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Native solitary bee reproductive success depends on early season precipitation and host plant richness

  • Population ecology – original research
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Abstract

Spring-emerging bees depend upon the synchronized bloom times of angiosperms that provide pollen and nectar for offspring. The emergence of such bees and bloom times are linked to weather but can be phenologically mismatched, which could limit bee developmental success. However, it remains unclear how such phenologically asynchrony could affect spring-emerging pollinators, and especially for those that forage over a relatively short time period. We examined the relationship between weather and host plant selection on the native spring-foraging solitary bee, Osmia lignaria, across 3 years at urban and rural sites in and around Seattle, Washington, USA. We used community science weather data to test the effects of precipitation, wind, and temperature on O. lignaria oviposition and developmental success. We also collected pollen data over two distinct foraging periods, early and late spring, and used Next-Generation Sequencing to identify plant genera from pollen. Among the weather variables, precipitation during the early foraging period adversely affected larval developmental success and adult bee emergence success, but not oviposition. Using DNA metabarcoding, we observed that increases in the number of plant genera in pollen increased adult emergence in both foraging periods, but not oviposition or larval development. We also observed that foraging bees consistently visited certain genera during each foraging period, especially Acer, Salix, and Rubus. However, pollen collected by O. lignaria over different years varied in the number of total genera visited, highlighting the importance of multi-year studies to ascertain bee foraging preferences and its link to developmental success.

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Data are archived through the University of Washington Research Works Archive: https://digital.lib.washington.edu/researchworks/

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References

  • Allen MP (1997) The problem of multicollinearity. In: Allen MP (ed) Understanding regression analysis. Springer, Boston, pp 176–180

    Google Scholar 

  • Arstingstall KA, DeBano SJ, Li X, Wooster DE, Rowland MM, Burrows S, Frost K (2021) Capabilities and limitations of using DNA metabarcoding to study plant–pollinator interactions. Mol Ecol 30:5266–5297

    Article  PubMed  Google Scholar 

  • Bartomeus I, Park MG, Gibbs J, Danforth BN, Lakso AN, Winfree R (2013) Biodiversity ensures plant-pollinator phenological synchrony against climate change. Ecol Lett 16:1331–1338

    Article  PubMed  Google Scholar 

  • Bell KL, Loeffler VM, Brosi BJ (2017) An rbcL reference library to aid in the identification of plant species mixtures by DNA metabarcoding. App Plant Sci 5:1600110

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch J, Kemp WP (2000) Development and emergence of the orchard pollinator Osmia lignaria (Hymenoptera: Megachilidae). Environ Entomol 29:8–13

    Article  Google Scholar 

  • Bosch J, Kemp WP, Peterson SS (2000) Management of Osmia lignaria (Hymenoptera: Megachilidae) populations for almond pollination: methods to advance bee emergence. Environ Entomol 29:874–883

    Article  Google Scholar 

  • Bosch J, Sgolastra F, Kemp WP (2010) Timing of eclosion affects diapause development, fat body consumption and longevity in Osmia lignaria, a univoltine, adult-wintering solitary bee. J Insect Physiol 56:1949–1957

    Article  CAS  PubMed  Google Scholar 

  • CaraDonna PJ, Cunningham JL, Iler AM (2018) Experimental warming in the field delays phenology and reduces body mass, fat content and survival: implications for the persistence of a pollinator under climate change. Funct Ecol 32:2345–2356

    Article  Google Scholar 

  • Christenhusz MJM (2012) Stauntonia Latifolia. Curtis’s Bot Mag 29:297–302

    Article  Google Scholar 

  • Cusser S, Neff JL, Jha S (2016) Natural land cover drives pollinator abundance and richness, leading to reductions in pollen limitation in cotton agroecosystems. Agr Ecosyst Environ 226:33–42

    Article  Google Scholar 

  • de Vere N, Rich TCG, Ford CR, Trinder SA, Long C, Moore CW, Satterthwaite D, Davies H, Allainguillaume J, Ronca S, Tatarinova T, Garbett H, Walker K, Wilkinson MJ (2012) DNA barcoding the native flowering plants and conifers of wales. PLoS ONE 7:e37945

    Article  PubMed  PubMed Central  Google Scholar 

  • de Vere N, Jones LE, Gilmore T, Moscrop J, Lowe A, Smith D, Hegarty MJ, Creer S, Ford CR (2017) Using DNA metabarcoding to investigate honey bee foraging reveals limited flower use despite high floral availability. Sci Rep 7:42838

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebeling A, Klein AM, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117:1808–1815

    Article  Google Scholar 

  • Eckhardt M, Haider M, Dorn S, Müller A (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Anim Ecol 83:588–597

    Article  PubMed  Google Scholar 

  • Fenesi A, Vágási CI, Beldean M, Földesi R, Kolcsár LP, Shapiro JT, Török E, Kovács-Hostyánszki A (2015) Solidago canadensis impacts on native plant and pollinator communities in different-aged old fields. Basic Appl Ecol 16:335–346

    Article  Google Scholar 

  • Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallant AL, Euliss NH Jr, Browning Z (2014) Mapping large-area landscape suitability for honey bees to assess the influence of land-use change on sustainability of national pollination services. PLoS ONE 9(6):e99268

    Article  PubMed  PubMed Central  Google Scholar 

  • Hawkins J, de Vere N, Griffith A, Ford CR, Allainguillaume J, Hegarty MJ, Baillie L, Adams-Groom B (2015) Using DNA metabarcoding to identify the floral composition of honey: a new tool for investigating honey bee foraging preferences. PLoS ONE 10:e0134735

    Article  PubMed  PubMed Central  Google Scholar 

  • Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proceed Nat Acad Sci USA 110:555–558

    Article  CAS  Google Scholar 

  • Keller A, Danner N, Grimmer G, Ankenbrand M, von der Ohe K, von der Ohe W, Rost S, Härtel S, Steffan-Dewenter I (2015) Evaluating multiplexed next-generation sequencing as a method in palynology for mixed pollen samples. Plant Biol 17:558–566

    Article  CAS  PubMed  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceed Royal Soc b 274:303–313

    Article  Google Scholar 

  • Koh I, Lonsdorf EV, Williams NM, Brittain C, Isaacs R, Gibbs J, Ricketts TH (2016) Modeling the status, trends, and impacts of wild bee abundance in the United States. Proceed Nat Acad Sci USA 113:140–145

    Article  CAS  Google Scholar 

  • Kraaijeveld K, de Weger LA, Ventayol García M, Buermans H, Frank J, Hiemstra PS, den Dunnen JT (2015) Efficient and sensitive identification and quantification of airborne pollen using next-generation DNA sequencing. Mol Ecol Resour 15:8–16

    Article  CAS  PubMed  Google Scholar 

  • Kral-O’Brien KC, O’Brien PL, Hovick TJ, Harmon JP (2021) Meta-analysis: Higher plant richness supports higher pollinator richness across many land use types. Ann Entomol Soc Am 114:267–275

    Article  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  • Li H, Wysoker A, Handsaker B, Marth G, Abecasis G, Ruan J, Homer N, Durbin R, Fennell T (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Lett 10:539–550

    Article  PubMed  Google Scholar 

  • Lucas A, Bodger O, Brosi BJ, Ford CR, Forman DW, Greig C, Hegarty M, Neyland PJ, de Vere N (2018) Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding. J Anim Ecol 87:1008–1021

    Article  PubMed  PubMed Central  Google Scholar 

  • MacInnis G, Forrest JRK (2019) Pollination by wild bees yields larger strawberries than pollination by honey bees. J Appl Ecol 56:824–832

    Article  Google Scholar 

  • MacIvor JS, Cabral JM, Packer L (2014) Pollen specialization by solitary bees in an urban landscape. Urban Ecosyst 17:139–147

    Article  Google Scholar 

  • Maglianesi MA, Hanson P, Brenes E, Benadi G, Schleuning M, Dalsgaard B (2020) High levels of phenological asynchrony between specialized pollinators and plants with short flowering phases. Ecology 101:e03162

    Article  PubMed  Google Scholar 

  • McFrederick QS, Rehan SM (2016) Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee. Mol Ecol 25:2302–2311

    Article  CAS  PubMed  Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant-pollinator interactions. Ann Bot 103:1355–1363

    Article  PubMed  PubMed Central  Google Scholar 

  • Moerman R, Vanderplanck M, Fournier D, Jacquemart AL, Michez D (2017) Pollen nutrients better explain bumblebee colony development than pollen diversity. Insect Conserv Diver 10:171–179

    Article  Google Scholar 

  • National Land Cover Database (2011) https://www.mrlc.gov/data/nlcd-2011-land-cover-conus

  • Nicholson CC, Ricketts TH (2019) Wild pollinators improve production, uniformity, and timing of blueberry crops. Agr Ecosyst Environ 272:29–37

    Article  Google Scholar 

  • Oksanen J, Blanchet GF, Friendly M, Kindt R, Legendre P, et al. (2020) vegan: Community Ecology Package (R package version 2.5–7).

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reilly JR, Artz DR, Biddinger D, Bobiwash K, Boyle NK et al (2020) Crop production in the USA is frequently limited by a lack of pollinators: pollination limitation in US crops. Proceed R Soc b 287:2–9

    Google Scholar 

  • Rust RW (1987) Collecting of Pinus (Pinaceae) pollen by Osmia bees (Hymenoptera: Megachilidae). Environ Entomol 16:668–671

    Article  Google Scholar 

  • Rust RW (1990) Spatial and temporal heterogeneity of pollen foraging in Osmia lignaria propinqua (Hymenoptera: Megachilidae). Environ Entomol 19:332–338

    Article  Google Scholar 

  • Settele J, Bishop J, Potts SG (2016) Climate change impacts on pollination. Nature Plants 2:16092

    Article  PubMed  Google Scholar 

  • Sutter L, Jeanneret P, Bartual AM, Bocci G, Albrecht M (2017) Enhancing plant diversity in agricultural landscapes promotes both rare bees and dominant crop-pollinating bees through complementary increase in key floral resources. J Appl Ecol 54:1856–1864

    Article  Google Scholar 

  • Switanek M, Crailsheim K, Truhetz H, Brodschneider R (2017) Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci Total Environ 579:1581–1587

    Article  CAS  PubMed  Google Scholar 

  • Torchio PF (1976) Use of Osmia lignaria Say (Hymenoptera: Apoidea, Megachilidae) as a pollinator in an apple and prune orchard. J Kansas Entomol Soc 49:475–482

    Google Scholar 

  • Weather Underground (2021) https://www.wunderground.com/

  • Urbanowicz C, Muñiz PA, McArt SH (2020) Honey bees and wild pollinators differ in their preference for and use of introduced floral resources. Ecol Evol 10:6741–6751

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM (2016) Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceed Nat Acad Sci USA 113:e4035–e4042

    Article  CAS  Google Scholar 

  • Vaudo AD, Tooker JF, Patch HM, Biddinger DJ, Coccia M et al (2020) Pollen protein: lipid macronutrient ratios may guide broad patterns of bee species floral preferences. InSects 11:132

    Article  PubMed  PubMed Central  Google Scholar 

  • Vicens N, Bosch J (2000) Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on ‘Red Delicious’ apple. Environ Entomol 29:235–240

    Article  Google Scholar 

  • Vitale N, Torretta JP, Durante S, Basilio A, Vázquez DP (2020) Similarities and differences in the realized niche of two allopatric populations of a solitary bee under environmental variability. Apidologie 51:439–454

    Article  Google Scholar 

  • Wasielewski O, Wojciechowicz T, Giejdasz K, Krishnan N (2013) Overwintering strategies in the red mason solitary bee—physiological correlates of midgut metabolic activity and turnover of nutrient reserves in females of Osmia bicornis. Apidologie 44:642–656

    Article  CAS  Google Scholar 

  • Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Amin Amos for his help in processing the weather data. We are grateful to Drs. Jonathan Bakker, Berry Brosi, and Julie Combs (University of Washington), and Quinn McFrederick (University of California, Riverside) for technical advice. This research was conducted by LRW in partial fulfillment of the requirements for the Ph.D. degree from the University of Washington.

Funding

This study was supported by USDA-NIFA McIntire Stennis Cooperative Forestry Program-Accession No. 1012774 (to PCT) and the University of Washington Hall Conservation Genetics Fund (to LRW).

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LRW and PCT conceived and designed the experiments. LRW performed the experiments. LRW, STW, and PCT analyzed the data. LRW wrote the manuscript; other authors provided editorial advice.

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Correspondence to Patrick C. Tobin.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Communicated by Riccardo Bommarco.

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Westreich, L.R., Westreich, S.T. & Tobin, P.C. Native solitary bee reproductive success depends on early season precipitation and host plant richness. Oecologia 201, 965–978 (2023). https://doi.org/10.1007/s00442-023-05354-5

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