THE HISTORY OF BIOGEOGRAPHY, like that of all natural sciences, is one whose exact origins are incredibly difficult if not impossible to pinpoint, and its conceptual threads split and again intertwine in a captivating, dynamic tapestry chronicling the geographic, ecological and evolutionary history of the world’s biota. While fascinating accounts in their own right, studies of the historical development of scientific theories (e.g., “discoveries” of the theory of natural selection by Charles Darwin and Alfred Russel Wallace, of continental drift by Alfred Lothar Wegener, or of the structure of DNA by James Watson and Francis Crick), also provide valuable lessons for developing some truly transformative advances in the future. Here we review the historical development of island biogeography theory, with special emphasis on MacArthur and Wilson’s equilibrium theory, to demonstrate how the science of biogeography develops, not just as a regular accumulation of facts and succession of paradigms, but through a reticulating phylogeny of insights and ideas often marked by alternating episodes of diversification and reintegration.
In the following section we present a brief history of island theory, in general, and summarize foundational insights that were available to scientists by the middle decades of the twentieth century in their attempts to explain patterns in geographic variation among insular biotas. Because MacArthur and Wilson’s seminal contributions are the focus of all chapters in this volume, we see little need to describe their theory in detail here, beyond noting that their intent was to develop a theory with a much broader domain than is generally appreciated. Thus, in the third section of this chapter we describe the ontogeny and contraction in the conceptual domain of MacArthur and Wilson’s theory, from the wealth of ecological and evolutionary phenomena comprising their general theory and monograph to an increasingly more narrow focus on the equilibrium model of species richness that came to preoccupy much of the field during the 1970s and 1980s. In the final sections of this chapter we observe that, like other disciplines in contemporary biogeography, evolution, and ecology, island theory may again be entering an exciting and perhaps transformative period of advance through consilience and reintegration. Toward this end, we conclude with a case study on biogeography, ecology, and evolution of insular mammals to illustrate an approach toward integration of island biogeography, which may ultimately lead to a more comprehensive and insightful understanding of the ecological and evolutionary development of insular biotas.
Below we summarize seven advancements or approaches developed by the early decades of the twentieth century that were integral to the final articulation of MacArthur and Wilson’s equilibrium theory.
1. Encyclopedia of patterns. Island research has a distinguished history of providing insights that have either fundamentally transformed existing fields of science, or spawned new ones. Indeed, that environmentally similar but geographically isolated regions are comprised of distinct biotas (Buffon’s law) was a discovery fundamental to the realization that life was dynamic—species evolved in isolation (Buffon 1761; for summaries on the historical development of biogeography, see also Briggs 1995, Lomolino et al. 2004, Lomolino et al. 2006:13–38). Following Buffon’s articulation of biogeography’s first law, others (e.g., Candolle 1820) would provide cogent arguments on the geographic and temporal dynamics of biotas, and how their distributions and evolution were strongly influenced by interactions among the species. Thus, the early naturalists of the Age of European Explorations—visionaries whom today we recognize as the founders of the fields of biogeography, evolution and ecology—set out to describe the diversity and the geographic and temporal variation of life across an expanding spectrum of domains from the local and short-term scales to global and geological (evolutionary) ones.
Certainly the most distinctive types of newly discovered biotas, and of unrivaled importance to development of theories in biogeography, evolution, and ecology, were those inhabiting isolated islands. The seminal works of Darwin and Wallace are legendary in this respect, but these nineteenth-century naturalists were far from the first to appreciate the heuristic value of studying insular biotas (see summaries in Berry 1984, Wagner and Funk 1995, Grant 1998, Whittaker and Fernandez-Palacios 2007). During the eighteenth century, Carolus Linnaeus’s explanation for the origin, diversity, and distribution of life on earth was premised on the existence of an insular Paradise of creation and, later, an isolated mountain range where the world’s biota persisted during the biblical deluge and then dispersed to occupy their current ranges (Linnaeus 1781). Given the difficulty of accommodating this single center of origin/persistence theory with Buffon’s discovery of the distinctiveness of regional biotas, Karl Ludwig Willdenow proposed that, rather than just one, there were many centers of origin, each situated in montane regions across the globe, where regional biotas were created or persisted during catastrophic periods (Willdenow 1792).
Perhaps most foundational to the origins of island biogeography theory were the accounts of Johann Reinhold Forster’s (1778) circumnavigational voyage with Captain James Cook on the H.M.S. Resolution (1772–75). Not only did he find compelling evidence to support the generality of Buffon’s law for plants as well as mammals and birds, and for other regional biotas beside those of the tropics, Forster also described patterns that continue to be at the core of research on the geographic, evolutionary, and ecological development of isolated biotas. He described the general tendency for isolated biotas to be less diverse than those on the mainland, and for the diversity of plants to increase with island area, availability of resources, variety of habitats, and heat energy from the sun. Thus, two fundamental patterns which island theory attempts to explain—the species-isolation and species-area relationships—along with basic explanations for those patterns (precursors of area per se and habitat diversity hypotheses, and species-energy theory; Hutchinson [1959], Preston [1960], Williams, [1964], MacArthur and Wilson [1967], Brown [1981], Wright [1983], Currie [1991], Ricklefs and Lovette [1999], Hawkins et al. [2003], Kalmar and Currie [2006]) were well established early in the historical development of these disciplines.
Charles Darwin, Alfred Russel Wallace, Joseph Dalton Hooker and many other naturalists of the late eighteenth and early nineteenth centuries would continue to add to the already voluminous accounts and explanations for the diversity and geography of island life. As we now well know, their efforts to explain this immense and ever-expanding encyclopedia of patterns would shake the very foundations of established doctrine and eventually lead to identification of the fundamental, dynamic processes influencing the diversity and geography of nature.
2. Dynamics of nature (global to regional scales). The Age of European Exploration and, indeed, the first globalization of the natural sciences, provided scientists with far more than just a fascinating and continually expanding catalogue of the marvels of nature. As engrossed as they may have been with describing empirical patterns, these early global explorers and naturalists must have also felt compelled to explain them. Thus, Buffon’s (1761) explanation for the distinctiveness of biotas included long distance dispersal and adaptive evolution of populations as their ranges shifted in response to changes in Earth’s regional climates and environmental conditions. Again, Forster’s (1778) explanation for gradients in diversity of plants among islands and across the continents was based on his understanding of the abilities of these species to respond to geographic variation in resources, habitat diversity, and solar energy. Thus, comparisons of the diversity and composition of biotas across regions and along geographic clines would eventually become irrefutable evidence that the natural world—its climate, geology, and species—was mutable, challenging those early naturalists to develop dynamic, causal explanations. Their theories of the historical development of regional biotas would focus on factors influencing the fundamental processes of biogeography—extinction, immigration, and evolution. That is, biotas responded to the regional- to global-scale dynamics of land and sea by suffering extinctions, by dispersing to other areas, or by evolving and adapting in place.
3. Ecological interactions and emergence of ecology. While the early global naturalists—the first “biogeographers”—continued to explore broad-scale and long-term patterns in biological diversity, others focused on the dynamics of biotas at more local spatial and shorter temporal scales. With each new revelation, it became increasingly more clear that patterns in distribution and abundance of species at these scales were strongly influenced, not just by the three fundamental biogeographic processes, but by interactions among species themselves. Thus, just as evolutionary theory diverged from that of biogeography during the early decades of the twentieth century, the field of ecology would diverge from other studies of the geography of life to become a distinctive and respected science in its own right. In fact, MacArthur and Wilson would include ecological interactions (in particular, “competition”) as one of the fundamental, albeit challenging processes to study.
Biogeography is a subject hitherto little touched by quantitative theory. The main reason is that the fundamental processes, namely dispersal, invasion, competition, adaptation and extinction, are among the most difficult in biology to study and to understand. (MacArthur and Wilson 1967, p. 4)
4. Advances in theoretical and mathematical ecology. Challenges in understanding dynamic systems led scientists to become increasingly more sophisticated and adept in their abilities to translate ideas and assumptions into graphic and mathematical models that would thus make them testable within an objective, logical framework. Theoretical and mathematical scientists from a broad diversity of disciplines realized that the system properties they studied, whether they were geological formations, climatic conditions, chemical concentrations, gene frequencies, population abundance, or species distributions, resulted from interactions among opposing processes (e.g., orogeny and erosion; precipitation and evaporation; oxidation and reduction; or mutations, drift, birth, and death; e.g., Hardy [1908], Weinberg [1908], Lotka [1925], Pearl [1925], Volterra [1926, 1931], Fisher [1930], Gause [1934]). Often, the mathematical solutions to such problems would be simplified by assuming dynamic steady states, or equilibrial conditions, which could also be visualized in associated graphical models as the intersection of a system of curves describing opposing processes. The emerging discipline of mathematical ecology, lead by such distinguished scientists as G. Evelyn Hutchinson and his students (including Robert H. MacArthur), were quick to apply the tools developed by colleagues modeling the dynamics of other systems to their own studies of dynamics in the distributions and diversity of life.
5. Earlier syntheses and integrations. As we observed above, throughout the history of biogeography, and likely that of all other disciplines of science, its early explorers not just reported, but almost simultaneously and perhaps irresistibly attempted to synthesize the accumulated facts and ideas to provide a comprehensive description of how nature works. Monographs and treatises of Wallace (1857, 1869, 1876), Darwin (1859, 1860), and Hooker (1853, 1867) are familiar, if not legendary, attempts at such syntheses and integrations of patterns and developing theory in biogeography. Less well known and seldom read, but arguably as impressive if not influential, were the earlier works of Buffon (1761), Forster (1778), Humboldt (1805), Candolle (1820), and Agassiz (1840), and later those of Sclater (1858, 1897), Raunkiaer (1904, 1934), Dammerman (1922, 1948), Elton (1927, 1958), Docters van Leeuwen (1936), Simpson (1940, 1943, 1956, 1980), Mayr (1942), Lack (1947), and Darlington (1957).
Brown and Lomolino (1989) described the early and independent development by Eugene Gordon Munroe of an equilibrium theory of island biogeography—one with predictions of species richness based on island characteristics and opposing processes of immigration, extinction, and evolution (excerpted pages of Munroe’s dissertation are available at www.biogeography.org/resources.htm). Unfortunately, he was unsuccessful in publishing his theory (outside of his 1948 dissertation, there is an abstract published in the 1953 Proceedings of the Seventh Pacific Science Congress, and a paper published in The Canadian Naturalist [Munroe 1963, pp. 304–305], which included a brief summary of his equilibrium theory), so there is no evidence that this work directly contributed to MacArthur and Wilson’s development of their theory. This episode of multiple discoveries in the history of science (sensu Merton [1961]) does, however, demonstrate the reticulating nature of island theory and that nearly all the requisites for an equilibrium theory of island biogeography were available over a decade before MacArthur and Wilson’s seminal collaboration.
Nearly simultaneously with the completion of Munroe’s dissertation, Karel Willem Dammerman published his comprehensive classic comparing the faunal dynamics of Krakatau to those of two continental islands (Durian and Berhala) and two oceanic islands (Christmas and Cocos-Keeling). While, as Thornton (1992) noted, Dammerman actually used the term “equilibrium,” his extensive and meticulous account of the fauna of these islands was almost purely descriptive, lacking any attempt at a conceptual synthesis of underlying, causal processes. Rather, his goal was to develop a detailed and comprehensive description of the faunas inhabiting these islands and to explain why certain species but not others were successful at colonizing these environments (Dammerman 1948, p. vii). He did attribute variation in number of species among islands, again not the focus of his monograph, to proximate factors including island isolation, island size, tropical versus arctic climates, elevation, topographic relief, and development and variety of the vegetative communities (described by Docters van Leeuwen 1936), but his concept of “equilibrium” is mentioned only in brief and only in a phenomenological sense. That is, he used this term to characterize the apparently asymptotic slowing of species accumulation on certain islands, but said nothing about a possible balance among opposing processes. Thus, his concept of equilibrium was more similar to that envisioned by John Willis (1922, p. 229) and later by David Lack (1947, 1976), with islands accumulating species until all ecological space was filled (perhaps also presaging Wilson’s [1959, 1961] concept of ecological “saturation” of islands).
Interestingly, early publications and insights from studies of the faunal dynamics of Krakatau had no obvious impact on Munroe’s development of his equilibrium theory (Munroe 1948 and 1953; personal communication to MVL, 2007), which may be somewhat understandable given that Dammerman’s book was not yet published, and that Munroe’s field research focused on the biota of a different and distant part of the globe (i.e., the Caribbean archipelagoes versus those of Indonesia). In contrast, reports from Docters van Leeuwen (1936), Dammerman (1948), and others studying colonization following the 1883 eruption of Krakatau provided key empirical insights for future syntheses on the subject, including those first developed by E. O. Wilson and, eventually, in his transformative collaborations with Robert MacArthur as well (see MacArthur and Wilson 1967, pp. 43–51).
Roughly one decade after Munroe developed his theory, the field would witness another confluence of ideas attempting to synthesize the encyclopedic accumulation of island patterns and existing theory. In this case, however, the synthesis was a genuine precursor to MacArthur and Wilson’s future theory—one presented in E. O. Wilson’s papers on the ecological and evolutionary development of ant communities across Melanesia, wherein Wilson described his theory of the taxon cycle (1959, 1961; see Ricklefs, this volume). While few would argue that these papers were not influential, we believe their impact on the field, in general, and on the theory MacArthur and Wilson were about to develop, in particular, may still be largely underappreciated. Indeed, careful study of Wilson’s taxon cycle papers reveals that they presented the first clear articulation of what would become the stated goal of MacArthur and Wilson’s collaboration: “to examine the possibility of a theory of biogeography at the species level” (MacArthur and Wilson 1967, p. 5). Thus, Wilson’s 1959 paper identified the concept of a biogeography of the species as being central to his theory of the ecological and evolutionary development of insular biotas.
There is a need for a “biogeography of the species” [quotes his], oriented with respect to the broad background of biogeographic theory but drawn at the species level and correlated with studies on ecology, speciation, and genetics. (Wilson 1959, p. 122)
It may well be that his theory of taxon cycles, and in particular the concept of a biogeography of the species, may again become foundational to emerging and more integrative theories of island biogeography (see our discussion in the final section of this chapter). Indeed, although the heuristic promise of the research agenda outlined in the above quotes was unappreciated by many biogeographers caught up in the “normal science” (sensu Kuhn 1994) of the 1970s and 1980s, a selection of insightful research programs continued to study the ecological and evolutionary development of insular communities as interrelated phenomena (e.g., Ricklefs and Cox 1972, 1978, Diamond 1975, 1977, Erwin 1981, Roughgarden and Pacala 1989).
6. Dynamics of nature at finer scales (from global and regional down to archipelago and island). Wilson, like Munroe before him, was strongly influenced by the theories of William Diller Matthew, George Gaylord Simpson, and Phillip J. Darlington (incidentally, Darlington provided advice to both Munroe and later Wilson during their early development as scientists). Matthew (1915), Simpson (1940, 1943, 1944) and Darlington (1938, 1943, 1957) each cogently asserted that the earth, its land and sea, its climate and its species were dynamic; with biotas expanding from their centers of origin, dispersing across new regions and then adapting, evolving and, in most cases, suffering eventual extinction depending on the vagaries of regional to global environments (views overlapping to some degree, but also in some ways contradicting those central to Willis’s [1915, 1922] age and area theory). Wilson was able to telescope Darwin and Wallace’s center of origin-dispersal-adaptation (CODA) perspective from global and geological scales down to more local spatial and short-term temporal scales. That is, his theory described the dynamic development of biotas on particular archipelagoes and islands in evolutionary and ecological time. Wilson recounted his scientific epiphany in his autobiography (1994, pp. 214–15).
It dawned on me that the whole cycle of evolution, from expansion and invasion to evolution into endemic status and finally into either retreat or renewed expansion, was a microcosm of the worldwide cycle envisioned by Matthew and Darlington. To find the same biogeographic pattern in miniature was a surprise then. . . . It came within a few minutes one January morning in 1959 as I sat in my first-floor office . . . sorting my newly sketched maps into different possible sequences—early evolution to late evolution. . . . Discovery of the cycle of advance and retreat was followed immediately by recognition of another ecological cycle. . . . I knew I had a candidate for a new principle of biogeography.
Thus, Wilson’s independent synthesis produced a “new principle”—a biogeography of the species, which was a process- and species-based theory that explained the dynamic distributions of species and the geographic variation in biodiversity among islands. Patterns in insular community structure among regions, archipelagoes, and islands were functions of the dynamics of processes operating across global and geological scales down to local and ecological ones. These processes included immigration and range expansion, evolutionary divergence and diversification, extinction, and ecological interactions; the latter affecting each of these more fundamental processes.
7. Advancing science through collaborative synthesis. Despite all its prescience and promise, the impact of Wilson’s independent synthesis developed in his taxon cycle papers was soon to be overshadowed by his future collaboration with Robert Helmer MacArthur. As noted earlier, Wilson’s theory of taxon cycles and his concept of a biogeography of the species arguably constituted an integral and precursory stage in the development of their equilibrium theory. Perhaps the most fundamental reason for the success of their collaboration is just that—it was a genuine collaboration, which melded and expanded the complementary strengths and visions of each beyond what they were capable of in their independent, albeit distinguished, research programs.
Exemplary cases of transforming science through collaborative syntheses included Watson and Crick’s legendary deciphering of the structure of DNA, achieved some ten years prior to MacArthur and Wilson’s first paper (see Watson 1968). The synergistic benefits of this and other, earlier collaborations in the natural sciences were not lost on Wilson and MacArthur, as evidenced, for example, by Wilson’s earlier collaboration with William Brown on the phenomenon of character release (one that would later be integrated into Wilson’s theory on taxon cycles; see Brown and Wilson [1956]), and those of MacArthur with his mentor, G. E. Hutchinson, and their students and colleagues (e.g., Hutchinson and MacArthur 1959, MacArthur and Levins 1964, 1967, MacArthur and Connell 1966). As Robert J. Whittaker (personal communication, 2008) observes, it seems ironic but perhaps fitting that the collaboration which contributed to the dominance of molecular biology in the 1950s and 1960s—for some time marginalizing whole-organism biology and community ecology—would be answered by the collaboration between MacArthur and Wilson, which reenergized ecology and biogeography by providing, as Whittaker puts it, a “radically updated framework for this branch of science” (see Wilson 1994, chap. 12, “The Molecular Wars”).
Rather than being satisfied with their first collaboration—the relatively focused, albeit intriguing, joint paper they published in 1963—MacArthur and Wilson were determined to develop a full-scale, integrative synthesis of island theory. At first rather humbly stated at the end of their 1963 paper, their goal was “to deal with the general equilibrium criteria, which might be applied to other faunas, together with some of the biological implications of the equilibrium condition.” But, fully realizing the revolutionary potential of their first collaboration, they had agreed by December of 1964 to once again join forces, this time to “write a full-scale book on island biogeography, with [the] aim of creating new models and extending [their] mode of reasoning into as many domains of ecology as [they] could manage” (Wilson 1994, p. 255).
In summary, the cumulative knowledge of the geography and diversity of nature and, more importantly, the deepening understanding of and ability to model the dynamics of the natural world and the underlying, scale-dependent causal processes, rendered the development of an equilibrium theory of island biogeography not only possible, but likely, if not inevitable. This appears to be a relatively common phenomenon, with the classic and best-known example in the biological sciences being the convergent and nearly simultaneous “discovery” or rediscovery of the theory of natural selection by Alfred Russell Wallace and Charles Darwin, providing some invaluable lessons on how transformative advances in the natural sciences are achieved (see also Merton’s [1961] review of episodes of multiple, independent discoveries in science).
As with other disciplines, biogeography advanced not just as a regular accumulation of facts and succession of alternative and increasingly more accurate concepts, but through syntheses and re-integrations in a reticulating phylogeny of sometimes convergent if not equivalent theories. Munroe’s independent development of an equilibrium theory, Lack’s (1947) concept of the filling of ecological space, and Wilson’s concept of “saturation” of insular biotas (as part of his taxon cycle theory), are illustrations of this phenomenon (in this case, incarnations of similar if not equivalent concepts of island biogeography). Yet these revolutionary advances in biogeography, along with its descendant disciplines of ecology and evolution, were ultimately achieved by addition of the final component in the above list of foundational elements—a genuine collaborative synthesis between two of the field’s established visionaries.
Despite some interesting and sometimes heated debate over the merits of the equilibrium model of species richness during the four decades since its initial articulation, there should be little question that MacArthur and Wilson’s theory has had a revolutionary influence on biogeography and related disciplines, and they certainly achieved one of their primary goals: “creating new models and extending [their] mode of reasoning into as many domains of ecology [and other disciplines] as [they] could manage” (Wilson 1994, p. 255).
Our purpose in this section is not to chronicle the hundreds if not thousands of studies that were stimulated by their theory: indeed, much of our own earlier research was developed to evaluate the tenets of their theory or to modify it to create other means of analyzing and understanding the ecological and evolutionary assembly of isolated biotas (Brown 1971, 1978, Brown and Kodric-Brown 1977, Lomolino 1986, 1990, 1994, 1996, 2000, Sax et al. 2002). Rather than focus here on how the theory influenced other research programs in these areas (which we believe is well covered in other chapters of this book), our purpose in the following paragraphs is to describe how the theory MacArthur and Wilson presented in their 1967 monograph was substantially transformed, at least in its predominant development and applications during the normal science (sensu Kuhn 1996) of the next two decades.
As we described earlier, the intended domain of MacArthur and Wilson’s theory was quite broad: again, in the introduction to their book, they made their ultimate goal quite clear.
The purpose of this book is to examine the possibility of a theory of biogeography at the species level. We believe that such a development can take place by looking at species distributions and relating them to population concepts, both known and still to be invented.(MacArthur and Wilson 1967, pp. 5–6)
In their conclusion (MacArthur and Wilson 1967, p. 183), they returned to this very general theme of a process- and species-based reintegration by calling for the field of biogeography to
be reformulated in terms of the first principles of population ecology and genetics . . . to deemphasize for the moment traditional problems concerning the distribution of higher taxa and the role of geological change . . . and to turn instead to detailed studies of selected species. A “biogeography of the species” [quotes theirs] requires both theory and experiments that must be in large part novel.
Despite these goals of developing a very general, species- and process-based theory—one covering not just patterns in richness, but including a host of other ecological and evolutionary phenomena (including r/k selection, niche dynamics, geometry and strategies of colonization, and evolution), the research agenda during the 1970s and 1980s seemed so captivated with the equilibrium model of species richness that it often lost sight of the broader agenda of a biogeography of the species. During this period, ecological biogeographers became intrigued with the abilities to model species as though they were “atoms in a gas law context” (personal communication, R. Ricklefs 2008): the very general theory could be recast in a more narrow sense—as a model of how richness of equivalent, noninteracting, and nonevolving species varies with island area and isolation (“mere curve-fitting,” sensu Haila [1986]; “a numbers game” sensu Whittaker [1998], Whittaker and Fernandez-Palacios [2007]). As we noted earlier, the heuristic promise of Wilson’s theory of taxon cycles and a biogeography of the species was not lost on everyone, as a group of distinguished ecologist and biogeographers continued to pursue and develop these concepts throughout this period. Eventually, their insights would be integrated into a set of now emerging theories that promise to provide some genuinely transformative advances in island theory (see other chapters in this volume, and the final sections of this chapter).
As Stuart Pickett and his colleagues explain in their important book Ecological Understanding: The Nature of Theory and the Theory of Nature, theories are far from static, but typically if not invariably undergo an ontogeny of their own (Pickett et al. 2007; see also Kuhn 1996). Most theories are first described in a premature form, well before the requisite knowledge and conceptual tools necessary to fully appreciate and develop their potential import. Wegener’s (1912a, 1912b, 1915) theory of continental drift—first proposed some five decades before the scientific community fully embraced it—is one of the most striking cases of delayed acceptance of a truly prescient and potentially transformative theory in natural science. Early articulations of equilibrium concepts by Munroe, and of Wilson’s theory of taxon cycles and his concept of species saturation and a biogeography of the species, represent similar episodes of unappreciated prescience in biogeography. By the time MacArthur and Wilson collaborated to develop their theory, however, the empirical and conceptual foundations of island biogeography, and in particular the abilities of scientists to visualize and model dynamic processes, had progressed to the point that a genuinely paradigmatic advance could be achieved and widely appreciated.
The ontogeny of MacArthur and Wilson’s equilibrium theory weaves a tapestry whose fabric and modified forms are just beginning to become clear after four decades of maturation and retrospection. One perhaps key factor, which was actually lacking from its subsequent development, was the continued involvement of its creators. Tragically, MacArthur died of renal cancer just five years after he and Wilson published their monograph. Wilson conducted some fascinating experiments in island biogeography in the late 1960s, again a collaboration (this time with his distinguished student—Daniel Simberloff (see Simberloff, this volume), but Wilson’s interests and energies soon turned to other demanding and highly successful endeavors, including evolutionary biology, sociobiology, and conservation of biological diversity. The subsequent period of over three decades of the theory’s maturation, then, were left to a rapidly growing community of biogeographers and ecologists, including critics as well as champions.
While it may appear that the theory’s subsequent development can be characterized by an expansion of the domain of its applications (e.g., application of the equilibrium model of species richness to a broad diversity of isolated ecosystems, including lakes, mountaintops, and other patches of terrestrial ecosystems, as clearly anticipated by MacArthur and Wilson [1967, pp. 3–4]; see Pickett et al. 2007, p. 104), we believe that just the opposite has occurred at least in terms of the theory’s conceptual domain. According to Yrjö Haila, during the 1970s and 1980s the theory suffered a “reification” (sensu Levins and Lewontin 1980) with an increasingly more narrow focus on species richness correlations and on the explanatory performance of the iconic, equilibrium model, with an apparent waning of appreciation for the broader value of “the theory as a research programme that directs attention to the dynamic nature of island communities in general, and to mechanisms that determine the colonization process in specific situations” (Haila 1986, p. 379; see also Sismondo 2000). A review of MacArthur and Wilson’s monograph, including the various excerpts included above which described their stated goals, makes it clear that the equilibrium model of species richness was just one component (albeit one of the most central, compelling, and easiest to visualize and remember) of their attempt to develop a truly comprehensive theory of island biogeography (“a biogeography of the species,” again, first articulated by Wilson in his original, taxon cycle paper of 1959).
Contraction in the conceptual domain of MacArthur and Wilson’s theory (at least as practiced by many biogeographers through the 1970s and 1980s) was symptomatic of concurrent specialization and splintering across the very broad domain of biogeography itself, including widening divisions between, as well as within, ecological and historical biogeography. We are, however, encouraged by the more recent groundswell of biogeographers now calling for a reexpansion in the domain of island theory and a reintegration of the field (e.g., Brown and Lomolino 2000, Brooks 2004, Brown 2004, Lieberman 2004, Lomolino and Heaney 2004, Riddle and Hafner 2004, Ebach and Tangney 2007, Stuessy, 2007; see also chapters in this volume, especially those by Grant and Grant, by Whittaker et al., by Losos and Parent, and by Ricklefs). We agree that this can best be accomplished by developing more integrative theories of island biogeography—those that encompass the full breadth of patterns in geographic variation among insular biotas, and are based on the premise that those patterns result from predictable variation in the fundamental biogeographic processes among islands and species, and across scales of space, time, and biological complexity.
Here we outline the fundamental components of one approach for developing theories that may advance the field through consilience and integration in order to achieve a new biogeography of the species, i.e., a process- and species-based explanation for the very broad diversity of interrelated patterns and underlying processes affecting insular biotas. First, we describe the conceptual domain of an integrative theory of island biogeography, and then list the tenets that are fundamental to this approach and, in combination, requisite to a genuinely transformative advance in the field. We then conclude with a case study illustrating how two apparently disparate phenomena (patterns of insular distributions and those of microevolution on islands) can be more fully understood within the context of the same, integrative theory.
Integration not only provides a means of expanding the variety of phenomena studied, but also provides us with a means of better understanding the causal nature of intriguing and interdependent phenomena, given that each is influenced by processes that operate across interdependent domains of space, time, and biological complexity. For example, interactions among species not only influences their abundance and distributions at local scales, but can strongly influence fundamental biogeographic processes, thus modifying patterns in distributions, diversity, and distinctiveness at regional to global scales as well.
The conceptual domain of an integrative theory of island biogeography should include a broad diversity of patterns in geographic variation in the characteristics of insular individuals, populations, and communities. One fundamental premise of this theory is that these patterns result from the regular and predictable variation among islands and among species in characteristics that influence the fundamental biogeographic processes—immigration, extinction, and evolution. That is, the fundamental capacities of species (to immigrate to islands, and survive and evolve there) should vary in a nonrandom manner among species (e.g., when those species are ordered by body size or energetic requirements), while rates of immigration, extinction, and evolution of those species should vary in a nonrandom manner among islands (e.g., when islands are ordered by area, isolation, primary productivity, or carrying capacity). Therefore, the successful integration, or reintegration, of island theory will depend on our abilities to evaluate the generality and validity of its fundamental tenets (described in the next section), to further develop its integration with theory in other domains of science, and to assess its potential applications for conserving the evolutionary and geographic context of isolated biotas (see Haila 1986, p. 385).
Among the most valuable approaches for discovering and understanding patterns emergent across multiple scales of space, time, and biological complexity are those developed by macroecologists (see Brown 1995, Gaston and Blackburn 2000). Thus, macroecology may well provide a useful conceptual and analytical framework for reintegration across the broad domain of island biogeography theory (sensu latissimo; i.e., all patterns in geographic variation among insular biotas). Below, we list and briefly describe seven tenets and conceptual elements that seem requisite to integrative theories of island biogeography. Taken separately, none of the assertions described in the following list is revolutionary, but in combination they comprise a conceptual framework that has much promise for achieving the species- and process-based theory at the core of Wilson’s biogeography of the species.
1. The relative importance of each of the fundamental biogeographic processes (immigration, extinction, and evolution) and of ecological interactions varies in a predictable manner across spatial and temporal scales and among species. For example, the relative importance of evolution in terms of its influence on patterns of diversity and distinctiveness among insular biotas likely increases as we consider broader spatial and temporal scales (e.g., archipelagoes spanning greater degrees of isolation and those including larger islands (figure 2.1); see also Lomolino 1999, 2000, Heaney 2000, Losos and Schluter 2000, Whittaker 2004, Whittaker et al. 2008).
2. Island biogeographic patterns result from both independent and interactive influences of immigration, evolution, and extinction, which should be functions of the system (island and archipelago) and species traits affecting those processes (see tenets 3 and 4, respectively). Distributions of particular species among islands, in turn, should be functions of their immigration capacities relative to their abilities to maintain populations on those islands: i.e., populations of a focal species are most likely to occur on those islands where conditions (e.g., isolation and area) are such that the probability of immigration by that species is high relative to its likelihood of extirpation following colonization of that island (figure 2.2). A species can inhabit even the most isolated islands of an archipelago if those islands are relatively large (such that extirpation probabilities for its populations are compensatorily low). Similarly, evolutionary divergence is also dependent on the combined effects of these processes—being most prevalent on those islands that are both isolated and large, such that gene flow is relatively low and persistence times and within-island barriers (e.g., major rivers and mountain chains) provide the requisite conditions for divergence among and within large islands (e.g., see Wagner and Funk 1995, Heaney 2000, Losos and Schluter, 2000).
3. System traits of primacy. Most important among the geographic or system variables influencing the fundamental biogeographic processes and feedback mechanisms (listed in tenet 7, below) are
• area, isolation, topographic relief, age and disturbance history of the islands, and
Figure 2.1. Scale dependence of the biogeographic and ecological processes (Immigration, Extinction, Evolution; Ecological Interactions, and Ecological Release) influencing community structure of insular biotas: here placed within the geographic context of two principal characteristics of island ecosystems (Area and Isolation). Because immigrations and extinctions of nearly all species in the focal biota are so frequent at relatively fine scales (i.e., on islands < Inear and Asmall), community structure on these islands tends to be driven by stochastic events, which produce apparently random assemblages of species, with richness and species composition varying independent of island isolation and area (i.e., the near-island effect, and the small-island effect [see MacArthur and Wilson 1967, pp. 30–32; Lomolino and Weiser 2001], respectively). On somewhat more isolated and larger islands, the structure and dynamics of insular communities should approach those envisioned by MacArthur and Wilson’s equilibrium model, although differences in immigration abilities and resource requirements among the species may result in non-random assemblages of communities on these islands (e.g., producing community nestedness across gradients of isolation and area [see Darlington 1957, p. 485, figure 57, Wilson 1959, p. 128, figure 2, Patterson and Atmar 1986, Lomolino 1996]). On islands that are very isolated and very large with respect to immigration abilities and resource requirements of most species in the focal biota (i.e., on islands > Ifar and Alarge), evolution becomes an important force influencing the diversity and distinctiveness of their communities (see Losos and Schluter 2000). Finally, the relative importance of ecological interactions and ecological release varies with diversity of insular communities (shown here as a gradient of decreasing shading from species-rich to depauperate islands; note that speciation within isolated archipelagoes comprised of relatively large islands [top, right-hand corner of the figure] can promote relatively high diversity as well as endemicity). Note also that the effects of geological dynamics of the islands (Whittaker et al. 2008) are not included in this version of the model.
Figure 2.2. The insular distribution function (dashed line) can serve as a fundamental level in an integrative and hierarchical approach to island biogeography theory, providing a means of placing a diversity of patterns of variation among insular biotas within a geographic context (here, as described by island area and isolation). The insular distribution function is essentially a constraint line (sensu Brown 1995), whose slope and intercept should vary in a predictable manner with characteristics of the archipelagoes (tenet 3) and focal species (tenet 4; see explanation in the text; see also Lomolino 1986, 1999, 2000, Hanski 1986, 1992, and this volume).
• latitudinal position, and nature of the immigration filters (characteristics of the intervening seascapes) of the archipelagoes.
These correlates of biogeographic variation among islands have been discussed throughout the history of the field, from the early studies of Forster (1778), through those of Darwin and Wallace, to current research in all aspects of island theory (see Lomolino et al. 2006, chapters 13 and 14, Whittaker and Fernandez-Palacios 2007).
4. Species traits of primacy. Most important among the species traits influencing the fundamental processes and capacities of species (i.e., their immigration abilities, and their abilities to survive, evolve, and dominate other species on islands) are those that most strongly influence resource requirements and how those resources are utilized for dispersal, survival, and ecological interactions, and are transformed into offspring. In animals, most important among these traits are body size, bauplän (i.e., the body plan common to particular groups of organisms, including such features as the degree of symmetry, specialization among body segments, or number of limbs) and trophic strategy (e.g., foliage gleaning insectivore, grazing herbivore, or cursorial, top carnivore). For plants, traits of primacy likely include size of gametophyte or sporophyte, growth form (e.g., epiphytic, herbaceous, shrub, or tree), propagule dispersal mechanisms, and principal energetic and metabolic pathways (e.g., parasitic, nitrogen fixing, C3, C4, and CAM).
5. Among systems. Along with exhibiting predictable patterns of variation along geographic gradients (e.g., along those of increasing area, isolation, or latitude), the fundamental processes also exhibit significant covariation among islands and archipelagoes. For example, larger islands may experience more immigrations (the target area effect; Gilpin and Diamond 1976, Hanski and Peltonen 1988, Lomolino 1990), fewer extinctions (Macarthur and Wilson 1963, 1967), and a greater degree of evolutionary divergence (e.g., see Lomolino et al. 2006, figure 14.19a, after Mayr and Diamond 2001); archipelagoes located in higher latitudes may experience fewer immigrations (except when those waters freeze over; Lomolino 1988, 1993), lower persistence times (due to lower ambient temperatures, productivity, and carrying capacities), and lower rates of evolutionary divergence (due to the decelerating effects of cooler temperatures on life history processes) (Rohde 1992, Cardillo 1999, Allen et al. 2002, Brown et al. 2004, Wright et al. 2006).
6. Among species. Given that natural selection operates on combinations of interdependent traits which comprise entire organisms, then the fundamental capacities of insular biotas (abilities to colonize, survive, dominate other species in ecological interactions, and evolve on islands) should exhibit significant covariation among species. For example, along a gradient of increasing body size of vertebrates, vagilities (for active immigration), resource requirements (and therefore their susceptibility to extirpation), and abilities to dominate other species in ecological interactions should increase, while rates of evolutionary divergence should decline (Lomolino 1989, 1985, 1993, McNab 2002, Millien 2006, Millien and Damuth 2004, Millien et al. 2006). In invertebrates, while resource requirements, ecological dominance, and evolutionary rates may exhibit similar trends, pagility (capacity for passive immigration) of at least some species groups (e.g., land snails; Vagvolygi 1975) may actually decline with increasing body size.
7. The generality of biogeographic patterns and the interdependence among underlying, fundamental processes are affected, and possibly enhanced by three important feedback mechanisms.
a. Ecological interactions among species, which can influence each of the fundamental capacities of other species (i.e., their abilities to immigrate to, and survive and evolve on, islands). Included here are well-demonstrated effects of competition (Brown and Wilson 1956, Grant 1968, 1971, 1996, 1998, Crowell 1962, Grant and Grant 2007 and their chapter in this volume, Losos and Queiroz 1997), predation (e.g., Lomolino 1984, Schoener et al. 2001, Schoener et al. 2002), parasitism (Apanius et al. 2000, Fallon et al. 2003), mutualism, commensalism, and succession driven by prior colonists (Thornton 1996, Whittaker et al. 1989) on immigration, establishment and extinction of insular plants and animals
b. Microevolution, which can substantially alter life histories and fundamental capacities of species. Perhaps most striking among these insular phenomena are the innumerable and intriguing cases of evolutionary divergence associated with reduced dispersal abilities of insular forms, including the development of flightlessness in thousands of species of insular invertebrates and birds (McNab 1994a,b, 2002, Steadman 2006) and reduced capacities for flight and enhanced terrestrial nature in many other species (e.g., the short-tailed bats of New Zealand—family Mystacinidae), and reduced dispersal mechanisms, and increased woodiness and arboreal growth forms in otherwise herbaceous plants (Carlquist 1974, Givnish 1998).
c. Macroevolution (speciation), which can strongly influence patterns in diversity and distinctiveness among insular communities. This is another scale-dependent process (tenet 1; figure 2.1) and, because it influences fundamental properties of insular communities (i.e., the number and types of species), it can have cascading effects by influencing each of the other fundamental biogeographic processes (immigration and extinction) and the above feedback mechanisms (ecological interactions and microevolution) as well (see Emerson and Kolm 2005). Where important (i.e., on very large and very isolated islands), macroevolution can play a predominant role in determining the structure of insular biotas, creating hotspots of diversity and distinctiveness rivaling and in some cases exceeding those of the richest mainland communities (e.g., mammals of the Philippines [Heaney 2004, Heaney and Regalado 1998]; ferns, drosophilids, snails and honeycreepers of Hawaii [Wagner and Funk 1995]; asters and Anolis lizards of the Caribbean [Losos and Schluter 2000, Losos and Thorpe 2004, Francisco-Ortegal et al. 2008]; cichlids of Africa’s Rift Valley Lakes [Meyer 1993]).
Transformative advances in science are often achieved by novel approaches for visualizing fundamental, underlying processes and their variation across scales (in this case, those of biogeographic, evolutionary, and biological complexity). Following MacArthur and Wilson’s (1967) exemplary graphical models, the developments in the field of macroecology also provide some compelling demonstrations of the utility of these transitional-scale models, or “macroscopes” (Brown 1995, Gaston and Blackburn 2000). Here, we utilize such graphical models to demonstrate how two sets of what have traditionally been viewed as intriguing but unrelated phenomena—ecological assembly (distributional patterns) and evolution of insular body size—can be better understood within the context of a more integrative approach to island biogeography theory.
As we pointed out earlier, the graphical model of insular species distributions illustrated in figure 2.2 can serve as a geographic template for integration among the scale-dependent processes influencing the ecological and evolutionary development of insular biotas (tenets 1 and 2). Lomolino (1999, 2000) presented an earlier version of this approach to island biogeography theory, which was hierarchical but also species-based because it was premised on the assumption that many patterns in assembly of insular communities derive from predictable variation among their focal species. Again, we are assuming that insular distributions of each focal species are functions of the combined effects of immigration and extinction (tenet 2). Therefore, islands whose coordinates (isolation and area) fall above the dashed constraint line (the insular distribution function) of figure 2.2 are more likely to be inhabited by the focal species. Elsewhere, we have shown how variation and covariation among important system and species traits (tenets 3–6) and ecological interactions among insular populations (tenet 7a) can be integrated into this hierarchical approach to explain ecological assembly and geographic variation among insular biotas (including intra- and interarchipelago patterns in species richness and species composition; see Lomolino 2000, figures 3–5, 9–11; see also Simberloff and Collins, this volume). Here, we demonstrate how evolutionary divergence among insular populations (tenet 7b) can be added to the theory to explain some intriguing insular patterns—in this case, the truly remarkable phenomenon of body size evolution on islands.
The “island rule” describes a graded trend away from norms of body size observed in species-rich, continental environments, such that on islands small species exhibit gigantism, whereas large species exhibit dwarfism (figures 2.3a and 2.3b). We describe this as a “graded” trend because the tendency toward gigantism or dwarfism declines as we move from species of extreme to those of more modal size.
The generality of the “rule” is, of course, not universal but still surprising given that it is now reported not just for terrestrial, nonvolant mammals (as in its original articulations by Foster [1964] and modifications by Van Valen [1973], Heaney [1978], and Lomolino [1985]), but also for a broad diversity of vertebrates and invertebrates (see reviews by Lomolino 2005, and Lomolino et al. 2006; see also Meiri et al. 2004, 2007, 2008a,b, Meiri 2007, Price and Phillimore 2007). Other reports of patterns consistent with the island rule include those for groups as varied as recent, deep-sea gastropods (McClain et al. 2006), Pliocene-Pleistocene ungulates (figure 2.3b), sauropod dinosaurs (Jianu and Weishampel 1999, Sander et al. 2006), and Pleistocene hominins (Brown et al. 2004, Morwood et al. 2004, Morwood 2005).
Figure 2.3. (Top) Body size trends for insular mammals. Si = relative size of insular forms expressed as a proportion of body mass of their mainland relative (see Lomolino 1985, 2005). (Bottom) Antiquity of the island rule: body size trends for ungulates and “elephants” (orders Artiodactyla, Perisodactyla, and Proboscidea) of Mediterranean islands during the Pliocene and Pleistocene (reanalysis of data from Raia and Meiri [2006], Raia [personal communication 2008]; body mass estimates from Palombo [personal communication 2008]). Si = insular body size as proportion of body size of the mainland population (as linear dimensions of metatarsus, metacarpal, humerus, or tibia).
On the other hand, some species groups appear anomalous or at least equivocal with respect to the patterns predicted by the island rule, and all show substantial variation about the general trendlines of figure 2.3 (i.e., beyond that accounted for simply by ancestral body size). This residual variation is at least partly a function of the fact that this relatively simple model does not take into account variation in key traits of the islands (tenet 3) or focal species (tenet 4), nor does it consider the possible effects of covariation (tenets 5 and 6) and feedback (tenet 7) among biogeographic processes. Yet, as we asserted above, at least some of these shortcomings can be addressed by using the model of scale dependence (figure 2.1) and the insular distribution function (figure 2.2) to place these evolutionary patterns in an ecological and geographic context. Our goals in this section are, therefore, threefold:
1. to provide an explanation for the island rule which is based on the tenets of the general theory, described above,
2. to place this explanation within the context of the geographic template provided by insular distribution functions, and
3. to explain some apparently anomalous trends in insular body size, including the tendency for carnivorous mammals to exhibit equivocal patterns (figure 2.4) and for rodents to exhibit dwarfism on some very disparate islands—i.e., on nearshore and on oceanic islands (in the latter case, with dwarfed elephants), but not on those of intermediate isolation.
As the Indonesian paleobiologist, Dirk Albert Hooijer observed in a paper published the same year as MacArthur and Wilson’s classic monograph, “wherever we find elephants we also have giant rodents. . . . we have no means of knowing how many generations were involved, it is, however, likely that evolutionary velocity has been higher under these conditions than is usual” (Hooijer 1967, p. 143).
Consistent with the tenets of an integrative theory of island biogeography, the explanation for the island rule featured here centers on the scale dependence of fundamental, causal processes (tenets 1 and 2)—in this case, how they vary between insular and mainland environments, among islands within the same archipelago, and among species. Body size influences all physiological process and life history characteristics of animals (Calder 1984, McNab 2002), in turn producing some very regular patterns of variation and covariation among the fundamental capacities of organisms (tenet 6); i.e., in their abilities to immigrate to islands, and survive, evolve, and dominate other species in ecological interactions there. The result is that there may be an optimal size (associated with an optimal combination of fundamental traits and capacities) for organisms with a given bauplän and trophic strategy (represented by the shaded triangle in figure 2.5). This optimum, however, should vary with characteristics of the insular environments that influence fundamental capacities of the species (i.e., with isolation, latitude, and area of the islands, affecting immigration, survival, and evolution; tenets 2, 3, and 4), and with diversity and species composition of particular insular communities, affecting ecological interactions (tenet 7a), which in turn drive niche and character dynamics (tenet 7b; Brown and Wilson 1956). Thus, in species-rich mainland communities, pressures from a diversity of predators and competitors should cause the optimal size of particular species to differ from that of the entire taxon or species group (again, as identified by similar baupläne and trophic strategies).
Figure 2.4. Body size of insular carnivores (Mammalia, Carnivora). It exhibits substantial variation about the trend, although the relationship appears to be statistically significant (P [one-tailed test that the slope is not < 0.0] is < 0.05) and in the direction consistent with the island rule (after Lomolino’s [2005, pp. 1684–85, figure 2] reanalysis of Meiri et al’s [2004] data; see also Price and Phillimore [2007]). Si is body mass of insular populations expressed as a proportion of that of their mainland relatives.
Figure 2.5. An explanation for body size evolution of insular vertebrates (i.e., the island rule). It is based on how selective pressures and fundamental capacities of species (to immigrate to, and survive, evolve, and dominate other species in ecological interactions on islands) varies with body size of their ancestral forms (see explanation in the text along with that in Lomolino [1985, 2005], Lomolino et al. [2006], and references therein).
A corollary of tenet 1, and one central to the explanation for the island rule presented here, is that relevant selective pressures vary in their importance in a predictable manner among species of different body size (figure 2.5; right-hand column of figure 2.6). Thus, insular populations of small species often increase in body size on ecologically simplified islands (i.e., in the absence of larger competitors and predators), converging back on the optimal body size for that species group (again, as determined by common bauplän and trophic strategy; figure 2.6). This trend toward gigantism in otherwise small species may also be reinforced by immigrant selection (selection for the larger, and consequently more vagile, phenotypes during active immigration), which should be most intense in the smaller species (see descriptions of “immigration selection,” sensu Lomolino [1984, 1985, 1989]; and the equivalent phenomenon of selection for “thrifty genotypes” in Polynesians, sensu Bindon and Baker [1997]). Typically large species, on the other hand, are less challenged by the physiological demands of immigration, but more limited in their abilities to obtain adequate resources to maintain populations on all but the very large islands. In addition, large species are also influenced by ecological interactions in species-rich systems. Indeed, deer, hippos, elephants, and other large vertebrates may have originally evolved their massive size in response to intense ecological pressures of mainland communities (i.e., to outcompete smaller, more specialized competitors, and to escape predators by “outgrowing” them). Once these ecological pressures are removed, such as what occurs on species-poor islands, species of extreme size should tend to converge on the hypothesized optimum for that functionally defined group of species (shaded triangles in figures 2.5 and 2.6).
Figure 2.6. A general explanation for body size evolution in populations of insular animals. It is based on the assumptions that there is an optimal body size for a functional group of species (as defined by their bauplän and trophic strategy), that ecological interactions (in mainland and other species-rich communities) cause the optimal size for each species to be different from that of the group, and that selection pressures associated with geographic and ecological gradients (normal and gray italics font, respectively) vary in a predictable manner with body size of the species (right-hand column).
The conceptual model in figure 2.6 also provides novel sets of predictions regarding the island rule. First, it explicitly adds a temporal component to the island rule, by suggesting that the length of time a species is on an island will influence the degree of dwarfism or gigantism it has developed. To date, this has not been an important consideration in the study of the island rule because most focal species have presumably been present on islands long enough for their trajectory in body size to have either been completed or to be near completion. The situation has changed, however, because species under study now include those introduced onto oceanic islands during periods of historic colonizations by Europeans, imperiled species purposely translocated onto islands (e.g., the small offshore islands of Australia and New Zealand), and species that persist within islandlike (i.e., heavily fragmented, smaller, and ecologically simplified) remnants of their native range. Indeed, recent evidence suggests that patterns consistent the island rule can manifest quickly (e.g., changes in body size of introduced mice on off-shore islets of New Zealand [King 2005] and by mammals and birds inhabiting heavily fragmented remnants of their native habitats in Denmark [Schmidt and Jensen 2003, 2005]). Thus, the temporal component of the island rule is likely to become a larger focus of research in the future (Lomolino et al. 2006). Second, the conceptual model (figure 2.6) predicts that the degree of change in body size attained by a focal organism (regardless of whether it is toward gigantism or dwarfism) is dependent on the geographic and ecological characteristics of the particular islands it inhabits (especially island area and isolation, and diversity of predators and competitors). Thus, much of the residual variation about the general trendline describing the island rule may be explicable once the characteristics of insular ecosystems are taken into account.
Third and most importantly, this conceptual model provides a general explanation for what seemed to be unrelated and sometimes contrary patterns (gigantism in some species, dwarfism in others), and across a broad range of functional groups and taxa (e.g., mammals, reptiles and invertebrates; terrestrial and aquatic species, both recent and extinct). We can, however, explain an even broader diversity of related patterns, including some apparent anomalies, if we overlay the causal models of body size evolution (figures 2.5 and 2.6) onto the geographic template of insular distributions (figure 2.2). As figure 2.7 reveals, once put in this context, the island rule emerges as not just one, but a set, of complementary patterns which vary depending on the species and the archipelagoes in question. Here, we generate insular distribution functions for three sets of species (small mammals, mesocarnivores, and large herbivorous mammals) by assuming a particular pattern of covariation in fundamental capacities of the species (tenet 6). In this case, we are assuming that larger species will tend to have greater vagilities and greater resource requirements (translating into lower slopes but higher intercepts of their insular distribution functions), which is reasonable and well evidenced at least for actively immigrating mammals (and likely other vertebrates as well; see Lomolino 1989, 1999, 2000; see also Calder 1984, McNab 2002).
Figure 2.7. The geographic and ecological context of the island rule: body size evolution of insular animals placed within the context of an integrative theory of island biogeography. See figures 2.1, 2.2, 2.5, and 2.6; dashed lines = insular distribution functions of three sets of species—small rodents, meso- to large carnivores (e.g., large canids, felids, and ursids), and large herbivores (e.g., ungulates and proboscideans; species present [“+”] above these constraint lines). The region marked with the asterisk delineates islands that are likely to lack meso- to large carnivores because, although within their immigration capacities, these islands are probably too isolated or too small to support persistent populations of their prey (rodents and large mammals). Note: the effects of in situ speciation (which would be most important on the very large and isolated islands) are not included in this version of the model.
This geographically and ecologically more explicit, process- and species-based model (figure 2.7) explains why these microevolutionary trends are not universal, but should vary in a predictable manner among species (differing in their original body size and in their fundamental capacities) and among islands (varying in area, isolation, and other factors influencing accessibility, carrying capacity and diversity of competitors and predators). As figure 2.7 illustrates, species such as small mammals should exhibit gigantism only on islands that they can colonize (either as active immigrators or as waifs) and where larger competitors and predators are likely to be absent (i.e., on relatively small, near islands for the active immigrators, and on larger but relatively isolated islands for the waifs. On the other hand, typically large mammals (e.g., deer, hippos, and elephants) should exhibit dwarfism only on the very large and isolated islands, which lack the mesoherbivores and carnivores that likely contributed to selection for their large size on the mainland in the first place (see Palombo 2001, 2005, Palombo et al. 2005, Raia and Meiri 2006). Thus, isolated islands—the evolutionary arenas for both the titanic and the Lilliputian marvels—are often inhabited by a depauperate but predictable assemblage of species; frequently dominated by large rodents and relatively small deer, hippos, or elephants, but lacking carnivorous mammals.
The inferences from this model with respect to body size evolution of insular carnivores are especially interesting. Central to this explanation for the island rule (figures 2.5 and 2.6) is that insular populations of extreme size will undergo gigantism or dwarfism on ecologically simplified islands, converging on an intermediate and presumed optimal size. Given the requirements of being carnivorous, however, those mammals are less likely to be of extreme size and seldom should they be able to maintain their populations on ecologically depauperate islands (i.e., those that by definition lack persistent prey populations) for periods required for substantial evolutionary divergence in body size. Indeed, although predators may repeatedly colonize such islands, we expect that either their residence will be ephemeral (because their predation—unchecked in species-poor systems—often leads to predatory exclusion of their prey and, in turn, collapse of their own populations as well; see Lomolino 1984, Schoener et al. 2001, 2002) or their diets will shift toward prey more readily available in insular environments (e.g., sea birds, fish, shoreline invertebrates, and carcasses of marine mammals; see Goltsman et al., 2005, pp. 406, 412). Given this catch-22 of being an insular carnivore, it is surprising, at least in retrospect, that there actually is a signal consistent with the island rule for such species (figures 2.3a and 2.4; the inferred significance of statistical analyses of this pattern depends on which measure of body size is used [that of skulls or teeth], whether the data include carnivores of extreme size and populations inhabiting very large, mainlandlike islands [e.g., Borneo, Sumatra, Great Britain, and Java], and whether the results are evaluated under the constraints of a one-tailed or two-tailed test; see Lomolino’s [2005, pp. 1684–85, figure 2] reanalysis of Meiri et al.’s [2004] data; see also Price and Phillimore 2007, Meiri 2007, Meiri et al. 2007). Meiri et al.’s (2008b) recent studies of body size of Borneo’s mammals are especially relevant to this hypothesis regarding the influence of large carnivores, resource requirements, and ecological release on body size evolution. They report a graded trend toward increased dwarfism in otherwise large (> 100 g) Bornean mammals (figure 2.8), being consistent with the island rule and presumably a function of the absence of large predators (e.g., tigers [Panthera tigris], leopards [P. pardus], and saber-toothed cats [Hemimachairodus zwierzyckii]) on this island at least since the early Holocene.
Figure 2.8. Body size trends of mammals from the island of Borneo. They exhibit a graded trend toward increased degree of dwarfism with increased ancestral body size, consistent with the island rule. Si is body size of insular populations expressed as a proportion of that of their mainland relatives (expressed as mass equivalents by comparing cubed linear dimensions; comparing condylobasal length of skulls of insular forms to that of the largest skulls of that species in the region (data from Meiri et al. 2008b).
Just as immigration, evolution, and extinction produce reticulated histories of biotas (Brooks 2004, Lieberman 2004) that colonize new regions and diverge in isolation, only to suffer eventual range collapse and extinction or reinitiate the cycle by colonizing other regions (including those of their ancestors), the natural sciences develop in an analogous fashion. The reticulating phylogeny of island theory weaves a complex web of early discoveries and articulations of new theories, followed by expansions and contractions in their conceptual domains, replacements by competing theories, or synthesis and reintegration with innovations from other relevant disciplines. Thus, the developmental history of island biogeography, and in particular the equilibrium model, provides invaluable lessons; not just on how MacArthur and Wilson achieved their paradigmatic masterpiece, but on how today’s biogeographers can once again transform the field. We are encouraged by the recent efforts of our colleagues, including the distinguished contributors to this volume, to provide such fundamental advances—not by derision of competing scientists and disproof of their ideas, but by genuine consilience and collaborative syntheses of complementary theories and insights to achieve a more comprehensive understanding of the ecological and evolutionary development of isolated biotas.
We thank Jonathan Losos and Robert Ricklefs for their invitation to participate in the symposium and contribute to this book, and we thoroughly enjoyed the opportunity to interact with other participants and colleagues in attendance. Jonathan Losos, Robert Ricklefs, Robert J. Whittaker, Michael Willig, and an anonymous reviewer provided numerous helpful comments, and Maria Rita Palombo provided data on body size of Mediterranean mammals during the Pleistocene.
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