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Microbial Experimental Systems in Ecology Microbial Experimental Systems in Ecology CHRISTINE M. JESSUP, SAMANTHA E. FORDE AND BRENDAN J.M. BOHANNAN I. Summary . .............................................. 273 II. Introduction. .......................................... 274 III. The History of Microbial Experimental Systems in Ecology . ...... 275 A. G.F. Gause and His Predecessors . ...................... 275 B. Studies Since Gause . .................................. 276 IV. Strengths and Limitations of Microbial Experimental Systems ...... 277 A. Strengths of Microbial Experimental Systems . .............. 277 B. Limitations of Microbial Experimental Systems . .......... 281 V. The Role of Microbial Experimental Systems in Ecology: Consensus and Controversy. .............................. 283 A. The Role of Microbial Experimental Systems . .............. 283 B. Controversies Surrounding Experimental Systems and Microbial Experimental Systems . ...................... 285 VI. Recent Studies of Microbial Experimental Systems . .............. 289 A. The Ecological Causes of Diversity . ...................... 290 B. The Ecological Consequences of Diversity.................. 296 C. The Response of Diversity to Environmental Change . ...... 298 D. Directions for Future Research .......................... 299 VII. Conclusions . .......................................... 300 Acknowledgments. .......................................... 300 References................................................... 300 I. SUMMARY The use of microbial experimental systems has traditionally been limited in ecology. However, there has recently been a dramatic increase in the number of studies that use microbial experimental systems to address ecological questions. In this chapter, we discuss the strengths, limitations, and criticisms of microbial experimental systems in ecology. We highlight a number of recent studies in which microbial experimental systems have been used to address one of the primary goals in ecology—identifying and understanding the causes and consequences of life’s diversity. Finally, we outline what we consider to be the characteristics of an ideal model system for advancing ADVANCES IN ECOLOGICAL RESEARCH VOL. 37 0065-2504/05 $35.00 # 2005 Elsevier Ltd. All rights reserved DOI: 10.1016/S0065-2504(04)37009-1 274 C.M. JESSUP, S.E. FORDE AND B.J.M. BOHANNAN ecological understanding, and discuss several microbial systems we feel fit this description. II. INTRODUCTION Ecology has been described as the ‘‘most intractable of the biological sciences’’ (Slobdokin, 1988). Ecologists are faced with the challenge of under- standing the distribution and abundance of organisms that are embedded in complex, dynamic systems of interactions. To make sense of such complexity, ecologists have relied on a number of approaches, including mathematical modeling, observations of natural systems, and field manipulations. Increas- ingly, ecologists are turning to another tool—laboratory experimental sys- tems. Microorganisms, in particular, have become increasingly popular as experimental systems with which to explore ecological processes (Fig. 1). These experimental systems include viruses, bacteria, and single‐celled eukaryotes (e.g., protists, algae and fungi). Detailed reviews of many of these experimental systems have been published previously on issues such as the generation and maintenance of diversity (Rainey et al., 2000) and the interplay between genetic change, ecological interactions, and community evolution (Bohannan and Lenski, 2000a), among others (e.g., Lawler, Figure 1 Increase in the proportion of published ecological studies using laboratory‐based microbial experimental systems from 1980 through 2001 in the journals Nature, Science, Proceedings of the Royal Society, Proceedings of the National Academy of Sciences, Ecology, American Naturalist, Ecology Letters, Oikos, Oecologia and Evolution. MICROBIAL EXPERIMENTAL SYSTEMS IN ECOLOGY 275 1998). In this chapter, we take a broader perspective and discuss the history of microbial experimental systems in ecology, the strengths and limitations of such systems, and controversies surrounding their use in ecology. We high- light the use of microbial experimental systems to explore the causes and consequences of ecological diversity. We conclude this chapter with a dis- cussion of microbial systems that may be ideal model systems in ecology, spanning theory, laboratory manipulation, and field experimentation. III. THE HISTORY OF MICROBIAL EXPERIMENTAL SYSTEMS IN ECOLOGY A. G.F. Gause and His Predecessors Microbial experimental systems have played a central, if sometimes under‐ appreciated, role in ecological history. The earliest published record of the use of a microbial experimental system in population biology is that of Rev. W. D. Dallinger who, in his address as the president of the Royal Microsco- py Society in 1887, described his attempt to discover ‘‘whether it was possible by change of environment, in minute life‐forms, whose life‐cycle was relatively soon completed, to superinduce changes of an adaptive character, if the observations extended over a suYciently long period’’ (Dallinger, 1887). Dallinger addressed this question using populations of protists as an experimental system, altering their environment by varying the temperature of the cultures. He demonstrated with these experiments that ecological specialization can incur a cost of adaptation (a decline in compet- itive fitness in environments other than the one to which the organisms have specialized) and that it was possible to study such phenomena with laboratory experimental systems. Over 20 years later, L.L. WoodruV (1911, 1912, 1914) used protists in hay infusions as an experimental system to study density‐dependent growth and succession. He concluded that interactions between organisms were an important driving force in the successional sequence of the protozoan com- munity that he observed. Similar studies by Skadovsky (1915) and Eddy (1928) were published in the decade following WoodruV’s work. In what were to become arguably the most famous microbial experiments in ecology, G.F. Gause built upon this earlier work by using experimental systems containing bacteria, yeast, and protists to ask ‘‘why has one species been victorious over another in the great battle of life?’’ (Gause, 1934). He coupled his laboratory experiments with the mathematical models of com- petitive and predator‐prey interactions first proposed by Alfred Lotka and Vito Volterra, and later popularized by Raymond Pearl (Kingsland, 1995). This combination of experiment and theory was especially powerful, allowing 276 C.M. JESSUP, S.E. FORDE AND B.J.M. BOHANNAN him to make quantitative predictions of the outcome of interactions between species, and then to test the plausibility of these predictions through carefully designed experiments with microorganisms. Several key principles in ecology are attributed to these studies. For example, Gause demonstrated that he was able to predict which of two species of Paramecium would be competitively dominant by estimating the growth parameters for each of the species grown alone. Subsequent interpretation of this work by Garrett Hardin led to the development of the principle of competitive exclusion, or ‘‘Gause’s Axiom’’ (Hardin, 1960). In another experiment using Didinium nasutum and Parame- cium caudatum, Gause demonstrated the importance of both spatial refugia and immigration for the co‐existence of predators and prey. B. Studies Since Gause Since Gause’s pioneering experiments, microbial experimental systems have been used to study a number of topics in ecology. For example, laboratory systems containing eukaryotic microorganisms (protists and/or microalgae) have been used to study succession (Gorden et al., 1979), the diversity‐ stability relationship (Hairston et al., 1968; Van Voris et al., 1980), predator‐ prey interactions (Luckinbill, 1973; van den Ende, 1973; Luckinbill, 1974, 1979), and the co‐existence of competitors (Vandermeer, 1969; Tilman, 1977; Sommer, 1984; Tilman and Sterner, 1984). The microbial experimental systems used by Tilman and his colleagues have particularly influenced the development of ecological theory. Although not the first to demonstrate the predictable nature of resource competition (this distinction would probably go to Levin, 1972), Tilman’s experiments with diatoms elegantly demonstrated the value of the resource‐explicit approach to competition theory first proposed by MacArthur (1972) and later developed by Tilman (1982). Experimental populations and communities of bacteria have also been used to explore ecological concepts such as resource competition (Hansen and Hubbell, 1980), the relationship between growth kinetics and population dynamics (Contois, 1959), specialist versus generalist strategies (Dykhuizen and Davies, 1980), optimality theory (Wang et al., 1996; Bull et al., 2004) and ecological diversification (Rosenzweig et al., 1994). The interaction between bacteria and bacteriophage (viruses that infect bacteria) has been utilized in many ecological and evolutionary studies of predator‐prey and parasite‐host interactions (Horne, 1970, 1971; Chao et al., 1977; Levin et al., 1977; Levin and Lenski, 1985; Lenski, 1988a; Schrag and Mittler, 1996; Bohannan and Lenski, 1997, 1999). These include studies of predator‐mediated co‐existence of competitors, trophic cascades, heterogeneity in prey vulnerability, the role of spatial refuges, and optimal foraging, among others. Studies of the MICROBIAL EXPERIMENTAL SYSTEMS
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