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16.1 Introduction

Gould (1980) established a distinction between idiographic and nomothetic paleobiology. Whereas the former deals with individual evolutionary events, the latter attempts to find regularities in the history of life. This book is rooted in an idiographic approach because most chapters review a single major evolutionary event. However, after gathering such a wealth of information on specific events, it is worth to close the book with a brief attempt at exploring the nomothetic perspective by trying to find recurrent patterns and processes in evolutionary paleoecology using ichnologic data. In fact, as noted by Gould (1980) himself regarding J. J. Sepkoski’s (1978, 1979, 1984) kinetic model of diversification, the approach employed here attempts to reach a balance between nomothetics and idiographics by producing a nomothetic model which is empirically grounded (see D. Sepkoski 2012 for an insightful review). Therefore, this chapter compares several evolutionary events, searching for common themes. In order to do so, we will compare organism-substrate interactions during evolutionary radiations, benthic fauna response to mass extinctions, patterns of ecospace colonization, and environmental shifts through time.

16.2 Evolutionary Radiations

Evolutionary radiations are dramatic proliferations of taxa within clades (Erwin 1992; Simões et al. 2016). From an ichnologic perspective, three major events in marine settings are compared in this book and are, therefore, addressed in this chapter, the Cambrian Explosion (see Chap. 3), the Great Ordovician Biodiversification Event (see Chap. 4) and the Mesozoic Marine Revolution (see Chap. 9). Figures 16.1 and 16.2 summarize changes in ichnodiversity and ichnodisparity through time, respectively. Only invertebrate trace fossils were considered. Ichnogeneric occurrences were compiled on a case-by-case basis, therefore summarizing actual occurrences. However, the curves were plotted as “range-through” data, and therefore they are based on lower and upper appearances for each ichnogenus/category of architectural design and then extrapolating their presence through any intervening gap in the continuity of its record. This allows eliminating the noise generated by small-scale fluctuations in ichnodiversity and ichnodisparity that may result from the uneven number of studies for each time span. However, a disadvantage of this approach is that it is not particularly useful to detect potential drops in ichnodiversity and ichnodisparity as a result of mass extinctions (see Sect. 16.3).

Fig. 16.1
figure 1

Ichnodiversity changes through geologic time. Compilation based on literature and personal data. The main literature sources used to compile the ichnogeneric list were the Treatise volume on trace fossils (Häntzschel 1975) and the more recent revision by Knaust (2012). In addition, we have checked each ichnogenus by consulting the original ichnologic literature and pertinent reviews in order to revise its validity and potential synonyms. The ichnodiversity curves were compiled at the ichnogenus level because the taxonomy is more firmly established than for ichnospecies. Total number of ichnogenera is 523 ichnogenera (417 for bioturbation structures and 106 for bioerosion structures). Synonymies have been checked to make ichnotaxonomy consistent. Individual curves were constructed for continental, shallow-marine and deep-marine bioturbation ichnotaxa, and marine and continental bioerosion. In turn, separate ichnodiversity curves were compiled for all marine bioturbation ichnogenera, all marine ichnogenera (bioerosion plus bioturbation), and all continental ichnogenera (bioerosion plus bioturbation). In order to differentiate between shallow marine, deep marine and continental occurrences, original paleoenvironmental interpretations in the literature, as well as personal data, were considered. Curves plotted as “range-through” data, and therefore based on lower and upper appearances for each ichnogenus, extrapolating their presence through any intervening gap in the continuity of its record. Temporal resolution is at Epoch rank. Because there are no formal subdivisions for the Ediacaran Period, this bin has been further divided using the informal subdivision of Vendian (560–550 Ma) and Namibian (550–541 Ma) (sensu Jensen et al. 2006). Biogenic structures recorded in modern sediments have been included in the Holocene. Although it occurs in both hardgrounds and firmgrounds, Gastrochaenolites was considered under bioerosion. The record of mirobioerosion ichnotaxa extends further into the Precambrian with Granulohyalichnus and Tubulohyalichnus ranging into 3.5 Ga (Furnes et al. 2004, 2007; Banerjee et al. 2006, 2007; McLoughlin et al. 2009), representing in fact the oldest trace fossils. Because these two ichnogenera are produced by microbial activity and our analysis is centered on invertebrates, they have not been considered in the discussion presented in the text

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Fig. 16.2
figure 2

Ichnodisparity changes through geologic time. Compilation based on literature and personal data. Total number of categories of architectural designs is 79 (58 for bioturbation structures and 21 for bioerosion structures). Curves were constructed for ichnodisparity following the same environmental subdivision used for ichnodiversity. Curves plotted as “range-through” data, and therefore based on lower and upper appearances for each category of architectural design, extrapolating their presence through any intervening gap in the continuity of its record. Ichnodisparity was compiled following the approach of Buatois and Mángano (2013; see also Chap. 1) and categories of architectural designs summarized by Buatois et al. (2016b). Table 16.1 summarizes the different categories and the ichnogenera included. For further information, see caption of Fig. 16.1

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Table 16.1 Categories of architectural designs and their ichnotaxa in alphabetical order (after Buatois et al. 2016b)
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Compilation of ichnogeneric diversity through geologic time indicates that the Cambrian Explosion, the Great Ordovician Biodiversification Event and the Mesozoic Marine Revolution, all evolutionary radiations established based on body fossils, are associated with increases in ichnodiversity (Fig. 16.1). This pattern shows a remarkable consistency with our knowledge derived from the analysis of diversity based on the body-fossil record . In fact, similarities between the curve of marine ichnodiversity and that of marine animal genera produced by Sepkoski (1997) are striking with regards to the Cambrian Explosion and the Great Ordovician Biodiversification Event (Buatois et al. 2016a). A 433 % increase in ichnodiversity took place in marine environments during the Terraneuvian (12 and 64 ichnogenera in the Ediacaran and Terraneuvian, respectively), whereas a 77 % occurred as a result of the Great Ordovician Biodiversification Event (82 ichnogenera in the Furongian and 145 ichnogenera by the Late Ordovician). Whereas the Cambrian Explosion is essentially restricted to bioturbation structures, the Great Ordovician Biodiversification Event is expressed by bioerosion structures as well, an event that has been referred to as the Ordovician bioerosion revolution (Wilson and Palmer 2006). Ichnogeneric compilations show that the explosion in bioerosion took place approximately 80 my after the Cambrian Explosion in bioturbation (Buatois et al. 2016a). The explosive diversification of the early Cambrian supports an exponential model for the early phases of diversification as advocated originally by Sepkoski (1978) based on shelly fossils. Despite these similarities, two main differences are apparent. First, trace-fossil data indicate that the rapid diversification took place in the early Cambrian, rather than in the late early Cambrian as indicated by shelly fossils, suggesting that the Fortunian may be regarded as part of the phylogenetic fuse (Mángano and Buatois 2014; see Chap. 3). Second, marine animal genera show minor diversity fluctuations during the middle to late Cambrian, but ichnodiversity reached a plateau that spanned from the middle Cambrian to the onset of the Great Ordovician Biodiversification Event (Buatois et al. 2016a).

The ichnodiversity curve for marine trace fossils shows another, but more modest, increase in the Early Jurassic (8 %; 165 and 178 ichnogenera in the Late Triassic and Early Jurassic, respectively) and a more important one in the Late Cretaceous (19 %; 187 and 223 ichnogenera in the Early and Late Cretaceous, respectively) (Fig. 16.1). A more limited, but constant, increase took place between the Early Jurassic and Early Cretaceous. These changes in ichnodiversity are expressed by both bioerosion and bioturbation structures. This increase is undoubtedly a reflection of the Mesozoic Marine Revolution. Comparing ichnodiversity levels between the Late Triassic (164 ichnogenera) and the Late Cretaceous (223 ichnogenera) reveals a total 35 % ichnodiversity increase that is attributed to this evolutionary radiation. Ichnologic data indicate that the Early Jurassic experienced a change in ichnotaxonomic composition and the complexity of infaunal tiering, which is consistent with the timing of the Mesozoic Marine Revolution as revealed by our compilations (see Chap. 9).

Analysis of ichnodiversity changes from the Ediacaran to the Holocene supports the three-phase kinetic model of Sepkoski (1984) based on analysis of marine body fossils. According to this model, the three main evolutionary radiations in the marine biosphere display an early exponential growth followed by subsequent slowing of growth. In the case of the Cambrian and Ordovician radiations there was very rapid growth of diversity in their initial stages until a plateau was reached later, whereas diversity rose slowly during the onset of the Mesozoic Marine Revolution and continues to do so. Controversies regarding this model have essentially revolved around potential geologic and paleontologic biases, such as increased exposure of sedimentary rocks, uneven number of studies per interval, and increased ease of fossil extraction (Raup 1976; Peters and Foote 2001; Alroy et al. 2008; Alroy 2010). For our interest here, the most serious controversy is the one on the diversity levels attained in the post-Paleozoic world. It has been argued that standardized curves show a final diversity only slightly higher than the Paleozoic maximum (e.g., Alroy et al. 2008; Alroy 2010, 2014) in sharp contrast with the much higher diversity levels shown by Sepkoski’s curves (see also Bambach et al. 2004). However, new standardized curves show that Cenozoic diversity doubles Paleozoic values, supporting sustained marine diversification during the Mesozoic–Cenozoic (Bush and Bambach 2015), a pattern more consistent with the original Sepkoski’s curves.

In particular, one of the potential biases affecting estimation of post-Paleozoic diversity levels is the so-called Pull of the Recent (Raup 1979). This effect operates in two ways. First, there is an increase in the volume of Cenozoic (and to a lesser extent Mesozoic) outcrops. Second, because the modern is much better sampled that the rest of the fossil record, taxa that occur in just one stratigraphic interval and have a modern representative will be plotted as occurring through the whole interval, resulting in an inflation of diversity levels in post-Paleozoic strata . Interestingly, the trace-fossil record is not biased in the same way. Certainly, neoichnologic studies are instrumental in recognizing some biogenic structures in the modern, helping to extend the stratigraphic range of some ichnotaxa. However, at the same time, modern counterparts of some trace fossils are lacking not because these behaviors have gone extinct, but because identification of modern traces is typically much more difficult than with fossil material, particularly in the case of bioturbation structures (Bromley 1996; Buatois and Mángano 2011a). Trace fossils tend to be enhanced by diagenetic processes that assist in their recognition (Magwood 1992) and many biogenic structures are cumulative structures, which consist of both abandoned and active components (Bromley and Frey 1974); casts of modern representatives of cumulative structures would only reflect the morphology of the open components occupied by the producer, resulting in a simpler morphology than the actual overall architecture, making identification of the ichnotaxon virtually impossible (Frey 1975; Frey and Seilacher 1980; Magwood 1992). The practical result of this would be an artificial drop in ichnodiversity in the modern. This more complex pattern exhibited by the trace-fossil record is referred herein as the Push and Pull of the Recent. To avoid this problem, we have plotted in the final curves together the Holocene and the modern.

Similar to Sepkoski’s curves , ichnologic data show a phase of exponential growth in ichnodiversity followed by an equilibrium stage during the Cambrian Explosion and the Great Ordovician Biodiversification Event. Identical to body fossils, the Mesozoic Marine Revolution is associated with a slower increase in ichnodiversity. The overall coincidence between Sepkoski’s curves and those presented in this chapter indicates similar diversity trajectories for animal diversity and their behaviors. However, in the case of post-Paleozoic faunas, whereas the curve for marine animals does not show any evidence of a plateau, ichnologic information seems to suggest that a plateau may have been reached for both marine bioturbation and bioerosion.

In contrast, trends in ichnodisparity reveal a more complicated picture (Fig. 16.2). Whereas the Cambrian Explosion is associated with an increase in both ichnodisparity and ichnodiversity (Mángano and Buatois 2014; see Chap. 3), the Great Ordovician Biodiversification Event and the Mesozoic Marine Revolution display different trends. A 263 % increase in ichnodisparity took place during the Terraneuvian as a result of the Cambrian Explosion (8 and 29 categories of architectural designs in the Ediacaran and Terraneuvian, respectively), but only a 45 % is associated with the Great Ordovician Biodiversification Event (38 categories of architectural design in the Furongian and 55 by the Late Ordovician). In addition, if bioturbation and bioerosion structures are considered separately, it is clear that bioerosion is responsible for the overall increase (17 % increase in ichnodisparity for bioturbation structures and 367 % for bioerosion structures). Whereas the Cambrian Explosion was the main event in the Phanerozoic for large-scale innovations in animal-sediment interactions, it is the Great Ordovician Biodiversification Event that played this role regarding bioerosion (Buatois et al. 2016a). If bioturbation structures are considered separately for shallow- and deep-marine environments, it is apparent that ichnodisparity in shallow-marine settings remained very close to Cambrian levels, whereas an increase took place in the deep sea (88 %; 17 categories of architectural design in the Furongian and 32 by the Late Ordovician). In the same fashion that broad innovations in bioerosion lagged behind those in bioturbation, the establishment of the main types of animal-sediment interactions in the deep sea took place later than in shallow-marine settings , as originally envisaged in models of deep-sea colonization (e.g., Uchman 2004). Because approximately half of the architectural categories that typify Ordovician deep-sea ichnofaunas first occurred in shallow-marine settings during the Cambrian, the overall impact of Ordovician deep-sea categories in global marine ichnodisparity levels is limited (Buatois et al. 2016a).

In turn, although an increase in ichnodisparity is apparent as a result of the Mesozoic Marine Revolution, distinguishing between bioturbation and bioerosion structures shows that the increase is restricted to the latter (19 % increase between the Late Triassic and the Late Cretaceous). Ichnodisparity of bioturbation structures in both shallow- and deep-marine settings does not display any significant increase in connection to the Mesozoic Marine Revolution.

A main conclusion of our analysis of secular changes in ichnodiversity and ichnodisparity during the Cambrian Explosion, the Great Ordovician Biodiversification Event and the Mesozoic Marine Revolution is that, although increases in ichnodiversity are invariably linked to evolutionary radiations, these are necessary but not sufficient conditions for ichnodisparity increases. In order to further explore the links between ichnodiversity and ichnodisparity and the possible underlying causes for increases in the latter, it is now useful to analyze the results of our compilations regarding continental environments.

Ichnodiversity compilations for continental environments show a more protracted process of colonization through the whole Phanerozoic as revealed by bioturbation structures (Fig. 16.1). Although the process of invasion of the continents seems to have been slow and gradual, an initial rapid increase took place by the Silurian-Devonian transition (see Chap. 6), with an impressive 967 % increase in ichnodiversity between the Wenlock and the Early Devonian (3 and 32 ichnogenera in the Wenlock and Early Devonian, respectively). As in the case of the Cambrian Explosion, this rapid diversification in continental settings is consistent with Sepkoski’s (1978) exponential model for early diversification. Subsequent to that increase a plateau until the Early Mississippian is apparent. However, this may be in part simply an artifact due to the scarcity of continental outcrops of Late Devonian age (see Chap. 6). Subsequently, a slow but constant increase in ichnodiversity took place until the early Permian (Cisuralian), which displays an unusual peak (65 %, 91 ichnogenera). This peak has been noted in earlier studies and deemed controversial (Buatois et al. 1998). It reflects the presence of a wide variety of arthropod trackways in overbank deposits, which at least in part results from a marked tendency towards oversplitting in trackway taxonomy. In particular, many arthropod are only known from the Permian of Germany (e.g., Holub and Kozur 1981; Walter 1983); many of these are considered doubtful (see Chap. 6). After a plateau that lasted the whole Triassic, another more modest peak is apparent in the Early Jurassic. This is, at least in part, a monographic effect (Raup 1976) resulting from the high number of new arthropod trackway genera introduced by Hitchcock (1858, 1865) based on his analysis of continental trace fossils from the Connecticut Valley . Many of these have never been recorded elsewhere and are now regarded as doubtful (Rainforth 2005), so they have been omitted in our compilation. However, even leaving aside these doubtful ichnotaxa and only retaining those regarded as valid, the Early Jurassic ichnodiversity peak still persists (21 %; 61 and 74 ichnogenera in the Late Triassic and Early Jurassic, respectively). Since the Middle Jurassic onwards, ichnodiversity experienced a relatively constant increase.

Bioerosion in continental environments experienced a much later development than bioturbation. Although wood borings were mentioned for the early Permian (von Kušta 1880), the earliest convincing evidence of bioerosion in continental environments is from the Late Triassic, with the recording of six ichnotaxa representing wood bioerosion (Tapanila and Roberts 2012). Notably, this record predates the earliest record of marine bioerosion in wood, which is Early Jurassic (Villegas-Martín et al. 2012). In turn, the earliest record of bioerosion in bone is from the Early Jurassic (undetermined ichnotaxon), with the ichnogenus Cubiculum being recorded for the first time in the Late Jurassic (Xing et al. 2015). This was followed by a plateau until the Late Cretaceous with the addition of ten new ichnogenera. Since then, ichnodiversity of bioerosion structures reached a plateau that continues until the Holocene.

After the initial rapid increase in ichnodiversity of bioturbation structures by the Silurian-Devonian transition , colonization of freshwater settings was apparently quite gradual. It has been suggested that this slow pace may have resulted from the need to develop innovative styles of reproduction and dispersal, as well as complex osmoregulatory systems (Miller and Labandeira 2002). The fact that no plateau indicating an equilibrium stage in diversification is apparent for bioturbation structures may suggest that the invasion of terrestrial environments is a still ongoing process. This is consistent with the fact that the utilization of freshwater infaunal ecospace seems to have been less complete than in their marine counterparts (Miller and Labandeira 2002). Continental bioerosion ichnogenera seem to have reached a plateau by the end of the Mesozoic, but their ichnotaxonomy is still in its infancy and it is not unexpected that this trend will change with further studies.

As with ichnodiversity, ichnodisparity in continental environments reflects the process of protracted colonization (Fig. 16.2). Ichnodisparity curves of bioturbation structures reveal a rapid increase with the onset of widespread colonization by the Silurian-Devonian transition (see Chap. 6), with a 267 % increase in ichnodisparity between the Wenlock and the Early Devonian (3 and 11 categories of architectural designs in the Wenlock and Early Devonian, respectively). This was followed by a very slow increase until the Late Cretaceous that records a hike (29 %; 28 categories of architectural design in the Early Cretaceous and 36 in the Late Cretaceous), albeit limited, reaching ichnodisparity levels that persist until the Recent. The Late Cretaceous ichnodisparity peak is also expressed by bioerosion structures. However, it should be noted that all categories of architectural designs in freshwater subaqueous environments and transitional terrestrial to subaqueous settings originated in marine environments and only subsequently occurred in continental settings. In contrast, there are six categories that are exclusive of terrestrial settings (see Chap. 11). In other words, the main innovations required to invade freshwater were already present in the marine realm, but the only true behavioral innovations in continental environments were those required to colonize subaerially exposed settings. These are mostly the architectural designs developed by insects nesting in paleosols (see Chap. 13).

To summarize, our analysis shows that the key factor in building up ichnodisparity is not the existence of an evolutionary radiation per se, but the colonization of empty ecospace. The Cambrian Explosion records the colonization of empty ecospace and, therefore, displayed an increase in both ichnodisparity and ichnodiversity. A similar situation is expressed by bioerosion during the Great Ordovician Biodiversification Event in connection with the colonization of hard substrates. A third increase in ichnodisparity is revealed by the colonization of paleosols which experienced dramatic evolutionary innovations by the end of the Mesozoic. Finally, the cradle of evolutionary innovations is in shallow-marine settings (see Sect. 16.5). This is revealed by the appearance in shallow seas of all the architectural designs that subsequently expanded into freshwater and a substantial number of those that later bloomed in the deep sea. In almost all these cases, the ichnodisparity increase is followed by a subsequent further increase in ichnodiversity, as it is illustrated, by the diversification of insect nesting structures during the Cenozoic, following the establishment of the basic architectural designs in the Late Cretaceous. This pattern supports analysis based on body fossils that indicates a “first disparity, then diversity” scenario (Foote 1993, 1997; Erwin 2007; see Chap. 6).

Finally, the limitations of ichnodiversity analysis to unravel evolutionary trends need to be addressed (see Buatois and Mángano 2013 for a detailed analysis). As stated many times, the fact that ichnodiversity cannot be equated with the actual diversity of organisms represents a cautionary note (Ekdale 1985). Behavioral convergence resulting in different organisms being able to produce the same ichnotaxon may mask evolutionary trends. The opposite case, the one of several ichnotaxa resulting from the work of a single producer, also undoubtedly introduced a bias in ichnodiversity analysis through geologic time. Because of this, the different chapters exploring the ichnologic blueprints of evolutionary radiations use a plurality of conceptual and methodological tools rather than being restricted to an analysis of the number of ichnogenera or architectural designs. For example, it is clear that burrows produced by decapod crustaceans represent one of the most, if not the most, archetypal biogenic structures of the Mesozoic Marine Revolution. However, because some of its most characteristic structures, namely burrow systems included in Thalassinoides, are produced not only by decapod crustaceans, but by other organisms with a stratigraphic range that extends well before the Mesozoic, the importance of crustacean burrows remains undetected if only ichnodiversity is considered. In other words, the long stratigraphic range of Thalassinoides is misleading with respect to its key role during the Mesozoic Marine Revolution. A clearer picture emerges when, for example, abundance is considered as well (Carmona et al. 2004; see Chap. 9).

Also, in part as a result of behavioral convergence , ichnogeneric extinction rates are remarkably low. It has been noted that increases in diversity within clades may be produced from a drop in extinction rate rather that diversification per se, resulting in the so-called “pseudoradiations” (Simões et al. 2016). In the case of trace-fossil data, extinction rates can be regarded not only as low but also as constant, the latter at least since the Ordovician. Because of the impossibility of equating biological diversity and ichnodiversity, the trace-fossil expression of evolutionary radiations is not primarily of a phylogenetic nature, but rather reflects behavioral innovations.

Other problems are evident while dealing with ichnodiversity changes in specific environments through the Phanerozoic. Because there is a trend to increased infaunalization through time, the colonization of deeper tiers is conducive to obliteration of the more shallowly emplaced structures, which in many cases represent a substantial contribution to ichnodiversity. As a result, a decrease in ichnodiversity through time rather than an increase, has been noted in the case of tidal flats (Mángano et al. 2002; Mángano and Buatois 2015) and lakes (see Chap. 11). These cases underscore the importance of careful evaluation of taphonomic overprints.

Also, using ichnodiversity at ichnogeneric level may preclude detection of other patterns. Ichnospecies reflect minor behavioral variations and, therefore, they may help to detect more subtle trends in behavioral innovations (see Chap. 3). A large number of ichnogenera that have their first occurrence early in the Paleozoic seem to have displayed an increase in the number of ichnospecies through the Phanerozoic (see Chaps. 3 and 9). Exploring patterns of ichnospecies distribution through time is a promising line of research, although this would imply in-depth critical reevaluation of trace-fossil taxonomy at this rank, something beyond the scope of the present study.

Regardless of potential shortcomings, our review indicates that ichnologic information (including both ichnodiversity and ichnodisparity) is highly useful as an independent line of evidence to understand paleobiologic trends through geologic time.

16.3 Benthic Fauna Response to Mass Extinctions

Ichnologic information typically reveals a set of common responses to the three mass extinctions analyzed in this book, the end-Permian (see Chap. 7), the end-Triassic (see Chap. 8), and the end-Cretaceous (see Chap. 12). Most of these extinction events are characterized by a reduction in ichnodiversity, decrease in degree of bioturbation, reduction of bioturbation depth, size reduction, dominance of simple trace fossils in post-extinction strata , preferential survival of ichnotaxa produced by deposit feeders, and selective extinction in shallow-marine ecosystems . How pronounced were these effects seems to depend on the severity of the mass extinction event, with the end-Permian mass extinction clearly showing the most severe impact from an ichnologic standpoint, showing consistency with body-fossil data. In turn, this is reflected in the pattern of recovery after the extinction, with longer recovery times involved in the end-Permian mass extinction in comparison with the end-Cretaceous event. Ichnologic information on the other two major events, the end-Ordovician and late Devonian extinctions is patchy, with only a few studies available (McCann 1990; Herringshaw and Davies 2008; Buatois et al. 2013) and, therefore, any generalization remains premature.

Although these extinctions are associated to a decrease in ichnodiversity, actual extinction of invertebrate ichnotaxa is quite rare. On the contrary, ichnotaxa that disappeared after the mass extinctions for the most part reappeared during the recovery time, representing Lazarus ichnotaxa (Gibert 2003). As noted previously, trace-fossil extinction rates tend to be very low, a fact that, at least in the case of relatively simple behaviors, results from behavioral convergence. Some ichnotaxa (e.g., the undermat miner Oldhamia , the large trail Climactichnites), however, seem to reflect behaviors that have apparently disappeared by the end of the Cambrian, together with their producers.

Because the curves illustrated in Figs. 16.1 and 16.2 have been compiled as range through data, they are of limited use to detect changes in ichnodiversity as a result of mass extinctions. For example, whereas a significant drop in ichnodiversity is associated with the end-Permian mass extinction (see Chap. 7), this is not reflected by the ichnodiversity curves. Similarly, the end-Triassic mass extinction resulted in a decrease in ichnodiversity, albeit more modest (see Chap. 8), which is not recorded in our ichnodiversity curves. The absence of an ichnodiversity drop in these curves is simply an artifact resulting from the methodology employed in their construction. It is therefore surprising that a 7 % decrease in total marine ichnodiversity (5 % for bioturbation structures and 15 % for bioerosion structures) is revealed by these curves in connection with the end-Cretaceous mass extinction. The Late Cretaceous peak and subsequent drop in ichnodiversity are also present in the curves that were plotted eliminating the occurrence of singletons.

Decrease in the degree of bioturbation has been noted in connection with many mass extinction events. Although comparative analysis of mass extinctions from a trace-fossil perspective are still in their infancy, available information seems to suggest that the extent of this decrease in intensity of bioturbation tends to reflect how profound was the impact of the event. This is illustrated by the end-Permian mass extinction, which shows a collapse of the mixed layer (see Chap. 7 and Sect. 16.4; Buatois and Mángano 2011b; Hofmann et al. 2015). A similar situation has not been recorded so far associated with any of the other mass extinction events. In fact, intense bioturbation has been noted in Danian post-extinction deposits (see Chap. 12).

Reduction in the size of trace fossils has been detected in connection with many mass extinction events, most notably the end-Permian (see Chap. 7) and end-Triassic (see Chap. 8). In other cases, such as the end-Cretaceous, this trend is not apparent (see Chap. 12, although see Wiest et al. 2015 for documentation of trace-fossil size reduction in the aftermath of the end-Cretaceous mass extinction). The so-called Lilliput effect has been noted in the paleobiologic literature to explain the sharp decrease in body size, based on both the body fossil and trace-fossil records, in the aftermath of mass extinctions (Urbanek 1993; Twitchett 2007). Explanations for this size reduction are still unclear, with both externalist and internalist causes being involved. Limited oxygen and food have been invoked as likely candidates for the former (Twitchett 2007), whereas survival of small taxa; the dwarfing of larger lineages and the evolutionary miniaturization from larger ancestral stocks fall among the later (Harries and Knorr 2009).

Dominance of simple trace fossils is another typical feature in post-extinction strata . For example, simple trace fossils attributed to Planolites are the first in reappearing after the end-Permian mass extinction (see Chap. 7). Simple forms, such as Planolites and Palaeophycus , seem to be common in Lower Jurassic post-extinction deposits as well (see Chap. 8). The prevalence of these simple morphologies overall reflect very simple feeding behaviors, most likely reflecting opportunistic population strategies in the aftermath of mass extinctions (Fraiser and Bottjer 2009).

It has long been noted that organisms are differentially affected during extinctions according to trophic type (Jablonski and Raup 1995; Smith and Jeffrey 1998; Hansen et al. 2004; Twitchett 2006). In particular, suspension feeders tend to have been more affected than deposit feeders during mass extinctions. In this regard, it has been concluded that both selective deposit feeding and omnivory significantly enhance survivability during mass extinction events (Twitchett 2006). This is clearly illustrated by the overwhelming dominance of deposit-feeding traces in Danian post-extinction deposits (see Chap. 12). Also, post-extinction late Devonian ichnofaunas are dominated by structures produced by selective deposit feeders, whereas suspension-feeding burrows are absent (Buatois et al. 2013).

Ichnofaunas from shallow-marine environments tend to be more strongly affected than those in marginal-marine and deep-marine settings. Marginal-marine, brackish-water faunas typically consist of opportunistic animals that flourish under extreme conditions. Therefore, they are able to rapidly colonize environments after a major disturbance, such as mass extinctions. Of the five colonization phases recognized for brackish-water settings by Buatois et al. (2005), only the end of the first (Ediacaran–Ordovician) and the third (Permian–Triassic) coincide with mass extinctions (the Late Ordovician and Late Triassic mass extinctions, respectively). The remaining three of the “Big Five”, the late Devonian, end-Permian, and end-Cretaceous mass extinctions, does not show any impact in marginal-marine biotas. In the same vein, ichnofaunas from deep-water settings do not seem to have been strongly affected by mass extinctions (Uchman 2004). No major crisis has been associated with any of the “Big Five” in the deep sea, other than a reduction in the diversity and abundance of graphoglyptids in the case of the end-Ordovician and end-Cretaceous mass extinctions (Uchman 2003).

16.4 Patterns of Ecospace Colonization

Having established that there are some recurrent ichnologic patterns involving evolutionary radiations and mass extinctions, we may now explore if recurrent motifs can be established in connection with colonization of empty or underutilized ecospace. In other words, is it possible to detect trace-fossil assemblages that recur through geologic time not as a response to environmental constrains (as is the case of ichnofacies), but driven by large-scale evolutionary controls instead? We have attempted to address this question in a previous paper, referring to this particular recurrence of ichnoassemblages revealing common strategies in ecospace colonization as “the Déjà vu effect” (Buatois and Mángano 2011b). In this chapter, we argue that three main types of trace-fossil assemblages can be recognized in connection with exploitation of empty or underutilized ecospace.

The first of these assemblages consists of very small grazing trails (e.g., Helminthopsis , Helminthoidichnites , Gordia ) produced by epifaunal or very shallow infaunal vermiform animals, very shallow-tier feeding structures (e.g., Treptichnus , Oldhamia , Pilichnus ) of infaunal vermiform organisms, and (in some cases) trackways (e.g., Diplichnites , Stiaria ) of epifaunal arthropods (Buatois and Mángano 2011b). Almost invariably trace fossils occur in association with structures suggestive of microbial stabilization, such as wrinkle marks, palimpsest ripples, and old elephant skin (Noffke 2010; Buatois and Mángano 2012a). The associated primary sedimentary fabric and bedding-plane physical sedimentary structures are superbly preserved (e.g., Buatois et al. 1997). Ichnofaunas reveal superficial and shallow-tier grazing and mining of microbial mats in the absence of substantial infaunal bioturbation. The presence of microbial mats allows preservation of minute trace fossils, displaying delicate fine morphologic features (Buatois and Mángano 2011b). These trace-fossil assemblages occur across a wide range of environmental settings, such as Ediacaran-lower Cambrian shallow-marine (e.g., Gehling 1999; Buatois et al. 2014), Cambrian deep-marine (e.g., Buatois and Mángano 2003), and late Paleozoic continental to fluvio-estuarine (Buatois et al. 1997; Mángano et al. 1997) settings, invariably in connection with empty or underutilized ecospace.

The second assemblage is characterized by shallow-tier burrows ( Spongeliomorpha , Halopoa ), trails ( Cruziana ), and resting traces ( Rusophycus ) with well-developed ornamentation, typically bioglyphs. Very shallow-tier burrows and trackways may be present as well. The occurrence of well-preserved bioglyphs and the sharp burrow boundaries suggest emplacement in sediment that was firm at or close to the sea bottom. These trace-fossil assemblages are associated with widespread firm substrates and the virtual absence of a mixed layer (Droser et al. 2004; Jensen et al. 2005; Buatois and Mángano 2011b; Mángano et al. 2013; Hofmann et al. 2015). This is illustrated by two apparently unrelated ichnofaunas: those in Cambrian–Ordovician and Lower Triassic shallow-marine environments . Both deposits are characterized by preferential preservation of epifaunal and very shallow-tier infaunal trace fossils; paucity of mid- and deep-tier trace fossils; absence of mottled bioturbation textures; and dominance of cohesive substrates in open-marine environments (Hofmann et al. 2015). In the case of lower Paleozoic strata, the mixed layer was still incipient and poorly developed (Droser et al. 2004; Jensen et al. 2005; Callow and Brasier 2009; Mángano et al. 2013), whereas in the Lower Triassic the mixed layer may have collapsed as a result of the end-Permian extinction (Buatois and Mángano 2011b; Hofmann et al. 2015; see Chap. 9). The ichnologic responses in both situations were essentially identical.

The third assemblage is characterized by the presence of horizontal branched burrow systems (e.g., Multina , Vagorichnus ) at the base of event sandstone beds (Buatois and Mángano 2011b). These burrow systems are preserved along lithologic interfaces creating virtually no disturbance in the primary sedimentary fabric. Multina is common at the base of lower Paleozoic marine tempestites and turbidites, where it records post-event colonization (e.g., Buatois and Mángano 2004, 2012b; Buatois et al. 2009). Vagorichnus has been recorded at the base of Jurassic lacustrine turbidites (Buatois et al. 1995, 1996). Although these occurrences are from disparate environments and from rocks of different ages, they are all associated with an increase in burrowing depth reflecting initial exploitation of the infaunal ecospace (Buatois and Mángano 2011b). From an evolutionary standpoint, this incipient colonization of the infaunal ecospace preceded the onset of more intense bioturbation and the establishment of a well-developed mixed layer.

The recurrent presence of these three types of trace-fossil assemblages in rocks of different ages and formed under a wide variety of environmental settings can only be understood under the light of the evolutionary prism. These assemblages reveal a limited repertoire of behavioral strategies that allow benthic faunas to colonize empty or underutilized ecospace. Fossilization of these behavioral strategies in the form of biogenic structures is mediated by a set of preservational conditions resulting from the recurrent opening of a taphonomic window. This window was responsible for the preservation of surface and shallow-tier structures which typically are obliterated by deeper-tier and more intense bioturbation (Bromley 1996).

16.5 Environmental Shifts Through Time

A number of studies published for the most part in the eighties and nineties revealed that the fossil record can be characterized by a recurrent pattern of onshore origination of evolutionary innovations and their subsequent expansion to deeper water, resulting in the proposal of the so-called “onshore–offshore model” (e.g., Jablonski et al. 1983; Sepkoski and Miller 1985; Jablonski and Bottjer 1990; Sepkoski 1991; Sepkoski and Sheehan 1983). In fact, it has been argued that an onshore–offshore pattern is displayed by Sepkoski’s evolutionary faunas themselves, as illustrated by the replacement of trilobite-rich communities by mollusk-rich communities in shallow-water niches throughout the Paleozoic (Sepkoski and Miller 1985).

The trace-fossil record provides further empirical support to this model across a broad range of scales. First, an onshore–offshore pattern is evident from individual ichnotaxa, showing either evidence of expansion or retreat. In the first case, an ichnogenus occurring for the first time in shallow water subsequently extends its environmental range into deeper-marine settings without loss of onshore representatives. In the second case, migration into deeper water occurs together with loss of onshore representatives (Bottjer et al. 1988; Stanley and Pickerill 1993). Examples of expansion include Ophiomorpha (Bottjer et al. 1988; Tchoumatchenco and Uchman 2001), Scolicia (Seilacher 1986) and Rhizocorallium commune (Knaust 2013). An example of retreat is Zoophycos (Bottjer et al. 1988).

Second, entire groups of trace fossils may display the onshore–offshore pattern. The best example is graphoglyptids, which in the early Cambrian occur in shallow water, but subsequently migrated to the deep sea (Crimes and Anderson 1985; Jensen and Mens 1999), where they became the core component of the Nereites Ichnofacies.

Third, the onshore–offshore pattern is also displayed by ichnofabrics. For example, it has been argued that in carbonate settings intense bioturbation first took place in shallow-water settings and only later seaward (Droser and Bottjer 1989). This pattern may reflect the fact that niche partitioning within the substrate first developed in shallow water and subsequently expanded into deeper water.

Fourth, and at a larger scale, the onshore–offshore pattern is displayed in connection with the colonization of empty or underutilized ecospace. This is shown by trace-fossil evidence of original colonization of shallow-marine settings and the progressive subsequent expansion into the deep sea, marginal-marine environments and continental settings. Also, this pattern is apparent within continental environments themselves, as demonstrated by the initial colonization of lake-margin settings and later expansion into subaqueous lacustrine settings (Buatois and Mangano 1993; Buatois et al. 1998; see Chaps. 5 and 6). This is certainly analogous to the migration of plants from upland areas to the lowlands during the Carboniferous-Permian transition (DiMichele and Aronson 1992) and the origination of aquatic insects in running water and subsequent expansion into lacustrine habitats (Wooton 1988).

16.6 Conclusions

Comparative analysis of the ichnologic record of major evolutionary events allows detecting recurrent patterns that may help to further increase our understanding of the underlying evolutionary dynamics of animal-substrate interactions through geologic time. In particular, we have detected recurrent patterns of organism-substrate interactions during evolutionary radiations, benthic fauna response to mass extinctions, strategies of ecospace colonization, and environmental shifts through time. Evolutionary radiations are invariably associated with an ichnodiversity increase, whereas increases in ichnodisparity are linked to the colonization of empty ecospace. Evaluation of mass extinction events suggests common responses from the perspective of animal-substrate interactions, namely a reduction in ichnodiversity, decrease in degree of bioturbation, reduction of bioturbation depth, size reduction, dominance of simple trace fossils in post-extinction strata, preferential survival of ichnotaxa produced by deposit feeders, and selective extinction in shallow-marine ecosystems. The recurrent presence of certain trace-fossil assemblages in rocks of different ages and formed under a wide variety of environmental settings seems to suggest a limited repertoire of behavioral strategies for colonization of empty or underutilized ecospace. The trace-fossil record provides further empirical support to the onshore–offshore model across a broad range of scales.