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Abstract
The pollen grains of Leiotulus aureus (syn. Malabaila aurea (Sm.) Boiss.) were examined by light and scanning electron microscopy in order to contribute to the taxonomical and melissopalynological studies of the species. Flower visitors have also been observed and analyzed aiming at the clarification of some pollination aspects including the species contribution to bee pasture. The pollen grains of L. aureus are isopolar, radially symmetrical, medium to large in size, tri- colporate and perprolate. They are slightly equatorially constricted with obtuse polar caps and triangular in polar view. The sculpturing pattern is rugulate–microperforate. With regard to flower visitors, the following pollination types oc- curred: melittophily, myophily and sapromyophily and cantharophily. Some insects attracted by L. aureus cannot be con- sidered pollinators but casual visitors. The flowers were the most frequently visited by honey bees during midday.
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Copyright (c) 2023 Marina Mačukanović-Jocić, DANIJELA STEŠEVIĆ, Dragana Rancic, Miloje ŠUNDIĆ
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References
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- Beug, J.-H., 2015: Leitfaden der Pollenbestimmung für Mittel- europa und angrenzende Gebiete, 2nd Edition, Verlag Dr. Friedrich Pfeil, München.
- Bouchard, P., Bousquet, Y. Davies, A.E., Alonso-Zarazaga, M.A., Lawrence, J.F., Lyal, C.H.C., Newton, A.F., Reid, C.A.M., Schmitt, M., Ślipiński, S.A., Smith A.B.T., 2011: Family-group names in Coleoptera (Insecta). ZooKeys 88, 1–972.
- Carvalheiro, L.G., Barbosa, E.R.M., Memmott, J., 2008: Pollina- tor networks, alien species and the conservation of rare plants: Trinia glauca as a case study. Journal of Applied Ecol- ogy 45, 1419–1427.
- Cassis, G., Schuh, R.T., 2012: Systematics, biodiversity, biogeo- graphy, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annual Review of Entomology 57, 377–404.
- Cerceau-Larrival, M.T., 1962: Le pollen d’Ombellifères Méditer- ranéennes. Pollen et spores 4, 955–104.
- Cerceau-Larrival, M.T., 1981: World Pollen and Spore Flora 9. Umbelliferae Juss. Hydrocotyloideae Drude/Hydrocotyleae Drude. Almqvist and Wiksell, Stockholm.
- Dafni, H., Lenski, Y., Fahn, A., 1988: Flower and nectar charac- teristics of nine species of Labiatae and their influence on honeybee visits. Journal of Apicultural Research 27, l03–114.
- Davila, Y.C., Wardle, G.M., 2002: Reproductive ecology of the Australian herb Trachymene incisa subsp. incisa (Apiaceae). Australian Journal of Botany 50, 619–626.
- Davila, Y.C., Wardle, G.M., 2008: Variation in native pollinators in the absence of honeybees: implications for reproductive success of an Australian generalist pollinated herb Trachymene incia (Apiaceae). Botanical Journal of the Linnean Society 156, 479– 490.
- Downie, S.R., Spalik, K., Katz-Downie, D.S., Reduron, J.-P., 2010: Major clades within Apiaceae subfamily Apioideae as in- ferred by phylogenetic analysis of nrDNA ITS sequences. Plant Diversity and Evolution 128, 111–136.
- Dustmann, JH., von Der Ohe, K., 1993: Scanning electron mi- croscopic studies on pollen from honey. IV. Surface pattern of pollen of Sapium sebiferum and Euphorbia spp. (Euphor- biaceae) . Apidologie 24, 59–66.
- Erdtman, G., 1971: Pollen morphology and plant taxonomy (An- giosperms). Hafner Publishing Company, New York.
- Faegri K., Iversen J. 1989 Textbook of pollen analysis. In: Faegri, K., Kakand, P.E., Krzywinski, K. (ed.) 4th Edition. John Wi- ley and Sons, Chichester.
- Freeman, P., Lane, R.P., 1985: Bibionid and scatopsid flies. Dip- tera: Bibionidae & Scatopsidae. Handbook for the Identifica- tion of British Insects 9/7: 1–74.
- Goldblatt, P., Manning, J.C., Bernhardt, P., 2005: Observations on the floral biology of Melasphaerula (Iridaceae): Is this monotypic genus pollinated by march flies (Diptera: Bibi- onidae). Annals of the Missouri Botanical Garden 92, 268– 274.
- Ishida, C., Kono, M., Sakai, S., 2009: A new pollination system: brood-site pollination by flower bugs in Macaranga (Euphor- biaceae). Annals of Botany 103, 39–44.
- Koul, P., Sharma, N., Koul, A.K., 1993: Pollination biology of Apiaceae. Current Science 65, 219–222.
- Lamborn, E., Ollerton, J., 2000: Experimental assessment of the functional morphology of inflorescences of Daucus carota (Apiaceae): testing the ‘fly catcher effect’. Functional Ecology 14, 445–454.
- Langenberger, M.W., Davis, A.R., 2002a: Temporal changes in floral nectar production, reabsorption, and composition as- sociated with dichogamy in annual caraway (Carum carvi, Apiaceae). American Journal of Botany 89, 1588–1598.
- Langenberger, M.W., Davis, A.R., 2002b: Honey bee pollen for- aging in relation to flowering phenology of biennial caraway (Carum carvi L.). Canadian Journal of Plant Science 82, 203– 215.
- Lindsey, A.H., 1984: Reproductive biology of Apiaceae. I. Floral visitors to Thaspium and Zizia and their importance in pollination. American Journal of Botany 71, 375–387.
- Lindsey, A.H., Bell, C.R., 1985: Reproductive biology of Apiaceae. II. Cryptic specialization and floral evolution in Thaspium and Zizia. American Journal of Botany 72, 231–247.
- Lupoli, R. 2017: Graphosoma lineatum (L., 1758) and G. italicum (O.F. Müller, 1766), two valid and distinct species, probably derived from the Zanclean mediterranean transgression (Hemiptera Pentatomidae). L’Entomologiste 73, 19–33.
- Mačukanović-Jocić, M., 2010: The Biology of Melliferous Plants with an Atlas of Serbian Apiflora. Monographic Study. Faculty of Agriculture University of Belgrade, Belgrade.
- Mačukanović-Jocić, M., Stešević, D., Rančić, D., Dajić Stevanović, Z., 2016: Pollen morphology and the flower vis- itors of Chaerophyllum coloratum L. (Apiaceae), Acta Bo- tanica Croatica 76, 1–8.
- Menemen, Y., Jury, S., 2001: A systematic study of the genus Malabaila Hoffm. (Umbelliferae) comparing with the closely related genera. In: Gozukkimizi, N. (ed.), The Proceedings of the 2nd Balkan Botanical Congress, 299–312. Marmara University, Istanbul.
- Niemirski, R., Zych, M., 2011: Fly pollination of dichogamous Angelica sylvestris (Apiaceae): How (functionally) specialized can a (morphologically) generalized plant be? Plant Sys- tematics and Evolution 2294, 147–158.
- Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P., 2007: The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 104, 19891–19896.
- Oosterbroek, P. 2006: The European families of the Diptera: identification, diagnosis, biology Utrecht: KNNV, Publi- shing. 205. pp.
- Perveen, A., Qaiser, M., 2006: Pollen Flora of Pakistan XLVIII. Umbelliferae. Pakistan Journal of Botany 38, 1–14.
- Pimenov, M., Ostroumova, T., 1994: The genus Malabaila Hof- fm. (Umbelliferae:Tordylieae): A carpological investigation and taxonomic implication. Feddes Repertorium 105, 141–155.
- Pospiech M, Javůrková Z, Hrabec P, Štarha P, Ljasovská S, Bednář J, Tremlová B. Identification of pollen taxa by differ- ent microscopy techniques. PLoS One. 2021. 16(9):e0256808.
- POWO 2022: Plants of the World Online. Facilitated by the Roy- al Botanic Gardens, Kew. Retrived 19 September 2022 from http://www.plantsoftheworldonline.org/
- Proctor, M., Yeo, P., Lack, A., 1996: The natural history of pol- lination. HarperCollins Publishers, London, UK.
- Punt, W., 1984: The Northwest European Pollen Flora, 37 Um- belliferae. Review of Palaeobotany and Palynology 42, 155– 364.
- Punt. W., Hoen, P.P., Blackmore, S., Nilsson, S., Le Thomas, A., 2007: Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143, 1–81.
- Rovira, A.M., Bosch, M., Molero, J., Blanche, C., 2002: Pollina- tion ecology and breeding system of the very narrow coastal endemic Seseli farrenyi (Apiaceae). Effects of population fragmentation. Nordic Journal of Botany 22, 727–740.
- Sivell, O. 2021: Blow flies (Diptera: Calliphoridae, Polleniidae, Rhiniidae). Handbook for the Identification of British In- sects 10/16, 1–206.
- Tollsten, L., Knudsen, J.T., Bergström, LG., 1994: Floral scent in generalistic Angelica (Apiaceae) – an adaptive character? Biochemical Systematics and Ecology 22, 161–169.
- Tollsten, L., Øvstedal, D.O., 1994: Differentiation in floral scent chemistry among populations of Conopodium majus (Apia- ceae). Nordic Journal of Botany 14, 361–368.
- Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., 1981: Flora Europaea. Volume 2. Rosaceae to Umbelliferae (3rd ed.). Cambridge University Press, Cambridge.
- Van Veen, M.P. 2004: Hoverflies of Northwest Europe, Identifi- cation Keys to the Syrphidae (Hardback). KNNV Publi- shing, Utrecht.
- Van Zeist, W., Bottema, S., 1977: Palynological investigation in western Iran. Paleohistoria 19, 19–85.
- Vazquez, X. A., 2002: European Fauna of Oedemeridae. Argania editio, Barcelona.
- Woodcock, T.S., Larson, B.M.H., Kevan, P.G., Inouye, D.W., Lunau, K., 2014: Flies and flowers II: floral attractants and rewards. Journal of Plant Ecology 12, 63–94.
- Wróblewska, A., 1993: Flowering and pollen value of selected species of umbelliferous family - Umbelliferae Juss. (Apia- ceae Lindl.) in Lublin region. Part II. Pollen efficiency and insect visit. Acta Agrobotanica 46, 51–65. (in Polish).
- Zych, M., 2006: Diurnal activity of the key pollinators of Heracleum sphondylium L. (Apiaceae). Acta Agrobotanica 59, 279–288.
- Zych, M., 2007: On flower visitors and true pollinators: The case of protoandrous Heracleum spondylium L. (Apiaceae), Plant Systematics and Evolution 263, 159–179.
References
Ajani, Y., Ajan, A., Cordes, J.M., Watson, M.F., Downie, S.R., 2008: Phylogenetic analysis of nrDNA ITS sequences reveals relationships within five groups of Iranian Apiaceae subfam- ily Apioideae. Taxon 57, 383–401.
Beug, J.-H., 2015: Leitfaden der Pollenbestimmung für Mittel- europa und angrenzende Gebiete, 2nd Edition, Verlag Dr. Friedrich Pfeil, München.
Bouchard, P., Bousquet, Y. Davies, A.E., Alonso-Zarazaga, M.A., Lawrence, J.F., Lyal, C.H.C., Newton, A.F., Reid, C.A.M., Schmitt, M., Ślipiński, S.A., Smith A.B.T., 2011: Family-group names in Coleoptera (Insecta). ZooKeys 88, 1–972.
Carvalheiro, L.G., Barbosa, E.R.M., Memmott, J., 2008: Pollina- tor networks, alien species and the conservation of rare plants: Trinia glauca as a case study. Journal of Applied Ecol- ogy 45, 1419–1427.
Cassis, G., Schuh, R.T., 2012: Systematics, biodiversity, biogeo- graphy, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annual Review of Entomology 57, 377–404.
Cerceau-Larrival, M.T., 1962: Le pollen d’Ombellifères Méditer- ranéennes. Pollen et spores 4, 955–104.
Cerceau-Larrival, M.T., 1981: World Pollen and Spore Flora 9. Umbelliferae Juss. Hydrocotyloideae Drude/Hydrocotyleae Drude. Almqvist and Wiksell, Stockholm.
Dafni, H., Lenski, Y., Fahn, A., 1988: Flower and nectar charac- teristics of nine species of Labiatae and their influence on honeybee visits. Journal of Apicultural Research 27, l03–114.
Davila, Y.C., Wardle, G.M., 2002: Reproductive ecology of the Australian herb Trachymene incisa subsp. incisa (Apiaceae). Australian Journal of Botany 50, 619–626.
Davila, Y.C., Wardle, G.M., 2008: Variation in native pollinators in the absence of honeybees: implications for reproductive success of an Australian generalist pollinated herb Trachymene incia (Apiaceae). Botanical Journal of the Linnean Society 156, 479– 490.
Downie, S.R., Spalik, K., Katz-Downie, D.S., Reduron, J.-P., 2010: Major clades within Apiaceae subfamily Apioideae as in- ferred by phylogenetic analysis of nrDNA ITS sequences. Plant Diversity and Evolution 128, 111–136.
Dustmann, JH., von Der Ohe, K., 1993: Scanning electron mi- croscopic studies on pollen from honey. IV. Surface pattern of pollen of Sapium sebiferum and Euphorbia spp. (Euphor- biaceae) . Apidologie 24, 59–66.
Erdtman, G., 1971: Pollen morphology and plant taxonomy (An- giosperms). Hafner Publishing Company, New York.
Faegri K., Iversen J. 1989 Textbook of pollen analysis. In: Faegri, K., Kakand, P.E., Krzywinski, K. (ed.) 4th Edition. John Wi- ley and Sons, Chichester.
Freeman, P., Lane, R.P., 1985: Bibionid and scatopsid flies. Dip- tera: Bibionidae & Scatopsidae. Handbook for the Identifica- tion of British Insects 9/7: 1–74.
Goldblatt, P., Manning, J.C., Bernhardt, P., 2005: Observations on the floral biology of Melasphaerula (Iridaceae): Is this monotypic genus pollinated by march flies (Diptera: Bibi- onidae). Annals of the Missouri Botanical Garden 92, 268– 274.
Ishida, C., Kono, M., Sakai, S., 2009: A new pollination system: brood-site pollination by flower bugs in Macaranga (Euphor- biaceae). Annals of Botany 103, 39–44.
Koul, P., Sharma, N., Koul, A.K., 1993: Pollination biology of Apiaceae. Current Science 65, 219–222.
Lamborn, E., Ollerton, J., 2000: Experimental assessment of the functional morphology of inflorescences of Daucus carota (Apiaceae): testing the ‘fly catcher effect’. Functional Ecology 14, 445–454.
Langenberger, M.W., Davis, A.R., 2002a: Temporal changes in floral nectar production, reabsorption, and composition as- sociated with dichogamy in annual caraway (Carum carvi, Apiaceae). American Journal of Botany 89, 1588–1598.
Langenberger, M.W., Davis, A.R., 2002b: Honey bee pollen for- aging in relation to flowering phenology of biennial caraway (Carum carvi L.). Canadian Journal of Plant Science 82, 203– 215.
Lindsey, A.H., 1984: Reproductive biology of Apiaceae. I. Floral visitors to Thaspium and Zizia and their importance in pollination. American Journal of Botany 71, 375–387.
Lindsey, A.H., Bell, C.R., 1985: Reproductive biology of Apiaceae. II. Cryptic specialization and floral evolution in Thaspium and Zizia. American Journal of Botany 72, 231–247.
Lupoli, R. 2017: Graphosoma lineatum (L., 1758) and G. italicum (O.F. Müller, 1766), two valid and distinct species, probably derived from the Zanclean mediterranean transgression (Hemiptera Pentatomidae). L’Entomologiste 73, 19–33.
Mačukanović-Jocić, M., 2010: The Biology of Melliferous Plants with an Atlas of Serbian Apiflora. Monographic Study. Faculty of Agriculture University of Belgrade, Belgrade.
Mačukanović-Jocić, M., Stešević, D., Rančić, D., Dajić Stevanović, Z., 2016: Pollen morphology and the flower vis- itors of Chaerophyllum coloratum L. (Apiaceae), Acta Bo- tanica Croatica 76, 1–8.
Menemen, Y., Jury, S., 2001: A systematic study of the genus Malabaila Hoffm. (Umbelliferae) comparing with the closely related genera. In: Gozukkimizi, N. (ed.), The Proceedings of the 2nd Balkan Botanical Congress, 299–312. Marmara University, Istanbul.
Niemirski, R., Zych, M., 2011: Fly pollination of dichogamous Angelica sylvestris (Apiaceae): How (functionally) specialized can a (morphologically) generalized plant be? Plant Sys- tematics and Evolution 2294, 147–158.
Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P., 2007: The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 104, 19891–19896.
Oosterbroek, P. 2006: The European families of the Diptera: identification, diagnosis, biology Utrecht: KNNV, Publi- shing. 205. pp.
Perveen, A., Qaiser, M., 2006: Pollen Flora of Pakistan XLVIII. Umbelliferae. Pakistan Journal of Botany 38, 1–14.
Pimenov, M., Ostroumova, T., 1994: The genus Malabaila Hof- fm. (Umbelliferae:Tordylieae): A carpological investigation and taxonomic implication. Feddes Repertorium 105, 141–155.
Pospiech M, Javůrková Z, Hrabec P, Štarha P, Ljasovská S, Bednář J, Tremlová B. Identification of pollen taxa by differ- ent microscopy techniques. PLoS One. 2021. 16(9):e0256808.
POWO 2022: Plants of the World Online. Facilitated by the Roy- al Botanic Gardens, Kew. Retrived 19 September 2022 from http://www.plantsoftheworldonline.org/
Proctor, M., Yeo, P., Lack, A., 1996: The natural history of pol- lination. HarperCollins Publishers, London, UK.
Punt, W., 1984: The Northwest European Pollen Flora, 37 Um- belliferae. Review of Palaeobotany and Palynology 42, 155– 364.
Punt. W., Hoen, P.P., Blackmore, S., Nilsson, S., Le Thomas, A., 2007: Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143, 1–81.
Rovira, A.M., Bosch, M., Molero, J., Blanche, C., 2002: Pollina- tion ecology and breeding system of the very narrow coastal endemic Seseli farrenyi (Apiaceae). Effects of population fragmentation. Nordic Journal of Botany 22, 727–740.
Sivell, O. 2021: Blow flies (Diptera: Calliphoridae, Polleniidae, Rhiniidae). Handbook for the Identification of British In- sects 10/16, 1–206.
Tollsten, L., Knudsen, J.T., Bergström, LG., 1994: Floral scent in generalistic Angelica (Apiaceae) – an adaptive character? Biochemical Systematics and Ecology 22, 161–169.
Tollsten, L., Øvstedal, D.O., 1994: Differentiation in floral scent chemistry among populations of Conopodium majus (Apia- ceae). Nordic Journal of Botany 14, 361–368.
Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., 1981: Flora Europaea. Volume 2. Rosaceae to Umbelliferae (3rd ed.). Cambridge University Press, Cambridge.
Van Veen, M.P. 2004: Hoverflies of Northwest Europe, Identifi- cation Keys to the Syrphidae (Hardback). KNNV Publi- shing, Utrecht.
Van Zeist, W., Bottema, S., 1977: Palynological investigation in western Iran. Paleohistoria 19, 19–85.
Vazquez, X. A., 2002: European Fauna of Oedemeridae. Argania editio, Barcelona.
Woodcock, T.S., Larson, B.M.H., Kevan, P.G., Inouye, D.W., Lunau, K., 2014: Flies and flowers II: floral attractants and rewards. Journal of Plant Ecology 12, 63–94.
Wróblewska, A., 1993: Flowering and pollen value of selected species of umbelliferous family - Umbelliferae Juss. (Apia- ceae Lindl.) in Lublin region. Part II. Pollen efficiency and insect visit. Acta Agrobotanica 46, 51–65. (in Polish).
Zych, M., 2006: Diurnal activity of the key pollinators of Heracleum sphondylium L. (Apiaceae). Acta Agrobotanica 59, 279–288.
Zych, M., 2007: On flower visitors and true pollinators: The case of protoandrous Heracleum spondylium L. (Apiaceae), Plant Systematics and Evolution 263, 159–179.