Heather pollen is not necessarily a healthy diet for bumble bees
DOI:
https://doi.org/10.26496/bjz.2023.111Keywords:
plant-pollinator interaction, pollen specialised metabolite, microcolony performance, bumble bee health, parasiteAbstract
There is evidence that specialised metabolites of flowering plants occur in both vegetative parts and floral resources (i.e., pollen and nectar), exposing pollinators to their biological activities. While such metabolites may be toxic to bees, it may also help them to deal with environmental stressors. One example is heather nectar which has been shown to limit bumble bee infection by a trypanosomatid parasite, Crithidia sp., because of callunene activity. Besides in nectar, heather harbours high content of specialised metabolites in pollen such as flavonoids but they have been poorly investigated. In this study, we aimed to assess the impact of Crithidia sp., heather pollen and its flavonoids on bumble bees using non-parasitised and parasitised microcolonies fed either control pollen diet (i.e., willow pollen), heather pollen diet, or flavonoid-supplemented pollen diet. We found that heather pollen and its flavonoids significantly affected microcolonies by decreasing pollen collection as well as offspring production, and by increasing male fat body content while parasite exposure had no significant effect except for an increase in male fat body. We did not find any medicinal effect of heather pollen or its flavonoids on parasitised bumble bees. Our results provide insights into the impact of pollen specialised metabolites on heather-bumble bee-parasite interactions. They underline the contrasting roles of the two floral resources for bumble bees and emphasize the importance of considering both nectar and pollen when addressing medicinal effects of a plant for pollinators.References
Amin M.R., Bussière L.F. & Goulson D. (2012). Effects of male age and size on mating success in the bumblebee Bombus terrestris. Journal of Insect Behavior 25 (4): 362–374. https://doi.org/10.1007/s10905-011-9306-4
Arnold S.E., Idrovo M., Arias L.J.L., Belmain S.R. & Stevenson P.C. (2014). Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness. Journal of Chemical Ecology 40 (8): 878–881. https://doi.org/10.1007/s10886-014-0467-4
Arrese E.L. & Soulages J.L. (2010). Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55: 207–225. https://doi.org/10.1146/annurev-ento-112408-085356
Ballantyne G., Baldock K.C. & Willmer P.G. (2015). Constructing more informative plant–pollinator networks: visitation and pollen deposition networks in a heathland plant community. Proceedings of the Royal Society B: Biological Sciences 282 (1814): e20151130. https://doi.org/10.1098/rspb.2015.1130
Baracchi D., Brown M.J. & Chittka L. (2015). Behavioural evidence for self-medication in bumblebees? F1000Research 4: 73. https://doi.org/10.12688/f1000research.6262.3
Baron G.L., Raine N.E. & Brown M.J. (2014). Impact of chronic exposure to a pyrethroid pesticide on bumblebees and interactions with a trypanosome parasite. Journal of Applied Ecology 51 (2): 460–469. https://doi.org/10.1111/1365-2664.12205
Bartolomé C., Jabal-Uriel C., Buendía-Abad M., Benito M., Ornosa C., De la Rúa P., ... & Maside X. (2021). Wide diversity of parasites in Bombus terrestris (Linnaeus, 1758) revealed by a high-throughput sequencing approach. Environmental Microbiology 23 (1): 478–483. https://doi.org/10.1111/1462-2920.15336
Baude M., Kunin W.E., Boatman N.D., Conyers S., Davies N., Gillespie M.A., Morton R.D., Smart S.M. & Memmott J. (2016). Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530 (7588): 85–88. https://doi.org/10.1038/nature16532
Berenbaum M.R. & Johnson R.M. (2015). Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science 10: 51–58. https://doi.org/10.1016/j.cois.2015.03.005
Biller O.M., Adler L.S., Irwin R.E., McAllister C. & Palmer-Young E. C. (2015). Possible synergistic effects of thymol and nicotine against Crithidia bombi parasitism in bumble bees. PLoS ONE 10 (12): e0144668. https://doi.org/10.1371/journal.pone.0144668
Brochu K.K., van Dyke M.T., Milano N.J., Petersen J.D., McArt S.H., Nault B.A., Kessler A. & Danforth B.N. (2020). Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae). Scientific Reports 10 (1): 1–12. https://doi.org/10.1038/s41598-020-58274-2
Brooks M.E., Kristensen K., Van Benthem K.J., Magnusson A.B., Nielsen C.W., Skaug A., Machler H.J., Bolker M. & Benjamin M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9 (2): 378–400. https://doi.org/10.3929/ethz-b-000240890
Brown M.J.F., Loosli R. & Schmid-Hempel P. (2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91 (3): 421–427. https://doi.org/10.1034/j.1600-0706.2000.910302.x
Brown M.J.F., Moret Y. & Schmid-Hempel P. (2003). Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parasitology 126 (3): 253–260. https://doi.org/10.1017/S0031182002002755
Butchart S.H., Walpole M., Collen B., Van Strien A., Scharlemann J.P., Almond R.E., ... & Watson R. (2010). Global biodiversity: indicators of recent declines. Science 328 (5982): 1164–1168. https://doi.org/10.1126/science.1187512
Campos M.G., Bogdanov S., de Almeida-Muradian L.B., Szczesna T., Mancebo Y., Frigerio C. & Ferreira F. (2008). Pollen composition and standardisation of analytical methods. Journal of Apicultural Research 47 (2): 154–161. https://doi.org/10.1080/00218839.2008.11101443
Cole R.J. (1970). The application of the “triangulation” method to the purification of Nosema spores from insect tissues. Journal of Invertebrate Pathology 15 (2): 193–195. https://doi.org/10.1016/0022-2011(70)90233-8
Dafni A., Kevan P.G. & Husband B.C. (2005). Practical pollination biology. Practical Pollination Biology.
Descamps C., Moquet L., Migon M. & Jacquemart A.L. (2015). Diversity of the insect visitors on Calluna vulgaris (Ericaceae) in Southern France heathlands. Journal of Insect Science 15 (1): 130. https://doi.org/10.1093/jisesa/iev116
Detzel A. & Wink M. (1993). Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4: 8–18. https://doi.org/10.1007/BF01245891
Dicks L.V., Breeze T.D., Ngo H.T., Senapathi D., An J., Aizen M.A., ... & Potts S.G. (2021). A global-scale expert assessment of drivers and risks associated with pollinator decline. Nature Ecology & Evolution 5 (10): 1453–1461. https://doi.org/10.1038/s41559-021-01534-9
Di Pasquale G., Salignon M., Le Conte Y., Belzunces L.P., Decourtye A., Kretzschmar A., Suchail S., Brunet J.-L. & Alaux C. (2013). Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PloS ONE 8 (8): e72016. https://doi.org/10.1371/journal.pone.0072016
Ellers J. (1996). Fat and eggs: an alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Netherlands Journal of Zoology 46: 227–235.
Fauser A., Sandrock C., Neumann P. & Sadd B.M. (2017). Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator. Ecological Entomology 42 (3): 306–314. https://doi.org/10.1111/een.12385
Fitch G., Figueroa L.L., Koch H., Stevenson P.C. & Adler L.S. (2022). Understanding effects of floral products on bee parasites: mechanisms, synergism, and ecological complexity. International Journal for Parasitology: Parasites and Wildlife 17: 244–256. https://doi.org/10.1016/j.ijppaw.2022.02.011
Folly A.J., Koch H., Stevenson P.C. & Brown M.J. (2017). Larvae act as a transient transmission hub for the prevalent bumblebee parasite Crithidia bombi. Journal of Invertebrate Pathology 148: 81–85. https://doi.org/10.1016/j.jip.2017.06.001
Gegear R.J., Otterstatter M.C. & Thomson J.D. (2006). Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society B: Biological Sciences 273 (1590): 1073–1078. https://doi.org/10.1098/rspb.2005.3423
Gekière A., Semay I., Gérard M., Michez D., Gerbaux P. & Vanderplanck M. (2022a). Poison or potion: effects of sunflower phenolamides on bumble bees and their gut parasite. Biology 11 (4): 545. https://doi.org/10.3390/biology11040545
Gekière A., Michez D. & Vanderplanck M. (2022b). Bumble bee breeding on artificial pollen substitutes. Journal of Economic Entomology 115 (5): 1423–1431. https://doi.org/10.1093/jee/toac126
Gekière A., Vanderplanck M. & Michez, D. (2023). Trace metals with heavy consequences on bees: A comprehensive review. Science of the Total Environment 895: e165084. https://doi.org/10.1016/j.scitotenv.2023.165084
Gekière A., Semay I., Michel A., Tourbez C., Gerbaux P., Michez D. & Vanderplanck M. (in prep.). Plant mediation: The delicate balance between herbivore deterrence and pollinator attraction.
Goulson D. (2010). Bumblebees: Behaviour, Ecology, and Conservation. Oxford University Press on Demand.
Goulson D. & Hughes W.O. (2015). Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biological Conservation 191: 10–19. https://doi.org/10.1016/j.biocon.2015.06.023
Goulson D., O’Connor S. & Park K.J. (2018). The impacts of predators and parasites on wild bumblebee colonies. Ecological Entomology 43 (2): 168–181. https://doi.org/10.1111/een.12482
Greenleaf S.S., Williams N.M., Winfree R. & Kremen C. (2007). Bee foraging ranges and their relationship to body size. Oecologia 153 (3): 589–596. https://doi.org/10.1007/s00442-007-0752-9
Hartig F. (2022). DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.3, 3.
Hendriksma H.P., Härtel S. & Steffan-Dewenter I. (2011). Testing pollen of single and stacked insect-resistant Bt-maize on in vitro reared honey bee larvae. PLoS ONE 6 (12) : e28174. https://doi.org/10.1371/journal.pone.0028174
Huang T., Jander G. & de Vos M. (2011). Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72 (13): 1531–1537. https://doi.org/10.1016/j.phytochem.2011.03.019
Irwin R.E., Cook D., Richardson L.L., Manson J.S. & Gardner D.R. (2014). Secondary compounds in floral rewards of toxic rangeland plants: impacts on pollinators. Journal of Agricultural and Food Chemistry 62 (30): 7335–7344. https://doi.org/10.1021/jf500521w
Johnson R.M., Mao W., Pollock H.S., Niu G., Schuler M.A. & Berenbaum M.R. (2012). Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PloS ONE 7 (2): e31051. https://doi.org/10.1371/journal.pone.0031051
Kassambara A., Kosinski M., Biecek P. & Fabian S. (2021). Survminer: drawing survival curves using Ggplot2. 2021. Available from https://cran.r-project.org/web/packages/survminer/index.html. R package version 0.4, 9.
Kleijn D. & Raemakers I. (2008). A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89 (7): 1811–1823. https://doi.org/10.1890/07-1275.1
Koch H., Woodward J., Langat M.K., Brown M.J. & Stevenson P.C. (2019). Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Current Biology 29 (20): 3494–3500. https://doi.org/10.1016/j.cub.2019.08.037
Lenth R. (2022). emmeans: estimated marginal means, aka least-squares means. R package version 1.4.7.2020.
Li J., Ou-Lee T.M., Raba R., Amundson R.G. & Last R.L. (1993). Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell 5 (2): 171–179. https://doi.org/10.1105/tpc.5.2.171
Li S., Yu X. & Feng Q. (2019). Fat body biology in the last decade. Annual Review of Entomology 64: 315–333. https://doi.org/10.1146/annurev-ento-011118-112007
Liao L.H., Wu W.Y. & Berenbaum M.R. (2017a). Behavioral responses of honey bees (Apis mellifera) to natural and synthetic xenobiotics in food. Scientific Reports 7 (1): e15924. https://doi.org/10.1038/s41598-017-15066-5
Liao L.H., Wu W.Y. & Berenbaum M.R. (2017b). Impacts of dietary phytochemicals in the presence and absence of pesticides on longevity of honey bees (Apis mellifera). Insects 8 (1): 22. https://doi.org/10.3390/insects8010022
Logan A., Ruiz-González M.X. & Brown M.J.F. (2005). The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130 (6): 637–642. https://doi.org/10.1017/S0031182005007304
Lucchetti M.A., Kilchenmann V., Glauser G., Praz C. & Kast C. (2018). Nursing protects honeybee larvae from secondary metabolites of pollen. Proceedings of the Royal Society B: Biological Sciences 285 (1875): e20172849. https://doi.org/10.1098/rspb.2017.2849
Mallinger R.E., Gaines-Day H.R. & Gratton C. (2017). Do managed bees have negative effects on wild bees? A systematic review of the literature. PloS ONE 12 (12): e0189268. https://doi.org/10.1371/journal.pone.0189268
Manson J.S., Otterstatter M.C. & Thomson J.D. (2010). Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162 (1): 81–89. https://doi.org/10.1007/s00442-009-1431-9
Martin C.D., Fountain M.T. & Brown M.J. (2018). Bumblebee olfactory learning affected by task allocation but not by a trypanosome parasite. Scientific Reports 8 (1): 1–8. https://doi.org/10.1038/s41598-018-24007-9
McMenamin A.J. & Genersch E. (2015). Honey bee colony losses and associated viruses. Current Opinion in Insect Science 8: 121–129. https://doi.org/10.1016/j.cois.2015.01.015
Meeus I., Brown M.J., De Graaf D.C. & Smagghe G. (2011). Effects of invasive parasites on bumble bee declines. Conservation Biology 25 (4): 662–671. https://doi.org/10.1111/j.1523-1739.2011.01707.x
Moquet L., Bacchetta R., Laurent E. & Jacquemart A.L. (2017). Spatial and temporal variations in floral resource availability affect bumblebee communities in heathlands. Biodiversity and Conservation 26 (3): 687–702. https://doi.org/10.1007/s10531-016-1266-8
Naug D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation 142 (10): 2369–2372. https://doi.org/10.1016/j.biocon.2009.04.007
Nicolson S.W. & Thornburg R.W. (2007). Nectar chemistry. Nectaries and Nectar: 215–264. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5937-7_5
Onkokesung N., Reichelt M., van Doorn A., Schuurink R.C., van Loon J.J. & Dicke M. (2014). Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3, 7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. Journal of Experimental Botany 65 (8): 2203–2217. https://doi.org/10.1093/jxb/eru096
Onyilagha J.C., Gruber M.Y., Hallett R.H., Holowachuk J., Buckner A. & Soroka J.J. (2012). Constitutive flavonoids deter flea beetle insect feeding in Camelina sativa L. Biochemical Systematics and Ecology 42: 128–133. https://doi.org/10.1016/j.bse.2011.12.021
Otterstatter M.C., Gegear R.J., Colla S.R. & Thomson J.D. (2005). Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioral Ecology and Sociobiology 58 (4): 383–389. https://doi.org/10.1007/s00265-005-0945-3
Otterstatter M.C. & Thomson J.D. (2006). Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133 (6): 749–761. https://doi.org/10.1017/S003118200600120X
Palmer-Young E.C., Farrell I.W., Adler L.S., Milano N.J., Egan P.A., Junker R.R., Irwin R.E. & Stevenson P.C. (2019). Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecological Monographs 89 (1): e01335. https://doi.org/10.1002/ecm.1335
Paris L., El Alaoui H., Delbac F. & Diogon M. (2018). Effects of the gut parasite Nosema ceranae on honey bee physiology and behavior. Current Opinion in Insect Science 26: 149–154. https://doi.org/10.1016/j.cois.2018.02.017
Pinheiro J. & Bates D. (2022). R Core Team (2022) nlme: linear and nonlinear mixed effects models. R package version 3.1–160.
Popp M., Erler S. & Lattorff H.M.G. (2012). Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.). Microbiology Open 1 (4): 362–372. https://doi.org/10.1002/mbo3.35
Pusztahelyi T., Holb I.J. & Pócsi I. (2015). Secondary metabolites in fungus-plant interactions. Frontiers in Plant Science 6: 573. https://doi.org/10.3389/fpls.2015.00573
R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org.
Regali A. & Rasmont P. (1995). Nouvelles méthodes de test pour l’évaluation du régime alimentaire chez des colonies orphelines de Bombus terrestris (L) (Hymenoptera, Apidae). Apidologie 26 (4) : 273–281. https://doi.org/10.1051/apido:19950401
Richardson L.L., Adler L.S., Leonard A.S., Andicoechea J., Regan K.H., Anthony W.E., Manson J.S. & Irwin R.E. (2015). Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society B: Biological Sciences 282 (1803): e20142471. https://doi.org/10.1098/rspb.2014.2471
Rosales C. (2017). Cellular and molecular mechanisms of insect immunity. In: Shields V.D.C. (ed.) Insect Physiology and Ecology: 179–212. https://doi.org/10.5772/67107
Sánchez-Bayo F. & Goka K. (2014). Pesticide residues and bees–a risk assessment. PloS ONE 9 (4): e94482. https://doi.org/10.1371/journal.pone.0094482
Sawyer R. & Pickard R.S. (1981). Pollen Identification for Beekeepers. University College Cardiff Press.
Schmid-Hempel P. (1998). Parasites in Social Insects. Princeton University Press.
Schmid-Hempel P. (2001). On the evolutionary ecology of host–parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88 (4): 147–158. https://doi.org/10.1007/s001140100222
Schmid-Hempel P. & Schmid-Hempel R. (1993). Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behavioral Ecology and Sociobiology 33: 319–327. https://doi.org/10.1007/BF00172930
Scott J.G., Liu N. & Wen Z. (1998). Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 121 (1–3): 147–155. https://doi.org/10.1016/S0742-8413(98)10035-X
Shykoff J.A. & Schmid-Hempel P. (1991). Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22 (2): 117–125. https://doi.org/10.1051/apido:19910204
Simmonds M.S. (2003). Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64 (1): 21–30. https://doi.org/10.1016/S0031-9422(03)00293-0
Svoboda J.A., Herbert Jr E.W., Thompson M.J. & Feldlaufer M.F. (1986). Selective sterol transfer in the honey bee: Its significance and relationship to other hymenoptera. Lipids 21 (1): 97–101. https://doi.org/10.1007/BF02534310
Tasei J.N. & Aupinel P. (2008). Validation of a method using queenless Bombus terrestris micro-colonies for testing the nutritive value of commercial pollen mixes by comparison with queenright colonies. Journal of Economic Entomology 101 (6): 1737–1742. https://doi.org/10.1603/0022-0493-101.6.1737
Therneau T.M. (2022). Mixed Effects Cox Models. R package coxme version 2.2-18.1.
Thorburn L.P., Adler L.S., Irwin R.E. & Palmer-Young E.C. (2015). Variable effects of nicotine, anabasine, and their interactions on parasitized bumble bees. F1000Research 4: 880. https://doi.org/10.12688/f1000research.6870.2
Treutter D. (2005). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology 7 (6): 581–591. https://doi.org/10.1055/s-2005-873009
Vanderplanck M., Moerman R., Rasmont P., Lognay G., Wathelet B., Wattiez R. & Michez D. (2014). How does pollen chemistry impact development and feeding behaviour of polylectic bees? PloS ONE 9 (1): e86209. https://doi.org/10.1371/journal.pone.0086209
Vanderplanck M., Decleves S., Roger N., Decroo C., Caulier G., Glauser G., Gerbaux P., Lognay G., Richel A., Escaravage N. & Michez D. (2018). Is non-host pollen suitable for generalist bumblebees? Insect Science 25 (2) : 259–272. https://doi.org/10.1111/1744-7917.12410
Vanderplanck M., Michez D., Albrecht M., Attridge E., Babin A., Bottero I., ... & Gérard M. (2021). Monitoring bee health in European agro-ecosystems using wing morphology and fat bodies. One Ecosystem 6: e63653. https://doi.org/10.3897/oneeco.6.e63653
Van Engelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier M., Frazier J., Cox-Foster D., Chen Y., Underwood R., Tarpy D. & Pettis J.S. (2009). Colony collapse disorder: a descriptive study. PloS ONE 4 (8): e6481. https://doi.org/10.1371/journal.pone.0006481
Vaudo A.D., Tooker J.F., Patch H.M., Biddinger D.J., Coccia M., Crone M.K., Fiely M., Francis J.S., Hines H.M., Hodges M., Jackson S.W., Michez D., Mu J., Russo L., Safari M., Treanore E.D., Vanderplanck M., Yip E., Leonard A.S. & Grozinger C.M. (2020). Pollen protein: lipid macronutrient ratios may guide broad patterns of bee species floral preferences. Insects 11 (2): e132. https://doi.org/10.3390/insects11020132
Wang S.D., Liu W., Xue C.B. & Luo W.C. (2010). The effects of luteolin on phenoloxidase and the growth of Spodoptera exigua (Hübner) larvae (Lepidoptera: Noctuidae). Journal of Pesticide Science 35 (4): 483–487. https://doi.org/10.1584/jpestics.G10-24
Wang X.Y., Tang J., Wu T., Wu D. & Huang S.Q. (2019). Bumblebee rejection of toxic pollen facilitates pollen transfer. Current Biology 29 (8): 1401–1406. https://doi.org/10.1016/j.cub.2019.03.023
Weber M. (2004). Alkaloids and Old Lace: Pollen Toxins Exclude Generalist Pollinators From Death Camas. https://doi.org/10.26076/dc24-fa2f
Wickham H. (2016). Data analysis. In: ggplot2: 189–201. Springer, Cham. https://doi.org/10.1007/978-3-319-24277-4_9
Wood S.N. (2006). Generalized Additive Models: An Introduction with R. Chapman and Hall: CRC Press, Boca Raton, FL.
Zaynab M., Fatima M., Abbas S., Sharif Y., Umair M., Zafar M.H. & Bahadar K. (2018). Role of secondary metabolites in plant defense against pathogens. Microbial pathogenesis 124: 198–202. https://doi.org/10.1016/j.micpath.2018.08.034
Published
How to Cite
Issue
Section
License
All published papers will be put on-line as high resolution PDF’s. Copyright thus remains with the authors. All manuscripts will be licensed under a Creative Commons Attribution 3.0 License https://creativecommons.org/licenses/by/4.0/.
