Mechanoecology: biomechanical aspects of insect-plant interactions

Abstract

Plants and herbivorous insects as well as their natural enemies, such as predatory and parasitoid insects, are united by intricate relationships. During the long period of co-evolution with insects, plants developed a wide diversity of features to defence against herbivores and to attract pollinators and herbivores' natural enemies. The chemical basis of insect-plant interactions is established and many examples are studied, where feeding and oviposition site selection of phytophagous insects are dependent on the plant's secondary chemistry. However, often overlooked mechanical interactions between insects and plants can be rather crucial. In the context of mechanoecology, the evolution of plant surfaces and insect adhesive pads is an interesting example of competition between insect attachment systems and plant anti-attachment surfaces. The present review is focused on mechanical insect-plant interactions of some important pest species, such as the polyphagous Southern Green Stinkbug Nezara viridula and two frugivorous pest species, the polyphagous Mediterranean fruit fly Ceratitis capitata and the monophagous olive fruit fly Bactrocera oleae. Their ability to attach to plant surfaces characterised by different features such as waxes and trichomes is discussed. Some attention is paid also to Coccinellidae, whose interaction with plant leaf surfaces is substantial across all developmental stages in both phytophagous and predatory species that feed on herbivorous insects. Finally, the role of different kinds of anti-adhesive nanomaterials is discussed. They can reduce the attachment ability of insect pests to natural and artificial surfaces, potentially representing environmental friendly alternative methods to reduce insect pest impact in agriculture.

Keywords: Adhesion; Adhesive pad; Biomechanics; Ecology; Epicuticular wax; Friction; Insects; Plants; Surface.

Fig. 1

Tarsus of Nezara viridula in cryo-scanning electron microscopy (a, b), transmission electron microscopy (c), confocal laser scanning microscopy (d) and schematic reconstruction of the tarsal gland of Coreus marginatus (e). a, Ventro-lateral view of the three tarsal segments (I–III) and the pretarsus with pulvilli (P) and claws (C). Note the hairy pad (HP) on the basitarsus and the two paraempodia (arrows). TC, tibial comb complex used for antennal grooming. b, Ventral view of the pretarsus showing the smooth ventral surface of pulvilli (P) and the two curved claws (C). c, Detail of the ventral cuticle of the pulvillus in its distal portion showing the cuticular rods (RD) branching into thinner fibres towards the pad surface (arrow) and oriented at an angle of 40° to the surface plane. d, Lateral view of the pretarsus showing pulvilli (P) and claws (C). Differences in the autofluorescence composition of the exoskeleton structures reveal different chemical composition of the cuticle. Red colour indicates chitinous and strongly sclerotised exoskeleton structures, green colour indicates chitinous and non- or weakly-sclerotised exoskeleton structures, and blue colour indicates exoskeleton structures with large proportions of the very elastic and soft protein resilin. e, Schematic reconstruction of the tarsal gland. The third tarsomere is cut longitudinally and transversally. C, claws; G, gland; UT, unguitractor tendon. Note the gland lumen (GL) in connection with the pulvillus lumen (PL). b, c, and d, Modified from Rebora et al. (2018). e modified from Rebora et al. (2021)

Fig. 2

Pretarsal attachment devices of the female of Ceratitis capitata (a, b) and Bactrocera oleae (c, d) in cryo-scanning electron microscopy. a, Dorsal view of hairy pulvilli (P) and curved claws (C). b, Detail of the ventral view of a pulvillus showing the tenent setae with the terminal plate (TP). c, Dorsal view of hairy pulvilli (P) and curved claws (C). d, Detail of the tenent setae constituted of a setal shaft (SH) and a circular terminal plate (TP). a and b, Modified from Salerno et al. (2020a). c and d,  Modified from Rebora et al. (2020b)

Fig. 3

Tarsi of the female (a, b) and larva (c, d) of Chnootriba elaterii in cryo-scanning electron microscopy. a, Hairy pads (HP) covered with numerous tenent setae located on the ventral side of the first (I) and second (II) tarsal segments. C, claws. b, Frontal view of the bifid claws with a basal tooth (asterisk). Note the deep clefts (arrows). c, Single pretarsal claw (C) and tarsal tenent setae (arrowheads) located on the tarsus (T). d, Detail of the pygopodium (P) at the end of the abdomen. Modified from Saitta et al. (2022)

Fig. 4

Leaf surface of Prunus avium (a), Syringa vulgaris (b), Solanum melongena (c), Phaseolus vulgaris (d) and fruit surface of Prunus domestica (e) and Olea europaea (f) in cryo-scanning electron microscopy. a, Abaxial leaf surface showing cuticular folds. b, Adaxial leaf surface showing cuticular folds running between neighboring cells. c, Adaxial leaf surface showing non-glandular branched trichomes. d, Adaxial leaf surface showing hooked non-glandular trichomes. e, Fruit surface characterized by a dense and regular 3D epicuticular wax coverage composed of numerous, very short, thin-walled tubules. f, Epicuticular wax coverage composed of platelets having irregular sinuate margins and protruding from the surface at different angles. a, Modified from Salerno et al. (2017). b), c, d, Modified from Salerno et al. (2018b). e, Modified from Salerno et al. (2020b). f, Modified from Rebora et al. (2020b)

Fig. 5

Egg adhesion (a) of two ladybird species to plant leaves characterized by different morphological features visible in cryo-scanning electron microscopy (b-e). a, Note that the higher reduction in adhesive strength is recorded on surfaces bearing waxes (Brassica oleracea) or trichomes (Solanum melongena). b, c, Egg interaction with the wax projections of B. oleracea. Note that the glue (G) adheres to the waxes (W), but these last detach easily from the leaf surface (arrow) leaving egg glue prints (arrow head) on the leaf. d, Egg interaction with the big stellate trichomes of S. melongena, which did not allow the egg glue (G) to reach the leaf surface. e, Egg interaction with the leaf of Rosa hybrida. The egg glue adheres well to the leaf surface, thus replicating the leaf topography. Modified from Salerno et al. (2022)

Fig. 6

Anti-adhesive nanoparticles (a, c, e) and tarsal attachment devices of Nezara viridula after walking on treated hydrophilic glass (b, d,f) in cryo-scanning electron microscopy. a, Hexagonal- or pseudo-hexagonal-shaped, horizontally placed plates of kaolin particle film. b, Kaolin powder plates (arrows) accumulated among the adhesive setae of the basitarsal hairy pad. c, Plates of zeolite with variable shapes and dimensions forming groups oriented at different angles to the surface. d, Zeolite particles (arrows) strictly adhering to the adhesive setae. e, Biogenic zinc oxide nanoparticles (ZnO-NPs). f, Ventral side of the tarsal attachment devices of N. viridula just after insects walked on glass treated with biogenic ZnO-NPs (visualized with SEM, backscattered electrons). Note the white zinc oxide nanoparticles (arrows)