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We are thankful to the Sao Paulo Research Foundation for the financial support and Ph.D.scholarship of the first author (Grants:2022/07920-7 and 2019/27863-5).

Analysis of institutional authors

Azpiazu, CelesteAuthor

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April 12, 2025
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Co-exposure to a honeybee pathogen and an insecticide: synergistic effects in a new solitary bee host but not in Apis mellifera

Publicated to:Proceedings Of The Royal Society B-Biological Sciences. 292 (2042): 20242809- - 2025-03-05 292(2042), DOI: 10.1098/rspb.2024.2809

Authors: Tadei, Rafaela; Cilia, Giovanni; da Silva, Elaine Cristina Mathias; Blanco, Gonzalo Sancho; Albacete, Sergio; Azpiazu, Celeste; Granato, Anna; Bortolin, Francesca; Martini, Antonio; Bosch, Jordi; Malaspina, Osmar; Sgolastra, Fabio

Affiliations

Alma Mater Studiorum Univ Bologna, Dept Agr & Food Sci, I-40127 Bologna, Italy - Author
CREA Res Ctr Agr & Environm, I-40128 Bologna, Italy - Author
Ist Zooprofilatt Sperimentale Venezie, Natl Reference Lab Honey bee Hlth, I-35020 Padua, Italy - Author
Sao Paulo State Univ, Dept Biol, BR-13506900 Rio Claro, SP, Brazil - Author
Univ Autonoma Barcelona, Barcelona 08193, Spain - Author
Univ Autonoma Barcelona, CREAF, Bellaterra 08193, Spain - Author
Univ Fed Sao Carlos, Dept Biol, BR-18052780 Sorocaba, SP, Brazil - Author
Univ Padua, Dept Biol, I-35131 Padua, Italy - Author
Univ Politecn Madrid, Madrid 28040, Spain - Author
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Abstract

Pesticides and pathogens are major drivers of bee declines. However, their potential interactions are poorly understood, especially for non-Apis bees. This study assessed the combined effects of infestation by the honeybee pathogen Vairimorpha ceranae and chronic exposure to the insecticide flupyradifurone on Osmia bicornis and Apis mellifera. We investigated whether V. ceranae could reproduce in a new solitary bee host (O. bicornis) and assessed sublethal and lethal effects of the pathogen and the pesticide, alone and in combination. We also analysed the interactive effects of the combined exposure on V. ceranae proliferation and bee survival in the two bee species. Newly emerged bees were orally infected with 100 000 spores of V. ceranae and then exposed ad libitum to flupyradifurone at field-realistic concentrations. We showed, for the first time to our knowledge, that V. ceranae can replicate in the midgut of O. bicornis, causing histological damage, impaired phototactic response, reduced food consumption and decreased longevity. The pathogen-pesticide combination caused a synergistic effect in O. bicornis, leading to an abrupt survival decline. In A. mellifera, V. ceranae and flupyradifurone showed antagonistic survival effects, but the pesticide promoted pathogen proliferation. Our results warn against the potential effects of pathogen spillover and multiple stressor exposure on non-Apis bees.

Keywords

4-butyrolactone<italic>osmia</italic><italic>vairimorpha </italic>(<italic>nosema</italic>)<italic> ceranae</italic>AnimalsBeesFlupyradifuroneInsecticidesMidgutMultiple stressorMultiple stressorsNosemaNosema-ceranaeOsmiaParasitePesticidesPhototaxisPyridinesStressTolerancVairimorpha (nosema) ceranae

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Proceedings Of The Royal Society B-Biological Sciences due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2025, it was in position 14/53, thus managing to position itself as a Q1 (Primer Cuartil), in the category Ecology.

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-26:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 12.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 9 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 1.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Brazil; Italy.