Figure 1 - uploaded by Kazuki Tagawa
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(A) Larva of Buckleria paludum licking mucilage secreted from glands on a trap leaf of a carnivorous Drosera rotundifolia. (B) Glandular hairs of D. rotundifolia bending in response to B. paludum feeding on the leaf blade. Photography: Kazuki Tagawa.
Source publication
Caterpillars of Buckleria spp. (Lepidoptera: Pterophoridae) have a unique feeding habit of eating trap leaves of carnivorous sundew plants (Drosera spp.). We observed the foraging behavior of Buckleria paludum on trap leaves of Drosera spp. and discussed how the moth species avoided being caught by trap leaves. In 81.5% (66/81) of encounters with g...
Contexts in source publication
Context 1
... June 2019, we observed the behavior of last instar B. paludum larvae on trap leaves of D. spatulata growing in a humid cliff located on a forest edge (Okinawa Island, Okinawa Prefecture, Japan). Buckleria paludum larvae only licked the mucilage secreted from glandular knobs without eating hairs and crawled on the processed hairs (Fig. 1A, Video S1). This behavior was not observed for B. parvulus in pioneer studies of Eisner and coworkers (Eisner & Shepherd 1965;Eisner 2005), and the adaptive significance of the behavior was unknown. We hypothesized that the last instar B. paludum larvae were able to prevent being captured by the traps, through this behavioral adaptation, and we ...
Context 2
... encounters they chewed bases of the glandular hairs without eating them. When B. paludum larvae licked mucilage, the glandular hairs on the trap leaf with B. paludum did not bend. However, when the larvae chewed the bases of glandular hairs or ate the leaf blades from the abaxial surface, the glandular hairs on both the trap leaf with B. paludum (Fig. 1B) and other leaves in the Drosera individual ...
Citations
... Buckleria spp. are specialist herbivores of Drosera that can safely eat Drosera traps by licking the mucilage (Osaki & Tagawa, 2020). Although feeding damage by Buckleria has been observed in both D. indica in Thailand and D. toyoakensis in Japan (Tagawa, personal observation), the intensity of feeding damage in each population has not yet been investigated. ...
Certain carnivorous plant species display geographical variation in trap coloration, which may impact interactions with prey. Our study focused on Drosera indica (Droseraceae) in tropical Thailand and its phylogenetically related species Drosera toyoakensis in temperate Japan. Drosera indica in Thailand has green leaf blades with red tentacles when flowering, making the entire trap appear red. In contrast, D. toyoakensis in Japan has green leaf blades with green‐white tentacles when flowering, and the entire trap appears white. Field observations revealed statistically significant differences in taxa and size of prey caught by D. indica and D. toyoakensis . Both species caught small flies, but D. toyoakensis additionally caught larger flies and butterflies, including pollinators. These differences in prey composition may reflect differences in trap coloration that evolved under different selection pressures for capturing prey. However, trap coloration and prey assemblages were influenced by various factors, and further research is required to elucidate their evolutionary significance.
... We hypothesized that the rapid flower closure of D. tokaiensis in response to mechanical stimulation might function as an induced physical defence against flower eating by the specialist herbivore Buckleria paludum (Pterophoridae). The larvae of B. paludum feed on the flowers, fruits and leaves of Drosera [5]. In some habitats in Japan, up to 40% of D. tokaiensis fruits were damaged by B. paludum [6]. ...
Certain plants exhibit rapid movement in response to mechanical stimulation; however, the ecological functions of this behaviour are largely unknown. Here, we show that the rapid flower closure of Drosera tokaiensis (Droseraceae) in response to mechanical stimulation functions as a physical defence against a specialist herbivore Buckleria paludum (Pterophoridae) caterpillar. Following feeding damage on fruits, flowers, flower stalks and buds by B. paludum , D. tokaiensis closed its flowers nine times faster than during natural circadian closure. The extent of damage to ovules was significantly reduced when the flowers were able to close compared with the condition in which closure was physically inhibited by the application of a resin. Nonetheless, flower closure had no effect on the feeding damage to stamens and styles and promoted further damage to petals. Given that feeding on petals, stamens and styles had no significant effect on the number of mature seeds, rapid flower closure leading to the protection of ovules had an overall positive effect on the reproductive success of D. tokaiensis . Our study showed rapid plant movement as a novel case of induced physical defence against herbivory.
... These symbiotic arthropods require particular biomechanical adaptations to overcome the adhesive forces of these sticky glands and maintain mobility (Voigt and Gorb, 2010). Caterpillars (Fletcher, 1908;Osaki and Tagawa, 2020) and a hoverfly larva (Fleischmann et al., 2016) have also evolved behavioral and physical adaptations to overcome mucilage adhesion to consume the leaves and tentacles or entrapped prey of Drosera. Almost nothing is known about the effects of viscoelastic fluid on the aquatic symbionts living in Nepenthes pitchers, but one study (Gilbert et al., 2020) revealed little difference in the microbial community composition between species with and without sticky fluid in a greenhouse setting. ...
To survive in nutrient-poor habitats, carnivorous plants capture small organisms comprising complex substances not suitable for immediate reuse. The traps of carnivorous plants, which are analogous to the digestive systems of animals, are equipped with mechanisms for the breakdown and absorption of nutrients. Such capabilities have been acquired convergently over the past tens of millions of years in multiple angiosperm lineages by modifying plant-specific organs including leaves. The epidermis of carnivorous trap leaves bears groups of specialized cells called glands, which acquire substances from their prey via digestion and absorption. The digestive glands of carnivorous plants secrete mucilage, pitcher fluids, acids, and proteins, including digestive enzymes. The same (or morphologically distinct) glands then absorb the released compounds via various membrane transport proteins or endocytosis. Thus, these glands function in a manner similar to animal cells that are physiologically important in the digestive system, such as the parietal cells of the stomach and intestinal epithelial cells. Yet, carnivorous plants are equipped with strategies that deal with or incorporate plant-specific features, such as cell walls, epidermal cuticles, and phytohormones. In this review, we provide a systematic perspective on the digestive and absorptive capacity of convergently evolved carnivorous plants, with an emphasis on the forms and functions of glands.
... The genus Pinguicula could be an exception due to its rosettelike growth habit and the general presence of sticky trichomes. In different Drosera species, sundew plume moth larvae (Buckleria paludum) were described to live and develop on the carnivorous plants, feeding on the sticky tentacles, leaf blade, flowers, and fruits or only licking the secreted mucilage (Eisner and Shepherd 1965;Osaki and Tagawa 2020). In particular, last instar larvae showed the licking behavior, very likely to remove sticky mucilage in order to escape the possibility of being captured (Osaki and Tagawa 2020). ...
... In different Drosera species, sundew plume moth larvae (Buckleria paludum) were described to live and develop on the carnivorous plants, feeding on the sticky tentacles, leaf blade, flowers, and fruits or only licking the secreted mucilage (Eisner and Shepherd 1965;Osaki and Tagawa 2020). In particular, last instar larvae showed the licking behavior, very likely to remove sticky mucilage in order to escape the possibility of being captured (Osaki and Tagawa 2020). No defensive plant reaction in any of these interactions have been described so far. ...
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.
... Plants in nutrient-poor environments often have slow growth rates (Grime 1977), and as a result may experience a higher relative cost of herbivory (Coley et al. 1985). Foliar herbivory has been studied in several carnivorous plant species (Atwater et al. 2006;Bauer et al. 2016;Gilbert et al. 2018;Lamb and Kalies 2020;Osaki and Tagawa 2020), but studies of florivory in carnivorous plants are rare. The purpose of this study was to investigate florivory on the carnivorous plant Sarracenia alata by the specialist herbivore Exyra semicrocea. ...
Losses of floral tissues to herbivory (florivory) can affect plant reproduction, population growth and structure, and community dynamics. Because carnivorous plants inhabit nutrient-poor environments and exhibit slow growth rates, losses to herbivory may be particularly costly. However, there has been no published study of florivory in carnivorous plants. We conducted a 2-year field study in Leon County, Texas USA, on the carnivorous Pale Pitcher Plant Sarracenia alata and its specialist herbivore Exyra semicrocea. We surveyed the proportions of flowers attacked and compared the mass of floral components (ovaries, anthers, petals, sepals, and style) between attacked and undamaged flowers. In 2017, a mean of 53% of flowers was attacked. The anther count and the masses of anthers, perianth (petals + sepals), and style were significantly lower in attacked flowers than in undamaged flowers, but ovary mass was not significantly affected. The total flower dry mass (without peduncle) of attacked flowers on the last collection date was 13.3% less than that of undamaged flowers, but this difference was not statistically significant. In 2018, a mean of 33% of flowers were attacked, with significant mass losses from all floral components, including ovaries. The total flower dry mass (without peduncle) of attacked flowers on the last collection date was significantly (48%) less than that of undamaged flowers. Herbivore population size, differences in emergence phenology of the host and/or herbivore, and differential defense of components may have contributed to differences between years in the proportion of flowers attacked and variation in the floral structures consumed.
The carnivorous habit has been interpreted as an outstanding adaptation that let some plants the acquisition of mineral nutrients in habitats characterized by a chronic scarcity of nutrients. Substantial evidence indicates how carnivorous plants benefit from its interaction with prey. However, fitness of carnivorous plants depends not only on the interaction with their prey but on other interactions such as pollination, herbivory, and kleptobiosis. It is also known that evolutionary ecology of carnivorous plants is regulated by the cost–benefit ratio that is imposed majorly by the abiotic environment limiting photosynthesis. We analyzed how these three little explored interactions in carnivorous plants could promote scenarios rising additional costs to those that are hypothesized to occur linked to the evolution of botanic carnivory. In specific, we (i) explained a general ecological context of each interaction, (ii) reviewed how the interactions increase costs in carnivorous plants, (iii) identified factors that regulate the negative effect on carnivorous plants, and (iv) identified lines for future research.
Carnivorous plants often spark broad interest due to their specialized adaptations for trapping and consuming animals. These notable organisms not only fix carbon through photosynthesis, but they also obtain essential nutrients such as nitrogen and phosphate from their captured prey. In typical angiosperms, interactions with animals are usually confined to such processes as pollination and herbivory, but another layer of complexity in these interactions is added for carnivorous plants. Here, we introduce carnivorous plants and their associated organisms - ranging from their prey to their symbionts - and highlight biotic interactions beyond carnivory to discuss how the 'default' interactions typical for flowering plants have changed in the case of the carnivorous plants (Figure 1).
