Arranging the bouquet of disease: Floral traits and the transmission of plant and animal pathogens

Ecology Letters

Volumn 17, Issue 5, 2014, Pages 624-636

  Mcart, Scott H ^a   Koch, Hauke ^b,c   Irwin, Rebecca E ^d   Adler, Lynn S ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d Lamont Doherty Earth Observatory   (United States)

Author keywords

Bacteria; Fungus; Host; Plant animal interactions; Pollinator decline; Protozoan; Systematic review; Vector; Virus

Indexed keywords

ANIMAL; DISEASE TRANSMISSION; DISEASE VECTOR; FUNGUS; HOST PLANT; HOST-PATHOGEN INTERACTION; PATHOGEN; POLLINATOR; PROTOZOAN;

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI; PROTOZOA;

ANIMAL; ANIMAL DISEASE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; DISEASE CARRIER; DISEASE TRANSMISSION; FLOWER; FUNGUS; HOST; MICROBIOLOGY; NECTAR; PHYSIOLOGY; PLANT; PLANT DISEASE; PLANT-ANIMAL INTERACTIONS; POLLINATOR DECLINE; PROTOZOON; REVIEW; SYSTEMATIC REVIEW; VECTOR; VIROLOGY; VIRUS;

BACTERIA; FUNGUS; HOST; PLANT-ANIMAL INTERACTIONS; POLLINATOR DECLINE; PROTOZOAN; SYSTEMATIC REVIEW; VECTOR; VIRUS;

ANIMAL DISEASES; ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; DISEASE VECTORS; FLOWERS; FUNGI; PLANT DISEASES; PLANT NECTAR; PLANTS;

EID: 84898058230     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12257     Document Type: Review

References (100)

1. Adler, L.S. & Irwin, R.E. (2005). Ecological costs and benefits of defenses in nectar. Ecology, 86, 2968-2978.
2. Adler, L.S., Seifert, M.G., Wink, M. & Morse, G.E. (2012). Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol. Lett., 15, 1140-1148.
3. Alaux, C., Brunet, J.-L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M. et al. (2010). Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol., 12, 774-782.
4. Alexander, H.M. (1989). An experimental field study of anther-smut disease of Silene alba caused by Ustilago violacea: genotypic variation and disease incidence. Evolution, 43, 835-847.
5. Alexander, H.M. (1990). Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence. J. Ecol., 78, 166-179.
6. Alexander, H.M. & Antonovics, J. (1988). Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago violacea. J. Ecol., 76, 91.
7. Alexander, H.M. & Antonovics, J. (1995). Spread of anther-smut disease (Ustilago violacea) and character correlations in a genetically variable experimental population of Silene alba. J. Ecol., 83, 783-794.
8. Alexander, H.M. & Maltby, A. (1990). Anther-smut infection of Silene alba caused by Ustilago violacea: factors determining fungal reproduction. Oecologia, 84, 249-253.
9. Alexandrova, M., Cimini, B., Carpana, E., Massi, S., Sabatini, A.G. & Bazzi, C. (2002). The role of honeybees in spreading Erwinia amylovora. Acta Horticulturae, 590, 55-60.
10. Antonovics, J., Hood, M. & Partain, J. (2002). The ecology and genetics of a host shift: microbotryum as a model system. Am. Nat., 160, S40-S53.
11. Bailey, L. (1975). Recent research on honeybee viruses. Bee World, 56, 55-64.
12. Batra, L.R. (1983). Monilinia vaccinii-corymbosi (Sclerotiniaceae): its biology on blueberry and comparison with related species. Mycologia, 75, 131-152.
13. Batra, L.R. & Batra, S.W.T. (1985). Floral mimicry induced by mummy-berry fungus exploits host's pollinators as vectors. Science, 228, 1011-1013.
14. Batra, L.R., Batra, S.W.T. & Bohart, G.E. (1973). The mycoflora of domesticated and wild bees (Apoidea). Mycopathologia et Mycologia Applicata, 49, 13-44.
15. Biere, A. & Antonovics, J. (1996). Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution, 50, 1098-1110.
16. Biere, A. & Honders, S.J. (1996a). Host adaptation in the anther smut fungus Ustilago violacea (Microbotryum violaceum): infection success, spore production and alteration of floral traits on two host species and their F1-hybrid. Oecologia, 107, 307-320.
17. Biere, A. & Honders, S.J. (1996b). Impact of flowering phenology of Silene alba and S. dioica on susceptibility to fungal infection and seed predation. Oikos, 77, 467-480.
18. Biere, A. & Honders, S.C. (2006). Coping with third parties in a nursery pollination mutualism: hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia. New Phytol., 169, 719-727.
19. Blacquiere, T., Smagghe, G., van Gestel, C.A.M. & Mommaerts, V. (2012). Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology, 21, 973-992.
20. Bristow, P.R. & Martin, R.R. (1999). Transmission and the role of honeybees in field spread of blueberry shock ilarvirus, a pollen-borne virus of highbush blueberry. Phytopathology, 89, 124-130.
21. Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F. et al. (2011). Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA, 108, 662-667.
22. Card, S.D., Pearson, M.N. & Clover, G.R.G. (2007). Plant pathogens transmitted by pollen. Australas. Plant Pathol., 36, 455-461.
23. Carter, C., Healy, R., O'Tool, N.M., Naqvi, S.M.S., Ren, G., Park, S. et al. (2007). Tobacco nectaries express a novel NADPH oxidase implicated in the defense of floral reproductive tissues against microorganisms. Plant Physiol., 143, 389-399.
24. Colla, S.R., Otterstatter, M.C., Gegear, R.J. & Thomson, J.D. (2006). Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol. Conserv., 129, 461-467.
25. Dedej, S., Delaplane, K.S. & Scherm, H. (2004). Effectiveness of honey bees in delivering the biocontrol agent Bacillus subtilis to blueberry flowers to suppress mummy berry disease. Biol. Control, 31, 422-427.
26. Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F. et al. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. USA, 110, 18466-18471.
27. Dotterl, S., Jurgens, A., Wolfe, L. & Biere, A. (2009). Disease status and population origin effects on floral scent: potential consequences for oviposition and fruit predation in a complex interaction between a plant, fungus, and Noctuid moth. J. Chem. Ecol., 35, 307-319.
28. Durrer, S. & Schmid-Hempel, P. (1994). Shared use of flowers leads to horizontal pathogen transmission. Proc. Royal Soc. B-Biol. Sci., 258, 299-302.
29. Eisikowitch, D., Lachance, M.A., Kevan, P.G., Willis, S. & Collinsthompson, D.L. (1990). The effect of the natural assemblage of microorganisms and selected strains of the yeast Metschnikowia reukaufii in controlling the germination of pollen of the common milkweed Asclepias syriaca. Canadian J. Botany-Revue Canadienne De Botanique, 68, 1163-1165.
30. Elmqvist, T., Liu, D., Carlsson, U. & Giles, B.E. (1993). Anther-smut infection in Silene dioica: variation in floral morphology and patterns of spore deposition. Oikos, 68, 207-216.
31. Evison, S.E.F., Roberts, K.E., Laurenson, L., Pietravalle, S., Hui, J., Biesmeijer, J.C. et al. (2012). Pervasiveness of parasites in pollinators. PLoS ONE, 7, e30641.
32. Farkas, A., Mihalik, E., Dorgai, L. & Buban, T. (2011). Floral traits affecting fire blight infection and management. Trees, 26, 1-20.
33. Foster, W.A. (1995). Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol., 40, 443-474.
34. Fouks, B. & Lattorff, H.M.G. (2011). Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS ONE, 6, e26328.
35. Ganter, P.F. (2006). Yeast and invertebrate associations. In: Biodiversity and Ecophysiology of Yeasts. (ed Rosa, C.A. and Gabor, P.). Springer-Verlag, Berlin, pp. 303-370.
36. Genersch, E. & Aubert, M. (2010). Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet. Res., 41, art. no. 54. DOI: 10.1051/vetres/2010027.
37. Golonka, A.M. (2002). Nectar-Inhabiting Microorganisms and the Dioecious Plant Species Silene Latifolia. Duke University Durham, NC.
38. Heil, M. (2011). Nectar: generation, regulation, and ecological functions. Trends Plant Sci., 16, 191-200.
39. Herrera, C.M., de Vega, C., Canto, A. & Pozo, M.I. (2009). Yeasts in floral nectar: a quantitative survey. Ann. Bot., 103, 1415-1423.
40. Herrera, C.M., Pozo, M.I. & Medrano, M. (2013). Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology, 94, 273-279.
41. Huang, M., Sanchez-Moreiras, A.M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J. et al. (2012). The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol., 193, 997-1008.
42. Imhoof, B. & Schmid-Hempel, P. (1999). Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Soc., 46, 233-238.
43. Jennersten, O. (1988). Insect dispersal of fungal disease: effects of Ustilago infection on pollinator attraction in Viscaria vulgaris. Oikos, 51, 163-170.
44. Jennersten, O. & Kwak, M.M. (1991). Competition for bumblebee visitation between Melampyrum pratense and Viscaria vulgaris with healthy and Ustilago-infected flowers. Oecologia, 86, 88-98.
45. Kaltz, O. & Shykoff, J.A. (2001). Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. J. Ecol., 89, 99-109.
46. Knudsen, J.T., Eriksson, R., Gershenzon, J. & Stahl, B. (2006). Diversity and distribution of floral scent. Bot. Rev., 72, 1-120.
47. Lara, C. & Ornelas, J.F. (2003). Hummingbirds as vectors of fungal spores in Moussonia deppeana (Gesneriaceae): taking advantage of a mutualism? Am. J. Bot., 90, 262-269.
48. Le Gac, M., Hood, M.E., Fournier, E., Giraud, T. & Hollocher, H. (2007). Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution, 61, 15-26.
49. Lee, J.A. (1981). Variation in the Infection of Silene dioica (L.) Clairv. by Ustilago violacea (Pers.) Fuckel in North West England. New Phytol., 87, 81-89.
50. Lehman, J.S., Igarashi, S. & Oudemans, P.V. (2007). Host resistance to Monilinia vaccinii-corymbosi in flowers and fruits of highbush blueberry. Plant Dis., 91, 852-856.
51. Li, J., Qin, H., Wu, J., Sadd, B.M., Wang, X., Evans, J.D. et al. (2012). The prevalence of parasites and pathogens in Asian honeybees Apis cerana in China. PLoS ONE, 7, e47955.
52. Lindh, J.M., Terenius, O., Eriksson-Gonzales, K., Knols, B.G.J. & Faye, I. (2006). Re-introducing bacteria in mosquitoes - A method for determination of mosquito feeding preferences based on coloured sugar solutions. Acta Trop., 99, 173-183.
53. Louda, S.M. (1982). Inflorescence spiders - a cost-benefit-analysis for the host plant, Haplopappus-venetus Blake (Asteraceae). Oecologia, 55, 185-191.
54. Manda, H., Gouagna, L.C., Foster, W.A., Jackson, R.R., Beier, J.C., Githure, J.I. et al. (2007). Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malaria J., 6, art. no. 113. DOI: 10.1186/1475-2875-6-113.
55. Manson, J.S., Otterstatter, M.C. & Thomson, J.D. (2010). Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia, 162, 81-89.
56. Mao, W., Schuler, M.A. & Berenbaum, M.R. (2013). Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc. Natl. Acad. Sci. USA, 110, 8842-8846.
57. McCall, A.C. & Irwin, R.E. (2006). Florivory: the intersection of pollination and herbivory. Ecol. Lett., 9, 1351-1365.
58. McClellan, W. & Hewitt, W. (1973). Early Botrytis rot of grapes: time of infection and latency of Botrytis cinerea Pers. in Vitis vinifera L. Phytopathology, 63, 1151-1157.
59. McFrederick, Q.S., Wcislo, W.T., Taylor, D.R., Ishak, H.D., Dowd, S.E. & Mueller, U.G. (2012). Environment or kin: whence do bees obtain acidophilic bacteria? Mol. Ecol., 21, 1754-1768.
60. Meeus, I., Vercruysse, V. & Smagghe, G. (2012). Molecular detection of Spiroplasma apis and Spiroplasma melliferum in bees. J. Invertebr. Pathol., 109, 172-174.
61. Mouches, C., Bove, J.M. & Albisetti, J. (1984). Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in Southwestern France. Ann. Microbiol, 135, 151-155.
62. Naef, A., Roy, B.A., Kaiser, R. & Honegger, R. (2002). Insect-mediated reproduction of systemic infections by Puccinia arrhenatheri on Berberis vulgaris. New Phytol., 154, 717-730.
63. Ngugi, H.K. & Scherm, H. (2004). Pollen mimicry during infection of blueberry flowers by conidia of Monilinia vaccinii-corymbosi. Physiol. Mol. Plant Pathol., 64, 113-123.
64. Ngugi, H.K., Scherm, H. & Lehman, J.S. (2002). Relationships between blueberry flower age, pollination, and conidial infection by Monilinia vaccinii-corymbosi. Phytopathology, 92, 1104-1109.
65. Palmer, M.J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G.A. & Connolly, C.N. (2013). Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun., 4, 1634.
66. Patt, J.M. (1992). Floral Odors as Gender Recognition Cues in an Aroid-Fly Mutualism. Rutgers Piscataway, New Jersey, USA.
67. Pellmyr, O. & Thien, L.B. (1986). Insect reproduction and floral fragrances - keys to the evolution of the Angiosperms. Taxon, 35, 76-85.
68. Pfunder, M. & Roy, B.A. (2000). Pollinator-mediated interactions between a pathogenic fungus, Uromyces pisi (Pucciniaceae), and its host plant, Euphorbia cyparissias (Euphorbiaceae). Am. J. Bot., 87, 48-55.
69. Pusey, P.L. (1999). Effect of nectar on microbial antagonists evaluated for use in control of fire blight of pome fruits. Phytopathology, 89, 39-46.
70. Pusey, P.L. & Smith, T.J. (2007). Relation of apple flower age to infection of hypanthium by Erwinia amylovora. Plant Dis., 92, 137-142.
71. van Putten, W.F., Elzinga, J.A. & Biere, A. (2007). Host fidelity of the pollinator guilds of Silene dioica and Silene latifolia: possible consequences for sympatric host race differentiation of a vectored plant disease. Int. J. Plant Sci., 168, 421-434.
72. Raguso, R.A. & Roy, B.A. (1998). 'Floral' scent production by Puccinia rust fungi that mimic flowers. Mol. Ecol., 7, 1127-1136.
73. Raju, B.C., Nyland, G., Meikle, T. & Purcell, A.H. (1981). Helical, motile mycoplasmas associated with flowers and honey bees in California. Can. J. Microbiol., 27, 249-253.
74. de Roode, J.C., Lefevre, T. & Hunter, M.D. (2013). Self-medication in animals. Science, 340, 150-151.
75. Roy, B.A. (1993). Floral mimicry by a plant pathogen. Nature, 362, 56-58.
76. Roy, B.A. (1994). The effects of pathogen-induced pseudoflowers and buttercups on each other's insect visitation. Ecology, 75, 352-358.
77. Roy, B.A. & Raguso, R.A. (1997). Olfactory versus visual cues in a floral mimicry system. Oecologia, 109, 414-426.
78. Roy, B.A., Vogler, D.R., Bruns, T.D. & Szaro, T.M. (1998). Cryptic species in the Puccinia monoica complex. Mycologia, 90, 846-853.
79. Salathe, R.M. & Schmid-Hempel, P. (2011). The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. PLoS ONE, 6, e22054.
80. Sasu, M.A., Seidl-Adams, I., Wall, K., Winsor, J.A. & Stephenson, A.G. (2010a). Floral transmission of Erwinia tracheiphila by cucumber beetles in a wild Cucurbita pepo. Environ. Entomol., 39, 140-148.
81. Sasu, M.A., Wall, K.L. & Stephenson, A.G. (2010b). Antimicrobial nectar inhibits a florally transmitted pathogen of a wild Cucurbita pepo (Cucurbitaceae). Am. J. Bot., 97, 1025-1030.
82. Schaeffer, R.N. & Irwin, R.E. (in press). Yeasts in nectar enhance male fitness in a montane perennial herb. Ecology, doi: 10.1890/13-740.1.
83. Schafer, A.M., Kemler, M., Bauer, R. & Begerow, D. (2010). The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Botany-Botanique, 88, 875-885.
84. Shykoff, J.A. & Bucheli, E. (1995). Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal disease of plants. J. Ecol., 83, 189-198.
85. Shykoff, J.A. & Kaltz, O. (1998). Phenotypic changes in host plants diseased by Microbotryum violaceum: parasite manipulation, side effects, and trade-offs. Int. J. Plant Sci., 159, 236-243.
86. Shykoff, J.A., Bucheli, E. & Kaltz, O. (1996). Flower lifespan and disease risk. Nature, 379, 779.
87. Shykoff, J.A., Bucheli, E. & Kaltz, O. (1997). Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits. Evolution, 51, 383-392.
88. Singh, R., Levitt, A.L., Rajotte, E.G., Holmes, E.C., Ostiguy, N., vanEngelsdorp, D. et al. (2010). RNA viruses in Hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis Hymenopteran species. PLoS ONE, 5, e14357.
89. Stephen, W.P., Vandenberg, J.D. & Fichter, B.L. (1981). Etiology and Epizootiology of Chalkbrood in the Leafcutting Bee, Megachile Rotundata (Fabricius), with Notes on Ascosphaera Species. Oregon State University, Corvallis, Ore, Agricultural Experiment Station.
90. Stephenson, A.G. (2012). Safe sex in plants. New Phytol., 193, 827-829.
91. Stone, C.M., Jackson, B.T. & Foster, W.A. (2012). Effects of plant-community composition on the vectorial capacity and fitness of the malaria mosquito Anopheles gambiae. Am. J. Trop. Med. Hyg., 87, 727-736.
92. Stoner, K.A. & Eitzer, B.D. (2012). Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS ONE, 7, e39114.
93. Strauss, S.Y. & Whittall, J.B. (2006). Non-pollinator agents of selection on floral traits. In: Ecology and Evolution of Flowers (eds Harder, L.D., Barrett, S.C.H.). Oxford University Press, Oxford, pp. 120-138.
94. Thomson, S.V. & Gouk, S.C. (2003). Influence of age of apple flowers on growth of Erwinia amylovora and biological control agents. Plant Dis., 87, 502-509.
95. Thornburg, R.W., Carter, C., Powell, A., Mittler, R., Rizhsky, L. & Horner, H.T. (2003). A major function of the tobacco floral nectary is defense against microbial attack. Plant Syst. Evol., 238, 211-218.
96. Thrall, P.H. & Jarosz, A.M. (1994). Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. J. Ecol., 82, 549-559.
97. Thrall, P.H., Biere, A. & Antonovics, J. (1993). Plant life-history and disease susceptibility-the occurrence of Ustilago violacea on different species within the Caryophyllaceae. J. Ecol., 81, 489-498.
98. Vannette, R.L., Gauthier, M.-P.L. & Fukami, T. (2013). Nectar bacteria, but not yeast, weaken a plant-pollinator mutualism. Proc. Royal Soc. B: Biol. Sci., 280, 20122601.
99. Vasquez, A., Forsgren, E., Fries, I., Paxton, R.J., Flaberg, E., Szekely, L. et al. (2012). Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE, 7, e33188.
100. Wardhaugh, C.W., Stork, N.E., Edwards, W. & Grimbacher, P.S. (2012). The overlooked biodiversity of flower-visiting invertebrates. PLoS ONE, 7, e45796.