Skip to main content
SpringerLink
Log in

Fungal Honeydew Elements as Potential Indicators of the Botanical and Geographical Origin of Honeys

  • Published:
Food Analytical Methods Aims and scope Submit manuscript

Abstract

The present study applied indicator value analysis as a novel approach to estimate honey authenticity: microscopic indicators of honey origin were identified based on the distinct fungal content of honeys from different sources. The abundance and the IndVal index of 34 selected fungal spore types were quantified in 82 melissopalynological honey samples originating from various honeydew (Pinus, Abies) or nectar sources using multivariate statistical approaches. A dissimilarity matrix of honey samples was obtained by computing Bray-Curtis coefficients, and the distances were visualized using non-metric multidimensional scaling. K-means clustering was applied to sample coordinates to create a classification based on the frequency of selected fungal taxa. Strikingly, the resulting clusters were on a high level of agreement with the melissopalynological or geographical classification of samples. Various fungal taxa were shown to characterize groups of honey samples with a significant indicator value: floral honeys (Metschnikowia reukaufii), Pinus honeydew honeys (Capnobotrys sp., Antennatula sp.), Abies honeydew honeys from Greece (staurospore and scolecospore types) and honeydew honeys from Italy (Tripospermum spp. and Excipularia fusispora). Having revealed that the mere presence of distinct fungal taxa can indicate differences in the botanical and geographical source of honeys, the present findings encourage the confirmation of honey origin also by recording the occurrence of given honeydew elements during routine melissopalynological analysis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Auclair JL (1963) Aphid feeding and nutrition. Annu Rev Entomol 8:439–490

    Article  Google Scholar 

  • Barsoum N, Fuller L, Ashwood F, Reed K, Bonnet-Lebrun AS, Leung F (2014) Ground-dwelling spider (Araneae) and carabid beetle (Coleoptera: Carabidae) community assemblages in mixed and monoculture stands of oak (Quercus robur L./Quercus petraea (Matt.) Liebl.) and Scots pine (Pinus sylvestris L.). For Ecol Manag 321:29–41

  • Bogdanov S, Martin P, Lullmann C (1997) Harmonised methods of the International Honey Commission (Extra Issue). Apidologie 28:1–59

  • Bogdanov S, Martin P (2002) Honey authenticity: a review. Mitt Lebensmittelunters Hyg 93:232–254

    CAS  Google Scholar 

  • Campos G, della Modesta RC, da Silva TJP, Raslan DS (2001) Comparison of some components between floral honey and honeydew honey. Rev Inst Adolfo Lutz 60:59–64

    CAS  Google Scholar 

  • Corlett M, Hughes SJ, Kaufert M (1973) New Zealand fungi: 19. Centrum organisation in some Euantennariaceae and Metacapnodiaceae. New Zeal J Bot 11(2):213–230

    Article  Google Scholar 

  • da Silva PM, Gauche C, Gonzaga LV, Costa ACO, Fett R (2016) Honey: chemical composition, stability and authenticity. Food Chem 196:309–323

    Article  Google Scholar 

  • De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

  • Demianowicz Z, Borowska A, Dubik G, Pielka J (1972) Fungi in fir honeydew honey. Ann Univ Mariae Curie-Sklodowska 25:203–212

    Google Scholar 

  • Díez MJ, Andrés C, Terrab A (2004) Physicochemical parameters and pollen analysis of Moroccan honeydew honeys. Int J Food Sci Technol 39:167–176

    Article  Google Scholar 

  • Dimou M, Katsaros J, Klonari KT, Thrasyvoulou A (2006) Discriminating pine and fir honeydew honey by microscopic characteristics. J Apic Res Bee World 45:16–21

    Article  Google Scholar 

  • Doner LW (1977) The sugars of honey—a review. J Sci Food Agric 28(5):443–456

    Article  CAS  Google Scholar 

  • Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible assymetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Ellis MB, Ellis JP (1997) Microfungi on land plants: an identification handbook. The Richmond Publishing Company Ltd., Slough

    Google Scholar 

  • Escuredo O, Fernández-González M, Del Carmen SM (2012) Differentiation of blossom honey and honeydew honey from Northwest Spain. Agriculture 2:25–37

    Article  Google Scholar 

  • González-Paramás AM, García-Villanova RJ, Bárez JAG, Sánchez JS, Albajar RA (2007) Botanical origin of monovarietal dark honeys (from heather, holm oak, pyrenean oak and sweet chestnut) based on their chromatic characters and amino acid profiles. Eur Food Res Technol 226(1–2):87–92

    Article  Google Scholar 

  • Gourbiere F (1986) Méthode d'étude simultanée de la décomposition et des mycoflores des aiguilles de conifères (Abies alba). Soil Biol Biochem 18(2):155–160

    Article  Google Scholar 

  • Guzmán B, Lachance MA, Herrera CM (2013) Phylogenetic analysis of the angiosperm-floricolous insect–yeast association: have yeast and angiosperm lineages co-diversified? Mol Phylogenet Evol 68(2):161–175

    Article  Google Scholar 

  • Ingold CT (1971) Fungal spores: their liberation and dispersal. Clarendon, Oxford

    Google Scholar 

  • Herrera CM, de Vega C, Canto A, Pozo MI (2009) Yeasts in floral nectar: a quantitative survey. Ann Bot 103:1415–1423

    Article  Google Scholar 

  • Hughes SJ (1976) Sooty moulds. Mycologia 68(4):693–820

    Article  Google Scholar 

  • Karabagias IK, Dimitriou E, Kontakos S, Kontominas MG (2016) Phenolic profile, colour intensity, and radical scavenging activity of Greek unifloral honeys. Eur Food Res Technol 242(8):1201–1210

    Article  CAS  Google Scholar 

  • Kurankowa Z (1977) Fungi occurring in honeydew on deciduous trees and shrubs. Acta Mycol 13:275–278

    Article  Google Scholar 

  • Lachman J, Orsák M, Hejtmánková A, Kovárová E (2010) Evaluation of antioxidant activity and total phenolics of selected Czech honeys. LWT Food Sci Technol 43(1):52–58

    Article  CAS  Google Scholar 

  • Lamarre GPA, Baraloto C, Fortunel C et al (2012) Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity. Ecology 93:195–210

    Article  Google Scholar 

  • Louveaux J, Maurizio A, Vorwohl G (1978) Methods of melissopalynology. Bee World 51:125–131

    Article  Google Scholar 

  • Magyar D, Gönczöl J, Révay Á, Grillenzoni F, Del Carmen S-CM (2005) Stauro- and scolecoconidia in floral and honeydew honeys. Fungal Divers 20:103–120

    Google Scholar 

  • Magyar D (2008) The tree bark: a natural spore trap. Asp Appl Biol 89:7–16

    Google Scholar 

  • Magyar D, Mura-Mészáros A, Grillenzoni F (2016a) Fungal diversity in floral and honeydew honeys. Acta Bot Hung 58:145–166

    Article  Google Scholar 

  • Magyar D, Vass M, Li DW (2016b) Dispersal strategies of microfungi. In: Li DW (ed) Biology of Microfungi. Springer International Publishing, Bern, pp 315–371

  • McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Oregon

  • Ni C, Zhu B, Wang N, Wang M, Chen S, Zhang J, Zhu Y (2016) Simple column-switching ion chromatography method for determining eight monosaccharides and oligosaccharides in honeydew and nectar. Food Chem 194:555–560

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-2. https://CRAN.R-project.org/package=vegan

  • Pérez-Atanes S, Del Carmen S-CM, Méndez-Álvarez J (2001) Contribution to the study of fungal spores in honeys of Galicia (NW Spain). Grana 40:217–222

    Article  Google Scholar 

  • Pita-Calvo C, Vázquez M (2016) Differences between honeydew and blossom honeys: a review. Trends Food Sci Technol 59:79–87

    Article  Google Scholar 

  • Popa M, Vica M, Axinte R, Glevitzky M, Varvara S (2009) Study concerning the honey qualities in Transylvania region. Ann Univ Apul S Oecon 11:1034–1040

    Google Scholar 

  • Reynolds DR (1975) Observation on the growth forms of sooty mould fungi. Hedwigia 26:179–183

    Google Scholar 

  • Sanz ML, Gonzalez M, De Lorenzo C, Sanz J, Martınez-Castro I (2005) A contribution to the differentiation between nectar honey and honeydew honey. Food Chem 91:313–317

    Article  CAS  Google Scholar 

  • Schaeffer RN, Vannette RL, Irwin RE (2015) Nectar yeasts in Delphinium nuttallianum (Ranunculaceae) and their effects on nectar quality. Fungal Ecol 18:100–106

    Article  Google Scholar 

  • Seeger J, Filser J (2008) Bottom-up down from the top: honeydew as a carbon source for soil organisms. Eur J Soil Biol 44(5):483–490

    Article  Google Scholar 

  • Seijo MC, Escuredo O, Fernández-González M (2011) Fungal diversity in honeys from northwest Spain and their relationship to the ecological origin of the product. Grana 50:55–62

    Article  Google Scholar 

  • Shaw DE (1999) Bees and fungi, with special reference to certain plant pathogens. Australas Plant Pathol 28:269–282

  • Simova S, Atanassov A, Shishiniova M, Bankova V (2012) A rapid differentiation between oak honeydew honey and nectar and other honeydew honeys by NMR spectroscopy. Food Chem 134(3):1706–1710

    Article  CAS  Google Scholar 

  • Truchado P, Ferreres F, Tomas-Barberan FA (2009) Liquid chromatography–tandem mass spectrometry reveals the widespread occurrence of flavonoid glycosides in honey, and their potential as floral origin markers. J Chrom A 1216(43):7241–7248

    Article  CAS  Google Scholar 

  • Tsigouri A, Passaloglou-Katrali M, Sabatakou O (2004) Palynological characteristics of different unifloral honeys from Greece. Grana 43:122–128

    Article  Google Scholar 

  • Wäckers FL, van Rijn PCJ, Bruin J (eds) (2005) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge

    Google Scholar 

  • Warakomska Z, Jaroszynska T (1992) Analysis of the honeydew honeys of Roztocze. Pszczelnicze Zesz Nauk 36:149–156

    Google Scholar 

  • Zábrodská B, Vorlová L (2014) Adulteration of honey and available methods for detection—a review. Acta Vet Brno 83:85–102

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Francesca Grillenzoni for providing Italian, Greek and Croatian honey samples for microscopic examination. This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Author information

Author notes

  1. Anna Mura-Mészáros

    Present address: Leibniz Institute on Aging - Fritz Lipmann Institute Jena, Beutenbergstrasse 11, 07745, Jena, Germany

Authors and Affiliations

  1. Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute, Beutenbergstrasse 11a, 07745, Jena, Germany

    Anna Mura-Mészáros

  2. Department of Air Hygiene and Aerobiology, National Public Health Center, Albert F. út 2-6, Budapest, 1049, Hungary

    Donát Magyar

Authors
  1. Anna Mura-Mészáros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donát Magyar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna Mura-Mészáros.

Ethics declarations

Conflict of Interest

Anna Mura-Mészáros declares that she has no conflict of interest. Donát Magyar declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

Not applicable.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mura-Mészáros, A., Magyar, D. Fungal Honeydew Elements as Potential Indicators of the Botanical and Geographical Origin of Honeys. Food Anal. Methods 10, 3079–3087 (2017). https://doi.org/10.1007/s12161-017-0862-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12161-017-0862-x

Keywords

Search

Navigation