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This lot will be open for bidding soon. You placed the highest bid! How do automatic bids work? Increase your chances of winning The full amount of your automatic bid has now been reached. All the flies observed to be caught in the 5-min sessions were alive. They all spent time cleaning themselves after removal from the fluid at the end of the experiment. This study shows that the fluid of carnivorous species of the genus Nepenthes has retentive properties that differ from those inherent to water. Both the viscoelasticity and the pH of the pitcher fluids are strongly correlated to insect capture.
Insect retention increased with fluid acidity earlier but more gradually in flies than in ants. The way the flies initially touched the fluid influenced their fate, all the more so as the fluid was acidic. Additional experiments in prepared acidic solutions showed an effect of acidity only in situations of insect wetting.
According to their properties, the fluids of Nepenthes species do not trap the same quantity and quality of insect species. These findings raise some important questions. What are the fine mechanisms at the insect—fluid interface that can explain insect trapping and the differences observed between insect categories?
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What are the possible implications for pest control? To what extent are these results relevant for the evolutionary ecology of Nepenthes carnivorous plants? Here the bioassays are shown to be conclusive in the field, using insects found on Nepenthes pitcher plants. It seems clear that C. Moreover, flies bear on their body numerous hairs which, among other functions, may protect them against wetting Perez-Goodwyn, This is at least so for Calliphora flies, which exhibit wide contact angles of water droplets on their hairy cuticle Holdgate, Trapping occurs as soon as the elastic forces created by insect movements have no time to relax.
Thus, an abrupt transition of capture rate with fluid viscoelasticity is expected. This is precisely what is observed, as attested by the sigmoid functions obtained for ants and flies Fig. Interestingly, the capture rate of the ant C. As discussed by Gaume and Forterre , escape of an insect from a viscoelastic fluid depends on how slowly it moves. This is probably the strategy adopted by the N. This slow period of swimming stroke might be the result of coevolution and denotes its adaptation to pitcher life. While insect definitive capture is a positive function of viscoelasticity, there is no significant correlation between time to death and viscoelasticity for the two insect types of this study flies and ants.
Unexpectedly, in species having a viscoelastic fluid, the estimated time to death was found to decrease with fluid age, i. This means that something else should explain rapid death of prey in old, weakly viscoelastic fluids. A conspicuous singularity of old fluids compared with younger fluids is that they are in contact with numerous prey items. It has been reported that secretion of naphtoquinones, known to have cytotoxic effects, is induced by prey in the pitcher of N.
Supporting this idea is our observation that no blue-fly died in the acidic solution during the 5-min experiments carried out in the laboratory. Without being lethal, acidity is revealed to affect insect performance. This result is new and worthy of attention as acidity was not previously suspected to take part in the trapping system of Nepenthes pitcher plants. First, it seems more credible that a cytolytic effect, such as that caused by enzymes, would be measurable over a longer time scale.
Acidity is more likely to trigger a rapid insect response, as observed in this study. Second, acidity is known to negatively influence insect behaviour and survival in freshwater habitats Tabak and Gibbs, ; Brodin and Gransberg, ; Harrison, Last but not least, we experimentally showed the isolated effect of acidity in laboratory experiments on fly retention in wetting situations. This highlights a synergetic effect of acidity and wetting properties of the fluid. In viscoelastic fluids, wetting occurs as soon as the insect begins to move wetting occurs in dynamic not in static situations, Gaume and Forterre According to our results, C.
This might be explained by the better anti-wetting properties of P. This is therefore not a hazard if the ant is associated with N. It is even argued that N. It is thus tempting to consider that for those species, particularly those forming substantial tanks, the primary role of acidity is insect retention.
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Finally, the way the fly initially touches the fluid influences its fate. This orientation effect appears to be significant when it is not concealed by the stronger effects of viscoelasticity. The magnitude of the fall orientation effect on death rate increases with the pH of the fluid. This is observed from our experiments using Nepenthes fluids and secondarily confirmed by our experiments in acidic solutions.
Falling dorsally on its wings reduces the survival chances of a fly, probably because 1 the wings offer a larger contact area and retention points compared with tarsi, and 2 the wings are not as rough as the rest of the insect body, and hence are more easily wetted Holdgate, ; Perez-Goodwyn, This effect may explain the higher capture and death rate of flies than of ants in all of the fluids tested. This observation on the importance of the insect landing position and the results pertaining to pH, wetting and viscoelasticity may help the design of biomimetic traps.
Synthetic pitfalls devoted to the trapping of flying insects could be greatly and easily improved if they also included an acidic substrate and a landing platform. Both the inclination angle and the height of the platform should be optimized and adapted to the insect weight, to make an insect systematically fall upside down on its wings and with a kinetic energy sufficient to cause body immersion. Such physical parameters have been shown to influence the fall orientation of buttered toast, which does not merely follow a binomial law with equiprobability random phenomenon: The viscoelastic properties of the Nepenthes fluid may also serve as a model for the development of insect glues.
Finally, at a larger scale, the development of pesticide or fertilizer sprays that avoid the problem of drop bouncing on plants may be economically and ecologically valuable, as it would prevent the release of large amounts of chemicals that otherwise would have spread with the well-known consequences for soil pollution. The fluid is thus an important part of the complex mechanism of capture in Nepenthes carnivorous pitcher plants, which have long being considered to rely on passive gravity-dependent pitfall traps.
Differences in both acidity and rheology partly explain inter-specific differences in capture strategies. First, it is noteworthy that fluids with trapping physico-chemical properties such as acidity and viscoelasticity characterize only insectivorous species. Species such as N.
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This may explain why its fluid is neither very acidic nor viscoelastic. But why do the young fluids of such Nepenthes species have high degrees of viscoelasticity if a weak viscoelasticity is sufficient to catch flies? Therefore, fluids initially having high concentrations of polysaccharides have a greater chance of circumventing the water-dilution problem. Secondly, the effect of fluid viscoelasticity is more progressive on at least water-resistant ants, which require a greater degree of viscoelasticity than flies to be retained.
As ants are abundant in most tropical forests Davidson and Patrell-Kim, , it is important for the plant to have a weapon that is also widely efficient on this more ubiquitous type of prey. The question remains as to why N. It is possible that this viscoelastic fluid is a remnant character from a common ancestry with the sister species, N. A second hypothesis is that insects are a more reliable food resource than bat faeces to N.
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Moreover, our unique observation that the orientation with which a fly lands on acidic fluids determines its fate leads to several novel questions as to how the structural associations of nectar glands, curved teeth and pitcher rim may manipulate the feeding position of an insect and its probability of being trapped. This provides a basis for the design of bio-inspired traps. We are deeply grateful to Hadzid, Ieney, Fina and the whole Hadzid family for their kind hospitality at Telamba homestay in Brunei.
The Brunei Forestry Department allowed us to carry out research in the forest. Zulhilmi Ab is acknowledged for his field assistance. Two anonymous reviewers are thanked for their helpful comments. National Center for Biotechnology Information , U. Journal List Ann Bot v. Published online Feb Author information Article notes Copyright and License information Disclaimer. For Permissions, please email: This article has been cited by other articles in PMC.
Acidity, ant capture, carnivorous plant, digestive fluid, fly capture, insect capture, Nepenthes , pest control, pitcher plant, viscoelasticity. Studied insect species Prior trial experiments revealed that most ant workers [a terrestrial black Crematogaster sp. Laboratory fly bioassays in pH-controlled solutions The isolated effect of fluid acidity on trapping efficiency was tested in the laboratory on the blue fly Calliphora vomitoria only because it was the easiest of the two ubiquitous flies to manipulate and because we did not have access to the ants used in the field. Statistical analyses Data were analysed using R version 2.
Open in a separate window. Plant and insect parameters affecting fluid retention. B Parameter estimates least square means z Value P Estimate s. Fluid and insect parameters affecting retention rates. Insect survival probability or killing ability of the plant Results of the model that best explained the variance for fly death and that minimized discordance between observed and predicted fly fates are given in Table 3 A. Isolated effect of acidity on flies Eleven of the 26 flies promptly immersed in the acidic solution were observed to be caught at the end of the 5-min observation sessions versus only four of the 26 flies promptly immersed in water.
Mechanisms at the insect—fluid interface in Nepenthes pitcher plants: Traps of carnivorous pitcher plants as a habitat: Annals of Botany Patterns of prey capture and prey availability among populations of the carnivorous plant Pinguicula moranensis Lentibulariaceae along an environmental gradient. American Journal of Botany Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. Effect of pitcher age on trapping efficiency and natural prey capture in carnivorous Nepenthes rafflesiana plants.
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Evidence for alternative trapping strategies in two forms of the pitcher plant, Nepenthes rafflesiana. Journal of Experimental Botany A carnivorous plant fed by its ant symbiont: Controlling droplet deposition with polymer additives. Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Ants swimming in pitcher plants: The language you choose must correspond to the language of the term you have entered. In which subject field? Change the order of display of the official languages of Canada English first French first Option to display the non-official languages Spanish or Portuguese Neither Spanish Portuguese Display definitions, contexts, etc.
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