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What does the ‘Lilliput Effect’ mean?
Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 4–10
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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / p a l a e o
What does the ‘Lilliput Effect’ mean? Peter J. Harries ⁎, Paul O. Knorr Department of Geology, University of South Florida, 4202 E. Fowler Ave., SCA 528, Tampa, FL 33620-5201, USA
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Article history: Received 25 April 2007 Received in revised form 10 October 2007 Accepted 15 August 2009 Available online 9 September 2009 Keywords: Lilliput Effect Mass extinction Size change Recovery Cope's Rule
a b s t r a c t The ‘Lilliput Effect’ represents a pronounced reduction in the size of the biota associated with the aftermath of mass extinctions. Although there is empirical evidence that suggests that it may be a common pattern during the recoveries from various mass extinction events, it remains to be analyzed in more detail to understand how pervasive the trend is from temporal, spatial, and taxonomic perspectives. The ‘Lilliput Effect’ could represent dynamics associated with or important diversions from a variety of biologic ‘rules’, such as Cope's and Bergmann's, governing size changes. Furthermore, there are a variety of possible patterns that could produce the ‘Lilliput Effect’ including: 1) the survival of small taxa; 2) the dwarfing of larger lineages; and 3) the evolutionary miniaturization from larger ancestral stocks. Finally, an interdisciplinary approach, involving stratigraphy, phylogenetics, and sclerochronology, is necessary to better understand the ecologic and evolutionary underpinnings of the ‘effect’. This approach needs to be more uniformly applied to different extinctions and taxonomic groups, allowing a more effective comparison and resulting in a more holistic perspective on the ‘Lilliput Effect’. © 2009 Elsevier B.V. All rights reserved.
1. Introduction One of, if not the most ubiquitous trend(s) seen in the evolutionary history of many lineages across a wide taxonomic spectrum are size changes. Because changes in size are so readily recognized, they have provided the fundamental data for attempts to develop various biological/evolutionary ‘rules’ and ‘laws’ — reflecting biology's aim to match the apparent simplicity of reductionist explanations provided by the more physical, rather than historical, scientific disciplines. To a degree, the search for biotic laws reflects the desire of biologists to develop a series of concepts, comparable to those developed for other disciplines, such as physics and chemistry, which broadly explain fundamental aspects of the physical world. The biotic dynamics during the initial survival and subsequent repopulation intervals have become an increasing focus of mass extinction research (e.g., Hart, 1996; Hallam and Wignall, 1997 and references therein). Initially, much of the effort devoted to investigating these intervals was focused on establishing the stratigraphic ranges of taxa to document the patterns and timing of biotic recovery events with the further aim of providing data related to selectivity and possible causation (e.g., Hansen et al., 1993a; Jin et al., 2000). In some cases, this has been combined with using relative abundances to examine the changing ecologic and environmental conditions and their variation (e.g., Harries, 1999; Harries and Little, 1999; Aberhan et al., 2007). In investigating the ecological aspects of mass
⁎ Corresponding author. Fax: +1 813 974 2654. E-mail addresses: [email protected] (P.J. Harries), [email protected] (P.O. Knorr). 0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.08.021
extinctions, an increasing number of studies have documented the presence of an overall diminution in the size of the faunal elements generally early in the recovery (e.g., Schmidt et al., 2004; Aberhan et al., 2007; Twitchett, 2007, see also papers in this volume). This trend towards smaller size of faunal elements associated with mass extinction events has been termed the ‘Lilliput Effect’. The term was initially coined by Urbanek (1993), although his original definition was much more restricted than current usage; it was limited to reduction in sizes within a single species through time. It remains to be tested how commonplace this effect is, both in terms of the taxonomic groups that display the trend as well as the number of extinction events, of both small and large magnitude, that provide evidence for it. Furthermore, how its relative frequency compares to that seen during background intervals is another important issue that needs to be addressed. Despite these shortcomings in the data currently available, a preponderance of the initial data suggests that the trend towards smaller size may be an additional selective characteristic that distinguishes the evolutionary and ecologic fabric of mass extinction from background intervals. In addition, given the important control that size plays on many aspects of how species function, the ‘Lilliput Effect’ has the potential to also reflect profound morphologic, physiologic, and behavioral changes within taxa (see Fig. 1). Thus, the various mass extinctions that punctuate the Phanerozoic history of life may force biotic responses that differ substantially from the patterns seen during background intervals. The magnitude of the impact of size reduction, in terms of its long-term impact on evolutionary patterns, following a mass extinction will depend, however, on what process(es) has/have acted to produce the pattern seen in the fossil record (see below).
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Fig. 1. Relationship between size and various other factors that display distinct size dependencies. A. Birds. B. Eutherian mammals. (Both figures reproduced with permission from Size, Function, and Life History, W. A. Calder, III, Dover Publications, 1996).
2. The importance of size Size is a feature that is easily measured both in modern organisms as well as in fossils culled from the geologic record, and, therefore, it has been an object of numerous studies spanning a wide range of taxonomic groups examined through various intervals in the geologic column (LaBarbera, 1989). Often paleontologists have viewed size simply as a character to be measured, and have not been especially concerned with what potential implications size changes may suggest or imply about the taxa undergoing these variations. However, there have been a plethora of neontologic studies that have focused on the implications changes in size can have for a wide spectrum of different organismal attributes (e.g., see summaries in Schmidt-Nielsen, 1984; Calder, 1996;
Brown and West, 2000, and references therein). It should be noted that many of the size-related trends and ‘rules’ are based largely on various terrestrial vertebrate groups, especially mammals and birds. In invertebrates, it is relatively poorly known exactly how, or even if, various changes in physiological processes scale with changes in size, although the literature that does exist suggests strong relationships between size and various physiological responses (e.g., Prior et al., 1979; Sylvester et al., 2004). Therefore, the direct applicability of the results of size-change studies from terrestrial mammals and birds to marine groups, especially the invertebrates that form much of the paleontologic record of mass extinctions, should be undertaken with caution. As documented in numerous sources (i.e., Peters, 1983; McKinney, 1990; Calder, 1996), size exerts a fundamental control on a plethora of
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elements associated with how organisms function and interact with their environment (see Fig. 1), and Martin and Palumbi (1993) have suggested that it may even exert a control on the nucleotide substitution rate. This control includes effects on a wide range of physiologic, metabolic, reproductive, and behavioral characteristics. Therefore, evolutionary changes in size must be accompanied by pronounced variation in other aspects of the organisms involved. Although many components of this variability, especially aspects of behavior and physiological changes, may be extremely difficult, if not impossible, to tease out of the fossil record, changes in morphology beyond simply the obvious changes in size, such as the reduction in skeletal components and the evolution of novel structures — as has been documented in various studies in Recent groups (e.g., Oster et al., 1988; Müller and Wagner, 1991 and references therein; Amores et al., 2004) — are readily discerned in fossil organisms. These types of changes are likely also associated with pronounced changes in the manner in which the more derived organisms function in comparison with their ancestors. 3. ‘Rules’ related to size changes In part because size is such a readily accessible quantity, even if the mechanisms forcing it may be far more difficult to understand and constrain, a variety of observations on size changes based on neontological as well as paleontological data have led to the development of several overarching hypotheses to explain the apparent size trends. It should be stressed that these are generalizations based on existing empirical observations and, as has been shown in various studies (see below for more discussion), they do not necessarily hold in all cases. Additionally, although numerous explanations have been put forward as the underpinning mechanisms that control these ‘rules’, there is considerable debate concerning their efficacy, especially because biologic data rarely allow for simple or unambiguous understanding of observed phenomena. Furthermore, there are too many potential, relatively ad hoc formulations to explain size trends in the fossil record that actually involve a plethora of interrelated mechanisms, and these do not readily allow for simple, allencompassing explanations. Despite these potential complications and confounding of variables, there have been numerous observations that depict trends from smaller to larger sizes through the phylogenetic histories in many lineages. This trend has been termed ‘Cope's Rule’ (as reviewed by Stanley, 1973 and later by McKinney, 1990) based on initial observations and interpretations by the 19th-century paleontologist, Edward Drinker Cope. Although Cope never formally developed ‘Cope's Rule’, his writings, which supported Neo-Lamarckian inheritance (Cope, 1896), imply its presence; for example, Cope believed that “cell division or growth force” not only regulated the growth and size of body parts but that its effects were to some degree heritable (Cope, 1871, 1896). The general applicability of this ‘rule’ has recently been called into question by Jablonski (1997) who, based on an analysis of various Cretaceous bivalve genera, has suggested that the number of size trajectories from smaller to larger — as predicated by ‘Cope's Rule’ — is not substantially greater than those that proceed from larger to smaller size. In addition, Gould and MacFadden's (2004) detailed analysis of the supposed stalwart of ‘Cope's Rule’, the Cenozoic equids, shows that although most lineages show increases in size with time, there are exceptions to this in which lineages trend toward smaller sizes. Even if continued analyses of size trends, such as those by Jablonski (1997; but see Alroy, 1998 for an alternative view), document that ‘Cope's Rule’ is not as dominant as initially hypothesized, the existing data suggest the likelihood that mass extinction intervals record a substantial increase in the relative proportion of lineages displaying size decreases as compared to that ratio during background intervals. This points to a fundamental change in size
trends during post-extinction repopulation as compared to background intervals. More studies devoted to the detailed analysis of size changes across these intervals are necessary to determine the prevalence of size reduction, and how broadly size reduction is distributed from taxonomic perspectives as well as between extinction events. How is ‘Cope's Rule’ expressed during intervals of mass extinctions? Data from several mass extinction events, especially the P–Tr (e.g. Twitchett, 2007, and references therein) and the K–T (e.g., Keller, 1988; Hansen et al., 1993b; Aberhan et al., 2007) boundaries, suggest that an ‘anti-Cope's Rule’ or ‘Lilliput Effect’ characterizes the biotic response following the mass extinction event. The implication of this ‘Lilliput Effect’ is that the overall increase in size documented in numerous lineages during background intervals should be reset during mass extinction intervals. Such a pattern has been documented by Hallam (1998) for various bivalve genera across the early Toarcian mass extinction, in stark contrast to the more typical increase in size seen in those lineages during background intervals. A second ‘rule’ related to size is the ‘Island Rule’, which was coined by Van Valen (1973) reflecting earlier work by Foster (1964). This rule is based on size trends observed in island taxa as compared to their presumed mainland progenitors. In contrast to ‘Cope's Rule’, the ‘Island Rule’ is based on the premise that once species arrive on islands their size changes can be variable; the larger organisms tend to become relatively smaller whereas the smaller organisms become relatively larger. It is thought that the former trend is a response to the relative paucity of resources whereas the latter trend reflects the reduction or lack of predators (Foster, 1964; Case, 1978). Although the actual mechanism(s) forcing this trend remain a source of considerable debate, tests of the rule both on islands and in other environments, such as the deep sea, that are considered to act in a similar fashion to islands based on their low absolute food resources combined with reduced predation pressures (e.g., McClain et al., 2006), point to its broad applicability. Others, however, such as Lomolino (1985), have suggested that the trend may not be as widespread as initially postulated. Furthermore, it is not necessarily obvious how organisms are identified as initially either large or small taxa; therefore, the ability to predict, rather than observe, size trajectories may be difficult. If populations are reduced in the abundance of their constituent individuals as well as in their geographic distribution during mass extinction events [perhaps resulting in Lazarus taxa (sensu Flessa and Jablonski (1983)), this may effectively promote the formation of genetic isolates which could respond morphologically in accordance to the ‘Island Rule’. One of the problems in evaluating this relates to the difficulty in determining which organisms should display size increases or reduction. Furthermore, it predicts that some groups should actually portray a size increase rather than with a uniform size decrease response. At this point, data depicting the former have not been widely documented across mass extinction intervals; a notable exception being the appearance of the large planktic foraminifer Whitenella archaeocretacea associated with the Late Cretaceous Cenomanian–Turonian mass extinction (Jarvis et al., 1988). In this case, the response likely reflects the response to an expanding oxygen-minimum zone. A third ‘rule’, ‘Bergmann's Rule’, relates weight trends (which obviously is directly associated with size for any broadly defined taxonomic group) relative to latitude among endothermic vertebrates. As originally formulated by Bergmann (1847), it formalized the observations that warm-blooded vertebrate species are larger in colder climates than their congeners inhabiting warmer climates. Recently, both Ashton et al. (2000) and Meiri and Dayan (2003) analyzed large datasets to investigate the basic validity of this rule. Ashton et al.'s (2000) study analyzed the relationship between size with both latitude and temperature, and found a positive correlation in the former and a negative one in the latter. Meiri and Dayan (2003) investigated body-
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size trends for 94 avian and 149 mammalian species. Based on their analysis, 72.34% and 65.10% of avian and mammalian species, respectively, conform to ‘Bergmann's Rule’. However, there has been considerable debate in the biological literature related to the general applicability of this ‘rule’ to a broad range of different groups expanding beyond endothermic vertebrates to poikilotherms and various invertebrate groups. For instance, Van Voorhies (1996) has suggested that ectotherms conform to ‘Bergmann's Rule’. However, others, such as Mousseau (1997), based on his analyses of phenotypic plasticity in insects independent of temperature, and Partridge and Coyne (1997), after a re-analysis of Van Voorhies' (1996) original data that they determined showed neither evidence for increased cell size related to temperature decrease nor evidence that increased cell size resulted in larger individuals, strongly contest his conclusions over the nature of the trend as well as mechanisms that may control the trend seen. Given the current lack of consensus over the applicability of ‘Bergmann's Rule’ to the majority of the fauna, it is difficult to speculate what role it may play in general and especially in regulating post-extinction dynamics. If it is a trend that applies broadly across all faunal components, for mass extinctions where the tropical taxa are replaced by colder-water forms the possibility exists that the postextinction taxa filling tropical niches may be dwarfed relative to their cool-water ancestral stocks. Such changes have been documented for the expansion of the Hirnantian fauna during the Ordovician–Silurian mass extinction (e.g., Rong et al., 2006) as well as for faunal changes associated with the Late Devonian Frasnian–Fammenian event (e.g., Copper, 1986). 4. Models for producing the ‘Lilliput Effect’ Another set of considerations that underlie our understanding of the ‘Lilliput Effect’ is related to the stratigraphic patterns as well as the nature of sorting across a mass extinction event. There are at least three possible patterns, none of which are mutually exclusive; individual lineages may respond to environmental and ecologic perturbations in different ways. The three patterns considered here are: 1) species sorting whereby smaller taxa preferentially survive or at least dominate during the survival and early recovery intervals with the preferred extinction or initial exclusion of larger taxa; 2) morphological responses and survivorship among species capable of undergoing rapid size reduction (approximating Urbanek's (1993) original definition of the ‘Lilliput Effect); and 3) the appearance of newly evolved lineages which are generally relatively small and are accompanied by substantial morphologic change from the ancestral stocks. The first pattern is predicated on the mass extinction events acting as filters that have a pronounced impact on the size of the fauna either in the short term or with a longer evolutionary impact (Fig. 2). In the
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example outlined here, there is no change in the size of the survivors relative to their pre-extinction event proportions, although the average size of the fauna may be reduced. Therefore, the fauna is not effectively ‘dwarfed’ or ‘miniaturized’, but the larger components preferentially either go extinct or are absent from the fauna during the initial phases of repopulation. Fundamentally, this is a process of species sorting whereby smaller taxa preferentially survive. We have termed this ‘faunal stunting’ in order to differentiate between what is ostensibly a response whereby certain smaller biotic elements are favored (at least in the initial stages of repopulation) from responses that involve evolutionary change towards smaller individuals in response to the environmental perturbations associated with biotic mass extinction. To differentiate between these two potential responses, size data of pre- and post-extinction taxa in combination with a thorough understanding of their phylogenies are necessary. The longer-term effects of this pattern could tend towards the more ecological where larger taxa reappear during the recovery with the broader distribution of environments favored by these forms (Fig. 2A) in contrast to the small taxa serving as the subsequent evolutionary stocks from which larger taxa evolve (Fig. 2B). In addressing these issues, it is unlikely that a uniform size limit could be meaningfully applied across the taxonomic spectrum. Due to differences in physiology between similarly sized taxa within different clades (i.e., compare for instance a shrew and a bivalve of similar masses), it seems unlikely that any size limit could be meaningfully applied to any mass extinction. However, initial data suggest that, even at fairly broad taxonomic levels, there may be an upper limit to the size selectivity of mass extinctions. This pattern has been most effectively documented for land vertebrates across the K–T boundary where the survivors did not exceed 25 kg (i.e., Buffetaut, 2006) and for the Pleistocene megafaunal extinctions on various continents (e.g., Brook and Bowman, 2002). The second pattern would be characterized by a change in size that would dominantly reflect the selection of smaller sizes within the range of variability displayed by a lineage prior to, during, and through the mass extinction, repopulation, and recovery intervals (Fig. 3). Typically, the morphologic pattern displayed by these responses is ‘dwarfing’ as defined by Marshall and Corruccini (1978) from their analysis of Late Quaternary marsupials of Australia. As used here, ‘dwarfing’ implies that the smaller, descendent species morphologically resemble the ancestral taxa, and the changes produced occur allometrically (i.e., there is a consistent relationship between morphologic elements between the ancestral and descendent forms). Due to the time-averaged nature of the record (e.g., Kowalewski and Bambach, 2003), it may be difficult to reconstruct the exact trajectory and timing of size reduction. Based on some examples associated with the rapid rate of sea-level rise associated with
Fig. 2. Hypothetical pattern for the ‘Lilliput Effect’ in which the immediate survivors are small taxa; the vertical lines represent taxonomic ranges and the thickness of lines are proportional to the size (i.e., the thicker the line, the larger the taxon). A. An ecological response in which small taxa appear early in the repopulation followed by the appearance of larger forms. B. An evolutionary response in which the small taxa survive and act as the ancestral stocks from which the new taxa radiate.
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between the two terms made by Hanken and Wake (1993). As used here, ‘miniaturization’ refers to not only to size reduction but also to accompanying morphologic change that results in taxa that dramatically depart from their ancestors. This type of change has been documented in a broad spectrum of different groups ranging from marine mollusks (e.g., Landman et al., 1991) to amphibians (e.g., Hanken, 1985) to insects (e.g., Klots and Klots, 1967). Although it is probable, indeed mandatory, that ‘dwarfing’ also result in physiologic change, given the difficulties of effectively assessing the extent and nature of such change in fossil organisms, the usage here will focus solely on the morphologic component of stunting.
Fig. 3. Hypothetical pattern for extinction involving dwarfing (see text for explanation and Fig. 2 for an explanation of the vertical lines). The inset displays the reduction of size that occurred if viewed at a higher temporal resolution.
Holocene deglaciation, such as the Florida Key Deer and various island mammoth populations (e.g., Raia et al., 2003), the reduction in size, at least among vertebrates, can occur rapidly, especially from a geologic perspective. Unfortunately, similar studies largely ignored invertebrates and their ability to display a rate of rapid morphologic change comparable to that displayed in various mammalian and avian clades remains to be documented. The third pattern, if present, would represent an evolutionary response to mass extinction events that results in the diminished size within various clades accompanied by significant morphologic modification (Fig. 4). To effectively evaluate the nature of this size change, well-constrained phylogenetic reconstructions are critical (see further discussion below), so that the size change, if present, can be effectively understood. It is important to determine whether the new taxa represent new species within surviving genera or whether they are members of newly evolved genera or higher taxonomic units. Typically, even when not associated with mass extinction events, the earliest taxa within new clades tend to be comparatively small (Stanley, 1973; McKinney, 1990), so there is the potential that size changes in these new groups may reflect a ‘normal’ pattern associated with the appearance of new clades and that the influence of the pattern is accentuated by the rapid and pronounced removal of larger species associated with the mass extinction events. Therefore, it is critical to establish the phylogenies of these taxa to determine if the ancestral stocks are substantially larger than the newly evolved clades. Furthermore, this needs to be tested against similar events during ‘background’ intervals to evaluate if there are qualitative and quantitative differences between the sizes of newly occurring clades as compared to the ancestors they have evolved from. This third pattern is termed ‘miniaturization’. Although this term and ‘dwarfism’ are used interchangeably, we follow the distinctions
5. Is the ‘Lilliput Effect’ ecological or evolutionary? One of the critical issues that demands a fuller explication revolves around the interval of time during which the ‘Lilliput Effect’ is displayed by the fauna. An important element of the ‘Lilliput Effect’ is whether the effects are largely ecological and, therefore, relatively transient with a limited evolutionary role for the dwarfed/miniaturized faunas, or whether they reflect a significant ‘resetting’ of life's evolutionary history. If the ‘effect’ is predominantly ecologic, it could mirror periods of environmental deterioration that accompany these events. These environmental disruptions are most effectively sensed, though not necessarily interpreted, from the geochemical perturbations that are associated with every known mass extinction event. As conditions ameliorated, the larger faunal elements would reappear producing a Lazarus pattern (see Fig. 2A). Such a pattern is predicted by the models of responses to mass extinctions developed by Harries and Kauffman (1990) as well as Harries et al. (1996) and may also reflect the short-term abundance of disaster and opportunistic species (see Levinton, 1970 for characteristics of the latter). Furthermore, there is considerable evidence suggesting that the initial surviving taxa play a limited role in the faunal recovery; i.e., they are not the evolutionary stocks from which the post-extinction radiations emanate. This may explain why certain groups, as illustrated by Lockwood's (2005) study of veneroid bivalves across the K–T and Eocene–Oligocene (E–O) mass extinctions, display no evidence of extinction-induced size reduction. The data in that study were ‘binned’ into intervals ranging from 2–4 Ma, and this could effectively obscure size changes that occur on ecologic time scales, especially for extinctions, such as the K–T, where the rate of repopulation is relatively rapid (b1 Ma) (Harries, 1999). 6. Data required to understand the Lilliput Effect Sufficient evidence exists to show that the ‘Lilliput Effect’ is a common dynamic associated with at least several mass extinction events. To gain further insight into the meaning of the trend and also to attempt to differentiate between the various processes that can produce the effect, a thorough account of the life history of the organism as well as an understanding of the phylogeny of the organism's lineage must be established. Furthermore, an understanding of the morphological response of modern fauna to ecological and environmental conditions is needed. 6.1. Life histories
Fig. 4. Hypothetical pattern for extinction involving miniaturization (see text for explanation and Fig. 2 for an explanation of the vertical lines).
An important approach, necessary to effectively examine the causes and ontogenetic trajectories associated with the ‘Lilliput Effect’, is to investigate the life histories of the taxa involved both prior to, directly following, and later in the recovery from mass extinctions. The technique of sclerochronology — using the secular trends in oxygen and carbon isotopes through the ontogeny of organisms as recorded in skeletons to examine the rate and life span of individuals (see Jones, 1988) — affords the potential to effectively examine putative changes in life history that are likely to accompany
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changes in size. This type of approach is required to discern the mechanics of how size reduction occurred, and which can readily relate to the various modes of heterochrony, such as acceleration and progenesis, that result in size reduction accompanied by morphologic change. Unfortunately, it also requires exceptionally well-preserved shell material that has been rigorously screened for diagenetic alteration and, therefore, it may not be reliably applied to all mass extinction events or across the taxonomic spectrum. 6.2. Erecting robust phylogenies One of the areas of paleobiologic research that lags behind other components of reconstructing post-mass-extinction patterns is the use of phylogenetic techniques to determine the evolutionary relationships between the taxa that are found prior to and following these bioevents. It is clear that all post-extinction taxa must have preextinction ancestors, but newly evolved groups are often portrayed as appearing almost magically. Not only is this type of analysis critical to establishing the ancestor–descendent relationships in taxa involved in the repopulation, but it is also required to deconvolve the ecologic and evolutionary potential of taxa involved in the ‘Lilliput Effect’. 6.3. Establishing modern ‘baselines’ Another avenue of research that could aid tremendously in augmenting our understanding of the ‘Lilliput Effect’ revolves around increasing our understanding of size relationships using studies of the modern fauna, especially of marine invertebrates. There is a pressing need for these studies to provide not only more data related to how size affects the functioning of specific organisms and reflects changes in environmental conditions, but also to examine broader spatial trends along latitudinal, onshore–offshore, and other environmental gradients to document whether there are ‘rules’ that underlie size trends in groups beyond terrestrial mammals and birds. These data are critical to sort out what may be reflections of habitat differences indicative of changes in recorded environments in a given section across a mass extinction boundary rather than mass-extinction-driven responses. 6.4. Questions for future research Because the study of the ‘Lilliput Effect’ is still in its relative infancy, there are a large number of important lines of research that remain to be addressed. These include, but are certainly not limited to: • How ubiquitous is the ‘Lilliput’ phenomenon both in terms of its taxonomic as well as temporal breadth (i.e., how many and which lineages portray the response and with how many mass extinctions and other smaller intensity bioevents it is associated)? • Is there a relationship between the magnitude of extinction and the nature of the fauna's response in terms of the temporal duration of the ‘effect’? • What is the spatial variability in size changes associated with a given mass extinction event? • What is temporal variability in the duration of the ‘effect’ for a mass extinction event as well as for different geographic settings, habitats, and taxonomic groups? • Are certain groups more prone to either dwarfing or miniaturization? • How are ‘small’ and ‘large’ defined for various clades? • What are the long-term evolutionary impacts of the ‘Lilliput Effect’? • How is it reflected in colonial organisms, and how do the mechanics of that response differ from or mirror those seen in solitary organisms? • From a more procedural/data collection perspective, what elements should be included in the evaluation of the ‘Lilliput Effect’? Should it include all the specimens, the largest specimen, or some subset? • What environmental changes are responsible for the size changes (see discussion in Mancini, 1978a)?
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7. Caveats An element that often plagues issues raised about mass extinction events is that many times the focus becomes the mass extinction event itself and trends as well as patterns documented for that interval cannot be compared to background intervals due to a dearth of equally detailed data for the latter. So, often elements that are considered to be relatively unique phenomena associated with mass extinction events may, in fact, not be so. Based on the literature, examples of size reduction in lineages have been documented in a wide range of different taxonomic groups throughout the Phanerozoic associated with mass extinction events (e.g., Fürsich et al., 2001; Wheeley and Twitchett, 2005) as well as with background intervals (e.g., Harris and Mundel, 1974; Mancini, 1978b; Raia et al., 2003). Another important issue that must be carefully evaluated when dealing with issues associated with mass extinctions revolves around the nature of the samples collected. For any point in geologic time, the amount of the Earth's surface that has been or even could be sampled is an extremely small fraction of global area. Therefore, although often results from a limited set of sections or even a single section are extrapolated to explain regional, if not global, patterns, it is difficult to determine how reasonable this is or how spatially variable the biotic response is to mass extinction. For instance, Twitchett et al. (2004) have documented a very rapid repopulation pattern (although data on size are unfortunately lacking) following the P–Tr mass extinction from the Central Oman Mountains, a section apparently unaffected by anoxia, as compared to the extremely lengthy delay in repopulation seen in other sections (e.g., Erwin, 1993). So, which pattern was globally more pervasive? This question is extremely difficult to answer for the P–Tr given the relative paucity of complete sections compounded by the pronounced sea-level lowstand and subsequent rise associated with the extinction interval (Hallam, 1992). Such fluctuations must have had a pronounced impact on the relatively shallow-water sections from which much of the data were collected. In addition, we need to be able to differentiate between trends that reflect relatively local environmental/habitat controls on organism size from global patterns. If the former, these could render the ‘Lilliput Effect’ more artifact than actual size trends reflecting the response to a global event. This may not be true in all cases and the ‘Lilliput Effect’ may be limited to certain environments, but we have such limited data from most mass extinctions and also a relatively poor understanding of size trends among invertebrates even in the Recent, that care must be taken not to overinterpret the records gleaned from the geologic column. 8. Conclusions Mass extinctions have had a dramatic impact on the taxonomic composition of the global biota and, therefore, have played important roles in terms of selection at a range of levels within the taxonomic hierarchy. Questions remain, however, in whether or not this selection is reflected in the ‘Lilliput Effect’ and also what types of processes, be they faunal sorting, dwarfing, miniaturization, or a combination of all three, underlie this ‘effect’. As with many elements associated with mass extinction events, there is rarely a simple, single explanation for all the data collected for a particular mass extinction, let alone for the numerous smaller events that punctuate the Phanerozoic history of life. It is likely that the ‘Lilliput Effect’ has variable causes and responses between taxonomic elements in both a given extinction event and between different mass extinctions; the expectation should be that lineages will respond differently and that various mass extinctions will induce different responses in terms of how size reduction is accomplished. To better understand the dynamics associated with the ‘Lilliput Effect’, we require a concerted, multidisciplinary research approach that documents more than simply changes in size, but attempts to garner data, such as detailed
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life histories and robust phylogenies, that can further elucidate the mechanics of how size reduction is occurring. Acknowledgments We would like to thank R. J. Twitchett and B. S. Wade who organized the GSA session ‘Extinction, Dwarfing and the Lilliput Effect’ from which this contribution originated and who shepherded it through the pipeline from talk to publication. Further thanks to U. J. Harries for her critiques and improvements of earlier drafts of this manuscript and to M. Aberhan as well as an anonymous reviewer who greatly aided in honing our arguments. References Aberhan, M., Weidemeyer, S., Kiessling, W., Scasso, R.A., Medina, F.A., 2007. Faunal evidence for reduced productivity and uncoordinated recovery in Southern Hemisphere Cretaceous–Paleogene boundary sections. Geology 35, 227–230. Alroy, J., 1998. Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science 731–734. Amores, A., Suzuki, T., Yan, Y.-L., Pomeroy, J., Singer, A., Amemiya, C., Postlethwait, J.H., 2004. Developmental roles of pufferfish Hox clusters and genome evolution in rayfin fish. Genome Research 14, 1–10. Ashton, K.G., Tracy, M.C., de Queiroz, A., 2000. Is Bergmann's rule valid for mammals? The American Naturalist 156, 390–415. Bergmann, C., 1847. Über die Verhältnisse der wärmeökonomie der Tiere zu ihrer Grösse. Göttinger Studien 3, 595–708. Brook, B.W., Bowman, D.M.J.S., 2002. Explaining the Pleistocene megafaunal extinctions: models, chronologies, and assumptions. Proceedings of the National Academy of Sciences 99, 14624–14627. Brown, J.H., West, G.B. (Eds.), 2000. Scaling in Biology. Oxford University Press, Oxford. 352 pp. Buffetaut, E., 2006. Continental vertebrate extinctions at the Triassic–Jurassic and Cretaceous–Tertiary boundaries: a comparison. In: Cockell, C., Koeberl, C., Gilmour, I. (Eds.), Biological Processes Associated with Impact Events. 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Patterns of molluscan extinction and recovery across the Cretaceous–Tertiary boundary in east Texas; report on new outcrops. Cretaceous Research 14, 685–706. Hansen, T.A., Farrell, B.R., Upshaw, B., 1993b. The first 2 million years after the Cretaceous– Tertiary boundary in east Texas: rate and paleoecology. Paleobiology 19, 251–265. Harries, P.J., 1999. Repopulations from Cretaceous mass extinctions: environmental and/or evolutionary controls. In: Barrera, E., Johnson, C.C. (Eds.), Evolution of the Cretaceous Ocean–Climate System. GSA Special Paper 332, pp. 345–364. Harries, P.J., Kauffman, E.G., 1990. Patterns of survival and recovery following the Cenomanian–Turonian (Late Cretaceous) mass extinction in the Western Interior Basin, United States. In: Kauffman, E.G., Walliser, O.H. (Eds.), Extinction Events in Earth History. Lecture Notes in Earth History. Springer Verlag, Berlin, pp. 277–298. Harries, P.J., Little, C.T.S., 1999. 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Harris, A.H., Mundel, P., 1974. Size reduction in bighorn sheep (Ovis canadensis) at the close of the Pleistocene. Journal of Mammalogy 55 (678), 680. Hart, M.B., 1996. Biotic Recovery from Mass Extinction Events, 102. Geological Society of London. Special Publication, 392 pp. Jablonski, D., 1997. Body-size evolution in Cretaceous molluscs and the status of Cope's rule. Nature 250–252. Jarvis, I., et al., 1988. Microfossil assemblages and the Cenomanian–Turonian (Late Cretaceous) oceanic anoxic event. Cretaceous Research 9, 3–103. Jin, Y.G., et al., 2000. Pattern of marine mass extinction near the Permian–Triassic boundary in South China. Science 289, 432–436. Jones, D.S., 1988. Sclerochronology and the size versus age problem. In: McKinney, M.L. (Ed.), Heterochrony in Evolution: A Multidisciplinary Approach. Topics in Geobiology 7. Plenum Press, New York, pp. 93–107. Keller, G., 1988. Extinction, survivorship and evolution of planktic foraminifera across the Cretaceous/Tertiary boundary at El Kef, Tunisia. Marine Micropaleontology 13, 239–263. Klots, A.B., Klots, E.B., 1967. Living Insects of the World. Doubleday, New York. 304 pp. Kowalewski, M., Bambach, R.K., 2003. The limits of paleontological resolution. In: Harries, P.J. (Ed.), High Resolution Approaches in Stratigraphic Paleontology. Topics in Geobiology 21. Kluwer Academic Publishers, Dordrecht, pp. 1–48. LaBarbera, M., 1989. Analyzing body size as a factor in ecology and evolution. Annual Review of Ecology and Systematics 20, 97–199. Landman, N.H., Dommergues, J.L., Marchand, D., 1991. The complex nature of progenetic species — examples from Mesozoic ammonites. Lethaia 24, 409–421. Levinton, J.S., 1970. The palaeoecological significance of opportunistic species. Lethaia 3, 69–78. Lockwood, R., 2005. Body size, extinction events, and the early Cenozoic record of veneroid bivalves; a new role for recoveries? Paleobiology 31, 578–590. Lomolino, M.V., 1985. Body size of mammals on islands: the island rule reexamined. The American Naturalist 125, 310–316. Mancini, E.A., 1978a. Origin of micromorph faunas in the geologic record. Journal of Paleontology 52, 311–322. Mancini, E.A., 1978b. Origin of the Grayson micromorph fauna (Upper Cretaceous) of north–central Texas. Journal of Paleontology 52, 1294–1314. Marshall, L.G., Corruccini, R.S., 1978. Variability, evolutionary rates, and allometry in dwarfing lineages. Paleobiology 4, 101–118. Martin, A.P., Palumbi, S.R., 1993. Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences 90, 4087–4091. McClain, C.R., Boyer, A.G., Rosenberg, G., 2006. The island rule and the evolution of body size in the deep sea. Journal of Biogeography 33, 1578–1584. McKinney, M.L., 1990. Trends in body-size evolution. In: McNamara, K.J. (Ed.), Evolutionary Trends. 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Raia, P., Barbera, C., Conte, M., 2003. The fast life of a dwarfed giant. Evolutionary Ecology 17, 293–312. Rong, J.-Y., Boucot, A.J., Harper, D.A.T., Zhan, R.-B., Neuman, R.B., 2006. Global analyses of brachiopod faunas through the Ordovician and Silurian transition: reducing the role of the Lazarus effect. Canadian Journal of Earth Sciences 43, 23–39. Schmidt-Nielsen, K., 1984. Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge. 241 pp. Schmidt, D.N., Thierstein, H.R., Bollman, J., 2004. The evolutionary history of size variation of planktic foraminiferal assemblages in the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 212, 159–180. Stanley, S.M., 1973. An explanation for Cope's rule. Evolution 27, 1–26. Sylvester, F., Dorado, J., Boltovskoy, D., Juárez, Á., Cataldo, D., 2004. Filtration rates of the invasive pest bivalve Limnoperna fortunei as a function of size and temperature. Hydrobiologia 534, 71–80. Twitchett, R.J., 2007. The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 132–144. Twitchett, R.J., Krystyn, L., Baud, A., Wheeley, J.R., Richoz, S., 2004. Rapid marine recovery after the end-Permian mass–extinction event in the absence of marine anoxia. Geology 32, 805–808. Urbanek, A., 1993. Biotic crises in the history of Upper Silurian graptoloids; a palaeobiological model. Historical Biology 7, 29–50. Van Valen, L., 1973. Pattern and the balance of nature. Evolutionary Theory 1, 31–49. Van Voorhies, W.A., 1996. Bergmann size clines: a simple explanation for their occurrence in ectotherms. Evolution 50, 1259–1264. Wheely, J.R., Twitchett, R.J., 2005. Palaeoecological significance of a new Griesbachian (Early Triassic) gastropod assemblage from Oman. Lethaia 38, 37–45.
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / p a l a e o
What does the ‘Lilliput Effect’ mean? Peter J. Harries ⁎, Paul O. Knorr Department of Geology, University of South Florida, 4202 E. Fowler Ave., SCA 528, Tampa, FL 33620-5201, USA
a r t i c l e
i n f o
Article history: Received 25 April 2007 Received in revised form 10 October 2007 Accepted 15 August 2009 Available online 9 September 2009 Keywords: Lilliput Effect Mass extinction Size change Recovery Cope's Rule
a b s t r a c t The ‘Lilliput Effect’ represents a pronounced reduction in the size of the biota associated with the aftermath of mass extinctions. Although there is empirical evidence that suggests that it may be a common pattern during the recoveries from various mass extinction events, it remains to be analyzed in more detail to understand how pervasive the trend is from temporal, spatial, and taxonomic perspectives. The ‘Lilliput Effect’ could represent dynamics associated with or important diversions from a variety of biologic ‘rules’, such as Cope's and Bergmann's, governing size changes. Furthermore, there are a variety of possible patterns that could produce the ‘Lilliput Effect’ including: 1) the survival of small taxa; 2) the dwarfing of larger lineages; and 3) the evolutionary miniaturization from larger ancestral stocks. Finally, an interdisciplinary approach, involving stratigraphy, phylogenetics, and sclerochronology, is necessary to better understand the ecologic and evolutionary underpinnings of the ‘effect’. This approach needs to be more uniformly applied to different extinctions and taxonomic groups, allowing a more effective comparison and resulting in a more holistic perspective on the ‘Lilliput Effect’. © 2009 Elsevier B.V. All rights reserved.
1. Introduction One of, if not the most ubiquitous trend(s) seen in the evolutionary history of many lineages across a wide taxonomic spectrum are size changes. Because changes in size are so readily recognized, they have provided the fundamental data for attempts to develop various biological/evolutionary ‘rules’ and ‘laws’ — reflecting biology's aim to match the apparent simplicity of reductionist explanations provided by the more physical, rather than historical, scientific disciplines. To a degree, the search for biotic laws reflects the desire of biologists to develop a series of concepts, comparable to those developed for other disciplines, such as physics and chemistry, which broadly explain fundamental aspects of the physical world. The biotic dynamics during the initial survival and subsequent repopulation intervals have become an increasing focus of mass extinction research (e.g., Hart, 1996; Hallam and Wignall, 1997 and references therein). Initially, much of the effort devoted to investigating these intervals was focused on establishing the stratigraphic ranges of taxa to document the patterns and timing of biotic recovery events with the further aim of providing data related to selectivity and possible causation (e.g., Hansen et al., 1993a; Jin et al., 2000). In some cases, this has been combined with using relative abundances to examine the changing ecologic and environmental conditions and their variation (e.g., Harries, 1999; Harries and Little, 1999; Aberhan et al., 2007). In investigating the ecological aspects of mass
⁎ Corresponding author. Fax: +1 813 974 2654. E-mail addresses: [email protected] (P.J. Harries), [email protected] (P.O. Knorr). 0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.08.021
extinctions, an increasing number of studies have documented the presence of an overall diminution in the size of the faunal elements generally early in the recovery (e.g., Schmidt et al., 2004; Aberhan et al., 2007; Twitchett, 2007, see also papers in this volume). This trend towards smaller size of faunal elements associated with mass extinction events has been termed the ‘Lilliput Effect’. The term was initially coined by Urbanek (1993), although his original definition was much more restricted than current usage; it was limited to reduction in sizes within a single species through time. It remains to be tested how commonplace this effect is, both in terms of the taxonomic groups that display the trend as well as the number of extinction events, of both small and large magnitude, that provide evidence for it. Furthermore, how its relative frequency compares to that seen during background intervals is another important issue that needs to be addressed. Despite these shortcomings in the data currently available, a preponderance of the initial data suggests that the trend towards smaller size may be an additional selective characteristic that distinguishes the evolutionary and ecologic fabric of mass extinction from background intervals. In addition, given the important control that size plays on many aspects of how species function, the ‘Lilliput Effect’ has the potential to also reflect profound morphologic, physiologic, and behavioral changes within taxa (see Fig. 1). Thus, the various mass extinctions that punctuate the Phanerozoic history of life may force biotic responses that differ substantially from the patterns seen during background intervals. The magnitude of the impact of size reduction, in terms of its long-term impact on evolutionary patterns, following a mass extinction will depend, however, on what process(es) has/have acted to produce the pattern seen in the fossil record (see below).
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Fig. 1. Relationship between size and various other factors that display distinct size dependencies. A. Birds. B. Eutherian mammals. (Both figures reproduced with permission from Size, Function, and Life History, W. A. Calder, III, Dover Publications, 1996).
2. The importance of size Size is a feature that is easily measured both in modern organisms as well as in fossils culled from the geologic record, and, therefore, it has been an object of numerous studies spanning a wide range of taxonomic groups examined through various intervals in the geologic column (LaBarbera, 1989). Often paleontologists have viewed size simply as a character to be measured, and have not been especially concerned with what potential implications size changes may suggest or imply about the taxa undergoing these variations. However, there have been a plethora of neontologic studies that have focused on the implications changes in size can have for a wide spectrum of different organismal attributes (e.g., see summaries in Schmidt-Nielsen, 1984; Calder, 1996;
Brown and West, 2000, and references therein). It should be noted that many of the size-related trends and ‘rules’ are based largely on various terrestrial vertebrate groups, especially mammals and birds. In invertebrates, it is relatively poorly known exactly how, or even if, various changes in physiological processes scale with changes in size, although the literature that does exist suggests strong relationships between size and various physiological responses (e.g., Prior et al., 1979; Sylvester et al., 2004). Therefore, the direct applicability of the results of size-change studies from terrestrial mammals and birds to marine groups, especially the invertebrates that form much of the paleontologic record of mass extinctions, should be undertaken with caution. As documented in numerous sources (i.e., Peters, 1983; McKinney, 1990; Calder, 1996), size exerts a fundamental control on a plethora of
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elements associated with how organisms function and interact with their environment (see Fig. 1), and Martin and Palumbi (1993) have suggested that it may even exert a control on the nucleotide substitution rate. This control includes effects on a wide range of physiologic, metabolic, reproductive, and behavioral characteristics. Therefore, evolutionary changes in size must be accompanied by pronounced variation in other aspects of the organisms involved. Although many components of this variability, especially aspects of behavior and physiological changes, may be extremely difficult, if not impossible, to tease out of the fossil record, changes in morphology beyond simply the obvious changes in size, such as the reduction in skeletal components and the evolution of novel structures — as has been documented in various studies in Recent groups (e.g., Oster et al., 1988; Müller and Wagner, 1991 and references therein; Amores et al., 2004) — are readily discerned in fossil organisms. These types of changes are likely also associated with pronounced changes in the manner in which the more derived organisms function in comparison with their ancestors. 3. ‘Rules’ related to size changes In part because size is such a readily accessible quantity, even if the mechanisms forcing it may be far more difficult to understand and constrain, a variety of observations on size changes based on neontological as well as paleontological data have led to the development of several overarching hypotheses to explain the apparent size trends. It should be stressed that these are generalizations based on existing empirical observations and, as has been shown in various studies (see below for more discussion), they do not necessarily hold in all cases. Additionally, although numerous explanations have been put forward as the underpinning mechanisms that control these ‘rules’, there is considerable debate concerning their efficacy, especially because biologic data rarely allow for simple or unambiguous understanding of observed phenomena. Furthermore, there are too many potential, relatively ad hoc formulations to explain size trends in the fossil record that actually involve a plethora of interrelated mechanisms, and these do not readily allow for simple, allencompassing explanations. Despite these potential complications and confounding of variables, there have been numerous observations that depict trends from smaller to larger sizes through the phylogenetic histories in many lineages. This trend has been termed ‘Cope's Rule’ (as reviewed by Stanley, 1973 and later by McKinney, 1990) based on initial observations and interpretations by the 19th-century paleontologist, Edward Drinker Cope. Although Cope never formally developed ‘Cope's Rule’, his writings, which supported Neo-Lamarckian inheritance (Cope, 1896), imply its presence; for example, Cope believed that “cell division or growth force” not only regulated the growth and size of body parts but that its effects were to some degree heritable (Cope, 1871, 1896). The general applicability of this ‘rule’ has recently been called into question by Jablonski (1997) who, based on an analysis of various Cretaceous bivalve genera, has suggested that the number of size trajectories from smaller to larger — as predicated by ‘Cope's Rule’ — is not substantially greater than those that proceed from larger to smaller size. In addition, Gould and MacFadden's (2004) detailed analysis of the supposed stalwart of ‘Cope's Rule’, the Cenozoic equids, shows that although most lineages show increases in size with time, there are exceptions to this in which lineages trend toward smaller sizes. Even if continued analyses of size trends, such as those by Jablonski (1997; but see Alroy, 1998 for an alternative view), document that ‘Cope's Rule’ is not as dominant as initially hypothesized, the existing data suggest the likelihood that mass extinction intervals record a substantial increase in the relative proportion of lineages displaying size decreases as compared to that ratio during background intervals. This points to a fundamental change in size
trends during post-extinction repopulation as compared to background intervals. More studies devoted to the detailed analysis of size changes across these intervals are necessary to determine the prevalence of size reduction, and how broadly size reduction is distributed from taxonomic perspectives as well as between extinction events. How is ‘Cope's Rule’ expressed during intervals of mass extinctions? Data from several mass extinction events, especially the P–Tr (e.g. Twitchett, 2007, and references therein) and the K–T (e.g., Keller, 1988; Hansen et al., 1993b; Aberhan et al., 2007) boundaries, suggest that an ‘anti-Cope's Rule’ or ‘Lilliput Effect’ characterizes the biotic response following the mass extinction event. The implication of this ‘Lilliput Effect’ is that the overall increase in size documented in numerous lineages during background intervals should be reset during mass extinction intervals. Such a pattern has been documented by Hallam (1998) for various bivalve genera across the early Toarcian mass extinction, in stark contrast to the more typical increase in size seen in those lineages during background intervals. A second ‘rule’ related to size is the ‘Island Rule’, which was coined by Van Valen (1973) reflecting earlier work by Foster (1964). This rule is based on size trends observed in island taxa as compared to their presumed mainland progenitors. In contrast to ‘Cope's Rule’, the ‘Island Rule’ is based on the premise that once species arrive on islands their size changes can be variable; the larger organisms tend to become relatively smaller whereas the smaller organisms become relatively larger. It is thought that the former trend is a response to the relative paucity of resources whereas the latter trend reflects the reduction or lack of predators (Foster, 1964; Case, 1978). Although the actual mechanism(s) forcing this trend remain a source of considerable debate, tests of the rule both on islands and in other environments, such as the deep sea, that are considered to act in a similar fashion to islands based on their low absolute food resources combined with reduced predation pressures (e.g., McClain et al., 2006), point to its broad applicability. Others, however, such as Lomolino (1985), have suggested that the trend may not be as widespread as initially postulated. Furthermore, it is not necessarily obvious how organisms are identified as initially either large or small taxa; therefore, the ability to predict, rather than observe, size trajectories may be difficult. If populations are reduced in the abundance of their constituent individuals as well as in their geographic distribution during mass extinction events [perhaps resulting in Lazarus taxa (sensu Flessa and Jablonski (1983)), this may effectively promote the formation of genetic isolates which could respond morphologically in accordance to the ‘Island Rule’. One of the problems in evaluating this relates to the difficulty in determining which organisms should display size increases or reduction. Furthermore, it predicts that some groups should actually portray a size increase rather than with a uniform size decrease response. At this point, data depicting the former have not been widely documented across mass extinction intervals; a notable exception being the appearance of the large planktic foraminifer Whitenella archaeocretacea associated with the Late Cretaceous Cenomanian–Turonian mass extinction (Jarvis et al., 1988). In this case, the response likely reflects the response to an expanding oxygen-minimum zone. A third ‘rule’, ‘Bergmann's Rule’, relates weight trends (which obviously is directly associated with size for any broadly defined taxonomic group) relative to latitude among endothermic vertebrates. As originally formulated by Bergmann (1847), it formalized the observations that warm-blooded vertebrate species are larger in colder climates than their congeners inhabiting warmer climates. Recently, both Ashton et al. (2000) and Meiri and Dayan (2003) analyzed large datasets to investigate the basic validity of this rule. Ashton et al.'s (2000) study analyzed the relationship between size with both latitude and temperature, and found a positive correlation in the former and a negative one in the latter. Meiri and Dayan (2003) investigated body-
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size trends for 94 avian and 149 mammalian species. Based on their analysis, 72.34% and 65.10% of avian and mammalian species, respectively, conform to ‘Bergmann's Rule’. However, there has been considerable debate in the biological literature related to the general applicability of this ‘rule’ to a broad range of different groups expanding beyond endothermic vertebrates to poikilotherms and various invertebrate groups. For instance, Van Voorhies (1996) has suggested that ectotherms conform to ‘Bergmann's Rule’. However, others, such as Mousseau (1997), based on his analyses of phenotypic plasticity in insects independent of temperature, and Partridge and Coyne (1997), after a re-analysis of Van Voorhies' (1996) original data that they determined showed neither evidence for increased cell size related to temperature decrease nor evidence that increased cell size resulted in larger individuals, strongly contest his conclusions over the nature of the trend as well as mechanisms that may control the trend seen. Given the current lack of consensus over the applicability of ‘Bergmann's Rule’ to the majority of the fauna, it is difficult to speculate what role it may play in general and especially in regulating post-extinction dynamics. If it is a trend that applies broadly across all faunal components, for mass extinctions where the tropical taxa are replaced by colder-water forms the possibility exists that the postextinction taxa filling tropical niches may be dwarfed relative to their cool-water ancestral stocks. Such changes have been documented for the expansion of the Hirnantian fauna during the Ordovician–Silurian mass extinction (e.g., Rong et al., 2006) as well as for faunal changes associated with the Late Devonian Frasnian–Fammenian event (e.g., Copper, 1986). 4. Models for producing the ‘Lilliput Effect’ Another set of considerations that underlie our understanding of the ‘Lilliput Effect’ is related to the stratigraphic patterns as well as the nature of sorting across a mass extinction event. There are at least three possible patterns, none of which are mutually exclusive; individual lineages may respond to environmental and ecologic perturbations in different ways. The three patterns considered here are: 1) species sorting whereby smaller taxa preferentially survive or at least dominate during the survival and early recovery intervals with the preferred extinction or initial exclusion of larger taxa; 2) morphological responses and survivorship among species capable of undergoing rapid size reduction (approximating Urbanek's (1993) original definition of the ‘Lilliput Effect); and 3) the appearance of newly evolved lineages which are generally relatively small and are accompanied by substantial morphologic change from the ancestral stocks. The first pattern is predicated on the mass extinction events acting as filters that have a pronounced impact on the size of the fauna either in the short term or with a longer evolutionary impact (Fig. 2). In the
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example outlined here, there is no change in the size of the survivors relative to their pre-extinction event proportions, although the average size of the fauna may be reduced. Therefore, the fauna is not effectively ‘dwarfed’ or ‘miniaturized’, but the larger components preferentially either go extinct or are absent from the fauna during the initial phases of repopulation. Fundamentally, this is a process of species sorting whereby smaller taxa preferentially survive. We have termed this ‘faunal stunting’ in order to differentiate between what is ostensibly a response whereby certain smaller biotic elements are favored (at least in the initial stages of repopulation) from responses that involve evolutionary change towards smaller individuals in response to the environmental perturbations associated with biotic mass extinction. To differentiate between these two potential responses, size data of pre- and post-extinction taxa in combination with a thorough understanding of their phylogenies are necessary. The longer-term effects of this pattern could tend towards the more ecological where larger taxa reappear during the recovery with the broader distribution of environments favored by these forms (Fig. 2A) in contrast to the small taxa serving as the subsequent evolutionary stocks from which larger taxa evolve (Fig. 2B). In addressing these issues, it is unlikely that a uniform size limit could be meaningfully applied across the taxonomic spectrum. Due to differences in physiology between similarly sized taxa within different clades (i.e., compare for instance a shrew and a bivalve of similar masses), it seems unlikely that any size limit could be meaningfully applied to any mass extinction. However, initial data suggest that, even at fairly broad taxonomic levels, there may be an upper limit to the size selectivity of mass extinctions. This pattern has been most effectively documented for land vertebrates across the K–T boundary where the survivors did not exceed 25 kg (i.e., Buffetaut, 2006) and for the Pleistocene megafaunal extinctions on various continents (e.g., Brook and Bowman, 2002). The second pattern would be characterized by a change in size that would dominantly reflect the selection of smaller sizes within the range of variability displayed by a lineage prior to, during, and through the mass extinction, repopulation, and recovery intervals (Fig. 3). Typically, the morphologic pattern displayed by these responses is ‘dwarfing’ as defined by Marshall and Corruccini (1978) from their analysis of Late Quaternary marsupials of Australia. As used here, ‘dwarfing’ implies that the smaller, descendent species morphologically resemble the ancestral taxa, and the changes produced occur allometrically (i.e., there is a consistent relationship between morphologic elements between the ancestral and descendent forms). Due to the time-averaged nature of the record (e.g., Kowalewski and Bambach, 2003), it may be difficult to reconstruct the exact trajectory and timing of size reduction. Based on some examples associated with the rapid rate of sea-level rise associated with
Fig. 2. Hypothetical pattern for the ‘Lilliput Effect’ in which the immediate survivors are small taxa; the vertical lines represent taxonomic ranges and the thickness of lines are proportional to the size (i.e., the thicker the line, the larger the taxon). A. An ecological response in which small taxa appear early in the repopulation followed by the appearance of larger forms. B. An evolutionary response in which the small taxa survive and act as the ancestral stocks from which the new taxa radiate.
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between the two terms made by Hanken and Wake (1993). As used here, ‘miniaturization’ refers to not only to size reduction but also to accompanying morphologic change that results in taxa that dramatically depart from their ancestors. This type of change has been documented in a broad spectrum of different groups ranging from marine mollusks (e.g., Landman et al., 1991) to amphibians (e.g., Hanken, 1985) to insects (e.g., Klots and Klots, 1967). Although it is probable, indeed mandatory, that ‘dwarfing’ also result in physiologic change, given the difficulties of effectively assessing the extent and nature of such change in fossil organisms, the usage here will focus solely on the morphologic component of stunting.
Fig. 3. Hypothetical pattern for extinction involving dwarfing (see text for explanation and Fig. 2 for an explanation of the vertical lines). The inset displays the reduction of size that occurred if viewed at a higher temporal resolution.
Holocene deglaciation, such as the Florida Key Deer and various island mammoth populations (e.g., Raia et al., 2003), the reduction in size, at least among vertebrates, can occur rapidly, especially from a geologic perspective. Unfortunately, similar studies largely ignored invertebrates and their ability to display a rate of rapid morphologic change comparable to that displayed in various mammalian and avian clades remains to be documented. The third pattern, if present, would represent an evolutionary response to mass extinction events that results in the diminished size within various clades accompanied by significant morphologic modification (Fig. 4). To effectively evaluate the nature of this size change, well-constrained phylogenetic reconstructions are critical (see further discussion below), so that the size change, if present, can be effectively understood. It is important to determine whether the new taxa represent new species within surviving genera or whether they are members of newly evolved genera or higher taxonomic units. Typically, even when not associated with mass extinction events, the earliest taxa within new clades tend to be comparatively small (Stanley, 1973; McKinney, 1990), so there is the potential that size changes in these new groups may reflect a ‘normal’ pattern associated with the appearance of new clades and that the influence of the pattern is accentuated by the rapid and pronounced removal of larger species associated with the mass extinction events. Therefore, it is critical to establish the phylogenies of these taxa to determine if the ancestral stocks are substantially larger than the newly evolved clades. Furthermore, this needs to be tested against similar events during ‘background’ intervals to evaluate if there are qualitative and quantitative differences between the sizes of newly occurring clades as compared to the ancestors they have evolved from. This third pattern is termed ‘miniaturization’. Although this term and ‘dwarfism’ are used interchangeably, we follow the distinctions
5. Is the ‘Lilliput Effect’ ecological or evolutionary? One of the critical issues that demands a fuller explication revolves around the interval of time during which the ‘Lilliput Effect’ is displayed by the fauna. An important element of the ‘Lilliput Effect’ is whether the effects are largely ecological and, therefore, relatively transient with a limited evolutionary role for the dwarfed/miniaturized faunas, or whether they reflect a significant ‘resetting’ of life's evolutionary history. If the ‘effect’ is predominantly ecologic, it could mirror periods of environmental deterioration that accompany these events. These environmental disruptions are most effectively sensed, though not necessarily interpreted, from the geochemical perturbations that are associated with every known mass extinction event. As conditions ameliorated, the larger faunal elements would reappear producing a Lazarus pattern (see Fig. 2A). Such a pattern is predicted by the models of responses to mass extinctions developed by Harries and Kauffman (1990) as well as Harries et al. (1996) and may also reflect the short-term abundance of disaster and opportunistic species (see Levinton, 1970 for characteristics of the latter). Furthermore, there is considerable evidence suggesting that the initial surviving taxa play a limited role in the faunal recovery; i.e., they are not the evolutionary stocks from which the post-extinction radiations emanate. This may explain why certain groups, as illustrated by Lockwood's (2005) study of veneroid bivalves across the K–T and Eocene–Oligocene (E–O) mass extinctions, display no evidence of extinction-induced size reduction. The data in that study were ‘binned’ into intervals ranging from 2–4 Ma, and this could effectively obscure size changes that occur on ecologic time scales, especially for extinctions, such as the K–T, where the rate of repopulation is relatively rapid (b1 Ma) (Harries, 1999). 6. Data required to understand the Lilliput Effect Sufficient evidence exists to show that the ‘Lilliput Effect’ is a common dynamic associated with at least several mass extinction events. To gain further insight into the meaning of the trend and also to attempt to differentiate between the various processes that can produce the effect, a thorough account of the life history of the organism as well as an understanding of the phylogeny of the organism's lineage must be established. Furthermore, an understanding of the morphological response of modern fauna to ecological and environmental conditions is needed. 6.1. Life histories
Fig. 4. Hypothetical pattern for extinction involving miniaturization (see text for explanation and Fig. 2 for an explanation of the vertical lines).
An important approach, necessary to effectively examine the causes and ontogenetic trajectories associated with the ‘Lilliput Effect’, is to investigate the life histories of the taxa involved both prior to, directly following, and later in the recovery from mass extinctions. The technique of sclerochronology — using the secular trends in oxygen and carbon isotopes through the ontogeny of organisms as recorded in skeletons to examine the rate and life span of individuals (see Jones, 1988) — affords the potential to effectively examine putative changes in life history that are likely to accompany
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changes in size. This type of approach is required to discern the mechanics of how size reduction occurred, and which can readily relate to the various modes of heterochrony, such as acceleration and progenesis, that result in size reduction accompanied by morphologic change. Unfortunately, it also requires exceptionally well-preserved shell material that has been rigorously screened for diagenetic alteration and, therefore, it may not be reliably applied to all mass extinction events or across the taxonomic spectrum. 6.2. Erecting robust phylogenies One of the areas of paleobiologic research that lags behind other components of reconstructing post-mass-extinction patterns is the use of phylogenetic techniques to determine the evolutionary relationships between the taxa that are found prior to and following these bioevents. It is clear that all post-extinction taxa must have preextinction ancestors, but newly evolved groups are often portrayed as appearing almost magically. Not only is this type of analysis critical to establishing the ancestor–descendent relationships in taxa involved in the repopulation, but it is also required to deconvolve the ecologic and evolutionary potential of taxa involved in the ‘Lilliput Effect’. 6.3. Establishing modern ‘baselines’ Another avenue of research that could aid tremendously in augmenting our understanding of the ‘Lilliput Effect’ revolves around increasing our understanding of size relationships using studies of the modern fauna, especially of marine invertebrates. There is a pressing need for these studies to provide not only more data related to how size affects the functioning of specific organisms and reflects changes in environmental conditions, but also to examine broader spatial trends along latitudinal, onshore–offshore, and other environmental gradients to document whether there are ‘rules’ that underlie size trends in groups beyond terrestrial mammals and birds. These data are critical to sort out what may be reflections of habitat differences indicative of changes in recorded environments in a given section across a mass extinction boundary rather than mass-extinction-driven responses. 6.4. Questions for future research Because the study of the ‘Lilliput Effect’ is still in its relative infancy, there are a large number of important lines of research that remain to be addressed. These include, but are certainly not limited to: • How ubiquitous is the ‘Lilliput’ phenomenon both in terms of its taxonomic as well as temporal breadth (i.e., how many and which lineages portray the response and with how many mass extinctions and other smaller intensity bioevents it is associated)? • Is there a relationship between the magnitude of extinction and the nature of the fauna's response in terms of the temporal duration of the ‘effect’? • What is the spatial variability in size changes associated with a given mass extinction event? • What is temporal variability in the duration of the ‘effect’ for a mass extinction event as well as for different geographic settings, habitats, and taxonomic groups? • Are certain groups more prone to either dwarfing or miniaturization? • How are ‘small’ and ‘large’ defined for various clades? • What are the long-term evolutionary impacts of the ‘Lilliput Effect’? • How is it reflected in colonial organisms, and how do the mechanics of that response differ from or mirror those seen in solitary organisms? • From a more procedural/data collection perspective, what elements should be included in the evaluation of the ‘Lilliput Effect’? Should it include all the specimens, the largest specimen, or some subset? • What environmental changes are responsible for the size changes (see discussion in Mancini, 1978a)?
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7. Caveats An element that often plagues issues raised about mass extinction events is that many times the focus becomes the mass extinction event itself and trends as well as patterns documented for that interval cannot be compared to background intervals due to a dearth of equally detailed data for the latter. So, often elements that are considered to be relatively unique phenomena associated with mass extinction events may, in fact, not be so. Based on the literature, examples of size reduction in lineages have been documented in a wide range of different taxonomic groups throughout the Phanerozoic associated with mass extinction events (e.g., Fürsich et al., 2001; Wheeley and Twitchett, 2005) as well as with background intervals (e.g., Harris and Mundel, 1974; Mancini, 1978b; Raia et al., 2003). Another important issue that must be carefully evaluated when dealing with issues associated with mass extinctions revolves around the nature of the samples collected. For any point in geologic time, the amount of the Earth's surface that has been or even could be sampled is an extremely small fraction of global area. Therefore, although often results from a limited set of sections or even a single section are extrapolated to explain regional, if not global, patterns, it is difficult to determine how reasonable this is or how spatially variable the biotic response is to mass extinction. For instance, Twitchett et al. (2004) have documented a very rapid repopulation pattern (although data on size are unfortunately lacking) following the P–Tr mass extinction from the Central Oman Mountains, a section apparently unaffected by anoxia, as compared to the extremely lengthy delay in repopulation seen in other sections (e.g., Erwin, 1993). So, which pattern was globally more pervasive? This question is extremely difficult to answer for the P–Tr given the relative paucity of complete sections compounded by the pronounced sea-level lowstand and subsequent rise associated with the extinction interval (Hallam, 1992). Such fluctuations must have had a pronounced impact on the relatively shallow-water sections from which much of the data were collected. In addition, we need to be able to differentiate between trends that reflect relatively local environmental/habitat controls on organism size from global patterns. If the former, these could render the ‘Lilliput Effect’ more artifact than actual size trends reflecting the response to a global event. This may not be true in all cases and the ‘Lilliput Effect’ may be limited to certain environments, but we have such limited data from most mass extinctions and also a relatively poor understanding of size trends among invertebrates even in the Recent, that care must be taken not to overinterpret the records gleaned from the geologic column. 8. Conclusions Mass extinctions have had a dramatic impact on the taxonomic composition of the global biota and, therefore, have played important roles in terms of selection at a range of levels within the taxonomic hierarchy. Questions remain, however, in whether or not this selection is reflected in the ‘Lilliput Effect’ and also what types of processes, be they faunal sorting, dwarfing, miniaturization, or a combination of all three, underlie this ‘effect’. As with many elements associated with mass extinction events, there is rarely a simple, single explanation for all the data collected for a particular mass extinction, let alone for the numerous smaller events that punctuate the Phanerozoic history of life. It is likely that the ‘Lilliput Effect’ has variable causes and responses between taxonomic elements in both a given extinction event and between different mass extinctions; the expectation should be that lineages will respond differently and that various mass extinctions will induce different responses in terms of how size reduction is accomplished. To better understand the dynamics associated with the ‘Lilliput Effect’, we require a concerted, multidisciplinary research approach that documents more than simply changes in size, but attempts to garner data, such as detailed
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life histories and robust phylogenies, that can further elucidate the mechanics of how size reduction is occurring. Acknowledgments We would like to thank R. J. Twitchett and B. S. Wade who organized the GSA session ‘Extinction, Dwarfing and the Lilliput Effect’ from which this contribution originated and who shepherded it through the pipeline from talk to publication. Further thanks to U. J. Harries for her critiques and improvements of earlier drafts of this manuscript and to M. Aberhan as well as an anonymous reviewer who greatly aided in honing our arguments. References Aberhan, M., Weidemeyer, S., Kiessling, W., Scasso, R.A., Medina, F.A., 2007. Faunal evidence for reduced productivity and uncoordinated recovery in Southern Hemisphere Cretaceous–Paleogene boundary sections. Geology 35, 227–230. Alroy, J., 1998. Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science 731–734. 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