DOI: 10.5061/dryad.4qrfj6qpt
title: When does temperature limit bee flight? Identifying the missing pieces of the puzzle

description: Bees are the most important insect pollinators, and nearly all
 bee-mediated pollination depends on flight. In this review, we identify
 five key gaps that limit our ability to predict how abiotic factors shape
 bee flight performance and ecology. First, while clade strongly influences
 endothermy and flight temperature limits, we still know little about how
 phylogeny, body size, and ecological traits shape thermal biology across
 the full diversity of bee species - most data come from temperate,
 northern hemisphere  Apinae. Second, because the mechanisms of
 thermal balance during flight have only been studied in a handful of
 species, and these vary, we clearly lack a predictive understanding of
 when bees will be physiologically stressed by temperature during flight.
 Third, although some studies suggest desiccation may limit flight more
 than overheating, the links between thermal balance and water regulation
 remain poorly understood. Fourth, we know very little about bees’ capacity
 to respond to thermal variation through acclimation, developmental
 plasticity, or evolutionary adaptation. Finally, we need advances in
 biophysical modeling to better simulate heat and water exchange in bees,
 including the role of cuticular structures and internal heat transfer
 among body regions. Filling these gaps is essential for building
 predictive, mechanistic models of how climate change will affect bee
 physiology and the pollination services bees provide.
description: The table-1 presents clade-level variation in the thermal biology
 of bees, which was created by searching scholar.google.com and Web of
 Science using relevant keywords such as: bees, temperature, thermal,
 flight, activity, foraging,
 <em>CT</em><sub>max</sub>, and thermal limit. Many
 of the references were not found through web searches, but rather by
 investigating the bibliographies of in-hand papers. We are sure that
 additional relevant papers exist, but feel that it is very likely that the
 papers found and used will provide representative numbers for each
 parameter. Clades were based on Henriquez-Piskulich et al. 2024. To
 indicate the approximate number of species per clade, we relied on
 Danforth et al. 2019. To indicate the number of species in the clade whose
 flight thermal biology has been studied, we summed the number of species
 whose data contributed to Table 1. The endothermic index (thorax
 temperature – operative temperature) was taken from papers that directly
 measured minimal air and thorax temperatures for flight or from the
 largest thorax and air temperature differential for lab studies. We did
 not include field data for the thorax and air differential, as bees in
 cool conditions routinely raise their body temperatures by solar basking,
 so such data do not provide a good index of endothermy (Herrera et al.
 2023). Thermal stability was calculated as (1 minus the slope of thorax
 temperature on air temperature), including for bees measured in either the
 field or laboratory, as surprisingly, thermal stability appeared similar
 for bees measured in both conditions, and there were some clades for which
 we lacked field data (Supplementary Table 1). Many studies reported these
 values directly. Herrera et al. 2023 and Herrera 2024 did not usually
 report clade-level slopes of thorax on air temperature, so we calculated
 these using linear regressions in Excel and the provided online data for
 these studies. The lowest and highest air temperatures and thorax
 temperatures at which bees could fly were calculated by pooling studies,
 which explicitly attempted to measure these in lab conditions and field
 studies that reported that they attempted to assess the full breadth of
 temperatures at which their target bees. If the study did not report these
 values explicitly, they were estimated from the presented figures. There
 were many more studies assessing minimal air temperatures for flight than
 maximal. For Herrera et al. 2023 and Herrera 2024, which provided raw data
 online, we assessed minimal and maximal air and thorax temperatures for
 each clade studied. <em>CT</em><sub>max</sub> data
 were mostly taken from Johnson et al. 2023, who recently compiled such
 data for pollinators, with the inclusion of a few new relevant studies.
 For each parameter and clade, we reported the median and range in Table
 1. We used the data in Table 1 to test for correlations
 across bee clades between degree of endothermy and thermal stability
 during flight, the lowest air and thorax temperature for flight, the
 highest air and thorax temperature for flight, and
 <em>CT</em><sub>max</sub>. We used Prism 10.5 for
 macOS for statistical analyses. All variables passed the
 Kolmogorov-Smirnov normality test, so we used Pearson's r to test for
 significant correlations.
description: # When does temperature limit bee flight? Identifying the missing pieces
 of the puzzle Dataset DOI:
 [10.5061/dryad.4qrfj6qpt](10.5061/dryad.4qrfj6qpt) ## Description of the
 data and file structure This review is organized around specific ‘missing
 pieces’ of information needed to build predictive models of how
 environmental temperature affects bee flight. Ecological and morphological
 differences affect flight energetics and thermoregulation. Therefore, the
 following data consist of physiological (e.g., CO~2~ production and O~2~
 consumption rates, *CT*~max~, and other metrics of thermoregulation and
 performance), morphological (e.g., pubescence, reflectance, emissivity,
 body size, and body mass), and behavioral measurements (e.g., activity
 time, thermal thresholds for flight, etc.). These data are either original
 to this study or are from the primary literature. Here, we consider
 phylogenetic contexts and ecological niches when interpreting patterns of
 thermal performance across clades of bees. Wherever the values are not
 known, the cells were left empty. ### Files and variables #### File:
 PGLS_fmr_wbf_mass_k.R **Description:** Code used to analyze
 the phylogenetic relationships between physiology (e.g., flight metabolic
 rate), morphology (e.g., body mass, thermal conductivity), and behavior
 (e.g., flight kinematics) across clades of bees. #### File:
 Andrena_Bombus_FTS.R **Description:** Code for calculating, analyzing, and
 visualizing the field thermal stability of *Andrena* versus *Bombus* bees.
 #### File: PGLS_CWC_mass.R **Description:** Code used to analyze
 the phylogenetic relationships between physiology (e.g., critical water
 content) and morphology (e.g., body mass) across clades of bees. ####
 File: bee_tree.nwk **Description:** Super-matrix phylogeny of the
 world's bees (generated from the Bee Tree of Life;
 beetreeoflife.org). #### File: lit_review_mass.WBF.FMR.csv
 **Description:** Data extracted from the primary literature used for
 phylogenetically corrected analyses. ##### Variables * Genus: Name of
 genus. * Species: The genus and species name. * Body mass (g): Body mass
 in g. * FMR (mL h-1): Flight metabolic rate in mL of gas per hour (either
 from *V*CO~2~ or *V*O~2~ values, standardized assuming carbohydrate
 catabolism and an oxyjoule equivalent of 21.164 J per mL of O~2~). * spFMR
 (mL CO2 h-1 g-1): Mass-specific flight metabolic rate in mL of gas per
 hour per gram of bee. * WBF (Hz): Wingbeat frequency in cycles per second
 (Hz). * Study: The study that which the data were extracted from. ####
 File: Thermal_stability_meta_reduced.csv **Description:** Primary
 literature data used to calculate the field thermal stability of *Andrena*
 versus *Bombus* bees. ##### Variables * study: The study from which the
 data were extracted from.Genus: The genus the bees belong tos.Speciess:
 The genus and species name of the bee.Castee: Defined by the role they
 play. Females, which reproduce, provision their brood, and do not have a
 worker caste to help. Queens are from social colonies and are primarily
 involved with reproduction, while workers provide and care fothe r closely
 related brood.  * Tair: Shaded air temperature in degrees Celsius. * Tth:
 Thoracic temperature in degrees Celsius. #### File: raw.K.data.csv
 **Description:** Mean warming constants (*k*) and mass (g) values for 30
 genera of bees taken from Herrera, C. M. (2024). Thermal biology diversity
 of bee pollinators: Taxonomic, phylogenetic, and plant community‐level
 correlates. *Ecological Monographs*, *94*(4), e1625. ##### Variables *
 species: Species name of bees measured.Genus: The genus to which the bee
 belongs.Family: The family to which the bee belongs. * Number: The
 bee-specific identifier.Mass (g): Body mass in g. * mass (mg): Body mass
 in mg.Datee: The date on which the data were collected. * Location: The
 location where the bee was collected. * Newton_K: The warming constant
 (*k*) per second. * K_se: Standard error of the reported warming constant
 (*k*). #### File: bee_tree_cwc.csv **Description:** Primary literature
 data used to compare the critical water content (CWC) of different bee
 clades. ##### Variables * genus: The genus to which the bee
 belongs.Family: The family to which the bee belongs. * cwc: The critical
 water content, which is the lowest amount of body water a bee can have
 before physiological functions are impaired, expressed as mass of water
 divided by hydrated animal wet mass.Mass.mg: Body mass in mg.Mass.g: Body
 mass in g.Reference: The study from which the data were extracted from.
 #### File: Reflectance_C.caesalpinae_Fig.5B.csv **Description:** These are
 original, unpublished data. Reflectance as a function of wavelength for an
 unshaved abdomen and thorax of the same bee (*n* = 1). ##### Variables *
 wavelength_nm: The wavelength at which measurements were taken. *
 bee1unshavedabdomen: The reflectance (%) of the bee's unshaved
 abdomen. * bee1unshavedthorax: The reflectance (%) of the bee's
 unshaved thorax. #### File: Reflectance_C.caesalpinae_Fig.5A.csv
 Description: These are original, unpublished data. The thoraxes of ten,
 freshly culled male *Centris* digger bees (*C. caesalpiniae*) were scanned
 in a Perkin-Lambda NIR-UC-VIS spectrophotometer. The thoraxes were
 carefully shaved with a surgical scalpel and re-scanned. Scans occurred
 from 250 to 2500 nm at 2 nm intervals. We calculated mean reflectance in
 near-infrared, visible, and ultraviolet bands. ##### Variables * bee_id:
 Identifier. Status: Either shaved or unshaved, meaning the setae were
 shaved off or left intact.Spectrum: The range of light at which the bees
 were measured. For this study, measurements were made within the following
 ranges: nir = near-infrared (700 - 2,500 nm), vis = visible (450 - 700
 nm), and UVv = ultraviolet (250 - 450 nm). Reflectance: The reflectance
 (%) of the bee's shaved or unshaved thorax. #### File:
 Table1CorrelationData.csv **Description:** Correlation data for different
 metrics of thermal performance and response. ##### Variables * endothermic
 index: The maximum thoracic temperature (*T*~th~) minus operative
 temperature (*T*~op~) of flying bees.Thermal stability: One minus the
 slope of thoracic temperature (*T*~th~) vs shaded air temperature
 (*T*~air~) of flying bees.Minimum air temperature for flight: The lowest
 air temperature at which a bee has been observed flying.Minimum thorax
 temperature for flight: The lowest thoracic temperature at which a bee has
 been observed able to fly.Maximall air temperature for flight: The highest
 air temperature at which a bee has been observed flying.Maximally thorax
 temperature for flight: The highest thoracic temperature at which a bee
 has been observed able to fly. * *CT*~max~: The highest body temperature
 the bee can tolerate before losing normal function, such as coordination
 or the ability to escape. #### File:
 Supplementary_table_to_support_Table_1.csv **Description:** Data extracted
 from the primary literature, used to calculate thermal metrics. #####
 Variables * Family: subfamily: tribe: The family, subfamily, and tribe to
 which the bee belongs.Total species in the clade: The total number of
 species in the clade. * \# species studied: The number of species that
 have been studied to date. Speciess if one: The name of the genus and
 species if only one species has been studied thus far.Labb endothermic
 index (max Tth - Top, oC): The calculated endothermic index [i.e., the
 maximum thoracic temperature (*T*~th~) minus operative temperature
 (*T*~op~)] of bees flying in laboratory settings.Field endothermic
 index: The calculated endothermic index [i.e., the maximum thoracic
 temperature (*T*~th~) minus operative temperature (*T*~op~)] of bees
 flying in the field.Field thermal stability: One minus the slope of
 thoracic temperature (*T*~th~) vs shaded air temperature (*T*~air~) of
 flying bees measured in the field.Lab thermal stability: One minus the
 slope of thoracic temperature (*T*~th~) vs shaded air temperature
 (*T*~air~) of flying bees measured in the laboratory.Field's lowest
 flight air temp, oC: The lowest air temperature at which a bee has been
 observed flying in the field.Labb lowest flight air temp, oC: The lowest
 air temperature at which a bee has been observed flying in laboratory
 settings.Field's lowest flight Tth, oC: The lowest thoracic
 temperature at which a bee has been observed being able to fly within the
 field.Labb lowest flight Tth, oC: The lowest thoracic temperature at which
 a bee has been observed being able to fly within laboratory settings. *
 Field highest flight air temp, oC: The highest air temperature at which a
 bee has been observed flying in the field.Labb's highest flight air
 temp, oC: The highest air temperature at which a bee has been observed
 flying in laboratory settings.Field's highest flight Tth, oC: The
 highest thoracic temperature at which a bee has been observed being able
 to fly within the field.Labb highest flight Tth, oC: The highest thoracic
 temperature at which a bee has been observed being able to fly within
 laboratory settings. * Ctmax mean: The average reported *CT*~max~ value in
 degrees Celsius. * Ctmax range: The range of reported *CT*~max~ values in
 degrees Celsius. * Notes: Specific notes regarding the study or studies. *
 Reference number: Arbitrarily assigned number to each reference. *
 Reference: The reference the data were extracted from. ## Code/software
 Scripts are described above. Most of our data were analyzed and visualized
 using R (v. 4.5.0), with two being analyzed and visualized using GraphPad
 Prism (v. 10.4.1). R-packages are listed in the supplemental references
 (supplementary materials of the original published article). ## Access
 information Other publicly accessible locations of the data: * The primary
 literature data can be found in its original publications. * New data
 presented here cannot be found anywhere else. Data was derived from the
 following sources: * See the supplementary materials for the references
 where the data were sourced.