The role of fetid olfactory signals in the shift to saprophilous fly pollination in Jaborosa (Solanaceae)

  • Marcela MoréEmail author
  • Pablo Mulieri
  • Moira Battán-Horenstein
  • Andrea A. Cocucci
  • Robert A. Raguso
Original Paper


Floral scents can act as important contributing factors to plant reproductive isolation mediated by pollinators. Plants may utilize fetid floral odors that specifically lure saprophilous flies seeking high protein content substrates, such as dung or carrion, to reach sexual maturity or as food sources for their larvae. In this work, we used baits with fetid volatile organic compounds (VOCs) that are produced during the decay of animal protein substrates (oligosulfides and a fermented bone-meal blend) to evaluate the role that olfactory signals may have played in the shift to saprophilous fly pollination in species of the nightshade genus Jaborosa Juss. Traps with the fetid baits attracted the same assemblage of saprophilous fly species that were recorded pollinating the flowers in different populations of the Andean-distributed species J. laciniata, whereas no flies were attracted to the control traps using mineral oil. Furthermore, the addition of oligosulfides to flowers of J. integrifolia, a lowland distributed species pollinated by nocturnal hawkmoths, resulted in the nearly immediate attraction of saprophilous flies (mainly Calliphoridae) to the flowers. These results provide evidence that the emission of fetid floral VOCs is sufficient to attract flies to flowers irrespective of other flower features and geographic region. This suggests that the evolutionary shift to saprophilous fly pollination in the genus Jaborosa could have been initiated with novel floral visitors attracted by the emission of fetid VOCs and then followed by major changes in other flower traits such as corolla color and morphology to optimize pollen export and placement.


Calliphoridae Deceit pollination Floral scent Oligosulfides Sarcophagidae 



This research project was funded by the Agencia Nacional de Promoción Científica y Tecnológica (BID 2008 PICT 620) to M. Moré. The authors acknowledge the assistance of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the Universidad Nacional de Córdoba, both of which support the research facilities.

Supplementary material

11829_2018_9640_MOESM1_ESM.xlsx (33 kb)
Supplementary material 1 (XLSX 32 KB)
11829_2018_9640_MOESM2_ESM.xlsx (30 kb)
Supplementary material 2 (XLSX 30 KB)


  1. Aak A, Knudsen GK, Soleng A (2010) Wind tunnel behavioural response and field trapping of the blowfly Calliphora vicina. Med Vet Entomol 24:250–257PubMedGoogle Scholar
  2. Adams RP (2001) Identification of essential oil components by gas chromatography/quadrupole mass spectrometry. Allured Publishing Corp., Carol StreamGoogle Scholar
  3. Arguello JR, Sellanes C, Lou YR, Raguso RA (2013) Can yeast (S. cerevisiae) metabolic volatiles provide polymorphic signaling? PLoS ONE 8:e70219CrossRefPubMedGoogle Scholar
  4. Armani AP, Dahinten SL, Centeno N (2016) Estudio de descomposición cadavérica en cerdo doméstico (Sus scrofa Linnaeus, 1758) en un ambiente ribereño en la región NO de Chubut, Argentina. Rev Col Entom 43:262–267Google Scholar
  5. 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
  6. Arroyo MT, Muñoz MS, Henríquez C, Till-Bottraud I, Pérez F (2006) Erratic pollination, high selfing levels and their correlates and consequences in an altitudinally widespread above-tree-line species in the high Andes of Chile. Acta Oecol 30:248–257CrossRefGoogle Scholar
  7. Ashman TL, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100:1061–1070CrossRefPubMedGoogle Scholar
  8. Bänziger H, Pape T (2004) Flowers, faeces and cadavers: Natural feeding and laying habits of flesh flies in Thailand (Diptera: Sarcophagidae, Sarcophaga spp.). J Nat Hist 38:1677–1694CrossRefGoogle Scholar
  9. Barboza GE (2013) Jaborosa Juss. Flora Argentina: flora vascular de la República Argentina. In: Barboza GE (ed) Dicotyledoneae: Solanaceae, vol 13. Instituto de Botánica Darwinion, San Isidro, pp 292–309Google Scholar
  10. Barros-Souza SA, Ferreira-Keppler RL, Agra DB (2012) Development period of forensic importance Calliphoridae (Diptera: Brachycera) in urban area under natural conditions in Manaus, Amazonas, Brazil. EntomoBrasilis 5: 99–105CrossRefGoogle Scholar
  11. Bonatto SR (1996) Ciclo de vida de Sarconesia chlorogaster (Wiedemann) (Diptera, Calliphoridae, Toxotarsinae), criada sobcondições de laboratorio em dieta artifical. Rev Bras Zool 13:685–706CrossRefGoogle Scholar
  12. Borg-Karlson AK, Englund FO, Unelius CR (1994) Dimethyl oligosulphides, major volatiles released from Sauromatum guttatum and Phallus impudicus. Phytochemistry 35:321–323CrossRefGoogle Scholar
  13. Castellanos MC, Wilson P, Thomson JD (2004) ‘‘Anti-bee’’ and “pro-bird” changes during the evolution of hummingbird pollination in Penstemon flowers. J Evol Biol 17:876–885CrossRefPubMedGoogle Scholar
  14. Chen G, Ma XK, Jürgens A, Lu J, Liu EX, Sun WB, Cai XH (2015) Mimicking Livor Mortis: a well-known but unsubstantiated color profile in sapromyiophily. J Chem Ecol 41:808–815CrossRefPubMedGoogle Scholar
  15. Cocucci AA (1988) Polinización en solanáceas neotropicales. Doctoral dissertation. Universidad Nacional de Córdoba, Córdoba, ArgentinaGoogle Scholar
  16. Cocucci AA (1999) Evolutionary radiation in neotropical Solanaceae. In: Nee M, Symon DE, Lester RN, Jessop JP (eds) Solanaceae IV. The Royal Botanic Gardens, Kew, pp 9–22Google Scholar
  17. Cruden RW, Kinsman S, Stockhouse RE, Linhart YB (1976) Pollination, fecundity, and the distribution of moth-flowered plants. Biotropica 8:204–210CrossRefGoogle Scholar
  18. Delpino (1867) Sugli apparecchi della fecondazione Nelle Piante Antocarpee (Fanerogame). Firenze, CelliniGoogle Scholar
  19. 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
  20. Freeman GH, Halton JH (1951) Note on an exact treatment of contingency, goodness of fit and other problems of significance. Biometrika 38:141–149CrossRefPubMedGoogle Scholar
  21. Goodrich KR, Raguso RA (2009) The olfactory component of floral display in Asimina and Deeringothamnus (Annonaceae). New Phytol 183:457–469CrossRefPubMedGoogle Scholar
  22. Goodrich KR, Zjhra ML, Ley CA, Raguso RA (2006) When flowers smell fermented: the chemistry and ontogeny of yeasty floral scent in pawpaw (Asimina triloba: Annonaceae). Int J Plant Sci 167:33–46CrossRefGoogle Scholar
  23. Hall MJR (1995) Trapping the flies that cause myiasis: their responses to host-stimuli. Ann Trop Med Parasitol 89:333–357CrossRefPubMedGoogle Scholar
  24. Heinrich B, Casey TM (1973) Metabolic rate and endothermy in sphinx moths. J Comp Physiol 82:195–206CrossRefGoogle Scholar
  25. Hetherington-Rauth MC, Ramírez SR (2015) Evolutionary trends and specialization in the euglossine bee-pollinated orchid genus Gongora. Ann Mo Bot Gard 100:271–299CrossRefGoogle Scholar
  26. Johnson SD, Jürgens A (2010) Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. S Afr J Bot 76:796–807CrossRefGoogle Scholar
  27. Johnson SD, Wester P (2017) Stefan Vogel’s analysis of floral syndromes in the South African flora: an appraisal based on 60 years of pollination studies. Flora. CrossRefGoogle Scholar
  28. Jüergens A, Wee SL, Shuttleworth A, Johnson SD (2013) Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms. Ecol Lett 16:1157–1167CrossRefGoogle Scholar
  29. Jürgens A, Shuttleworth A (2015) Carrion and Dung Mimicry in Plants. In: Benbow ME, Tomberlin JK, Tarone AM (eds) Carrion Ecology, evolution, and their applications. CRC Press, Boca Raton, pp 361–386CrossRefGoogle Scholar
  30. Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytol 172:452–468CrossRefPubMedGoogle Scholar
  31. Kaczorowski R, Seliger AR, Gaskett AC, Wigsten SK, Raguso RA (2012) Corolla shape vs. size in flower choice by a nocturnal hawkmoth pollinator. Funct Ecol 26:577–587CrossRefGoogle Scholar
  32. Kaiser R (2006) Flowers and fungi use scents to mimic each other. Science 311:806–807CrossRefPubMedGoogle Scholar
  33. Kasper J, Hartley S, Schatkowski S, Hoch H (2015) The influence of the physiological stage of Lucilia caesar (L.) (Diptera: Calliphoridae) females on the attraction of carrion odor. J Insect Behav 28:183–201CrossRefGoogle Scholar
  34. Kevan PG (1972) Insect pollination of high arctic flowers. J Ecology 60:831–847CrossRefGoogle Scholar
  35. Mariluis JC, Mulieri PR (2003) La distribución de las Calliphoridae en la Argentina (Diptera). Rev Soc Entomol Argent 62:85–97Google Scholar
  36. Medan D, Montaldo NH, Devoto M, Mantese A, Vasellati V, Roitman GG, Bartoloni NH (2002) Plant-pollinator relationships at two altitudes in the Andes of Mendoza, Argentina. Arct Antarct Alp Res 34:233–241CrossRefGoogle Scholar
  37. Mendes J, Linhares AX (1993) Atratividade por iscas e estágios de desenvolvimento ovariano em várias espécies sinantrópicas de Calliphoridae (Diptera). Rev Bras Entomol 37:157–166Google Scholar
  38. Miller TJ, Raguso RA, Kay KM (2013) Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors. Ann Bot 113:317–329CrossRefPubMedGoogle Scholar
  39. Moré M, Kitching IJ, Cocucci AA (2005) Sphingidae: Esfíngidos de Argentina. Hawkmoths of Argentina. LOLA Literature of Latin America, Buenos AiresGoogle Scholar
  40. Moré M, Cocucci AA, Raguso RA (2013) The importance of oligosulfides in the attraction of fly pollinators to the brood-site deceptive species Jaborosa rotacea (Solanaceae). Int J Plant Sci 174:863–876CrossRefGoogle Scholar
  41. Moré M, Benitez-Vieyra S, Sérsic AN, Cocucci AA (2014) Patrones de depósito de polen sobre el cuerpo de los polinizadores en comunidades esfingófilas de Argentina subtropical. Darwiniana Nueva Serie 2(1):174–196CrossRefGoogle Scholar
  42. Moré M, Cocucci AA, Sérsic AN, Barboza GE (2015) Phylogeny and floral trait evolution in Jaborosa (Solanaceae). Taxon 64:523–534CrossRefGoogle Scholar
  43. Muchhala N (2007) Adaptive trade-off in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds. Am Nat 169:494–504PubMedGoogle Scholar
  44. Mulieri PR, Patitucci LD, Olea MS (2015) Sex-biased patterns of saprophagous Calyptratae (Diptera) collected with different baits of animal origin. J Med Entomol 52:386–393CrossRefPubMedGoogle Scholar
  45. Navarro-Pérez ML, López J, Fernández-Mazuecos M, Rodríguez-Riaño T, Vargas P, Ortega-Olivencia A (2013) The role of birds and insects in pollination shifts of Scrophularia (Scrophulariaceae). Mol Phylogenet Evol 69:239–254CrossRefPubMedGoogle Scholar
  46. Nilsson LA, Rabakonandrianina E (1988) Hawk-moth scale analysis and pollination specialization in the epilithic Malagasy endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae). Bot J Linn Soc 97:49–61CrossRefGoogle Scholar
  47. Okamoto T, Okuyama Y, Goto R, Tokoro M, Kato M (2015) Parallel chemical switches underlying pollinator isolation in Asian Mitella. J Evol Biol 28:590–600CrossRefPubMedGoogle Scholar
  48. Olea MS, Patitucci LD, Mariluis JC, Alderete M, Mulieri PR (2017) Assessment of sampling methods for sarcosaprophagous species and other guilds of Calyptratae (Diptera) in temperate forests of southern South America. J Med Entomol 54:349–362. PubMedGoogle Scholar
  49. Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Ann Bot 103:1471–1480CrossRefPubMedGoogle Scholar
  50. Patitucci LD, Mulieri PR, Schnack JA, Mariluis JC (2011) Species composition and heterogeneity of blowflies assemblages (Diptera: Calliphoridae) in urban-rural gradients at regional scale in Argentinean Patagonia. Stud Neotrop Fauna Environ 46:49–58CrossRefGoogle Scholar
  51. Policha T, Davis A, Barnadas M, Dentinger B, Raguso RA, Roy BA (2016) Disentangling visual and olfactory signals in mushroom-mimicking Dracula orchids using realistic three-dimensional printed flowers. New Phytol 210:1058–1071CrossRefPubMedGoogle Scholar
  52. Renner SS (2006) Rewardless flowers in the angiosperms and the role of insect cognition in their evolution. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 123–144Google Scholar
  53. Sazatornil FD, Moré M, Benitez-Vieyra S, Cocucci AA, Kitching IJ, Schlumpberger BO, Oliveira P, Sazima M, Amorim FW (2016) Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth–plant networks. J Anim Ecol 85(6):1586–1594CrossRefGoogle Scholar
  54. Shuttleworth A, Johnson SD (2008) Bimodal pollination by wasps and beetles in the African milkweed Xysmalobium undulatum. Biotropica 40:568–574CrossRefGoogle Scholar
  55. Shuttleworth A, Johnson SD (2010) The missing stink: sulphur compounds can mediate a shift between fly and wasp pollination systems. Proc R Soc Lond B 277:2811–2819CrossRefGoogle Scholar
  56. Shuttleworth A, Johnson SD, Jürgens A (2017) Entering through the narrow gate: a morphological filter explains specialized pollination of a carrion-scented stapeliad. Flora. CrossRefGoogle Scholar
  57. Stensmyr MC, Urru I, Collu I, Celander M, Hansson BS, Angioy AM (2002) Pollination: rotting smell of dead-horse arum florets. Nature 420:625–626CrossRefPubMedGoogle Scholar
  58. Thomson JD, Wilson P (2008) Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. J Plant Sci 169:23–38CrossRefGoogle Scholar
  59. Urech R, Green PE, Rice MJ, Brown GW, Webb P, Jordan D et al (2009) Suppression of populations of Australian sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae), with a novel blowfly trap. Aust J Entomol 48:182–188CrossRefGoogle Scholar
  60. Urru I, Stensmyr MC, Hansson BS (2011) Pollination by brood-site deception. Phytochemistry 72:1655–1666CrossRefPubMedGoogle Scholar
  61. van der Niet T, Hansen DM, Johnson SD (2011) Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses. Ann Bot 107:981–992CrossRefPubMedGoogle Scholar
  62. Vereecken NJ, McNeil JN (2010) Cheaters and liars: chemical mimicry at its finest. Can J Zool 88:725–752CrossRefGoogle Scholar
  63. Vesprini JL, Galetto L (2000) The reproductive biology of Jaborosa integrifolia (Solanaceae): why its fruits are so rare? Plant Syst Evol 225:15–28CrossRefGoogle Scholar
  64. Vogel S (1954) Blütenbiologische typen als elemente der sippengliederung: dargestellt anhand der Flora Südafrikas. G. Fischer, JenaGoogle Scholar
  65. Vogel S (1978a) Pilsmückenblumen als pilzmimeten, erster Teil. Flora 167:329–366CrossRefGoogle Scholar
  66. Vogel S (1978b) Pilsmückenblumen als pilzmimeten, fortsetzung und schluss. Flora 167:367–398CrossRefGoogle Scholar
  67. Vogel S, Martens J (2000) A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Bot J Linn Soc 133:61–100CrossRefGoogle Scholar
  68. Whitall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–710CrossRefGoogle Scholar
  69. Zito P, Sajeva M, Raspi A, Dötterl S (2014) Dimethyl disulfide and dimethyl trisulfide: so similar yet so different in evoking biological responses in saprophilous flies. Chemoecology 24:261–267CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Instituto Multidisciplinario de Biología Vegetal (CONICET - Universidad Nacional de Córdoba)CórdobaArgentina
  2. 2.Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (CONICET)Buenos AiresArgentina
  3. 3.Instituto de Diversidad y Ecología Animal (CONICET - Universidad Nacional de Córdoba)CórdobaArgentina
  4. 4.Department of Neurobiology and BehaviorCornell UniversityIthacaUSA

Personalised recommendations