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Plant surface–bug interactions: Dicyphus errans stalking along trichomes

Abstract

In contrast to many arthropods whose locomotion on plant surfaces is impeded by trichomes, the omnivorous mirid bug Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae) lives on pubescent plants and preys on a variety of phytophagous arthropods. Morphological (slim body, long slender legs, elongated curved claws) and behavioural (locomotion) adaptations to hairy plant substrates result in higher predation effectiveness and fecundity, as well as a shorter developmental cycle of the bug compared to insects on plants without trichomes. To understand the bug–plant interactions from the biomechanical point of view, the bug’s attachment system and the leaf surfaces of various plant species were analysed. Bug attachment ability was estimated in an inversion experiment on the adaxial and abaxial sides of leaves in 40 plant species. Furthermore, bug traction forces on the abaxial leaf side of 14 plant species were measured. Morphometrical variables of trichomes and the adhesive properties of plant surfaces were estimated. The bugs’ traction force ranged from 0.07 mN on Brassica oleracea (Brassicaceae) to 1.21 mN on Plectranthus ambiguus (Lamiaceae) and Solanum melongena (Solanaceae). Bugs performed considerably better on hairy surfaces where a significant positive correlation between the force and both the trichome length and diameter was found. The trichome density and aspect ratio did not influence the force. Adhesion properties of plant surfaces covered with trichomes may also significantly impede the traction force. Based on the results obtained, it is concluded that hairy plants provide a more suitable environment for D. errans than either smooth ones or those covered with wax crystals. Hairy plant surfaces are predicted to support stronger attachment and therefore more reliable locomotion of the bug.

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Acknowledgements

The first author thanks C. Neinhuis and the staff of the Botanical Garden as well as V. Pohris, M. Müller, and the staff of the Chair for Forest Protection at the Institute of Silviculture and Forest Protection, Faculty of Forestry, Geo and Hydro Sciences, Department of Forestry, Dresden University of Technology (Dresden, Germany) for providing space for the rearing of test plants and insects and for valuable discussions. The bug species were determined by K. Arnold (Geyer, Germany). The German companies Ernst Benary Samenzucht GmbH (Hann/Muenden), Quedlinburger Saatgut GmbH (Quedlinburg), Bruno Nebelung GmbH & Co. (Everswinkel), Cyclamen-Sprünken (Straelen), Eich Jungpflanzen Vertriebs GmbH (Grolsheim), Florensis Deutschland GmbH and Selecta Klemm GmbH & Co. KG (Stuttgart) provided seeds and seedlings. V. Kastner (Max-Planck Institute of Developmental Biology, Tübingen, Germany) helped with the experiments and linguistic corrections of the manuscript, and J. Schuppert (Max-Planck Institute for Metals Research, Stuttgart, Germany) with Cryo-SEM techniques. M. Varenberg (Max-Planck Institute for Metals Research, Stuttgart, Germany) and P. Perez Goodwyn (Graduated School of Agriculture, Kyoto University, Japan) are acknowledged for motivating discussion. The Federal Ministry of Education and Research, Germany (project BIOKON Phase II, 01RS0411) and the German National Academic Foundation (doctoral scholarship, E2002D0730) provided funding for the project.

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Appendix

Appendix

Below we provide a detailed description of the plant surfaces tested, according to the structural types shown in Fig. 4. Names of plant species are arranged alphabetically for quick access.

Aristolochia elegans Mart. (Aristolochiaceae) is covered with transversely ridged wax crystal rodlets, very densely distributed, almost without gaps, on the abaxial leaf side. There, sparsely distributed, inclined unicellular, hook-shaped trichomes are also found (Fig. 5A).

Begonia × semperflorens Link & Otto (Begoniaceae) has a smooth and shiny leaf surface. On the adaxial side, membraneous whole wax platelets are sparsely arranged (Fig. 5C). On the abaxial side, dispersed polygonal wax granules were found (Fig. 5B).

Borago officinalis L. (Boraginaceae) bears a densely hirsute indumentum, consisting of perpendicular and inclined, unicellular, tapered, cone-shaped, and strongly nodose trichomes on both leaf sides (Fig. 6B). Longer trichomes have a convex multicellular base, while shorter ones possess a convex unicellular base. Moreover, dispersed short capitate trichomes (stalked glandular heads) were found (Fig. 6B, see Fig. 4B, S4).

Brassica oleracea L. var. gongylodes L. ‘Gigant’ (Brassicaceae): the pruinouse surface of this plant is densely covered with filamentous wax crystals (polygonal rodlets and threads) (Fig. 5D).

Calendula officinale L. ‘Orangestrahlen’ (Compositae) has different trichomes on both leaf sides: (1) uniseriate, 2- to 10-celled and multiseriate, multicellular capitate trichomes with glandular heads (Fig. 6L), (2) rounded, cone-shaped, multicellular, glandular trichomes without a head, and (3) sparsely dispersed capitate trichomes (stalked glandular heads, see Fig. 4B, S4).

Capsicum annuum L. ‘Yolo Wonder’ (Solanaceae) has a smooth appearing adaxial leaf surface that bears very sparsely dispersed wax crystals, arranged in groups from 3 to 10 platelets (Fig. 5I). Groups of numerous curved, finger-shaped, unicellular trichomes occur in the leaf domatia on the abaxial leaf surface (Fig. 7C).

Cissus njegerre Gilg (Vitaceae), a tropical liana, has a pilose indumentum. On the adaxial leaf side, following trichomes occur: (1) regularly dispersed, bent, uniseriate, 5- to 11-celled ones, (2) perpendicular, 2- to 3-cellular, cone-shaped, nodose trichomes with multicellular convex base, and (3) several dispersed, 1- and 4-celled, peltate trichomes (Fig. 6C). The abaxial leaf surface is covered with regularly dispersed, strongly curved, cone-shaped, uniseriate, 2-celled trichomes with one convex basal cell, as well as with bent, 5- to 11-cellular, nodose trichomes with a multi-cellular convex base, mostly with distally oriented tips (Fig. 6D). The trichomes are more densely concentrated along leaf veins. Moreover, perpendicular 2- to 4-cellular capitate trichomes are scattered all over the leaf lamina. The abaxial leaf surface is also covered with 1- and 4-cellular peltate trichomes.

Cleome hirsuticaulis J. F. Macbr. (Capparidaceae): the leaves have a pilose indumentum, which is most dense along leaf veins and on the abaxial side (Fig. 7A). It consists of dispersed, both inclined and bent, multiseriate, multicellular, cone-shaped glandular trichomes with small glandular heads and a multicellular convex base. Very long and slightly shorter trichomes of this type were found. Multicellular clavate trichomes as well as uniseriate, 3- to 10-cellular trichomes (Fig. 7B) seldom occur.

Cucumis sativus L. ‘Rawa’ (Curcurbitaceae): the hirsute indumentum shows regularly dispersed, perpendicular (or inclined), uniseriate, uni- to 4-cellular, tapered cone-shaped (or dart-shaped) trichomes with a multi-cellular base (Fig. 7E, F). The trichome density is higher on the adaxial leaf side. Trichomes are orientated towards the leaf margin.

Cuphea lanceolata W. T. Aiton (Lythraceae): regularly dispersed, unicellular, spindle-shaped, nodose trichomes were found on the leaf. They are procumbent and located close to the leaf surface (Fig. 6I). Only the trichome tip and the distal half are bent away from the lamina at an angle of approximately 45°. On the abaxial side, trichomes occur more densely along leaf veins and sparsely in the intercostal areas. Besides, long inclined, multiseriate, multicellular trichomes with small glandular heads are scattered on both leaf sides (Fig. 6H).

Curcurbita pepo L. ‘Hokkaido’ (Curcurbitaceae) possesses a dense (adaxial side), and sparse (abaxial side) hirsute pubescence, consisting of regularly dispersed, perpendicular and inclined, uniseriate, 3- to rarely 5-cellular, tapered cone-shaped trichomes with thickened bases, as well as sparse 2-celluar capitate trichomes. Trichomes are most densely concentrated along leaf veins.

Cyclamen persicum Mill. ‘Sierra F1’ (Primulaceae) the leaves bear, on the adaxial side, sparsely distributed, single, entire wax platelets. On the abaxial lamina surface, these can be also clustered in rosettes (Fig. 5K).

Datura innoxia Mill. (Solanaceae) shows a pilose indumentum, composed of dispersed, uniseriate, 3- to 5-cellular, inclined, cone-shaped, nodose and capitate trichomes (Fig. 6A). The adaxial pubescence is denser than the abaxial one.

Digitalis purpurea L. ‘Excelsior’ (Scrophulariaceae) has dispersed, bent, uniseriate, 3- to 5-cellular, nodose, cone-shaped, partially finger-shaped trichomes, distributed very densely along leaf veins (Fig. 7N, O). Sparsely dispersed, inclined capitate trichomes (stalked 2-cellular glandular heads, Fig. 7N) and capitate ones with 4-cellular heads were also found.

Fuchsia × hybrida Hort. ex Vilm ‘Winston Churchill’ (Onagraceae): the adaxial leaf side possesses sparsely dispersed, inclined (on veins also bent), unicellular, thread-like and spiral-shaped, nodose trichomes with a rounded tip and a convex unicellular base. The surface is also covered with individual, entire, crystal wax platelets, often arranged in clusters (Fig. 5H). On the abaxial side, trichomes are inclined, bent and curved, unicellular, cone- and spiral-shaped, and nodose with a convex unicellular base, concentrated along the leaf vein and sparsely dispersed in the intercostal areas (Fig. 7K).

Geranium robertianum L. (Geraniaceae) bears bent, 2- to 4-cellular, capitate, nodose trichomes with a multicellular base as well as sparse, inclined, unicellular, cone-shaped, nodose trichomes on the abaxial leaf side. Capitate trichomes (stalked glandular heads, see Fig. 4B, S4) cover the entire surface. On the abaxial leaf side, dense, curved, unicellular, thread-shaped trichomes as well as inclined 4-cellular, capitate, nodose trichomes were found on the leaf veins. Additionally, stiff cone-shaped, nodose trichomes with a multicellular base and capitate trichomes (stalked glandular heads) are present.

Gerbera jamesonii × hybrida Adlam (Compositae): the adaxial leaf side is covered with sparse, inclined and bent uniseriate 4-cellular thread-shaped trichomes as well as dispersed clusters of membranous crystalline wax platelets. The felt-like indumentum of the abaxial surface along and around the leaf veins consists of inclined, bent, curved, uniseriate, multi-cellular, spiral-shaped, often twisted trichomes with convex unicellular bases (Fig. 7H). Inclined, bent, curved, uniseriate, multicellular, spiral-shaped trichomes as well as occasional, entire crystal wax platelets also appear sparsely in the intercostal areas.

Hibiscus rosa-chinensis L. (Malvaceae) shows the following surface structures on the adaxial leaf surface: (1) inclined and bent, unicellular trichomes on leaf veins, (2) sparsely distributed, 4-cellular peltate trichomes in the intercostal areas as well as wax crystals (clusters of membraneous and entire platelets) (Fig. 5F). On the abaxial side, there are inclined and bent, unicellular trichomes, and 2- to 8-cellular stellate trichomes on the leaf veins (Fig. 6N) as well as sparsely distributed 4-cellular peltate trichomes in the intercostal areas.

Ibicella lutea (Lindl.) Van Eselt. (Martynaceae) is densely covered with the following trichomes: (1) glandular-pubescent, perpendicular and inclined, uniseriate, 3- to 8-cellular, capitate with convex unicellular base, (2) perpendicular, uniseriate, 4-cellular, cone-shaped, (3) perpendicular, 3-cellular, finger-shaped, (4) multicellular clavate, and (5) peltate.

Lactuca sativa L. ‘Attraktion’ (Asteraceae): membraneous wax platelets, arranged as rosettes, are found on the adaxial leaf surface (Fig. 5E). On the abaxial surface there are clusters of irregular wax platelets.

Lagenaria siceria (Mol) Stadley (Curcurbitaceae) exhibits a pilose coverage, consisting of (1) capitate trichomes with an unicellular stem and 4-cellular head, (2) perpendicular and inclined, uniseriate 2- to 5-cellular, dart-shaped, nodose trichomes with thickened basal cell, (3) dispersed 4-cellular peltate trichomes as well as (4) stalked 4-cellular heads (Fig. 6K). Trichomes are located sparsely on the adaxial side and densely on the abaxial surface, and concentrated especially along leaf veins.

Lophospermum erubescens D. Don (Scrophulariaceae): the leaf surface is covered with dispersed perpendicular, 3- to 4-celled, cone-shaped glandular trichomes of different length, with glandular head or with rounded tip, and always with one convex basal cell. Clavate trichomes are regularly dispersed.

Lycopersicon esculentum Mill. ‘Grit’ (Solanaceae) bears regularly dispersed (1) 2-cellular, bent and curved, tapered, cone-shaped, nodose trichomes with convex unicellular bases, (2) inclined and bent, uniseriate, 3- to 5-cellular, cone-shaped, nodose glandular trichomes, (3) sporadic uniseriate, 5- to 12-cellular, cone-shaped trichomes with a multi-cellular base, and (4) capitate trichomes with 4-cellular glandular heads; these are mainly concentrated along leaf veins (Fig. 7L, M).

Malus domestica Borkh. (Rosaceae): the leaf surface appears adaxially smooth with sparsely occurring irregular, membraneous wax platelets arranged in clusters (Fig. 5M), whereas on the abaxial side, a felt-like pubescence was found (Fig. 6S). The inclined and bent unicellular thread-shaped and spiral-shaped, partly twisted trichomes are concentrated along the leaf veins. Besides, sparsely occurring irregular wax crystal platelets arranged in clusters are present on both the trichomes and lamina surface (Fig. 5L).

Nicotiana sylvestris Spegazz. et Gomez (Solanaceae) is covered with (1) dispersed inclined, 2- to 6-cellular, capitate, (2) cone-shaped, glandular trichomes, (3) stalked glandular heads, (4) perpendicular, 2- to 5-cellular finger-shaped trichomes with a convex unicellular base. They all were concentrated along the leaf veins (Fig. 7J).

Ocimum basilicum L. (Lamiaceae): the surface is smooth with some dispersed 1-, 2- and 4-cellular peltate trichomes (Fig. 6M). Cone-shaped, nodose, tapered trichomes are present along the adaxial veins (Fig. 6J).

Oenothera biennis L. (Onagraceae): regularly dispersed, inclined and bent, unicellular, cone-shaped, nodose, tapered trichomes as well as clavate ones were found on the adaxial leaf side (Fig. 6Q, R). The abaxial, felt-like indumentum consists of (1) curved thread-shaped trichomes, (2) dispersed, inclined and bent unicellular cone-shaped tapered nodose trichomes, and (3) densely distributed clavate trichomes.

Pelargonium zonale (L.) L’Hérit. (Geraniaceae): the adaxial lamina side is predominantly covered with regularly dispersed, inclined and bent, unicellular, cone-shaped, tapered trichomes with a slightly thickened base. Inclined, 2- to 4-cellular capitate trichomes with uni- and multicellular bases as well as regularly dispersed, capitate trichomes (stalked glandular heads, Fig. 4B, S4) were also found. The abaxial leaf surface bears mainly (1) regularly dispersed, inclined 2- to 4-cellular capitate trichomes with a uni- and multicellular base, but also (2) regularly dispersed capitate trichomes (stalked glandular heads, see Fig. 4B, S4) as well as (3) irregularly dispersed, inclined and bent, unicellular, cone-shaped, tapered trichomes with slightly thickened bases (Fig. 6G).

Petunia × hybrida Vilm. (Solanaceae): the pilose, glandular indumentum consists of dispersed perpendicular and inclined uniseriate 1- to 3-, rarely 5-cellular capitate trichomes (Fig. 7I).

Plectranthus ambiguus (Bolus) Codd. (Lamiaceae) has a pilose indumentum on both leaf sides with (1) regularly dispersed, inclined and bent, on the veins especially curved, uniseriate, 4- to 15-cellular, cone-shaped, tapered, nodose trichomes with convex multicellular base, (2) dispersed 4-cellular peltate trichomes, (3) capitate trichomes (stalked glandular heads, see Fig. 4B, S4), and (4) sparsely occurring perpendicular 2- to 4-cellular capitate trichomes (Fig. 7D).

Rosa × hybrida L. ‘Bernstein’ (Rosaceae) bears adaxially, sparsely dispersed, irregular wax crystal platelets arranged in small groups (Fig. 5J). On the abaxial leaf side, very sparsely dispersed, irregular wax platelets, and unicellular peltate trichomes are present.

Saintpaulia ionantha Wendl. (Gesneriaceae) possesses a pilose indumentum, consisting of (1) densely dispersed, inclined, bent and curved, uniseriate, 2- to 12-cellular, cone-shaped, tapered trichomes, rarely with small rounded glandular heads, and (2) 1- to 4-cellular peltate trichomes.

Solanum melongena L. ‘Black Beauty’ (Solanaceae): the felt-like hairy coverage exhibits multicellular, stellate nodose trichomes, consisting of 5–9 branches, with the central branch perpendicularly oriented and other branches, arising perpendicularly from the central one, in a ray-like manner around it (Fig. 7G). Trichomes are very densely distributed along veins and on the abaxial side. Inclined, unicellular, cone-shaped trichomes were found only on the adaxial leaf surface.

Solanum tuberosum L. ‘Acapella’ (Solanaceae) is covered with regularly dispersed, inclined, uniseriate, 3- to 5-cellular, nodose trichomes as well as clavate ones, which are denser on the abaxial side than on the adaxial one.

Stellaria media (L.) Vill. (Caryophyllaceae): the leaf lamina is smooth without any crystalline waxes or trichomes. Cell irregularities determine the surface topography.

Syngonium auritum Schott (Araceae): leaves appear shiny with membraneous and irregular wax platelets, arranged in rosettes. Crystals on the abaxial side are much more densely distributed around the stomata (Fig. 5N).

Tropaeolum majus L. (Tropaeolaceae) is densely covered with tubular wax crystals on the glaucous adaxial leaf surface. The abaxial side bears scattered, perpendicular, and inclined, uniseriate, 2- to 6-cellular, cone-shaped trichomes with a convex unicellular base. The entire surface here, including the trichomes, is densely covered with tubular wax crystals (Fig. 5G, 6O).

Urtica dioica L. (Urticaceae) has (1) inclined, unicellular, cone-shaped, nodose trichomes, (2) stinging trichomes, and (3) bent, unicellular, cone-shaped, nodose trichomes with thickened bases. Trichomes are orientated distally.

Verbascum thapsus L. (Scrophulariaceae): the felt-like indumentum consists abaxially of bent multicellular branched, tree-shaped (dendroid) trichomes (Fig. 6P). Additionally, 4- to 6-cellular stellate trichomes are located on the adaxial side of the leaf.

Viola tricolor L. (Violaceae) has a smooth appearing surface with polygonal wax crystal plates arranged in groups, partially covering the stomata on the abaxial leaf side (Fig. 5O).

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Voigt, D., Gorb, E. & Gorb, S. Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interactions 1, 221–243 (2007). https://doi.org/10.1007/s11829-007-9021-4

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Keywords

  • Adhesion
  • Attachment
  • Biomechanics
  • Bryocorinae
  • Heteroptera
  • Insect–plant interactions
  • Locomotion
  • Miridae
  • Traction force
  • Trichomes