Smithsonian National Museum of Natural History

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Department ofBotany

No. 355
July 2014

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In This Issue

Diverse Forests are Stronger against Deer

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In deer-populated forests, tastier plants can avoid being eaten if they are surrounded by less appealing plants. But with deer gone, diverse plots become weaker as plant survival drops, according to a study from the Smithsonian Environmental Research Center, published in the Proceedings of the Royal Society B.

Despite their reputation for destroying plant life, deer can actually make diverse forests stronger. Diverse forests can hide tastier plants by surrounding them with repellant ones. But without deer the benefits of biodiversity drop. (Photo by Steve Hillebrand, U.S. Fish and Wildlife Service)

Despite their reputation for destroying plant life, deer can actually make diverse forests stronger. Diverse forests can hide tastier plants by surrounding them with repellant ones. But without deer the benefits of biodiversity drop. (Photo by Steve Hillebrand, U.S. Fish and Wildlife Service)

Ecologists have long suspected that a diverse forest is a better forest: stronger, healthier and more adept at resisting pests, diseases and environmental stresses like droughts and fires. But few had done experiments to disentangle the effects of biodiversity from other factors like herbivores, because forests are slow growing and hard to manipulate. The Smithsonian study shows that by eating the most dominant plants, deer can dramatically change the pros and cons of diversity.

"Even though forests cover a third of the Earth's land surface and can be incredibly diverse, we know remarkably little about the function of diversity in forests," said Susan Cook-Patton, a Smithsonian postdoctoral fellow and the study's lead author. "Tree seedlings are small, but they will become the forests of the future, so we wanted to track survival at this critical life-history stage."

To uncover whether tree seedling survival hinged on diversity, the research team set up hundreds of experimental plots in a forest, some with 15 seedlings of only a single species, and some with up to 15 different species. Then they put wire cages around half to exclude browsing by deer, which in many areas can be the single most important determinant for tree-species survival. This was a critical step in the research. Without cages it is impossible to disentangle the effects of plant–plant interactions from the effects of plant–herbivore interactions. Both can drive diversity effects, but they have completely different consequences for thinking about managing ecosystems.

The researchers meticulously tracked the plots for three years, recording growth, survival and herbivore damage. They discovered that the dominant species—including red maple, green ash and red oak—all suffered intense deer browsing. Meanwhile, deer shunned most of the least productive species, including hickory. By selectively consuming the dominant species, deer gave suppressed plants a chance to thrive, as even the slow-growing hickories and other species grew bigger in more diverse plots.

These patterns, however, depended on whether tree seedlings were in a diverse or species-poor plot. Where deer browsed, single-species plots suffered 53 percent more damage than mixed plots. "Red maples were heavily browsed when surrounded by other red maples, but survived and thrived when surrounded by less palatable tree seedlings," said Cook-Patton. "By the third year, red maples were roughly three-and-a-half times bigger in more diverse communities."

The authors speculate that deer were first drawn to the mixed plots because those plots all contained species they prefer to eat—red maple, red oak and green ash. However, once there, they were turned off by the more repellant species surrounding them.

But with deer out of the picture, the tables turned. In deer-free plots, plants were less likely to survive in a diverse forest, although these survivors did grow slightly bigger. "We've discovered that ecosystem function depends on diversity at different levels of the food chain," said John Parker, senior ecologist at SERC. "Feedbacks among the different levels can ultimately change the picture of how diversity works, and to better manage forests we need to understand the interactive effects of diversity throughout the food web."

The researchers are now testing their findings on a larger scale in BiodiversiTree, an experimental forest of more than 20,000 trees the team planted in 2013 that is designed to last at least a hundred years. "Forests are increasingly threatened by climate change and invasive pests, and experiments like these will tell us if diverse forests are better poised to weather these future challenges," Cook-Patton said.

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Rendall, A.R., Sutherland, D.R., Cooke, R., and White, J. 2014. Camera trapping: a contemporary approach to monitoring invasive rodents in high conservation priority ecosystems. PLoS ONE 9(3):e86592.

Richards, M.B., and Méndez, V.E. 2014. Interactions between carbon sequestration and shade tree diversity in a smallholder coffee cooperative in El Salvador. Conserv. Biol. 28(2):489-497.

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Rodríguez, V., Brown, R.P., Terrasa, B., Pérez-Mellado, V., Picornell, A., Castro, J.A., and Ramon, C. 2014. Genetic diversity and historical biogeography of the Maltese wall lizard, Podarcis filfolensis (Squamata: Lacertidae). Conserv. Genet. 15(2):295-304.

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Savaria, M.C., and O'Connor, N.J. 2013. Predation of the non-native Asian shore crab Hemigrapsus sanguineus by a native fish species, the cunner (Tautogolabrus adspersus). J. Exp. Marine Biol. Ecol. 449:335-339.

Scheele, B., Guarino, F., Osborne, W., Hunter, D.A., Skerratt, L.F., and Driscoll, D.A. 2014. Decline and re-expansion of an amphibian with high prevalence of chytrid fungus. Biol. Conserv. 170:86-91.

Scherer, A.E., and Santangelo, N. 2014. Assessment of reproductive requirements in habitat conservation efforts: a case study on blackside dace (Chrosomus cumberlandensis), a federally listed threatened species. Can. J. Fish. Aquat. Sci. 71(3):408-415.

Scherson, R.A., Albornoz, A.A., Moreira-Muñoz, A.S., and Urbina-Casanova, R. 2014. Endemicity and evolutionary value: a study of Chilean endemic vascular plant genera. Ecol. Evol. 4(6):806-816.

Seddon, P.J., Moehrenschlager, A., and Ewen, J. 2014. Reintroducing resurrected species: selecting DeExtinction candidates. Trends Ecol. Evol. 29(3):140-147.

Segura, L.N., Depino, E.A., Gandoy, F., Di Sallo, F.G., and Arturi, M.F. 2014. Distance between forest patches and individual tree canopy size influence the abundance of red-crested cardinals (Paroaria coronata) in natural forests of Argentina. Interciencia 39(1):54-59.

Senko, J., Mancini, A., Seminoff, J.A., and Koch, V. 2014. Bycatch and directed harvest drive high green turtle mortality at Baja California Sur, Mexico. Biol. Conserv. 169:24-30.

Sharma, M.V., and Armstrong, J.E. 2013. Pollination of Myristica and other nutmegs in natural populations. Trop. Conserv. Sci. 6(5):595-607.

Siler, C.D., Lira-Noriega, A., and Brown, R.M. 2014. Conservation genetics of Australasian sailfin lizards: flagship species threatened by coastal development and insufficient protected area coverage. Biol. Conserv. 169:100-108.

Silva, J.P., Palmeirim, J.M., Alcazar, R., Correia, R., Delgado, A., and Moreira, F. 2014. A spatially explicit approach to assess the collision risk between birds and overhead power lines: a case study with the little bustard. Biol. Conserv. 170:256-263.

Sinu, P.A., and Sharma, M.V. 2013. Insect functional guilds in the flowering canopy of Myristica fatua in a lowland swamp, central Western Ghats, India. Trop. Conserv. Sci. 6(5):653-662.

Smith, D.A.E. 2014. The effects of land-use policies on the conservation of Borneo's endemic Presbytis monkeys. Biodivers. Conserv. 23(4):891-908.

Smith, L.L., and Barney, J.N. 2014. The relative risk of invasion: evaluation of Miscanthus × giganteus seed establishment. Invas. Plant Sci. Manage. 7(1):93-106.

Snäll, T., Forslund, P., Jeppsson, T., Lindhe, A., and O'Hara, R.B. 2014. Evaluating temporal variation in Citizen Science Data against temporal variation in the environment. Ecography 37(3):293-300.

Soh, Y.H., Carrasco, L.R., Miquelle, D.G., Jiang, J.S., Yang, J., Stokes, E.J., Tang, J.R., Kang, A.L., Liu, P.Q., and Rao, M. 2014. Spatial correlates of livestock depredation by Amur tigers in Hunchun, China: relevance of prey density and implications for protected area management. Biol. Conserv. 169:117-127.

Stapleton, S., Atkinson, S., Hedman, D., and Garshelis, D. 2014. Revisiting Western Hudson Bay: using aerial surveys to update polar bear abundance in a sentinel population. Biol. Conserv. 170:38-47.

Staunton, K.M., Robson, S.K.A., Burwell, C.J., Reside, A.E., and Williams, S.E. 2014. Projected distributions and diversity of flightless ground beetles within the Australian wet tropics and their environmental correlates. PLoS ONE 9(2):e88635.

Stelkens, R.B., Pompini, M., and Wedekind, C. 2014. Testing the effects of genetic crossing distance on embryo survival within a metapopulation of brown trout (Salmo trutta). Conserv. Genet. 15(2):375-386.

Stockan, J.A., Baird, J., Langan, S.J., Young, M.R., and Iason, G.R. 2014. Effects of riparian buffer strips on ground beetles (Coleoptera, Carabidae) within an agricultural landscape. Insect Conserv. Divers. 7(2):172-184.

Stokes, D.L., Boersma, P.D., de Casenave, J.L., and García-Borboroglu, P. 2014. Conservation of migratory Magellanic penguins requires marine zoning. Biol. Conserv. 170:151-161.

Strubbe, D., and Matthysen, E. 2014. Patterns of niche conservatism among non-native birds in Europe are dependent on introduction history and selection of variables. Biol. Invasions 16(4):759-764.

Sullivan, B.L., Aycrigg, J.L., Barry, J.H., Bonney, R.E., Bruns, N., Cooper, C.B., Damoulas, T., Dhondt, A.A., Dietterich, T., Farnsworth, A., Fink, D., Fitzpatrick, J.W., Fredericks, T., Gerbracht, J., Gomes, C., Hochachka, W.M., Iliff, M.J., Lagoze, C., La Sorte, F.A., Merrifield, M., Morris, W., Phillips, T.B., Reynolds, M., Rodewald, A.D., Rosenberg, K.V., Trautmann, N.M., Wiggins, A., Winkler, D.W., Wong, W.K., Wood, C.L., Yu, J., and Kelling, S. 2014. The eBird enterprise: an integrated approach to development and application of citizen science. Biol. Conserv. 169:31-40.

Suurkuukka, H., Virtanen, R., Suorsa, V., Soininen, J., Paasivirta, L., and Muotka, T. 2014. Woodland key habitats and stream biodiversity: does small-scale terrestrial conservation enhance the protection of stream biota? Biol. Conserv. 170:10-19.

Swanson, K.M., Drexler, J.Z., Schoellhamer, D.H., Thorne, K.M., Casazza, M.L., Overton, C.T., Callaway, J.C., and Takekawa, J.Y. 2014. Wetland Accretion Rate Model of Ecosystem Resilience (WARMER) and its application to habitat sustainability for endangered species in the San Francisco Estuary. Estuaries Coasts 37(2):476-492.

Tadesse, G., Zavaleta, E., and Shennan, C. 2014. Coffee landscapes as refugia for native woody biodiversity as forest loss continues in southwest Ethiopia. Biol. Conserv. 169:384-391.

Tamayo, M., and Olden, J.D. 2014. Forecasting the vulnerability of lakes to aquatic plant invasions. Invas. Plant Sci. Manage. 7(1):32-45.

Thiers, L., Delord, K., Barbraud, C., Phillips, R.A., Pinaud, D., and Weimerskirch, H. 2014. Foraging zones of the two sibling species of giant petrels in the Indian Ocean throughout the annual cycle: implication for their conservation. Mar. Ecol. Progr. Ser. 499:233-248.

Thogmartin, W.E., and McKann, P.C. 2014. Large-scale climate variation modifies the winter grouping behavior of endangered Indiana bats. J. Mammal. 95(1):117-127.

Thomaes, A., De Keersmaeker, L., Verschelde, P., Vandekerkhove, K., and Verheyen, K. 2014. Tree species determine the colonisation success of forest herbs in post-agricultural forests: results from a 9 yr introduction experiment. Biol. Conserv. 169:238-247.

Thompson, C., Sweitzer, R., Gabriel, M., Purcell, K., Barrett, R., and Poppenga, R. 2014. Impacts of rodenticide and insecticide toxicants from marijuana cultivation sites on fisher survival rates in the Sierra National Forest, California. Conserv. Lett. 7(2):91-102.

Torres, I., and Arizaga, S. 2014. Notes on new localities of wild populations of black sapote (Diospyros xolocotzii, Ebenaceae), threatened species of western Mexico. Acta Bot. Mex. 107:19-26.

Toth, A.B., Lyons, S.K., and Behrensmeyer, A.K. 2014. A century of change in Kenya's mammal communities: increased richness and decreased uniqueness in six protected areas. PLoS ONE 9(4):e93092.

Trivellone, V., Schoenenberger, N., Bellosi, B., Jermini, M., de Bello, F., Mitchell, E.A.D., and Moretti, M. 2014. Indicators for taxonomic and functional aspects of biodiversity in the vineyard agroecosystem of Southern Switzerland. Biol. Conserv. 170:103-109.

Troupin, D., and Carmel, Y. 2014. Can agro-ecosystems efficiently complement protected area networks? Biol. Conserv. 169:158-166.

Turvey, S.T., Fernández-Secades, C., Nuñez-Miño, J.M., Hart, T., Martinez, P., Brocca, J.L., and Young, R.P. 2014. Is local ecological knowledge a useful conservation tool for small mammals in a Caribbean multicultural landscape? Biol. Conserv. 169:189-197.

Tyrrell, M., and Clark, D.A. 2014. What happened to climate change? CITES and the reconfiguration of polar bear conservation discourse. Global Environ. Change 24:363-372.

Valle, M., Chust, G., del Campo, A., Wisz, M.S., Olsen, S.M., Garmendia, J.M., and Borja, Á. 2014. Projecting future distribution of the seagrass Zostera noltii under global warming and sea level rise. Biol. Conserv. 170:74-85.

Van Colen, C., Verbelen, D., Devos, K., Agten, L., Van Tomme, J., Vincx, M., and Degraer, S. 2014. Sediment-benthos relationships as a tool to assist in conservation practices in a coastal lagoon subjected to sediment change. Biodivers. Conserv. 23(4):877-889.

Van Houtan, K.S., and Kittinger, J.N. 2014. Historical commercial exploitation and the current status of Hawaiian green turtles. Biol. Conserv. 170:20-27.

Vanderplank, S.E., Mata, S., and Ezcurra, E. 2014. Biodiversity and archeological conservation connected: aragonite shell middens increase plant diversity. BioScience 64(3):202-209.

VanderWaal, K.L., Atwill, E.R., Isbell, L.A., and McCowan, B. 2014. Quantifying microbe transmission networks for wild and domestic ungulates in Kenya. Biol. Conserv. 169:136-146.

VanZandt, M., Delparte, D., Hart, P., Duvall, F., and Penniman, J. 2014. Nesting characteristics and habitat use of the endangered Hawaiian petrel (Pterodroma sandwichensis) on the island of Lana'i. Waterbirds 37(1):43-51.

Velevski, M., Grubac, B., and Tomović, L. 2014. Population viability analysis of the Egyptian vulture Neophron percnopterus in Macedonia and implications for its conservation. Acta Zool. Bulgar. 66(1):43-58.

Venter, J.A., Prins, H.H.T., Balfour, D.A., and Slotow, R. 2014. Reconstructing grazer assemblages for protected area restoration. PLoS ONE 9(3):e90900.

Verdiell-Cubedo, D., Ruiz-Navarro, A., Torralva, M., Moreno-Valcárcel, R., and Oliva-Paterna, F.J. 2014. Habitat use of an endangered cyprinodontid fish in a saline wetland of the Iberian Peninsula (SW Mediterranean Sea). Mediterr. Mar. Sci. 15(1):27-36.

Vihotogbé, R., Kakaï, R.G., Bongers, F., van Andel, T., van den Berg, R.G., Sinsin, B., and Sosef, M.S.M. 2014. Impacts of the diversity of traditional uses and potential economic value on food tree species conservation status: case study of African bush mango trees (Irvingiaceae) in the Dahomey Gap (West Africa). Plant Ecol. Evol. 147(1):109-125.

Vit, P., Wolfová, K., Urfus, T., Tájek, P., and Suda, J. 2014. Interspecific hybridization between rare and common plant congeners inferred from genome size data: assessing the threat to the Czech serpentine endemic Cerastium alsinifolium. Preslia 86(1):95-117.

Volkmann, L., Martyn, I., Moulton, V., Spillner, A., and Mooers, A.O. 2014. Prioritizing populations for conservation using phylogenetic networks. PLoS ONE 9(2):e88945.

Wang, W.J., He, H.S., Fraser, J.S., Thompson, F.R., Shifley, S.R., and Spetich, M.A. 2014. LANDIS PRO: a landscape model that predicts forest composition and structure changes at regional scales. Ecography 37(3):225-229.

Webb, E.L., Jachowski, N.R.A., Phelps, J., Friess, D.A., Than, M.M., and Ziegler, A.D. 2014. Deforestation in the Ayeyarwady Delta and the conservation implications of an internationally-engaged Myanmar. Global Environ. Change 24:321-333.

Wen, J., Ree, R.H., Ickert-Bond, S.M., Nie, Z.L., and Funk, V. 2013. Biogeography: where do we go from here? Taxon 62(5):912-927.

Westermann, F.L., Suckling, D.M., and Lester, P.J. 2014. Disruption of foraging by a dominant invasive species to decrease its competitive ability. PLoS ONE 9(3):e90173.

Wetterer, J.K. 2014. A South American fire ant, Solenopsis nr. saevissima, in Guadeloupe, French West Indies. Biol. Invasions 16(4):755-758.

Whitehead, A.L., Lyver, P.O., Jones, C.J., Bellingham, P.J., MacLeod, C.J., Coleman, M., Karl, B.J., Drew, K., Pairman, D., Gormley, A.M., and Duncan, R.P. 2014. Establishing accurate baseline estimates of breeding populations of a burrowing seabird, the grey-faced petrel (Pterodroma macroptera gouldi) in New Zealand. Biol. Conserv. 169:109-116.

Wilder, B.T., Betancourt, J.L., Epps, C.W., Crowhurst, R.S., Mead, J.I., and Ezcurra, E. 2014. Local extinction and unintentional rewilding of bighorn sheep (Ovis canadensis) on a desert island. PLoS ONE 9(3):e91358.

Williams, R., Clark, C.W., Ponirakis, D., and Ashe, E. 2014. Acoustic quality of critical habitats for three threatened whale populations. Anim. Conserv. 17(2):174-185.

Williams, R., Grand, J., Hooker, S.K., Buckland, S.T., Reeves, R.R., Rojas-Bracho, L., Sandilands, D., and Kaschner, K. 2014. Prioritizing global marine mammal habitats using density maps in place of range maps. Ecography 37(3):212-220.

Williams, W.I., Friedman, J.M., Gaskin, J.F., and Norton, A.P. 2014. Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol. Appl. 7(3):381-393.

Wilsey, C.B., Lawler, J.J., Cimprich, D., and Schumaker, N.H. 2014. Dependence of the endangered black-capped vireo on sustained cowbird management. Conserv. Biol. 28(2):561-571.

Winiarski, K.J., Miller, D.L., Paton, P.W.C., and McWilliams, S.R. 2014. A spatial conservation prioritization approach for protecting marine birds given proposed offshore wind energy development. Biol. Conserv. 169:79-88.

Woziwoda, B., Kopeć, D., and Witkowski, J. 2014. The negative impact of intentionally introduced Quercus rubra L. on a forest community. Acta Soc. Bot. Pol. 83(1):39-49.

Wuczyński, A., Dajdok, Z., Wierzcholska, S., and Kujawa, K. 2014. Applying red lists to the evaluation of agricultural habitat: regular occurrence of threatened birds, vascular plants, and bryophytes in field margins of Poland. Biodivers. Conserv. 23(4):999-1017.

Yineger, H., Schmidt, D.J., and Hughes, J.M. 2014. Genetic structuring of remnant forest patches in an endangered medicinal tree in North-western Ethiopia. BMC Genet. 15:31.

Zaccara, S., Crosa, G., Vanetti, I., Binelli, G., Harper, D.M., Mavuti, K.M., Balarin, J.D., and Britton, J.R. 2014. Genetic and morphological analyses indicate high population mixing in the endangered cichlid Alcolapia flock of East Africa. Conserv. Genet. 15(2):429-440.

Zachos, F.E., Mattioli, S., Ferretti, F., and Lorenzini, R. 2014. The unique Mesola red deer of Italy: taxonomic recognition (Cervus elaphus italicus nova ssp., Cervidae) would endorse conservation. Italian J. Zool. 81(1):136-143.

Zakkak, S., Kakalis, E., Radović, A., Halley, J.M., and Kati, V. 2014. The impact of forest encroachment after agricultural land abandonment on passerine bird communities: the case of Greece. J. Nature Conserv. 22(2):157-165.

Zapata, V.M., and Robledano, F. 2014. Assessing biodiversity and conservation value of forest patches secondarily fragmented by urbanisation in semiarid southeastern Spain. J. Nature Conserv. 22(2):166-175.

Zhang, R., Liu, J.L., Mo, L.C., and Zhang, Z.M. 2014. Environmental and human factors influencing invasive plant species in Songshan National Nature Reserve. Forest Chron. 90(2):197-201.

Zheng, Y.L., and Deng, Y.F. 2014. A new species of Primulina (Gesneriaceae) from Guangdong, China. Phytotaxa 163(1):48-53.

Zomer, R.J., Trabucco, A., Wang, M.C., Lang, R., Chen, H.F., Metzger, M.J., Smajgl, A., Beckschafer, P., and Xu, J.C. 2014. Environmental stratification to model climate change impacts on biodiversity and rubber production in Xishuangbanna, Yunnan, China. Biol. Conserv. 170:264-273.

Zou, Y., Sang, W.G., Zhou, H.C., Huang, L.Y., and Axmacher, J.C. 2014. Altitudinal diversity patterns of ground beetles (Coleoptera: Carabidae) in the forests of Changbai Mountain, Northeast China. Insect Conserv. Divers. 7(2):161-171.

Zulka, K.P., Abensperg-Traun, M., Milasowszky, N., Bieringer, G., Gereben-Krenn, B.A., Holzinger, W., Hölzler, G., Rabitsch, W., Reischütz, A., Querner, P., Sauberer, N., Schmitzberger, I., Willner, W., Wrbka, T., and Zechmeister, H. 2014. Species richness in dry grassland patches of eastern Austria: A multi-taxon study on the role of local, landscape and habitat quality variables. Agricult. Ecosyst. & Environ. 182:25-36.

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