KLAUS ROHDE: SCIENCE, POLITICS AND ART

See Rohde (Nonequilibrium Ecology, Cambridge University Press 2005) online support material

This is a follow-up to questions about a paper discussed in a seminar which I gave two weeks ago at the School of Environmental Sciences and Natural Resources Management.

I have given a causal explanation of the much greater species richness in tropical than in cold-temperate environments in my post “Faster Evolution in the Tropics ? Effective Evolutionary Time”. A recent paper by Wright, S., Keeling, J. and Gillman, L. in PNAS (Proceedings of the National Academy of Science) 103, 7718, 2006) specifically tests this hypothesis using molecular evidence from tropical and cold-temperate tree species and finds convincing evidence. The authors used the ITS (internal transcribed spacer) –region of ribosomal RNA-encoding DNA of 45 pairs of phylogenetically independent congeneric or conspecific rainforest trees. One representative of each pair was from the lowland or low mountainous region in the tropics, the other from the highest possible latitude and altitude. The pairs did not overlap in their geographical distribution, and trees belonged to genera that were as species-rich or richer at high latitudes than in the tropics (which excludes the possibility that higher molecular substitution rates in the tropics were a consequence of faster speciation). In order to reduce the effect of genetic drift, population sizes of all species examined were large. – The speed of molecular evolution was found to be twice as great in the tropics than at high latitudes.

A brief note on this paper appeared in Science NOW Daily News, 1 May 2006, based on interviews with Jim Brown of the University of New Mexico, and me. Here is the interview with me, which clarifies some points and implications of the paper.

1) Have other scientists put forward empirical evidence that species evolve faster in the tropics before this study, or is this the first? And if there have been other kinds of studies, how is this one different or more enlightening?

There are several studies which provide strong evidence in support of various partial aspects of the hypothesis of faster evolutionary rates in the tropics, such as accelerated mutation rates, shorter generation times, and availability of many vacant niches which can absorb newly evolved species. There also are some studies which suggest faster rates of molecular evolution. However, the latter have never solved the problem of whether faster molecular evolution is the result of underlying metabolic rates (mutation rates especially) as suggested by the hypothesis, or whether faster molecular evolution is the result of higher speciation rates (in other words, which way round should the story be read). Allen et al. 2002 provide very strong evidence that metabolic rates are correlated with generation times and mutation rates, and they conclude that these finding support Rohde’s hypothesis, but only by inference. The present study, to my knowledge, is the first that provides direct and convincing empirical evidence that the hypothesis in toto is indeed valid.

2) What factor do you believe this study suggests might be responsible for the difference in molecular evolution rate between temperate and tropical regions?

As just said, the factor responsible was shown, in this study, to be increased mutation rates at higher temperatures, (as well as shorter generation times).

3) Are there weaknesses in the method that this group used?

I cannot see any. The authors have been very cautious: they state that further studies are necessary to definitively rule out the alternative explanation that genetic drift in small populations may be responsible. But this alternative really is only a remote possibility, considering that temporary reductions in population size in the evolutionary past are not more likely for tropical than cold-latitude species (as pointed out by the authors themselves).

4) What are the implications of species evolving faster in the tropics, either on how biodiversity is distributed around the world

The hypothesis predicts that evolution is faster not only in the tropics but in habitats which have higher temperatures and energy inputs generally, for example in deepsea sites which are fed by volcanic hot water upwellings. Scientists should therefore put special emphasis on studying such spots, if they want to get a true understanding of marine diversity. – Also, global warming will affect different areas of the globe differently. A re-distribution of diversity patterns must therefore be expected, although changes due to different evolutionary rates will take some time.

– or on how scientists conduct studies of evolution?

Looking at the vast number of evolutionary and ecological studies, some using very sophisticated statistical analyses, one is struck by the fact that potential DIRECT temperature effects on diversity until recently have been largely neglected. Such effects may be far greater than any effects due, for example, to area, heterogeneity of the habitat etc. etc. Many of the older studies are therefore quite useless. I don’t want to mention specific authors or books, but even some of the most widely cited monographs on general ecological and evolutionary patterns lead the reader astray because of the neglect of such direct temperature effects, concentrating instead on factors that are at best of secondary significance, such as area.- (It may be of interest that one of the truly great contemporary ecologists, when I presented my ideas at a symposium in the U.S., at first thought me “mad” (he told me and others), but he is now fully “converted”).

5) Does this speedier pace have any impact on species conservation in tropical locales?

It is obvious, of course, that devastation of tropical habitats has far greater implications for reducing global plant and animal diversity than devastation of cold-latitude habitats, because of the vastly greater species diversity in the tropics. Important here is to realize that species numbers in such tropical (and other) habitats are vastly underestimated, because parasites, the huge number of small invertebrates and microorganisms, most of which have not even been described yet, are usually ignored. Such species are not only of aesthetic and theoretical interest, but may play very significant roles in ecosystems. The role they play is even less well known than the species themselves. – To understand the cause of increased diversity in the tropics is of great significance: it may lead to more realistic estimates of diversity of these smaller organisms, because evolutionary rates will vary depending on the metabolism of these organisms. However, metabolic rates of these organisms are largely unknown. The present study may induce others to follow this up and look at mutation rates and their temperature dependence in various groups of organisms lower down the “hierarchy”.

Altogether, I believe that this paper is of extreme importance and will stimulate a lot of further research.

Here is the reference by Allen et al.:

Allen, A.P., Brown, J.H. and Gillooly, J.F. (2002). Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science, 297, 1545-1548.

I wish to draw your attention to a series of e-conferences on climate change.

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The series, which will be offered free of charge, starts off in April 2007 with a two-week dialogue on a topic of increasing urgency: expanding and accelerating an ecocentric philosophy among societies around the world. The need for such a shift has long been recognized. Based on the UN’s Rio Declaration of Environment and Development, in 1992 Al Gore observed, “Our challenge is to accelerate the needed change in thinking about our relationship to the environment in order to shift the pattern of our civilization to a new equilibrium – before the world’s ecological system loses its current one.” (Earth in the Balance)

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This post is based on my earlier entry in Wikipedia. This seems necessary because Wikipedia permits changes made by anybody, whether with the necessary knowledge or not.

The concept of a vacant or empty niche has been controversial in ecology. It is at the basis of any discussion of whether equilibrium or nonequilibrium conditions prevail in ecological systems. A vacant niche can be defined as the possibility that in ecosystems or habitats more species can exist than are present at a particular point in time, because many possibilities are not used by potentially existing species (K. Rohde 2005 Nonequilibrium Ecology, Cambridge University Press, Cambridge, http://www.cambridge.org/9780521674553).

1. History of the concept

Hutchinson, G. E. (1957) Concluding remarks. Cold Spring Harbour Symposium on Quantitative Biology 22, 415-427 was apparently the first who considered the possibility of vacant niches. He writes: (p.424): “The question raised by cases like this is whether the three Nilghiri Corixinae fill all the available niches……….. or whether there are really empty niches.”…….“The rapid spread of introduced species often gives evidence of empty niches, but such rapid spread in many instances has taken place in disturbed areas.”

Since then, the concept “vacant niche” or “empty niche” has been used regularly in the scientific literature. Some of the many examples are Elton, C. (1958) The ecology of invasions by animals and plants. Chapman and Hall, London, UK. 181 pp.; Rohde, K. (1977). A non-competitive mechanism responsible for restricting niches. Zoologischer Anzeiger 199, 164-172; Rohde, K. (1979). A critical evaluation of intrinsic and extrinsic factord responsible for restricting niches. American Naturalist 114, 648-671; Rohde, K. (1980 ). Warum sind ökologische Nischen begrenzt? Zwischenartlicher Antagonismus oder innerartlicher Zusammenhalt?. Naturwissenschaftliche Rundschau, 33, 98-102;
Lawton, J.H. (1984). Non-competitive populations, non-convergent communities, and vacant niches: the herbivores of bracken. In: Strong, D.R. Jr., Simberloff, D., Abele, L.G. and Thistle, A.B. eds. Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, N.J., pp. 67-101; Price, P.W. (1984). Alternative paradigms in community ecology. In: Price, P.W., Slobodchikoff, C.N. and Gaud, W.S. eds. (1984). A new ecology. Novel approaches to interactive systems. John Wiley & Sons, New York, Chichester, Brisbane, Toronto, Singapore, pp.353-383; Compton, S.G., Lawton, J.H. and Rashbrook, V.K. (1989). Regional diversity, local community structure and vacant niches: the herbivorous arthropods of bracken in South Africa. Ecological Entomology 14, 365-373; Begon, M.J., Harper, L. and Townsend, C.R. (1990). Ecology. Individuals, populations and communities, second edition. Blackwell Scientific, Boston; and Cornell, H.V. (1999). Unsaturation and regional influences on species richness in ecological communities: a review of the evidence. Ecoscience 6, 303-315.
Further examples, some of them in great detail, are discussed in K. Rohde (2005) Nonequilibrium Ecology, Cambridge University Press, Cambridge.

2. Causes of vacant niches

Vacant niches can have several causes.

One cause is radical disturbances in a habitat (biotop). For example, draughts or forest fires can destroy a flora and fauna partially or completely. However, in such cases species suitable for the habitat usually survive in the neighbourhood and colonize the vacated niches, leading to a relatively fast reestablishment of the original conditions.

Further causes of vacant niches are radical and long-lasting changes in the environment, such as ice ages.

Vacant niches can also be due to evolutionary contingencies: suitable species did not evolve for usually unknown reasons.

3. Demonstration of vacant niches

Vacant niches can best be demonstrated by comparing the spatial component of niches in simple habitats. For example, Lawton and collaborators compared the insect fauna of the bracken , Pteridium aquilinum, a widely distributed species, in different habitats and geographical regions and found vastly differing numbers of insect species. They concluded that many niches remain vacant (e.g., Lawton, J.H. (1984). Non-competitive populations, non-convergent communities, and vacant niches: the herbivores of bracken. In: Strong, D.R. Jr., Simberloff, D., Abele, L.G. and Thistle, A.B. eds. Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, N.J., pp. 67-101.

Rohde and collaborators have shown that the number of ectoparasitic species on the gills of different species of marine fishes varies from 0 to about 30, even when fish of similar size and from similar habitats are compared. Assuming that the host species with the largest number of parasite species has the largest possible number of parasite species, only about 16% of all niches are occupied. However, the maximum may well be greater, since the possibility cannot be excluded that even on fish with a rich parasite fauna, more species could be accommodated (recent review in K. Rohde (2005) Nonequilibrium Ecology, Cambridge University Press, Cambridge.

Using a similar way of reasoning, Walker, T.D. und Valentine, J.W. (1984). Equilibrium models of evolutionary diversity and the number of empty niches. American Naturalist 124, 887-899. estimated that 12-54% of niches for marine invertebrates are empty.
The ground breaking theoretical investigations of Kauffman, S.A. (1993). The origins of order. Self-organization and selection in evolution. Oxford University Press, New York Oxford and Wolfram, S. (2002). A new kind of science. Wolfram Media Inc. Champaign, Il. also suggest the existence of a vast number of vacant niches. Using different approaches, both have shown that species rarely if ever reach global adaptive optima. Rather, they get trapped in local optima from which they cannot escape, i.e., they are not perfectly adapted. As the number of potential local optima is almost infinite, the niche space is largely unsaturated and species have little opportunity for interspecific competition.

The packing rules of Ritchie, M. und Olff, H. (1999). Spatial scaling laws yield a synthetic theory of biodiversity. Nature 400, 557-562 can be used as a measure of the filling of niche space. They apply to savanna plants and large herbivorous mammals, but not to any of the parasite species examined so far. It seems likely that they do not apply to most animal groups. In other words, most species are not densely packed: many niches remain empty (Rohde, K. (2001). Spatial scaling laws may not apply to most animal species. Oikos 93, 499-503).

That niche space may be nonsaturated, is also shown by introduced pest species. Such species lose almost without exception all or many of their parasites (Torchin, M.E. and Kuris, A.M. (2005). Introduced parasites. In: Rohde, K. (Ed.) Marine Parasitology. CSIRO Publishing Melbourne und CABI Wallingford, Oxon., pp. 358-366). Species that could occupy the vacant niches either do not exist or, if they exist, have not had the chance to invade these niches.

Diversity of marine benthos, interrupted by some collapses and plateaus, has increased from the Cambrian to the Recent, and there is no evidence that saturation has been reached (Jablonski, D. (1999) The future of the fossil record, Science 284, 2114-2116).

Simulations of latitudinal gradients in species diversity using the Chowdhury ecosystem model, have shown that results are closest to reality when many niches are kept empty (Rohde, K. and Stauffer, D . 2005 Simulation of geographical trends in the Chowdhury ecosystem model. Advances in Complex Systems 8, 451-464).

4. Consequences of the nonsaturation of niche space

The view that niche space is largely or completely saturated with species is widespread. It is thought that new species are accommodated mainly by subdivision of niches occupied by previously existing species, although an increase in diversity by colonization of large empty living spaces (such as land in the geologic past) or by the formation of new bauplans also occurs. It is also recognized that many populations never completely reach a climax state (i.e., they may come close to an equilibrium but never quite reach it). However, altogether the view prevails that individuals and species are densely packed and that interspecific competition is of paramount significance. According to this view, nonequilibria are generally caused by environmental disturbances.

Many recent studies (above and Rohde, K. (2005) Eine neue Ökologie. Aktuelle Probleme der evolutionären Ökologie. Naturwissenschaftliche Rundschau, 58, 420-426; Rohde, K. 2005: Nonequilibrium Ecology, Cambridge University Press, Cambridge support the view that niche space is largely unsaturated, i.e. that numerous vacant niches exist. As a consequence, competition between species is not as important as usually assumed. Nonequilibria are caused not only by environmental disturbances, but are widespread because of nonsaturation of niche space. Newly evolved species are absorbed into empty niche space, that is, niches occupied by existing species do not necessarily have to shrink.

5. Relative frequency of vacant niches in various groups of animals and plants

Available evidence suggests that vacant niches are more common in some groups than in others. Using SES values (standardized effect sizes) for various groups, which can be used as approximate predictors of the filling of niche space, Gotelli, N.J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: null-model analysis. Ecology Letters 5, 86-94 have shown that SES values are high for animal populations which occur in large population densities and/or are of large body size and are vagile, they are low for animal groups which occur in small population densities and/or are of small body size and have little vagility. In other words, more vacant niches can be expected for the latter.

6. Criticisms of the concept

The concept of vacant niche is not accepted by all. The reason given is that a niche is a property of a species and does therefore not exist if no species is present. In other words, the term is thought to be “illogical”. However, some authors who have contributed most to the formulation of the modern niche concept (Hutchinson, Elton) apparently saw no difficulties in using the term. If a niche is defined as the interrelationship of a species with all the biotic and abiotic factors affecting it, there is no reason not to admit the possibility of additional potential interrelationships. So, it seems logical to refer to vacant niches.

Furthermore, it seems that authors most critical of the concept vacant niche really are critical of the view that niche space is largely empty and can easily absorb additional species. They instead adhere to the view that everything is much of the time in equilibrium (or at least close to it), resulting in a continual strong competition for resources. This view, indeed, is the basis of Darwinian natural selection. Many recent studies, some empirical , some theoretical, have provided support for the alternate view that nonequilibrium conditions are widespread (see above and the recent review in Rohde K. Rohde 2005) Nonequilibrium Ecology, Cambridge University Press, Cambridge.

In the German literature, an alternate term for vacant niches has found some acceptance. It is that of “freie ökologische Lizens” (free ecological license) (Sudhaus,W. und Rehfeld, K. 1992. Einführung in die Phylogenetik und Systematik. Gustav Fischer Verlag Jena. It has the disadvantage that it does not convey immediately and easily what is meant, and it indeed does not correspond exactly to the term vacant niche. The usefulness of a term should be measured on the basis of its pregnancy and easy understandability, and on how fertile it is in promoting future research. The term vacant niche appears to fulfill these requirements.