Skip to main content
Log in

Plant surface–bug interactions: Dicyphus errans stalking along trichomes

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Andersen SO, Weis-Fogh T (1964) Resilin, a rubber-like protein in arthropod cuticle. Adv Insect Physiol 2:1–65

    CAS  Google Scholar 

  • Andow DA, Prokrym DR (1990) Plant structural complexity and host-finding by a parasitoid. Oecologia 82:62–165

    Google Scholar 

  • Andres MR, Connor EF (2003) The community-wide and guild-specific effects of pubescence on the folivorous insects of manzanitas Arctostaphylos spp. Ecol Entomol 28:383–396

    Google Scholar 

  • Arzet H-R (1972) Suchverhalten und Nahrungsverbrauch der Larven von Chrysopa carnea Steph. Dissertation, Georg-August-Universität, Göttingen, Germany, pp. 93

  • Avé DA, Gregory P, Tingey WM (1987) Aphid repellent sesquiterpenes in glandular trichomes of Solanum berthaultii and S. tuberosum. Entomol Exp Appl 44:131–138

    Google Scholar 

  • Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botan J Linn Soc126:237–260

    Google Scholar 

  • Becerra JX (2003) Synchronous coadaption in an ancient case of herbivory. PNAS 100:12804–12807

    PubMed  CAS  Google Scholar 

  • Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing Ltd., 738 pp

  • Belcher DW, Thurston R (1982) Inhibition of movement of larvae of the convergent lady beetle by leaf trichomes of tobacco. Environ Entomol 11:91–94

    Google Scholar 

  • Benedict HJ, Leigh TF, Hyer AH (1983) Lygus hesperus (Heteroptera: Miridae) oviposition behaviour, growth, and survival in relationship to cotton trichome density. Environ Entomol 12:331–335

    Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Contemporary topics in entomology, 2nd edn. Chapman & Hall, pp. 312

  • Betz O (2002) Performance and adaptive value of tarsal morphology in rove beetles of the genus Stenus (Coleoptera, Staphylinidae). J Exp Biol 205:1097–1113

    PubMed  Google Scholar 

  • Brennan EB, Weinbaum SA (2001) Stylet penetration and survival of three psyllid species on adult leaves and ‘waxy’ and ‘de-waxy’ juvenile leaves of Eucalyptus globulus. Entomol Exp Appl 100:355–363

    Google Scholar 

  • Carter MC, Sutherland D, Dixon AFG (1984) Plant structure and the searching efficiency of coccinellid larvae. Oecologia 63:394–397

    Google Scholar 

  • Chapman RF (1977) The role of leaf surface in food selection by acridids and other insects. Coll Int CNRS 265:133–149

    Google Scholar 

  • Coll M, Smith LA, Ridgway RL (1997) Effect of plants on the searching efficiency of a generalist predator: the importance of predator-prey spatial associations. Entomol Exp Appl 83:1–10

    Google Scholar 

  • Coll M (1998) Living and feeding on plants in predatory heteroptera. In: Coll M, Ruberson JR (eds) Predatory Heteroptera: their ecology and use in biological control. Proc Entomol Soc Am, pp 89–130

  • Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding manipulating plant attributes to enhance biological control. Biol Control 17:35–49

    Google Scholar 

  • Dalin P, Björkman C, Eklund K (2004) Leaf beetle grazing does not induce willow trichome defence in the coppicing willow Salix viminalis. Agr Forest Entomol 6:105–109

    Google Scholar 

  • Dixon AFG (1986) Habitat specifity and foraging behaviour of aphidophagous insects. In: Hodek I (ed) Ecology of aphidophaga. Proceedings of the 2nd symosium held at Zvíkovské Podhradí, September 2–8, 1984, Series Entomologica 35, pp 151–154

  • Dos Santos TM, Júnior ALB, Soares JJ (2003) Influência de tricomas do algodoeiro sobre os aspectos biológicos e capacidade predatória de Chrysoperla externa (Hagen) alimentada com Aphis gossypii Glover. Bragantia, Campinas 62:243–254

    Google Scholar 

  • Duffey SS (1986) Plant glandular trichomes: their partial role in defense against insects. In: Juniper B, Southwood R (ed) Insects and the plant surface. Edward Arnold Publishers, London, pp 151–172

    Google Scholar 

  • Ecole CC, Picanço MC, Guedes RNC, Brommonschenkel SH (2001) Effect of cropping season and possible compounds involved in the resistance of Lycopersicon hirsutum f. typicum to Tuta absoluta (Meyrick) (Lep., Gelechiidae). J Appl Entomol 125:193–200

    CAS  Google Scholar 

  • Eigenbrode SD (1996) Plant surface waxes and insect behaviour. In: Kerstiens G (eds) Plant cuticles—an integral functional approach. BIOS Publ., Oxford, pp 201–222

    Google Scholar 

  • Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthr Struct Dev 33:91–102

    CAS  Google Scholar 

  • Eigenbrode SD, Castagnola T, Roux M-B, Steljes L (1996) Mobility of three generalist predators is greater on cabbage with glossy leaf wax than on cabbage with a wax bloom. Entomol Exp Appl 81:335–343

    Google Scholar 

  • Eisner T, Eisner M, Hoebeke ER (1998) When defense backfires: detrimental effect of a plant’s protective trichomes on an insect beneficial to the plant. Proc Natl Acad Sci USA 95:4410–4414

    PubMed  CAS  Google Scholar 

  • Elsey KD (1974) Influence of plant host on searching speed of two predators. Entomophaga 19:3–6

    Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. John Wiley & Sons, pp 767

  • Evans HF (1976) Mutual interference between predatory anthocorids. Ecol Entomol 1:283–286

    Google Scholar 

  • Federle W, Brainerd WL, McMahon T, Hölldobler B (2001) Biomechanics of the movable pretarsal adhesive organ in ants and bees. PNAS 98:6215–6220

    PubMed  CAS  Google Scholar 

  • Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B (1997) Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112:217–224

    Google Scholar 

  • Federle W, Rohrseitz K, Hölldobler B (2000) Attachment forces of ants measured with a centrifuge: better “wax-runners” have poorer attachment to a smooth surface. J Exp Biol 203:505–512

    PubMed  CAS  Google Scholar 

  • Fordyce JA, Agrawal AA (2001) The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. J Anim Ecol 70:997–1005

    Google Scholar 

  • Frantsevich L, Gorb S (2004) Structure and mechanics of the tarsal chain in the hornet, Vespa crabro (Hymenoptera: Vespidae): implications on the attachment mechanism. Arthr Struct Dev 33:77–89

    Google Scholar 

  • Frazier SF, Larsen GS, Neff D, Quimby L, Carney M, DiCaprio RA, Zill SN (1999) Elasticity and movements of the cockroach tarsus in walking. J Comp Physiol A 185:157–172

    Google Scholar 

  • Gassmann AJ, Hare JD (2005) Indirect cost of a defensive trait: variation in trichomes type affects the natural enemies of herbivorous insects on Datura wrightii. Oecologia 144:62–71

    PubMed  Google Scholar 

  • Gaume L, Perret P, Gorb E, Gorb S, Labat J-J, Rowe N (2004) How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthr Struct Dev 33:103–111

    CAS  Google Scholar 

  • Gepp J (1977) Bewegungsbehinderung von Arthropoden durch Trichome an Bohnenpflanzen (Phaseolus vulgaris L.). Anz Schädlingskde Pflanzenschutz Umweltschutz 50:8–12

    Google Scholar 

  • Ghazi-Bayat A (1979) Zur Oberflächenstruktur der tarsalen Haftlappen von Coreus marginatus (L.) (Coreidae, Heteroptera). Zool Anz 203:345–347

    Google Scholar 

  • Ghazi-Bayat A, Hasenfuss I (1980) Die Oberflächenstrukturen des Prätarsus von Elasmucha ferrugata (Fabricius) (Acanthosomatidae, Heteroptera). Zool Anz 205:76–80

    Google Scholar 

  • Ghazi-Bayat A, Hasenfuss I (1981) Über den Transportweg der Haftflüssigkeit der Pulvilli bei Coptosoma scutellatum (Geoffr.) (Plataspididae, Heteroptera). Nachrichtenblatt der Bayerischen Entomologen 30:58

  • Gibson RW (1971) Glandular hairs providing resistance to aphids in certain wild potato species. Ann Appl Biol 68:113–119

    Google Scholar 

  • Gibson RW, Pickett JA (1983) Wild potato repels aphids by release of aphid alarm pheromone. Nature 302:608–609

    CAS  Google Scholar 

  • Gilbert LE (1971) Butterfly-plant coevolution: has Passiflora adenopoda won the selectional race with Heliconiine butterflies? Science 172:585–586

    PubMed  CAS  Google Scholar 

  • Gingras D, Boivin G (2002) Effect of plant structure, host density and foraging duration on host finding by Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Environ Entomol 31:1153–1157

    Article  Google Scholar 

  • Goffreda JC, Mutschler MA, Avé DA, Tingey WM, Steffens JC (1989) Aphid deterrence by glucose esters in glandular trichome exudate of the wild tomato, Lycopersicon pennelli. J Chem Ecol 15:2135–2147

    CAS  Google Scholar 

  • Gorb E, Gorb S (2006a) Combination of the surface profile and chemistry reduces the attachment of the beetle Gastrophysa viridula on the Rumex obtusifolius leaf surface. Proceedings of the 5th plant biomechanics conference, August 28th–September 1st, 2006, vol 2. Stockholm, Sweden, pp 537–542

  • Gorb E, Gorb S (2006b) Do plant waxes make insect attachment structures dirty? Experimental evidence for the contamination hypotheses. In: Herrel A, Speck T, Rowe NP (eds) Ecology and biomechanics. CRC Press, Taylor & Francis, Boca Raton, Florida, pp 147–162

    Google Scholar 

  • Gorb EV, Gorb SN (2002) Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomol Exp Appl 105:13–28

    Google Scholar 

  • Gorb E, Haas K, Henrich A, Enders S, Barbakadze N, Gorb S (2005) Composite structure of the crystalline wax layer of the slippery zone in the pitchers of the carnivorous plant Nepenthes alata and its effect on insect attachment. J Exp Biol 208:4651–4662

    PubMed  CAS  Google Scholar 

  • Gorb E, Kastner V, Peressadko A, Arzt E, Gaume L, Rowe N, Gorb S (2004) Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. J Exp Biol 207:2974–2963

    Google Scholar 

  • Gorb SN (1996) Design of insect unguitractor apparatus. J Morphology 230:219–230

    Google Scholar 

  • Gorb SN (1999) Serial elastic elements in the damselfly wing: mobile vein joints contain resilin. Naturwissenschaften 86:552–555

    PubMed  CAS  Google Scholar 

  • Gorb SN (2001) Attachment devices of insect cuticle. Kluwer Academic Publishers, Dordrecht, pp 305

    Google Scholar 

  • Gorb SN, Beutel RG (2001) Evolution of locomotory attachment pads of hexapods. Naturwissenschaften 88:530–534

    PubMed  CAS  Google Scholar 

  • Goundoudaki S, Tsitsipis JA, Margaritopoulos JT, Zarpas KD, Divanidis S (2003) Performance of the tobacco aphid Myzus persicae (Hemiptera: Aphididae) on oriental and Virginia tobacco varieties. Agr Forest Entomol 5:285–291

    Google Scholar 

  • Gregory P, Ave DA, Bouthyette PJ, Tingey WM (1986) Insect-defensive chemistry of potato glandular trichomes. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold Publishers, London, pp 173–184

    Google Scholar 

  • Grevstad FS, Klepetka BW (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399–404

    Google Scholar 

  • Grimaldi D, Engel MS (2004) Evolution of the insects. Cambridge University Press, New York, pp 755

    Google Scholar 

  • Haddad NM, Hicks WM (2000) Host pubescence and the behavior and performance of the butterfly Papilio troilus (Lepidoptera: Papilionidae). Environ Entomol 29:299–303

    Google Scholar 

  • Hare JD (2005) Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores. J Chem Ecol 31:1475–1491

    PubMed  CAS  Google Scholar 

  • Hare JD, Elle E (2002) Variable impact of diverse insect herbivores on dimorphic Datura wrightii. Ecology 83:2711–2720

    Article  Google Scholar 

  • Hare JD, Smith II JL (2005) Competition, herbivory, and reproduction of trichome phenotypes of Datura wrightii. Ecology 86:334–339

    Google Scholar 

  • Hoffmann GD, McEvoy PB (1985) The mechanism of trichome resistance in Anaphalis margaritacea to the meadow spittlebug Philaenus spumarius. Entomol Exp Appl 39:123–129

    Google Scholar 

  • Hosoda N, Gorb SN (2004) Critical roughness for insect attachment: experimental evidences for the beetle Gastrophysa viridula. Abstracts of 2 Bremer Bionik-Kongress, 29.-30.10.2004, Bremen

  • Hoxie RP, Wellso SG, Webster JA (1975) Cereal leaf beetle response to wheat trichome length and density. Environ Entomol 4:365–370

    Google Scholar 

  • Hummel K, Staesche K (1962) Die Verbreitung der Haartypen in ihren natürlichen Verwandtschaftsgruppen. In: Zimmermann W, Ozenda PG (eds) Handbuch der Pflanzenanatomie, Gebrüder Bornträger, Berlin, 2. v. neub. Aufl., Band IV, Teil 5. Abteilung: Histologie, Gebrüder Borntraeger, Berlin-Nikolassee, pp 207–292

  • Jeffree CF (1986) The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, functions and evolution. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold Publishers, London, pp 23–64

    Google Scholar 

  • Jervis M, Kidd N (1996) Insect natural enemies. Practical approaches to their study and evaluation. Chapman & Hall, London, 491 pp

    Google Scholar 

  • Johnson B (1953) The injurious effects of the hooked epidermal hairs of french beans (Phaseolus vulgaris L.) on Aphis craccivora Koch. Bull Entomol Res 44:779–788

    Article  Google Scholar 

  • Johnson B (1956) The influence on aphids of the glandular hairs on tomato plants. Plant Pathology 5:131–132

    Google Scholar 

  • Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258

    Article  Google Scholar 

  • Jolivet P (1998) Interrelationship between insects and plants. CRC Press, Boca Raton, Florida, 309 pp

    Google Scholar 

  • Jordan KHC (1962) Landwanzen. Die neue Brehm-Bücherei, Bd. 294, A.-Ziemsen-Verlag, Wittenberg-Lutherstadt, 116 pp

  • Juniper BE (1995) Waxes on plant surfaces and their interactions with insects. In: Hamilton RJ (ed) Waxes: chemistry, molecular biology and functions. Oily, West Ferry, Dundee, pp 157–174

    Google Scholar 

  • Juniper BE, Jeffree CE (1983) Plant surfaces. Edward Arnold Limited, London, 93 pp

    Google Scholar 

  • Kareiva P, Sahakian R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–434

    Google Scholar 

  • Kashyap RK, Kennedy GG, Farrar RR Jr (1991) Behavioral response of Trichogramma pretiosum Riley and Telenomus sphingis (Ashmead) to trichome/methyl ketone mediated resistance in tomato. J Chem Ecol 17:543–556

    CAS  Google Scholar 

  • Keller MA (1987) Influence of leaf surfaces on movements by the hymenopterous parasitoid Trichogramma exiguum. Entomol Exp Appl 43:55–59

    Google Scholar 

  • Kennedy CEJ (1986) Attachment may be a basis for specialization in oak aphids. Ecol Entomol 11:291–300

    Google Scholar 

  • Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu Rev Entomol 48:51–72

    PubMed  CAS  Google Scholar 

  • Kowalewski E, Robinson RW (1978) White fly species resistance in Cucumis species. Cucurbit Genetics Cooperative Report 1:38

    Google Scholar 

  • Kullenberg B (1946) Studien über die Biologie der Capsiden. Zool Bidrag Uppsala 23:1–522

    Google Scholar 

  • Lapointe SL, Tingey WM (1986) Glandular trichomes of Solanum berthaultii confer resistance to green peach aphid (Homoptera: Aphididae). J Econ Entomol 79:1264–1268

    Google Scholar 

  • Lauenstein G (1976) Untersuchungen zu Biologie und Verhaltensweisen der Räuberischen Blumenwanze Anthocoris nemorum L. (Het.: Anthocoridae). Dissertation, G.-August-Universität Göttingen, Germany

  • Lee YI, Kogan M, Larsen JR Jr (1986) Attachment of the potato leafhopper to soybean plant surfaces as affected by morphology of the pretarsus. Entomol Exp Appl 42:101–107

    Google Scholar 

  • Lees AD, Hardie J (1988) The organs of adhesion in the aphid Megoura viciae. J Exp Biol 136:209–228

    Google Scholar 

  • Leite GLD, Picanço M, Della Lucia TMC, Moreira MD (1999) Role of canopy height in the resistance of Lycopersicon hirsutum f. glabrum to Tuta absoluta (Lep., Gelechiidae). J Appl Entomol 123:459–463

    Google Scholar 

  • Levin DA (1973) The role of trichomes in plant defense. Quart Rev Biol 48:3–15

    Google Scholar 

  • Malakar R, Tingey WM (2000) Glandular trichomes of Solanum berthaultii and its hybrids with potato deter oviposition and impair growth of potato tuber moth. Entomol Exp Appl 94:249–257

    Google Scholar 

  • McKinney KB (1938) Physical characteristics on the foliage of beans and tomatoes that tend to control some small insect pests. J Econ Ent 31:630–631

    Google Scholar 

  • Metcalfe CR, Chalk L (1988) Anatomy of the dicotyledons. Leaves, stem, and wood in relation to taxonomy with notes on economic uses, vol II, 2nd edn. Oxford University Press, 330 pp

  • Müller C (2006) Plant-insect interactions on cuticular surface. In: Riederer M, Müller C (eds) Biology of plant cuticle. Blackwell Publishing, Oxford, pp 398–422

    Google Scholar 

  • Musetti L, Neal JJ (1997) Resistance to the pink potato aphid, Macrosiphum euphorbiae, in two accessions of Lycopersicon hirsutum f. glabratum. Entomol Exp Appl 84:137–146

    Google Scholar 

  • Napp-Zinn K (1973) Anatomie des Blattes. II Blattanatomie der Angiospermen. A. Entwicklungsgeschichte und topographische Anatormie des Angiospermenblattes. In: Linsbauer K (ed) Handbuch der Pflanzenanatomie, Bd. VIII, Teil 2 A, Bornträger-Verlag, Berlin

  • Niederegger S, Gorb S (2003) Tarsal movements in flies during leg attachment and detachment on a smooth substrate. J Ins Physiol 49:611–620

    CAS  Google Scholar 

  • Obrycki JJ (1986) The influence of foliar pubescence on entomophagous species. In: Boerthel DJ, Eikenbarry RD (eds) Interactions of plant resistance and parasitoids and predators of insects. J. Wiley & Sons, New York, 200 pp

    Google Scholar 

  • Obrycki JJ, Tauber MJ (1984) Natural enemy activity on glandular pubescent potato plants in the greenhouse: An unreliable predictor of effects in the field. Environ Entomol 13:679–683

    Google Scholar 

  • Payne WW (1978) A glossary of plant hair terminology. Brittonia 30:239–255

    Google Scholar 

  • Peeters PJ (2002) Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biol J Linnean Soc 77:43–65

    Google Scholar 

  • Pillemer EA, Tingey WM (1978) Hooked trichomes and resistance of Phaseolus vulgaris to Empoasca fabae (Harris). Entomol Exp Appl 24:83–94

    Google Scholar 

  • Putman WL (1955) Bionomics of Stethorus punctillum Weise (Coleoptera: Coccinellidae) in Ontario. Can Entomol 86:9–33

    Article  Google Scholar 

  • Quilici S, Iperti G (1986) The influence of host plant on the searching ability of first instar larvae of Propylea quadrodecimpunctata. In: Hodek I (ed) Ecology of aphidophaga. Series Entomologica 35:99–111

  • Rabb RL, Bradley JR (1968) The influence of host plants on parasitism of eggs of the tobacco hornworm. J Econ Entomol 61:1249–1252

    Google Scholar 

  • Ranger CM, Hower AA (2002) Glandular trichomes on perennial alfalfa affect host-selection behavior of Empoasca fabae. Entomol Exp Appl 105:71–81

    Google Scholar 

  • Ringlund K, Everson EH (1968) Leaf pubescence in common wheat, Triticum aestivum L., and resistance to the cereal leaf beetle, Oulema melanopus (L.). Crop Science 8:705–710

    Google Scholar 

  • Roberts JJ, Foster JE (1983) Effect of leaf pubescence in wheat on the bird cherry oak aphid (Homoptera: Aphidae). J Econ Entomol 76:1320–1322

    Google Scholar 

  • Rudgers JA, Strauss SY, Wendel JF (2004) Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). Am J Bot 91:871–880

    Google Scholar 

  • Schoonhoven LM, van Loon JA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University press, New York, 421 pp

    Google Scholar 

  • Schuh RT (1976) Pretarsal structure in the Miridae (Hemiptera) with a cladistic analysis of relationships within the family. Am Mus Novit 2601:1–39

    Google Scholar 

  • Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera): Classification and natural history. Cornell University Press, London, 336 pp

    Google Scholar 

  • Seidenstücker G (1967) Eine Phyline mit Dicyphus-Kralle (Heteroptera, Miridae). Reichenbachia Bd. 8. 27:215–220

    Google Scholar 

  • Sengonca C, Gerlach S (1984) Einfluss der Blattoberfläche auf die Wirksamkeit des räuberischen Thrips, Scolothrips longicornis (Thysan.: Thripidae). Entomophaga 29:55–61

    Google Scholar 

  • Shanower TG, Romeis J, Peter AJ (1996) Pigeonpea plant trichomes: Multiple trophic level interactions. In: Ananthakrishnan TN (ed) Biotechnological perspectives in chemical ecology of insects. Oxford & IBH, New Delhi, pp 76–88

    Google Scholar 

  • Shah MA (1980) Beutesuchverhalten von Coccinelliden. Dissertation, Universität Hohenheim, Germany

  • Shah MA (1982) The influence of plant surfaces on the searching behaviour of coccinellid larvae. Entomol Exp Appl 31:377–380

    Google Scholar 

  • Simmons AT, Gurr GM (2004) Trichomes-based host plant resistance of Lycopersicon species and the biocontrol agent Mallada signata: are they compatible? Entomol Exp Appl 113:95–101

    Google Scholar 

  • Simmons AT, Gurr GM (2005) Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agr Forest Entomol 7:265–276

    Google Scholar 

  • Simmons AT, Gurr GM, McGrath D, Martin PM, Nicol HI (2004) Entrapment of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on glandular trichomes of Lycopersicon species. Australian J Entomol 43:196–200

    Google Scholar 

  • Simmons AT, Gurr GM, McGrath D, Nicol HI, Martin PM (2003) Trichomes of Lycopersicon spp. and their effect on Myzus persicae (Sulzer) (Hemiptera: Aphidiae). Australian J Entomol 42:373–378

    Google Scholar 

  • Smith CM (2005) Plant resistance to arthropods. Springer, Dordrecht, 423 pp

    Google Scholar 

  • Southwood TRE (1973) The insect/plant relationship—an evolutionary perspective. Symp Roy Entomol Soc London 6:3–30

    Google Scholar 

  • Southwood R (1986) Plant surfaces and insects-an overview. In: Juniper B, Southwood R (ed) Insects and the plant surface. Edward Arnold Publishers, London, pp 1–22

    Google Scholar 

  • Stork NE (1980b) Role of wax blooms in preventing attachment to brassicas by the mustard beetle, Phaedon cochleariae. Entomol Exp Appl 28:100–107

    Google Scholar 

  • Stork NE (1986) The form of plant waxes: a means of preventing insect attachment? In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold Publishers, London, pp 346–347

    Google Scholar 

  • Thurston R (1970) Toxicity of trichome exudates of Nicotiana and Petunia species to tobacco hornworm larvae. J Econ Entomol 63:272–274

    Google Scholar 

  • Thurston R, Webster JA (1962) Toxicity of Nicotiana gossei domin to Myzus persicae (Sulzer). Entomol Exp Appl 5:233–238

    Google Scholar 

  • Thurston R, Smith WT, Cooper BP (1966) Alkaloid secretion by trichomes of Nicotiana species and resistance to aphids. Entomol Exp Appl 9:428–423

    CAS  Google Scholar 

  • Uphof JCT (1962) Plant hairs. In: Zimmermann W, Ozenda PG (eds) Handbuch der Pflanzenanatomie, Gebrüder Bornträger, Berlin, 2. v. neub. Aufl., Band IV, Teil 5, Abteilung: Histologie, Gebrüder Borntraeger, Berlin-Nikolassee, pp 1–206

  • Valverde PL, Fornoni J, Núnez-Farfán J (2001) Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J Evol Biol 14:424–432

    Google Scholar 

  • Van Dam NM, Hare JD (1998) Differences in distribution and performance of to sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecol Entomol 23:22–32

    Google Scholar 

  • Voigt D (2004) Relevanz der Pflanzen im Räuber-Beute-(Wirts-)Pflanzen-Komplex der Weichwanze Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae). Mitteilungen der BBA, Berlin-Dahlem 396:480

    Google Scholar 

  • Voigt D (2005) Untersuchungen zur Morphologie, Biologie und Ökologie der räuberischen Weichwanze Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae). Dissertation, TU Dresden, Germany, http://nbn-resolving.de/urn:nbn:de:swb:14-1138036391273-82564

  • Voigt D, Pohris V, Wyss U (2006) Zur Nahrungsaufnahme von Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae): Nahrungsspektrum, Potenzial und Verhalten. Mitt Dtsch Ges Allg Angew Ent 15:305–308

    Google Scholar 

  • Wagner E (1955) Bemerkungen zum System der Miridae (Hemiptera, Heteroptera). Dtsch Entomol Z 2:230–242

    Article  Google Scholar 

  • Walters PJ (1974) A method for culturing Stethorus spp. (Coleoptera: Coccinellidae) on Tetranychus urticae (Koch) (Acarina: Tetranychidae). J Aust Ent Soc 13:245–246

    Google Scholar 

  • Wheeler AG (2001) Biology of the plant bugs (Hemiptera: Miridae): Pests, predators, opportunists. Cornell University Press, London, pp. 507

    Google Scholar 

  • Wigglesworth VB (1959) Physiologie der Insekten. Reihe Exp. Biologie, Bd. 14, Birkhäuser Verlag, Basel & Stuttgart, 2. Aufl

  • Zvereva EL, Kozlov MV, Niemelä P (1998) Effects of leaf pubescence in Salix borealis on host-plant choice and feeding behaviour of the leaf beetle, Melasoma lapponica. Entomol Exp Appl 89:297–303

    Google Scholar 

  • Zwölfer H (2003) Insekten und Pflanzen. In: Dettner K, Peters W (eds) Lehrbuch der Entomologie. Spektrum Akademischer Verlag, Heidelberg, 2. neub. Aufl, pp 499–520

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dagmar Voigt.

Additional information

Handling editor: Heikki Hokkanen

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).

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-007-9021-4

Keywords

Navigation