The salivary gland and salivary enzymes of the giant waterbugs (Heteroptera; Belostomatidae)

Swart, Charles C.; Deaton, Lewis E.; Felgenhauer, Bruce E.

doi:10.1016/j.cbpa.2006.05.010

Cited by 57 publications

(52 citation statements)

References 36 publications

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“…Immobilization is a prerequisite for the subsequent injection of the saliva into the prey to be digested before ingestion. Previous studies focused on antihemostatic and digestive properties of salivary components of arthropods engaged in Type I EOD (Swart et al, 2006). Here, we have focused on a previously overlooked aspect of major importance in feeding success.…”

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confidence: 99%

Paralytic activity of lysophosphatidylcholine from saliva of the waterbugBelostoma anurum

Silva-Cardoso

Caccin

Magnabosco

et al. 2010

Journal of Experimental Biology

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SUMMARYLysophosphatidylcholine (LPC) is a major bioactive lipid that is enzymatically generated by phospholipase A 2 (PLA 2 ). Previously, we showed that LPC is present in the saliva of the blood-sucking hemipteran Rhodnius prolixus and modulates cell-signaling pathways involved in vascular biology, which aids blood feeding. Here, we show that the saliva of the predator insect Belostoma anurum contains a large number of lipids with LPC accounting for 25% of the total phospholipids. A PLA 2 enzyme likely to be involved in LPC generation was characterized. The activity of this enzyme is 5-fold higher in Belostoma saliva than in other studied hemipterans, suggesting a close association with the predator feeding habits of this insect. Belostoma employs extra-oral digestion, which allows for ingestion of larger prey than itself, including small vertebrates such as amphibians and fish. Therefore, prey immobilization during digestion is essential, and we show here that Belostoma saliva and B. anurum saliva purified LPC have paralytic activity in zebrafish. This is the first evidence that lysophospholipids might play an important role in prey immobilization, in addition to contributing to blood feeding, and might have been an evolutionary acquisition that occurred long before the appearance of hematophagy in this animal group.Key words: Belostoma, extra-oral digestion, lysophosphatidylcholine, paralysis, phospholipase A2, saliva. THE JOURNAL OF EXPERIMENTAL BIOLOGY 33062003), and have described the dual anti-hemostatic activity of LPC that inhibits platelet aggregation and induces NO production in endothelial cells. Belostoma saliva enables different feeding strategies when compared with hematophagous hemipterans from the Reduviidae family. After catching prey, Belostoma inserts its piercing mouthparts to inject saliva and liquefy the prey tissues. Accordingly, Belostoma saliva must contain an array of digestive enzymes. Their saliva is white and viscous, indicating that it may contain an unusual amount of lipids. In the present study, we demonstrate for the first time the presence of lipids and bioactive lysophospholipids in the saliva of a heteropteran predator, B. anurum. We show that these compounds are toxic to neurons in culture, can block neurally evoked twitch contractions, and can paralyze and kill zebrafish (Dario rerio). MATERIALS AND METHODS Belostoma anurum salivaAdult specimens of Belostoma anurum were collected from Picinguaba (São Paulo, Brazil). The belostomatids were kept, under laboratory conditions, in tanks with 200 ml of non-chlorinated tap water and provided with synthetic floats. Aedes aegypti fifth instar larvae and Biomphalaria glabrata served as food. The saliva was obtained from the proboscis by means of electrical stimulation using an isolated pulse stimulator (Model 2100 A-M Systems, Sequim, WA, USA) at the insertion of the first pair of legs to the thorax (50-100V, 3-4Hz, and square pulses of 3ms duration), as previously described (Dan et al., 1993). Lipid analysisSamples of B. anurum s...

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confidence: 99%

Paralytic activity of lysophosphatidylcholine from saliva of the waterbugBelostoma anurum

Silva-Cardoso

Caccin

Magnabosco

et al. 2010

Journal of Experimental Biology

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“…Several authors have compared the capabilities of the available software (Lautenschlager, 2016) and step‐by‐step protocols have been published recently (Abel, Laurini, & Richter, 2012; Fedorov et al., 2012; Smith et al., 2016; Supporting information), but still segmentation remains largely context‐dependent (Swart, Deaton, & Felgenhauer, 2006). …”

Section: Processing Of X‐ray Ct Imagesmentioning

confidence: 99%

X‐ray computed tomography and its potential in ecological research: A review of studies and optimization of specimen preparation

Gutiérrez

Ott

Töpperwien

et al. 2018

Ecology and Evolution

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Imaging techniques are a cornerstone of contemporary biology. Over the last decades, advances in microscale imaging techniques have allowed fascinating new insights into cell and tissue morphology and internal anatomy of organisms across kingdoms. However, most studies so far provided snapshots of given reference taxa, describing organs and tissues under “idealized” conditions. Surprisingly, there is an almost complete lack of studies investigating how an organism′s internal morphology changes in response to environmental drivers. Consequently, ecology as a scientific discipline has so far almost neglected the possibilities arising from modern microscale imaging techniques. Here, we provide an overview of recent developments of X‐ray computed tomography as an affordable, simple method of high spatial resolution, allowing insights into three‐dimensional anatomy both in vivo and ex vivo. We review ecological studies using this technique to investigate the three‐dimensional internal structure of organisms. In addition, we provide practical comparisons between different preparation techniques for maximum contrast and tissue differentiation. In particular, we consider the novel modality of phase contrast by self‐interference of the X‐ray wave behind an object (i.e., phase contrast by free space propagation). Using the cricket Acheta domesticus (L.) as model organism, we found that the combination of FAE fixative and iodine staining provided the best results across different tissues. The drying technique also affected contrast and prevented artifacts in specific cases. Overall, we found that for the interests of ecological studies, X‐ray computed tomography is useful when the tissue or structure of interest has sufficient contrast that allows for an automatic or semiautomatic segmentation. In particular, we show that reconstruction schemes which exploit phase contrast can yield enhanced image quality. Combined with suitable specimen preparation and automated analysis, X‐ray CT can therefore become a promising quantitative 3D imaging technique to study organisms′ responses to environmental drivers, in both ecology and evolution.

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“…They are typically found sitting along the water's edge posing with their front legs below and their abdominal spiracles above the water surface, from where they catch bypassing prey with their raptorial forelegs that are strongly incrassate, with the femora often grooved to accept the tibiae (Menke 1979). Upon capture, belostomatids inject toxins causing prey paralysis and digestive enzymes causing tissue necrosis (Swart and Felgenhauer 2003;Swart et al 2006).…”

Section: Introductionmentioning

confidence: 99%

“…While the large-bodied members of the subfamily Lethocerinae feed on small snakes, anurans, and fish, the much smaller members of the subfamily Belostomatinae mainly feed on various invertebrates and anuran larvae, but do not regularly prey on fish (Cullen 1969;Babbitt and Jordan 1996;Swart and Felgenhauer 2003;Mori and Ohba 2004;Ohba and Nakasuji 2006;Swart et al 2006;Ohba 2011). Prey selection in belostomatines has been thoroughly investigated in the predator-prey relationship between Belostoma cf.…”

Section: Introductionmentioning

confidence: 99%

Characterizing a novel predator–prey relationship between native Diplonychus esakii (Heteroptera: Belostomatidae) and invasive Gambusia affinis (Teleostei: Poeciliidae) in central China

et al. 2017

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A considerable body of the literature considers the potential impact of exotic predators on native prey organisms, while comparatively, few studies have asked whether and how native predators include novel prey types into their diet spectrum. Here, we asked whether the native aquatic heteropteran Diplonychus esakii preys on the highly invasive western mosquitofish (Gambusia affinis), which has been introduced to southern China and threatens native fish species through competition and predation on their fry. We conducted 48-h prey choice experiments under semi-natural conditions. In a 'no-choice' experiment (one predator and one potential prey; n = 200), we found the heteropterans to prey more on large-bodied fish, a pattern that was also described for other belostomatids, while prey sex had no effect on capture rates. Moreover, large-bodied heteropterans caught more fish than small-bodied individuals. However, overall capture rates in our study were low (11.5-30%) compared to studies on other belostomatids, which explains why subsequent binary prey choice experiments using one predator and two prey-either large and small females or male and female (with smaller sample sizes of n = 20 and 30, respectively)-did not confirm the results of our first experiment. Our study exemplifies how a pattern of body size-dependent predation can arise in a novel (not coevolved) predator-prey interaction. We tentatively argue that the observed pattern could be driven by intrinsic features of the predator, namely, altered prey preferences with increasing age coupled with a general preference for large-bodied prey, or changing nutritional needs at different developmental stages.

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The salivary gland and salivary enzymes of the giant waterbugs (Heteroptera; Belostomatidae)

Cited by 57 publications

References 36 publications

Paralytic activity of lysophosphatidylcholine from saliva of the waterbugBelostoma anurum

Paralytic activity of lysophosphatidylcholine from saliva of the waterbugBelostoma anurum

X‐ray computed tomography and its potential in ecological research: A review of studies and optimization of specimen preparation

Characterizing a novel predator–prey relationship between native Diplonychus esakii (Heteroptera: Belostomatidae) and invasive Gambusia affinis (Teleostei: Poeciliidae) in central China

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