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Hypothesis-driven canonical correspondence analysis (CCA) of honey bees gut microbiota testing the significance of the treatment and dose effects on the abundances of all analysed OTUs. Samples are labelled according to the 6 groups studied.
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Apis mellifera is an important provider of ecosystem services, and during flight and foraging behaviour is exposed to environmental pollutants including airborne particulate matter (PM). While exposure to insecticides, antibiotics, and herbicides may compromise bee health through alterations of the gut microbial community, no data are available on...
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... structure of honey bee gut bacterial community was investigated at OTUs level, testing with a CCA model if the treatment (control vs chronic vs acute) and the dose had significant effects on the bacterial gut communities of the studied bees. Results (Fig. 3) indicated that the bees from the acute and the chronic experiments, being sampled at different life stages, hosted very different gut microbiota. Within each exposure time, it was found that samples were clearly grouped among doses for chronic exposure, but not for the acute. Similar outcomes were obtained by Principal Component ...Context 2
... features in the gut microbiota of honey-bees acutely exposed to TiO 2 . After defining that the two bee groups from the acute and the chronic exposure experiments had very different gut bacterial compositions (Figs. 3 and 5), separate analyses were carried out on the two groups, focusing on the relative presence of the most abundant OTUs classified at the species ...Context 3
... bacterial gut populations (Figs. 5, 6 and 7). This is expected since analyses were carried out after 1 dpe (day post-emergence) for the acute experiment and at 4 dpe for the chronic experiment. The β-diversity analyses here carried out by means of unconstrained (PCA and hierarchical clustering, Fig. 5 and Figure S2) and constrained (CCA, Fig. 3) analyses showed a clear distinction in bacterial community structure between the chronic and the acute experiments, and in the chronic experiments among controls and treated bees. These results are in line with several studies on other chemical stressors [16][17][18][19][20] , thus confirming that also PM modulates the honey bees gut ...Context 4
... as we know, this is the first study where the effects of TiO 2 particles where specifically studied on bees gut microbiota, but they can be compared with a number of studies that previously assessed the detrimental impacts of airborne PM on the bees physiology 12,13 . Regarding α-diversity indexes, we found a dose-dependent increase in diversity, (Fig. 3), while the opposite was found for the neonicotinoid insecticide Thiacloprid 18 , polystyrene particles at µm levels 52 , and antibiotics 16 . It must be highlighted that in these cited works a significant mortality was detected, whereas in our study sub-lethal doses were tested and no mortality registered. It can thus be speculated ...Similar publications
To determine the effect of honey bee (Apis mellifera L.) pollination on sunflower yield using the most appropriate number of beehives per unit area of crops is very important. By comparing the number of hives and yield components, we can satisfy optimal pollination needs and improve economic yields. For this purpose, a series of experiments were co...
Citations
... Research exploring the effects of oral exposure to pollutant PM on bees focused on alterations in the gut microbial population or cytological and histological abnormalities of the gut epithelium (Al Naggar et al. 2021). Worker bees exposed to submicrometric TiO 2 particles, a widespread airborne contaminant, showed differences in the bacterial community and alterations in the abundance of putative probiotic species (Papa et al. 2021b). ...
Several factors, including environmental degradation, air pollution, intense urbanization, excessive agriculture, and climate change, endanger the well-being of animals and plants. One of the major issues with an increasingly negative impact is agricultural contamination with pesticides and antibiotics. Seed coatings with neonicotinoid insecticides used as a protective layer against pests are shown to exceed the permissible limits in most cases. Neonicotinoid compounds bind to nicotinic acetylcholine receptors, therefore affecting the honey bees’ brain. Heavy metals in higher concentrations are lethal for honey bees, and the residue in bee products might pose a threat to human health. Highly effective acaricides used to treat Varroa destructor infestations in honey bee colonies have negative effects on honey bee reproduction, olfaction, and honey production. Furthermore, amitraz and fluvalinate are mostly found in the highest amounts and lead to decreased honey production and reduced colony reproduction, along with decreased learning ability and memory. However, scientific studies have shown that honey bees act as a reliable bio-indicator of environmental pollution. In response to the growing demand for bee products, the effects of adulteration and improper storage conditions have gotten worse and represent a new risk factor. In light of the shifting global economy, it is important to analyze consumer expectations and adjust manufacturing accordingly. By ensuring the manufacture of high-quality, traceable products devoid of drug residues, consumers will be better protected from subsequent health problems. This review’s objectives are based on the necessity of identifying the risks associated with honey bees and bee products.
Graphical abstract
... In the last decades, several studies have investigated the effects of PM in pollinators, and some have explored such effects using the toxicology and ecotoxicology approaches, especially targeting heavy metals PM (e.g., Zn, Ti, Pb, Cd, and Ag; Table 2) (Özkan et al. 2015;Dabour et al. 2019;AL Naggar et al. 2020;Papa et al. 2021c). While field-based studies correlating the health of pollinators with levels of pollutant PM are necessary to understand the actual effect of Fig. 5 A BSE image and B-D elemental maps of a mineral aggregate. ...
... Another study investigated the ecotoxicological effects of titanium dioxide (TiO 2 ), i.e., a widely used compound in various industries such as food and cosmetics as a filler and whitening agent, albeit classified as a possible human carcinogen (Group 2B) by the International Agency for Research on Cancer (IARC). In 2021, Papa and colleagues (Papa et al. 2021c) demonstrated the sublethal effects of TiO 2 sub-micrometer particles on the bee gut microbiota following acute and chronic exposure. In acute exposure, the probiotic Lactobacillus kimbladii was found to be significantly affected. ...
... In acute exposure, the probiotic Lactobacillus kimbladii was found to be significantly affected. Conversely, in chronic exposure, the L. kimbladii did not show inhibition but other important probiotic species were inhibited as L. apis and L. melliventris (Papa et al. 2021c). Finally, new studies demonstrated the presence of PM emitted from industries and vehicular traffic in honey and bee pollen (Papa et al. 2021a, b), suggesting the potential risk of pollutant particles entering the food chain and exposing bees and other pollinators to their ingestion (Fig. 1). ...
The honey bee Apis mellifera has long been recognized as an ideal bioindicator for environmental pollution. These insects are exposed to pollutants during their foraging activities, making them effective samplers of environmental contaminants, including heavy metals, pesticides, radionuclides, and volatile organic compounds. Recently, it has been demonstrated that honey bees can be a valuable tool for monitoring and studying airborne PM pollution, a complex mixture of particles suspended in the air, known to have detrimental effects on human health. Airborne particles attached to the bees can be characterised for their morphology, size, and chemical composition using a scanning electron microscopy coupled with X-ray spectroscopy, thus providing key information on the emission sources of the particles, their environmental fate, and the potential to elicit inflammatory injury, oxidative damage, and other health effects in living organisms. Here, we present a comprehensive summary of the studies involving the use of honey bees to monitor airborne PM, including the limits of this approach and possible perspectives. The use of honey bees as a model organism for ecotoxicological studies involving pollutant PM is also presented and discussed, further highlighting the role of the bees as a cornerstone of human, animal, and environmental health, according to the principles of the “One Health” approach.
... The visualization of sample surface morphologies of TiO 2 nanoparticles, PAA@TiO 2 , and CV adsorbed PAA@TiO 2 nanocomposite has been realized using SEM-EDX analysis, as depicted in Fig. 6. As seen in Fig. 6a, TiO 2 nanoparticles have an ellipsoid, spherical, and uniform size distribution structure [50,51]. The EDX mapping image and EDX spectrum of TiO 2 showed that TiO 2 contained the elements Ti and O (Figs. 6d and g). ...
The present paper focused on synthesizing a polyacrylamide-titanium dioxide (PAA@TiO2) nanocomposite using a cross-linking method with N, N′-methylenebisacrylamide and then using this composite to eliminate crystal violet (CV) dye from water and to characterize the adsorbent by XRD, FT-IR, and SEM-EDX techniques. The characterization revealed that TiO2 nanoparticles dispersed homogeneously within the polymer matrix. The maximum amount of adsorption was about 38.9 mg g⁻¹ under the adsorbent dose of 5 g L⁻¹, 500 mg L⁻¹ CV dye concentration, and pH 6.9. The interaction between the CV molecule and the PAA@TiO2 nanocomposite surface was studied using Monte Carlo (MC) and molecular dynamics (MD) simulations. The negative value of the Eads (− 586.56 kcal mol⁻¹) of the CV molecules onto the PAA@TiO2 nanocomposite surface gives credibility to the experimental results. All obtained results showed that PAA@TiO2 hybrid polymer nanocomposite could be an alternative adsorbent for crystal violet dye removal from wastewater.
... The concentration of TiO 2 used (250 ng/μL) exceeded the concentrations used in chronic exposure of honey bees. However, the dose of TiO 2 applied in our experiment (10 μg/ bee) was lower than the primary dose of TiO 2 employed in honey bee studies [3.2 or 32 μg/bee TiO 2 , converted from 10 and 100 ng/μL, respectively (Papa et al., 2021)]. Preliminary tests with P. helleri were performed to select the most appropriate doses for our study. ...
... These particles' size is like particle size encountered in nature (Cole et al., 2011;Gigault et al., 2018), as well as found in the bodies of honey bees (0.5 mm for PS or PET) (Edo et al., 2021). In the case of TiO 2 , similar particle sizes were also employed in assays involving bees (0.2 μm) (Papa et al., 2021). ...
The disposal of plastics and metal-derived compounds results in the contamination of the environment with nano/microparticles, leading to the exposure of various organisms to these harmful particles. However, the impacts of these particles on pollinating insects, which provide relevant ecosystem services, are not well understood. The aim of this study was to assess the effects of microscopic particles on the tropical pollinator Partamona helleri (Apinae: Meliponini), specifically evaluating the toxicity of plastic microparticles (polystyrene – PS, and polyethylene terephthalate – PET) and nanoparticles of a metal oxide (titanium dioxide – TiO2) via larval ingestion by bees reared in vitro. The survival rate of P. helleri larvae was not affected by the ingestion of particles of PS (500 ng/bee), PET (500 ng/bee), or TiO2 (10 μg/bee) compared to the non-treated diet (control or diet without the particles). Adults derived from treated larvae had increased body weight compared to the control, and the walking behavior of adults was altered by the ingestion of particles. Adults that ingested PET or TiO2 as larvae tended to rest for a longer time and interact more with other bees than the control. Hemocyte counts also changed, with a shift in the proportion of plasmatocytes and prohemocytes in treated individuals. Our findings suggest that even levels considered low for honey bees of exposure to plastic microparticles or metal nanoparticles can harm the health and behavior of stingless bees.
... Isolates were affiliated with 4 species: Fructobacillus fructosus (10), Apilactobacillus kunkeei (5), Lactobacillus kimbladii and Lactobacillus kullabergensis (4). These are a part of the honeybee microbiota, which is dominated by nine to ten phylotypes [8,22,56,57], within the predominant genera Lactobacillus (formerly) and Bifidobacterium [58,59]. These microbiota play a key role in the production of honey [7,22] and bee bread [60][61][62], which is in consistent with our findings since two identified species (Apilactobacillus kunkeei and Fructobacillus fructosus) were found in both honeybees and their honey. ...
Using culture enrichment methods, 100 strains of bacilli of lactic acid bacteria (LAB) were isolated from honeybee Apis mellifera intermissa and fresh honey, collected from apiaries located in the north-east of Algeria. Amongst all of the isolated LAB, 19 selected strains were closely affiliated to four species—Fructobacillus fructosus (10), Apilactobacillus kunkeei (5), Lactobacillus kimbladii and/or Lactobacillus kullabergensis (4)—using phylogenetic and phenotypic approaches. The in vitro probiotic characteristics (simulated gastrointestinal fluids tolerance, autoaggregation and hydrophobicity abilities, antimicrobial activity and cholesterol reduction) and safety properties (hemolytic activity, antibiotic resistance and absence of biogenic amines) were evaluated. The results indicated that some strains showed promising potential probiotic properties. In addition, neither hemolytic activity nor biogenic amines were produced. The carbohydrate fermentation test (API 50 CHL) revealed that the strains could efficiently use a broad range of carbohydrates; additionally, four strains belonging to Apilactobacillus kunkeei and Fructobacillus fructosus were found to be exopolysaccharides (EPS) producers. This study demonstrates the honeybee Apis mellifera intermissa and one of her products as a reservoir for novel LAB with potential probiotic features, suggesting suitability for promoting host health.
... Air pollution is the main environmental risk to health in the world, causing respiratory and cardiovascular diseases (World Health Organization, 2020). Particulate matter (PM) may be also ingested through contaminated food, causing alterations of gut microbiota (Li et al., 2017;Papa et al., 2021c). In urban areas, vehicular traffic is one of the major sources of PM, which may derive from both exhaust (i.e., tailpipe emissions) and non-exhaust sources, the latter primarily including wearing down of brake pads, discs and tyres, and the resuspension of road dust. ...
... SEM-EDX analyses were carried out on brake wear debris to assess the morphology, chemical composition, and size of the particles (Papa et al., 2021c). This technique was also used to identify the morphological and chemical markers of the brake wear debris in springtails and faeces samples. ...
... Samples were covered with graphite for SEM-EDX analysis (Zeiss Gemini 500, Oberkochen, Germany -Bruker QuantaX-Flash 6|30, Berlin, Germany) (Capitani et al., 2021;Negri et al., 2015;Papa et al., 2021aPapa et al., , 2021bPellecchia and Negri, 2018). Secondary electrons (SE), backscattered electrons (BSE) images, EDX point analyses, and EDX maps were acquired (Papa et al., 2021c;Pellecchia and Negri, 2018). A sample of brake wear debris and treated yeast samples plus control were also analysed. ...
Most of the heavy metals in urban environments derives from road traffic, particularly from tyres and brake wear (non-exhaust emission sources). These pollutants contaminate the soil, where several organisms have a primary ecosystem role (e.g., springtails, ants, earthworms). Springtails (Collembola) are soil-dwelling animals regulating soil fertility, flow of energy through above- and below-ground food webs, and they contribute to soil microbial community dispersion and biodiversity maintenance. In this study we investigated the ecotoxicological effects of oral exposure to particles emitted from brake pads and cast-iron brake discs in the euedaphic collembola species Orthonychiurus folsomi under laboratory conditions. Our results showed that chronic exposure to brake wear particles can have sub-lethal effects both at low and high concentrations and it can cause histological alterations. Here, SEM-EDX was applied to observe the particulate and we found its chemical markers in the gut and faeces of collembola, while histological analysis detected alterations of the digestive and reproductive systems and of the abdominal fat body at high concentrations.
... A wide range of xenobiotics can affect size, composition and functional properties of the honey bee gut microbiota (Daisley et al., 2020), as it has been demonstrated for pesticides (i.e., glyphosate, Motta et al., 2018), airborne particular matters (i.e., titanium dioxide, Papa et al., 2021) and antibiotics (e.g., tetracycline, Raymann et al., 2017). In certain countries, including the United States, antibiotics, mainly tetracycline derivates, are applied in apiculture as a preventive or control measure against two common larval diseases, American and European Foulbrood, caused by Paenibacillus larvae and Melissococcus plutonius, respectively (Genersch, 2010;Tian et al., 2012;Daisley et al., 2020). ...
Gut microbiota are known to foster pollen digestion in honey bee workers, Apis mellifera, thereby enhancing longevity and body weight gain. However, it is currently not known how longevity and body weight gain are effected when gut microbiota are reduced in bees with or without access to pollen. Here, using a hoarding cage setup with freshly emerged summer workers, we manipulated the gut microbiota of half the bees with the antibiotic tetracycline (ABX), and left the other half untreated on a sucrose solution diet. Afterwards, all bees were assigned to either sucrose diets or sucrose plus ad libitum access to pollen (N = 4 treatments, N = 26 bees/treatment, N = 10 replicates/treatment, N = 1,040 total workers). The data confirm that pollen has a positive effect on longevity and body weight in workers with an unmanipulated gut microbiota. Surprisingly, the antibiotics alone also improved the longevity and body weight of the workers fed a strictly sucrose diet, potentially explained by the reduction of harmful bacteria. However, this positive effect was reversed from an observed antagonistic interaction between pollen and antibiotics, underscoring the innate value of natural microbiota on pollen digestion. In conclusion, a combination of adequate pollen supply and an unmanipulated gut microbiota appears crucial to honey bee worker health, calling for respective efforts to ensure both in managed colonies.
... Current studies on the oral exposure of pollinators to particles indicate both lethal and sub-lethal effects [101,102]. In particular, cytological and histological modifications of the gut epithelium or alterations in the gut microbial community have been demonstrated [103][104][105]. Indeed, ingested particles can come into contact with epithelial cells and the microbiome lining the gut, posing hazards to the gut community [105]. ...
... In particular, cytological and histological modifications of the gut epithelium or alterations in the gut microbial community have been demonstrated [103][104][105]. Indeed, ingested particles can come into contact with epithelial cells and the microbiome lining the gut, posing hazards to the gut community [105]. Recent evidence also suggests that gut microbiota disruption can severely affect the health of bees [106] and further studies are urgently needed to highlight any potential role of the gut microbiome alteration in the Colony Collapse Disorder, a phenomenon that causes loss of bee colonies worldwide [102]. ...
Ecosystems provide many services that are essential for human activities and for our well-being. Many regulation services are interconnected and are fundamental in mitigating and hindering the negative effects of several phenomena such as pollution. Pollution, in particular airborne particulate matter (PM), represents an important risk to human health. This perspective aims at providing a current framework that relates ecosystem services, regulating services, pollination, and human health, with particular regards to pollution and its impacts. A quantitative literature analysis on the topic has been adopted. The health repercussions of problems related to ecosystem services, with a focus on the effects of atmospheric particulate matter, have been highlighted in the work throughout a case study. In polluted environments, pollinators are severely exposed to airborne PM, which adheres to the insect body hairs and can be ingested through contaminated food resources, i.e., pollen and honey. This poses a serious risk for the health of pollinators with consequences on the pollination service and, ultimately, for human health.
... Pollen contamination by PM may also threaten the overall health of bees. Previous studies on the oral exposure of bees to airborne particles indicate cytological and histological modifications of the gut epithelium or alterations in the gut microbial community [11,12]. ...
The global demand for bee pollen as a dietary supplement for human nutrition is increasing. Pollen, which comprises proteins and lipids from bees’ diets, is rich in essential amino acids, omega fatty acids, and bioactive compounds that can have beneficial effects on human health. However, bee pollen may also contain contaminants due to environmental contamination. To date, data on bee pollen contamination by environmental pollutants refer almost exclusively to pesticides and heavy metals, and very little information is available on the potential contamination of bee pollen by airborne particulate matter (PM), a ubiquitous pollutant that originates from a wide range of anthropogenic sources (e.g., motor vehicles, industrial processes, agricultural operations). In the present study, pollen grains collected by forager bees living in an industrial area of the Po Valley (Northern Italy) were analyzed for contamination by inorganic PM. The morpho-chemical characterization of inorganic particles using SEM/EDX allowed us to identify different emission sources and demonstrate the potential risk of PM entering the food chain and exposing bees to its ingestion.
... The publication trends of the relationships between honey and health research are reported in Figure 2. The first paper on this topic was published in 1915 by an anonymous author and concerns extra-floral nectaries [215]. The most recent work was published by Papa et al. [216] and studied the acute and chronic effects of titanium dioxide (TiO 2 ) particulate matter on honeybee gut microbiota under laboratory conditions. Acute and chronic oral administration of ultrapure TiO 2 particulate matter to adult bees altered the bee microbial community; therefore, airborne particulate matter may represent an additional risk factor for honeybee health, promoting sublethal effects against the gut microbiota [216]. ...
... The most recent work was published by Papa et al. [216] and studied the acute and chronic effects of titanium dioxide (TiO 2 ) particulate matter on honeybee gut microbiota under laboratory conditions. Acute and chronic oral administration of ultrapure TiO 2 particulate matter to adult bees altered the bee microbial community; therefore, airborne particulate matter may represent an additional risk factor for honeybee health, promoting sublethal effects against the gut microbiota [216]. The second most recent paper was a work by Sharif et al. [217] that, by looking for new, non-invasive methods to monitor the health status of the colony, introduced new features for classifying beehive audio samples using the soundscape indices [217]. ...
Biodiversity strengthens the productivity of any ecosystem (agricultural land, forest, lake, etc.). The loss of biodiversity contributes to food and energy insecurity; increases vulnerability to natural disasters, such as floods or tropical storms; and decreases the quality of both life and health. Wild and managed bees play a key role in maintaining the biodiversity and in the recovery and restoration of degraded habitats. The novelty character of this perspective is to give an updated representation of bee products’ biodiversity, sustainability, and health relationship. The role of bees as bioindicators, their importance in the conservation of biodiversity, their ecosystem services, and the variety of the bee products are described herein. An overview of the main components of bee products, their biological potentials, and health is highlighted and detailed as follows: (i) nutritional value of bee products, (ii) bioactive profile of bee products and the related beneficial properties; (iii) focus on honey and health through a literature quantitative analysis, and (iv) bee products explored through databases. Moreover, as an example of the interconnection between health, biodiversity, and sustainability, a case study, namely the “Cellulose Park”, realized in Rome (Italy), is presented here. This case study highlights how bee activities can be used to assess and track changes in the quality of agricultural ecosystems—hive products could be valid indicators of the quality and health of the surrounding environment, as well as the changes induced by the biotic and abiotic factors that impact the sustainability of agricultural production and biodiversity conservation in peri-urban areas.
