Acta agriculturae Slovenica, 118/3, 1–7, Ljubljana 2022 doi:10.14720/aas.2022.118.3.2690 Original research article / izvirni znanstveni članek Pollen quality and sensory attributes of Algerian jujube (Ziziphus lotus (L.) Lam.) honeys Scherazad MEKIOUS 1, 2, 3, Carine MASSEAUX 4, Wahida LOUCIF-AYAD 5, 6, Monica VERCELLI 7 Received May 14, 2022; accepted September 23, 2022. Delo je prispelo 14. maja 2022, sprejeto 23. septembra 2022 1 University of Djelfa, Faculty of Nature and Life Sciences, Djelfa, Algeria 2 University of Blida, Faculty of Nature and Life Sciences, Medicinal and Aromatic Plants Laboratory, Blida, Algeria 3 Corresponding author, e-mail: mekious.sch.uni.djelfa@gmail.com 4 Catholic University of Louvain, Beekeeping Research and Information Center (CARI), Louvain-la-Neuve, Belgium 5 Faculty of Medicine, Badji Mokhtar University, Annaba, Algeria 6 Laboratory of Applied Animal Biology, Faculty of Science, Badji Mokhtar University, Annaba, Algeria 7 Department of Agricultural, Forest and Food Sciences (DISAFA), University of Torino, Torino, Italy Pollen quality and sensory attributes of Algerian jujube (Ziziphus lotus (L.) Lam.) honeys Abstract: Honey bees and beekeeping activity are of huge importance for the crop production and biodiversity conser- vation as well as for the economic impact due to ecosystem services. In the south of Algeria, the jujube blooming is an essential forage source for honey bees. The aim of this study was to determine the melissopalynological and sensory char- acteristics of Algerian jujube honey. Nineteen samples of jujube honey collected in south Algeria over the period from 2016 to 2018 were analyzed. The unifloral designation attributed to the honey was confirmed by a pollen analysis following the estab- lished standard methods. Sensory analysis is carried out test- ing the color, the odor and aromas. The results showed that Ziziphus lotus pollen was predominant in all samples, and in terms of sensory analysis, color ranged from amber yellow to light brown; the determined scent classes were warm, floral and woody with medium intensity; the aroma was represented by medium intensity with the warm caramelized, floral fruity and woody classes. Sweet flavor is perceived at medium intensity, acidic flavor is weak, astringent sensation is average and the pi- quant note is perceived with a low intensity. This work proves to be important for improving the knowledge in typical honeys. Key words: jujube; Ziziphus lotus; honey; melissopalynol- ogy; sensory analysis; pollen Kakovost peloda in senzorične lastnosti medu iz alžirske vrste čičimaka (Ziziphus lotus (L.) Lam.) Izvleček: Medonosne čebele in njihova reja imajo velik pomen za pridelavo gojenih rastlin in ohranjanje biodiverzitete kot tudi velik ekonomski pomen pri ekosistemskih storitvah. Na jugu Alžirije je cvetenje alžirskega čičimaka (žižole) najpo- membnejša paša za medonosne čebele. Namen raziskave je bil določiti sestavo in senzorične lastnosti medu, nabranega na tej rastlini. Analiziranih je bilo 19 vzorcev čičimakovega medu, na- branih na jugu Alžirije v obdobju 2016-2018. Pripadnost medu tej medonosni vrsti je bila potrjena s pelodno analizo in in drugimi uveljavljenimi standardnimi metodami. Pri senzorič- ni analizi so bili preiskušeni barva, vonj in aroma. Rezultati so pokazali, da je v vseh vzorcih medu prevladoval pelod te vrste čičimaka. Barva medu je bila od oranžnorumene do svetlorja- ve, vonj je bil srednje močan, določen kot topel, cvetlični do lesni. Aroma medu je bila srednje močna, po toplih karamelah, cvetno-sadna z odtenki po lesu.Sladkost je bila srednja, kislost šibka, trpkost srednja, pikantnost je bila zaznana kot šibke jako- sti. Raziskava je pomembna, ker prispeva k poznavanju tipičnih medov. Ključne besede: čičimak; Ziziphus lotus; med; melisopali- nologija; senzorična analiza; pelod Acta agriculturae Slovenica, 118/3 – 20222 S. MEKIOUS et al. 1 INTRODUCTION Bees are the primary animal pollinators in most ecosystems (Neff & Simpson, 1993) and honey bees (Apis mellifera L., 1758) in particular play a key role as provid- ers of pollination services essential for agricultural pro- ductivity and biodiversity conservation (Potts et al., 2003; Klein et al., 2007; Salami et al., 2016; Ferrazzi et al., 2017). An economic study demonstrated that the total econom- ic value of pollination services globally amounts to ap- proximately €153 billion annually (Gallai et al., 2009), corresponding to about 9 % of the total economic value of agricultural crops grown for human consumption. Moreover, beekeeping supplies market beehive products (honey, pollen, royal jelly, propolis and wax) and live- stock (artificial swarms, packed bees, queens). Currently, a total of 92.3 million hives have been recorded around the world and the honey production amounts to around 1.8 million tons (Vercelli et al., 2021). Mediterranean basin represents an important area for beekeeping activity and honey production character- ized by typical unifloral and multifloral honeys (Battesti, 1990). However, in Mediterranean areas, climate change is a severe threat to honey bees (Le Conte &Navajas, 2008; IPBES, 2016; Novelli et al., 2021; Vercelli et al., 2021), influencing significantly other strictly related fac- tors such as diseases, parasites, predators, parasitoids, vi- ruses and pesticide use (Goulson et al., 2015; Zawislak et al. 2019).In arid and semi-arid areas of southern Algeria, the jujube (Ziziphus lotus L.) blooming is essential for- age sources (nectar and pollen) for honey bees usually between May and June as well as other flowering present during the year (Mekious et al.,2015). Due to this im- portant source, it is possible to produce unifloral honey that is highly sought and appreciated by beekeepers and consumers. As Jujube honey is exposed to a lot of fraud, particularly with regard to its unifloral appellation, the identification and characterization of this honey is essen- tial to preserve the quality as well as geographical and botanical origins. Some studies have been targeted the characterization of this unifloral honey but there is an in- sufficient knowledge about its sensory properties (Song et al., 2012; Zhou et al., 2013; Mekious et al., 2015; Cha- kir, et al., 2016; Zerrouk et al., 2017; Mekious et al., 2020; Zerrouk et al., 2021). Melissopalynological and sensory properties are one of the main ways used to identify unifloral and mul- tifloral honeys (Ferrazzi&Medrzycki, 2002; Piana et al., 2004; Ferrazzi& Vercelli, 2014; Prđun et al., 2020). The aim of this study was to determine pollen characteristics and sensory properties in several of honey samples of the same floral origin. The study of the pollen profile is im- portant to verify the unifloral attributed designation and to know the botanical origin of pollen collected by honey bees. This analysis provides valuable information on the foraging activity of honey bee (Battesti, 1992; Floris et al., 2020). When pollen of one species is highly present in a honey, it is very likely that that species gives an im- portant contribution in terms of nectar in the process of elaboration of this honey except for some honeys derived from plants that do not provide much pollen (pollen un- der-represented, e.g. lavender honeys) or from plants that produce much more pollen than nectar (pollen over-rep- resented, e.g. eucalyptus honey) (Louveaux et al., 1978; Von Der Ohe et al., 2004). Furthermore, sensory properties describe the gen- eral physical characteristics of honey perceptible by our senses. Taste and aroma vary and depend on the plant origin. Usually, sensory evaluation is commonly used to complete physico-chemical and pollen analyses. It is used to confirm quality, to verify the absence of defects, to establish sensory profiles of unifloral honeys, and also to understand consumer preferences (Piana et al., 2004; Marcazzan, 2018). Organoleptic qualities are also consid- ered as markers of floral origin (Amiot et al., 1989). In the absence of sensory standards specific to jujube honey, this study was based on the evaluation of the intensity of organoleptic attributes in 19 honey samples of the same floral origin in order to define the majority aromatic notes. 2 MATERIALS AND METHODS 2.1 STUDY AREA AND HONEY COLLECTION During the years 2016-2018, in the regions of Djelfa (34° 40′ 0″ N, 3° 15′ 0″ E) and Laghouat (33° 48′ 23″ N, 2° 52′ 56″ E) located in the south of Algeria, character- ized by a hot and dry climate with pastoral vegetation well adapted to pedoclimatic conditions of these regions. According to the information collected by the profes- sional climatological stations of the national metrological office of Djelfa and Laghouat, in the years of our study, the maximum average temperature reached 33.82 °C in Djelfa and 41.09 °C in Laghouat  Regarding the precipi- tation, 275 mmyear-1 and163 mmyear-1were registered in Djelfa and in Laghouat, respectively.19 unifloral declared as Z. lotus honey samples were collected from hives be- longing to professional beekeepers and placed in jujube blossom area. Acta agriculturae Slovenica, 118/3 – 2022 3 Pollen quality and sensory attributes of Algerian jujube (Ziziphus lotus (L.) Lam.) honeys 2.2 QUALITATIVE MELISSOPALYNOLOGICAL ANALYSIS In order to complete a qualitative melissopalyno- logical analysis, the extraction and analysis of the pol- len spectra were carried out using methods established by the International Commission of Apicultural Botany, described by Louveaux et al. (1978), Ferrazzi (1992) and Von der Ohe et al. (2004). Ten grams of honey was dis- solved in 20 ml of distilled hot water (20-40  °C). The solution was centrifuged once for 10 min (30,000 rpm), and then another centrifugation was done for 5 min under the same conditions. The sediment was put on a slide with an area of 24× 24 mm. 500 pollen grains were counted and their relative frequency classes were determined according to the in- ternational melissopalynological nomenclature: predom- inant pollen for pollen occurring for more than 45 % of the total pollen count, accompanying pollen or second- ary pollen (16-45 %), important minor pollen (3-15 %) and minor pollen, occurring < 3 %. The identification of pollen types was carried out by comparing the morphology and dimensions of the pol- len grains present in our samples observed under a light microscope with those of microphotographs of refer- ence pollens established by Ricciardelli d’Albore (1998), by our database (Laboratory of aromatic and medicinal plants, University of Blida1) and other pollen atlas. The pollen type includes species and/or genera present in the area, which have the same or similar pollen morphology microscopically. 2.3 SENSORY ANALYSIS The sensory analysis, visual, olfactory, and gustatory characteristics was performed using the technique de- scribed by Piana et al. (2004). The samples were tested by a panel of three assessors from the CARI (Center for Bee- keeping Research and Information) trained to identify a sensory stimulus on the basis of odor and aroma wheel developed by CARI laboratory (Bruneau et al., 2000). The wheel synthesizes a common lexicon of refer- ence and defines a list of descriptors with a precise mean- ing and the same meaning for all, and on the other hand to approve standardized aromatic references correspond- ing to each descriptor. Assessors recorded the color using the Pfund method. The intensity of odor and aroma is carried by a system of quantified evaluation on a scale of 1 to 3. 1: low intensity, 2: medium intensity, 3: high intensity. 3 RESULTS AND DISCUSSION 3.1 QUALITATIVE MELISSOPALYNOLOGICAL ANALYSIS The unifloral declaration attributed to the honey samples was confirmed by a qualitative pollen analysis. The types of pollen present in honey samples divided into four classes of pollen frequencies are illustrated in Table 1. The pollen grains of nectarless species from the families such as Poaceae, Chenopodiaceae, Pinaceae, Cistaceae, Plantaginaceae and Oleaceae were calculated separately (Louveaux et al., 1978 and Von Der Ohe et al., 2004). The taxa Ziziphuslotus,Thapsia garganica, Centau- rea, Carduus, Euphorbia bupleuroides, Retama retam and Peganum harmala have a large distribution (>50  %) in the honey samples. Usually, these pollens are markers of the floristic environment, having a high pollen frequency Figure1:The jujube tree in the steppe region of Djelfa and the pollen grain of Ziziphus lotus (photo credit: Scherazad Mekious) Acta agriculturae Slovenica, 118/3 – 20224 S. MEKIOUS et al. Family Taxon (Pollen type) F (%) M (<3 %) I (3-15 %) S (16-45 %) P (>45 %) Max Anacardiaceae Pistacia lentiscus L.* 10.53 10.53 - - - 1.1 Apiaceae Thapsia garganica L. 89.47 42.11 36.84 10.53 - 17.3 Apiaceae A Daucus carota L. 36.84 36.84 - - - 7.6 Arecaceae Arecaceae 21.05 21.05 - - - 1.6 Asteraceae Echinops 47.37 47.37 - - - 2.5 Centaurea 68.42 52.63 15.79 - - 6.1 Carthamus 10.53 10.53 - - - 1.1 Asteraceae S Carduus 57.89 31.58 26.32 - - 15.2 Calendula 42.11 42.11 - - - 2.7 Scolymus 15.79 15.79 - - - 1.2 Asteraceae T Taraxacum 26.32 26.32 - - - 1.2 Boraginaceae Echium 15.79 15.79 - - - 2.7 Brassicaceae Sinapis form 21.05 21.05 - - - 1.7 Brassicaceae Brassica form 21.05 21.05 - - - 1.2 Caprifoliaceae Caprifoliaceae 31.58 31.58 - - - 1.1 Chenopodiaceae Chenopodiaceae* 15.79 15.79 - - - 2.8 Cistaceae Cistus* 21.05 21.05 - - - 1.4 Ericaceae Erica 10.53 10.53 - - - 1.2 Euphorbiaceae Euphorbia bupleuroides (Desf.) Soják, 57.89 42.11 - 15.79 - 23.7 Fabaceae         Acacia 10.53 10.53 - - - 1.7 Vicia 21.05 21.05 - - - 1.1 Medicago 10.53 10.53 - - - 2.5 Ononis 31.58 31.58 - - - 1.7 Retama retam (Forssk.) Webb & Berthel. 42.11 31.58 5.26 5.26 - 19.2 Fagaceae Quercus* 10.53 10.53 - - - 1.1 Lamiaceae Thymus 26.32 26.32 - - - 1.7 Liliaceae Asphodelus microcarpus Parl. 10.53 10.53 - - - 1.2 Malvaceae Malva 15.79 15.79 - - - 2.7 Myrtaceae Eucalyptus 10.53 10.53 - - - 1.7 Oleaceae Olea* 21.05 21.05 - - - 1.4 Papaveraceae Papaver rhoeas L.* 10.53 10.53 - - - 2.2 Pinaceae Pinaceae* 5.26 5.26 - - - 1.1 Plantaginaceae Plantaginaceae* 15.79 15.79 - - - 5.2 Poaceae Poaceae* 31.58 31.58 - - - 6.3 Continued on the next page Table1: Frequency of distribution of taxa and their frequency classes in honey samples Acta agriculturae Slovenica, 118/3 – 2022 5 Pollen quality and sensory attributes of Algerian jujube (Ziziphus lotus (L.) Lam.) honeys in relation to the widespread distribution in the region (Battesti, 1990). Qualitative pollen analysis highlighted the dominance of Z. lotus (Figure 1) in honey samples as predominant with a maximum frequency of 97.1 %. The determination of botanical origin was based on the relative frequencies of the pollen types of nectarifer- ous species. In general, a honey is considered unifloral when the relative pollen frequency of onetaxon exceeds 45 % (Von Der Ohe et al., 2004). Z. lotus constitutes an abundant source of nectar frequently collected by honey bees justifying the unifloral designation “Jujube honey” attributed by beekeepers. Jujube is a species also visited for the pollen harvest. Moreover, we noted the second- ary presence of pollens from Thapsia garganica, Euphor- bia bupleuroides, Retama retam and Peganum harmala, important sources of nectar and pollen, with respective maximum levels of 17.3  %, 23.7  %, 19.2  % and 27.6  % (Table 1). 3.2 SENSORY ANALYSIS Regarding visual analysis, slight variations in color, ranging from 61 to 99 mm Pfund, were observed, which corresponds to a color range from amber yellow to light brown. Studies reported that the color interval of Al- gerian honeys ranged from 18 to 119  mm Pfund cor- responding to a color range varying from very light to dark brown. The very light honey samples are dominated by Citrus and Hedysarum while dark brown honeys are characterized by predominance ofEucalyptus, Apiaceae as Daucus and Rubus (Ouchemoukhet al., 2007; Bena- ziza et al., 2010). The profile of the aromas and flavors perceived in the 19 honey samples analyzed were shown in Table 2. The odor classes determined by the tasters were warm, floral and woody, with medium intensity. In terms of the perception of aromas, the general intensity is medium, and the aromatic classes perceived were warm caramel- ized, floral fruity and woody. The perception of chemical aroma was found only in two samples with low intensity. The sweet flavor was perceived with medium to high in- tensity. Z. lotus honey samples are characterized by higher fructose contents than glucose, and pH values between 5.17-5.8 for jujube honey from North Africa (Mekious et al., 2015; Chakir et al., 2016; Zerrouket al., 2017), and an average value of pH equal to 6.71 for jujube honey from China (Zhou et al., 2013). In all samples, the acidic flavor was weak, and the astringent sensation was medium. The piquant note was perceived in all the samples, but with a lower rate in 84.21 % of honey samples and *: nectarless species. F: Frequency of distribution of taxa in honey samples, M: Minor pollen (< 3 %), I: important minor pollen (3-15 %), A: Second- ary pollen (16-45 %), P: Predominant (> 45 %), Max: maximum recorded of pollen frequency Ranunculaceae Ranunculaceae 26.32 26.32 - - - 1.7 Resedaceae Reseda 10.53 10.53 - - - 1.2 Rhamnaceae Ziziphus lotus (L.) Lam. 100.00 - - - 100 97.1 Rosaceae Rosaceae 15.79 15.79 - - - 1.2 Tamaricaceae Tamarix 36.84 36.84 - - - 7.2 Nitrariaceae Peganum harmala L. 68.42 31.58 26.32 10.53 - 27.6 Sensory characteristics Olfactory assessment Intensity: medium Description: warm, floral, woody Intensity: low Description: chemical Tasting assessment Intensity Medium Sweetness Medium to high Acidity Low Aroma Intensity: medium Description: warm caramelised, floral-fruity, woody Persistence Medium Other sensations Intensity: low to medium Description: astringent, piquant Crystallization Absent Table 2: Sensory characteristics of Ziziphus lotus honey samples Acta agriculturae Slovenica, 118/3 – 20226 S. MEKIOUS et al. with medium rate in the rest of the samples. Pollen analy- sis of these samples showed the presence of Euphorbia bupleuroides pollen, either as an accompaniment with a maximum pollen frequency of 23.7 % or in rare, isolated cases at <3 %(Table 1). The nectar of this species gives a piquant note to honey; this is confirmed by the reference system for unifloral honeys established by the laboratory specifying that the honey samples were obtained from nectars of the Euphorbiaceae family species. Some notes are linked to the flora foraged by bees without exogenous contamination (Guyot-Declerck, 2001). The unifloral honey samples derived mainly from a single plant species (at least 45  % of pollen grain), may considerably differ in their sensory properties with highly prominent flavor and aroma (Lippolis, 2020).In all honey samples crystallization was absent. 4 CONCLUSION This study describes the melissopalynological and sensory characteristics of honey from the same floral ori- gin “Ziziphus lotus” produced in arid and semi-arid areas in Algeria. Overall, all the honey samples were character- ized by the predominance of Z. lotus pollen. This type of honey has slight variations in color, ranging from amber yellow to light brown. The perceived odor and aromatic classes were warm caramelized, floral fruity and spicy woody, with medium intensity. Sweet flavor, astringent sensation, acid flavor and spicy notes were also perceived in the honey samples. This work proves to be important for improving the knowledge in typical Algerian honeys and in particular in Jujube honey. In this context, the protection and the promotion of regional honeys will be ensured effectively when the various physicochemical, pollen and aromatic components can be described quite precisely. The definition of floral and regional appella- tions should be supported, and they are necessary for any quality approach to honey. It is therefore necessary to de- fine a set of pollen and sensory physicochemical stand- ards characteristic of unifloral honey. The acquisition of new data regarding melissopalynological and sensory analysis of honey allows the protection and the promo- tion of specific regional honeys. In this context, more studies based on the characterization of Z. lotus L. are needed to provide a normative framework and to deter- mine future specific standards composition for this type of honey. 5 ACKNOWLEDGMENTS We would like to thank the collaboration of the CARI laboratory, in particular the tasters Beatrice Per- at, Laurence Leclercq and Christine Delcourt. 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