Holocene invasions: finally the resolution ecologists were waiting for!

NEWS & COMMENT References 1 Hammond, P.M. (1992) Species inventory, in Global Diversity: Status of the Earth’s Living Resources (Groombridge, B., ed.), pp. 17–39, Chapman & Hall 2 Wake, D.B. (1996) A new species of Batrachoseps (Amphibia: Plethodontidae) from the San Gabriel Mountains, southern California, Contrib. Sci. Nat. Hist. Mus. Los Ang. 463, 1–12 3 Blaustein, A.R. et al. (1998) Effects of ultraviolet radiation on amphibians: field experiments, Am. Zool. 38, 799–812 4 Berger, L. et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rainforests of Australia and Central America, Proc. Natl. Acad. Sci. U. S. A. 95, 9031–9036 5 Duellman, W.E. (1993) Amphibian Species of the World: Additions and Corrections, Museum of Natural History, University of Kansas, Lawrence (Spec. Publ. 21) 6 Frost, D.R., ed. (1985) Amphibian Species of the World: A Taxonomic and Geographic Reference, Association of Systematics Collections, Lawrence, Kansas 7 Glaw, F. and Köhler, J. (1998) Amphibian species diversity exceeds that of mammals, Herpetol. Rev. 29, 11–12 8 Das, I. (1998) A new species of Rana from the Terai of Nepal, J. Herpetol. 32, 223–229 9 Hanken, J. and Wake, D.B. (1998) Biology of tiny animals: systematics of the minute salamanders (Thorius: Plethodontidae) from Veracruz and Puebla, Mexico, with descriptions of five new species, Copeia 1998, 312–345 10 Pombal, J.P., Jr, Wistuba, E.M. and Bornschein, M.R. (1998) A new species of brachycephalid (Anura) from the Atlantic rain forest of Brazil, J. Herpetol. 32, 70–74 11 Bell, B., Daugherty, C.H. and Hay, J.M. (1998) Leiopelma pakeka, n. sp. (Anura: Leiopelmatidae), a cryptic species of frog from Maud Island, New Zealand, and a reassessment of the conservation status of L. hamiltoni from Stephens Island, J. R. Soc. N. Z. 28, 39–54 12 Hillis, D.M., Moritz, C. and Mable, B.K., eds (1996) Molecular Systematics (2nd edn), Sinauer 13 Tilley, S.G. and Mahoney, M.J. (1996) Patterns of genetic differentiation in salamanders of the Desmognathus ochrophaeus complex (Amphibia: Plethodontidae), Herpetol. Monogr. 10, 1–42 14 Good, D.A. and Wake, D.B. (1992) Geographic variation and speciation in the torrent salamanders of the genus Rhyacotriton (Caudata: Rhyacotritonidae), Univ. Calif. Publ. Zool. 126, 1–91 Holocene invasions: finally the resolution ecologists were waiting for! W hat makes particular ecosystems more or less resistant to biological invasions? After many years of suggestive observations and speculations1–3, at last a few rigorous experiments with herbaceous vegetation have been conducted4–6. However, the spatial and temporal scale of invasions of woody species in forest ecosystems are too large to allow such experiments. Can we learn anything from Holocene invasions documented by pollen analyses? Unfortunately, the lake and bog sediments that are used for conventional pollen analyses recruit pollen from large areas and therefore permit the reconstruction of regional vegetation only on the scale of tens of kilometers. Such data normally lack sufficient spatial resolution to detect what happened in individual plant communities. In this context, recent papers by Randy Calcote7 and by Margaret Davis and colleagues8 represent a real breakthrough in our understanding of Holocene invasions. It has been known for some time9 that small wet sites within woods (forest hollows of about 5 m in diameter) gather most of their pollen from their surround- 8 ings and can provide a spatially detailed history of forest changes on the scale of a stand (1–3 ha). Also, application of a very suitable multivariate technique – canonical variate analysis – in vegetation paleoecology (Box 1) has been known for almost 30 years (D.P. Adam, PhD thesis, University of Arizona, 1970). Margaret Davis and her colleagues not only used these options efficiently, but also obtained better data than researchers had previously, and came up with a mechanistic interpretation of reconstructed standscale history of Holocene tree invasions. The basic data set is based on ten sediment cores from eight small forest hollows. Four hollows were in stands that are now dominated by eastern hemlock (Tsuga canadensis) and four in hardwood stands dominated by sugar maple (Acer saccharum). For neoecologists, this might sound like a small sample. However, it is unusually large when one considers that most such studies are based on only one to four cores. At all the hollows they studied, once organic sediment accumulation had started, it appeared to continue at 1–3 cm per century without 0169-5347/99/$ – see front matter © 1999 Elsevier Science. All rights reserved. PII: S0169-5347(98)01517-1 15 Highton, R. (1995) Speciation in eastern North American salamanders of the genus Plethodon, Annu. Rev. Ecol. Syst. 26, 579–600 16 Jockusch, E.L., Wake, D.B. and Yanev, K.P. (1998) New species of slender salamanders, Batrachoseps (Amphibia: Plethodontidae), from the Sierra Nevada of California, Contrib. Sci. Nat. Hist. Mus. Los Ang. 472, 1–17 17 Green, D.M. et al. (1997) Cryptic species of spotted frogs, Rana pretiosa complex, in western North America, Copeia 1997, 1–8 18 Mayr, E. (1942) Systematics and the Origin of Species, Columbia University Press 19 Frost, D.R. and Hillis, D.M. (1990) Species in concept and practice: herpetological applications, Herpetologica 46, 87–104 20 Ghiselin, M.T. (1997) Metaphysics and the Origin of Species, State University of New York Press 21 Stebbins, R.C. (1949) Speciation in salamanders of the plethodontid genus Ensatina, Univ. Calif. Publ. Zool. 48, 377–526 22 Moritz, C., Schneider, C.J. and Wake, D.B. (1992) Evolutionary relationships within the Ensatina eschscholtzii complex confirms the ring species interpretation, Syst. Zool. 41, 273–291 23 Wake, D.B. and Schneider, C.J. (1998) Taxonomy of the plethodontid salamander genus Ensatina, Herpetologica 54, 279–298 24 Highton, R. (1998) Is Ensatina eschscholtzii a ring-species? Herpetologica 54, 254–278 interruption, in what seemed to be a response to a continuously rising water table. Sediment age was established for each core by plotting depth against the calibrated radiocarbon age of seeds of terrestrial plants or charcoal fragments isolated from the sediment8. The fossilpollen composition in all analysed core layers was then compared with surfacepollen assemblages from forest hollows in northern Michigan and adjacent Wisconsin7 (USA, Box 1). Four hemlock stands originated as patches of white pine (Pinus strobus) forest that were invaded by hemlock about 3000 years ago, when hemlock expanded its range in northern Michigan. Over the next several thousand years, hemlock coexisted with white pine, but eventually hemlock became dominant and white pine almost completely disappeared (Box 1b, trajectory 1). The history of four nearby maple stands is more variable and less well understood. Unlike the hemlock stands, three of the four maple patches were not dominated by white pine at the time of the hemlock invasion, but instead had abundant northern red oak (Quercus rubra) and maples (sugar maple and red maple, A. rubrum). Two of these stands were never dominated by hemlock (Box 1b, trajectory 2). The other two were invaded by hemlock but only temporarily. Sugar maple and basswood (Tilia americana) increased in these TREE vol. 14, no. 1 January 1999 NEWS & COMMENT Box 1. Reconstruction of vegetation history of a hemlock–hardwood forest mosaic in northern Michigan using canonical variate analysis Surface pollen samples from a large number of forest hollows (66) in northern Michigan (USA) are a priori classified into vegetation types (white pine, sugar maple, etc.) based on actual vegetation (distanceweighted basal area of tree species within a 50 m radius of individual hollows)7,8. A multivariate method called canonical variate analysis (CVA, or multiple discriminant analysis) is then applied to the data. This technique derives linear combinations of measured variables (pollen amounts of 13 recognized tree taxa in surface pollen samples) called ‘canonical variates’ or ‘discriminant functions’. Canonical variates are independent of each other and ensure maximum separation among the classified samples. (a) Eastern hemlock White pine CVA axis 2 Maple–hemlock Northern red oak Sugar maple Black ash CVA axis 1 (b) Eastern hemlock White pine CVA axis 2 1 2 Maple–hemlock Northern red oak Sugar maple Black ash CVA axis 1 The first two variates, which explain most of the total variance (84%) are then plotted as two orthogonal axes in an ordination diagram (a) where individual samples are positioned according to their canonical scores based on pollen composition. Ranges of surface samples from individual vegetation types are expressed as circular or less regular envelopes in the same diagram. (b) Fossil pollen samples can now be positioned on the canonical variates and vegetation-type envelopes derived from surface samples. Two generalized trajectories of pollen assemblages from hemlock (1) and hardwood (2) hollows illustrate vegetation changes in these two types of forest over the past 6000 years. Hemlock reached the area some 3000 years ago. Apparently, depending on the initial amount of hardwood litter in a mosaic of pine–oak forests, hemlock either could or could not invade and persist in particular vegetation patches. Species names: white pine, Pinus strobus; northern red oak, Quercus rubra; black ash, Fraxinus nigra; eastern hemlock, Tsuga canadensis; sugar maple, Acer saccharum. (Online: Fig. I ) stands and, by 2000 to 800 years ago, they resembled modern maple stands. One of the authors’ major conclusions is that the invasion of hemlock was sensitive to the species composition of the resident forests. TREE vol. 14, no. 1 January 1999 At the time of the hemlock invasion, the invaded forest stands resembled modern white-pine stands, whereas stands that were not invaded, or at least never dominated by hemlock, resembled oak forest with abundant maples. One possible inter- pretation of the preferential invasion of pine stands involves differences in the physical environment. However, both GIS analysis and detailed studies of soil profiles failed to identify significant differences in abiotic factors between upland hemlock and maple patches. Conditions could have been different 3000 years ago. If not, we might ask what had been responsible for the origin of the pre-hemlock pine–oak mosaic? For example, perhaps this mosaic was initiated by clustered dispersal of red-oak acorns into pine forests by squirrels, mice and, although less likely, jays10. A second interpretation involves biotically caused differences in the environment. Within the pine–hardwood mosaic, canopy composition and litter structure and chemistry influence the microclimate, light environment, humus type and humus thickness, as well as nutrient availability. Both white pine and red oak form an open canopy with sufficient light on the forest floor for hemlock growth. However, white-pine forests apparently provided a better seedbed for hemlock than oak or maple stands11. Hemlock seedlings are unable to penetrate hardwood leaf litter, and they can be smothered by leaf litter if they are buried during the first years when they are very small. In contrast, sugar maple seedlings can penetrate thick, coarse litter and are often found growing on the undisturbed floor of hardwood forests. Intolerance of low nitrogen availability is thought to contribute to low survival and poor growth of sugar maple under a hemlock canopy, where the litter has high carbon:nitrogen ratios and relatively low mineralization. Therefore, positive neighborhood feedbacks on recruitment probably reinforce the continued dominance of hemlock and sugar maple in their respective patches11,12. Such biotic control of the environment plays an important role in determining the invasibility of individual plant communities. This must also be one of the mechanisms by which increasing between-habitat heterogeneity can result in strikingly divergent vegetation succession. Neither Gleason nor Clements – the pioneers of plant community ecology – would be particularly happy with these results. Gleason denied that there were ever sharp spatial vegetational changes without a causative sharp abiotic environmental change12. According to Clements, all successional series in an area with the same climate will eventually converge towards only one final community13. The hemlock–hardwood forest mosaic appears to be an excellent example of a ‘stable mosaic situation’ (in contrast to ‘disturbance mosaic’ or ‘mosaic-cycle’ phenomena) as discussed in the context of positive feedback ‘switches’ by Wilson and Agnew11,12. 9 NEWS & COMMENT This whole story makes a lot of sense. A bridge between Holocene paleoecology and neoecology has been built. Nevertheless, as a neoecologist, I am still missing other vegetation components and potential players. For example, Maguire and Forman14, who worked in mature hemlock–hardwood forests in West Virginia (USA), found that patches of a herbaceous partridge-berry (Mitchella repens) represent habitats that seem especially suitable for hemlock seedlings. As they explain, this might just be a passive positive association: it could be a result of negative effects of certain ferns, such as Dryopteris carthusiana (D. spinulosa), on hemlock seedlings. It would be interesting to know what the situation is in Michigan – here, both Mitchella and Dryopteris occur. M. Rejmánek Section of Evolution and Ecology, University of California, Davis, CA 95616, USA References 1 Trepl, L. (1990) Zum problem der Resistenz von Pflanzengesellschaften gegen biologische Invasionen, Verh. Berl. Bot. Ver. 8, 195–230 2 Rejmánek, M. (1996) Species richness and resistance to invasions, in Biodiversity and Ecosystem Processes in Tropical Forests (Orians, G.H., Dirzo, R. and Cushman, J.H., eds), pp. 153–172, Springer-Verlag 3 Stohlgren, T.J. et al. Exotic plant species invade hot spots of native plant diversity, Ecol. Monogr. (in press) 4 Burke, M.J.W. and Grime, J.P. (1996) An experimental study of plant community invasibility, Ecology 77, 776–790 5 Tilman, D. (1997) Community invasibility, recruitment limitation, and grassland biodiversity, Ecology 78, 81–92 6 Lavorel, S., Prieur, A-H. and Grigulis, K. Invasibility and diversity of plant communities: from patterns to processes, Divers. Distrib. (in press) 7 Calcote, R. (1998) Identifying forest stand types using pollen from forest hollows, The Holocene 8, 423–432 8 Davis, M.B., Calcotte, R., Sugita, S. and Takahara, H. (1998) Patchy invasion and the origin of a hemlock–hardwood forest mosaic, Ecology 79, 2641–2659 9 Larsson, C. and Sernander, R. (1935) Lokalt betonade pollendiagram i den historiska växtsociologiens tjänst, Geol. Fören. Stockholm Förehandl. 57, 59–83 10 Johnson, W.C. et al. (1997) Nut caching by blue jays (Cyanocitta cristata L.): implications for tree demography, Am. Midl. Nat. 138, 357–370 11 Davis, M.B. et al. (1994) Historical development of alternate communities in a hemlock–hardwood forest in northern Michigan, USA, in Large-scale Ecology and Conservation Biology (Edwards, P.J., May, R.M. and Webb, N.R., eds), pp. 19–39, Blackwell 12 Wilson, J.B. and Agnew, A.D.Q. (1992) Positivefeedback switches in plant communities, Adv. Ecol. Res. 23, 263–336 13 Leps, J. and Rejmánek, M. (1991) Convergence or divergence: what should we expect from vegetation succession? Oikos 62, 261–264 14 Maguire, D.A. and Forman, R.T.T. (1983) Herb cover effects on seedling patterns in a mature hemlock–hardwood forest, Ecology 64, 1367–1380 Coming soon in TREE : • Constraints in the restoration of ecological diversity in grassland and heathland communities, J.P. Bakker and F. Berendse • The Y chromosome as a battle ground for sexual selection, E.R.S. Roldan and M. Gomendio • The evolution of mutualisms: exploring the paths between conflict and cooperation, E.A. Herre, N. Knowlton, U.G. Mueller and S.A. Rehner • The costs of helping, R. Heinsohn and S. Legge • Tempo and mode of speciation in the sea, J.B.C. Jackson and A.H. Cheetham • The evolution of genomic anatomy, L.D. Hurst • Food exploitation: searching for the optimal joining policy, L. Giraldeau and G. Beauchamp • Heritable variation and evolution under favourable and unfavourable conditions, A.A. Hoffmann and J. Merilä • Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal, D. Sherbakov • Growing up with dinosaurs: molecular dates and the mammalian radiation, L. Bromham, M.J. Phillips and D. Penny 10 TREE vol. 14, no. 1 January 1999