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Department ofBotany

No. 342
June 2013

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In This Issue

Warming Climate Unlikely to Cause Near-Term Extinction of Ancient Amazon Trees

Adapted from the University of Michigan News Service

A new genetic analysis has revealed that many Amazon tree species are likely to survive human-caused climate warming in the coming century, contrary to previous findings that temperature increases would cause them to die out.

However, the authors of the new study warn that extreme drought and forest fires will impact Amazonia as temperatures rise, and the over-exploitation of the region's resources continues to be a major threat to its future. Conservation policy for the Amazon should remain focused on reducing global greenhouse-gas emissions and preventing deforestation, they said.

The study by University of Michigan evolutionary biologist Christopher Dick, Eldredge Bermingham of the Smithsonian Tropical Research Institute, Simon Lewis of University College London and the University of Leeds and colleagues demonstrates the surprising age of some Amazonian tree species – more than 8 million years – and thereby shows that they have survived previous periods as warm as many of the global warming scenarios forecast for the year 2100.

The new study, published in the journal Ecology and Evolution, is at odds with earlier papers, based on ecological niche-modeling scenarios, which predicted tree species extinctions in response to relatively small increases in global average air temperatures.

"Our paper provides evidence that common Amazon tree species endured climates warmer than the present, implying that – in the absence of other major environmental changes – they could tolerate near-term future warming under climate change," said Dick, an associate professor of ecology and evolutionary biology and acting director of the U-M Herbarium.

But Lewis cautioned that "the past cannot be compared directly with the future."

"While tree species seem likely to tolerate higher air temperatures than today, the Amazon forest is being converted for agriculture and mining, and what remains is being degraded by logging and increasingly fragmented by fields and roads," Lewis said. "Species will not move as freely in today's Amazon as they did in previous warm periods, when there was no human influence. Similarly, today's climate change is extremely fast, making comparisons with the past difficult.

"With a clearer understanding of the relative risks to the Amazon forest, we conclude that direct human impacts, such as forest clearance for agriculture or mining, should remain a focus of conservation policy," Lewis said. "We also need more aggressive action to reduce greenhouse gas emissions in order to minimize the risk of drought and fire impacts to secure the future of most Amazon tree species."

The scientists used a molecular clock approach to determine the ages of 12 widespread Amazon tree species, including the kapok and the balsa. Then they looked at climatic events that have occurred since those tree species emerged. In general, they inferred that the older the age of the tree species, the warmer the climate it has previously survived.

The researchers determined that nine of the tree species have been around for at least 2.6 million years, seven have been present for at least 5.6 million years, and three have existed in the Amazon for more than 8 million years.

Air temperatures across Amazonia in the early Pliocene Epoch (3.6 million to 5 million years ago) were similar to Intergovernmental Panel on Climate Change projections for the region in 2100 using moderate carbon-emission scenarios. Air temperatures in the late Miocene Epoch (5.3 to 11.5 million years ago) were about the same as IPCC projections for the region in 2100 using the highest carbon-emission scenarios.

The 12 tree species used in the study are broadly representative of the Amazon tree flora. Primary forest collection sites were in central Panama, western Ecuador and Amazonian Ecuador. Additional collections were made in Brazil, Peru, French Guiana and Bolivia. Other plant samples were obtained from herbarium specimens.

"The most lasting finding of our study may be the discovery of ancient geographic variation within widespread species, indicating that many rain forest tree species were widely distributed before the major uplift of the northern Andes," said Eldredge Bermingham of the Smithsonian Tropical Research Institute.

To determine the age of each tree species, the researchers extracted and sequenced DNA from plant samples, then looked at the number of genetic mutations contained in those sequences. Using a molecular clock approach and population genetic models, they estimated how long it would take for each of the tree populations to accumulate the observed number of mutations, which provided a minimum age for each species.

"An important caveat is that because we've been in a cold period over the past 2 million years – basically the whole Quaternary Period – some of the trees' adaptations to warmth tolerance may have been lost," Dick said. "Additional research is needed to test whether this has occurred."

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Siamudaala, V.M., Munyeme, M., Matandiko, W., Muma, J.B., and Munang'andu, H.M. 2012. Monitoring the endangered population of the antelope Kobus leche smithemani (Artiodactyla: Bovidae), in the Bangweulu ecosystem, Zambia. Rev. Biol. Trop. 60(4):1631-1639.

Silcock, J.L., and Fensham, R.J. 2013. Arid vegetation in disequilibrium with livestock grazing: evidence from long-term exclosures. Austral Ecol. 38(1):57-65.

Silveira, J.M., Barlow, J., Andrade, R.B., Louzada, J., Mestre, L.A., Lacau, S., Zanetti, R., Numata, I., and Cochrane, M.A. 2013. The responses of leaf litter ant communities to wildfires in the Brazilian Amazon: a multi-region assessment. Biodivers. Conserv. 22(2):513-529.

Simkanin, C., Dower, J.F., Filip, N., Jamieson, G., and Therriault, T.W. 2013. Biotic resistance to the infiltration of natural benthic habitats: examining the role of predation in the distribution of the invasive ascidian Botrylloides violaceus. J. Exp. Marine Biol. Ecol. 439:76-83.

Sindt, A.R., Quist, M.C., and Pierce, C.L. 2012. Habitat associations of fish species of greatest conservation need at multiple spatial scales in wadeable Iowa streams. North Am. J. Fish. Manag. 32(6):1046-1061.

Sliwinski, M.S., and Koper, N. 2012. Grassland bird responses to three edge types in a fragmented mixed-grass prairie. Avian Conserv. Ecol. 7(2):6.

Soga, M., and Koike, S. 2013. Mapping the potential extinction debt of butterflies in a modern city: implications for conservation priorities in urban landscapes. Anim. Conserv. 16(1):1-11.

Soga, M., Yamaura, Y., and Koike, S. 2013. From ecological pessimism to conservation chance: reviving living dead in changing landscapes. Anim. Conserv. 16(1):16-18.

Solefack, M.C.M., Chabrerie, O., Gallet-Moron, E., Nkongmeneck, B.A., Leumbe, O.N.L., and Decocq, G. 2012. Analysing deforestation by remote sensing coupled with structural equation models: example of the cloud forest of mount Oku (Cameroon). Acta Bot. Gallica 159(4):451-466.

Somaweera, R., Shine, R., Webb, J., Dempster, T., and Letnic, M. 2013. Why does vulnerability to toxic invasive cane toads vary among populations of Australian freshwater crocodiles? Anim. Conserv. 16(1):86-96.

Soomers, H., Karssenberg, D., Verhoeven, J.T.A., Verweij, P.A., and Wassen, M.J. 2013. The effect of habitat fragmentation and abiotic factors on fen plant occurrence. Biodivers. Conserv. 22(2):405-424.

Sorte, C.J.B., Ibáñez, I., Blumenthal, D.M., Molinari, N.A., Miller, L.P., Grosholz, E.D., Diez, J.M., D'Antonio, C.M., Olden, J.D., Jones, S.J., and Dukes, J.S. 2013. Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol. Lett. 16(2):261-270.

Stamper, T.J., Hicke, J.A., Jennings, M., and Aycrigg, J. 2013. Spatial and temporal patterns of changes in protected areas across the Southwestern United States. Biodivers. Conserv. 22(2):343-356.

Steen, D.A., Conner, L.M., Smith, L.L., Provencher, L., Hiers, J.K., Pokswinski, S., Helms, B.S., and Guyer, C. 2013. Bird assemblage response to restoration of fire-suppressed longleaf pine sandhills. Ecol. Appl. 23(1):134-147.

Stockwell, C.A., Heilveil, J.S., and Purcell, K. 2013. Estimating divergence time for two evolutionarily significant units of a protected fish species. Conserv. Genet. 14(1):215-222.

Stucki, D.S., Rodhouse, T.J., Lyon, J.W., and Garrett, L.K. 2013. Natural resource conservation in a cultural park: evaluating the importance of Big Hole National Battlefield to the endemic Lemhi penstemon (Penstemon lemhiensis). Nat. Areas J. 33(1):50-58.

Studeny, A.C., Buckland, S.T., Harrison, P.J., Illian, J.B., Magurran, A.E., and Newson, S.E. 2013. Fine-tuning the assessment of large-scale temporal trends in biodiversity using the example of British breeding birds. J. Appl. Ecol. 50(1):190-198.

Sullivan, B.K., and Sullivan, K.O. 2012. Common chuckwalla (Sauromalus ater) in an urban preserve: persistence of a small population and estimation of longevity. Herpetol. Conserv. Biol. 7(3):437-441.

Sun, J., and Southworth, J. 2013. Remote sensing-based fractal analysis and scale dependence associated with forest fragmentation in an Amazon tri-national frontier. Remote Sens. 5(2):454-472.

Sushinsky, J.R., Rhodes, J.R., Possingham, H.P., Gill, T.K., and Fuller, R.A. 2013. How should we grow cities to minimize their biodiversity impacts? Global Change Biol. 19(2):401-410.

Swanepoel, L.H., Lindsey, P., Somers, M.J., van Hoven, W., and Dalerum, F. 2013. Extent and fragmentation of suitable leopard habitat in South Africa. Anim. Conserv. 16(1):41-50.

Tabeni, S., Spirito, F., and Ojeda, R.A. 2013. Conservation of small and medium-sized mammals following native woodland regrowth: a case study in a long-term UNESCO Biosphere Reserve, Argentina. J. Arid Environ. 88:250-253.

Tan, D.T., Thu, P.Q., and Dell, B. 2012. Invasive plant species in the national parks of Vietnam. Forests 3(4):997-1016.

Tanentzap, A.J., Lee, W.G., and Monks, A. 2013. Increased nitrogen cycling facilitates native forest regeneration: potential for restoring extinct ecological processes? Ecol. Appl. 23(1):36-45.

Tantipisanuh, N., and Gale, G.A. 2013. Representation of threatened vertebrates by a protected area system in Southeast Asia: the importance of non-forest habitats. Raffles Bull. Zool. 61(1):359-395.

Thaulow, J., Borgstrom, R., and Heun, M. 2013. Brown trout population structure highly affected by multiple stocking and river diversion in a high mountain national park. Conserv. Genet. 14(1):145-158.

Thaxter, C.B., Lascelles, B., Sugar, K., Cook, A.S.C.P., Roos, S., Bolton, M., Langston, R.H.W., and Burton, N.H.K. 2012. Seabird foraging ranges as a preliminary tool for identifying candidate Marine Protected Areas. Biol. Conserv. 156:53-61.

Thiem, J.D., Broadhurst, B.T., Lintermans, M., Ebner, B.C., Clear, R.C., and Wright, D. 2013. Seasonal differences in the diel movements of Macquarie perch (Macquaria australasica) in an upland reservoir. Ecol. Freshw. Fish 22(1):145-156.

Tingley, R., Phillips, B.L., Letnic, M., Brown, G.P., Shine, R., and Baird, S.J.E. 2013. Identifying optimal barriers to halt the invasion of cane toads Rhinella marina in arid Australia. J. Appl. Ecol. 50(1):129-137.

Tocco, C., Negro, M., Rolando, A., and Palestrini, C. 2013. Does natural reforestation represent a potential threat to dung beetle diversity in the Alps? J. Insect Conserv. 17(1):207-217.

Torma, A., and Császár, P. 2013. Species richness and composition patterns across trophic levels of true bugs (Heteroptera) in the agricultural landscape of the lower reach of the Tisza River Basin. J. Insect Conserv. 17(1):35-51.

Torretta, J.P., and Poggio, S.L. 2013. Species diversity of entomophilous plants and flower-visiting insects is sustained in the field margins of sunflower crops. J. Nat. Hist. 47(3-4):139-165.

Touroult, J., and Le Gall, P. 2013. Fruit feeding Cetoniinae community structure in an anthropogenic landscape in West Africa. J. Insect Conserv. 17(1):23-34.

Tscheulin, T., and Petanidou, T. 2013. The presence of the invasive plant Solanum elaeagnifolium deters honeybees and increases pollen limitation in the native co-flowering species Glaucium flavum. Biol. Invasions 15(2):385-393.

Unfried, T.M., Hauser, L., and Marzluff, J.M. 2013. Effects of urbanization on Song Sparrow (Melospiza melodia) population connectivity. Conserv. Genet. 14(1):41-53.

Valderrama, S.V., Molles, L.E., and Waas, J.R. 2013. Effects of population size on singing behavior of a rare duetting songbird. Conserv. Biol. 27(1):210-218.

van der Grift, E.A., van der Ree, R., Fahrig, L., Findlay, S., Houlahan, J., Jaeger, J.A.G., Klar, N., Madriñan, L.F., and Olson, L. 2013. Evaluating the effectiveness of road mitigation measures. Biodivers. Conserv. 22(2):425-448.

van der Hoek, Y., Renfrew, R., and Manne, L.L. 2013. Assessing regional and interspecific variation in threshold responses of forest breeding birds through broad scale analyses. PLoS ONE 8(2):e55996.

Van der Hoop, J.M., Moore, M.J., Barco, S.G., Cole, T.V.N., Daoust, P.Y., Henry, A.G., McAlpine, D.F., McLellan, W.A., Wimmer, T., and Solow, A.R. 2013. Assessment of management to mitigate anthropogenic effects on large whales. Conserv. Biol. 27(1):121-133.

van der Walt, J., Nel, L.H., and Hoelzel, A.R. 2013. Differentiation at mitochondrial and nuclear loci between the blesbok (Damaliscus pygargus phillipsi) and bontebok (D.p. pygargus): implications for conservation strategy. Conserv. Genet. 14(1):243-248.

Vargas-Salinas, F., and Lopez-Aranda, F. 2012. Could roads restraint the movement of small mammals in Andean forests of Colombia? Study case in the bosque de Yotoco, Valle del Cauca. Caldasia 34(2):409-420.

Vasconcelos, H.L., and Bruna, E.M. 2012. Arthropod responses to the experimental isolation of Amazonian forest fragments. Zoologia 29(6):515-530.

Vaz-Pinto, F., Olabarria, C., and Arenas, F. 2013. Role of top-down and bottom-up forces on the invasibility of intertidal macroalgal assemblages. J. Sea Res. 76:178-186.

Vellend, M., and Kharouba, H.M. 2013. Setting conservation priorities when what you see is not what you get. Anim. Conserv. 16(1):14-15.

Venturas, M., Fuentes-Utrilla, P., Ennos, R., Collada, C., and Gil, L. 2013. Human-induced changes on fine-scale genetic structure in Ulmus laevis Pallas wetland forests at its SW distribution limit. Plant Ecol. 214(2):317-327.

Verlinden, M., Van Kerkhove, A., and Nijs, I. 2013. Effects of experimental climate warming and associated soil drought on the competition between three highly invasive West European alien plant species and native counterparts. Plant Ecol. 214(2):243-254.

Villalobos, F., Dobrovolski, R., Provete, D.B., and Gouveia, S.F. 2013. Is rich and rare the common share? Describing biodiversity patterns to inform conservation practices for South American anurans. PLoS ONE 8(2):e56073.

Virkkala, R., Heikkinen, R.K., Fronzek, S., Kujala, H., and Leikola, N. 2013. Does the protected area network preserve bird species of conservation concern in a rapidly changing climate? Biodivers. Conserv. 22(2):459-482.

Von Holle, B. 2013. Environmental stress alters native-nonnative relationships at the community scale. Biol. Invasions 15(2):417-427.

Wagner, C.M., and Grossman, G.D. 2013. Input matching and patch use by native and invasive minnows. Ecol. Freshw. Fish 22(1):55-65.

Waibel, A., Griffiths, C.J., Zuel, N., Schmid, B., and Albrecht, M. 2013. Does a giant tortoise taxon substitute enhance seed germination of exotic fleshy-fruited plants? J. Plant Ecol. 6(1):57-63.

Walker, R., Arima, E., Messina, J., Soares, B., Perz, S., Vergara, D., Sales, M., Pereira, R., and Castro, W. 2013. Modeling spatial decisions with graph theory: logging roads and forest fragmentation in the Brazilian Amazon. Ecol. Appl. 23(1):239-254.

Walker, R.C.J., and Rafeliarisoa, T.H. 2012. Distribution of radiated tortoise (Astrochelys radiata) bush meat poaching effort. Chelonian Conserv. Biol. 11(2):223-226.

Walzer, C., Kowalczyk, C., Alexander, J.M., Baur, B., Bogliani, G., Brun, J.J., Füreder, L., Guth, M.O., Haller, R., Holderegger, R., Kohler, Y., Kueffer, C., Righetti, A., Spaar, R., Sutherland, W.J., Ullrich-Schneider, A., Vanpeene-Bruhier, S.N., and Scheurer, T. 2013. The 50 most important questions relating to the maintenance and restoration of an ecological continuum in the European Alps. PLoS ONE 8(1):e53139.

Wang, W., Pechacek, P., Zhang, M.X., Xiao, N.W., Zhu, J.G., and Li, J.S. 2013. Effectiveness of nature reserve system for conserving tropical forests: a statistical evaluation of Hainan Island, China. PLoS ONE 8(2):e57561.

Wang, Z.H., Fang, J.Y., Tang, Z.Y., and Lin, X. 2012. Relative role of contemporary environment versus history in shaping diversity patterns of China's woody plants. Ecography 35(12):1124-1133.

Wedekind, C., Evanno, G., Székely, T., Pompini, M., Darbellay, O., and Guthruf, J. 2013. Persistent unequal sex ratio in a population of grayling (Salmonidae) and possible role of temperature increase. Conserv. Biol. 27(1):229-234.

Weinbaum, K.Z., Brashares, J.S., Golden, C.D., and Getz, W.M. 2013. Searching for sustainability: are assessments of wildlife harvests behind the times? Ecol. Lett. 16(1):99-111.

Whitall, D., Mason, A., and Pait, A. 2012. Nutrient dynamics in coastal lagoons and marine waters of Vieques, Puerto Rico. Trop. Conserv. Sci. 5(4):495-509.

Wilson, J.N., Bekessy, S., Parris, K.M., Gordon, A., Heard, G.W., and Wintle, B.A. 2013. Impacts of climate change and urban development on the spotted marsh frog (Limnodynastes tasmaniensis). Austral Ecol. 38(1):11-22.

Womble, J.N., and Gende, S.M. 2013. Post-breeding season migrations of a top predator, the harbor seal (Phoca vitulina richardii), from a marine protected area in Alaska. PLoS ONE 8(2):e55386.

Worm, B., and Branch, T.A. 2012. The future of fish. Trends Ecol. Evol. 27(11):594-599.

Wunder, J.L., Lampazzi, N.M., Acre, K.D., Bent, N.J., Canter, S.A., Chapman, A.M., Davies, M.A., Kashan, D., Keiley, J.W., Macintyre, R.I., Milton, T.F., Weichler, K.L., Wilson, M.J., and Takahashi, M.K. 2012. Promoting amphibian conservation through the college classroom: detection of Batrachochytrium dendrobatidis among local amphibians. Herpetol. Conserv. Biol. 7(3):462-469.

Xie, W.J., and Gao, S. 2013. Invasive Spartina alterniflora-induced factors affecting epibenthos distribution in coastal salt marsh, China. Acta Oceanologica Sinica 32(2):81-88.

Xin, K., Zhou, Q., Arndt, S.K., and Yang, X. 2013. Invasive capacity of the mangrove Sonneratia apetala in Hainan Island, China. J. Trop. For. Sci. 25(1):70-78.

Yacelga, M., Cayot, L.J., and Jaramillo, A. 2012. Dispersal of neonatal Galápagos marine iguanas Amblyrhynchus cristatus from their nesting zone: natural history and conservation implications. Herpetol. Conserv. Biol. 7(3):470-480.

Zachos, F.E. 2013. Species splitting puts conservation at risk. Nature 494(7435):35.

Zepeda-Martínez, V., Mandujano, M.C., Mandujano, F.J., and Golubov, J.K. 2013. What can the demography of Astrophytum ornatum tell us of its endangered status? J. Arid Environ. 88:244-249.

Zhang, L., Liu, J.Z., Wang, D.J., Schaller, G.B., Wu, Y.L., Harris, R.B., Zhang, K.J., and Lu, Z. 2013. Distribution and population status of Przewalski's gazelle, Procapra przewalskii (Cetartiodactyla, Bovidae). Mammalia 77(1):31-40.

Zhang, W., Fan, X.H., Zhu, S.F., Zhao, H., and Fu, L.Z. 2013. Species-specific identification from incomplete sampling: applying DNA barcodes to monitoring invasive Solanum plants. PLoS ONE 8(2):e55927.

Żmihorski, M., Dziarska-Pałac, J., Sparks, T.H., and Tryjanowski, P. 2013. Ecological correlates of the popularity of birds and butterflies in Internet information resources. Oikos 122(2):183-190.

Zylberberg, M., Lee, K.A., Klasing, K.C., and Wikelski, M. 2013. Variation with land use of immune function and prevalence of avian pox in Galapagos finches. Conserv. Biol. 27(1):103-112.

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