Ecotypic differentiation of mid-Atlantic Quercus species in response to ultramafic soils
Jerry Burgess A E , Katalin Szlavecz A , Nishanta Rajakaruna B C and Christopher Swan D
+ Author Affiliations
- Author Affiliations
A Department of Earth and Planetary Sciences, Johns Hopkins University, Baltimore, MD 21218, USA.
B College of the Atlantic, 105 Eden Street, Bar Harbor, ME 04609, USA.
C Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa.
D Department of Geography & Environmental Systems, University of Maryland, Baltimore County, Baltimore, MD 21250, USA.
E Corresponding author. Email: jerry.burgess@jhu.edu
Australian Journal of Botany 63(4) 308-323 https://doi.org/10.1071/BT14274
Submitted: 16 October 2014 Accepted: 24 March 2015 Published: 8 May 2015
Abstract
Spatial heterogeneity of soil conditions combined with intraspecific variation confer site-specific edaphic tolerance, resulting in local adaptation and speciation. To understand the geoecological processes controlling community assembly of woodland tree species on serpentine and mafic soils, we investigated resource gradients and provenance (geographic area of propagule collection) as variables affecting typical representative upland oak (Quercus) species distribution. Accordingly, we conducted a year-long reciprocal transplant experiment in the greenhouse with serpentine and mafic soils, using seedlings of five oak species (Quercus marilandica, Q. stellata, Q. montana, Q. michauxii and Q. alba). All seedlings, regardless of provenance or soil depth, displayed more robust growth in the mafic soils. Soil depth was an important determinant, with all species exhibiting increased growth in the deeper-soil treatments. Fitness surrogates such as stem height, relative growth rate, and leaves per plant were greater when seedlings were grown in their home soil than when they were grown in the non-resident soil, suggesting an ecotypic effect. Mean stomatal conductance and stem growth were positively correlated with soil depth in all treatments. Taken together, the study showed provenance-specific growth responses of oak seedlings to soil type and depth, providing a better understanding of the mechanisms controlling species assembly in woodland communities.
Additional keywords: edaphic, intra-specific variation, local adaptation, reciprocal transplant, seedling growth, serpentine.
References
Abrahamson WG (1979) A comment on vegetative and seed reproduction in plants. Evolution 33, 517–519.| A comment on vegetative and seed reproduction in plants.Crossref | GoogleScholarGoogle Scholar |
Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiology 7, 227–238.
| Adaptations and responses to drought in Quercus species of North America.Crossref | GoogleScholarGoogle Scholar | 14972920PubMed |
Abrams MD (2003) Where has all the white oak gone? Bioscience 53, 927–939.
| Where has all the white oak gone?Crossref | GoogleScholarGoogle Scholar |
Ågren J, Schemske DW (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytologist 194, 1112–1122.
| Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range.Crossref | GoogleScholarGoogle Scholar | 22432639PubMed |
Anacker BL (2014) The nature of serpentine endemism. American Journal of Botany 101, 219–224.
| The nature of serpentine endemism.Crossref | GoogleScholarGoogle Scholar | 24509800PubMed |
Anacker B, Rajakaruna N, Ackerly D, Harrison S, Keeley J, Vasey M (2011) Ecological strategies in California chaparral: interacting effects of soils, climate, and fire on specific leaf area. Plant Ecology & Diversity 4, 179–188.
| Ecological strategies in California chaparral: interacting effects of soils, climate, and fire on specific leaf area.Crossref | GoogleScholarGoogle Scholar |
Balok CA, Hilaire RS (2002) Drought responses among seven southwestern landscape tree taxa. Journal of the American Society for Horticultural Science 127, 211–218.
Barton A, Wallenstein M (1997) Effects of invasion of Pinus virginiana on soil properties in serpentine barrens in southeastern Pennsylvania. The Journal of the Torrey Botanical Society 124, 297–305.
| Effects of invasion of Pinus virginiana on soil properties in serpentine barrens in southeastern Pennsylvania.Crossref | GoogleScholarGoogle Scholar |
Baythavong BS, Stanton ML (2010) Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity. Evolution 64, 2904–2920.
Bereczki K, Ódor P, Csóka G, Mag Z, Báldi A (2014) Effects of forest heterogeneity on the efficiency of caterpillar control service provided by birds in temperate oak forests. Forest Ecology and Management 327, 96–105.
| Effects of forest heterogeneity on the efficiency of caterpillar control service provided by birds in temperate oak forests.Crossref | GoogleScholarGoogle Scholar |
Beuker E (1994) Long‐term effects of temperature on the wood production of Pinus sylvestris L. and Picea abies (L.) Karst. In old provenance experiments. Scandinavian Journal of Forest Research 9, 34–45.
| Long‐term effects of temperature on the wood production of Pinus sylvestris L. and Picea abies (L.) Karst. In old provenance experiments.Crossref | GoogleScholarGoogle Scholar |
Bieger A, Rajakaruna N, Harrison S (2014) Little evidence for local adaptation to soils or microclimate in the post-fire recruitment of three Californian shrubs. Plant Ecology & Diversity 7, 411–420.
| Little evidence for local adaptation to soils or microclimate in the post-fire recruitment of three Californian shrubs.Crossref | GoogleScholarGoogle Scholar |
Boyd RS, Martens SN (1998) The significance of metal hyperaccumulation for biotic interactions. Chemoecology 8, 1–7.
| The significance of metal hyperaccumulation for biotic interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVOjsLw%3D&md5=a478df99f35e1ca551d1ec1f4c03f643CAS |
Branco S (2009) Are oaks locally adapted to serpentine soils? Northeastern Naturalist 16, 329–340.
| Are oaks locally adapted to serpentine soils?Crossref | GoogleScholarGoogle Scholar |
Burgess JL (2013) Geologic and edaphic controls on serpentine vegetation dynamics. Thesis Dissertation, Johns Hopkins University, Baltimore, MD, USA.
Burgess JL, Szlavecz K, Rajakaruna N, Lev S, Swan CM (2015) Vegetation dynamics and mesophication in response to conifer encroachment within an ultramafic system. Australian Journal of Botany 63, 292–307.
| Vegetation dynamics and mesophication in response to conifer encroachment within an ultramafic system.Crossref | GoogleScholarGoogle Scholar |
Carter KK (1996) Provenance tests as indicators of growth response to climate change in 10 north temperate tree species. Canadian Journal of Forest Research 26, 1089–1095.
| Provenance tests as indicators of growth response to climate change in 10 north temperate tree species.Crossref | GoogleScholarGoogle Scholar |
Clausen J, Keck DD, Hiesey WM (1940) ‘Experimental studies on the nature of species. I. Effect of varied environment on western North American plants.’ (USA Carnegie Institution of Washington: Washington, DC)
Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In ‘Advances in photosynthesis and respiration’. (Ed. N Baker) pp. 347–366. (Springer: Dordrecht, The Netherlands)
Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecological Monographs 79, 109–126.
| Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California.Crossref | GoogleScholarGoogle Scholar |
Darwin C (1859) ‘On the origins of species by means of natural selection.’ (Murray: London)
Davies KF, Harrison S, Safford HD, Viers JH (2007) Productivity alters the scale dependence of the diversity–invasibility relationship. Ecology 88, 1940–1947.
| Productivity alters the scale dependence of the diversity–invasibility relationship.Crossref | GoogleScholarGoogle Scholar | 17824424PubMed |
Dickson RE, Tomlinson PT (1996) Oak growth, development and carbon metabolism in response to water stress. Annales des Sciences Forestieres 53, 181–196.
| Oak growth, development and carbon metabolism in response to water stress.Crossref | GoogleScholarGoogle Scholar |
Dyer JM (2001) Using witness trees to assess forest change in southeastern Ohio. Canadian Journal of Forest Research 31, 1708–1718.
| Using witness trees to assess forest change in southeastern Ohio.Crossref | GoogleScholarGoogle Scholar |
Ellison AM, Bank MS, Clinton BD (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3, 479–486.
| Loss of foundation species: consequences for the structure and dynamics of forested ecosystems.Crossref | GoogleScholarGoogle Scholar |
Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends in Ecology & Evolution 17, 177–183.
| Spatial soil ecology.Crossref | GoogleScholarGoogle Scholar |
Evans GC (1972) ‘The quantitative analysis of plant growth.’ (University of California Press: Oakland, CA)
Fralish JS (2004) The keystone role of oak and hickory in the central hardwood forest. Proceedings of the upland oak ecology symposium: history, current conditions, and sustainability. General Technical Report SRS-73, USDA Forest Service Southern Research Station, Asheville, NC.
Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. International Journal of Plant Sciences 164, S21–S42.
| Inheritance and natural selection on functional traits.Crossref | GoogleScholarGoogle Scholar |
Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends in Microbiology 20, 131–138.
| Emergence of the sudden oak death pathogen Phytophthora ramorum.Crossref | GoogleScholarGoogle Scholar | 22326131PubMed |
Gupta UC, Solanki HA (2013) Impact of boron deficiency on plant growth. International Journal of Bioassays 2, 1048–1050.
Harrison SP, Rajakaruna N (2011) What have we learned from serpentine about evolution, ecology, and other sciences. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 417–427. (University of California Press: Berkeley, CA)
Harrison S, Safford HD, Grace JB, Viers JH, Davies KF (2006) Regional and local species richness in an insular environment: serpentine plants in California. Ecological Monographs 76, 41–56.
| Regional and local species richness in an insular environment: serpentine plants in California.Crossref | GoogleScholarGoogle Scholar |
Hawrylak-Nowak B, Kalinowska M, Szymanska M (2012) A study on selected physiological parameters of plants grown under lithium supplementation. Biological Trace Element Research 149, 425–430.
| A study on selected physiological parameters of plants grown under lithium supplementation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs12ltrnI&md5=4d2bcdf71dff57f40debcd771b243158CAS | 22576984PubMed |
Heikinheimo O (1949) Tuloksia kuusen ja männyn maantieteellisillä roduilla suoritetuista kokeista. Communicationes Instituti Forestalis Fenniae 37, 1–44.
Hendrix PF, Parmelee RW, Crossley DA, Coleman DC, Odum EP, Groffman PM (1986) Detritus food webs in conventional and no-tillage agroecosystems. Bioscience 36, 374–380.
| Detritus food webs in conventional and no-tillage agroecosystems.Crossref | GoogleScholarGoogle Scholar |
Hereford J, Winn AA (2008) Limits to local adaptation in six populations of the annual plant Diodia teres. New Phytologist 178, 888–896.
| Limits to local adaptation in six populations of the annual plant Diodia teres.Crossref | GoogleScholarGoogle Scholar | 18384510PubMed |
Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610–617.
| How do plants respond to nutrient shortage by biomass allocation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eqtbzE&md5=0a63c69e653892dd348e7e474c8a5d62CAS | 17092760PubMed |
Högberg MN, Chen Y, Högberg P (2007) Gross nitrogen mineralisation and fungi-to-bacteria ratios are negatively correlated in boreal forests. Biology and Fertility of Soils 44, 363–366.
| Gross nitrogen mineralisation and fungi-to-bacteria ratios are negatively correlated in boreal forests.Crossref | GoogleScholarGoogle Scholar |
Hunt R (1990) ‘Basic growth analysis.’ (Unwin Hyman: Dordrecht, The Netherlands)
Ingham ER, Klein DA (1982) Relationship between fluorescein diacetate-stained hyphae and oxygen utilization, glucose utilization, and biomass of submerged fungal batch cultures. Applied and Environmental Microbiology 44, 363–370.
Ingham ER, Coleman DC, Moore JC (1989) An analysis of food-web structure and function in a shortgrass prairie, a mountain meadow, and a lodgepole pine forest. Biology and Fertility of Soils 8, 29–37.
| An analysis of food-web structure and function in a shortgrass prairie, a mountain meadow, and a lodgepole pine forest.Crossref | GoogleScholarGoogle Scholar |
Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology & Biochemistry 40, 2977–2991.
| Quantitative assessment of the fungal contribution to microbial tissue in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGgsLvF&md5=433cb19064d6679051e9c465c2ecbb41CAS |
Johnson KD, Scatena FN, Johnson AH, Pan Y (2009) Controls on soil organic matter content within a northern hardwood forest. Geoderma 148, 346–356.
| Controls on soil organic matter content within a northern hardwood forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1Cl&md5=1f507757cf519576e29c82b09fa61ea1CAS |
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters 7, 1225–1241.
| Conceptual issues in local adaptation.Crossref | GoogleScholarGoogle Scholar |
Kay KM, Ward KL, Watt LR (2011) Plant speciation. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 71–96. (University of California Press: Berkeley, CA)
Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biological Reviews of the Cambridge Philosophical Society 83, 495–508.
Kolb TE, Steiner KC, McCormick LH, Bowersox TW (1990) Growth response of northern red-oak and yellow-poplar seedlings to light, soil moisture and nutrients in relation to ecological strategy. Forest Ecology and Management 38, 65–78.
| Growth response of northern red-oak and yellow-poplar seedlings to light, soil moisture and nutrients in relation to ecological strategy.Crossref | GoogleScholarGoogle Scholar |
Kruckeberg AR (1986) An essay: the stimulus of unusual geologies for plant speciation. Systematic Botany 11, 455–463.
| An essay: the stimulus of unusual geologies for plant speciation.Crossref | GoogleScholarGoogle Scholar |
Lechowicz MJ, Bell G (1991) The ecology and genetics of fitness in forest plants. II. Microspatial heterogeneity of the edaphic environment. Journal of Ecology 79, 687–696.
| The ecology and genetics of fitness in forest plants. II. Microspatial heterogeneity of the edaphic environment.Crossref | GoogleScholarGoogle Scholar |
Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3, e4010
| A meta-analysis of local adaptation in plants.Crossref | GoogleScholarGoogle Scholar | 19104660PubMed |
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27, 237–277.
| Evolutionary significance of local genetic differentiation in plants.Crossref | GoogleScholarGoogle Scholar |
Loach K (1970) Shade tolerance in tree seedlings. New Phytologist 69, 273–286.
| Shade tolerance in tree seedlings.Crossref | GoogleScholarGoogle Scholar |
Loats KV, Rebbeck J (1999) Interactive effects of ozone and elevated carbon dioxide on the growth and physiology of black cherry, green ash, and yellow-poplar seedlings. Environmental Pollution 106, 237–248.
| Interactive effects of ozone and elevated carbon dioxide on the growth and physiology of black cherry, green ash, and yellow-poplar seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yrtL8%3D&md5=ed7bac742b5d654e4750a2b9b13ec6f8CAS | 15093051PubMed |
Lorimer CG (1993) Causes of the oak regeneration problem. Oak regeneration: serious problems, practical recommendations. USDA Forest Service general technical report SE-84, Southeastern Forest Experiment Station, Asheville, NC.
McEwan RW, Dyer JM, Pederson N (2011) Multiple interacting ecosystem drivers: toward an encompassing hypothesis of oak forest dynamics across eastern North America. Ecography 34, 244–256.
| Multiple interacting ecosystem drivers: toward an encompassing hypothesis of oak forest dynamics across eastern North America.Crossref | GoogleScholarGoogle Scholar |
McShea WJ, Healy WM, Devers P, Fearer T, Koch FH, Stauffer D, Waldon J (2007) Forestry matters: decline of oaks will impact wildlife in hardwood forests. The Journal of Wildlife Management 71, 1717–1728.
| Forestry matters: decline of oaks will impact wildlife in hardwood forests.Crossref | GoogleScholarGoogle Scholar |
Moore KA, Elmendorf SC (2011) Plant competition and facilitation in systems with strong environmental gradients. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 223–236. (University of California Press: Berkeley, CA)
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends in Ecology & Evolution 13, 403–407.
| The adaptive significance of maternal effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itF2rtg%3D%3D&md5=e8adc4bf6e28f4ebca02a1b6f8893d86CAS |
Nowacki GJ, Abrams MD (1992) Community, edaphic, and historical analysis of mixed oak forests of the Ridge and Valley Province in central Pennsylvania. Canadian Journal of Forest Research 22, 790–800.
| Community, edaphic, and historical analysis of mixed oak forests of the Ridge and Valley Province in central Pennsylvania.Crossref | GoogleScholarGoogle Scholar |
O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 97–137. (University of California Press: Berkeley, CA)
O’Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca : Mg than in tolerance of low N, low P, or heavy metals. Plant and Soil 280, 49–64.
| Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca : Mg than in tolerance of low N, low P, or heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslOrsbw%3D&md5=98a556cf2d87fd35cb1bc526548cf13eCAS |
Pallardy SG, Rhoads JL (1993) Morphological adaptations to drought in seedlings of deciduous angiosperms. Canadian Journal of Forest Research 23, 1766–1774.
| Morphological adaptations to drought in seedlings of deciduous angiosperms.Crossref | GoogleScholarGoogle Scholar |
Rajakaruna N (2004) The edaphic factor in the origin of plant species. International Geology Review 46, 471–478.
| The edaphic factor in the origin of plant species.Crossref | GoogleScholarGoogle Scholar |
Rajakaruna N, Bradfield GE, Bohm BA, Whitton J (2003) Adaptive differentiation in response to water stress by edaphic races of Lasthenia californica (Asteraceae). International Journal of Plant Sciences 164, 371–376.
| Adaptive differentiation in response to water stress by edaphic races of Lasthenia californica (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
R Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at: http://www.R-project.org/
Rehfeldt GE, Ying CC, Spittlehouse DL, Jr DAH (1999) Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecological Monographs 69, 375–407.
| Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation.Crossref | GoogleScholarGoogle Scholar |
Rehfeldt GE, Tchebakova NM, Parfenova YI, Wykoff WR, Kuzmina NA, Milyutin LI (2002) Intraspecific responses to climate in Pinus sylvestris. Global Change Biology 8, 912–929.
| Intraspecific responses to climate in Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar |
Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164, S143–S164.
| The evolution of plant functional variation: traits, spectra, and strategies.Crossref | GoogleScholarGoogle Scholar |
Rice KJ, Mack RN (1991) Ecological genetics of Bromus tectorum. Oecologia 88, 91–101.
| Ecological genetics of Bromus tectorum.Crossref | GoogleScholarGoogle Scholar |
Römheld V, Marschner H (1991) Function of micronutrients in plants. In ‘Micronutrients in agriculture’. 2nd edn. SSSA Book Series, No. 4. (Eds JJ Mordvedt, FR Cox, LM Shuman, RM Welch) pp. 297–328. (SSSA: Madison, WI)
Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and Environmental Microbiology 75, 1589–1596.
| Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFKgsLo%3D&md5=0173ea3381dd82e93223885e7996711bCAS | 19151179PubMed |
Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annual Review of Ecology Evolution and Systematics 38, 595–619.
| Gene flow and local adaptation in trees.Crossref | GoogleScholarGoogle Scholar |
Schedlbauer JL, Pistoia VL (2013) Water relations of an encroaching vine and two dominant C4 grasses in the serpentine barrens of southeastern Pennsylvania 1. The Journal of the Torrey Botanical Society 140, 493–505.
| Water relations of an encroaching vine and two dominant C4 grasses in the serpentine barrens of southeastern Pennsylvania 1.Crossref | GoogleScholarGoogle Scholar |
Schluter D (2009) Evidence for ecological speciation and its alternative. Science 323, 737–741.
| Evidence for ecological speciation and its alternative.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlert78%3D&md5=3e241f145cfed9ff6724b7eb79d20736CAS | 19197053PubMed |
Selmants PC, Zavaleta ES, Pasari JR, Hernandez DL (2012) Realistic plant species losses reduce invasion resistance in a California serpentine grassland. Journal of Ecology 100, 723–731.
| Realistic plant species losses reduce invasion resistance in a California serpentine grassland.Crossref | GoogleScholarGoogle Scholar |
Shaw JN, West LT, Hajek BF (2001) Ca–Mg ratios for evaluating pedogenesis in the piedmont province of the southeastern United States of America. Canadian Journal of Soil Science 81, 415–421.
| Ca–Mg ratios for evaluating pedogenesis in the piedmont province of the southeastern United States of America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotlGhtLk%3D&md5=fde6beb6fa3857a4dbc66adcb0e7d972CAS |
Shutyaev AM, Giertych M (2000) Genetic subdivisions of the range of Scots pine (Pinus sylvestris L.) based on a transcontinental provenance experiment. Silvae Genetica 49, 137–151.
Siegwart Collier LCS, Mallik AU (2010) Does post-fire abiotic habitat filtering create divergent plant communities in black spruce forests of eastern Canada? Oecologia 164, 465–477.
| Does post-fire abiotic habitat filtering create divergent plant communities in black spruce forests of eastern Canada?Crossref | GoogleScholarGoogle Scholar |
Tyndall RW (1992) Historical considerations of conifer expansion in Maryland serpentine’ barrens’. Castanea 57, 123–131.
van der Putten WH, de Ruiter PC, Bezemer TM, Harvey JA, Wassen M, Wolters V (2004) Trophic interactions in a changing world. Basic and Applied Ecology 5, 487–494.
| Trophic interactions in a changing world.Crossref | GoogleScholarGoogle Scholar |
Vithanage M, Rajapaksha A, Oze C, Rajakaruna N, Dissanayake CB (2014) Metal release from serpentine soils in Sri Lanka. Environmental Monitoring and Assessment 186, 3415–3429.
| Metal release from serpentine soils in Sri Lanka.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht12jsL0%3D&md5=6fdc44a6057a8a0746022f272fe8038bCAS | 24464398PubMed |
Walker BH, Noy-Meir I (1982) Aspects of the stability and resilience of savanna ecosystems. In ‘Aspects of the stability and resilience of savanna ecosystems’. (Eds BJ Huntley and BH Walker) pp. 556–590. (Springer-Verlag: Berlin)
Walter H, Mueller-Dombois D (1971) ‘Ecology of tropical and subtropical vegetation.’ (Oliver & Boyd: Edinburgh, UK)
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.
| Ecological linkages between aboveground and belowground biota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Cgsrs%3D&md5=cb76cfdd6e120edc93896eae7f1fe220CAS | 15192218PubMed |
Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Annals of Botany 37, 629–672.
Whittaker RH (1954) The ecology of serpentine soils. Ecology 35, 258–288.
| The ecology of serpentine soils.Crossref | GoogleScholarGoogle Scholar |
Wright JW (2007) Local adaptation to serpentine soils in Pinus ponderosa. Plant and Soil 293, 209–217.
| Local adaptation to serpentine soils in Pinus ponderosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaktb0%3D&md5=80039d41d9ef39cb30dfba1fa4b2fcd1CAS |
Wright JW, Stanton ML (2011) Local adaptation in heterogeneous landscapes. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 155–179. (University of California Press: Berkeley, CA)
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany 76, 167–179.
| Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsFOksbk%3D&md5=0e3db153222012e0071cd622ac1e28a8CAS |
Yost JM, Barry T, Kay KM, Rajakaruna N (2012) Edaphic adaptation maintains the coexistence of two cryptic species on serpentine soils. American Journal of Botany 99, 890–897.
| Edaphic adaptation maintains the coexistence of two cryptic species on serpentine soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsFKkurg%3D&md5=df6abc174337008f436f1a86840d206dCAS | 22539516PubMed |
