Assessment of heavy metal levels in bee pollen (Apis mellifera L) from urban and rural areas of Egypt: implications for bioindication and food safety

Avaliação dos níveis de metais pesados ​​no pólen de abelha (Apis mellifera L) de áreas urbanas e rurais do Egito: implicações para bioindicação e segurança alimentar

Abstract

This study examined pollen samples from several parts of Egypt to assess the heavy metal levels present. Assessment of the performance of bee pollen (Apis mellifera L) as a bioindicator for the presence of Zn, Cd, Fe, Cu, Ni, Pb, Mo, and Cr in municipal and countryside areas was the main objective of this research and concurrently the study's central premise. Four places were in rural areas, and one was near the city center, giving five locations for three honeybee colonies. In order to compare pollen samples from urban and rural locations, heavy metal (Zn, Cd, Fe, Cu, Ni, Pb, Mo, and Cr) levels were measured in those gathered from these colonies. The study found that there were no significant differences in the levels of Cd in the pollen samples collected from different sites. Compared to urban areas, pollen sample heavy metal values in countryside regions generally decreased (P <0.05). It was determined that the concentrations of Cr, Fe, Cu, Ni, Mn, and Zn in pollen specimens varied significantly (P< 0.05) across the localities. Consistent with International Food Standards, the levels of heavy metals in pollen specimens collected from diverse areas were determined to be acceptable.

Keywords:
bee pollen; heavy metals; Apis mellifera ; Egypt

Resumo

Este estudo examinou amostras de pólen de várias partes do Egito para avaliar os níveis de metais pesados ​​presentes. A avaliação do desempenho do pólen de abelha (Apis mellifera L) como bioindicador da presença de Zn, Cd, Fe, Cu, Ni, Pb, Mo e Cr em áreas municipais e rurais foi o principal objetivo desta pesquisa e, ao mesmo tempo, a premissa central do estudo. Quatro lugares estavam em áreas rurais e um perto do centro da cidade, resultando em cinco locais para três colônias de abelhas. Para comparar amostras de pólen de locais urbanos e rurais, os níveis de metais pesados ​​(Zn, Cd, Fe, Cu, Ni, Pb, Mo e Cr) foram medidos naquelas coletadas dessas colônias. O estudo descobriu que não houve diferenças significativas nos níveis de Cd nas amostras de pólen coletadas de diferentes locais. Em comparação com áreas urbanas, os valores de metais pesados ​​da amostra de pólen nas regiões rurais geralmente diminuíram (P <0,05). Foi determinado que as concentrações de Cr, Fe, Cu, Ni, Mn e Zn nas amostras de pólen variaram significativamente (P<0,05) entre as localidades. De acordo com os Padrões Alimentares Internacionais, os níveis de metais pesados ​​em amostras de pólen coletadas em diversas áreas foram considerados aceitáveis.

Palavras-chave:
pólen de abelha; metais pesados; Apis mellifera ; Egito

1. Introduction

Propolis and bee pollen are frequently used to treat cancer, diabetes, and heart disease. Due to their high flavonoid and other phenolic component concentrations, propolis and bee pollen exhibit antioxidant and anti-inflammatory capabilities (Paulino et al., 2008; Newairy et al., 2009).

Understanding their contamination is crucial, given bee products' nourishing and curative qualities. Various types and pollution concentrations are present in some places where apiaries are situated. According to Przybyłowski and Wilczyńska (2001) honeybees may forage up to several kilometers away from their hives, an efficient way to sample the environment for air, soil, and plant pollutants.

Substantial heavy metals levels were detected in bee colonies' products in areas with rapid industrial or agriculture-related activity. Because of this, honey and other products made by honeybees are thought to be useful for detecting environmental pollution (Gilbert and Lisk, 1978; Üren et al., 1998).

There are instances where beekeeping is conducted near or within industrial and residential zones. Apiaries that are not suited for colonies of bees and manufacturing faults decrease the quality and intrinsic characteristics of bee products. The frequency of environmental issues caused by urbanization, industrialization, population growth, and shifting consumption patterns is rising. As an illustration, heavy metals are discharged into the atmosphere via ash and dust from diverse origins amass on vegetation (Taha et al., 2017), subsequently inducing soil and water resource contamination via sedimentation or precipitation. Furthermore, the buildup of heavy metals in fertilizers, wastewater, and agricultural compounds can have detrimental effects on both animals and humans (Yılmaz, 1996; Türközü and Şanlıer, 2012; Squadrone et al., 2020; Manouchehri et al., 2021).

According to literature, Apis mellifera L (honey bee) is a reliable bioindicator due to its intrinsic connection to its natural habitat (Skorbiłowicz et al., 2018).

Numerous researchers have been interested in the prevalence of metal contamination, which can be observed even at significant distances from industrial hubs and densely populated economic regions. Both environmental and artificial factors can contribute to the presence of metals in the environment (Aleksander-Kwaterczak and Rajca, 2015). Organic matter deposition, volcanic discharges, and soil development processes are all natural origins of metals. Human activities, including industrial and municipal effluent discharges, mining and metallurgical sector operations, road transport emissions, agricultural practices, and urban street pollution, are all considered anthropogenic metal sources (Bojakowska and Sokołowska, 1996, Kļaviņs et al., 2000; Kaniuczak, 2004). Prominent contributors to environmental pollution and metal contamination are sources associated with human activities. The environment becomes saturated with toxic elements entering plant and animal organisms (Skorbiłowicz et al., 2018). The detrimental impacts that metals have on ecosystems constitute a substantial ecological issue. Bioindication, as described by (Liu et al., 2009), is among the most ancient techniques used to evaluate the condition of the natural environment. Concerning managing the natural environment, evaluating the environment's condition by living organisms has emerged as a critical focus (Roman and Bico, 2010).

Heavy metals are absorbed through the epidermis, ingestion (including food and water), and respiration in animals and humans. These elements can be categorized as either essential or non-essential (Bayir and Aygun, 2022). Certain elements, including Se, Fe, Mn, and Cu, are crucial for the growth and optimal operation of the body. Conversely, even at low concentrations, the cellular composition can be altered by the accumulation of non-essential elements such as Pb, Cd, and Hg, thereby causing a variety of disorders (Tuzen et al., 2007; Uluozlu et al., 2007). In order to assess ecological contamination in a given area, it is possible to employ living organisms (known as biological indicators or biological monitors) that exhibit varying degrees of sensitivity to distinct pollutants (Yılmaz, 1996). Pollutant residues have been detected in honeybees and bee products, rendering them significant markers of ecological contamination (Porrini et al., 2003; Bogdanov et al., 2008; Ahmida et al., 2012; Zhelyazkova, 2012; Taha et al., 2017). Honeybees are adaptable to various environments, simple to maintain, exhibit a short life span and rapid reproduction rate, and can be transported anywhere as a colony. In pursuit of sustenance, they traverse an approximate 7 km² area surrounding the apiary; during flight activity, samples may be collected for analysis (Leita et al., 1996; Conti and Botrè, 2001; Perugini et al., 2011). Pollutants can contaminate bees and bee products from various sources, and the extent of contamination can vary based on the ecological circumstances of the beekeeping region (Hennessy et al., 2010; Costa-Silva et al., 2011; Pohl et al., 2012). According to studies, bee products in industrial districts and places with considerable automotive activity, especially near big towns and waste-burning facilities, have a higher concentration of heavy metal deposition (Aksoy et al., 2005; Bogdanov et al., 2008). This study aimed to assess the potential food safety risks associated with pollen and honey collected from areas close to suburban and industrial zones compared to rural regions, according to an evaluation of the levels of heavy metals in these substances.

In an investigation conducted in southern Poland, Formicki et al. (2013) assessed the metal quantities of cadmium, nickel, lead, iron, magnesium, and zinc in propolis, wax, multi-floral honey, and bee pollen sourced from various apiaries located in Małopolska Voivodeship.

According to environmental monitoring in this region, agriculture and industry are the primary sources of contamination, with heavy metals constituting the most prevalent and hazardous pollutants (Zamudio et al., 2010).

2. Materials and Methods

The current investigation was conducted in the apiary at the agriculture research center's Department of Bee Research, Institute of Plant Protection Research, from 2021 to 2023. Apiaries from various governorates in Egypt, including Doki (P1), Luxor (P2), Kafr Elzayate (P3), Tammai (P4), and Bshwyi (P5), were sampled for honey bee pollen. Fifteen randomly selected honeybee colonies of F1 Carniolan bees, Apis mellifera L. Five groups were formed, each with 3 colonies at every governorate. Pollen receptacles were emptied daily of fresh pollen granules, which were subsequently preserved in deep freeze until utilization. Prior to analysis, the gathered specimens were placed in containers made of plastic, kept at a temperature of -18 °C, and desiccated in a microwave at 120^o C for 10 minutes.

2.1. Sample preparation:

Different digestion methods can be used for pollen sample preparation, such as dry ash, wet digestion (Olaifa et al., 2004), and microwave digestion techniques (Parr et al., 2001). In our instance, the pollen samples were processed via microwave digestion. A precise weighing of ≈ 0.5 g of the specimen was achieved by adding ten mL of HNO₃. The samples were digested utilizing a preloaded technique dedicated to the MARS6 (CEM, Corporation, USA) microwave. The quantitative dilution of the solution to 25 mL was achieved by adding ultrapure water after it had cooled. Table 1 outlines the microwave digestion parameters.

Table 1
Microwave digestion system parameters.

Options	Internal Fiber Optic Temperature Control
	Internal Pressure Control
	DuoTemp Control
Pressure	800 psi
Temperature	210°C
Time	Hold: 15 min
	Ramp: 21 min
Power	400- 1800
Vessels	Easy Prep Full Starter Set, P/T Control

2.2. Instrumentation

Every measurement was executed utilizing the cutting-edge Agilent 4200 MP-AES model for microwave plasma atomic emission spectrometry, fueled by an Agilent 4107 Nitrogen Generator that provided the nitrogen gas plasma. The generator eliminates the necessity and financial burden associated with procuring gases of analytical grade. The One Neb nebulizer and a double-pass cyclonic spray chamber constituted the sample introduction system. The groundbreaking 4200 MP-AES is equipped with a torch and waveguide of the second generation, as well as mass flow-controlled nebulizer gas flow (Liberato et al., 2017). Compared to the FAAS, the central channel temperature of ≈5,000 K and the 4200 MP-AES's robust toroidal plasma eradicate many chemical interferences and increase the instrument's concentration working range. This eliminates the need for a procedure for element-specific preparation of samples, which is customary when employing FAAS, and increases the usability and affordability of the 4200 MP-AES. Model 4200 MP-AES represents a refinement of the initial emergent model 4100 MP-AES, which was made in an effort to improve performance and address certain deficiencies.

Delivering samples to the instrument via an Agilent SPS 3 autosampler enabled the system to function without human intervention. The apparatus functioned in a rapid sequential mode and was equipped with a CCD detector cooled by Peltier. The MP Expert software from Agilent enables the simultaneous, accurate, and effortless correction of both spectroscopic and noise interferences. The parameters of the procedure are detailed in Tables 2 and 3. Table 4 presents the quantification and detection limits for the method employed in determining metals in spices.

Table 2
Metals determined in pollen samples and their wavelengths and calibration ranges.

Metal	Wavelength (nm)	Calibration range (μg/mL)	Correlation coefficient
Cd	228.8	0 – 2.500	0.9992
Cr	425.4	0 – 2.000	0.9998
Cu	324.8	0 – 2.500	0.9992
Mn	403.1	0 – 2.000	0.9999
Pb	405.9	0 – 2.500	0.99996
Zn	213.9	0 – 1.500	0.9904
Fe		0 – 2.500	0.9991
Ni		0 – 2.500	0.9992

Table 3
Microwave plasma atomic emission parameters.

Parameter	Value
Replicates	3
Sample uptake delay	15 seconds
Pump rate	15 rpm
Stabilization time	15 second
Rinse time	30 seconds
Spray chamber	Double pass cyclonic
Autosampler	Agilent SPS 3
Sample pump tubing	Orange/green
Waste pump tubing	Blue/blue
Nebulizer	One Neb
Fast Pump during Uptake and Rinse	On (80 rpm)

Table 4
Determined limits of quantification (LOQ) and detection (LOD) for metals in pollen types.

Metal	LOQ (μg/mL)	LOD (μg/mL)
Cd	7.000X10-3	2.100 X10-3
Cr	0.333 X10-3	0.100 X10-3
Cu	2.333 X10-3	0.700 X10-3
Mn	0.667 X10-3	0.200 X10-3
Pb	0.011	3.300 X10-3
Zn	0.015	4.500 X10-3
Fe
Ni

• The limit of detection (LOD) is equivalent to a triplicate multiple of the standard deviation of ten measurements in a reference matrix. The LOQ is three times the length of the LOD. The apiary experiments were carried out at the Beekeeping Research Department, Dokki, Giza Governorate. This work was conducted during two years 2021-2022.

2.3. Statistical analysis

Heavy metal concentrations in five pollen, honey, and honey samples collected from each of the eight locations were determined. The information was analyzed by means of analysis of variance (ANOVA) utilizing the “SPSS” statistical software. The multiple-range test developed by Duncan in 1955 was utilized for comparing means. The data were displayed as the mean and standard error.

3. Results and Discussion

Table 5 and Figure 1, provide the standard errors and mean values of the following elements: cadmium, iron, chromium, nickel, lead, copper, manganese, and zinc, as detected in pollen samples. With the exception of Cd, the results revealed statistically significant variations in pollen specimens from various locations compared to the other elements (P < 0.05).

Table 5
Detection of the heavy metals contents in bee pollen samples with results from different locations in Egypt.

±SE	P5	P4	P3	P2	P1	Items
0.0003	0.0023 c	0.0016 cd	0.0012 d	0.0152 b	0.0250 a	Zn
0.00006	0.0075 a	0.0002b	0.0002 b	0.0002 b	0.0002 b	Cd
0.00006	0.0022 c	0.0986 a	0.0016 d	0.0008 e	0.0172 b	Fe
0.00006	0.0018 e	0.0022 d	0.0077 a	0.0044 c	0.0074 b	Cu
0.00026	0.0015 b	0.0012 b	0.0020 ab	0.0016 b	0.0027 a	Ni
0.00006	0.0063 b	0.0004 d	0.0005 d	0.0092 a	0.0022 c	Pb
0.00036	0.0070 c	0.0068 c	0.0059 c	0.0089 b	0.0150 a	Mo
0.00006	0.0007 c	0.0006 cd	0.0005 d	0.0082 a	0.0014 b	Cr

Figure 1
Comparison of the heavy metals contents in bee pollen samples with results from different locations in Egypt.

The pollen samples exhibited a variety of Cd levels ranging from 0.0002 to 0.0075 µg/kg. While the variation between locations was not statistically significant, Beshowi demonstrated a significantly different Cd content.

Similarly, Arslan and Arıkan 2013 reported that the Cd concentrations of pollen specimens collected from colonies situated on the highway at varying locations did not differ significantly.

In contrast to the Cd values reported by several literatures, 2022 for pollen from Poland and Turkey, respectively, the Cd value obtained in our study (0.0002–0.0075 µg/kg) was lower (Formicki et al., 2013; Bayir and Aygun, 2022).

The pollen produced by bees exhibited the greatest zinc content, with pollen from P1 being the most abundant in Zn. Propolis and wax derived from Bukowno and Proszowice, respectively, contained substantial quantities of zinc. Statistically significant variations in the level of zinc were observed among the specimens collected from each locality, as determined by one-way ANOVA.

The Ni, Mo, and Cr values of pollen samples were highest at P1 (0.025 mg/kg, 0.0027 mg/kg, 0.0150 mg/kg, 0, respectively) and lowest in the other four places.

One-way ANOVA revealed that the cadmium concentrations in the examined apiaries varied considerably and significantly. The level of significance was 0.0075. In general, bee pollen was predicted to contain the least amount of cadmium, with the lowest value found in bee pollen from samples P1, P2, P3, and P4. The bee pollen from P4 contained the least amount of nickel, while the pollen from P1 contained the most.

In every area that was examined, Pb was detected. The minimal level was observed in P4. From P2, elevated levels of lead were estimated. ANOVA indicated significant differences between all localities.

P4 exhibited the greatest estimated Fe content. Particular emphasis should be placed on the elevated levels of Fe observed in bee pollen sourced from the apiary in P1. One-way ANOVA revealed that differences between pollen samples from all locales were statistically significant.

Moreover, Conti and Botrè 2001 discovered that pollen samples collected from inner-city areas contained greater concentrations of Cr than those collected from urban areas (P < 0.01). Taha, Al-Jabr et al. 2017 conducted a study wherein they noticed that pollen specimens picked up from colonies situated at various points away from a cement manufacturing facility exhibited a significantly higher concentration of Cu (P < 0.05) in comparison to specimens gathered in proximity to the manufacturing facility. In addition, Taha, Al-Jabr et al. 2017 identified statistically significant variations in the Fe content of pollen collected from various plant species (P < 0.05). In their study, they did not identify any statistically significant variation in the Fe contents of pollen samples collected from colonies positioned at varying distances (Arslan and Arıkan, 2013).

Prasad et al. (2021) stated that Cr represents a significant global pollution concern. Environmentally hazardous sources of chromium include the printing and graphics industry, the metallurgical and chemical industries, electroplating or producing stainless steel alloys, and the manufacturing of fungicides. Numerous everyday items, including cement, pigments, and detergents, comprise Cr. The observed elevated levels of Cr in the bee organisms under investigation may have been influenced by factors such as print shops, jig and fixture factories, and allotments that have likely been treated with fungicides. Additionally, the combustion of coal can release chromium into the atmosphere and the environment, which undoubtedly contributes to the elevated concentration of chromium in bee bodies.

Furthermore, Fakhimzadeh and Lodenius (2000) discovered no statistically significant difference in the levels of manganese (Mn) in pollen samples between industrial, urban, and rural regions. In their study, Taha, Al-Jabr et al. 2017 discovered that the pollen samples collected from colonies positioned at varying distances from a cement factory exhibited a significantly higher Ni content in the samples closest to the factory (P < 0.05). In their study, It was discovered that pollen samples collected from colonies located in the city center contained significantly higher levels of Pb than those collected from colonies situated on the borders of the city (P < 0.01) (İlhan et al., 2023).

The pollen samples from the urban site contained the highest concentration of zinc (20.27 mg/kg), while those from the rural location contained the lowest (10.25 mg/kg) (P < 0.05), however, no statistically significant differences were observed in the Zn values of pollen samples collected from colonies positioned at varying distances from the highway (Arslan and Arıkan, 2013).

Our study yielded a zinc value ranging from 10.25 to 20.27 mg/kg, which was found to be lower than the value of 75.2 to 159.3 µg/g determined by (Formicki et al., 2013) in pollen from Poland. According to (Altunatmaz et al., 2017), botanical species influence mineral concentrations more than soil composition and geographical location.

Zinc may have its sources in the vicinity of allotments, the printing industry, the plastics sector, the application of plant protection products, and the utilization of fertilizers. Besides, a significant hazard is the combustion of coal. It has been confirmed that Zn near transportation routes originates primarily from motor oil and frequent and abrupt deceleration (Arslan and Arıkan, 2013).

4. Conclusions

Cr, Cu, Fe, Mn, Ni, and Zn values were lower in samples collected in rural areas. Notable variations were noted in the pollen samples in terms of Cr, Cu, Fe, Mn, Ni, Pb, and Zn. Specifically, the concentrations were found to be comparatively lower in rural regions than in urban areas. Additionally, Cd, Cr, Fe, Mn, Ni, Pb, and Zn concentrations in honeybee samples were lower in rural regions compared to urban ones. The pollen and honey samples exhibited Cd and Pb concentrations corresponding to the values specified by the International Food Standards. It is advisable to locate bee colonies in areas remote from residential and industrial zones, highways, contaminated water sources, and potential contamination hotspots for bee products in order to ensure the health of the bees and their products.

Bee pollen sourced from various apiaries and localities exhibited concentrations of toxic metals that are significantly below the permissible thresholds. Conversely, certain apiaries exhibited a significant degree of bee pollen contamination. There are correlations among the concentrations of certain metals. The absence of interdependencies in metal accumulation among successive products is likely due to unintentional contamination of plants and pollinators. Furthermore, various plant species and plant organs may contain varying metal concentrations. Thus, conducting exhaustively intricate analyses of all bee products could be beneficial for monitoring environmental metal contamination.

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Publication Dates

• Publication in this collection
  14 Mar 2025
• Date of issue
  2025

History

• Received
  02 July 2024
• Accepted
  09 Dec 2024