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Stink Bug Communication with Multimodal Signals Transmitted Available online at www.ijournalse.org Emerging Science Journal Vol. 3, No. 6, December, 2019 Review Article Stink Bug Communication with Multimodal Signals Transmitted through Air and Substrate Andrej Čokl a*, Alenka Žunič-Kosi a, Raul Alberto Laumann b a Department of Organisms and Ecosystems Research, National Institute of Biology, Večna pot 111, SI-1000 Ljubljana, Slovenia b Laboratorio de Semioquimicos, Embrapa Recursos Geneticos e Biotecnologia, Avda W5 Norte (Final), 71070, Brasilia, DF, Brazil Abstract Keywords: This review represents complex mechanisms and processes of multimodal communication in stink Insects; bugs. During reproductive behavior the airborne and substrate-borne signals enable mate recognition, Pentatomidae; mediate directionality of movement, eliminate rivals and motivate partners for copulation. Species Communication; specific characteristics prevent hybridization at various levels of mating behavior. Male sex and/or Signals; aggregation pheromones as uni- or multicomponent signals attract mates to land on the same plant Multimodality; and there, trigger females to call males by vibratory signals, transmitted through the plant. Transmission Medium; Communication during courtship runs at short distance with visual, airborne, substrate-borne and Environment. contact chemical and mechanical signals. Abdomen vibrations produce the main repertoire of female and male calling, courtship and rival vibratory signals. To increase their informational value, stink bugs tune signal frequency, amplitude and temporal characteristics with mechanical properties of plants. The airborne component of species non-specific and high amplitude signals, produced by body tremulation and wing buzzing enables communication contact between mates standing on mechanically isolated plants. Female vibratory signals increase the amount of male emitted pheromone and the latter keeps female calling. Interaction, synergy and characteristics of visual, contact chemical and vibratory signals, exchanged during courtship remain under-investigated. Female and male competition for access to copulation in imbalanced sex conditions is characterized Article History: by duetting with rival song vibratory signals. Different receptors in and on different parts of the body are able to detect with high sensitivity multimodal airborne and substrate-borne communication Received: 10 September 2019 signals. The relevance of the multimodal communication for the reproductive success of stink bugs is Accepted: 21 November 2019 discussed. Published: 01 December 2019 1- Introduction Millions of insect species inhabit air, water and land. Population success depends crucially on efficient communication, which enables solitary species to meet in the field and holds insect societies together. To preserve above-threshold signal-to-noise ratio at the necessary distance, solitary insects developed, through evolution, efficient mechanisms to communicate by unimodal, multimodal and multicomponent signals [1] transmitted through different media. Investigation of insect communication demands a holistic approach to understand the role, synergy and interaction of specific processes underlying different phases of behavior. The study on the wandering spider Cuppienius salei (Keyserlink, 1877) represents a nice example of such an approach, showing the complex system of communication through different channels in various environmental conditions [2]. Comparable studies are rare in insects and, despite numerous solutions and a variety of mechanisms, there are very few common and general conclusions. Stink bugs (Heteroptera: Pentatomidae: Pentatominae) represent a smaller but economically important group of * CONTACT: [email protected] DOI: http://dx.doi.org/10.28991/esj-2019-01203 © 2019 by the authors. Licensee ESJ, Italy. This is an open access article under the terms and conditions of the Creative Commons Attribution (CC-BY) license (https://creativecommons.org/licenses/by/4.0/). Page | 407 Emerging Science Journal | Vol. 3, No. 6 plant-dwelling phytophagous insects with several pest species that inspired numerous studies of their biology, ecology, feeding habits and conditions of their plant environment [3]. This knowledge represents the important and valuable background for investigating communication by chemical, mechanical and visual signals adapted for efficient transmission through air and substrate [4] and for developing various biorational control methods [5]. The present review starts with a description of the stink bug’s general biology, ecology, feeding habits and environment. Environmental conditions and properties of transmission media have determined characteristics of chemical, mechanical and visual signals. The authors then present a comparative overview on characteristics of stink bug chemical and mechanical signals, together with the evolution of signal production and sensory mechanisms. The review terminates by describing the recognition, orientation, rivalry and social conflict processes that take place during group mating behavior. The authors are aware that this review on stink bug communication is incomplete. We can expect that comparative studies among stink bugs and other groups will represent exceptions that will in the future enable a broader and deeper understanding of communication in plant-dwelling insects. 2- Biology and Environment Stink bugs (Pentatomidae) represent the fourth largest family of Heteroptera with nine subfamilies, about 900 genera and more than 4,700 species [6]. This relatively small group of solitary living insects contains several invasive and economically important pest species [3, 7]. Pentatomidae are predominantly plant feeders, with the exception of the subfamily Asopinae whose species feed principally on soft-bodied dipteran, lepidopteron and hymenopteran larvae [8]. The subfamily Pentatominae represents the most diverse pentatomide subfamily with over 2,800 species, divided into more than 40 tribes. Pentatominae feed and mate exclusively on different host plants, although generalists like Nezara viridula (L.) prefer brassicaceous plants and legumes [9]. Species that feed predominantly on immature seeds and fruits move in their absence to plants available at the time where they stay [10]. Many polyphagous stink bugs that feed preferentially on plants of particular taxa get attracted to them at long distance by their physical and/or chemical traits, such as chemical volatiles, surface waxes, nutrients and secondary compounds [10]. Preference for certain taxa is not genus-specific and, for example, Chinavia, Dichelops, Euschistus, Nezara, Palomena, Piezodorus and Thyanta species gather on soybean, wild beans and other legumes [3, 7, 9-12]. Less-preferred alternative host plants from families Amaranthaceae, Solenaceae and Fabaceae attract non-specific species like N. viridula, Piezodorus guildinii (Westwood), Euschistus heros (Fabr.), Edessa meditabunda (Fabr.), Dichelops furcatus (Fabr.), Dichelops melacanthus (Dallas) and Thyanta perditor (Fabr.) [10]. This less-preferred associated host may improve stink bug fitness when it complements the diet or in the lack of host plants [13]. The life cycle of Pentatomidae includes the reproductive and non-reproductive (hibernation, diapause) phases. Saulich and Musolin [14] investigated diapause in 43 stink bug species from the Temperate Zone, with the majority of them hibernating as adults, just two species overwintering as nymphs and another two as eggs. Day-length and temperature induce most Pentatominae to enter adult diapause irrespective of their feeding preferences. Obligate diapause was described in Palomena prasina (L.) and Palomena angulosa (Motschulsky). In Menida scotti (Puton) the obligate diapause for females was confirmed, with males remaining active over winter. During diapause N. viridula adults migrate to hidden places, change color and decrease the metabolic rate [15]. Santos and co-workers [16] demonstrated abdominal fat hypertrophy in the early stage of diapausing in Oebalus poecillus (Fabr.). During diapausing the authors measured decreased amount of body fat filled in the abdominal cavity. Dimensions of ovaries and testes steadily increase during development from immature to reproductive phase [16]. O. poecillus males reach sexual maturation inside and females outside the hibernation sites. Profound knowledge on stink bug biology, ecology, life cycle and feeding habits gives a solid basis to understand the group’s highly invasive status in different environments on all continents except the Arctic and Antarctic. Stink bug population success depends on efficient communication during reproductive behavior in the field by attraction of dispersed mates to meet on the same plant, where mating proceeds to copulation during calling, courtship and rivalry phases. During these processes stink bugs communicate on a long-range scale in the field by air-transmitted chemical signals, on a middle-range scale on a plant by substrate-borne vibratory signals and over a short distance by visual, airborne and contact mechanical and chemical signals. 3- Reproductive Behavior and Communication Reproductive behavior of solitary stink bugs runs through different phases, starting in the field with long-range attraction of mates to meet on a plant, and there it proceeds to copulation by rivalry, calling and courtship. Communication provides information on species identity and directionality of movement to reach the calling mate, and it resolves social conflicts in imbalanced
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