Mating behavior in Atheloca subrufella Hulst, 1887 (Lepidoptera: Pyralidae: Phycitinae)
Comportamento
de acasalamento em Atheloca
subrufella Hulst, 1887 (Lepidoptera: Pyralidae:
Phycitinae)
Abel Felipe de Oliveira Queiroz1,
Jakeline Maria dos Santos2, Mariana
Oliveira Breda3, Antônio Euzébio Goulart Santana4
1Doutor em
Química e Biotecnologia, Universidade Federal de Alagoas, abelfelipi@gmail.com; 2Pós-doutoranda
PNPD na Rede Nordeste de Biotecnologia, Universidade Federal de Alagoas, jackbilu@hotmail.com; 3Professora
Doutora do Centro de Ciências Agrárias, Universidade Federal de Alagoas, breda.mariana@hotmail.com; 4Professor
Doutor do Centro de Ciências Agrárias, Universidade Federal de Alagoas, aegs@ceca.ufal.br.
Recebido: 09/03/2019; Aprovado:
16/05/2019
Abstract:
The
mating behavior of the moth Atheloca subrufella Hulst, 1887 (Lepidoptera:
Pyralidae) was investigated in laboratory arenas. The
descriptions of courtship and copulation in males and females were based on
direct observations of virgin couples. The courtship and copulation bioassays
results comprise several behavior patterns such as antennation,
female searching (walking and/or flying); female encounter; female calling
behavior; exhibition of pheromone gland; male approach and copulation. For
that, courtship and copulation behavior ethograms
were presented. The results also suggest that the mating behavior in A. subrufella
is mediated by a long-range pheromone and the presence of a short-range
pheromone. In overall, this research presents itself as a basis study to
further investigations upon A. subrufella sex pheromone and to improve the development
of new strategies of behavioral control techniques.
Key words: Cocos nucifera; Coconut moth; Courtship behavior.
Resumo: O
comportamento de acasalamento da mariposa Atheloca subrufella Hulst,
1887 (Lepidoptera: Pyralidae)
foi investigado em arenas de laboratório. As descrições de corte e cópula em
machos e fêmeas foram baseadas em observações diretas de casais virgens. Os
resultados dos bioensaios de corte e cópula
compreendem diversos padrões comportamentais tais como, antenação,
busca pela fêmea (caminhando e/ou voando), encontro da
fêmea, comportamento de chamamento da fêmea, exibição da glândula de feromônio,
tentativa de cópula e cópula. Para isso, foram apresentados etogramas
comportamentais de corte e cópula. Os resultados também sugerem que o
comportamento de acasalamento em A. subrufella é mediado por um feromônio de longa
distância e pela presença de um feromônio de curta distância. De maneira geral,
esta pesquisa apresenta-se como estudo base para futuras investigações sobre o
feromônio sexual de A. subrufella e desenvolvimento de novas estratégias de
controle comportamental.
Palavras-chave:
Cocos nucifera;
Traça
do coco; Comportamento de corte
INTRODUCTION
The study of mating
behavior in insects is the first step for the development of sexual behavioral
control strategies. Researches regarding calling behavior, presence or absence
of pheromone gland, courtship and copulation patterns are being developed and stand
as important tools to allow a better understanding and more accurate application
of Lepidoptera control techniques (BARRADAS-JUAN et al., 2016; NASCIMENTO et
al., 2016; SHI et al., 2018). According to Parra-Pedrazolli
and Leal (2006), female moths produce a mixture of pheromone compounds and the
complete bouquet is responsible for male attraction. Nevertheless, control by
sex pheromone may be achieved by the use of a single major constituent or by
the use of a partial mixture.
The coconut moth Atheloca subrufella (Hulst,
1887) [=Hyalospila ptychis (Dyar, 1919)] (Lepidoptera: Pyralidae)
is an important coconut pests, presenting wide distribution in Brazil (FERREIRA
et al. 2002), it was also reported in other countries such as the USA, Mexico,
Cuba, and the Virgin Islands (BONDAR, 1940; HEINRICH, 1956; KIMBAL, 1965; HABECK;
NICKERSON, 1982; HODGES et al., 1983; MOORE, 2001). According to
FAO (2017) Brazil is
the world's fifth largest producer of coconuts, reaching approximately a production of 2.4 million of tonnes in an area of 108,629.00 ha.
The A. subrufella
damage is performed by the caterpillars that develop inside of the coconut
inflorescences and fruits, they feed on the mesocarp
and blocking the flow of the sap. Infested fruits and inflorescences are
aborted and those that do not fall from the coconut palm tree become deformed
and commercially depreciated. The management of this pest by traditional
methods is restricted to the collection of infested coconut fruits and the use
of chemical insecticides (FONTES; FERREIRA, 2006). Nevertheless, these
techniques are often hampered by the caterpillars
endophytic habit consequently, studies of new and efficient control measures
are required.
Behavioral
control strategies is not used for A.
subrufella. However, some studies were developed to
describe biological aspects and calling behavior of this moth (BENTO et al., 2006;
NASCIMENTO et al., 2016). In order to contribute as basis to the development of
new behavioral management techniques, the objective of this study is to
describe the courtship and copulation behavior of A. subrufella.
MATERIAL AND METHODS
The A. subrufella rearing was kept in the Natural Resources
Research Laboratory of Federal University of Alagoas (LPQRN/UFAL) under
laboratory conditions at 25 ± 2 °C, 80% RH and photoperiod 14L: 10D. The
insects were collected in the field, from coconut fruits with signs of
infestation by A. subrufella
caterpillars. The collections were performed in the states of Sergipe and
Alagoas, Brazil. The coconut fruits were kept in plastic containers (10 L)
covered with voile fabric until the caterpillars reached the pupal stage. Pupae
were sexed and after adult emergence, couples were kept in plastic cages (1 L)
lined inside with paper towel as oviposition substrate. Eggs were daily
collected and kept in Petri dishes with moistened filter paper. The
caterpillars were daily fed with mesocarp coconut fruit cube of 2x2cm until
reached pupal stage.
Courtship
bioassays
The courtship male
behavior was direct observed through bioassays using a rectangular shaped glass
arena (20 x 10 x 15 cm) containing a female trapped in a cage (hair roller of 5
cm) exhibiting calling behavior. The cage containing the female was covered by
voile fabric to allow the compounds release and physical contact of male and
female, but preventing the mating. Ten replicates were performed. For each
replicate a different couple of adults was used. Four
points were demarcated in the arena and in each replicate the female was
allocated at a different point, aiming the elimination of any external
physical, chemical or visual influence. A.
subrufella adults with at least 24 hours age were
used in the bioassays, ensuring sexual maturity (BENTO et al., 2006). The
bioassays were performed from the first hour of scotophase,
according to the period of A. subrufella female calling behavior (NASCIMENTO et al.,
2016) under laboratory conditions of 25 ± 2 °C and 60% RH. The couples were
observed during 10 min.
Copulation behavior
The copulation
behavior was direct observed in plastic containers cages (250 mL) containing a
virgin couple, the adults used in the bioassays were 24h to 96h of aged. Three
replicates were performed. For each replicate a different couple of adults was used. The couple behavior was recorded during the female
first scotophase period, according to the female
calling behavior (NASCIMENTO et al., 2016). The description of the copulation
behavior was performed through a video analyses made under red light conditions.
The virgin couple was observed since the moment that the female exhibited the
calling behavior until the moment of the copula.
RESULTS AND DISCUSSION
Courtship bioassays
During the arena bioassays was
observed some behavioral patterns presented by A. subrufella adults. Both, males and
females showed continuous antennation during courtship. The females performed
the calling behavior throughout all the bioassay period. The male courtship
behavioral patterns were classified as: antennation, female searching (walking
and/or flying on the arena); female encounter; walking over the female cage
surface, resting over the female cage surface; antennation on the female cage;
mating attempt (flapping wings and arched abdomen); no mating attempt (Figure
1).
Figure 1. Courtship
bioassays ethogram of Atheloca subrufella
Hulst, 1887 (Lepidoptera: Pyralidae) (n=10).
Copulation behavior
The copulation behavior
patterns are described as follow: male and female presented antennation
behavior; the female exhibited the calling behavior, with wings slightly apart
exposing the pheromone gland at the final portion of the arched abdomen; the
female rotated the final portion of the abdomen spinning the pheromone gland
360°; the male rotated its body 360°; the female rotated its body 360° in both
directions (clockwise and anticlockwise); the male approached the female; male
and female showed antennation behavior facing each other and touching their
antennae; the male lifted its wings exhibiting the hairpencil
on the final portion of the abdomen; the male jumped over the female in a
backflip resting on the ground with its abdomen opposite to the female abdomen;
finally male and female initiated the copulation (Figure 2).
Figure 2. Mating behavior
ethogram of Atheloca subrufella Hulst,
1887 (Lepidoptera: Pyralidae). Male and female antennation (A), female calling
behavior (B, C), male and female body rotation (D, E), male and female touching
antennae (F), male lifted its wings exhibiting the hairpencil
(G), male jumped over the female in a backflip resting on the ground with its
abdomen opposite to the female abdomen (H, I), mating position (J).
Based on the
behavioral patterns showed by A. subrufella adults in the present study it is possible
to assume that courtship and copulation in this species may be mediated by the
presence of sex pheromone. A. subrufella females seems to
release a long-range pheromone to attract the males, which recognize the
females through contact, probably mediated by a short-range pheromone and/or
cuticular hydrocarbons. This pattern of short distance recognition was also
observed in other Pyralidae moth species, the Amyelois transitella Walker,
1863 (Lepidoptera: Pyralidae: Phycitinae),
which exhibited similar behavior patterns such as antennation indicating a
major characteristic of male and female sexual activity, the extrudation of a female abdominal (pheromone) gland and
male recognition of female through antennation
(PARRA-PEDRAZZOLI; LEAL 2006).
The Dioryctria abietella [Denis & Schiffermüller],
1775 (Lepidoptera: Pyralidae: Phycitinae) also
presented a very similar behavior to A. subrufella, such as the same pattern of female calling
behavior; the behavior of the male and female of touching the antennae after assuming
the frontal position; and the attempt of male copulation, where the male lifted
its wings exhibiting the hairpencil on the final
portion of the abdomen and jumped over the female in a backflip resting on the
ground with its abdomen opposite to the female abdomen (FATZINGER; ASHER,
1971).
The results of the
present study suggest that mating behavior in A. subrufella
may be mediated by a primary mixture of compounds which acts as long-range sex pheromone
and also by a secondary mixture of compounds which acts as a short-range
pheromone.
Same as that, the
primary sex pheromone of Choristoneura fumiferana Clemens, 1865 (Lepidoptera: Tortricidae) is composed of (E)- and (Z)-11-tetradecenal,
produced by the females and are efficient capturing virgin males on baited
traps in a ratio 95: 5 (SANDERS; WEATHERSTON 1976; SILK et al., 1980). After
cuticular compounds analyses, the presence of unsaturated alkanes in both sexes
was noted, but the compounds (Z,Z,Z)-3,6,9-tricosatriene and (Z,Z,Z)-3,6,9-pentacosatriene
were identified only in females. Arena and wind tunnel bioassays using C. fumiferana adults showed that males exhibit patterns
behavior as flapping wings and arched abdomen in the presence of female body
parts extracts and the female unsaturated alkanes. In addition, two female cuticular
compounds, (Z)-5-tricosene and (Z,Z,Z)-3,6,9-tricosatriene,
enhanced male responses to the primary sex pheromone components, acting in the
male orientation and short-range courtship. (SILK et al.,
2017).
Among the
subfamilies of Pyralidae, the Phycitinae
is one of the most abundant, comprising about 5,000 species distributed
throughout the world (LI; REN, 2009). However, only 35 female sex pheromones
were identified in this subfamily. The pheromonal mixtures identified to the Phycitinae species are characterized by the presence of
aldehydes, acetates, alcohols and hydrocarbons (ANDO; YAMAMOTO, 2018). The
number of identified pheromones compared to the number of species in Phycitinae reinforces the requirement and importance of
this study.
The use of sex
pheromones as a behavioral control strategy offer an environmentally friendly
practice, successfully applied in several techniques such as monitoring, mass
control and mating disruption. Nevertheless, for A. srubufella, there is no sex pheromone
identification until this moment and the control strategies are restricted to
collection of infested coconut fruits and the use of chemical insecticides.
In overall, this
research shows itself as a basis study to improve the development of new
strategies of control, allowing further investigations upon A. subrufella
sex pheromone, cuticular hydrocarbons and behavioral management techniques,
within the principles of the Integrated Pest Management (IPM).
CONCLUSIONS
Based at the
results of this research it is possible to conclude that in the mating behavior
of A. subrufella,
the female produces compounds to attract the male, and the male is responsible by
the search, recognition of the female and attempted copulation. This knowledge is
essential to apply techniques of population control using pheromone.
ACKNOWLEDGEMENTS
The authors would
like to thank the research funding agency CAPES for the scholarships (protocol
number: 1538957) granted to the post-graduate students participating in the
study.
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