Do diesel exhaust particles in pollen affect colony founding in the bumblebee B. terrestris?

doi:10.21203/rs.3.rs-3764354/v1

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Do diesel exhaust particles in pollen affect colony founding in the bumblebee B. terrestris?

https://doi.org/10.21203/rs.3.rs-3764354/v1

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The global insect decline threatens ecosystem functioning because insects provide many essential services, such as pollination or nutrient cycling. Pollution is one of the main drivers of insect decline besides land-use change, global warming, and invasive species. Airborne particulate matter, such as diesel exhaust particles (DEPs), is ubiquitous in the environment. Their effects on insects are still largely unknown. We provided queens and workers of the bumblebee Bombus terrestris with DEP-spiked pollen at the early colony founding stage and compared the colony development to control colonies. After ten weeks, we investigated individual and colony-level life history traits. We did not see any effects of DEP-spiked pollen on worker count, brood count, worker size and relative fat body weight. These results indicate no harmful effects of DEP on colony founding in B. terrestris in our single-stressor setup. Our novel approach adds to the understanding of the role that airborne particulate matter plays in the global insect decline and we are looking forward to seeing similar studies with other species and additional stressors, such as heat stress or food shortages.

air pollution

particulate matter

insect decline

pollinator

The rapid decline in insects is a major threat to many ecosystems around the globe as insects provide many vital ecosystem functions such as pollination, nutrient cycling, and linking of trophic levels (Cardoso et al. 2020, Noriega et al. 2018). Pollution is one of the main drivers of insect decline besides changes in land use, invasive species, and global warming (Miličić et al. 2021, Müller et al. 2023, Sanchez-Bayo & Wyckhuys 2019, Wagner 2020). Pesticides, specifically designed to harm certain groups of organisms, negatively affect important pollinators such as honeybees or bumblebees on different levels ranging from behavioral changes over impaired development to increased mortality (Desneux et al. 2007, Gill & Raine 2014, Ndakidemi et al. 2016, Sanchez-Bayo 2021, Schuhmann et al. 2022). Effects of other anthropogenic pollutants, such as airborne pollutants, on insects are less well-studied. Airborne particulate matter (APM) is defined by size rather than chemical composition and comprises all airborne particles with diameters typically between 100 nm and 10 µm. As these particles originate from various sources such as dust and soil, wood and coal smoke, sea salt, and road traffic exhaust among others, they are highly variable in terms of chemical composition, concentration, and spatial distribution (Harrison 2020). A thorough documentation of the adverse effects of APM on human health exists (Kim et al. 2015, Valavanidis et al. 2008), but studies on their impacts on other organisms are scarce. Due to the small particle size, APM, such as diesel exhaust particles (DEPs), may enter insects’ bodies via tracheae or by consuming contaminated food, such as pollen, which contains APM at least in industrial areas (Feldhaar & Otti 2020, Papa et al. 2021). Chemically, DEPs are composed of a carbon core with different organic and inorganic substances adsorbed to its surface, including polycyclic aromatic hydrocarbons (PAHs) (Hüftlein et al. 2023, Wichmann 2007), which are known to be harmful to various life forms (Patel et al. 2020, Sun et al. 2021).

One group of insects in decline and exposed to anthropogenic pollution are wild bees, especially social bees. On the one hand, social bees often have large foraging areas where they can encounter an array of pollutants, and transfer them to their nests, which could result in early exposure of their offspring (Morales et al. 2020). On the other hand, the large colony sizes may also buffer the negative effect of pollutants and contaminated patches can be avoided by having large foraging areas (Crall et al. 2019, Feldhaar & Otti 2020, Straub et al. 2015). The most vulnerable stage in eusocial insects is the colony founding stage because the colony's future depends solely on the survival of one or very few individuals (Helanterä 2006). As the colony grows, the risk of colony failure due to the death of single individuals decreases, and harmful effects are buffered better (Crall et al. 2019). In bumblebees, only the queens hibernate. In early spring, queens emerge from their hibernacula, start to forage for pollen and search for a suitable nesting place. Once the queen finds a good spot, she lays the first batch of eggs to start the new colony. This first generation of bumblebee workers the queen raises on her own (Alford 1975). During the colony founding phase, pollution might directly affect the queen or the larvae she feeds with potentially polluted pollen. In both cases, potential negative effects at such an early stage may lead to a significant reduction of the long-term colony fitness, such as a lower number of brood and workers, and a higher risk of colony failure (Baron et al. 2017). Chronic exposure to high doses of DEPs in sugar water, as a surrogate for plant nectar, increases the mortality of workers of the bumblebee Bombus terrestris, and sublethal doses cause changes in their transcriptome and gut microbiome (Hüftlein et al. 2023, Seidenath et al. 2023). However, the impact such effects have on the colony level, including the brood, is still unknown. Moreover, the effects could differ when bumblebees are exposed to DEPs via pollen rather than sugar water.

In this study, we provided bumblebees with pollen spiked with DEP particles at the early colony founding stage and then observed colony development compared to controls fed with uncontaminated pollen. Due to its chemical composition and observed negative effects on workers during chronic exposure, we expect negative effects of DEPs on larval development, resulting in impaired colony development. We expect fewer workers and smaller broods in the colonies treated with DEPs. Moreover, we expect the condition of workers, measured by relative fat body content as a proxy, to be worse in the DEP treatment than in the control.

Experimental procedure

Twenty queenright colonies were ordered from Biobest (Westerlo, Belgium) in January 2022. Colonies were kept in a climate chamber at 26° C and 70% humidity under a constant, inverted 12:12 h light:dark cycle. At the start of the experiment, we removed the queen and ten randomly selected workers from each colony. To observe colony initiation, we placed them in fresh boxes (21 x 13 x 27 cm) provided with sugar water (50% Apiinvert, Südzucker AG, Mannheim, Germany) ad libitum. Half of the queen-worker groups were randomly assigned to the control group receiving pollen cakes made from ground pollen (Imkerpur, Osnabrück, Germany) and Apiinvert (ratio 5:1 (g:ml)) (Figure A1A). The other half we assigned to the DEP treatment receiving pollen cakes made from ground pollen spiked with 0.2% DEPs (w/w) and Apiinvert (ratio 5:1 (g:ml) (Figure A1B). At the beginning of the experiment each colony received 4 pellets (ca. 1.5 g each) of pollen cake. Afterwards, we added two pollen pellets to the colonies twice per week. We replaced the sugar water once per week to prevent molding. Once per week, we removed dead workers. On day 35, 43 and 63 we randomly removed 20% of the workers from each colony to simulate a natural mortality rate and prevent overcrowding (Otti and Schmid-Hempel 2007). After 66 days all colonies were frozen at -20° C.

After defrosting, we counted the number of workers, larvae, and pupae. For each colony, we pooled all larvae and pupae in 10 ml glass vials, respectively, and placed them at 70° C for 96 hours in a drying oven (UFE 600, Memmert GmbH + Co. KG, Schwabach, Germany) to measure larvae and pupae dry weight using a fine scale to the nearest 0.01 mg (SM1265Di, VWR, Darmstadt, Germany). We calculated brood number and dry weight by adding numbers and dry weights of larvae and pupae, respectively.

Fat body assay

We randomly selected ten workers per colony and measured the radial cell length of the right forewing under a light microscope (Leica DFC290, Leica M165, Leica, Wetzlar, Germany) to determine worker size (Medler 1962). Additionally, we measured the fat body content of the selected workers according to Hüftlein et al. (2023). For that purpose, we separated the abdomen from head and thorax and slightly opened the sternites with tiny scissors. Then we placed each abdomen in a 5 ml glass vial and dried it in a drying oven (UFE 600, Memmert GmbH + Co. KG, Schwabach, Germany) at 70° C for 72 hours. Then, the dry weight including the fat body of each abdomen was weighed on a fine scale to the nearest 0.01 mg (PLE 420-3N, Kern & Sohn GmbH, Balingen-Frommern, Germany). Then we removed the fat content added 2 ml chloroform to each vial. Every 24 hours we replaced the chloroform with 2ml fresh one. After 72 hours we removed the chloroform and placed the vials in the drying oven again at 70° C for 72 hours. Then we weighed the abdomens again without the fat body. We calculated the fat body content by subtracting the dry weight after fat body removal from the initial dry weight of the abdomen. To correct for body size, we calculated relative fat body weight by dividing the fat body content by the radical cell length.

Generation of diesel exhaust particles (DEPs)

We produced DEP-samples on a test bench with a four-cylinder diesel engine (OM 651, Daimler AG, Stuttgart, Germany) as described in Zöllner (2019). When analyzed with a fast response differential mobility particulate spectrometer DMS500 (Combustion, Cambridge, England), raw exhaust samples showed a median diameter between 52.1 nm and 101.9 nm within an inner-city driving cycle. Elemental carbon accounted for 72.2 ± 1.1% of the DEP mass, organic matter for 23.2 ± 0.9% w/w, and inorganic matter for 4.6 ± 0.7% w/w, according to thermogravimetric analysis (TGA, STA 449 F5 Jupiter, Netzsch-Gerätebau GmbH, Selb, Germany). We analyzed the DEP-samples for polycyclic aromatic hydrocarbons (PAH) and detected a concentration of 444 ppm for pyrene, 220 ppm for phenanthrene, and 107 ppm for fluoranthene. The elemental composition showed fractions of calcium (1.63% w/w), copper (1.03% w/w), zinc (0.53% w/w), phosphorus (0.50% w/w), sulphur (0.17% w/w), boron (0.13% w/w) and magnesium (0.10% w/w). More details on the characterization and sampling methods of DEP-samples can be found in Hüftlein et al. (2023) and Seidenath et al. (2023).

Statistical analysis

All statistical analyses were performed using R 4.2.1 (R Core Team 2022). Worker number, larvae number, pupae number, brood number (sum of larvae and pupae), larvae dry weight, pupae dry weight and brood dry weight (total weight larvae and pupae) were analyzed fitting generalized linear models (GLMs) with treatment as a predictor. Relative fat body weight and worker size were analyzed fitting generalized linear mixed models (GLMMS) with treatment as a predictor and colony as a random factor using the package glmmTMB (Brooks et al. 2017). We checked model assumptions using model diagnostic test plots, i.e., qqplot and residual vs. predicted plot from the package DHARMa (Hartig 2022). For the GLMs we then produced F-statistics with the function Anova() from the package car (Fox & Weisberg 2019) to calculate p-values for differences between the two groups. For the GLMMs we performed chi-squared tests with the function Anova() from the package car (Fox & Weisberg 2019) to calculate p-values for differences between the two groups.

Overall, we did not find any differences between the two groups. All colonies survived until the end of the experiment after 66 days. The number of workers did not differ between groups (GLM with gaussian distribution: F_1,18 = 0.308, P = 0.586). Likewise, neither the number of larvae differed between groups (GLM with gaussian distribution: F_1,18 = 0.001, P = 0.975) nor the number of pupae (GLM with gaussian distribution: F_1,18 = 0.209, P = 0.653) or the brood number (GLM with gaussian distribution: F_1,18 = 0.023, P = 0.882). We also did not find differences in dry weight for comparisons between the groups of larvae (GLM with gaussian distribution: F_1,18 = 0.051, P = 0.823), pupae (GLM with gaussian distribution: F_1,18 = 0.229, P = 0.638), or brood (GLM with gaussian distribution: F_1,18 < 0.001, P = 0.982). The relative fat body weight did not differ between groups (GLMM with gamma distribution: X² = 0.396, df = 1, P = 0.529). The worker size did not differ between groups (GLMM with gamma distribution: X² = 0.848, df = 1, P = 0.357) (Fig. 1).

Our study is the first to evaluate the effects of DEPs on whole bumblebee colonies in a laboratory setup. We did not detect any effect of DEP-contaminated pollen on the colony founding of B. terrestris. All the colony life history traits we measured, i.e. the number of workers and brood, as well as individual life history traits, i.e. worker size and relative fat body content, were similar between the treatments.

These results indicate that DEP exposure via pollen alone does not impair colony and worker development at an early colony founding stage. Hence, we have no reason to expect effects at later colony stages. However, as we have not measured the production and development of sexual offspring for the next generation, we should be careful with further speculations. Still hidden effects that were not investigated in this study might come to light once a complete colony cycle is investigated. Also, when fed with DEP-spiked sugar water, bumblebee workers had a significant shift in gut microbiome composition compared to controls (Seidenath et al. 2023). It remains speculative how such shifts affect the performance of whole colonies. As the microbiome plays an important role in detoxification and in the protection against parasites (Koch & Schmid-Hempel 2011, Rothman et al. 2019), the colony-level effects might only show when additional stressors are present. In nature, insects face a multi-stressor environment, including parasites, food limitations, heat stress and more (Holmstrup et al. 2010, Padda & Stahlschmidt 2022). Adding sublethal effects due to pollution could then be the cause of a colony failure. In contrast, ad libitum food provision in a controlled environment, as in this study, may enable the insects to compensate for the effects of DEP exposure.

Because identifying and quantifying airborne particulate matter, such as DEP, in terrestrial environments is very difficult, we lack reliable data on the level of exposure for insects. Isotopic analyses revealed that certain Arizona soils contain up to 0.54% (w/w) of soot black carbon, presumably produced by burning fossil fuels (Hamilton & Hartnet 2013). While reports exist of contaminated bees in the wild (Negri et al. 2015, Thimmegowda et al. 2020), we still lack realistic modelling on the uptake of these particles. Other experiments on effects of DEP on individual workers showed increased mortality in B. terrestris workers after oral DEP exposure via sugar water with concentrations of 1 g/l and more (Hüftlein et al. 2023). In contrast, we did not see any difference in mortality or other life-history parameters. This may be due to the different exposure route via pollen or the colony setup, which might enable the bumblebees to buffer individual negative effects (Crall et al. 2019).

B. terrestris is one of the most abundant European wild bees, especially in urban areas (Herbertsson et al. 2021, Whitehorn et al. 2022). Thus, B. terrestris is possibly more tolerant towards anthropogenic pollution, such as DEP, or has already adapted to higher levels of air pollution than other species. That a species is common might mean that it is more tolerant towards stressors than a rarer, often more specialized species (Vincent et al. 2020), and e.g., B. terrestris has been shown to be less affected by pesticides in comparison to other wild bee species (Schmolke et al. 2021). We thus need to be careful when trying to extrapolate the results of our study to other rarer species with more specific dietary needs or narrower niches. Physiological differences between insect populations and species, translate into variation of the susceptibility to different stressors (Chown 2001, Spurgeon et al. 2020). Therefore, in the future we should also incorporate rarer species to evaluate the impact of potentially harmful substances in a comparative approach.

In our study, we successfully exposed whole bumblebee colonies to DEPs in the laboratory. We found no measurable effects of exposure to DEP-contaminated pollen on the colony founding of B. terrestris. Our novel approach adds to the understanding of the role that airborne particulate matter plays in the global insect decline and we are looking forward to seeing the results of future studies adding additional stressors to the setup, such as heat stress or food shortages.

Data availability statement

The data that support the findings of this study are available upon request.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Author contributions

DS, OO, and HF conceived the idea, designed the experiment, and wrote the manuscript. AM, TH, and DB produced and analyzed the particulate matter. DS carried out the experiment. DS performed the data analysis. DS, OO, and HF interpreted the results. All authors read and approved of the final manuscript.

Funding

This project was funded by the Bavarian State Ministry of the Environment and Consumer Protection as part of the project network BayOekotox.

Acknowledgements

We thank Franziska Jung and Jonas Heinz for helping with the lab work.

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Appendix.jpg
Figure A1: Control pollen cake (A) and DEP-spiked pollen cake (B).

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Do diesel exhaust particles in pollen affect colony founding in the bumblebee B. terrestris?

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