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Department ofBotany

No. 383
November 2016

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In This Issue

Rising CO2 Depletes Pollen's Nutritional Potency, Bees Suffer

-Adapted from Smithsonian Insider

Unless you've been living under a rock for the last few years, you've doubtless caught at least a passing reference to the plight of the beleaguered bee. Bees of all types pollinate an estimated 75 percent of our fruit, nut and vegetable crops, and they've been suffering population declines in recent years from a variety of suspected sources. These die-offs are a major concern to farmers and hobby beekeepers, as well as anyone who likes to eat.

A honeybee getting nectar and pollen from goldenrod in southern Michigan. The pollen is the orange substance attached to the bee's leg. (Flickr image by Steve Burt)

A honeybee getting nectar and pollen from goldenrod in southern Michigan. The pollen is the orange substance attached to the bee's leg. (Flickr image by Steve Burt)

Bees like food, too, but a new study led by the U.S. Department of Agriculture's Agricultural Research Service has found that recent increases in carbon dioxide emissions over the last several decades have made a key autumnal food source less nutritious than in the past. This adds one more potential factor to the cocktail of stressors making bees vulnerable to attack by pests, pathogens and pesticides.

USDA Agricultural Research Service plant physiologist Lewis Ziska, together with colleagues from Purdue University, Williams College and the Smithsonian compared the protein content of pollen from historic specimens of Canada goldenrod (Solidago canadensis) from the U.S. National Herbarium collection at the Smithsonian's National Museum of Natural History with pollen from field trials simulating varying levels of atmospheric carbon dioxide. They found that as CO2 levels increased, the protein content of the pollen decreased. The study was published in the journal Proceedings of the Royal Society B (283: 20160414; 2016).

Goldenrod, which blooms from July through October across most of North America, is one of the most widely available sources of pollen for late-year foraging. Though nectar is bees' main food source during the warmer months, bees need the fats, vitamins and minerals from pollen protein to make it through the winter. Because they only store small amounts of it, fluctuations in the amount or quality of the pollen itself can directly affect bee health.

"Goldenrod was the focus because it's the last source of pollen for bees before they overwinter," Ziska says. "Whatever happens to goldenrod in the fall can be a harbinger of overall bee health and their ability to survive until spring."

Three of the many historical goldenrod records kept in the U.S. National Herbarium at the Smithsonian's National Museum of Natural History. These plants were collected in Arizona, Florida and Alabama (left to right). Goldenrod samples in this herbarium were used to measure how rising atmospheric CO2 has impacted protein in pollen. (Photo courtesy Smithsonian's National Museum of Natural History)

Three of the many historical goldenrod records kept in the U.S. National Herbarium at the Smithsonian's National Museum of Natural History. These plants were collected in Arizona, Florida and Alabama (left to right). Goldenrod samples in this herbarium were used to measure how rising atmospheric CO2 has impacted protein in pollen. (Photo courtesy Smithsonian's National Museum of Natural History)

How rising CO2 affects insects' food sources has never been investigated in much depth, despite more than 100 such studies on human food sources suggesting the same kind of impact, Ziska said. Using Smithsonian herbarium samples dating from 1842 through to 1998, as well as more recently collected samples from other sources, Ziska found that pollen protein content has declined by about one third since 1960, from 18 to 12 percent.

A field experiment that simulated a similar range of CO2 exposures, but included future CO2 concentrations up to 500 parts per million (ppm) confirmed the herbarium results.  Still, as Ziska pointed out, it's not clear if there's an upper limit to the effect, or if the protein content will eventually stabilize regardless of the CO2 concentration in the atmosphere.

The silver lining to the study, he said, is that commercial and hobby honeybee keepers may be able to counteract any nutritional deficiencies by supplying additional protein late in the fall. How to ameliorate the impact on wild, solitary bees is, however, unclear.

"We wanted to conduct a robust study by looking at both the historical record and field experiments," Ziska says.  Though he started out by visiting herbariums around the world, including in Australia, the Smithsonian's herbarium "has by far the best and most diverse set of herbarium samples for studying long term climate effects," he adds.

Andrew Clark, who now works for the USDA but at the time of the study was an Smithsonian herbarium collections specialist guiding Ziska through the Solidago specimens, says that the use of goldenrod in this way is a fairly novel approach to the kinds of research typically conducted with herbariums. Pollen studies, for example, aren't done very often any more, and typically focus on the structure of the pollen itself to aid in plant family classification.

"The Smithsonian herbarium goes right to the heart of America's past, because when it started our first collections were from people like Lewis and Clark, frontiersmen who were identifying what was unique to America. No European had seen what was there," Clark said. "It's a very clear snapshot of what our natural environment looked like at that time."

Whether or not the bees will be able to adjust to a degraded pollen source is still in unclear.

"As with most biological organisms, there is some capacity for adaptation, but how much is an open question," Ziska paused, then continued. "I often read where 'CO2 is plant food', but that simple meme falls short of understanding the complexity of CO2 in plant biology. I suspect that plant pollinators are just the tip of the iceberg—or flower."

Biodiversity Shields Fish Communities from Warming

-Adapted from Smithsonian Insider

In a recently completed survey of more than 3,000 fish species in 44 countries around the world marine biologists have discovered that communities with a high diversity of fish species are more resilient to rising temperatures and temperature swings, and are more productive.

A Reef Life Survey diver surveys reef fishes in Raja Ampat, West Papua. (Photo by Rick Stuart-Smith)

A Reef Life Survey diver surveys reef fishes in Raja Ampat, West Papua. (Photo by Rick Stuart-Smith)

Armed with a comprehensive global dataset on marine biodiversity involving standardized counts compiled under the Reef Life Survey, researchers tracked how 11 different environmental factors influenced total fish biomass on coral and rocky reefs around the world. Remarkably biodiversity was one of the strongest indicators of ecosystem resilience. Species richness and functional diversity—how fish use their environment—enhance fish biomass and the ability of a fish community to tolerate warm temperatures.

"Biodiversity is not just an aesthetic or spiritual issue—it's critical to the healthy functioning of ecosystems and the important services they provide to humans, like seafood," says Emmett Duffy, director of the Tennenbaum Marine Observatories Network and senior scientist at the Smithsonian Environmental Research Center. Duffy is lead author of a study published today in the Proceedings of the National Academy of Sciences, offering strong proof that preserving marine biodiversity benefits the oceans, and with it humans.

The discovery came out of the Reef Life Survey, a global study "based on more than 4,000 underwater surveys," said co-author Rick Stuart-Smith of the University of Tasmania. The large survey "was only possible with the enthusiastic contributions of highly trained volunteer divers in the Reef Life Survey program, which allowed us to achieve this comprehensive coverage of the world's reefs, from tropical to polar waters."

A reef diver surveys fish on a transect in Isla Pastores, on the Caribbean coast of Panama. (Photo by Emmett Duffy)

A reef diver surveys fish on a transect in Isla Pastores, on the Caribbean coast of Panama. (Photo by Emmett Duffy)

Warmer ocean temperatures tend to boost fish biomass on average, the scientists found, while wide temperature fluctuations hinder it. Overall, biodiversity made fish communities more resilient to a changing climate. In communities with only a few species, fish biomass tended to increase with rising temperatures until seas warmed above 20 degrees Celsius (68 degrees Fahrenheit)—at which point biomass started to fall. Communities with many species remained stable at these higher temperatures.

Diversity had a similar buffering effect against temperature swings, the researchers found. While both high- and low-diversity communities were less productive under fluctuating temperatures, high-diversity communities suffered half as much as low-diversity ones. Communities with more species are better equipped to handle temperature changes because they have more of their bases covered, the researchers suspect. When temperatures fluctuate, a community with numerous species has better odds that at least a few species can thrive in the new normal.

"Biodiversity is paramount to how natural systems work," says co-author Jonathan Lefcheck of the Virginia Institute of Marine Science. This study "shows that experimental ecologists have in fact been on the right track for 20 years."

"Preserving local biodiversity is not only an ethical directive with aesthetical and genetic insurance value," co-author Sergio Navarrete of the Pontifical Catholic University of Chile says. "It is an imperative for human life because of the critical role it plays in providing an essential ecosystem function."

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Hammond, K.R., O'Keefe, J.M., Aldrich, S.P., and Loeb, S.C. 2016. A presence-only model of suitable roosting habitat for the endangered Indiana bat in the southern Appalachians. PLoS ONE 11(4):e0154464.

Hansen, B.K., Krist, A.C., and Tibbets, T.M. 2016. Foraging differences between the native snail, Fossaria sp. and the invasive New Zealand mudsnail (Potamopyrgus antipodarum) in response to phosphorus limitation. Aquat. Ecol. 50(2):297-306.

Hanson, C.T., and Odion, D.C. 2016. Historical forest conditions within the range of the Pacific Fisher and Spotted Owl in the central and southern Sierra Nevada, California, USA. Nat. Areas J. 36(1):8-19.

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Hawkins, T.S., Schiff, N., Wilson, A.D., Leininger, T.D., and Devall, M.S. 2016. Growth and competitive abilities of the federally endangered Lindera melissifolia and the potentially invasive Brunnichia ovata in varying densities, hydrologic regimes, and light availabilities. Botany 94(4):269-276.

Heiss, M. 2016. Migratory behaviour of bird species occurring in critical numbers at Besh Barmag bottleneck in Azerbaijan. Bird Conserv. Int. 26(2):243-255.

Hempel, M., Neukamm, R., and Thiel, R. 2016. Effects of introduced round goby (Neogobius melanostomus) on diet composition and growth of zander (Sander lucioperca), a main predator in European brackish waters. Aquat. Invasions 11(2):167-178.

Henn, J.J., Anderson, C.B., and Pastur, G.M. 2016. Landscape-level impact and habitat factors associated with invasive beaver distribution in Tierra del Fuego. Biol. Invasions 18(6):1679-1688.

Herbert, D.G., and Moussalli, A. 2016. Revision of the dwarf cannibal snails (Nata s.l.) of southern Africa-Nata s.s. and Natella (Mollusca: Gastropoda: Rhytididae), with description of three new species. Zootaxa 4094(1):1-67.

Herriman, K.R., Davis, A.S., Apostol, K.G., Kildisheva, O.A., Ross-Davis, A.L., and Dumroese, R.K. 2016. Do container volume, site preparation, and field fertilization affect restoration potential of Wyoming big sagebrush? Nat. Areas J. 36(2):194-201.

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Hinkson, K.M., and Richter, S.C. 2016. Temporal trends in genetic data and effective population size support efficacy of management practices in critically endangered dusky gopher frogs (Lithobates sevosus). Ecol. Evol. 6(9):2667-2678.

Hintz, W.D., Glover, D.C., Garvey, J.E., Killgore, K.J., Herzog, D.P., Spier, T.W., Colombo, R.E., and Hrabik, R.A. 2016. Status and habitat use of Scaphirhynchus sturgeons in an important fluvial corridor: implications for river habitat enhancement. Trans. Am. Fish. Soc. 145(2):386-399.

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Holzapfel, S.A., Dodgson, J., and Rohan, M. 2016. Successful translocation of the threatened New Zealand root-holoparasite Dactylanthus taylorii (Mystropetalaceae). Plant Ecol. 217(2):127-138.

Honarvar, S., Fitzgerald, D.B., Weitzman, C.L., Sinclair, E.M., Echube, J.M.E., O'Connor, M., and Hearn, G.W. 2016. Assessment of important marine turtle nesting populations on the southern coast of Bioko Island, Equatorial Guinea. Chelonian Conserv. Biol. 15(1):79-89.

Hong, M.S., Wei, W., Yang, Z.S., Yuan, S.B., Yang, X.Y., Gu, X.D., Huang, F., and Zhang, Z.J. 2016. Effects of timber harvesting on Arundinaria spanostachya bamboo and feeding-site selection by giant pandas in Liziping Nature Reserve, China. Forest Ecol. Manag. 373:74-80.

Honsey, A.E., Donabauer, S.B., and Höök, T.O. 2016. An analysis of lake morphometric and land-use characteristics that promote persistence of Cisco in Indiana. Trans. Am. Fish. Soc. 145(2):363-373.

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Huang, F.F., and Peng, S.L. 2016. Intraspecific competitive ability declines towards the edge of the expanding range of the invasive vine Mikania micrantha. Oecologia 181(1):115-123.

Hughes, K.A., López-Martínez, J., Francis, J.E., Crame, J.A., Carcavilla, L., Shiraishi, K., Hokada, T., and Yamaguchi, A. 2016. Antarctic geoconservation: a review of current systems and practices. Environ. Conserv. 43(2):97-108.

Huijser, M.P., Fairbank, E.R., Camel-Means, W., Graham, J., Watson, V., Basting, P., and Becker, D. 2016. Effectiveness of short sections of wildlife fencing and crossing structures along highways in reducing wildlife-vehicle collisions and providing safe crossing opportunities for large mammals. Biol. Conserv. 197:61-68.

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Whitfield, A.K., James, N.C., Lamberth, S.J., Adams, J.B., Perissinotto, R., Rajkaran, A., and Bornman, T.G. 2016. The role of pioneers as indicators of biogeographic range expansion caused by global change in southern African coastal waters. Estuarine Coast. Shelf Sci. 172:138-153.

Wiest, W.A., Correll, M.D., Olsen, B.J., Elphick, C.S., Hodgman, T.P., Curson, D.R., and Shriver, W.G. 2016. Population estimates for tidal marsh birds of high conservation concern in the northeastern USA from a design-based survey. Condor 118(2):274-288.

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Wilder, B.T., O'Meara, C., Monti, L., and Nabhan, G.P. 2016. The importance of indigenous knowledge in curbing the loss of language and biodiversity. BioScience 66(6):499-509.

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Wu, H., Carrillo, J., and Ding, J.Q. 2016. Invasion by alligator weed, Alternanthera philoxeroides, is associated with decreased species diversity across the latitudinal gradient in China. J. Plant Ecol. 9(3):311-319.

Wurtzebach, Z., and Schultz, C. 2016. Measuring ecological integrity: history, practical applications, and research opportunities. BioScience 66(6):446-457.

Yi, Y.J., Cheng, X., Yang, Z.F., and Zhang, S.H. 2016. Maxent modeling for predicting the potential distribution of endangered medicinal plant (H. riparia Lour) in Yunnan, China. Ecol. Eng. 92:260-269.

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Zhang, W.T., Hu, G.Q., Dang, Y., Weindorf, D.C., and Sheng, J.D. 2016. Afforestation and the impacts on soil and water conservation at decadal and regional scales in Northwest China. J. Arid Environ. 130:98-104.

Zhang, Y.B., Liu, Y.L., Fu, J.X., Phillips, N., Zhang, M.G., and Zhang, F. 2016. Bridging the "gap" in systematic conservation planning. J. Nature Conserv. 31:43-50.

Ziegler, S., Merker, S., Streit, B., Boner, M., and Jacob, D.E. 2016. Towards understanding isotope variability in elephant ivory to establish isotopic profiling and source-area determination. Biol. Conserv. 197:154-163.

Ziemba, J.L., Hickerson, C.A.M., and Anthony, C.D. 2016. Invasive Asian earthworms negatively impact keystone terrestrial salamanders. PLoS ONE 11(5):e0151591.

Ziska, L.H., Pettis, J.S., Edwards, J., Hancock, J.E., Tomecek, M.B., Clark, A., Dukes, J.S., Loladze, I., and Polley, H.W. 2016. Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proc. Roy. Soc. B 283(1828):20160414.

Zolotarjova, V., Kraut, A., and Lõhmus, A. 2016. Slash harvesting does not undermine beetle diversity on small clear-cuts containing sufficient legacies. J. Insect Conserv. 20(2):285-294.

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