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1. Beneficial ‘services’ in mutualistic interactions have often not evolved de novo , but from ancestral traits that had a function before the emergence of the association. These traits can then acquire novel functions in a mutualism. Even in many close insect–plant relationships, the services provided by each partner are still unclear.
2. In the w...
Context in source publication
Context 1
... association between the Bornean pitcher plant, Nepenthes bicalcarata Hook f., and the ant, Camponotus schmitzi Sta¨rkeSta¨rke (Fig. 1), is a very special case in this context, because it is both a carnivorous plant and an ant-plant (Beccari 1904). Like other Nepenthes pitcher plants, N. bicalcarata possesses specialised leaves to attract, capture, retain and digest arthropod prey. At the same time, however, its pitcher tendrils are swollen and hollow, providing ...
Citations
... Because ants mechanically remove microbes and secrete antibiotic substances from several glands (Offenberg & Damgaard, 2019), the effects of ants on plant pathogens have been suggested to be potentially high (Offenberg & Damgaard, 2019). Several studies have shown that ants regulate plant pathogens; most of these studies use myrmecophytes (Belin-Depoux et al., 1997;Heil et al., 1999Heil et al., , 2001Letourneau, 1998;Roux et al., 2011;Thornham et al., 2012). ...
... Antibiotics and the cleaning removal behavior of the ants, which have been reported as mechanisms that affect microorganisms (Offenberg & Damgaard, 2019), are likely to play a significant role in shaping fungal community composition. To the best of our knowledge, this is the first study to show the effect of ants on the phyllosphere fungal community composition based on robust quantitative evi- , 2001Letourneau, 1998;Peng & Christian, 2005Roux et al., 2011;Thornham et al., 2012). Another study showed a reduction in the abundance of phyllosphere fungi by cultivation but did not assess community composition (González-Teuber & Heil, 2010). ...
... Considering many studies that have shown that ants reduce specific plant pathogens, Fusarium verticillioides (formerly Fusarium moniliforme) (Belin-Depoux et al., 1997;Roux et al., 2011), Pestalotia sp. (de la Fuente & Marquis, 1999, Elsinoe mangiferae (Peng & Christian, 2005) and unidentified plant pathogens (González-Teuber et al., 2014;González-Teuber & Heil, 2010;Heil et al., 1999Heil et al., , 2001Letourneau, 1998;Peng & Christian, 2013;Thornham et al., 2012), ants probably affect each fungal species differently even within the same functional guild. ...
Many microorganisms inhabit the aboveground parts of plants (i.e. the phyllosphere), which mainly comprise leaves. Understanding the structure of phyllosphere microbial communities and their drivers is important because they influence host plant fitness and ecosystem functions. Despite the high prevalence of ant–plant associations, few studies have used quantitative community data to investigate the effects of ants on phyllosphere microbial communities. In the present study, we investigated the effects of ants on the phyllosphere fungal communities of Mallotus japonicus using high‐throughput sequencing. Mallotus japonicus is a myrmecophilous plants that bears extrafloral nectaries, attracting several ant species, but does not provide specific ant species with nest sites like myrmecophytes do. We experimentally excluded ants with sticky resins from the target plants and collected leaf discs to extract fungal DNA. The ribosomal DNA internal transcribed spacer 1 (ITS1) regions of the phyllosphere fungi were amplified and sequenced to obtain fungal community data. Our results showed that the exclusion of ants changed the phyllosphere fungal community composition; however, the effect of ants on OTU richness was not clear. These results indicate that ants can change the community of phyllosphere fungi, even if the plant is not a myrmecophyte.
... 9,10 In addition to pest control, ants provide several other ecosystem services such as enhancing soil quality and nutrient availability, host-plant leaf nutrient uptake 11 and sometimes serving as pollinators. 10,12 Furthermore, ants also reduce plant pathogens by either eating fungal spores 13 or excreting antibiotics onto the plant when walking. 14,15 However, ants also have negative effects because they engage in trophobiotic mutualisms with harmful sap-sucking homopterans. ...
BACKGROUND
Wood ants are promising biocontrol agents in fruit plantations because they prey on pest insects and inhibit plant diseases. However, these ants also attend plant‐feeding homopterans to harvest their honeydew secretions, thereby increasing their numbers. This problem can be solved by offering ants alternative sugar sources that are more attractive than honeydew. From natural interactions, it is known that some species manipulate mutualistic partners toward loyalty by adding alkaloids to the food they offer their mutualists. Inspired by this, the addition of alkaloids might be used to make ants loyal to artificial sugar feeders and thus used to reduce populations of ant‐farmed homopterans in ant‐mediated biological control. We aimed to explore whether wood ants (Formica polyctena) would develop a taste preference for morphine‐containing sugar solutions in two‐choice laboratory tests.
RESULTS
After having fed on a morphine/sugar solution for 1 week, ants showed a significant preference for morphine solutions compared with equal concentration sugar solutions without morphine. Furthermore, ants lost this preference after 6–9 days on a morphine‐free diet.
CONCLUSION
The results show that wood ants react to morphine in their food, enabling chemical manipulation of their behavior, most likely through a taste preference. Thus, ants are susceptible to manipulation by mutualistic partners in natural interactions and furthermore may be manipulated artificially in biocontrol programs to avoid ant‐mediated build‐up of homopteran populations. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
... The emergence of pitcher traps has likely facilitated the diversification in Nepenthes and Sarraceniaceae by allowing them to adapt to new ecological niches, resulting in dramatic morphological variations in pitcher traps (Pavlovič, 2012;Clarke et al., 2018;Thorogood et al., 2018). Many Nepenthes species have diversified and further modified their pitcher traps to specialize in novel symbiotic relationships (e.g., antmutualism in N. bicalcarata Hook.f.) or novel nutrient acquisition strategies (e.g., detritus-feeding in N. ampullaria Jack, fecal-feeding in N. lowii Hook.f., and subterraneanfeeding in N. pudica Dančák & Majeský) (Moran et al., 2012;Thornham et al., 2012;Dančák et al., 2022;Gilbert et al., 2022). A similar radiation has occurred across Sarraceniaceae lineages, giving rise to many species with novel trap types (e.g., lobster traps of Darlingtonia californica Torr. ...
Premise
The evolution of carnivorous pitcher traps across multiple angiosperm lineages represents a classic example of morphological convergence. Nevertheless, no comparative study to‐date has examined pitcher evolution from a quantitative morphometric perspective.
Methods
In the present study, we used comparative morphometric approaches to quantify the shape space occupied by Heliamphora pitchers and to trace evolutionary trajectories through this space to examine patterns of divergence and convergence within the genus. We also investigated pitcher development, and, how the packing of pitchers is affected by crowding, a common condition in their natural environments.
Results
Our results showed that Heliamphora pitchers have diverged along three main axes in morphospace: (1) pitcher curvature; (2) nectar spoon elaboration; and (3) pitcher stoutness. Both curvature and stoutness are correlated with pitcher size, suggesting structural constraints in pitcher morphological evolution. Among the four traits (curvature, spoon elaboration, stoutness, and size), all but curvature lacked phylogenetic signal and showed marked convergence across the phylogeny. We also observed tighter packing of pitchers in crowded conditions, and this effect was most pronounced in curved, slender pitchers.
Conclusions
Overall, our study demonstrates that diversification and convergent evolution of carnivory‐related traits extends to finer evolutionary timescales, reinforcing the notion that ecological specialization may not necessarily be an evolutionary dead end.
... ant-mutualism in N. bicalcarata) or novel nutrient acquisition strategies (e.g. detritus-feeding in N. ampullaria, fecal-feeding in N. lowii, and subterranean-feeding in N. pudica) (Thornham et al. 2012;Moran et al. 2012;Gilbert et al. 2022;Dančák et al. 2022). A similar radiation has occurred across Sarraceniaceae lineages, giving rise to many species with novel trap types (e.g. ...
The evolution of carnivorous pitcher traps across multiple angiosperm lineages represents a classic example of morphological convergence. Nevertheless, no comparative study to-date has examined pitcher evolution from a quantitative morphometric perspective. In the present study, we used comparative morphometric approaches to quantify the shape space occupied by Heliamphora pitchers and to trace evolutionary trajectories through this space to examine patterns of divergence and convergence within the genus. We also investigated pitcher development, and in particular, how the packing of pitchers is affected by crowding, a common condition in their natural environments. Our results showed that Heliamphora pitchers have diverged along three main axes in morphospace: pitcher curvature, nectar spoon elaboration, and pitcher stoutness. Both curvature and stoutness were correlated with pitcher size, suggesting structural constraints in pitcher morphological evolution. Among these four traits (curvature, spoon elaboration, stoutness and size), all but curvature lacked phylogenetic and showed marked convergence across the phylogeny. We also observed tighter packing of pitchers in crowded conditions, and this effect was most pronounced in curved, slender pitchers. Overall, our study demonstrates that diversification and convergent evolution of carnivory-related traits extends to finer evolutionary timescales, reinforcing the notion that ecological specialization may not necessarily be an evolutionary dead end.
... This is further facilitated by a cleaning behavior of the ants. In this process, they remove everything such as particles and hyphae from the peristome to keep it as slippery as possible (Thornham et al. 2012). Finally, the ants remove the caught insects and feed on them before they dropped the remaining uneaten pieces back into the pitcher (Bonhomme et al. 2011). ...
Carnivorous plants reverse the order we expect in nature: here, animals do not feed on plants, but plants hunt and feed on animal prey, primarily insects, thereby enabling these plants to survive in nutrient-poor environments. In addition to this strategy, some carnivorous plants also form unique symbiotic relationships with animals other than insects to access nutrients. Other important interactions of carnivorous plants with insects, such as pollinators and herbivores, have received far less attention or have been largely neglected. This review describes and summarizes various ecologically relevant biotic interactions between carnivorous plants and other organisms reported in recent studies. In particular, our understanding on how carnivorous plants, for example, handle the pollinator–prey-conflict or interact with and respond to herbivores is still incomplete. Strategies and mechanisms on how carnivorous plants address these challenges are presented. Finally, future directions in carnivorous plant research are proposed.
... grown in Bukit Setiam Forest, Malaysia, 58.82% belonged to the order Hymenoptera (primarily ant species) and 15.78% belonged to the order Diptera (15.87%). Some studies have also demonstrated that selected ant species inhabit the outside of pitcher plants (Bazile et al. 2012;Grafe & Kohout 2013;Thornham et al. 2012). Therefore, we chose ants and blowfly larvae for our research, the largest quantities of which were found in the pitchers. ...
The aim of this study was to determine if feeding Hooker’s pitcher (Nepenthes × hookeriana) with blowfly larvae (Calliphora vicina Rob-Desvoidy) or ants (Formica fusca L.) affected the plant’s biometric and biochemical parameters. The research included measurements of length and width of the laminae and pitchers, and the total contents of the ash, assimilation pigments, polyphenols, and flavonoids. These parameters were measured 30 days after the last feeding. This study demonstrated that feeding the plants with blowfly larvae resulted in increases in the lengths and widths of both the laminae and pitchers. Moreover, the laminae had reduced carotenoid content after feeding with blowfly larvae and ants whereas the pitchers of Hooker’s pitcher had increased chlorophyll and carotenoid content after feeding with blowfly larvae. Feeding Hooker’s pitcher plants with blowfly larvae also resulted in a reduction of the total polyphenol content in the laminae whereas the total flavonoid content increased in both the laminae and pitchers of Hooker’s pitcher. Feeding Nepenthes × hookeriana with insects ensures that their nutritional needs are met and leads to pitchers with good physiological condition.
... Second, even if these wax layers could be rendered less hydrophobic, the high surface energy required to achieve full wetting based on chemistry alone would likely attract contaminating particles and chemicals. Particle contamination strongly reduces the trapping efficiency of the peristome [50] , and, as we demonstrated above, roughness can relax the conditions posed on surface chemistry considerably, in turn reducing the propensity for contamination. Combining a cuticle with moderate wettability with microscopic roughness may hence serve to maintain the peristome functional over prolonged periods of time (to the best of our knowledge, there is no evidence that Nepenthes pitcher plants make use of surfactants to wet the peristome [17] , as reported for saponines in Ruellia devosiana [16] ). ...
Nepenthes pitcher plants capture prey with leaves specialised as pitfall traps. Insects are trapped when they ‘aquaplane’ on the pitcher rim (peristome), a surface structured with macroscopic and microscopic radial ridges. What is the functional significance of this hierarchical surface topography? Here, we use insect pad friction measurements, photolithography, wetting experiments and physical modelling to demonstrate that the ridges enhance the trap's efficacy by satisfying two functional demands on prey capture: Macroscopic ridges restrict lateral but enhance radial spreading of water, thereby creating continuous slippery tracks which facilitate prey capture when little water is present. Microscopic ridges, in turn, ensure that the water film between insect pad and peristome remains stable, causing insects to aquaplane. In combination, the hierarchical ridge structure hence renders the peristome wettable, and water films continuous, so avoiding the need for a strongly hydrophilic surface chemistry, which would compromise resistance to desiccation and attract detrimental contamination.
... Second, even if these wax layers could be rendered less hydrophobic, the high surface energy required to achieve full wetting based on chemistry alone would likely attract contaminating particles and chemicals. Particle contamination strongly reduces the trapping efficiency of the peristome [50], and, as we demonstrated above, roughness can relax the conditions posed on surface chemistry considerably, in turn reducing the propensity for contamination. Combining a cuticle with moderate wettability with microscopic roughness may hence serve to maintain the peristome functional over prolonged periods of time (to the best of our knowledge, there is no evidence that Nepenthes pitcher plants make use of surfactants to wet the peristome [17], as reported for saponines in Ruellia devosiana [16]). ...
Nepenthes pitcher plants capture prey with leaves specialised as pitfall traps. Insects are trapped when they ‘aquaplane’ on the pitcher rim (peristome), a surface structured with macroscopic and microscopic radial ridges. What is the functional significance of this hierarchical surface topography? Here, we use insect pad friction measurements, photolithography, wetting experiments and physical modelling to demonstrate that the ridges enhance the traps’ efficacy by satisfying two functional demands on prey capture: Macroscopic ridges restrict lateral but enhance radial spreading of water, thereby creating continuous slippery tracks which facilitate prey capture when little water is present. Microscopic ridges, in turn, ensure that the water film between insect pad and peristome remains stable, causing insects to aquaplane. In combination, the hierarchical ridge structure hence renders the peristome wettable, and water films continuous, so avoiding the need for a strongly hydrophilic surface chemistry, which would compromise resistance to desiccation and attract detrimental contamination.
... Nepenthes plants have evolved pitchers growing from the tips of their conspicuous leaves to efficiently capture insects (Ellison & Gotelli 2009, 2001, which provide almost the entire nutrients required to survive in the infertile habitats (Bonn & Federle 2004;Juniper & Burras 1962;Moran 1996;Moran et al. 1999;Thornham et al. 2012). Considering the observable difference in macromorphology and microstructure, the pitchers can be typically distinguished by four parts: A leaf-shaped lid, a collar-formed peristome, a slippery zone and a digestive zone (Benz et al. 2012;Gaume & Giusto 2009;Gaume et al. 2002;Moran & Clarke 2010;Page & Lennon 1999). ...
... Symbiotic associations between (predominantly) terrestrial animals and pitcher plants are much less common. Among the better known is the association of Colobopsis schmitzi ants with the myrmecophyte ("ant plant") Nepenthes bicalcarata, where the plant provides food and shelter for the ants (Clarke & Kitching, 1995) which, in turn, defend the plant against herbivores (Merbach et al., 2007) and keep the trapping surfaces clean and slippery (Thornham, Smith, Grafe, & Federle, 2012). Remarkably, the ants are able to safely navigate the slippery surfaces and even swim and dive in the digestive liquid to forage for freshly captured prey (Bohn, Thornham, & Federle, 2012). ...
Pitcher plants are flagship species for conservation and nature education alike. The diversity of interactions with animals beyond the plants' prey in particular captures people's imagination and ignites their interest and love for the natural world. Here we present observations and experimental data on the biology and behaviour of the pitcher‐inhabiting crab spider, Misumenops nepenthicola.
