Arthropod-Plant Interactions

, Volume 9, Issue 6, pp 547–565 | Cite as

How many species of arthropods visit flowers?

Review Paper


The majority of living plant species are pollinated by insects, and this interaction is thought to have played a major role in driving the diversification of modern angiosperms. But while flower–insect interactions have been well studied from the perspective of plants in the form of pollination biology, few studies have been carried out from an entomological perspective, where flowers are resources to exploit. As a consequence, it remains unknown how many insect species actually utilise floral resources, especially since many flower-visitors do not carry out pollination and may therefore be widely ignored in pollination studies. In this review, I attempt to present an overview of the taxonomic range of flower-visiting invertebrates and estimate the proportion of described species that regularly utilise flowers. The flower-visiting habit has likely evolved independently hundreds of times across more than a dozen modern invertebrate orders. I speculate, based on reviewing the literature and discussions with experts, that ~30 % of arthropod species (>350,000 described species) may regularly utilise flowers to feed, find a mate, or acquire other resources. When extrapolated to the estimated global diversity of the phylum Arthropoda, perhaps more than a million species regularly visit flowers. However, generating more accurate estimates will require much more work from the perspective of flower-visiting insects, including the often-ignored species that do not pollinate host plants. In particular, sampling techniques in addition to traditional observation protocols should be encouraged to ensure that all flower-visitors are recorded. Greater efforts to identify flower-visiting species beyond the level of order or family will also enhance our understanding of flower-visitor diversity.


Cantharophily Coevolution Florivory Melittophily Myophily Phalaenophily Pollination syndrome Pollen-feeding Psychophily Sphecophily 



I thank Jacob Solomon Raju Aluri, András Bozsik, Tibor Bukovinszky, Christopher A. Hamm, Luc Legal, Jorge Llorente, David G. Notton, Fabio Prezoto, Iral Raganovich, Peter Smetacek, John R. G. Turner, and Ravi Kant Upadhyay for helpful advice on flower-visiting insect diversity. I also thank Nigel Stork, Lars Chittka, and an anonymous reviewer for commenting on an earlier version of this manuscript. This study was completed with the help of funding from the Czech Grant Agency, Project Number 14-36098G.

Supplementary material

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Supplementary material 1 (DOCX 28 kb)


  1. Abbott KR (2010) Background evolution in camouflage systems: a predator-prey/pollinator-flower game. J Theor Biol 262:662–678PubMedCrossRefGoogle Scholar
  2. Adar E, Inbar M, Gal S, Gan-Mor S, Palevsky E (2014) Pollen on-twine for food provisioning and oviposition of predatory mites in protected crops. Biocontrol 59:307–317CrossRefGoogle Scholar
  3. Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones CE, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio P, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17CrossRefGoogle Scholar
  4. Altshuler DL (1999) Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest. Oecologia 119:600–606CrossRefGoogle Scholar
  5. Anderson NH (2009) Megaloptera (Alderflies, Fishflies, Hellgrammites, Dobsonflies). In: Resh VH, Cardé RT (eds) Encyclopedia of Insects, 2nd edn. Elsevier Academic Press, Burlington, pp 620–623CrossRefGoogle Scholar
  6. André HM, Noti M-I, Lebrun P (1994) The soil fauna: the other last biotic frontier. Biodivers Conserv 3:45–56CrossRefGoogle Scholar
  7. Arenas A, Farina WM (2014) Bias to pollen odors is affected by early exposure and foraging experience. J Insect Physiol 66:28–36PubMedCrossRefGoogle Scholar
  8. Armstrong JE, Irvine AK (1989) Floral biology of Myristica insipida (Myristicaceae), a distinctive beetle pollination syndrome. Am J Bot 76:86–94CrossRefGoogle Scholar
  9. Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97CrossRefGoogle Scholar
  10. Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44–66CrossRefGoogle Scholar
  11. Aspöck H (2002) The biology of Raphidioptera: a review of present knowledge. Acta Zool Hung 48(Suppl. 2):35–50Google Scholar
  12. Ballantyne G, Willmer P (2012) Floral visitors and ant scent marks: noticed but not used? Ecol Entomol 37:402–409CrossRefGoogle Scholar
  13. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593CrossRefGoogle Scholar
  14. Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433PubMedCrossRefGoogle Scholar
  15. Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O, Novotny V, Ødegaard F, Roslin T, Schmidl J, Tishechkin AK, Winchester NN, Roubik DW, Aberlenc H-P, Bail J, Barrios H, Bridle JR, Castaño-Meneses G, Corbara B, Curletti G, Duarte da Rocha W, De Bakker D, Delabie JHC, Dejean A, Fagan LL, Floren A, Kitching RL, Medianero E, Miller SE, Gama de Oliveira E, Orival J, Pollet M, Rapp M, Ribeiro SP, Roison Y, Schmidt JB, Sørensen L, Leponce M (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484PubMedCrossRefGoogle Scholar
  16. Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020PubMedCrossRefGoogle Scholar
  17. Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21:399–422CrossRefGoogle Scholar
  18. Bawa KS, Bullock SH, Perry DR, Coville RE, Grayum MH (1985) Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Am J Bot 72:346–356CrossRefGoogle Scholar
  19. Beaman RS, Decker PJ, Beaman JH (1988) Pollination of Rafflesia (Rafflesiaceae). Am J Bot 75:1148–1162CrossRefGoogle Scholar
  20. Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. Am J Bot 71:421–426CrossRefGoogle Scholar
  21. Becerra JX (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256PubMedCrossRefGoogle Scholar
  22. Beckman N, Hurd LE (2003) Pollen feeding and fitness in praying mantids: the vegetarian side of a tritrophic predator. Environ Entomol 32:881–885CrossRefGoogle Scholar
  23. Bernays EA, Janzen DH (1988) Saturniid and sphingid caterpillars: two ways to eat leaves. Ecology 69:1153–1160CrossRefGoogle Scholar
  24. Bernhardt P (2000) Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Syst Evol 222:293–320CrossRefGoogle Scholar
  25. Bernhardt P, Thien LB (1987) Self-isolation and insect pollination in the primitive angiosperms: new evaluations of older hypotheses. Plant Syst Evol 156:159–176CrossRefGoogle Scholar
  26. Beutel RG, Baum E (2008) A longstanding entomological problem finally solved? Head morphology of Nannochorista (Mecoptera, Insecta) and possible phylogenetic implications. J Zool Syst Evol Res 46:346–367CrossRefGoogle Scholar
  27. Blüthgen N, Gebauer G, Fiedler K (2003) Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community. Oecologia 137:426–435PubMedCrossRefGoogle Scholar
  28. Boulter SL, Kitching RL, Gross CL, Goodall KL, Howlett BG (2008) Floral morphology, phenology and pollination in the Wet Tropics. In: Stork NE, Turton SM (eds) Living in a dynamic tropical forest landscape. Blackwell Publishing, Carlton, pp 224–239Google Scholar
  29. Brock PD, Hasenpusch JW (2009) The complete field guide to stick and leaf insects of Australia. CSIRO Publishing, CollingwoodGoogle Scholar
  30. Büttiker W, Krenn HW, Putterill JF (1996) The proboscis of eye-frequenting and piercing Lepidoptera (Insecta). Zoomorphology 116:77–83CrossRefGoogle Scholar
  31. Byers GW (2009) Mecoptera. In: Resh VH, Cardé RT (eds) Encyclopedia of Insects, 2nd edn. Elsevier Academic Press, Burlington, pp 611–614CrossRefGoogle Scholar
  32. Carisey N, Bauce E (1997) Impact of balsam fir flowering on pollen and foliage biochemistry in relation to spruce budworm growth, development and food utilization. Entomol Exp Appl 85:17–31CrossRefGoogle Scholar
  33. Chittka L (2001) Camouflage of predatory crab spiders on flowers, and the colour perception of bees. Entomol Gen 25:181–187CrossRefGoogle Scholar
  34. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377CrossRefGoogle Scholar
  35. Colwell RK (1995) Effects of nectar consumption by the hummingbird flower mite Proctolaelaps kirmsei on nectar availability in Hamelia patens. Biotropica 27:206–217CrossRefGoogle Scholar
  36. Crepet WL (1984) Advanced (constant) insect pollination mechanisms: pattern of evolution and implications vis-á-vis angiosperm diversity. Ann Mo Bot Gard 71:607–630CrossRefGoogle Scholar
  37. Crome FHJ, Irvine AK (1986) “Two bob each way”: the pollination and breeding system of the Australian rain forest tree Syzygium cormiflorum (Myrtaceae). Biotropica 18:115–125CrossRefGoogle Scholar
  38. Danieli-Silva A, Varassin IG (2013) Breeding system and thrips (Thysanoptera) pollination in the endangered tree Ocotea porosa (Lauraceae): implications for conservation. Plant Spec Biol 28:31–40CrossRefGoogle Scholar
  39. Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. John Murray, LondonGoogle Scholar
  40. Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972PubMedCrossRefGoogle Scholar
  41. Dicks LV, Abrahams A, Atkinson J, Biesmeijer J, Bourne N, Brown C, Brown MJF, Carvell C, Connolly C, Cresswell JE, Croft P, Darvill B, De Zylva P, Effingham P, Fountain M, Goggin A, Harding D, Harding T, Hartfield C, Heard MS, Heathcote R, Heaver D, Holland J, Howe M, Hughes B, Huxley T, Kunin WE, Little J, Mason C, Memmott J, Osborne J, Pankhurst T, Paxton RJ, Pocock MJO, Potts SG, Power EF, Raine NE, Ranelagh E, Roberts S, Saunders R, Smith K, Smith RM, Sutton P, Tilley LAN, Tinsley A, Tonhasca A, Vanbergen AJ, Webster S, Wilson A, Sutherland WJ (2013) Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: a collaborative cross-sectoral exercise. Insect Conserv Divers 6:435–446CrossRefGoogle Scholar
  42. Dourson DC (2008) The feeding behavior and diet of an endemic West Virginia land snail, Triodopsis platysayoides. Am Malacol Bull 26:153–159CrossRefGoogle Scholar
  43. Downes JA, Dahlem GA (1987) Keys to the evolution of Diptera: role of Homoptera. Environ Entomol 16:847–854CrossRefGoogle Scholar
  44. Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–567CrossRefGoogle Scholar
  45. Dutton EM, Fredrickson ME (2012) Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis. Arthropod-Plant Inte 6:561–569CrossRefGoogle Scholar
  46. Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE, Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursar TA, Coley PD (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448:696–699PubMedCrossRefGoogle Scholar
  47. Farrell BD (1998) “Inordinate fondness” explained: why are there so many beetles? Science 281:555–559PubMedCrossRefGoogle Scholar
  48. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  49. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:e1PubMedCentralPubMedCrossRefGoogle Scholar
  50. Fontaine C, Thébault E, Dajoz I (2009) Are insect pollinators more generalist than insect herbivores? Proc R Soc B 276:3027–3033PubMedCentralPubMedCrossRefGoogle Scholar
  51. Frame D (2003) Generalist flowers, biodiversity and florivory: implications for angiosperm origins. Taxon 52:681–685CrossRefGoogle Scholar
  52. Frame D, Durou S (2001) Morphology and biology of Napoleonaea vogelii (Lecythidaceae) flowers in relation to the natural history of insect visitors. Biotropica 33:458–471CrossRefGoogle Scholar
  53. Frankie GW, Haber WA, Vinson SB, Bawa KS, Ronchi PS, Zamora N (2003) Flowering phenology and pollination systems diversity in the seasonal dry forest. In: Frankie GW, Mata A, Vinson SB (eds) Biodiversity conservation in costa rica: learning the lessons in a seasonal dry forest. University of California Press, Berkeley, pp 17–29Google Scholar
  54. García MB, Antor RJ, Espadaler X (1995) Ant pollination of the palaeoendemic dioecious Borderea pyrenaica (Dioscoreaceae). Plant Syst Evol 198:17–27CrossRefGoogle Scholar
  55. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westpal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611PubMedCrossRefGoogle Scholar
  56. Gerson U, Weintraub PG (2007) Mites for the control of pests in protected cultivation. Pest Manag Sci 63:658–676PubMedCrossRefGoogle Scholar
  57. Ghazoul J (2001) Can floral repellents pre-empt potential ant-plant conflicts? Ecol Lett 4:295–299CrossRefGoogle Scholar
  58. Gilbert F, Jervis M (1998) Functional, evolutionary and ecological aspects of feeding-related mouthpart specializations in parasitoid flies. Biol J Linn Soc 63:495–535CrossRefGoogle Scholar
  59. Gómez JM, Zamora R, Hódar JA, García D (1996) Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236–242CrossRefGoogle Scholar
  60. Gottsberger G (2012) How diverse are Annonaceae with regard to pollination? Bot J Linn Soc 169:245–261CrossRefGoogle Scholar
  61. Gottsberger G, Silberbauer-Gottsberger I (2006) Life in the Cerrado: a South American tropical seasonal ecosystem, Volume II, Pollination and Seed Dispersal. Ulm: RetaGoogle Scholar
  62. Gottsberger G, Silberbauer-Gottsberger I, Ehrendorfer F (1980) Reproductive biology in the primitive relic angiosperm Drimys brasiliensis (Winteraceae). Plant Syst Evol 135:11–39CrossRefGoogle Scholar
  63. Grimaldi D (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann Mo Bot Gard 86:373–406CrossRefGoogle Scholar
  64. Guerra TJ, Romero GQ, Costa JC, Lofego AC, Benson WW (2012) Phoretic dispersal on bumblebees by bromeliad flower mites (Mesostigmata, Melicharidae). Insect Soc 59:11–16CrossRefGoogle Scholar
  65. Guerrant EO Jr, Fiedler PL (1981) Flower defenses against nectar-pilferage by ants. Biotropica 13(suppl.):25–33CrossRefGoogle Scholar
  66. Haber WA, Frankie GW, Baker HG, Baker I, Koptur S (1981) Ants like flower nectar. Biotropica 13:211–214CrossRefGoogle Scholar
  67. Hamilton AJ, Novotny V, Waters EK, Basset Y, Benke KK, Grimbacher PS, Miller SE, Samuelson GA, Weiblen GD, Yen JDL, Stork NE (2013) Estimating global arthropod species richness: refining probabilistic models using probability bounds analysis. Oecologia 171:357–365PubMedCrossRefGoogle Scholar
  68. Hammond PM (1994) Practical approaches to the estimation of the extent of biodiversity in specious groups. Phil Trans R Soc Lond B 345:119–136CrossRefGoogle Scholar
  69. Hansman DJ (2001) Floral biology of dry rainforest in north Queensland and a comparison with adjacent savanna woodland. Aust J Bot 49:137–153CrossRefGoogle Scholar
  70. Heiling AM, Herberstein ME, Chittka L (2003) Pollinator attraction: crab-spiders manipulate flower signals. Nature 421:334PubMedCrossRefGoogle Scholar
  71. Hopper SD (1980) Pollination of the rain-forest tree Syzygium teirneyanum (Myrtaceae) at Kuranda, northern Queensland. Aust J Bot 28:223–237CrossRefGoogle Scholar
  72. Hu S, Dilcher DL, Jarzen DM, Winship Taylor D (2008) Early steps of angiosperm-pollinator coevolution. Proc Natl Acad Sci USA 105:240–245PubMedCentralPubMedCrossRefGoogle Scholar
  73. Hunt T, Bergsten J, Levkanicova Z, Papadopoulou A, St. John O, Wild R, Hammond PM, Ahrens D, Balke M, Caterino MS, Gómez-Zurita J, Ribera I, Barraclough TG, Bocakova M, Bocak L, Vogler AP (2007) A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 318:1913–1916PubMedCrossRefGoogle Scholar
  74. Ings TC, Chittka L (2009) Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences. Proc R Soc B 276:2031–2036PubMedCentralPubMedCrossRefGoogle Scholar
  75. Insausti TC, Casas J (2008) The functional morphology of color changing in a spider: development of ommochrome pigment granules. J Exp Biol 211:780–789PubMedCrossRefGoogle Scholar
  76. Ishida C, Kono M, Sakai S (2009) A new pollination system: brood-site pollination by flower bugs in Macaranga (Euphorbiaceae). Ann Bot 103:39–44PubMedCentralPubMedCrossRefGoogle Scholar
  77. Itioka T, Kato M, Kaliang H, Merdeck MB, Nagamitsu T, Sakai S, Mohamad SU, Yamane S, Hamid AA, Inoue T (2003) Insect responses to general flowering in Sarawak. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 126–134Google Scholar
  78. Ivancic A, Roupsard O, Garcia JQ, Lebot V, Pochyla V, Okpul T (2005) Thermogenic flowering of the giant taro (Alocasia macrorrhizos, Araceae). Can J Bot 83:647–655CrossRefGoogle Scholar
  79. Janssens F, Christiansen KA (2011) Class Collembola Lubbock, 1870. In: Zhang Z-Q (ed.) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:192–194Google Scholar
  80. Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev 81:219–235PubMedCrossRefGoogle Scholar
  81. Jervis MA (1998) Functional and evolutionary aspects of mouthpart structure in parasitoid wasps. Biol J Linn Soc 63:461–493CrossRefGoogle Scholar
  82. Jervis MA, Vilhelmsen L (2000) Mouthpart evolution in adults of the basal, ‘symphytan’, hymenopteran lineages. Biol J Linn Soc 70:121–146Google Scholar
  83. Jervis MA, Kidd NAC, Fitton MG, Huddleston T, Dawah HA (1993) Flower-visiting by hymenopteran parasitoids. J Nat Hist 27:67–105CrossRefGoogle Scholar
  84. Johnson SA, Nicolson SW (2001) Pollen digestion by flower-feeding Scarabaeidae: protea beetles (Cetoniini) and monkey beetles (Hopliini). J Insect Physiol 47:725–733PubMedCrossRefGoogle Scholar
  85. Jones EI, Dornhaus A (2011) Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behav Ecol Sociobiol 65:1505–1511CrossRefGoogle Scholar
  86. Junker R, Chung AYC, Blüthgen N (2007) Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecol Res 22:665–670CrossRefGoogle Scholar
  87. Karban R, Myers JH (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20:331–348CrossRefGoogle Scholar
  88. Kato M (1996) Plant-pollinator interactions in the understory of a lowland mixed dipterocarp forest in Sarawak. Am J Bot 83:732–743CrossRefGoogle Scholar
  89. Kato M, Matsumoto M, Kato T (1993) Flowering phenology and anthophilous insect community in the cool-temperate subalpine forests and meadows at Mt. Kushigata in the central part of Japan. Contrib Biol Lab Kyoto Univ 28:119–172Google Scholar
  90. Kato M, Kosaka Y, Kawakita A, Okuyama Y, Kobayashi C, Phimminith T, Thongphan D (2008) Plant-pollinator interactions in tropical monsoon forests in Southeast Asia. Am J Bot 95:1375–1394PubMedCrossRefGoogle Scholar
  91. Kearns CA (2001) North American dipteran pollinators: assessing their value and conservation status. Conserv Ecol 5(1):5Google Scholar
  92. Kevan PG, Baker HG (1983) Insects as flower-visitors and pollinators. Annu Rev Entomol 28:407–453CrossRefGoogle Scholar
  93. Kevan PG, Kevan DKM (1970) Collembola as pollen feeders and flower visitors with observations from the high arctic. Quaest Entomol 6:311–326Google Scholar
  94. Kirmse S, Adis J, Morawetz W (2003) Flowering events and beetle diversity in Venezuela. In: Basset Y, Novotný V, Miller SE, Kitching RL (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 256–265Google Scholar
  95. Kitching RL, Boulter SL, Howlett BG, Goodall K (2007) Visitor assemblages at flowers in a tropical rainforest canopy. Austral Ecol 32:29–42CrossRefGoogle Scholar
  96. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313PubMedCentralPubMedCrossRefGoogle Scholar
  97. Krenn HK (2010) Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annu Rev Entomol 55:307–327PubMedCentralPubMedCrossRefGoogle Scholar
  98. Krenn HW, Plant JD, Szucsich NU (2005) Mouthparts of flower-visiting insects. Arthropod Struct Dev 34:1–40CrossRefGoogle Scholar
  99. Krenn HK, Gereben-Krenn B-A, Steinwender BM, Popov A (2008) Flower-visiting Neuroptera: mouthparts and feeding behaviour of Nemoptera sinuate (Nemopteridae). Eur J Entomol 105:267–277CrossRefGoogle Scholar
  100. Kress WJ, Beach JH (1994) Flowering plant reproductive systems. In: McDade LA (ed) La selva, ecology and natural history of a neotropical rain forest. University of Chicago Press, Chicago, pp 161–182Google Scholar
  101. Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Ecol Syst 28:153–193CrossRefGoogle Scholar
  102. Labandeira CC (1998) How old is the flower and the fly? Science 280:57–59CrossRefGoogle Scholar
  103. Labandeira CC (2010) The pollination of mid Mesozoic seed plants and the early history of long-proboscid insects. Ann Mo Bot Gard 97:469–513CrossRefGoogle Scholar
  104. Lack AJ, Kevan PG (1984) On the reproductive biology of a canopy tree, Syzygium syzygioides (Myrtaceae), in a rain forest in Sulawesi, Indonesia. Biotropica 16:31–36CrossRefGoogle Scholar
  105. Larson BMH, Kevan PG, Inouye DW (2001) Flies and flowers: taxonomic diversity of anthophiles and pollinators. Can Entomol 133:439–465CrossRefGoogle Scholar
  106. Lewinsohn TM, Roslin T (2008) Four ways towards tropical herbivore megadiversity. Ecol Lett 11:398–416PubMedCrossRefGoogle Scholar
  107. Lord JM, Huggins L, Little LM, Tomlinson VR (2013) Floral biology and flower visitors on subantarctic Campbell Island. NZ J Bot 51:168–180CrossRefGoogle Scholar
  108. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  109. Louda SM (1982) Inflorescence spiders: a cost/benefit analysis for the host plant, Haplopappus venetus Blake (Asteraceae). Oecologia 55:185–191CrossRefGoogle Scholar
  110. Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–376PubMedCentralPubMedCrossRefGoogle Scholar
  111. Marques MI, Adis J, dos Santos GB, Battirola LD (2006) Terrestrial arthropods from tree canopies in the Pantanal of Mato Grosso, Brazil. Rev Bras Entomol 50:257–267CrossRefGoogle Scholar
  112. McMurtry JA, De Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320CrossRefGoogle Scholar
  113. Memmott J (1999) The structure of a plant-pollinator food web. Ecol Lett 2:276–280CrossRefGoogle Scholar
  114. Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B 271:2605–2611CrossRefGoogle Scholar
  115. Messelink GJ, van Steenpaal SEF, Ramakers PMJ (2006) Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber. Biocontrol 51:753–768CrossRefGoogle Scholar
  116. Messelink GJ, van Maanen R, van Steenpaal SEF, Janssen A (2008) Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol Control 44:372–379CrossRefGoogle Scholar
  117. Micheneau C, Fournel J, Warren BH, Hugel S, Gauvin-Bialecki A, Pailler T, Strasberg D, Chase MW (2010) Orthoptera, a new order of pollinator. Ann Bot 105:355–364PubMedCentralPubMedCrossRefGoogle Scholar
  118. Moldenke AR (1976) California pollination ecology and vegetation types. Phytologia 34:305–361Google Scholar
  119. Molleman F, Krenn HW, Van Alphen ME, Brakefield PM, DeVries PJ, Zwann BJ (2005) Food intake of fruit-feeding butterflies: evidence for adaptive variation in proboscis morphology. Biol J Linn Soc 86:333–343CrossRefGoogle Scholar
  120. Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501PubMedCrossRefGoogle Scholar
  121. Morse DH (1993) Some determinants of dispersal by crab spiderlings. Ecology 74:427–432CrossRefGoogle Scholar
  122. Morse DH (2000) Flower choice by naïve young crab spiders and the effect of subsequent experience. Anim Behav 59:943–951PubMedCrossRefGoogle Scholar
  123. Mound LA (2009) Thysanoptera. In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Elsevier Academic Press, Burlington, pp 999–1003CrossRefGoogle Scholar
  124. Nadkarni NM, Longino JT (1990) Invertebrates in canopy and ground organic matter in a Neotropical montane forest, Costa Rica. Biotropica 22:286–289CrossRefGoogle Scholar
  125. Nagamistu T, Inoue T (1997) Cockroach pollination and breeding system of Uvaria elmeri (Annonaceae) in a lowland mixed-dipterocarp forest in Sarawak. Am J Bot 84:208–213CrossRefGoogle Scholar
  126. Naumann ID (1991) Hymenoptera. The insects of australia: a textbook for students and research workers, vol II. Melbourne University Press, Victoria, pp 916–1000Google Scholar
  127. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514CrossRefGoogle Scholar
  128. Novotny V, Miller SE (2014) Mapping and understanding the diversity of insects in the tropics: past achievements and future directions. Austral Entomol 53:259–267CrossRefGoogle Scholar
  129. Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, Drozd P (2002) Low host specificity of herbivorous insects in a tropical forest. Nature 416:841–844PubMedCrossRefGoogle Scholar
  130. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118PubMedCrossRefGoogle Scholar
  131. Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566CrossRefGoogle Scholar
  132. O’Hanlon JC, Holwell GI, Herberstein ME (2014) Pollinator deception in the orchid mantis. Am Nat 183:126–132PubMedCrossRefGoogle Scholar
  133. Ødegaard F (2000) The relative importance of trees versus lianas as hosts for phytophagous beetles (Coleoptera) in tropical forests. J Biogeogr 27:283–296CrossRefGoogle Scholar
  134. Ødegaard F, Frame D (2007) Generalist flowers and phytophagous beetles in two tropical canopy trees: resources for multitudes. Taxon 56:696–706CrossRefGoogle Scholar
  135. Ollerton J, Johnson SD, Hingston AB (2006) Geographical variation in diversity and specificity of pollination systems. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, USA. Pp, pp 283–308Google Scholar
  136. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  137. Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proc R Soc B 282:20142934PubMedCentralPubMedCrossRefGoogle Scholar
  138. Peakall R, Beattie AJ, James SH (1987) Pseudocopulation of an orchid by male ants: a test of two hypotheses accounting for the rarity of ant pollination. Oecologia 73:522–524CrossRefGoogle Scholar
  139. Peñalver E, Labandeira CC, Barrón E, Delclòs X, Nel P, Nel A, Tafforeau P, Soriano C (2012) Thrips pollination of Mesozoic gymnosperms. Proc Natl Acad Sci USA 109:8623–8628PubMedCentralPubMedCrossRefGoogle Scholar
  140. Perry DR (1978) Paratropes bilunata (Orthoptera: Blattidae): an outcrossing pollinator in a Neotropical wet forest canopy? Proc Entomol Soc Wash 80:656–657Google Scholar
  141. Popov A (2002) Autecology and biology of Nemoptera sinuata Olivier (Neuroptera: Nemopteridae). Acta Zool Hung 48(Suppl. 2):293–299Google Scholar
  142. Porsch O (1957) Alte Insektentypen als Blumenausbeuter. Österreichische Botanische Zeitschrift 104:115–164CrossRefGoogle Scholar
  143. Potts SG, Biesmeijer JC, Kremen C, Neimann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353PubMedCrossRefGoogle Scholar
  144. Primack RB (1983) Insect pollination in the New Zealand mountain flora. NZ J Bot 21:317–333CrossRefGoogle Scholar
  145. Qiu Y-L, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (1999) The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404–407PubMedCrossRefGoogle Scholar
  146. Ramirez N, Seres A (1994) Plant reproductive biology of herbaceous monocots in a Venezuelan tropical cloud forest. Plant Syst Evol 190:129–142CrossRefGoogle Scholar
  147. Ramsay M (1995) Ant pollination of the perennial herb Blandfordia grandiflora (Liliaceae). Oikos 74:265–272CrossRefGoogle Scholar
  148. Rankin SM, Palmer JO (2009) Dermaptera (earwigs). In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Elsevier Academic Press, Burlington, pp 259–261CrossRefGoogle Scholar
  149. Ren D (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280:85–88PubMedCrossRefGoogle Scholar
  150. Ren D, Labandeira CC, Santiago-Blay JA, Rasnitsyn A, Shih C, Bashkuev A, Logan MAV, Hotton CL, Dilcher D (2009) A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326:840–847PubMedCentralPubMedCrossRefGoogle Scholar
  151. Renner SS, Feil JP (1993) Pollinators of tropical dioecious angiosperms. Am J Bot 80:1100–1107CrossRefGoogle Scholar
  152. Rentz DC (2010) A guide to the katydids of Australia. CSIRO Publishing, CollingwoodGoogle Scholar
  153. Rentz DCF, Clyne D (1983) A new genus and species of pollen- and nectar-feeding katydids from eastern Australia (Orthoptera: Tettigoniidae: Zaprochilinae). J Aust Entomol Soc 22:155–160CrossRefGoogle Scholar
  154. Rodgers DJ, Kitching RL (1998) Vertical stratification of rainforest collembolan (Collembola: Insecta) assemblages: description of ecological patterns and hypotheses concerning their generation. Ecography 21:392–400CrossRefGoogle Scholar
  155. Rodgers DJ, Kitching RL (2011) Rainforest Collembola (Hexapoda: Collembola) and the insularity of epiphyte microhabitats. Insect Conserv Diver 4:99–106CrossRefGoogle Scholar
  156. Romero GQ, Vasconcellos-Neto J (2004) Beneficial effects of flower-dwelling predators on their host plant. Ecology 85:446–457CrossRefGoogle Scholar
  157. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209CrossRefGoogle Scholar
  158. Sarma K, Tandon R, Shivanna KR, Ram HYM (2007) Snail pollination in Volvulopsis nummularium. Curr Sci India 93:826–831Google Scholar
  159. Saunders RMK (2012) The diversity and evolution of pollination systems in Annonaceae. Bot J Linn Soc 169:222–244CrossRefGoogle Scholar
  160. Schiestl FP, Schlüter PM (2009) Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu Rev Entomol 54:425–446PubMedCrossRefGoogle Scholar
  161. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422CrossRefGoogle Scholar
  162. Schleuning M, Fründ J, Klein A-M, Abrahamczyk S, Alarcón R, Albrecht M, Andersson GKS, Bazarian S, Böhning-Gaese K, Bommarco R, Dalsgaard B, Dehling DM, Gottlieb A, Hagen M, Hickler T, Holzschuh A, Kaiser-Bunbury CN, Kreft H, Morris RJ, Sandel B, Sutherland WJ, Svenning J-C, Tscharntke T, Watts S, Weiner CN, Werner M, Williams NM, Winqvist C, Dormann CF, Blüthgen N (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr Biol 22:1925–1931PubMedCrossRefGoogle Scholar
  163. Schuster JC (1974) Saltatorial Orthoptera as common visitors to tropical flowers. Biotropica 6:138–140CrossRefGoogle Scholar
  164. Shakya S, Weintraub PG, Coll M (2009) Effect of pollen supplement on intraguild predatory interactions between two omnivores: the importance of spatial dynamics. Biol Control 50:281–287CrossRefGoogle Scholar
  165. Slipinski SA, Leschen RAB, Lawrence JF (2011) Order Coleoptera Linneaus, 1758. In: Zhang, Z–Q. (ed.) Animal Biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:203–208Google Scholar
  166. Ssymank A, Kearns CA, Pape T, Thompson FC (2008) Pollinating flies (Diptera): a major contribution to plant diversity and agricultural production. Biodiversity 9:86–89CrossRefGoogle Scholar
  167. Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326CrossRefGoogle Scholar
  168. Stork NE (1991) The composition of the arthropod fauna of Bornean lowland rain forest trees. J Trop Ecol 7:161–180CrossRefGoogle Scholar
  169. Stork NE, Grimbacher PS (2006) Beetle assemblages from an Australian tropical rainforest show that the canopy and the ground strata contribute equally to biodiversity. Proc R Soc Lond B 273:1969–1975CrossRefGoogle Scholar
  170. Teulon DAJ, Penman DR (1990) Host records for the New Zealand flower thrips (Thrips obscuratus (Crawford) Thysanoptera: Thripidae). NZ Entomol 13:46–51CrossRefGoogle Scholar
  171. Thien LB, Bernhardt P, Devall MS, Chen Z-D, Luo Y-B, Fan J-H, Yuan L-C, Williams JH (2009) Pollination biology of basal angiosperms (ANITA grade). Am J Bot 96:166–182PubMedCrossRefGoogle Scholar
  172. Tylianakis JM (2013) The global plight of pollinators. Science 339:1532–1533PubMedCrossRefGoogle Scholar
  173. van Dulmen A (2001) Pollination and phenology of flowers in the canopy of two contrasting rain forest types in Amazonia, Colombia. Plant Ecol 153:73–85CrossRefGoogle Scholar
  174. Velázquez T, Ornelas JF (2010) Pollen consumption by flower mites in three hummingbird-pollinated plant species. Exp Appl Acarol 50:97–105PubMedCrossRefGoogle Scholar
  175. Villenave J, Thierry D, Mamun AA, Lodé T, Rat-Morris E (2005) The pollens consumed by common green lacewings Chrysoperla spp. (Neuroptera: Chrysopidae) in cabbage crop environment in western France. Eur J Entomol 102:547–552CrossRefGoogle Scholar
  176. Vlasáková B, Kalinová B, Gustafsson MHG, Teichert H (2008) Cockroaches as pollinators of Clusia aff. sellowiana (Clusiaceae) on Inselbergs in French Guiana. Ann Bot 102:295–304PubMedCentralPubMedCrossRefGoogle Scholar
  177. Vranjic JA, Ash JE (1997) Scale insects consistently affect roots more than shoots: the impact of infestation size on growth of eucalypt seedlings. J Ecol 85:143–149CrossRefGoogle Scholar
  178. Wagner D, Kay A (2002) Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evol Ecol Res 4:293–305Google Scholar
  179. Walter DE (2004) Hidden in plain sight: mites in the canopy. In: Lowman MD, Rinker HB (eds) Forest Canopies, 2nd edn. Elsevier Academic Press, Burlington, pp 224–241CrossRefGoogle Scholar
  180. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS (2012) The overlooked biodiversity of flower-visiting invertebrates. PLoS ONE 7:e45796PubMedCentralPubMedCrossRefGoogle Scholar
  181. Wardhaugh CW, Edwards W, Stork NE (2013a) Variation in beetle community structure across five microhabitats in Australian tropical rainforest trees. Insect Conserv Diver 6:463–472CrossRefGoogle Scholar
  182. Wardhaugh CW, Stork NE, Edwards W (2013b) Specialisation of rainforest canopy beetles to host trees and microhabitats: not all specialists are leaf-feeding herbivores. Biol J Linn Soc 109:215–228CrossRefGoogle Scholar
  183. Wardhaugh CW, Stork NE, Edwards W (2014) Canopy invertebrate community composition on rainforest trees: different microhabitats support very different invertebrate communities. Austral Ecol 39:367–377CrossRefGoogle Scholar
  184. Wardhaugh CW, Edwards W, Stork NE (2015) The specialization and structure of antagonistic and mutualistic networks of beetles on rainforest canopy trees. Biol J Linn Soc 114:287–295CrossRefGoogle Scholar
  185. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060CrossRefGoogle Scholar
  186. Williams G, Adam P (1994) A review of rainforest pollination and plant-pollinator interactions with particular reference to Australian subtropical rainforests. Aust Zool 29:177–212CrossRefGoogle Scholar
  187. Willmer PG, Nuttman CV, Raine NE, Stone GN, Pattrick JG, Henson K, Stillman P, McIlroy L, Potts SG, Knudsen JT (2009) Floral volatiles controlling ant behaviour. Funct Ecol 23:888–900CrossRefGoogle Scholar
  188. Wyatt R (1981) Ant-pollination of the granite outcrop endemic Diamorpha smallii (Crassulaceae). Am J Bot 68:1212–1217CrossRefGoogle Scholar
  189. Zhang Z-Q (2011) Phylum Arthropoda von Siebold, 1848. In: Zhang Z-Q. (ed.) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 4138:99–103Google Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Biology Center, Faculty of ScienceUniversity of South Bohemia, and Czech Academy of SciencesCeske BudejoviceCzech Republic

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