze the frequency of the behavioral interactions between the ants and the eggs, according
to the identity of the ant species and of the behavior, considering their possible interactions.
Differences between the two ant species concerning single behaviors performed were ana-
lyzed using Mann–Whitney U tests. We used a GLM with binomial distribution followed
by Tukey’s post hoc tests to analyze the frequency of the behavioral interactions between
the ants and the larvae, according to the identity of the ant species and of the behavior,
considering their possible interactions. Differences between the two ant species for single
behaviors performed were then analyzed using the chi-square test. The data were analyzed
using the software R 4.2.2 and RStudio [34,35].
3. Results
In the interactions between the ants and the eggs, only three behaviors were observed:
antennation, mandible opening, and walking over (see Supplementary File S1). We found
no significant difference in the frequency of the different behaviors (0.864
≤
p
≤
0.997),
while T. magnum interacted more frequently with the eggs as compared with C. scutellaris
(p= 0.009). All three behaviors were more frequently expressed by T. magnum as compared
to C. scutellaris (Antennation: W = 37, p= 0.038; Mandible opening: W = 39.5, p= 0.021;
Walking over: W = 29.5, p= 0.009; Figure 1, Supplementary File S2). No eggs were harmed
by the ants during the trials.
In the interactions between the ants and the larvae, four behaviors were observed:
antennation, biting and transportation/feeding, and mandible opening (see Supplementary
File S1). Each behavior was observed only once per experiment. Mandible opening was
performed significantly less frequently than antennation (p= 0.023), while no significant
differences were detected between the frequency of the interaction by the two ant species
(p= 0.705) nor between the frequency of individual behaviors (Antennation:
χ2
= 0.14,
p= 0.705; Biting and Transportation/feeding:
χ2
= 0.13, p= 0.712; Mandible opening:
χ2= 2.16
,p= 0.142; Figure 2, Supplementary File S2). Biting and transportation/feeding
always implied that the larvae were dead by the end of the experiment; so, 43% of the
larvae were killed during the 10-min trials.
Insects 2023,14, 97 4 of 7
Insects 2023, 14, x FOR PEER REVIEW 4 of 7
Figure 1. The interactions observed between the ants (Crematogaster scutellaris and Tapinoma mag-
num) and the Cydia pomonella eggs. Asterisks represent the significance level of the differences be-
tween the two species (*, p ≤ 0.05; **, 0.001 < p ≤ 0.01).
In the interactions between the ants and the larvae, four behaviors were observed:
antennation, biting and transportation/feeding, and mandible opening (see Supplemen-
tary File S1). Each behavior was observed only once per experiment. Mandible opening
was performed significantly less frequently than antennation (p = 0.023), while no signifi-
cant differences were detected between the frequency of the interaction by the two ant
species (p = 0.705) nor between the frequency of individual behaviors (Antennation: χ
2
=
0.14, p = 0.705; Biting and Transportation/feeding: χ
2
= 0.13, p = 0.712; Mandible opening:
χ
2
= 2.16, p = 0.142; Figure 2, Supplementary File S2). Biting and transportation/feeding
always implied that the larvae were dead by the end of the experiment; so, 43% of the
larvae were killed during the 10-min trials.
Figure 2. The interactions observed between the ants (Crematogaster scutellaris and Tapinoma mag-
num) and the Cydia pomonella larvae. No statistically significant differences (n.s.) between the two
ant species were detected.
4. Discussion
Our data revealed that common Mediterranean ants may act as predators of newly
hatched C. pomonella larvae. Newly hatched larvae are particularly vulnerable to preda-
tors, as well as temperature variation and rainfall, until they can locate and excavate into
Figure 1.
The interactions observed between the ants (Crematogaster scutellaris and Tapinoma magnum)
and the Cydia pomonella eggs. Asterisks represent the significance level of the differences between the
two species (*, p≤0.05; **, 0.001 < p≤0.01).
Insects 2023, 14, x FOR PEER REVIEW 4 of 7
Figure 1. The interactions observed between the ants (Crematogaster scutellaris and Tapinoma mag-
num) and the Cydia pomonella eggs. Asterisks represent the significance level of the differences be-
tween the two species (*, p ≤ 0.05; **, 0.001 < p ≤ 0.01).
In the interactions between the ants and the larvae, four behaviors were observed:
antennation, biting and transportation/feeding, and mandible opening (see Supplemen-
tary File S1). Each behavior was observed only once per experiment. Mandible opening
was performed significantly less frequently than antennation (p = 0.023), while no signifi-
cant differences were detected between the frequency of the interaction by the two ant
species (p = 0.705) nor between the frequency of individual behaviors (Antennation: χ
2
=
0.14, p = 0.705; Biting and Transportation/feeding: χ
2
= 0.13, p = 0.712; Mandible opening:
χ
2
= 2.16, p = 0.142; Figure 2, Supplementary File S2). Biting and transportation/feeding
always implied that the larvae were dead by the end of the experiment; so, 43% of the
larvae were killed during the 10-min trials.
Figure 2. The interactions observed between the ants (Crematogaster scutellaris and Tapinoma mag-
num) and the Cydia pomonella larvae. No statistically significant differences (n.s.) between the two
ant species were detected.
4. Discussion
Our data revealed that common Mediterranean ants may act as predators of newly
hatched C. pomonella larvae. Newly hatched larvae are particularly vulnerable to preda-
tors, as well as temperature variation and rainfall, until they can locate and excavate into
Figure 2.
The interactions observed between the ants (Crematogaster scutellaris and Tapinoma magnum)
and the Cydia pomonella larvae. No statistically significant differences (n.s.) between the two ant
species were detected.
4. Discussion
Our data revealed that common Mediterranean ants may act as predators of newly
hatched C. pomonella larvae. Newly hatched larvae are particularly vulnerable to predators,
as well as temperature variation and rainfall, until they can locate and excavate into fruit,
which may take from 10 min to a few hours to accomplish [
25
,
36
]. In our experiments,
both C. scutellaris and T. magnum behaved similarly towards the larvae, killing them
in approximately half of the short trials by repeatedly biting their soft parts and then
immediately feeding on them or transporting them with their mandibles. Detection through
antennation was typically followed by attacks, while in most trials in which no attacks were
recorded, the larvae remained undetected. We can speculate that very small newly hatched
larvae may be a more attractive and more easily encountered item for smaller ants. While
both species did not attack the eggs, these attracted the attention of T. magnum significantly,
as the workers were repeatedly observed performing stereotyped mandible threats and
often kept antennating or walking over them several times. Eggs may offer little foothold
to the ants’ mandibles and can adhere strongly to the substratum of leaves and fruits, thus
becoming physically invulnerable at least to the species we tested [
37
,
38
]. Larger ants with
stronger and larger mandibles may be more capable of damaging or feeding on the eggs,
Insects 2023,14, 97 5 of 7
but they are often less frequent in agroecosystems [
32
]. While we cannot entirely discard
other possible mechanisms of protection (e.g., chemical repellency or insignificancy), the
eggs appeared to be attractive for ants during our experiments (especially in the case of
T. magnum), which may at least increase the chances that ant workers can take advantage
of the moment they hatch to prey upon the larvae. In our experiment, whenever the ants
attempted to attack a larva, the larva was always successfully killed. However, even if
young larvae manage to escape ants, any delay in their effort to find and excavate fruit
is expected to result in significantly higher mortality rates [
36
]. Based on the evidence of
other ant–plant–phytophagous interactions, it is also possible that the excavation behavior
by the young larvae releases semiochemicals that are attractive to ants [39].
Both ant species we used in our experiments are known to be able to act as predators
of many other agricultural pest insects [
31
,
40
–
42
]. Potentially problematic relationships
with aphids or coccids are also possible in some cases [
43
,
44
]. Manipulation of nesting site
availability and trophic resource may be crucial to maximizing the benefits of these ants in
biological control strategies [
30
,
32
]. Further efforts should focus on interactions between
C. pomonella and ants in the field [
18
,
30
]. For instance, potential interference between ants
and ovideposing adults has so far not been investigated but may contribute to explaining
the reduction in damaged fruits in ant-visited plants [
30
]. In fact, in several ant species,
more or less specialized workers may function as a constant “presidium”, exploring and
patrolling even large areas in search for suitable resources [1,45,46].
If predation of C. pomonella larvae in the field is confirmed to be significant, it is
possible that adult moths prefer to avoid laying their eggs in ant-visited fruits even without
coming into direct contact with the ants, as observed in similar interactions with fruit flies
or scolytid beetles, which are mediated by semiochemicals [
42
,
47
]. In fact, it is well known
that, apart from chemical trails, both arboreal and ground-dwelling ants may lay additional
markers on patrolled and defended areas [48–50].
In conclusion, the predatory role of ants in temperate agroecosystems is for the most
part still little understood [
30
,
31
,
51
,
52
], but due to their ubiquitous presence and generalist
feeding habits, ants are likely to play a significant yet overlooked role in the control of the
populations of several pest insects.
Supplementary Materials:
The following supporting information can be downloaded at: https://
www.mdpi.com/article/10.3390/insects14020097/s1, Supplementary File S1: Video documentation
of behavioral interactions; Supplementary File S2: Behavioral data and GLM output.
Author Contributions:
Conceptualization, E.S., D.G. and D.A.G.; methodology, E.S. and D.G.; soft-
ware, E.S.; validation, E.S., D.G. and D.A.G.; formal analysis, E.S.; investigation, E.S.; resources, E.S.,
D.G. and D.A.G.; data curation, E.S.; writing—original draft preparation, E.S.; writing—review and
editing, D.G. and D.A.G.; visualization, E.S.; supervision, D.A.G.; project administration, D.A.G.; fund-
ing acquisition, D.A.G. All authors have read and agreed to the published version of the manuscript.
Funding:
The work benefited from the equipment and framework of the COMP-HUB Initiative,
funded by the “Departments of Excellence” program of the Italian Ministry for University and
Research (2018–2022).
Data Availability Statement:
The data presented in this study are available in the Supplementary
Materials.
Acknowledgments: We thank two anonymous referees for their suggestions.
Conflicts of Interest: The authors declare no conflict of interest.
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