Honeybees and Wild Bees Health

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Behavior and Pathology".

Deadline for manuscript submissions: closed (30 June 2021) | Viewed by 56652

Special Issue Editors


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Guest Editor
Department of Agricultural Science, University of Sassari, Viale Italia 39, 07100 Sassari, Italy
Interests: honeybee biology and behaviour; social immunity; honeybee pathogens and parasites; host-parasite interactions; wild bees; pollinators; stress factors.

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Guest Editor
General Zoology, Institute of Biology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, D-06120 Halle (Saale), Germany
Interests: insect evolutionary ecology; plant–pollinator interactions; insect biodiversity; host–parasite interactions; pollination

Special Issue Information

Dear colleague,

The pollination services provided by bees are vitally important for ecosystem functioning and crop production. However, in recent decades, numerous reports have shown extensive losses of honeybee colonies and a decline in numbers of wild bees, with negative consequences for terrestrial ecosystems, the economy, and food security.

These losses have been attributed to many stress factors, including pesticide exposure, habitat loss or degradation, invasive species, predators, parasites, diseases, and climate change. These factors do not act alone and often show synergistic interactions that are difficult to predict.

In this Special Issue, we would like to publish original, theoretical or empirical research, reviews, quantitative meta-analyses or perspective articles focusing on how stress factors affect the health of managed and wild bees and on the defense mechanisms adopted at the individual level and, in the case of social species, also at the colony level. The topics can be related to molecular, physiological, behavioral, and other aspects of honeybees’ and wild bees’ health and extend to bee declines and pollination services.

Prof. Alberto Satta
Dr. Panagiotis Theodorou
Guest Editors

Manuscript Submission Information

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Keywords

  • pollinators
  • stress factors
  • immune defense
  • social immunity
  • bee nutritional health
  • colony performance
  • pesticides
  • fitness
  • population declines

Published Papers (12 papers)

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Research

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12 pages, 3539 KiB  
Article
Study of Morphological Features in Pre-Imaginal Honey Bee Impaired by Varroa destructor by Means of Computer Tomography
by Tamás Sipos, Tamás Donkó, Ildikó Jócsák and Sándor Keszthelyi
Insects 2021, 12(8), 717; https://doi.org/10.3390/insects12080717 - 11 Aug 2021
Cited by 3 | Viewed by 1963
Abstract
The honey bee (Apis mellifera L. 1778) is an essential element in maintaining the diversity of the biosphere and food production. One of its most important parasites is Varroa destructor, Anderson and Trueman, 2000, which plays a role in the vectoring [...] Read more.
The honey bee (Apis mellifera L. 1778) is an essential element in maintaining the diversity of the biosphere and food production. One of its most important parasites is Varroa destructor, Anderson and Trueman, 2000, which plays a role in the vectoring of deformed wing virus (DWV) in honey bee colonies. Our aim was to measure the potential morphometric changes in the pre-imaginal stage of A. mellifera caused by varroosis by means of computed tomography, hence supplying evidence for the presumable role that V. destructor plays as a virus vector. Based on our results, the developmental disorders in honey bees that ensued during the pre-imaginal stages were evident. The total-body length and abdomen length of parasitized specimens were shorter than those of their intact companions. In addition, the calculated quotients of the total-body/abdomen, head/thorax, and head/abdomen in parasitized samples were significantly altered upon infestation. In our view, these phenotypical disorders can also be traced to viral infection mediated by parasitism, which was confirmed by reverse transcriptase polymerase chain reaction (RT-PCR) analysis. Capitalizing on a non-destructive method, our study reveals the deformation of the honey bee due to mite parasitism and the intermediary role this pest plays in viral infection, inside the brood cell. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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32 pages, 4076 KiB  
Article
Combined Effects of Pesticides and Electromagnetic-Fields on Honeybees: Multi-Stress Exposure
by Daniela Lupi, Marco Palamara Mesiano, Agnese Adani, Roberto Benocci, Roberto Giacchini, Paolo Parenti, Giovanni Zambon, Antonio Lavazza, Maria Beatrice Boniotti, Stefano Bassi, Mario Colombo and Paolo Tremolada
Insects 2021, 12(8), 716; https://doi.org/10.3390/insects12080716 - 10 Aug 2021
Cited by 14 | Viewed by 10034
Abstract
Honeybee and general pollinator decline is extensively reported in many countries, adding new concern to the general biodiversity loss. Many studies were addressed to assess the causes of pollinator decline, concluding that in most cases multi-stress effects were the most probable ones. In [...] Read more.
Honeybee and general pollinator decline is extensively reported in many countries, adding new concern to the general biodiversity loss. Many studies were addressed to assess the causes of pollinator decline, concluding that in most cases multi-stress effects were the most probable ones. In this research, the combined effects of two possible stress sources for bees, pesticides and electromagnetic fields (multi-stress conditions), were analyzed in the field. Three experimental sites were chosen: a control one far from direct anthropogenic stress sources, a pesticide-stress site and multi-stress one, adding to the same exposure to pesticides the presence of an electromagnetic field, coming from a high-voltage electric line. Experimental apiaries were monitored weekly for one year (from April 2017 to April 2018) by means of colony survival, queen activity, storage and brood amount, parasites and pathogens, and several biomarkers in young workers and pupae. Both exposure and effect biomarkers were analysed: among the first, acetylcholinesterase (AChE), catalase (CAT), glutathione S-transferase (GST) and alkaline phosphatase (ALP) and Reactive Oxygen Species (ROS); and among the last, DNA fragmentation (DNAFRAGM) and lipid peroxidation (LPO). Results showed that bee health conditions were the worst in the multi-stress site with only one colony alive out of the four ones present at the beginning. In this site, a complex picture of adverse effects was observed, such as disease appearance (American foulbrood), higher mortality in the underbaskets (common to pesticide-stress site), behavioral alterations (queen changes, excess of honey storage) and biochemical anomalies (higher ALP activity at the end of the season). The overall results clearly indicate that the multi-stress conditions were able to induce biochemical, physiological and behavioral alterations which severely threatened bee colony survival. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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14 pages, 2093 KiB  
Article
Impact of Nosema Disease and American Foulbrood on Gut Bacterial Communities of Honeybees Apis mellifera
by Poonnawat Panjad, Rujipas Yongsawas, Chainarong Sinpoo, Chonthicha Pakwan, Phakamas Subta, Sasiprapa Krongdang, Ammarin In-on, Siriwadee Chomdej, Panuwan Chantawannakul and Terd Disayathanoowat
Insects 2021, 12(6), 525; https://doi.org/10.3390/insects12060525 - 06 Jun 2021
Cited by 12 | Viewed by 3201
Abstract
Honeybees, Apis mellifera, are important pollinators of many economically important crops. However, one of the reasons for their decline is pathogenic infection. Nosema disease and American foulbrood (AFB) disease are the most common bee pathogens that propagate in the gut of honeybees. [...] Read more.
Honeybees, Apis mellifera, are important pollinators of many economically important crops. However, one of the reasons for their decline is pathogenic infection. Nosema disease and American foulbrood (AFB) disease are the most common bee pathogens that propagate in the gut of honeybees. This study investigated the impact of gut-propagating pathogens, including Nosema ceranae and Paenibacillus larvae, on bacterial communities in the gut of A. mellifera using 454-pyrosequencing. Pyrosequencing results showed that N. ceranae was implicated in the elimination of Serratia and the dramatic increase in Snodgrassella and Bartonella in adult bees’ guts, while bacterial communities of P. larvae-infected larvae were not affected by the infection. The results indicated that only N. ceranae had an impact on some core bacteria in the gut of A. mellifera through increasing core gut bacteria, therefore leading to the induction of dysbiosis in the bees’ gut. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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17 pages, 3465 KiB  
Article
Honey Bee Health in Maine Wild Blueberry Production
by Francis A. Drummond, Jennifer Lund and Brian Eitzer
Insects 2021, 12(6), 523; https://doi.org/10.3390/insects12060523 - 05 Jun 2021
Cited by 5 | Viewed by 2567
Abstract
A two-year study was conducted in Maine wild blueberry fields (Vaccinium angustifolium Aiton) on the health of migratory honey bee colonies in 2014 and 2015. In each year, three or five colonies were monitored at each of nine wild blueberry field locations [...] Read more.
A two-year study was conducted in Maine wild blueberry fields (Vaccinium angustifolium Aiton) on the health of migratory honey bee colonies in 2014 and 2015. In each year, three or five colonies were monitored at each of nine wild blueberry field locations during bloom (mid-May until mid-June). Colony health was measured by assessing colony strength during wild blueberry bloom. Potential factors that might affect colony health were queen failure or supersedure; pesticide residues on trapped pollen, wax comb, and bee bread; and parasites and pathogens. We found that Varroa mite and pesticide residues on trapped pollen were significant predictors of colony health measured as the rate of change in the amount of sealed brood during bloom. These two factors explained 71% of the variance in colony health over the two years. Pesticide exposure was different in each year as were pathogen prevalence and incidence. We detected high prevalence and abundance of two recently discovered pathogens and one recently discovered parasite, the trypanosome Lotmaria passim Schwartz, the Sinai virus, and the phorid fly, Apocephalus borealis Brues. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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12 pages, 11762 KiB  
Article
Modeling the Invasion of the Large Hive Beetle, Oplostomusfuligineus, into North Africa and South Europe under a Changing Climate
by Hossam Abou-Shaara, Sara A. Alashaal, Eslam M. Hosni, Mohamed G. Nasser, Mohammad J. Ansari and Sulaiman Ali Alharbi
Insects 2021, 12(4), 275; https://doi.org/10.3390/insects12040275 - 24 Mar 2021
Cited by 21 | Viewed by 3667
Abstract
Some beetle species can attack honeybee colonies, causing severe damage to beekeeping. These pests include Oplostomus fuligineus, which is also known as the Large Hive Beetle (LHB). This beetle is native to Sub-Saharan Africa and has recently also been recorded in some [...] Read more.
Some beetle species can attack honeybee colonies, causing severe damage to beekeeping. These pests include Oplostomus fuligineus, which is also known as the Large Hive Beetle (LHB). This beetle is native to Sub-Saharan Africa and has recently also been recorded in some parts of North Africa. It feeds mainly on young bee larvae and stored food within the colonies, causing severe damage to weak colonies. The present work sheds light on the current and future distribution (from 2050 to 2070) of this beetle in Africa and South Europe using species distribution modeling. Maxent was used to model the invasion of LHB. The Shared Socioeconomic Pathways (SSPs) 126 and 585 were used to model the future distribution of LHB. The Maxent models showed satisfactory results with a high Area Under Curve (AUC) value (0.85 ± 0.02). Furthermore, the True Skill Statistics (TSS) value was equal to 0.87. The current and future maps showed a high risk of invasion because of temperature variation in most of the parts of North Africa and South Europe. The maps also predicted the future invasion of LHB into other countries, mainly through southern Europe. These predictive risk maps will help quarantine authorities in highly relevant countries to prevent the expansion of this pest outside of its natural range. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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18 pages, 15467 KiB  
Article
Evaluating the Impact of Post-Emergence Weed Control in Honeybee Colonies Located in Different Agricultural Surroundings
by Ivana N. Macri, Diego E. Vázquez, Eduardo A. Pagano, Jorge A. Zavala and Walter M. Farina
Insects 2021, 12(2), 163; https://doi.org/10.3390/insects12020163 - 14 Feb 2021
Cited by 4 | Viewed by 3338
Abstract
The honeybee Apis mellifera is exposed to agricultural intensification, which leads to an improved reliance upon pesticide use and the reduction of floral diversity. In the present study, we assess the changes in the colony activity and the expression profile of genes involved [...] Read more.
The honeybee Apis mellifera is exposed to agricultural intensification, which leads to an improved reliance upon pesticide use and the reduction of floral diversity. In the present study, we assess the changes in the colony activity and the expression profile of genes involved in xenobiotic detoxification in larvae and adult honeybees from three apiaries located in agricultural environments that differ in their proportion of the crop/wild flora. We evaluated these variables before and after the administration of a mixture of three herbicides during the summer season. The expression of several cytochrome P450 monooxygenases decreased significantly in larvae after post-emergence weed control and showed significant differences between apiaries in the case of honeybee workers. Principal component analysis (PCA) revealed that colonies located in the plot near to a wetland area exhibited a different relative gene expression profile after herbicide application compared with the other plots. Moreover, we found significant positive correlations between pollen collection and the pesticide detoxification genes that discriminated between plots in the PCA. Our results suggest that nutrition may modify herbicide impact on honeybees and that larvae are more harmed than adults in agroecosystems, a factor that will alter the colonies’ population growth at the end of the blooming period. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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13 pages, 1420 KiB  
Article
Host-Parasite Co-Evolution in Real-Time: Changes in Honey Bee Resistance Mechanisms and Mite Reproductive Strategies
by Arrigo Moro, Tjeerd Blacquière, Delphine Panziera, Vincent Dietemann and Peter Neumann
Insects 2021, 12(2), 120; https://doi.org/10.3390/insects12020120 - 29 Jan 2021
Cited by 17 | Viewed by 7141
Abstract
Co-evolution is a major driving force shaping the outcome of host-parasite interactions over time. After host shifts, the lack of co-evolution can have a drastic impact on novel host populations. Nevertheless, it is known that Western honey bee (Apismellifera) populations [...] Read more.
Co-evolution is a major driving force shaping the outcome of host-parasite interactions over time. After host shifts, the lack of co-evolution can have a drastic impact on novel host populations. Nevertheless, it is known that Western honey bee (Apismellifera) populations can cope with host-shifted ectoparasitic mites (Varroa destructor) by means of natural selection. However, adaptive phenotypic traits of the parasites and temporal variations in host resistance behavior are poorly understood. Here, we show that mites made adaptive shifts in reproductive strategy when associated with resistant hosts and that host resistance traits can change over time. In a fully-crossed field experiment, worker brood cells of local adapted and non-adapted (control) A.mellifera host colonies were infested with mites originating from both types of host colonies. Then, mite reproduction as well as recapping of cells and removal of infested brood (i.e., Varroa Sensitive Hygiene, VSH) by host workers were investigated and compared to data from the same groups of host colonies three years earlier. The data suggest adaptive shifts in mite reproductive strategies, because mites from adapted hosts have higher probabilities of reproduction, but lower fecundity, when infesting their associated hosts than mites in treated colonies. The results confirm that adapted hosts can reduce mite reproductive success. However, neither recapping of cells nor VSH were significantly expressed, even though the latter was significantly expressed in this adapted population three years earlier. This suggests temporal variation in the expression of adaptive host traits. It also appears as if mechanisms not investigated here were responsible for the reduced mite reproduction in the adapted hosts. In conclusion, a holistic view including mite adaptations and studies of the same parasite/host populations over time appears overdue to finally understand the mechanisms enabling survival of V.destructor-infested honey bee host colonies. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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12 pages, 1282 KiB  
Article
Network Centrality as an Indicator for Pollinator Parasite Transmission via Flowers
by Niels Piot, Guy Smagghe and Ivan Meeus
Insects 2020, 11(12), 872; https://doi.org/10.3390/insects11120872 - 08 Dec 2020
Cited by 15 | Viewed by 2773
Abstract
Parasites are important actors within ecosystems. However, a key aspect to unraveling parasite epidemiology is understanding transmission. The bee pollinator community harbors several multihost parasites, which have been shown to be able to spread between species via flowers. Hence the plant–pollinator network can [...] Read more.
Parasites are important actors within ecosystems. However, a key aspect to unraveling parasite epidemiology is understanding transmission. The bee pollinator community harbors several multihost parasites, which have been shown to be able to spread between species via flowers. Hence the plant–pollinator network can provide valuable information on the transmission of these parasites between species. Although several controlled experiments have shown that flowers function as a transmission hub for parasites, the link with the plant–pollinator network has rarely been addressed in the field. Here, one can hypothesize that the most central flowers in the network are more likely to enable parasite transmission between species. In this study, we test this hypothesis in three local plant–pollinator networks and show that the centrality of a plant in a weighted plant–pollinator network is a good predictor of the presence of multihost pollinator parasites on the plant’s flowers. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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12 pages, 900 KiB  
Article
Positive Correlation between Pesticide Consumption and Longevity in Solitary Bees: Are We Overlooking Fitness Trade-Offs?
by Verena Strobl, Domenic Camenzind, Angela Minnameyer, Stephanie Walker, Michael Eyer, Peter Neumann and Lars Straub
Insects 2020, 11(11), 819; https://doi.org/10.3390/insects11110819 - 20 Nov 2020
Cited by 11 | Viewed by 3442
Abstract
The ubiquitous use of pesticides is one major driver for the current loss of biodiversity, and the common practice of simultaneously applying multiple agrochemicals may further contribute. Insect toxicology currently has a strong focus on survival to determine the potential hazards of a [...] Read more.
The ubiquitous use of pesticides is one major driver for the current loss of biodiversity, and the common practice of simultaneously applying multiple agrochemicals may further contribute. Insect toxicology currently has a strong focus on survival to determine the potential hazards of a chemical routinely used in risk evaluations. However, studies revealing no effect on survival or even indicating enhanced survival are likely to be misleading, if potential trade-offs between survival and other physiological factors are overlooked. Here, we used standard laboratory experiments to investigate the sublethal (i.e., food consumption) and lethal (i.e., survival) effects of two common agricultural pesticides (Roundup® and clothianidin) on adult female solitary bees, Osmia bicornis. The data showed no significant effect of the treatment on cumulative survival; however, a significant positive correlation between herbicide and insecticide exposure and age was revealed, i.e., bees exposed to higher dosages lived longer. As no significant differences in daily food consumption were observed across treatment groups, increased food intake can be excluded as a factor leading to the prolonged survival. While this study does not provide data on fitness effects, two previous studies using solitary bees observed significant negative effects of neonicotinoid insecticides on fitness, yet not on survival. Thus, we conjecture that the observed non-significant effects on longevity may result from a trade-off between survival and reproduction. The data suggest that a focus on survival can lead to false-negative results and it appears inevitable to include fitness or at least tokens of fitness at the earliest stage in future risk assessments. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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20 pages, 3153 KiB  
Article
Physiological Analysis and Transcriptome Analysis of Asian Honey Bee (Apis cerana cerana) in Response to Sublethal Neonicotinoid Imidacloprid
by Jing Gao, San-Sheng Jin, Yan He, Jin-Hong Luo, Chun-Qin Xu, Yan-Yan Wu, Chun-Shen Hou, Qiang Wang and Qing-Yun Diao
Insects 2020, 11(11), 753; https://doi.org/10.3390/insects11110753 - 03 Nov 2020
Cited by 25 | Viewed by 3782
Abstract
Asian honey bee (Apis cerana) is the most important Chinese indigenous species, while its toxicological characteristic against neonicotinoids is poorly known. Here, we combined physiological experiments with a genome-wide transcriptome analysis to understand the molecular basis of genetic variation that responds [...] Read more.
Asian honey bee (Apis cerana) is the most important Chinese indigenous species, while its toxicological characteristic against neonicotinoids is poorly known. Here, we combined physiological experiments with a genome-wide transcriptome analysis to understand the molecular basis of genetic variation that responds to sublethal imidacloprid at different exposure durations in A. cerana. We found that LC5 dose of imidacloprid had a negative impact on climbing ability and sucrose responsiveness in A. cerana. When bees were fed with LC5 dose of imidacloprid, the enzyme activities of P450 and CarE were decreased, while the GSTs activity was not influenced by the pesticide exposure. The dynamic transcriptomic profiles of A. cerana workers exposed to LC5 dose of imidacloprid for 1 h, 8 h, and 16 h were obtained by high-throughput RNA-sequencing. We performed the expression patterns of differentially expressed genes (DEGs) through trend analysis, and conducted the gene ontology analysis and KEGG pathway enrichment analysis with DEGs in up- and down-regulated pattern profiles. We observed that more genes involved in metabolism, catalytic activity, and structural molecule activity are down-regulated; while more up-regulated genes were enriched in terms associated with response to stimulus, transporter activity, and signal transducer activity. Additionally, genes related to the phenylalanine metabolism pathway, FoxO signaling pathway, and mTOR signaling pathway as indicated in the KEGG analysis were significantly up-related in the exposed bees. Our findings provide a comprehensive understanding of Asian honey bee in response to neonicotinoids sublethal toxicity, and could be used to further investigate the complex molecular mechanisms in Asian honey bee under pesticide stress. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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20 pages, 2182 KiB  
Article
Chronic High Glyphosate Exposure Delays Individual Worker Bee (Apis mellifera L.) Development under Field Conditions
by Richard Odemer, Abdulrahim T. Alkassab, Gabriela Bischoff, Malte Frommberger, Anna Wernecke, Ina P. Wirtz, Jens Pistorius and Franziska Odemer
Insects 2020, 11(10), 664; https://doi.org/10.3390/insects11100664 - 27 Sep 2020
Cited by 21 | Viewed by 4082
Abstract
The ongoing debate about glyphosate-based herbicides (GBH) and their implications for beneficial arthropods gives rise to controversy. This research was carried out to cover possible sublethal GBH effects on the brood and colony development, adult survival, and overwintering success of honey bees ( [...] Read more.
The ongoing debate about glyphosate-based herbicides (GBH) and their implications for beneficial arthropods gives rise to controversy. This research was carried out to cover possible sublethal GBH effects on the brood and colony development, adult survival, and overwintering success of honey bees (Apis mellifera L.) under field conditions. Residues in bee relevant matrices, such as nectar, pollen, and plants, were additionally measured. To address these questions, we adopted four independent study approaches. For brood effects and survival, we orally exposed mini-hives housed in the “Kieler mating-nuc” system to sublethal concentrations of 4.8 mg glyphosate/kg (T1, low) and 137.6 mg glyphosate/kg (T2, high) over a period of one brood cycle (21 days). Brood development and colony conditions were assessed after a modified OECD method (No. 75). For adult survival, we weighed and labeled freshly emerged workers from control and exposed colonies and introduced them into non-contaminated mini-hives to monitor their life span for 25 consecutive days. The results from these experiments showed a trivial effect of GBH on colony conditions and the survival of individual workers, even though the hatching weight was reduced in T2. The brood termination rate (BTR) in the T2 treatment, however, was more than doubled (49.84%) when compared to the control (22.11%) or T1 (20.69%). This was surprising as T2 colonies gained similar weight and similar numbers of bees per colony compared to the control, indicating an equal performance. Obviously, the brood development in T2 was not “terminated” as expected by the OECD method terminology, but rather “slowed down” for an unknown period of time. In light of these findings, we suggest that chronic high GBH exposure is capable of significantly delaying worker brood development, while no further detrimental effects seem to appear at the colony level. Against this background, we discuss additional results and possible consequences of GBH for honey bee health. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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20 pages, 1673 KiB  
Review
Resin Use by Stingless Bees: A Review
by Maggie Shanahan and Marla Spivak
Insects 2021, 12(8), 719; https://doi.org/10.3390/insects12080719 - 11 Aug 2021
Cited by 42 | Viewed by 8946
Abstract
Stingless bees (Meliponini) are highly social bees that are native to tropical and sub-tropical ecosystems. Resin use is vital to many aspects of stingless bee colony function. Stingless bees use resin to build essential nest structures, repel predators, and kill would-be invaders. Furthermore, [...] Read more.
Stingless bees (Meliponini) are highly social bees that are native to tropical and sub-tropical ecosystems. Resin use is vital to many aspects of stingless bee colony function. Stingless bees use resin to build essential nest structures, repel predators, and kill would-be invaders. Furthermore, resin-derived compounds have been found to enrich the cuticular chemical profiles of many stingless bee species, and resin may play an important role in shaping the microbial communities associated with stingless bees and their nests. Despite its importance for colony function, previous reviews of resin use by stingless bees are lacking. This topic grows increasingly urgent as changes in beekeeping and land use practices occur, potentially diminishing stingless bees’ ability to incorporate resin into the nest environment. In this article, we review existing literature on resin use by stingless bees and discuss potential areas of future research. Full article
(This article belongs to the Special Issue Honeybees and Wild Bees Health)
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