Diversity by Default

 

David Tilman*

Science Jan 22 1999: 495-496.

One of the mysteries of biology is how the estimated 5 to 50 million species on Earth coexist [HN1]. Some of the diversity results from the separation of Earth into five continents and the somewhat parallel diversifications of each. Diversity within a continent is partly explained by large-scale gradients in climate, resource availability, productivity, and disturbance--in combination with interspecific trade-offs that cause each species to have optimal performance at a particular point on these gradients [HN2]. The largest part of the world's diversity, however, may come from a poorly understood phenomenon--the ability of hundreds to thousands of species that seemingly compete for the same few resources to coexist in relatively homogeneous local sites in lakes, grasslands, rainforests, coral reefs, and intertidal habitats. A long-term study in a Panamanian rainforest [HN3], reported by Hubbell and colleagues [HN4] on page 554 of this issue, has now provided important insights into how such coexistence may occur (1).

Almost 40 years ago G. E. Hutchinson [HN5] noted that the coexistence of hundreds of species of algae in lakes was paradoxically high compared with the prediction of then-current theory that the number of species should not exceed the number of resources for which they competed (2). Comparably diverse assemblages of potential competitors occur in many types of ecosystems around the world. Four major classes of theoretical solutions to this paradox of diversity have since been proposed, all of which predict, as a first approximation, almost unlimited diversity [HN6]. Given the appropriate trade-offs in species traits, high diversity can be caused by local spatial heterogeneity (3), by nonequilibrium conditions (4, 5), by interactions among at least three trophic levels (for example, plants, herbivores, and parasites) (3, 6), or by neighborhood recruitment limitation (local absence of young of superior competitors) (7-9). These theories solved the paradox, but the mystery remains: What actually explains high local diversity in nature?


Rainforest diversity. The diversity of this Panamanian rainforest, and of other ecosystems, may hinge on spatially patchy dispersal. Local absence of a superior competitor can allow an inferior species to win by default.

Since 1980, Hubbell and collaborators have been studying the dynamics of a tropical rainforest on Barro Colorado Island, Panama [HN7], by mapping and periodically recensusing the locations of treefall gaps [HN8] and of more than 300,000 individual trees. They used these data to test two hypotheses frequently cited as possibly accounting for high diversity in rainforests--the intermediate disturbance hypothesis [HN9] (one of many variants of nonequilibrium coexistence) and the recruitment limitation hypotheses. The intermediate disturbance hypothesis (10, 11) states that disturbances, such as treefall gaps, lead to a predictable successional sequence [HN10] in which one tree species replaces another, and another, culminating in dominance by a canopy tree species [HN11]. If disturbances are rare, almost all sites are dominated by the late successional canopy species, and total stand diversity is low. If disturbances are frequent, almost all sites are dominated by early successional, pioneer species, and diversity is again low. However, at intermediate rates of disturbance, there are a range of sites, some newly disturbed, some of intermediate age, and some old enough to be dominated by late successional canopy species. This would allow the full range of species traits to coexist and lead to maximal species diversity.

Hubbell's team also examined the importance of coexistence by recruitment limitation (8, 9). Plants compete only with individuals living sufficiently nearby that each could cast shade on or have roots that overlap with the other. Because of poor dispersal ability, low local abundance, or chance events, however, many plant species may be absent from such a neighborhood and thus have their abundance be recruitment limited. Like a team that fails to appear at a sporting event, a species that is locally absent has forfeited any chance of competitive victory at the site. This can allow inferior competitors to win by default. If there is recruitment limitation, the winners of local competition are not necessarily the best competitors that exist in the region, but the best competitors that happened to colonize a particular site. This can lead to essentially unlimited diversity (8, 9).

Much of the evidence that Hubbell and colleagues gathered supports recruitment limitation over the intermediate disturbance hypothesis. For example, they found that the composition of gaps was amazingly constant over the 12 years of their study. Because this suggests that little successional replacement was occurring, it fails to support the intermediate disturbance hypothesis. They also observed a significant positive correlation between changes in species abundances in gaps and those in non-gap areas, which further suggests that the changes in composition that did occur were not successional. They found a low diversity of seedling and sapling species in gaps. This seemed to result from the low number of seeds and of plant species in the seed that fell on a site, which they measured using a series of 200 seed traps spread throughout their plot. The absence of most species from any given gap is highly suggestive of recruitment limitation. In support of the victory-by-default hypothesis, they observed that pioneer species, which presumably are poorer competitors, persisted in gaps.

One of their assertions, however, and related tests, seems open to debate. They suggested that the intermediate disturbance hypothesis assumes higher diversity within gaps. Diversity within gaps, though, need not change during succession for the intermediate disturbance hypothesis to explain high diversity of a locality. All that is needed is for the species composition of gaps to change through time, and for intermediate disturbance to lead to the greatest range of gap ages.

In combination with work in rocky intertidal (12), grassland (13, 14) [HN12], and other habitats (15), this new work suggests that local recruitment limitation may be a universal feature of sessile [HN13] species. The issue, now, is which of at least three alternative recruitment-limitation hypotheses actually explains the high-local diversity of such habitats. Is diversity maintained by a trade-off between recruitment ability versus competitive ability (8)? Or, does recruitment limitation allow local coexistence of species that already are capable of regional coexistence (9)? Or, does recruitment limitation so slow the rate of competitive displacement that high-local diversity can be maintained, without any such trade-offs, by a regional equilibrium between extinction and the evolution of new species (16)? Or, is there a diversity of explanations for diversity?

The growing consensus on the importance of recruitment limitation puts us a significant step closer to understanding the mystery of Earth's high diversity. This mystery was of only academic interest 40 years ago, but the preservation of Earth's diversity is an increasingly important societal goal. Habitat destruction and fragmentation, invasions by exotic species, and nutrient pollution all cause loss of local diversity and species extinctions. Our ability to preserve maximal diversity in the face of this increasingly great human domination of the world's ecosystems, however, requires a much more complete understanding of diversity. The causes and conservation of Earth's diversity remain one of the greatest challenges facing ecology and society [HN14].

References and Notes

  1. S. P. Hubbell et al., Science 283, 554 (1999).
  2. G. E. Hutchinson, Am. Nat. 95, 137 (1961).
  3. D. Tilman, Resource Competition and Community Structure, Monographs in Population Biology (Princeton Univ. Press, Princeton, NJ, 1982) [publisher's information].
  4. R. A. Armstrong and R. McGehee, Am. Nat. 115, 151 (1980).
  5. P. L. Chesson, in Community Ecology, J. Diamond and T. Case, Eds. (Harper and Row, NY, 1986), pp. 240-256.
  6. D. H. Janzen, Am. Nat. 104, 501 (1970).
  7. H. S. Horn and R. H. MacArthur, Ecology 53, 749 (1972).
  8. D. Tilman, ibid. 75, 2 (1994).
  9. G. C. Hurtt and S. W. Pacala, J. Theor. Biol. 176, 1 (1995).
  10. J. H. Connell, Science 199, 1302 (1978).
  11. S. A. Levin and R. T. Paine, Proc. Natl. Acad. Sci. U.S.A. 71, 2744 (1974) [Medline].
  12. S. Gaines and J. Roughgarden, ibid. 82, 3707 (1985).
  13. P. F. Grubb, Biol. Rev. 52, 107 (1977).
  14. D. Tilman, Ecology 78, 81 (1997).
  15. M. D. Fox and B. J. Fox, in Ecology of Biological Invasions: an Australian Perspective, R. H. Groves and J. J. Burdon, Eds. (Australian Academy of Science, Canberra, Australia, 1986), pp. 57-66.
  16. S. P. Hubbell, A Unified Theory of Biogeography and Biodiversity (Princeton Univ. Press, Princeton, NJ), in press.
  17. I thank N. Haddad for his comments.

The author [HN15] is in the Department of Ecology, University of Minnesota, St. Paul, MN 55108, USA. E-mail: tilman@lter.umn.edu

HyperNotes
Related Resources on the World Wide Web

General Hypernotes

 
The Institute of Ecosystem Studies gives an overview and definition of ecology.
The Ecological Society of America presents an online brochure about ecology and a fact sheet on biodiversity and its importance.
CSUBIOWEB from California State University, Stanislaus, provides extensive annotated lists of Web resources in the biological sciences. Among the subjects covered are ecology and biodiversity.
The Ecology WWW Page, maintained by A. Brach, is a searchable list of ecology resources on the Internet.
The Center for Conservation Biology Network maintains the Virtual Library of Ecology, Biodiversity and the Environment, a collection of links to Web resources organized by topic.
The Mining Company Guide to Ecology provides lists of ecology resources on the Internet. Biodiversity and ecosystems Web links are included.
Biodiversity and Conservation is a Web hypertext book by P. Bryant, Department of Biological Sciences, University of California, Irvine.
R. Russo, Department of Biology, Indiana University/Purdue University, Indianapolis, provides extensive lecture notes for a course of the principles of ecology.
M. Knee, Department of Horticulture and Crop Science, Ohio State University, presents an introduction to ecology and to biomes for a course in general plant biology.
The World Resources Institute presents a Biodiversity page. A glossary of biodiversity terms is included.
The World Conservation Monitoring Centre presents an overview of biodiversity.
The Association for Tropical Botany was founded in 1963 to promote research and to foster the exchange of ideas among biologists working in tropical environments. It publishes the journal Biotropica. The Web site provides links to Web resources on tropical biology.
Exploring the Tropics is an educational presentation by the Missouri Botanical Garden.
The Smithsonian Tropical Research Institute conducts basic research on the ecology, behavior, and evolution of tropical organisms; it traces its history to the construction of the Panama Canal, which created Barro Colorado Island.
The Tropical Rain Forest Information Center at Michigan State University presents information about the science of rain forests in the Rain Forest Report Card section and offers a tour of a Virtual Rain Forest.
The Long-Term Ecological Research (LTER) Network is a collaborative effort of scientists and students investigating ecological processes operating at long time scales and over broad spatial scales; summaries of some recent research projects are provided.

 

Numbered Hypernotes

  1. In lecture notes on biogeography for a Web course on physical geography, M. Pidwirny, Department of Geography, Okanagan University College, Kelowna, BC, defines species, populations, communities, and ecosystems. W. Walsh's Diversity of Life Web Index provides links to resources available on the Web for exploring the diversity of species. The World Resources Institute Biodiversity page discusses how many species there are in the world; a list of numbers of species by taxa is also provided. A discussion of the number of species on Earth is included in the chapter on global patterns of diversity in P. Bryant's Biodiversity and Conservation hypertext book.
  2. The lecture notes for a course on global change at the University of Michigan includes a presentation on the geography and ecology of species distributions. A. Ditto reviews patterns of species diversity and mechanisms influencing diversity in a tutorial developed for a course on landscape ecology and macroscopic dynamics at the University of New Mexico. Introduction to Biomes, a module by S. Woodward, Radford University, VA, in the Virtual Geography Department project, includes information on the characteristics of the tropical rainforest and other terrestrial biomes. In lecture notes for a course on conservation biology, P. Schappert, Department of Zoology, University of Texas, provides an introduction to biodiversity and discusses the patterns and processes of species diversity. M. Bleeker's Botanic Diversity Pages include a collection of links to Web resources on botanical diversity and field biology and a multimedia tour of a tropical rainforest in Suriname.
  3. The Encarta Web encyclopedia presents an introduction to the rain forest. "Rainforest structure and diversity" is a chapter from A Neotropical Companion by J. Kricher that is made available by the publisher, Princeton University Press. Live from the Rainforest is an educational "Passport to Knowledge" Web site sponsored by NASA and the National Science Foundation. The Rainforest Database from the Living Earth educational Web site is a collection of texts and images that give an overview of rainforest ecology, people, uses, and deforestation issues.
  4. S. Hubbell, Department of Ecology and Evolutionary Biology, Princeton University, summarizes his research interests in tropical forests. Researchers at the Center for Tropical Forest Science of the Smithsonian Tropical Research Institute are contributors to this study.
  5. G. E. Hutchinson's 1958 address to the American Society of Naturalists titled "Homage to Santa Rosalia or Why are there so many kinds of animals?" is provided as a reading assignment for a course on ecology at Plymouth State College, NH.
  6. E. Iglich, Biology Department, Western Maryland College, Westminster, discusses theories of species diversity and types of succession in lecture notes for an ecology course. The Oak Ridge National Laboratory Review (vol. 29., no. 3, 1996) featured an article by C. Krause titled "Life on Earth: Why biodiversity varies," which discusses M. Huston's research on species diversity. For a course on ecology A. Lloyd, Department of Biology, Middlebury College, VT, provides an outline of a lecture on disturbance ecology. P. Schappert, Department of Zoology, University of Texas, discusses the role of disturbance in nonequilibrium community models in lecture notes on conservation biology. J. Bartleet discusses possible reasons for high fish diversity in lecture notes about coral reefs for a course on coastal ecosystems at the North East Wales Institute for Higher Education, Wrexham, UK.
  7. A map provided on the Smithsonian Tropical Research Institute Web site shows the location of Barro Colorado Island; information about the island's history and natural history is provided. The Net Primary Production (NPP) Database from the Oak Ridge National Laboratory includes an illustrated entry for the Barro Colorado Island site. Scientific research on Barro Colorado Island is discussed in a 1996 report titled "The key role of specific lands in the Panama Canal area in preserving the value of Panama's natural heritage," which is available from the DENIX (Defense Environmental Network and Information eXchange) Public Menu Web site.
  8. The Rainforest Database contains a section about tree gaps and the ecology of rainforest regeneration.
  9. The intermediate disturbance hypothesis in regard to coral reefs and hurricanes is discussed by J. Battey in lecture notes for a course in coral reef biology at the University of the Virgin Islands.
  10. R. Russo, Department of Biology, Indiana University/Purdue University, Indianapolis, discusses community structure and succession in lecture notes for an ecology course. Plant succession is discussed in the lecture notes for a course on plant biology offered by the Department of Cell Biology and Molecular Genetics, University of Maryland. M. Pidwirny, Department of Geography, Okanagan University College, Kelowna, BC, presents lecture notes on community properties and structure and on plant succession for the biogeography section of a physical geography course.
  11. The GardenWeb Glossary of Botanical Terms defines canopy. The Living Earth Rainforest Database includes a section on the canopy. A discussion of rainforest layers is presented on Science in the Rainforest, the Web site for a 1995-96 electronic field trip series presented by the Public Broadcasting Service and Turner Adventure Learning. An illustration, with definitions, of the layers of a rainforest is provided by the Forestry Advisers Network of the Canadian International Development Agency.
  12. Information about grassland biodiversity research and other the long-term studies undertaken at the Cedar Creek Natural History Area, an ecological reserve operated by University of Minnesota in cooperation with the Minnesota Academy of Science, is presented.
  13. Sessile is defined in the Glossary of Forest Protection from the Finnish Forest Research Institute (METLA). The WWWebster Dictionary defines sessile.
  14. The Biodiversity Group of Environment Australia presents a paper on biodiversity and its value. "The current state of biological diversity," the first chapter of the 1988 book Biodiversity by E. O. Wilson, is made available on the Web site of CIESEN (Center for International Earth Science Information Network). Access Excellence provides the text of a speech about why diversity matters given by P. Raven at the 1994 Conference of the Parties to the Convention on Biological Diversity, Nassau, Bahamas. The Convention on Biological Diversity Web site provides information related to the Convention and the conservation and sustainable use of biological diversity; a leaflet with basic information about the Convention is available. The Biodiversity Information Unit of the Natural History Museum, London, presents a Web site about measuring the value of biodiversity. The 15 June 1997 issue of Conservation Ecology featured an article titled "The multifaceted aspects of ecosystem integrity" by G. De Leo and S. Levin about the importance of understanding the complexity of natural systems.
  15. D. Tilman is in the Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul