Extrafloral nectar at the plant-insect interface: A spotlight on chemical ecology, phenotypic plasticity, and food webs

Annual Review of Entomology

Volumn 60, Issue , 2015, Pages 213-232

  Heil, Martin ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

Ant plant interaction; Community effects; Herbivory; Indirect defense; Invertase; Optimal defense hypothesis

Indexed keywords

ACARI; ARANEAE; ARTHROPODA; COLEOPTERA; HEXAPODA;

NECTAR;

ANGIOSPERM; ANIMAL; BIOLOGICAL PEST CONTROL; FEEDING BEHAVIOR; FOOD CHAIN; INSECT; METABOLISM; MITE; NECTAR; PHYSIOLOGY; SPIDER; SYMBIOSIS;

ANGIOSPERMS; ANIMALS; FEEDING BEHAVIOR; FOOD CHAIN; INSECTS; MITES; PEST CONTROL, BIOLOGICAL; PLANT NECTAR; SPIDERS; SYMBIOSIS;

EID: 84920808839     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-010814-020753     Document Type: Review

References (183)

1. Agarwal VM, Rastogi N. 2010. Ants as dominant insect visitors of the extrafloral nectaries of sponge gourd plant, Luffa cylindrica (L.) (Cucurbitaceae). Asian Myrmecol. 3:45-54
2. Agrawal AA, Karban R. 1997. Domatia mediate plant-arthropod mutualism. Nature 387:562-63
3. Agrawal AA, Karban R, Colfer RG. 2000.Howleaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89:70-80
4. Aguirre A, Coates R, Cumplido-Barragan G, Campos-Villanueva A, Diaz-Castelazo C. 2013. Morphological characterization of extrafloral nectaries and associated ants in tropical vegetation of Los Tuxtlas, Mexico. Flora 208:147-56
5. Almeida LM, Correa GH, Giorgi JA, Grossi PC. 2011. New record of predatory ladybird beetle (Coleoptera, Coccinellidae) feeding on extrafloral nectaries. Rev. Bras. Entomol. 55:447-50
6. Alves-Silva E, Baronio GJ, Torezan-Silingardi HM, Del-Claro K. 2013. Foraging behavior of Brachygastra lecheguana (Hymenoptera: Vespidae) on Banisteriopsis malifolia (Malpighiaceae): extrafloral nectar consumption and herbivore predation in a tending ant system. Entomol. Sci. 16:162-69
7. Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, et al. 2012. Highly similar microbial communities are shared among related and trophically similar ant species. Mol. Ecol. 21:2282-96
8. Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz JC. 2004. Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol. 164:157-64
9. Arnold TM, Schultz JC. 2002. Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585-93
10. Assuncao MA, Torezan-Silingardi HM, Del-Claro K. 2014. Do ant visitors to extrafloral nectaries of plants repel pollinators and cause an indirect cost of mutualism? Flora 209:244-49
11. Barrett LG, Heil M. 2012. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 17:282-92
12. Beach RM, Todd JW, Baker SH. 1985. Nectaried and nectariless cotton cultivars as nectar sources for the adult soybean looper. J. Entomol. Sci. 20:233-36
13. Belt T. 1874. The Naturalist in Nicaragua. London: Dent
14. Benrey B, Callejas A, Rios L, Oyama K, Denno RF. 1998. The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol. Contr. 11:130-40
15. Bentley BL. 1976. Plants bearing extrafloral nectaries and the associated ant community: interhabitat differences in the reduction of herbivore damage. Ecology 57:815-20
16. Bentley BL. 1977. Extrafloral nectaries and protection by pugnacious bodyguards. Annu. Rev. Ecol. Syst. 8:407-27
17. Bixenmann RJ, Coley PD, Kursar TA. 2011. Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant-plant mutualism? Oecologia 165:417-25
18. Bleil R, Bluethgen N, Junker RR. 2011. Ant-plant mutualism in Hawaii? Invasive ants reduce flower parasitism but also exploit floral nectar of the endemic shrub Vaccinium reticulatum (Ericaceae). Pacific Sci. 65:291-300
19. Bogatek R, Come D, Corbineau F, Ranjan R, Lewak S. 2002. Jasmonic acid affects dormancy and sugar catabolism in germinating apple embryos. Plant Physiol. Biochem. 40:167-73
20. Brown MW, Mathews CR, Krawczyk G. 2010. Extrafloral nectar in an apple ecosystem to enhance biological control. J. Econ. Entomol. 103:1657-64
21. Byk J, Del-Claro K. 2011. Ant-plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Popul. Ecol. 53:327-32
22. Cardoso-Gustavson P, Bignelli Valente Aguiar JMR, Pansarin ER, de Barros F. 2013. A light in the shadow: the use of Lucifer Yellow technique to demonstrate nectar reabsorption. Plant Methods 9:20
23. Carter C, Thornburg RW. 2000. Tobacco Nectarin I: purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues. J. Biol. Chem. 275:36726-33
24. Carter C, Thornburg RW. 2004. Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci. 9:320-24
25. Chamberlain SA, Holland JN. 2009. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384-92
26. Chamberlain SA, Kilpatrick JR, Holland JN. 2010. Do extrafloral nectar resources, species abundances, and body sizes contribute to the structure of ant-plant mutualistic networks? Oecologia 164:741-50
27. Chamberlain SA, Rudgers JA. 2012. How do plants balance multiple mutualists? Correlations among traits for attracting protective bodyguards and pollinators in cotton (Gossypium). Evol. Ecol. 26:65-77
28. Chavarro-RodriguezN, Diaz-Castelazo C, Rico-Gray V. 2013. Characterization and functional ecology of the extrafloral nectar of Cedrela odorata in contrasting growth environments in central Veracruz, Mexico. Bot. Botanique 91:695-701
29. Choh Y, Kugimiya S, Takabayashi J. 2006. Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites. Oecologia 147:455-60
30. Choh Y, Takabayashi J. 2006. Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics. J. Chem. Ecol. 32:2073-77
31. Coulter A, Poulis BAD, von Aderkas P. 2012. Pollination drops as dynamic apoplastic secretions. Flora 207:482-90
32. Darwin F. 1876. On the glandular bodies on Acacia sphaerocephala and Cecropia peltata serving as food for ants.With an appendix on the nectar-glands of the common brake fern, Pteris Aquilina. Bot. J. Linn. Soc. Lond. 15:398-409
33. Davidson DW, Cook SC, Snelling RR, Chua TH. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969-72
34. Delpino F. 1874. Rapporti tra insetti e nettari extranuziali nelle plante. Boll. Soc. Entomol. Ital. 6:234-39
35. Delpino F. 1886. Funzione mirmecofila nel regno vegetale. Memoria Acad. Sci. Inst. Bologna 4:215-323
36. Escalante-Perez M, JaborskyM, Lautner S, Fromm J, Muller T, et al. 2012. Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores. Plant Physiol. 159:1176-91
37. Fiala B, Linsenmair KE. 1995. Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia. Biodiv. Conserv. 4:165-82
38. Frey-Wyssling A, Zimmermann M, Maurizio A. 1954. Uber den enzymatischen Zuckerumbau in Nektarien. Experientia 10:490-91
39. Gaffal KP. 2012. How common is the ability of extrafloral nectaries to produce nectar droplets, to secrete nectar during the night and to store starch? Plant Biol. 14:691-95
40. Geneau CE, Wackers FL, Luka H, Balmer O. 2013. Effects of extrafloral and floral nectar of Centaurea cyanus on the parasitoid wasp Microplitis mediator: olfactory attractiveness and parasitization rates. Biol. Contr. 66:16-20
41. Geneau CE, Wackers FL, Luka H, Daniel C, Balmer O. 2012. Selective flowers to enhance biological control of cabbage pests by parasitoids. Basic Appl. Ecol. 13:85-93
42. Gonzalez-TeuberM, Eilmus S, Muck A, Svatos A, Heil M. 2009. Pathogenesis-related proteins protect extrafloral nectar from microbial infestation. Plant J. 58:464-73
43. Gonzalez-Teuber M, Heil M. 2009. Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal. Behav. 4:809-13
44. Gonzalez-Teuber M, Heil M. 2009. The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists. J. Chem. Ecol. 35:459-68
45. Gonzalez-Teuber M, Kaltenpoth M, Boland W. 2014. Mutualistic ants as an indirect defence against leaf pathogens. New Phytol. 202:640-50
46. Gonzalez-Teuber M, Pozo MJ, Muck A, Svatos A, Adame-Alvarez RM, Heil M. 2010. Glucanases and chitinases as causal agents in the protection of Acacia extrafloral nectar from infestation by phytopathogens. Plant Physiol. 152:1705-15
47. Gonzalez-TeuberM, Silva-Bueno JC, BolandW, HeilM. 2012. Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLOS ONE 7:e46598
48. Gouinguene S, Degen T, Turlings TCJ. 2001. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9-16
49. Guillermo-Ferreira R, Cardoso-Leite R, Gandolfo R. 2012. First observation of alternative food usage (extrafloral nectar) by the assassin bug Atopozelus opsimus (Hemiptera, Reduviidae). Revista Brasil. Entomol. 56:489-91
50. Guimaraes PR, Rico-Gray V, dos Reis SF, Thompson JN. 2006. Asymmetries in specialization in antplant mutualistic networks. Proc. R. Soc. Lond. B 273:2041-47
51. Guimaraes PR, Rico-Gray V, Oliveira PS, Izzo TJ, dos Reis SF, Thompson JN. 2007. Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Curr. Biol. 17:1797-803
52. Hagenbucher S, Olson DM, Ruberson JR, Wackers FL, Romeis J. 2013. Resistance mechanisms against arthropod herbivores in cotton and their interactions with natural enemies. Crit. Rev. Plant Sci. 32:458-82
53. Heil M. 2004. Induction of two indirect defences benefits lima bean (Phaseolus lunatus, Fabaceae) in nature. J. Ecol. 92:527-36
54. Heil M. 2008. Indirect defence via tritrophic interactions. New Phytol. 178:41-61
55. Heil M. 2011. Nectar: generation, regulation and ecological functions. Trends Plant Sci. 16:191-200
56. Heil M. 2013. Let the best one stay: Screening of ant defenders by Acacia host plants functions independently of partner choice or host sanctions. J. Ecol. 101:684-88
57. Heil M, Barajas-Barron A, Orona-TamayoD, Wielsch N, Svatos A. 2014. Partnermanipulation stabilises a horizontally transmitted mutualism. Ecol. Lett. 17:185-92
58. Heil M, Fiala B, Baumann B, Linsenmair KE. 2000. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct. Ecol. 14:749-57
59. Heil M, Fiala B, Boller T, Linsenmair KE. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86:146-49
60. Heil M, Greiner S, Meimberg H, Kruger R, Noyer J-L, et al. 2004. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205-8
61. Heil M, Hilpert A, Kruger R, Linsenmair KE. 2004. Competition among visitors to extrafloral nectaries as a source of ecological costs of an indirect defence. J. Trop. Ecol. 20:201-8
62. HeilM, Ibarra-Laclette E, Adame-Alvarez RM, MartinezO, Ramirez-Chavez E, et al. 2012.How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLOS ONE 7:e30537
63. Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE. 2001. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc. Natl. Acad. Sci. USA 98:1083-88
64. Heil M, Kost C. 2006. Priming of indirect defences. Ecol. Lett. 9:813-17
65. Heil M, McKey D. 2003. Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu. Rev. Ecol. Evol. Syst. 34:425-53
66. Heil M, Rattke J, Boland W. 2005. Post-secretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308:560-63
67. Heil M, Silva Bueno JC. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104:5467-72
68. Hernandez LM, Tupac Otero J, Manzano MR. 2013. Biological control of the greenhouse whitefly by Amitus fuscipennis: understanding the role of extrafloral nectaries from crop and non-crop vegetation. Biol. Contr. 67:227-34
69. Hernandez-Cumplido J, Benrey B, Heil M. 2010. Attraction of flower visitors to plants that express indirect defence can minimize ecological costs of ant-pollinator conflicts. J. Trop. Ecol. 26:555-57
70. Hillwig MS, Kanobe C, ThornburgRW, MacIntoshGC. 2011. Identification of S-RNase and peroxidase in petunia nectar. J. Plant Physiol. 168:734-38
71. Holland JN, Chamberlain SA, Horn KC. 2009. Optimal defence theory predicts investment in extrafloral nectar resources in an ant-plant mutualism. J. Ecol. 97:89-96
72. Holland JN, Chamberlain SA, Horn KC. 2010. Temporal variation in extrafloral nectar secretion by reproductive tissues of the senita cactus, Pachycereus schottii (Cactaceae), in the Sonoran Desert of Mexico. J. Arid Environ. 74:712-14
73. Holland JN, Chamberlain SA, Miller TEX. 2011. Consequences of ants and extrafloral nectar for a pollinating seed-consuming mutualism: ant satiation, floral distraction or plant defense? Oikos 120:381-88
74. Horner HT, Healy RA, Ren G, Fritz D, Klyne A, et al. 2007. Amyloplast to chromoplast conversion in developing ornamental tobacco floral nectaries provides sugar for nectar and antioxidants for protection. Am. J. Bot. 94:12-24
75. Huxley CR, Cutler DF. 1991. Ant-Plant Interactions. Oxford, UK: Oxford Univ. Press
76. Izaguirre M, Mazza C, Astigueta M, Ciarla A, Ballare C. 2013. No time for candy: passionfruit (Passiflora edulis) plants down-regulate damage-induced extra floral nectar production in response to light signals of competition. Oecologia 173:213-21
77. Jaber LR, Vidal S. 2009. Interactions between an endophytic fungus, aphids and extrafloral nectaries: Do endophytes induce extrafloral-mediated defences in Vicia faba? Funct. Ecol. 23:707-14
78. Jamont M, Crepelliere S, Jaloux B. 2013. Effect of extrafloral nectar provisioning on the performance of the adult parasitoid Diaeretiella rapae. Biol. Contr. 65:271-77
79. Janzen DH. 1985. On ecological fitting. Oikos 45:308-10
80. Jones ME, Paine TD. 2012. Ants impact sawfly oviposition on bracken fern in Southern California. Arthropod-Plant Interact. 6:283-87
81. Katayama N, Hembry DH, HojoMK, Suzuki N. 2013. Why do ants shift their foraging from extrafloral nectar to aphid honeydew? Ecol. Res. 28:919-26
82. Katayama N, Suzuki N. 2011. Anti-herbivory defense of two Vicia species with and without extrafloral nectaries. Plant Ecol. 212:743-52
83. Keeler KH. 1979. Distribution of plants with extrafloral nectaries and ants at two different elevations in Jamaica. Biotropica 11:152-54
84. KeelerKH.1980. Distribution of plants with extrafloral nectaries in temperate communities. Am.Midland Nat. 104:274-79
85. Koptur S. 1989. Is extrafloral nectar an inducible defense? In The Evolutionary Ecology of Plants, ed. JH Bock, YB Linhart, pp. 323-29. Boulder, CO:Westview
86. Koptur S, Palacios-Rios M, Diaz-Castelazo C, Mackay WP, Rico-GrayV. 2013. Nectar secretion on fern fronds associated with lower levels of herbivore damage: field experiments with a widespread epiphyte of Mexican cloud forest remnants. Ann. Bot. 111:1277-83
87. Koptur S, Rico-Gray V, Palacios-Rios M. 1998. Ant protection of the nectaried fern Polypodium plebeium in Central Mexico. Am. J. Bot. 85:736-39
88. Koricheva J, Romero GQ. 2012. You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants. Biol. Lett. 8:628-30
89. Kost C, Heil M. 2005. Increased availability of extrafloral nectar reduces herbivory in lima bean plants (Phaseolus lunatus, Fabaceae). Basic Appl. Ecol. 6:237-48
90. Kost C, Heil M. 2006. Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J. Ecol. 94:619-28
91. Lach L. 2003. Invasive ants: unwanted partners in ant-plant interactions? Ann. Mo. Bot. Gard. 90:91-108
92. Lach L, Hobbs RJ, Majer JD. 2009. Herbivory-induced extrafloral nectar increases native and invasive ant worker survival. Popul. Ecol. 51:237-43
93. Lach L, Hoffmann BD. 2011. Are invasive ants better plant-defense mutualists? A comparison of foliage patrolling and herbivory in sites with invasive yellow crazy ants and native weaver ants. Oikos 120:9-16
94. Lach L, Tillberg CV, Suarez AV. 2010. Contrasting effects of an invasive ant on a native and an invasive plant. Biol. Invasions 12:3123-33
95. Lanan MC, Bronstein JL. 2013. An ants-eye view of an ant-plant protection mutualism. Oecologia 172:779-90
96. Lee JC, Heimpel GE. 2007. Sugar feeding reduces short-term activity of a parasitoid wasp. Physiol. Entomol. 32:99-103
97. Li T, Holopainen JK, Kokko H, Tervahauta AI, Blande JD. 2012. Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants. Funct. Ecol. 26:1176-85
98. Lin IW, Sosso D, Chen L-Q, Gase K, Kim S-G, et al. 2014. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508:546-49
99. Loughrin J, Manukian A, Heath R, Tumlinson J. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 21:1217-27
100. Lundgren JG, Seagraves MP. 2011. Physiological benefits of nectar feeding by a predatory beetle. Biol. J. Linn. Soc. 104:661-69
101. Luttge U. 2013. Green nectaries: the role of photosynthesis in secretion. Bot. J. Linn. Soc. Lond. 137:1-11
102. Marazzi B, Ane C, Simon MF, Delgado-Salinas A, Luckow M, Sanderson MJ. 2012. Locating evolutionary precursors on a phylogenetic tree. Evolution 66:3918-30
103. Marazzi B, Bronstein J, Koptur S. 2013. The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Ann. Bot. 111:1243-50
104. Marazzi B, Sanderson MJ. 2010. Large-scale patterns of diversification in the widespread legume genus Senna and evolutionary role of extrafloral nectaries. Evolution 64:3570-92
105. MathewsCR, Bottrell DG, BrownMW. 2009. Extrafloral nectaries alter arthropod community structure and mediate peach (Prunus persica) plant defense. Ecol. Appl. 19:722-30
106. Mathews CR, Bottrell DG, Brown MW. 2011. Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on peach (Rosales: Rosaceae). Environ. Entomol. 40:42-51
107. Mathews CR, BrownMW, Bottrell DG. 2007. Leaf extrafloral nectaries enhance biological control of a key economic pest, Grapholita molesta (Lepidoptera: Tortricidae), in peach (Rosales: Rosaceae). Environ. Entomol. 36:383-89
108. Mathur V, Wagenaar R, Caissard J-C, Reddy AS, Vet LEM, et al. 2013. A novel indirect defence in Brassicaceae: structure and function of extrafloral nectaries in Brassica juncea. Plant Cell Environ. 36:528-41
109. McKey D. 1974. Adaptive patterns in alkaloid physiology. Am. Nat. 108:305-20
110. McKeyD. 1979. The distribution of secondary compounds within plants. In Herbivores: Their Interactions with Secondary Plant Metabolites, ed. GA Rosenthal, DH Janzen, pp. 55-133. New York: Academic
111. Melo Y, Machado SR, Alves M. 2010. Anatomy of extrafloral nectaries in Fabaceae from dry-seasonal forest in Brazil. Bot. J. Linn. Soc. Lond. 163:87-98
112. Millan-Canongo C, Orona-Tamayo D, Heil M. 2014. Phloem sugar flux and jasmonic acid-responsive cell wall invertase control extrafloral nectar secretion in Ricinus communis. J. Chem. Ecol. 40:760-769
113. Mondor EB, Addicott JF. 2003. Conspicuous extra-floral nectaries are inducible in Vicia faba. Ecol. Lett. 6:495-97
114. Nahas L, GonzagaMO, Del-Claro K. 2012. Emergent impacts of ant and spider interactions: herbivory reduction in a tropical savanna tree. Biotropica 44:498-505
115. Navarro-Melendez AL, Heil M. 2014. Symptomless endophytic fungi suppress endogenous levels of salicylic acid and interact with the jasmonate-dependent indirect defense traits of their host, Lima bean (Phaseolus lunatus). J. Chem. Ecol. 40:816-25
116. Nepi M, Soligo C, Nocentini D, Abate M, Guarnieri M, et al. 2012. Amino acids and protein profile in floral nectar: much more than a simple reward. Flora 207:475-81
117. Nepi M, von Aderkas P, Wagner R, Mugnaini S, Coulter A, Pacini E. 2009. Nectar and pollination drops: How different are they? Ann. Bot. 104:205-19
118. Ness JH. 2003. Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia 134:210-18
119. Ness JH, Bronstein JL. 2004. The effects of invasive ants on prospective ant mutualists. Biol. Invasions 6:445-61
120. Newman JR, Wagner D. 2013. The influence of water availability and defoliation on extrafloral nectar secretion in quaking aspen (Populus tremuloides). Botany 91:761-67
121. Nicklen EF, Wagner D. 2006. Conflict resolution in an ant-plant interaction: Acacia constricta traits reduce ant costs to reproduction. Oecologia 148:81-87
122. Nicolson SW, Thornburg RW. 2007. Nectar chemistry. In Nectaries and Nectar, ed. SW Nicolson, M Nepi, E Pacini, pp. 215-63. Dordrecht, Neth.: Springer
123. Nieuwenhuis-von Uxkull-Guldenband M. 1907. Extraflorale Zuckerausscheidungen und Ameisenschutz. Ann. Jard. Bot. Buitenzorg, Ser. 2 6:195-328
124. Nogueira A, GuimaraesE, Machado SR, Lohmann LG. 2012.Doextrafloral nectaries present a defensive role against herbivores in two species of the family Bignoniaceae in a Neotropical savannas? Plant Ecol. 213:289-301
125. Oliveira PS, Brandao CRF. 1991. The ant community associated with extrafloral nectaries in the Brazilian cerrados. See Ref. 75, pp. 198-212
126. Olson DM, Wackers FL. 2007. Management of field margins to maximize multiple ecological services. J. Appl. Ecol. 44:13-21
127. Orona-Tamayo D, Wielsch N, Blanco-Labra A, Svatos A, Faria-Rodriguez R, Heil M. 2013. Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock-key system to protect Acacia food bodies from exploitation. Mol. Ecol. 22:4087-100
128. Orona-Tamayo D, Wielsch N, Escalante-Perez M, Svatos A, Molina-Torres J, et al. 2013. Short-term proteomic dynamics reveal metabolic factory for active extrafloral nectar secretion by Acacia cornigera ant-plants. Plant J. 73:546-54
129. Orre-Gordon G, Wratten SD, JonssonM, Simpson M, Hale R. 2013. Attract and reward: combining a herbivore-induced plant volatile with floral resource supplementation-multi-trophic level effects. Biol. Contr. 64:106-15
130. Paiva EAS, Martins LC. 2014. Structure of the receptacular nectary and circadian metabolism of starch in the ant-guarded plant Ipomoea cairica (Convolvulaceae). Plant Biol. 16:244-51
131. Passmore HA, BrunaEM, Heredia SM, VasconcelosHL.2012. Resilient networks of ant-plantmutualists in Amazonian forest fragments. PLOS ONE 7:e40803
132. PembertonRW, Lee JH. 1996. The influence of extrafloral nectaries on parasitism of an insect herbivore. Am. J. Bot. 83:1187-94
133. Pereira MF, Trigo JR. 2013. Ants have a negative rather than a positive effect on extrafloral nectaried Crotalaria pallida performance. Acta Oecol. 51:49-53
134. Pfannenstiel RS, Patt JM. 2012. Feeding on nectar and honeydew sugars improves survivorship of two nocturnal cursorial spiders. Biol. Contr. 63:231-36
135. Philpott SM, Foster PF. 2005. Nest-site limitation in coffee agroecosystems: Artificial nests maintain diversity of arboreal ants. Ecol. Appl. 15:1478-85
136. Piovia-Scott J. 2011. The effect of disturbance on an ant-plant mutualism. Oecologia 166:411-20
137. Portillo N, Alomar O, Wackers F. 2012. Nectarivory by the plant-tissue feeding predator Macrolophus pygmaeus Rambur (Heteroptera: Miridae): nutritional redundancy or nutritional benefit? J. Insect Physiol. 58:397-401
138. Possobom CCF, Guimaraes E, Machado SR. 2010. Leaf glands act as nectaries in Diplopterys pubipetala (Malpighiaceae). Plant Biol. 12:863-70
139. Pulice CE, Packer AA. 2008. Simulated herbivory induces extrafloral nectary production in Prunus avium. Funct. Ecol. 22:801-7
140. Pumarino L, Alomar O, Lundgren JG. 2012. Effects of floral and extrafloral resource diversity on the fitness of an omnivorous bug, Orius insidiosus. Entomol. Exp. Appl. 145:181-90
141. Radhika V, Kost C, Bartram S, Heil M, Boland W. 2008. Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 228:449-57
142. Radhika V, Kost C, BolandW, HeilM. 2010. The role of jasmonate signalling in floral nectar secretion. PLOS ONE 5:e9265
143. RadhikaV, KostC, Mithofer A, BolandW. 2010. Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proc. Natl. Acad. Sci. USA 107:17228-33
144. RhoadesDF. 1979. Evolution of plant chemical defense against herbivores. In Herbivores: Their Interaction with Secondary Plant Metabolites, ed. GA Rosenthal, DH Janzen, pp. 4-53. New York: Academic
145. Rico-Gray V, Diaz-Castelazo C, Ramirez-Hernandez A, Guimaraes PR, Holland JN. 2012. Abiotic factors shape temporal variation in the structure of an ant-plant network. Arthropod-Plant Interact. 6:289-95
146. Rogers WE, Siemann E, Lankau RA. 2003. Damage induced production of extrafloral nectaries in native and invasive seedlings of Chinese tallow tree (Sapium sebiferum). Am. Midl. Nat. 149:413-17
147. RomeroGQ, Koricheva J. 2011. Contrasting cascade effects of carnivores on plant fitness: ameta-analysis. J. Anim. Ecol. 80:696-704
148. Rose USR, Lewis J, Tumlinson JH. 2006. Extrafloral nectar from cotton (Gossypium hirsutum) as a food source for parasitic wasps. Funct. Ecol. 20:67-74
149. Rostas M, Eggert K. 2008. Ontogenetic and spatio-temporal patterns of induced volatiles in Glycine max in the light of the optimal defence hypothesis. Chemoecology 18:29-38
150. Rosumek FB, Silveira FAO, de S Neves F, de U Barbosa NP, Diniz L, et al. 2009. Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537-49
151. Rudgers J, Gardener MC. 2004. Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85:1495-502
152. Rudgers JA. 2004. Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85:192-205
153. Ruhlmann JM, Kram BW, Carter CJ. 2010. CELL WALL INVERTASE 4 is required for nectar production in Arabidopsis. J. Exp. Bot. 61:395-404
154. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. 2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl. Acad. Sci. USA 106:21236-41
155. Savage AM, Rudgers JA. 2013. Non-additive benefit or cost? Disentangling the indirect effects that occur when plants bearing extrafloral nectaries and honeydew-producing insects share exotic ant mutualists. Ann. Bot. 111:1295-307
156. Savage AM, Whitney KD. 2011. Trait-mediated indirect interactions in invasions: unique behavioral responses of an invasive ant to plant nectar. Ecosphere 2:106
157. Schremmer F. 1969. Extranuptiale Nektarien. Beobachtungen an Salix eleagnos Scop. und Pteridium aquilinum (L.) Kuhn. Osterr. Bot. Z. 117:205-22
158. Schupp EW, Feener DH. 1991. Phylogeny, life form, and habitat dependence of ant-defended plants in a Panamanian forest. See Ref. 75, pp. 175-97
159. Seo PJ, Wielsch N, Kessler D, Svatos A, Park CM, et al. 2013. Natural variation in floral nectar proteins of two Nicotiana attenuata accessions. BMC Plant Biol. 13:101
160. Shenoy M, Radhika V, Satish S, Borges RM. 2012. Composition of extrafloral nectar influences interactions between the myrmecophyte Humboldtia brunonis and its ant associates. J. Chem. Ecol. 38:88-99
161. Soren R, Chowdhury S. 2011. Spider nectivory by Phintella vittata Koch (Araneae: Salticidae) from the extrafloral nectaries of Urena lobata L. from the Indian region. Curr. Sci. 100:1123-24
162. Stapel JO, CorteseroAM, DeMoraesCM, Tumlinson JH, LewisWJ. 1997. Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environ. Entomol. 26:617-23
163. Stephenson AG. 1982. The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63:663-69
164. Tempel AS. 1983. Bracken fern (Pteridium aquilinum) and nectar-feeding ants: a nonmutualistic interaction. Ecology 64:1411-22
165. Tobin JE. 1995. Ecology and diversity of tropical forest canopy ants. In Forest Canopies, ed.MDLowman, NM Nadkarni, pp. 129-47. San Diego, CA: Academic
166. Trager MD, Bhotika S, Hostetler JA, AndradeGV, Rodriguez-CabalMA, et al. 2010. Benefits for plants in ant-plant protective mutualisms: a meta-analysis. PLOS ONE 5:e14308
167. Villamil N, Marquez-Guzman J, Boege K. 2013. Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries. Ann. Bot. 112:701-9
168. Wackers FL, Bonifay C. 2004. How to be sweet? Extrafloral nectar allocation by Gossypium hirsutum fits optimal defense theory predictions. Ecology 85:1512-18
169. Wackers FL, van Rijn PCJ, Bruin J. 2005. Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and Its Applications. Cambridge, UK: Cambridge Univ. Press
170. Wackers FL, Wunderlin R. 1999. Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomol. Exp. Appl. 91:149-54
171. Wackers FL, Zuber D, Wunderlin R, Keller F. 2001. The effect of herbivory on temporal and spatial dynamics of foliar nectar production in cotton and castor. Ann. Bot. 87:365-70
172. Wagner D, Nicklen EF. 2010. Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: Does extrafloral nectar attract ant nests and thereby enhance plant nutrition? J. Ecol. 98:614-24
173. Wang Y, Carrillo J, SiemannE, Wheeler GS, Zhu L, et al. 2013. Specificity of extrafloral nectar induction by herbivores differs among native and invasive populations of tallow tree. Ann. Bot. In press
174. Weber MG, Clement WL, Donoghue MJ, Agrawal AA. 2012. Phylogenetic and experimental tests of interactions among mutualistic plant defense traits in Viburnum (Adoxaceae). Am. Nat. 180:450-63
175. WeberMG, Keeler KH. 2013. The phylogenetic distribution of extrafloral nectaries in plants. Ann. Bot. 111:1251-61
176. White RA, Turner MD. 2012. The anatomy and occurrence of foliar nectaries in Cyathea (Cyatheaceae). Am. Fern J. 102:91-113
177. Wilder SM, Eubanks MD. 2010. Extrafloral nectar content alters foraging preferences of a predatory ant. Biol. Lett. 6:177-79
178. Wilder SM, Holway DA, Suarez AV, Eubanks MD. 2011. Macronutrient content of plant-based food affects growth of a carnivorous arthropod. Ecology 92:325-32
179. Wu L, Yun Y, Li J, Chen J, Zhang H, Peng Y. 2011. Preference for feeding on honey solution and its effect on survival, development, and fecundity of Ebrechtella tricuspidata. Entomol. Exp. Appl. 140:52-58
180. Wunderlin R, Keller F, Wackers FL. 1997. A comparison between Spodoptera littoralis (Boisduval) damaged and undamaged Gossypium herbaceum (L.) with respect to sugar composition and concentration of extrafloral nectar. Proc. Sect. Exp. Appl. Entomol. Neth. Entomol. Soc. 8:189-92
181. Zhang L, Cohn NS, Mitchell JP. 1996. Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol. 112:1111-17
182. Zimmermann J. 1932. Uber die extrafloralen Nektarien der Angiosperm. Beih. Bot. Cent. 49:99-196
183. Zimmermann M. 1954. Uber die Sekretion saccharosespaltender Transglucosidasen im pflanzlichen Nektar. Experientia 15:145-46