ApidologiePub Date : 2025-01-07DOI: 10.1007/s13592-024-01127-y
Carolina Fernández, María Amparo Blanco Mendez, María Federica Faure, Ana Paula Murray, Silvana Rodríguez, Ailen Melisa Poza, Fernando Gaspar Dellatorre, Leticia Andrea Fernández
{"title":"Macroalgal extracts as an alternative for the control of Paenibacillus larvae","authors":"Carolina Fernández, María Amparo Blanco Mendez, María Federica Faure, Ana Paula Murray, Silvana Rodríguez, Ailen Melisa Poza, Fernando Gaspar Dellatorre, Leticia Andrea Fernández","doi":"10.1007/s13592-024-01127-y","DOIUrl":"10.1007/s13592-024-01127-y","url":null,"abstract":"<div><p>The present study evaluated the potential use of methanolic extracts from two seaweeds from the Argentine Patagonian coasts, <i>Macrocystis pyrifera</i> and <i>Undaria pinnatifida</i>, as natural alternatives against <i>Paenibacillus larvae</i>. We carried out a detailed characterization of both seaweeds, comparing vegetative and reproductive thallus portions. We also assessed their phenolic content and antioxidant activity and evaluated the <i>in vitro</i> antibacterial action. Based on the minimal inhibitory concentration results, extracts from sporophyll of <i>Undaria</i> (US) and basal thallus portion of <i>Macrocystis</i> (MB) are strong inhibitors. US showed the best activity against <i>P. larvae</i> strain CMM(B)35 (12.2 μg/mL), and MB showed the same activity for strains CMM(B)35 and MAR1 (18.6 μg/mL). Antioxidant activity was higher in US, followed by MB, and a positive correlation was found with phenolic content. Taken together, our results indicate the role of specific chemical compounds present in algal extracts on antioxidant properties and antibacterial activity against <i>P. larvae</i>. We conclude that these seaweeds are promising alternatives against <i>P. larvae</i>.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939015","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2025-01-02DOI: 10.1007/s13592-024-01139-8
Berkant İsmail Yıldız, Kemal Karabağ, Uğur Bilge, Aziz Gül
{"title":"Explainable artificial intelligence for differentiating honey bee genotypes using morphometrics and SSR markers","authors":"Berkant İsmail Yıldız, Kemal Karabağ, Uğur Bilge, Aziz Gül","doi":"10.1007/s13592-024-01139-8","DOIUrl":"10.1007/s13592-024-01139-8","url":null,"abstract":"<div><p>This study aims to classify honey bee genotypes by integrating explainable artificial intelligence techniques, particularly decision trees, with both morphometric and molecular data. A total of 4949 samples were collected from 500 colonies across five regions in Türkiye, representing diverse subspecies and ecotypes. Morphometric data included 16 key wing characteristics, while molecular data contained 26 highly informative SSR loci. First, we used 16 morphometric wing parameters to classify bees into five regions where they originate. The decision tree algorithm resulted in a tree with wing length and O26 and L13 angles, but the classification accuracy was low (51%). Later, we included 26 molecular variables and obtained a decision tree with four SSR loci—Ap218, Ap274, Ap001, and Ap289—and achieved a high classification accuracy of 96.38%. The findings also revealed the first-ever identification of a SSR locus (Ap218) strongly associated with wing length in honey bees. Finally, we explained wing length with molecular data by modeling a regression decision tree. This tree identified Ap218, Ap223, and Ap001 as the most significant SSR loci for the wing length model. This study provides a powerful approach for differentiating honey bee genotypes while offering valuable insights into the genetic factors influencing wing morphology. The results have significant implications for the conservation and sustainable management of honey bee genetic resources, particularly in regions like Türkiye where genetic diversity is at risk.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142912998","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2025-01-02DOI: 10.1007/s13592-024-01132-1
Rosaline A. Hulse, Annette Van Oystaeyen, Joanne D. Carnell, Danielle Beckett, William G. Grey, Dave Goulson, Felix Wackers, William O. H. Hughes
{"title":"The effects of diet enhancement on the health of commercial bumblebee colonies","authors":"Rosaline A. Hulse, Annette Van Oystaeyen, Joanne D. Carnell, Danielle Beckett, William G. Grey, Dave Goulson, Felix Wackers, William O. H. Hughes","doi":"10.1007/s13592-024-01132-1","DOIUrl":"10.1007/s13592-024-01132-1","url":null,"abstract":"<div><p>Commercially reared bees provide economically important pollination services for a diversity of crops. Improving their health is important both to maximise their pollination services and to avoid possible pathogen spillover or spillback with wild pollinators. Diet quality may directly or indirectly affect diverse aspects of bumblebee health, including colony development, individual size and immune health, but the impact of this remains unclear. Here we investigate experimentally the effect of diet quality during bumblebee colony development using three diets: (1) a standard pollen diet used in commercial rearing of colonies for sale, (2) an enhanced diet comprised of a wildflower pollen mix that was expected to be nutritionally superior (including by having an elevated protein content) and (3) a diet of pollen substitute mixed with the standard diet that was expected to be nutritionally poorer. The effect of diet quality on colony health was quantified using colony-level measures (colony weight, size [number of live workers] and number of dead individuals), and individual-level measures (body size, fat body size [proportion of body weight], total haemocyte count and phenoloxidase immune enzyme activity). Diet quality significantly affected colony growth, with colonies fed the enhanced diet growing larger and producing more reproductives than those fed either a standard or poor diet. The enhanced diet also resulted in bees that were significantly larger and had better immune health. The results show that diet can have important effects on the health of commercially reared bumblebees and suggest that the enhancement of standard-rearing diets may improve colony health.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://link.springer.com/content/pdf/10.1007/s13592-024-01132-1.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142912997","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-22DOI: 10.1007/s13592-024-01134-z
Antoine Gekière, Maxence Gérard, Dimitri Evrard, Luna Breuer, Luca Dorio, Philippe Maesen, Maryse Vanderplanck, Denis Michez
{"title":"Copper-accelerated pupation in larvae of the buff-tailed bumble bee","authors":"Antoine Gekière, Maxence Gérard, Dimitri Evrard, Luna Breuer, Luca Dorio, Philippe Maesen, Maryse Vanderplanck, Denis Michez","doi":"10.1007/s13592-024-01134-z","DOIUrl":"10.1007/s13592-024-01134-z","url":null,"abstract":"<div><p>With the expansion of industrial activities, the escalation of pollution by trace metals poses an increasing threat to bees. While the effects of metals on adult bees have been extensively studied in ecotoxicological research, a critical gap persists concerning their impact on bee larvae. Here, we conducted the first study exposing bumble bee larvae to field-realistic concentrations of copper via an in vitro assay, over a span of 25 days. We monitored the duration of their developmental stages, including moments of defecation, pupation, and emergence, alongside their survival rates. Additionally, we recorded their area growth as well as their adult body mass post-emergence. Despite copper exposure exhibiting no discernible influence on the overall duration of development, survival, growth, or adult mass, a significant positive effect was observed on the pupation rate. This outcome is likely attributable to heightened copper-dependent metabolic activities and disturbances in the redox balance. Furthermore, our investigation underscored the pivotal role of initial body size in developmental success, with larger larvae showing elevated emergence and survival rates. Given the efficacy of this assay, we urge regulatory institutions responsible for approving pesticides and other xenobiotics for market use to embrace this experimental approach in future risk assessments.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142870369","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-19DOI: 10.1007/s13592-024-01126-z
Hongmei Li-Byarlay, Kaila Young, Xaryn Cleare, Deng Cao, Shudong Luo
{"title":"Biting behavior against Varroa mites in honey bees is associated with changes in mandibles, with tracking by a new mobile application for mite damage identification","authors":"Hongmei Li-Byarlay, Kaila Young, Xaryn Cleare, Deng Cao, Shudong Luo","doi":"10.1007/s13592-024-01126-z","DOIUrl":"10.1007/s13592-024-01126-z","url":null,"abstract":"<div><p>Certain populations of feral or wild European Honey Bees (EHB), <i>Apis mellifera</i>, have developed a tolerance of or persistence against the parasitic mite <i>Varroa destructor</i> in the USA. Although the grooming or mite-biting behavior is a trait bees use to defend against parasitic <i>Varroa</i> mites, little information is available concerning the grooming or mite-biting behavior of feral EHBs. Accordingly, we observed damaged mites of feral bees in Ohio (<i>Apis mellifera ligustica</i>) and commercial bees in four field seasons, 2020 to 2023, as well as feral bees in Kentucky (<i>A. mellifera mellifera</i>) in 2023, for a total of 7494 mites. When the mite-biting behavior was compared among these three populations, feral bees of Ohio (<i>A. m. ligustica</i>) and Kentucky (<i>A. m. mellifera</i>) displayed a significantly higher percentage (22% and 27% more) than the commercial bees. To investigate the mechanism of the mite-biting behavior, we examined bee mandibles. Mandibles are the primary mouthparts and tools used to remove or amputate the <i>Varroa</i> mites. Gentle Africanized honey bees (gAHB, <i>A. mellifera scutellata-</i>hybrid) in Puerto Rican exhibit mite resistance through microevolution on the island. Asian honey bees (<i>A. cerana</i>) are the original natural host of <i>V. destructor</i>. However, little has been reported on the morphometric analysis of mandibles between the two species <i>A. cerana</i> and <i>A. mellifera</i> and between the subspecies <i>A. m. scutellata-</i>hybrid and <i>A. m. ligustica</i>. Utilizing X-ray micro-computed tomography (microCT), we then examined the three-dimensional morphology of mandibles in (1) <i>A. cerana</i>, (2) gAHB <i>A. m. scutellata-</i>hybrid, (3) Ohio feral <i>A. m. ligustica</i>, and (4) package or commercial colonies <i>A. m. ligustica</i>. Our findings revealed distinctive three-dimensional shapes of mandibles, indicating substantial variations among these populations. These variations suggest that mandible morphology has an integral role in the bee’s defensive mechanisms against parasitic mites. We also developed the first smartphone application to quantify the mite damage by applying artificial intelligence to image analysis. This research contributes valuable insights into the prospective selection and breeding of honey bees with enhanced mite resistance, thus promoting the sustainability of apiculture.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://link.springer.com/content/pdf/10.1007/s13592-024-01126-z.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142844983","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-19DOI: 10.1007/s13592-024-01133-0
Esmaeil Amiri, Hossam Abou-Shaara, Alison McAfee
{"title":"The effect of major abiotic stressors on honey bee (Apis mellifera L.) queens and potential impact on their progeny","authors":"Esmaeil Amiri, Hossam Abou-Shaara, Alison McAfee","doi":"10.1007/s13592-024-01133-0","DOIUrl":"10.1007/s13592-024-01133-0","url":null,"abstract":"<div><p>Queen health and quality play a significant role in the survival, expansion, and productivity of honey bee colonies. Nevertheless, modern beekeeping practices, intensified agriculture, and climate change can leave queens vulnerable to diverse stressors. These stressors can exert a negative impact on queens, resulting in a range of morphological and physiological abnormalities. The repercussions of queen stress may not only cause direct impacts on her survival and performance, but it may also extend to the offspring of surviving queens through transgenerational mechanisms. Here, we review the current knowledge regarding the effects of major abiotic stressors (namely, nutrition, pesticides, and extreme temperatures) on queen health and their potential impacts on the queen’s progeny. Gaining insight into the effects of these factors across individual and colony levels is vital for prioritizing further research on queen and colony health.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://link.springer.com/content/pdf/10.1007/s13592-024-01133-0.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142845061","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-18DOI: 10.1007/s13592-024-01128-x
Jaya Sravanthi Mokkapati, Johanna Hehl, Lars Straub, Christina M. Grozinger, Natalie Boyle
{"title":"Short-term heat exposure at sublethal temperatures reduces sperm quality in males of a solitary bee species, Osmia cornifrons","authors":"Jaya Sravanthi Mokkapati, Johanna Hehl, Lars Straub, Christina M. Grozinger, Natalie Boyle","doi":"10.1007/s13592-024-01128-x","DOIUrl":"10.1007/s13592-024-01128-x","url":null,"abstract":"<div><p>Increased temperature variability and extreme weather events associated with climate change can be detrimental to bees and lead to their population declines. While there is some research on the effects of heatwaves on insect biology and reproduction, impacts on male insect reproduction are not well described. Solitary bees may be more exposed to temperature variation than social bees, since there is no mitigation by group thermoregulation. Here, we evaluated the effects of sublethal heat exposure (at 30 °C and 38 °C) on reproductive fitness of adult males of a solitary bee species, <i>Osmia cornifrons</i>. After 4 h of heat exposure, bees were maintained at 24 °C for 48 h in laboratory cages to reach sexual maturity and later analyzed for sperm abundance (quantity) and proportion of viable sperm (quality). Bees that were reared and maintained at 24 °C served as controls. Despite rehabilitation after heat exposure, both sperm quantity and quality of male <i>O. cornifrons</i> bees were significantly reduced in heat-treated groups compared to controls. These results demonstrate that the exposure to elevated non-lethal temperatures, even for short periods and allowing time for recovery, may negatively affect the reproductive capacity of male solitary bees. Our findings reveal a possible mechanistic explanation for wild bee population declines. Given the importance of solitary bee species (such as <i>O. cornifrons</i>) in natural and agricultural landscapes, our study provides valuable insights into the potential consequences of climate change on these insect populations and the ecosystems they inhabit.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"56 1","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://link.springer.com/content/pdf/10.1007/s13592-024-01128-x.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142844956","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-06DOI: 10.1007/s13592-024-01123-2
Florencia Palottini, Carolina Fernández, María Sol Balbuena
{"title":"Antennal sensilla pattern distribution and odor detection in Bombus pauloensis foragers (Hymenoptera: Apidae)","authors":"Florencia Palottini, Carolina Fernández, María Sol Balbuena","doi":"10.1007/s13592-024-01123-2","DOIUrl":"10.1007/s13592-024-01123-2","url":null,"abstract":"<div><p>Insects rely on chemical information from the environment to survive. The reception of this information mainly occurs through the antennae, when the stimuli contact the sensory receptors located within specialized structures named sensilla. Some bee species present a different number of olfactory sensilla on both antennae and dissimilar responses, denoting olfactory lateralization evidenced by asymmetrical learning abilities. Here, we studied the antennae sensilla pattern and antennal odor detection in the bumblebee <i>Bombus pauloensis</i>, to evaluate olfactory lateralization. By scanning electron microscopy, we quantified and identified antennae sensilla types, and, by electroantennography, we recorded the responses to odors with different hedonic values. We found nine types of sensilla, being the trichodea the most prevalent type. Neither the number of sensilla nor the olfactory responses were different between the left and right antennae. Our findings suggest the absence of olfactory lateralization in <i>B. pauloensis</i>, providing new insights into the complexity of the bee olfactory system and shedding light on the biology of this commercially important bumblebee species, widely employed for crop pollination services.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"55 6","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142789212","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-12-06DOI: 10.1007/s13592-024-01125-0
Kathleen A. Dogantzis, Andrés Vargas-Fernández, María Angélica Larraín, Cristián Araneda, Amro Zayed
{"title":"Honey bees in Chile: a national survey of ancestry and admixture","authors":"Kathleen A. Dogantzis, Andrés Vargas-Fernández, María Angélica Larraín, Cristián Araneda, Amro Zayed","doi":"10.1007/s13592-024-01125-0","DOIUrl":"10.1007/s13592-024-01125-0","url":null,"abstract":"<div><p>Since the rapid spread and establishment of Africanized honey bee populations in South America, Africanized bees have persisted as the dominant strain. Remarkably, Chile has remained free of Africanized bee populations, making the country a valuable exporter of mated queens. Given Chile’s pivotal role in the apiculture industry, monitoring the genetic makeup of its honey bee colonies is crucial, yet documentation has been limited to a few studies. Here, we evaluate the ancestral composition of honey bees across eleven different regions in Chile. We find that Chilean honey bees have low levels of admixture, which is markedly lower relative to commercial colonies located internationally. The genetic ancestry of Chilean honey bees is primarily of Eastern European origin, with low levels of Western European ancestry. Finally, we detect a significant relationship between geography and genetic ancestry, suggesting regional adaptations that warrant further investigation.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"55 6","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142789213","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ApidologiePub Date : 2024-11-26DOI: 10.1007/s13592-024-01124-1
Maggie M. Mayberry, Jacob S. Francis, Jenny K. Burrow, Faith E. Dall, Michelle Bowe, Anne S. Leonard, Parker M. Campbell, Avery L. Russell
{"title":"One for the road: bumble bees consume pollen at flowers","authors":"Maggie M. Mayberry, Jacob S. Francis, Jenny K. Burrow, Faith E. Dall, Michelle Bowe, Anne S. Leonard, Parker M. Campbell, Avery L. Russell","doi":"10.1007/s13592-024-01124-1","DOIUrl":"10.1007/s13592-024-01124-1","url":null,"abstract":"<div><p>Bees are the primary consumers of pollen in many ecosystems, but pollen consumption by adult bees while foraging is rarely studied, leaving a gap in our understanding of the nutritional ecology of collective foraging and pollination biology more generally. For example, while eusocial bees feed upon pollen from colony stores, whether they also consume pollen directly from flowers to meet their own needs or to assess its quality for the broader collective is unknown. We therefore captured wild bumble bee colonies (<i>Bombus bimaculatus</i> and <i>Bombus griseocollis</i>) and tested whether individual workers consumed pollen directly from flowers in a lab-based foraging assay. After confirming the presence of floral pollen in worker crops (i.e., consumption at flowers), in a field setting, we tested alternative hypotheses for the function of this behavior using information about the composition, abundance, and diversity of pollen found in the crops vs. pollen baskets of three species of pollen- and nectar-foraging bumble bees (<i>Bombus bimaculatus</i>, <i>B. griseocollis</i>, and <i>B. impatiens</i>). Consistent with the hypothesis that consuming pollen at flowers reflects sampling, total pollen quantity in crops was consistently smaller than in pollen baskets, and basket pollen tended to be a subset of that found in crops. Further, pollen foragers consumed more and different kinds of pollen than nectar foragers. Pollen consumption at flowers is thus unlikely to be purely incidental or to substantially benefit workers nutritionally. Instead, consuming pollen directly from flowers likely allows foragers to quickly assess pollen quality before collecting it to feed the colony as a whole.</p></div>","PeriodicalId":8078,"journal":{"name":"Apidologie","volume":"55 6","pages":""},"PeriodicalIF":2.4,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142714194","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}