Is the mating process of Mahanarva spectabilis (Hemiptera: Cercopidae) mediated by chemical signals?

O processo de acasalamento de Mahanarva spectabilis (Hemiptera: Cercopidae) é mediado por sinais químicos?

Abstract

Mahanarva spectabilis (Distant) is an important pasture pest in Brazil and represents an obstacle to forage production. Elucidating the chemical signals involved in the communication of this species is essential for finding new control alternatives. Therefore, the aim of this study was to determine whether chemical signals are involved in the mating process of M. spectabilis. In the first trial, the insect's behavior was evaluated in cages with male: female ratios of 4:1 and 1:4. As soon as copulation began, the behavior of males or females around the copulating couple was recorded. In subsequent trials, the olfactory responses of males and females of M. spectabilis were evaluated in a Y-shaped olfactometer for volatiles released by males, females and mating pairs. At a male: female ratio of 4:1, there were significantly more touches by the other males of the copulating couple. The number of individuals attached to the copulating couple and the copulation time did not differ significantly in relation to the male: female ratio used. The attractiveness of males to copulating pairs was also observed in the olfactometry test, in which males were significantly attracted only to copulating pairs and to the extract of copulating pairs. The females showed no olfactory attraction to any of the odor sources offered. This shows that chemical signals are involved in the mating process of M. spectabilis.

Keywords:
male-female interaction; olfactory preference; chemical signals

Resumo

Mahanarva spectabilis (Distant) é uma importante praga de pastagens no Brasil e representa um obstáculo à produção de forragem. Elucidar os sinais químicos envolvidos na comunicação dessa espécie é essencial para encontrar novas alternativas de controle. Portanto, o objetivo deste estudo foi determinar se os sinais químicos estão envolvidos no processo de acasalamento de M. spectabilis. No primeiro ensaio, o comportamento do inseto foi avaliado em gaiolas com proporções de macho: fêmea de 4:1 e 1:4. Assim que a cópula começou, o comportamento dos machos ou das fêmeas ao redor do casal em cópula foi registrado. Em testes subsequentes, as respostas olfativas de machos e fêmeas de M. spectabilis foram avaliadas em um olfatômetro em forma de Y para voláteis liberados por machos, fêmeas e casal em cópula. Na proporção macho/fêmea de 4:1, houve significativamente mais toques dos outros machos no casal em cópula. O número de indivíduos próximos ao casal em cópula e o tempo de cópula não diferiram significativamente em relação à proporção macho: fêmea utilizada. A atração dos machos pelos casais em cópula também foi observada no teste de olfatometria, no qual os machos foram significativamente atraídos apenas pelos casais em cópula e pelo extrato desses. As fêmeas não demonstraram atração olfativa por nenhuma das fontes de odor oferecidas. Isso mostra que os sinais químicos estão envolvidos durante o processo de acasalamento de M. spectabilis.

Palavras-chave:
interação macho-fêmea; preferência olfativa; sinais químicos

1. Introduction

In Brazil, a third of the country's territory is used for farming, of which more than 58% is pastureland for cattle rearing in an extensive system (Cavalheiro, 2023) using various species of forage. Mahanarva spectabilis (Distant) (Hemiptera: Cercopidea) hinders the production of these forages (Auad et al., 2007) by promoting phytotoxicity, which consequently reduces biomass production and palatability for cattle (Valério and Nakano, 1988), ultimately impacting beef and milk production (Dias-Filho, 2014).

The control of with Chemical control of spittlebugs is unsustainable and costly due to the need for large-scale application (Valério, 2009; Silva et al., 2019). To mitigate spittlebug damage, studies examine plants resistance mechanism (Auad et al., 2007; Valverde, 2009; Congio et al., 2012; Resende et al., 2013; Alvarenga et al., 2019; Congio et al., 2020), diversifying pasture with spittlebug-resistant forages (Alvarenga et al. 2019), the use of bioinsecticides (Dias et al., 2019; Nascimento et al., 2021), entomopathogenic fungi (Campagnani et al., 2017, Pereira et al., 2018; Pitta et al., 2019; Ribeiro and Cazarotto, 2019; Campagnani et al., 2024; Oliveira Netto et al., 2024) and the use of chemical signals (Fonseca et al., 2013; Silva et al., 2019).

Recognizing chemical stimuli is a complex process in insects (Liu et al., 2023), involving precise olfactory systems that capture chemical and volatile signals from plants and conspecifics, enabling adaptation to diverse environments and ecological niches (Gadenne et al., 2016; Haverkamp et al., 2018). Insects use multiple visual, chemical, and vibroacoustic signals to mediate behavior, including mating (Shorey, 1973; Faal et al., 2022). Chemical signals used for communication within a species are called pheromones (Faal et al., 2022). Understanding the dynamics of these chemical signals makes it possible to implement strategies to mitigate pest outbreaks (Fonseca et al., 2013). Sexual chemical signals can be used to control and monitor pests in crops (Zarbin et al., 2009; El-Wahab et al., 2021), allowing a reduction in the use of insecticides and minimizing environmental impact (Ghini and Bettiol, 2000). However, this method remains underutilized and costly. Female-produced olfactory signals mediating mating have been described in hemipteran species (Pickett et al., 1992; Boullis, 2016), Male-emitted olfactory signals also function as sexual pheromones, as seen in Pentatomidae, where these compounds are produced exclusively by males and primarily serve to attract females or aggregate both sexes (Tholl, 2021).

The mating behavior of M. spectabilis described by Fonseca et al. (2013) elucidated the behaviors involved in intraspecific communication between males and females. However, the chemical signals mediating conspecific attraction during mating in this species remain unknown. Therefore, the aim of this study was to determine whether chemical signals are involved in the mating process of M. spectabilis.

2. Methods

2.1. Plants and insects

Brachiaria ruziziensis seedlings were planted in PVC tubes (5 cm in diameter and 8 cm long) and kept in a greenhouse at Embrapa Gado de Leite, Juiz de Fora, MG, Brazil. Plants that were 60 days old and approximately 20 cm tall were used in the experiments.

To obtain adults of M. spectabilis, nymphs of this species were collected in the experimental field of Embrapa Gado de Leite, located in Coronel Pacheco-MG, Brazil, and taken to the Entomology Laboratory of Embrapa Gado de Leite. The nymphs were then individualized using a fine-tipped brush in PVC rearing units (5 cm in diameter and 8 cm long) containing a B. ruziziensis plant with the roots exposed for feeding. Each rearing unit was capped with a lid, and foam was wrapped around the plant stem to prevent nymph escape. These were maintained in phytotron-type growth chambers at 24 ± 1 °C, with a 14-hour photoperiod and 70 ± 10% RH. Adult emergence, monitored daily, provided the insects used in the experiments.

2.2. Bioassay 01- Behavioral response of Mahanarva spectabilis adults in cages

This experiment tested the hypothesis that copulating pairs attract surrounding males, as suggested by empirical observations in the laboratory, greenhouse, field and rearing cages. Two male: female ratios were used: 4:1 and 1:4.

Transparent cages (25 cm high x 10 cm diameter) were used to facilitate behavioral observations. Each cage was covered with organza fabric at the top and connected at the bottom to a PVC tube containing a B. ruziziensis plant for insect feeding. Fifteen cages per treatment (male: female ratio) were maintained in a phytotron at 24 ± 1 °C, 70 ± 10% RH, and a 14:10 L:D photoperiod.

When mating onset was detected (at times predetermined by Fonseca et al. (2013), the number of touches by males and females on copulating pairs, and the time of first copulation were recorded. Observations were made every 5 min throughout the species' copulation period (averaging 5 h).

A completely randomized design with two male:female rations (treatments) and 15 replicates was used. Data were analyzed using analysis of variance (ANOVA), and means were compared using Tukey’s test (p < 0.05) in Sisvar 5.8 (Universidade Federal de Lavras, Minas Gerais, Brazil).

2.3. Bioassay 02- Olfactometry analysis of the behavioral response of Mahanarva spectabilis adults

Olfactometry bioassays were conducted at the Entomology Laboratory, Embrapa Gado de Leite, using an olfactometer with a continuous air flow of 1.0 L/min, previously humidified and filtered through activated charcoal. The Y-shaped glass olfactometer had a 3.5 cm diameter, with a 30 cm main arm and two 23 cm side arms angled at 120°. Prior to testing, plume distribution within the olfactometer was visualized by simulating odor dispersal using hydrochloric acid and ammonium hydroxide, following the method of Baker and Linn (1984).

The arms of the olfactometer were connected by silicone tubes to two glass chambers (42 cm high × 16 cm in diameter) where the odors (live insects) tested were placed. A male or female was introduced into the base of the olfactometer's main tube, and its behavior was observed for 10 minutes. A response was recorded when a spittlebug walked against the air flow and reached the end of one of the arms containing the odor source, and a nonresponse was recorded when the insect did not walk against the air flow and/or did not reach the end of any of the arms containing the odor sources during the 10 min observed. After observing 5 insects, the olfactometer was cleaned with alcohol and the position of the olfactometer arms was inverted to avoid any external interference.

The females and males were separated approximately 30 minutes before the bioassays began. Six combinations were tested: (i) response of males to 10 females versus air; (ii) response of males to 10 males versus air; (iii) response of males to 10 copulating pair versus air; (iv) response of females to 10 females versus air; (v) response of females to 10 males versus air; and (vi) response of females to 10 copulating pairs versus air.

All the olfactometry tests were performed between 2 pm and 4 pm, when the insects were most active (Fonseca et al., 2013). Each insect was tested only once. The total number of insects of each sex of M. spectabilis tested varied for each combination mentioned above, with at least 30 positive responses.

Choice response data were analyzed using the chi-squared test in the BioEstat χ2 program (Ayres et al., 2003). Insects that did not respond to the stimuli were excluded from the analysis.

2.4. Collection of volatiles.

Volatiles were collected from virgin females and mating pairs using the aeration technique (Zarbin, 2001). For the collection of extracts, 10 virgin females and 10 copulating pairs were selected. The females and pairs were placed separately in a glass chamber (42 cm high x 16 cm in diameter). A continuous air flow of 1.0 L/m, humidified and filtered with activated charcoal and calibrated using a flow meter, passed through the chamber carrying the volatiles released by the insects. The volatiles were retained in a glass column (11 cm long x 1 cm in diameter) containing 0.8 grams of adsorbent polymer (Haye Sep® D 80/100 Supelco, Belfonte, PA) as described by Zarbin (2001). After 24 hours of aeration, the compounds were desorbed using distilled hexane (J.T. Backer® 95% hexane, Sovereign, Taboão da Serra, SP, Brazil) in borosilicate glass vials. The samples were preconcentrated under a stream of nitrogen (99.99% pure) to approximately 100 µL (one female or couple for 10 µL) and placed in a freezer (-25°) for later use in bioassay 03.

2.5. Bioassay 03 - Olfactory responses of Mahanarva spectabilis adults to extracts of virgin females and copulating pairs.

To test the olfactory response of M. spectabilis to volatile extracts obtained from virgin females and copulating pairs, a “Y” olfactometer was used, as described previously. The following combinations of treatments were used: (i) response of females to female extract vs. n-hexane; (ii) response of females to extract from copulating couples vs. n-hexane; (iii) response of males to female extract vs. n-hexane; and (iv) response of males to extract from copulating pairs vs. n-hexane. Hexane was used as a control.

To assess the effect of the volatile extracts, a filter paper strip (3 cm × 2 cm) was impregnated with 10 µL (equivalent to one insect) of the extracts from virgin females,mating pairs, or n-hexane and placed at the distal end of each olfactometer arm. At least 30 positive responses were obtained for each sex of M. spectabilis in each test combination. The odor source was replaced after each insect. All olfactometry tests were conducted between 2 pm and 4 pm, when insects are most active (Fonseca et al., 2013).

Response data were analyzed using a chi-squared test in BioEstat χ2 (Ayres et al., 2003). No- responding insects were excluded from subsequent analyses.

3. Results

3.1. Behavioral response of Mahanarva spectabilis adults in cages

In cages with 4:1 male: female ratio, there were significantly more touches (F = 4.97, P = 0.036) by other males on copulating pairs (Fig. 1A), supporting the hypothesis that copulating pairs attract other males. However, the number of individuals near the copulating pairs (F = 0.19, P = 0.67) and the time to first copulation (F = 1.05, P = 0.32) did not differ significantly between male: female ratios (Fig. 1 A and B).

Figure 1
Behavioral interactions of Mahanarva spectabilis in cages containing four males and one female (4:1) or one male and four females (1:4) in terms of touch and number of insects seen near the couple during copulation (A) and mating time (B). Means followed by the same lowercase letter compared between sexual ratios and number of touch or number of insects near the couple or mating time do not differ from each other by Tukey Test (P<0.05).

3.2. Olfactometry analysis of the behavioral response of Mahanarva spectabilis adults

The responses of males and females of M. spectabilis in the Y olfactometer when stimulated with different odor sources are shown in Figures 2 and 3. Females were not significantly attracted to volatiles from males (χ 2 = 2.56; GL = 1; P = 0.1096), volatiles from females (χ 2 = 1.96; GL = 1; P = 0.1615) or volatiles from mating pairs (χ 2 = 4.00; GL = 1; P = 0.0555) compared to the control (clean air) (Fig. 2A). The same was observed for males, which were not significantly attracted to male volatiles (χ 2 = 6.25; GL = 1; P = 0.0124) or female volatiles (χ 2 = 1.00; GL = 1; P = 0.3173) (Fig. 2B). On the other hand, males were significantly more attracted to copulating pairs than to the control (χ 2 = 13.414; GL = 1; P = 0.0002) (Fig. 2B).

Figure 2
Olfactory choices of females (A) and males (B) of M. spectabilis to clean air versus females, males and couples in a Y olfactometer. Asterisks (*) denote significant differences (P ˂ 0.05). Numbers in brackets indicate the number of insects that responded, the number of insects that did not respond and the total number of insects tested.

Figure 3
Olfactory choices of males (A) and females (B) of M. spectabilis to an extract of volatiles released from females orcopulating couples versus hexane (control) in a Y olfactometer. Asterisks (*) denote significant differences (P ˂ 0.05). Numbers in brackets indicate the number of insects that responded, the number of insects that did not respond and the total number of insects tested.

When extracts of volatiles released from females or copulating pairs were used, 70% of the males were significantly attracted to extracts of volatiles released from copulating pairs compared to the control (n-hexane) (χ 2 = 15.52; GL = 1; P < 0.0001) (Fig. 3A). However, the males were not significantly attracted to the extract of volatiles released by the females (χ 2 = 4.00; GL = 1; P = 0.0455) (Fig. 3A). Similarly, the females were not significantly attracted to the volatiles released from the copulating pairs compared to those released from the control (χ 2 =1.53; GL = 1; P < 0.2150) (Fig. 3B). This indicates that copulating M. spectabilis release a volatile substance attractive only to males.

4. Discussion

Studying the mating behavior of M. spectabilis is a step toward understanding intraspecific communication, as has already been elucidated for other hemipterans (Rojas et al., 1990; Pires et al., 2004; Zang and Liu, 2007; Vitta and Lorenzo, 2009; Liu et al., 2023). López and Peck (1999), suggest that Cercopis sanguinolenta (Scopoli 1763) males produce an acoustic signal, and it is likely that all members of the suborder Auchenorryncha have a mechanism for recognizing and locating partners based on acoustic signals. Machado et al. (2001) showed that communication between cercopids is carried out by the production of sounds from both sexes, as these signals are transmitted through a host plant. However, other signals may also be involved in the intraspecific communication of these species, such chemicals or vision. It has been proposed that the formation and maintenance of aggregations of stink bug (Pentatomidae) is mediated by various types of stimuli, including tactile, visual and olfactory signals, but the functions of these signals need to be elucidated (Pavis et al., 1994; Fucarino et al., 2004).

Behavioral interactions of M. spectabilis males, such as touching and standing around copulating couple, have been observed in the field, greenhouse and laboratory rearing cages (Auad AM - Personal Information). This led to the hypothesis that mating M. spectabilis release substances attractive to other males. This hypothesis was supported by cage experiments using different male: female ratios and by olfactometry tests (Figures 1, 2 and 3). The consistent results across these tests, using only extracts in the olfactometer (eliminating potential interference from plants), strongly suggest the action of chemical signals.

Several orders of insects release a sex pheromone to attract individuals of the same species of the opposite sex for mating purposes (Rosén et al., 2003). Some pheromones are generally produced and released by females to attract males, which can elicit a sequence of behaviors such as males searching for females, courtship and copulation (Hickel et al., 1991; Fu et al., 2022). Fonseca et al. (2013) observed mating behavior in M. spectabilis in which males approached females to initiate the mating sequence, suggesting that males of this species may respond to chemical, visual or sound signals emitted by females. However, this study did not confirm female attraction of male in M. spectabilis (Figure 2B and 3A); males were attracted only to mating pairs.

Some studies have indicated that olfactory chemical signals mediate insect mating (Soroker et al., 2004). In fact, behavioral evidence has shown that Rhodnius prolixus (Hemiptera: Reduviidae) couples emit volatiles that promote the aggregation of males of the same species (Pontes et al., 2014), a behavior also demonstrated for Triatoma infestans (Hemiptera: Reduviidae) (Manrique and Lazzari, 1995) and for M. spectabilis in this study. Pontes and Lorenzo (2012) reported that occlusion of the metasternal glands affected mating success and male aggregation around mating pairs in T. infestans and R. prolixus, inferring that these glands release chemical signals that mediate these behaviors in insects.

In electrophysiology studies (Sanchez et al., 1995) suggested the presence of chemical signals released by one or both sexes during mating in T. infestans. Ondarza et al. (1986) reported the existence of a chemical signal for Triatoma mazzottii (Usinger), which acts as an “aphrodisiac” and is released when the insects are copulating. In the olfactometer study carried out in this study, the males were not attracted to the extracts of males or females, but they were attracted to the extracts of copulating pairs (Figures 2 and 3)., In olfactometer tests with Lycorma delicatula (White) (Hemiptera: Fulgoridae), Faal et al. (2022) reported male attraction of both same- and opposite-sex conspecifics via insect-derived volatiles, suggesting the presence of pheromones used by males to find conspecifics for aggregation and females for mating. They also found that prior to mating, only males were attracted to volatiles from both sexes, whereas during mating, males distinguished between females and male volatiles. Cardé (2014) stated that these behaviors may be explained by the existence of two chemical signals, one for aggregation and the other for sexual aggregation; a single chemical signal for sexual aggregation could be responsible for the release of both sexes before mating.

In this study, M. spectabilis was found to interact more (touch) with the other males in the copulating pairs in the cages with four males to one female (4:1) (Figure 1 A) than with the pair surrounded by females (1:4). In both cages and olfactometry assays, only males were attracted to copulating pairs or their extracts. Gregarious mature male locusts (Locusta migratoria L.,1758) emit high levels of the aggregation pheromone 4-vinylanisole, which synchronizes female sexual maturation, promoting synchronous copulation and oviposition, and ultimately ensuring synchronous hatching of offspring (Chen et al., 2022). This behavior could also explain the presence of males around the pair in copulation with M. spectabilis, but the mechanisms may not be the same and need to be elucidated. Pontes (2010) observed that in R. prolixus cages with four males and a virgin female, free males tended to aggregate around the copulating pair. This aggregation may increase reproductive efficiency by facilitating faster location of receptive females in infested areas, maximizing reproductive success by reducing time and energy expent searching for mates. Furthermore, aggregation can intensify male-male competition for mating opportunities, favoring sexual selection and promoting advantageous phenotypic characteristics.

The same aggregation trend was recorded for males of the bed bug Riptortus pedestris (R. clavatus) (Heteroptera: Alydidae), one component of the chemical blend release affects the attractiveness of other males (Mizutani et al., 2008). The responses at close proximity to the sources of these volatiles were in response to physical contact between the male and the female, suggesting that these chemical attraction signals are emitted during copulation, with the male oriented toward the source of the pheromone (searching behavior).

Mahanarva sp. copulate up to three times in their lifetime (Ballesteros and Gallego, 1999; Fonseca et al., 2013). Although infrequent, M. spectabilis copulations are long, lasting 300 ± 35 min in this study, with no significant difference based on male:female ratio. This extended copulation time in Mahanarva sp. suggests that male of some species require more time for seminal fluid transfer (Rodrigues et al., 2009; Fonseca et al., 2013). Partner guarding by male to ensure paternity has also been observed in other Hemiptera (Carroll, 1991; Schöfl and Taborsky, 2002; Fonseca et al., 2013). Mating guarding through prolonged mating is common in some insect species (Arnqvist 1997). Post-mating associations are one mechanism by which males reduce the likelihood of their female partners remating (Alcock 1994). In the heteropteran Gerris lateralis (Schummel) (Heteroptera: Gerridae), males remain on the female's back for extended period without genital contact (Arnqvist, 1988), and in some species, such as in Gerris remigis (Say), guarding males stridulate to deter rival intrusions (Wilcox and Di Stefano, 1991).

Insect pest monitoring and control programs that use chemical signals are important for various insect groups (Moreira et al., 2013). The use of these substances can increase the effectiveness of pheromone traps for controlling outbreaks of these pests (Pal et al., 2023). Our results demonstrated that there are attractiveness of males to copulating pairs in the olfactometry test, in which males were significantly attracted only to copulating pairs and to the extract of copulating pairs. The females showed no olfactory attraction to any of the odor sources offered. Thus, additional experiments should be carried out to determine whether the mechanisms involved in communication between individuals of M. spectabilis are repeated in the field with extracts from copulating pairs. Confirming the presence of these volatiles was a crucial first step in understanding their function in chemical communication during mating. These data suggested that chemical communication during mating could informe new control strategies, such as push-pull tactics, using combined stimuli to manipulate the distribution and abundance of M. spectabilis.

Acknowledgements

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico; Fundação de Amparo à Pesquisa do Estado de Minas Gerais and Embrapa Gado de Leite (CNPGL) for supporting our research. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - 307956/2023-7) Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG- APQ 03630/23).

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Publication Dates

• Publication in this collection
  26 May 2025
• Date of issue
  2025

History

• Received
  28 Oct 2024
• Accepted
  12 Mar 2025