Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae)

Zhang, G. and Weirauch, C. 2011. Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). —Acta Zoologica (Stockholm) 00 : 1–10. For more than 50 years, specialized dermal glands that secrete sticky substances and specialized setae have been known from the legs of New World assassin bugs in the genus Zelus Fabricius (Reduviidae: Harpactorinae). The gland secretions and specialized ‘sundew setae’ are involved in enhancing predation success. We here refer to this predation strategy as ‘sticky trap predation’ and the specialized dermal glands as ‘sticky glands’. To determine how widespread sticky trap predation is among Reduviidae, we investigated taxonomic distribution of sticky glands and sundew setae using compound light microscopical and scanning electron microscopical techniques and sampling 67 species of Reduviidae that represent 50 genera of Harpactorini. We found sticky glands in 12 genera of Harpactorini and thus show that sticky trap predation is much more widespread than previously suspected. The sticky glands vary in shape, size and density, but are always located in a dorsolateral position on the fore tibia. Sundew setae are present in all taxa with sticky glands with the exception of Heza that instead possesses unique lamellate setae. The sticky trap predation taxa are restricted to the New World, suggesting a New World origin of this unique predation strategy.     

Factors regulating predation by first-instar spined assassin bugs [Sinea diadema (Fabricius)] (Hemiptera: Reduviidae)

Selected nutritional and developmental factors regulating the predatory behavior of first-instar spined assassin bugsSinea diadema (Fabricius) (Hemiptera: Reduviidae) were investigated. The longevity of unfed nymphs provided with free water, bean pod sections, or glucose solutions was not significantly greater than that of unfed nymphs which were not provided with a source of water. First-instarS. diadema that were provided with larvae ofEphestia kuehniella Zeller (Lepidoptera: Pyralidae) as prey began feeding 1.9 (±0.9) days after hatching. In contrast, first-instarS. diadema that were provided with conspecifics of the same age did not begin feeding until they were 3.9 (±0.9) days old. These results suggest that the potential nutritional benefits to be gained from feeding equal or outweigh the risk of attacking prey capable of effective self-defense only when nymphs have not fed for 4 days after hatching. Providing the nymphs with water or glucose solutions significantly delayed the onset of conspecific predation. Additional data are presented which demonstrate that first-instarS. diadema are not restrained from preying on siblings by kin recognition.     

Comparative trichome morphology in feather-legged assassin bugs (Insecta: Heteroptera: Reduviidae: Holoptilinae)

The trichome in ant-feeding Holoptilinae (Insecta: Heteroptera: Reduviidae) comprises remarkable modifications of abdominal sternites 2 and 3. It has been hypothesized that this structure plays a role in attracting and drugging ants. In the present study the trichome of 14 species of Holoptilini, comprising 11 species of Ptilocnemus Westwood and representatives of three additional genera of Holoptilini, is examined using scanning electron and light microscopy. The astoundingly diverse species-level modifications of sternites and vestiture are described and primary homology hypotheses are proposed. The trichome provides species-specific diagnostic characters within Ptilocnemus and evidence for species-groups within the genus, but also for the sistergroup relationship of Ptilocnemus and Smiliopus Bergroth. The comparative morphology establishes a framework for investigations into systematics, functional morphology, and behavioral ecology of these myrmecophagous assassin bugs.     

Comparative trichome morphology in feather-legged assassin bugs (Insecta: Heteroptera: Reduviidae: Holoptilinae)

The trichome in ant-feeding Holoptilinae (Insecta: Heteroptera: Reduviidae) comprises remarkable modifications of abdominal sternites 2 and 3. It has been hypothesized that this structure plays a role in attracting and drugging ants. In the present study the trichome of 14 species of Holoptilini, comprising 11 species of Ptilocnemus Westwood and representatives of three additional genera of Holoptilini, is examined using scanning electron and light microscopy. The astoundingly diverse species-level modifications of sternites and vestiture are described and primary homology hypotheses are proposed. The trichome provides species-specific diagnostic characters within Ptilocnemus and evidence for species-groups within the genus, but also for the sistergroup relationship of Ptilocnemus and Smiliopus Bergroth. The comparative morphology establishes a framework for investigations into systematics, functional morphology, and behavioral ecology of these myrmecophagous assassin bugs.     

Encounters between adult spined assassin bugs,Sinea diadema (F.) (Hemiptera: Reduviidae): The occurrence and consequences of stridulation

The sequence of events leading to the resolution of agonistic interactions between adult femaleSinea diadema (F.) (Hemiptera: Reduviidae) is described. Contact between these predatory bugs resulted in a series of defensive and offensive actions, including stereotypical posturing and striking movements of the forelegs. Although these encounters usually escalated in intensity and frequency of contact, they rarely resulted in injury or cannibalism. Instead, one individual retreated from the perch. The original resident on the perch retreated in 70% of the encounters. Stridulation was observed during 33% of the encounters. Stridulating individuals retreated more often than their nonstridulating opponents, indicating that stridulation may be a startle mechanism employed by temporarily disadvantaged individuals to escape from encounters. These encounters were conflicts in which the participants are both potential predators and possible prey. The combinations of posturing, striking, and stridulation that occurred during encounters may have provided each bug with information concerning the identity and relative fitness of its opponent. If an individual is fit, it may be advantageous for it to probe the defensive capabilities of its opponent, since its own risk is low, and a less fit opponent could be killed and eaten.     

Morphology of arolia in Auchenorrhyncha (Insecta,Hemiptera)

The pretarsal arolium serves as an attachment device in many groups of insects, enabling them to walk efficiently on smooth surfaces, where claws alone do not provide sufficient foothold. The arolia of representatives of all major lineages of Auchenorrhyncha are described and illustrated, mainly using scanning electron microscopy and histology. Glands inside the lumen of the arolia are described for the first time in this group. It is shown that the morphology of arolia within Auchenorrhyncha differs considerably. Some of them are even distinctly bilobed. The cuticle of the contact zone is thickened and formed of branching chitinous rods. In some cases, two layers of rods oriented in different directions were found. An extended definition of “arolium” is proposed. J. Morphol. 275:1217–1225, 2014. © 2014 Wiley Periodicals, Inc.     

Effect of predators and host phenology on the maternal and reproductive behaviors ofGargaphia lace bugs (Hemiptera: Tingidae)

Lace bugs of the genus Gargaphia specialize on taxonomically and ecologically diverse host plants. To examine the impact of predation pressure and host phenology on Gargaphia subsocial and reproductive behavior, we compared G. tiliae, a woodland species restricted to riparian trees in the genus Tilia, and G. solani, a specialist on Solanum in early successional habitats. Both lace bug species exhibit maternal care of eggs and nymphs. Predator densities associated with Solanum were higher than those associated with Tilia and were correlated with higher levels of maternal aggression exhibited by G. solani. In both habitats, artificial exclusion of predators significantly increased nymphal survivorship over maternally guarded broods. Both species reduced the costs associated with maternal care by ovipositing into the egg masses of conspecifics. Gargaphia solani and G. tiliae differed most strikingly in voltinism and thus the potential for iteroparity. Leaf age determined the reproductive future of G. tiliae nymphs independent of photoperiod or temperature. Feeding on plants with young foliage was sufficient to trigger oviposition. Constraints imposed by host plants on life-history patterns and maternal options are discussed.     

Aggression and risk assessment during predatory interactions between first-instarSinea diadema (Fabricius) (Hemiptera: Reduviidae)

The behaviors exhibited by first-instarSinea diadema (F.) (Hemiptera: Reduviidae) during intraspecific interactions are described. Five distinct behaviors were characterized: posturing, striking, stalking, stridulating, and beaking. Distinct bouts of grappling were also noted. Interactions between unfed 2-day-old nymphs, unfed 3-day-old nymphs, and unfed 5-day-old nymphs were recorded and analyzed. The behavior of the nymphs changed with the duration of food deprivation. As the period of food deprivation increased from 2 to 5 days, the frequency of posturing decreased as the frequency of beaking increased. During noncannibalistic interactions, posturing or striking by one nymph was most frequently followed by posturing by the other nymph. In contrast, during cannibalistic interactions, posturing or striking was usually followed by beaking. The incidence of grappling increased with the duration of food deprivation. Moreover, grappling always preceded cannibalism. Although first instars were capable of capturing and killing conspecifics of the same age, cannibalism occurred only after 4 days of food deprivation. These results suggest that a decision-making process is involved. During interactions the nymphs can assess the vulnerability of the opponent. Whereas recently emerged nymphs usually forego the risk of attacking conspecifics, the attacks made by nymphs deprived of food are more persistent despite the danger of predation by their opponent.     

Phylogeny and the colourful history of jewel bugs (Insecta: Hemiptera: Scutelleridae)

Members of the family Scutelleridae (Heteroptera: Pentatomomorpha: Pentatomoidea) are also called shield bugs because of the greatly enlarged scutellum, or jewel bugs because of the brilliant colours of many species. All scutellerids are phytophagous, feeding on various parts of their host plants. Due to lack of obvious synapomorphies and the failure to apply rigorous phylogenetic methods, the higher classification of Scutelleridae has been disputed for more than 150 years. Here we reconstructed a phylogeny of Scutelleridae based on complete sequences of 18S and 28S nuclear rDNAs and all 13 protein‐coding genes of the mitochondrial genome, with the sampled taxa covering all of the currently recognized subfamilies. The monophyly of Scutelleridae was confirmed by the congruence of the results of analyses conducted using Bayesian inference, maximum likelihood and maximum parsimony. The phylogenetic relationships among subfamilies were well resolved for the first time. Furthermore, time‐divergence studies estimated that the time of origin of Scutelleridae was in the Early Cretaceous (142.1–122.8 Ma), after the origin of the angiosperms. The diversification between the extant subfamilies of Scutelleridae and within the subfamilies occurred from the late Palaeocene to the late Miocene, simultaneously with the rise of the major groups of angiosperms and other phytophagous insects.     

A lesser predilection for bugs: Hemiptera (Insecta) diversity in tropical rain forests

Data are presented on the Hemiptera fauna of a moderately large and topographically diverse area of tropical rain forest in Sulawesi Utara, Indonesia. Insects were sampled using several methods at several sites over a 1-year period. The numbers of described and undescribed species captured is used to predict the number of extant species of both Hemiptera and total insects in the world. The global estimates of 1.84–2.57 million species of insect are much lower than the 10–80 million predicted by Erwin and Stork from a study of tropical Coleoptera. The reasons for believing that the lower estimates are more reliable are discussed.     

Phylogeny and diversification of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha)

Climate fluctuations and tectonic reconfigurations associated with environmental changes play large roles in determining patterns of adaptation and diversification, but studies documenting how such drivers have shaped the evolutionary history and diversification dynamics of limnic organisms during the Mesozoic are scarce. Members of the heteropteran infraorder Nepomorpha, or aquatic bugs, are ideal for testing the effects of these determinants on their diversification pulses because most species are confined to aquatic environments during their entire life. The group has a relatively mature taxonomy and is well represented in the fossil record. We investigated the evolution of Nepomorpha based on phylogenetic analyses of morphological and molecular characters sampled from 115 taxa representing all 13 families and approximately 40% of recognized genera. Our results were largely congruent with the phylogenetic relationships inferred from morphology. A divergence dating analysis indicated that Nepomorpha began to diversify in the late Permian (approximately 263 Ma), and diversification analyses suggested that palaeoecological opportunities probably promoted lineage diversification in this group.     

Novel peptides from assassin bugs (Hemiptera: Reduviidae): isolation, chemical and biological characterization.

Three novel peptides were isolated from the venomous saliva of predatory reduviids. They were identified by mass spectrometry and HPLC analysis and consist of 34-36 amino acid residues. They are relatively homologous to the calcium channel blockers omega-conotoxins from marine cone snails and belong to the four-loop Cys scaffold structural class. Ptu1, the shortest peptide, was chemically synthesized (sPtu1) and co-eluted with its native form. Circular dichroism spectra of the sPtu1 showed a high content of beta-turns similar to that of omega-conotoxins GVIA and MVIIA. Electrophysiological experiments demonstrated that sPtu1 reversibly blocks the N-type calcium channels expressed in BHK cells.     

Fine structure of the salivary glands of Triatoma infestans (Hemiptera: Reduviidae)

The fine structure of the salivary glands of adult Triatoma infestans (Hemiptera: Reduviidae) bugs has been analyzed. Stereomicroscopy and scanning electron microscopy showed that each insect presents a pair of salivary glands, each pair containing three distinct units (main, supplementary, and accessory) with different sizes and colors. Transmission electron microscopy demonstrated that all gland units consist of a monolayer of epithelial cells surrounding a large central lumen. The gland units are enveloped by a thick basal lamina containing bundles of muscle cells. Microvilli are present at the apical plasma membrane domain of the gland cells, thus enlarging the available membrane area for saliva secretion towards the large gland lumen, although occasionally budding vesicles could be observed among the microvilli. Cytochemical analysis showed that the salivary gland cells of T. infestans present abundant endoplasmic reticulum profiles and several lipid droplets.     

Influence of the intestinal anticoagulant in the feeding performance of triatomine bugs (Hemiptera; Reduviidae)

Triatomines are haematophagous insects in all post-embryonic life stages. They are vectors of Trypanosoma cruzi, the causative agent of Chagas disease. Their vectorial ability is influenced by their feeding performance, which varies greatly amongst species. Recent work showed that inhibition of the coagulation process in the anterior midgut (crop) environment considerably influences the blood meal size. In this work, we performed a comparative study of the level of anticoagulant activity in the saliva and crop contents of three triatomine species - Triatoma infestans, Triatoma brasiliensis and Rhodnius prolixus - and correlated this with their feeding performance on live hosts. Moreover, the feeding parameters on a large diameter vessel influenced by the crop anticoagulants were evaluated in detail. The anticoagulant activity was significantly higher in the crop contents than in salivary glands, varying from 1.6-fold higher for R. prolixus to 70-fold higher for T. brasiliensis. Amongst the species, T. brasiliensis had the lowest crop anticoagulant activity, the lowest concentration of thrombin inhibitor, and took the longest to feed. Triatoma brasiliensis nymphs that had their intestinal anticoagulant (brasiliensin) knocked down by RNA interference had the lowest capacity to maintain cibarial pump frequency at higher levels throughout the feeding process and consequently a lower ingestion rate (mg/min), even when fed under favourable conditions (large diameter vessel). However, the feeding difficulty for brasiliensin knockdown T. brasiliensis nymphs was reversed by treating the host mice with heparin (a potent systemic anticoagulant) before blood feeding. The results indicate that crop anticoagulant activity influences modulation of the blood-pumping frequency to the intestine and significantly affects the feeding efficiency of triatomine spp. on live hosts.     

Evaluating potential trap crops for managing leaffooted (Hemiptera: Coreidae) and phytophagous stink bug (Hemiptera: Pentatomidae) species in peaches

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Egg size increases with maternal age in the cotton stainer bugs Dysdercus fasciatus and D.cardinalis (Hemiptera: Pyrrhocoridae)

Abstract.

• 1 Egg-size variation over the reproductive span of laboratory-reared females is described in two species of cotton stainers: Dysdercus fasciatus Sign. from woody Malvales and D.cardinalis Gerst. from herbaceous Malvales.
• 2 Egg size increases with maternal age due to a decrease in clutch size as maternal age advances in both species.
• 3 The two species are similar in size, but egg size is about 28% larger and clutch size about 19% smaller in D.fasciatus than in D.cardinalis. These contrasts may be related to the host-plant biology which differs between the two species.

     

Sampling and distribution pattern of Trioza erytreae Del Guercio, 1918 (Hemiptera: Triozidae) in citrus orchard

Developing efficient sampling protocols is essential to monitor crop pests. One vector of the citrus disease HLB, the African citrus psyllid Trioza erytreae Del Guercio, 1918 (Hemiptera: Triozidae), currently threatens the lemon industry throughout the Mediterranean region. In this work, a pool of sampling methods devoted to monitoring the population of T. erytreae was compared, its spatial distribution in the orchard was assessed, and the minimum sampling effort for the best sampling method was estimated. Three lemon orchards in North-western Portugal were sampled for one year using two types of yellow sticky traps (standard yellow and fluorescent Saturn yellow), B-vac sampling and sweep net sampling. The method that best performed, in terms of cost-efficiency, was the yellow sticky traps. The two colours of the sticky traps tested did not yield a significantly different number of catches. The spatial distribution throughout the orchards was found to be aggregated towards the borders. A minimum of three sticky traps per hectare was found to be enough to estimate the population at 90% accuracy for the mean during the outbreak. These results should help to monitor and anticipate outbreaks that may even colonize neighbour orchards. Studies on the local dispersion patterns of T. erytreae throughout the orchard are mandatory to further refine and optimize efficient monitoring protocols.     

Functional response and predation of Nabis kinbergii （Hemiptera. Nabidae） to Plutella xylostella （Lepidoptera. Plutellidae）

The functional response of adult Nabis kinbergii （Hemiptera： Nabidae） to density of diamondback moth Plutella xylostella （Lepidoptera： Plutellidae） was investigated under laboratory conditions. Holling＇ s （1959） type Ⅱ model was found to be a good fit for the observed functional response of this predator. The numbers of P. xylostella consumed increased with temperature from 15℃ to 35℃. The maximum number of prey killed was observed at 35℃, with average of 10.3 and 8.3 forth instar larvae consumed by adult females and males of N. kinbergii, respectively. The predation of N. kinbergii on P. xylostella increased with successive immature stages. The number of prey consumed by predators decreased as the body size of prey increased. An average of 131 eggs or 95 larvae of P. xylostella were killed by a single of female adult in 24 hours at 24＂C. The pupae of P. xylostella were observed to be eaten by fifth instar nymphs and adults N. kinbergiiin numbers of less than an average of 0.7 pupae per predator in 24 hours at 24＂C. Predation preference by N. kinbergii was also investigated. The number of P. xylostella and Myzus persicae killed by female N. kinbergii was not significantly different, but males killed significantly more P. xylostella than M. persicae. Both eggs and larvae of P. xylosteUa were killed in significantly greater number than those of Pieris rapae in the same feeding arena.     

Influence of data conflict and molecular phylogeny of major clades in Cimicomorphan true bugs (Insecta: Hemiptera: Heteroptera)

Cimicomorpha, which consists of 16 families representing more than 19,400 species, is the largest infraorder in Heteroptera, Insecta. We present the first molecular phylogenetic investigation of family relationships of Cimicomorpha, including 46 taxa from 12 of 16 Cimicomorphan families. Three genes, with a total of 3277 bp of sequence data (nuclear 18S rDNA: 2022 bp, 28S rDNA: 755 bp, and mitochondrial 16S rDNA: 498 bp) were analyzed. Data partitions were analyzed separately and in combination, by employing ML (maximum likelihood), MP (maximum parsimony), and Bayesian methods. As saturation was detected in substitutions of 16S rDNA, influence of data conflict in combined analyses was further explored by three methods: the incongruence length difference (ILD) test, the partitioned Bremer support (PBS), and the partition addition bootstrap alteration approach (PABA). PBS and PABA approaches suggested that 16S rDNA was not very suitable for addressing relationships at this level in Cimicomorpha. Our results also supported the nabid-cimicoid lineage for Cimicoidea proposed by Schuh and Stys [Schuh, R.T., Stys, P., 1991. Phylogenetic analysis of Cimicomorphan family relationships (Heteroptera). J. NY Entomol. Soc. 99 (3), 298-350]. Data incongruence and the utility of the three genes were briefly discussed.