The Importance of Gut Symbionts in the Development of the Brown Marmorated Stink Bug, Halyomorpha halys (Stål)

Taylor, Christopher M.; Coffey, Peter L.; DeLay, Bridget D.; Dively, Galen P.

doi:10.1371/journal.pone.0090312

Cited by 94 publications

(83 citation statements)

References 32 publications

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“…In the control group, most of the nymphs (44/48 ϭ 91.7%) were symbiont positive, which was in sharp contrast with the sterilized group, wherein all the nymphs (0/48 ϭ 0%) were symbiont negative. These results indicate that the symbiont is vertically transmitted to the next generation of P. splendens via egg surface contamination, as known for many other stinkbugs (1,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21). Population dynamics of the symbiont.…”

Section: Resultsmentioning

confidence: 54%

“…4). Such obligate symbiotic bacteria associated with the midgut symbiotic organs have been described from a variety of stinkbugs of the families Pentatomidae (15,17,18,20,21,34,44), Scutelleridae (16,45,46), Cydnidae (19), Plataspidae (24,25,47,48), Acanthosomatidae (14), Parastrachiidae (22), Urostylididae (26), and others. As are the cases of the gut symbiotic bacteria associated with the stinkbugs representing the superfamily Pentatomoidea (21,49,50), the gut symbiont of P. splendens was placed within the Enterobacteriaceae of the Gammaproteobacteria, in contrast to the betaproteobacterial gut symbionts widely found across the superfamilies Lygaeoidea and Coreoidea (5).…”

Section: Discussionmentioning

confidence: 99%

“…In these stinkbugs, adult females excrete symbiont-containing materials from the anus, which are orally acquired by their offspring for vertical symbiont transmission. Most commonly, as observed in the families Pentatomidae, Scutelleridae, Acanthosomatidae, and Cydnidae, vertical symbiont transmission is set up upon oviposition by egg surface contamination with symbiont-containing materials and establishes upon egg hatching by nymphal oral exploitation of the egg surface (1,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21). In several presocial stinkbugs of the families Parastrachiidae and Cydnidae, adult females continuously attend and take care of their eggs and excrete symbiont-containing materials just before or after egg hatching, which newborns consume and establish vertical symbiont transmission (22,23).…”

mentioning

confidence: 99%

“…In acanthosomatid stinkbugs, novel paired organs for symbiont transmission, which are similar to but anatomically distinct from those of urostylidid stinkbugs, are present near the female genital chamber (14). On the other hand, such femalespecific traits for vertical symbiont transmission have been poorly described for stinkbugs of the family Pentatomidae, except for a few early morphological observations (1,30,31), although members of the largest stinkbug group, embracing over 900 genera and 4,500 species and economically the most important (32,33), are generally associated with midgut symbiotic bacteria that are vertically transmitted via egg surface contamination (1,12,12,13,15,17,18,20,34).…”

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confidence: 99%

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Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Hayashi

Hosokawa

Meng

et al. 2015

Appl Environ Microbiol

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dMany stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug, Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugs Plautia stali and Carbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae. Many insects are associated with microbial mutualists in the gut lumen, inside the body cavity, or within the cells (1, 2). For ecological and evolutionary persistence of such mutualistic associations, vertical symbiont transmission through host generations is among the pivotal processes, although nonvertical (i.e., horizontal or environmental) symbiont transmission may also be prevalent in marine invertebrates, plants, and some insects (3-5).In intracellular associations such as Buchnera in aphids and Wigglesworthia in tsetse flies, vertical symbiont transmission usually occurs prenatally to developing eggs or embryos within maternal bodies (1,(6)(7)(8). In extracellular associations such as gut microbes in termites and stinkbugs, by contrast, vertical symbiont transmission tends to occur postnatally outside the maternal bodies via nymphal feeding of symbiont-containing excrements (1, 9, 10).The majority of plant-sucking stinkbugs (order Hemiptera: suborder Heteroptera: infraorder Pentatomomorpha: superfamily Pentatomoidea) are associated with bacterial symbionts of a beneficial nature in a posterior region of the midgut, where numerous crypts develop and harbor specific symbiotic bacteria the...

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Section: Resultsmentioning

confidence: 54%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Hayashi

Hosokawa

Meng

et al. 2015

Appl Environ Microbiol

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“…These insects possess a number of sacs or tubular outgrowths called crypts or ceca in a posterior region of the midgut, wherein a specific bacterial symbiont is harbored (3)(4)(5). When the gut symbionts are suppressed or eradicated experimentally, the symbiont-free insects tend to suffer retarded growth and elevated mortality (6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18), indicating important biological roles of the symbionts for their hosts. In addition to harboring these primary gut symbionts, many stinkbugs also harbor endosymbiotic bacteria of a facultative nature, such as Wolbachia, Rickettsia, Sodalis, and Lariskella species (19)(20)(21)(22), although it has been poorly understood how these secondary symbionts affect their host's phenotype and fitness.…”

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confidence: 99%

Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)

Matsuura

Hosokawa

Serracin

et al. 2014

Appl Environ Microbiol

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dStinkbugs of the genus Antestiopsis, so-called antestia bugs or variegated coffee bugs, are notorious pests of coffee plants in Africa. We investigated the symbiotic bacteria associated with Antestiopsis thunbergii, a major coffee plant pest in Rwanda. PCR, cloning, sequencing, and phylogenetic analysis of bacterial genes identified four distinct bacterial lineages associated with A. thunbergii: a gammaproteobacterial gut symbiont and symbionts representing the genera Sodalis, Spiroplasma, and Rickettsia. In situ hybridization showed that the gut symbiont densely occupied the lumen of midgut crypts, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont sparsely and sporadically infected various cells and tissues. Diagnostic PCR survey of 154 A. thunbergii individuals collected at 8 localities in Rwanda revealed high infection frequencies (100% for the gut symbiont, 51.3% for the Sodalis symbiont, 52.6% for the Spiroplasma symbiont, and 24.0% for the Rickettsia symbiont). These results suggest that the gut symbiont is the primary symbiotic associate of obligate nature for A. thunbergii, whereas the Sodalis symbiont, the Spiroplasma symbiont, and the Rickettsia symbiont are the secondary symbiotic associates of facultative nature. We observed high coinfection frequencies, i.e., 7.8% of individuals with quadruple infection with all the symbionts, 32.5% with triple infections with the gut symbiont and two of the secondary symbionts, and 39.6% with double infections with the gut symbiont and any of the three secondary symbionts, which were statistically not different from the expected coinfection frequencies and probably reflected random associations. The knowledge of symbiotic microbiota in A. thunbergii will provide useful background information for controlling this devastating coffee plant pest.

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Effects of three chitin synthesis inhibitors on egg masses, nymphs and adults of Halyomorpha halys (Hemiptera: Pentatomidae)

Masetti

Rathé²,

Robertson

et al. 2023

Pest Management Science

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Background Halyomorpha halys, (brown marmorated stink bug, BMSB), is a high‐concern invasive species causing severe damage to orchards in many countries outside its native Asian range. Management methods other than frequent sprays of broad‐spectrum insecticides are needed to restore integrated pest management (IPM) practices in orchards. Chitin synthesis inhibitors are usually regarded as desirable options in IPM programs because of lower toxicity to beneficial insects and non‐target organisms compared to neurotoxic insecticides. In this study, the activity of three chitin synthesis inhibitors (namely buprofezin, novaluron and triflumuron) was investigated on BMSB egg masses, third instars and adults by means of laboratory bioassays. Results Novaluron and to a lesser extent triflumuron were detrimental to BMSB nymphs exposed to residues on potted peach plants. Novaluron caused high mortality among early instars that emerged from sprayed egg masses. No significant differences were found between buprofezin and water control on eggs or third instars. When sprayed on BMSB adults, none of the chitin synthesis inhibitors affected survival, fecundity, or egg hatching. Conclusion Given the activity on nymphs, but the lack of effects on adults, novaluron and triflumuron might be considered for field applications only as a tool in a wider management strategy along with other methods aimed at preventing the invasion of crops by BMSB adults. © 2023 Society of Chemical Industry.

show abstract

The Importance of Gut Symbionts in the Development of the Brown Marmorated Stink Bug, Halyomorpha halys (Stål)

Cited by 94 publications

References 32 publications

Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)

Effects of three chitin synthesis inhibitors on egg masses, nymphs and adults of Halyomorpha halys (Hemiptera: Pentatomidae)

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