the trace-fossil record of tidal flats through the phanerozoic: evolutionary innovations and faunal...

PLEASE RESPECT COPYRIGHT

Considerable investment goes into the production of any publication. Recovering that investment

helps ensure the publishing program can continue to provide books at reasonable prices, and

continue to create publishing opportunities to future authors.

GAC is a not-for-profit association. We thank our many

volunteer authors, editors, contributors, councillors, committee members and others who support our

continuing activities in the earth sciences in Canada and the world.

157

The Trace-fossil Record of Tidal Flats Through the

Phanerozoic: Evolutionary Innovations and Faunal Turnover

*M.G. Mángano and L.A. BuatoisDepartment of Geological Sciences, University of Saskatchewan, Saskatoon, Saskatchewan, S7N 5E2, Canada

*Corresponding author, E-mail: [email protected]

Mángano, M.G. and Buatois, L.A., 2015, The trace-fossil record of tidal flats through the Phanerozoic:Evolutionary innovations and faunal turnover, in McIlroy, D., ed., ICHNOLOGY: Papers from ICHNIA III:Geological Association of Canada, Miscellaneous Publication 9, p. 157-177.

ABSTRACT

A comparison of tidal-flat ichnofaunas through geologic time allows distinction of five main evolutionaryphases: 1) the initial invasion by animals (earliest Cambrian), 2) the arthropod expansion (Cambrian–Ordovician), 3) diversification and faunal turnover (Silurian–Devonian), 4) setting the stage for the ModernFauna (Carboniferous–Permian), and 5) infaunalization and the role of crustaceans (Mesozoic–Cenozoic).This framework allows understanding of the importance of tidal flats as sites of evolutionary innovationsand the associated faunal turnover that took place in the intertidal realm through the Phanerozoic. Tidal-flat colonization started during the Fortunian, as revealed by the presence of monospecific suites ofTreptichnus pedum in extremely shallow water. Later in the early Paleozoic, ichnologic data reveal theestablishment of an intertidal fauna dominated by mollusc-like animals, euthycarcinoids and trilobites.Early Paleozoic tidal flats, and particularly in the Cambrian, were anactualistic, reflecting reduced preda-tion pressure, absence of terrestrially derived food and microbial binding. The rest of the Paleozoic wit-nessed faunal turnover, with the appearance of new tracemakers, and a consequent increase in ichnodiver-sity. In particular, bivalves became dominant in late Paleozoic tidal flats, including relatively deep-tiersiphonate representatives. Mesozoic–Cenozoic tidal-flat ichnofaunas are dominated by deep-tier bioturba-tors, particularly crustaceans, as well as polychaetes and bivalves. The evolutionary history of tidal-flat ich-nofaunas reflects an increasing role of ecosystem engineers, culminating in the Mesozoic–Cenozoic phase.Global and alpha ichnodiversity both steadily increased through the Paleozoic. However, ichnodiversity ofMesozoic–Cenozoic tidal flats decreased with respect to Paleozoic levels. This pattern is regarded as apreservational bias, resulting from increased shallow-tier destruction by deep-tier key bioturbators in post-Paleozoic times.

INTRODUCTION

Ichnology is a prime example of the tension betweentime’s arrow and time’s cycle as discussed by Gould (1987).In this dichotomy, time’s arrow envisions history as an irre-versible sequence of unrepeatable events, whereas time’scycle underscores a non-directional time in which events arerepeated according to a recurrent pattern. The applicability ofichnology to facies analysis and paleoenvironmental recon-struction relies on the notion of archetypal ichnofacies astrace-fossil suites that record responses to a given set of envi-ronmental conditions and that recur through geologic time.Therefore, the ichnofacies concept is strongly rooted in acyclic idea of geologic time (Mángano and Buatois, 2012).This approach provides a nomothetic program for ichnology,which has been extremely useful to solve problems in sedi-mentary geology (e.g., MacEachern et al., 2007). However,this success came at a price: the overlooking of broad evolu-tionary changes. Understanding animal-substrate interac-tions as a fundamental element of the changing ecology ofthe past brings back time’s arrow to ichnology, allowingtrace fossils to be at the forefront of evolutionary paleoecol-ogy (Mángano and Buatois, 2007, 2012). Evaluating thetrace-fossil record of the colonization of specific sedimenta-ry environments is one of the central components of this lineof research. Examples include the colonization through timeof the deep sea (Seilacher, 1974, 1977; Crimes, 1974; Orr,2001; Uchman, 2003, 2004), estuaries (Buatois et al., 2005),and continental environments (Buatois and Mángano, 1993;Buatois et al., 1998).

The aim of this paper is to expand this research programby discussing the ichnologic record of tidal-flat colonizationthrough the Phanerozoic. Tidal flats are heterogeneous,harsh, but predictable environments, in which interspecificinteractions are poorly regulated and therefore open tonumerous possibilities (Reise, 1985). Heterogeneity andunrefined interactions, together with predictability, may havepromoted major steps in evolution (Reise, 1985), and in thissense tidal flats can be viewed as nurseries of evolutionaryinnovation (Mángano et al., 2002).

CHARACTERISTICS OF TIDAL FLATS

For this study, tidal flats are regarded as that zoneextending between spring high- and spring low-tide levels,grading landward into the supratidal marshes and seawardinto the shallow subtidal region (van Straaten, 1954). This isin contrast with the wider view that also includes, flat to gen-tly sloping upper-subtidal areas and lower-supratidal areas(Reineck, 1967; Weimer et al., 1981). Rocky shorelines areexcluded from this analysis as they display their own peculi-arities and evolutionary trends (Johnson and Baarli, 2012).The intertidal zone in tide-dominated shorelines is made of

extensive tidal flats dissected by a network of meanderingtidal channels and creeks. Tidal flats are harsh ecosystemswhere marine organisms often approach the survival bound-aries of their tolerance range to environmental extremes. Inaddition to typical marine environmental factors, tidal flatsare strongly affected by an additional set of controls result-ing from their intertidal position within the depositional pro-file (Reise, 1985, 2002). Intertidal biotas are controlled most-ly by the interplay of, 1) salinity, 2) sediment mobility andhydrodynamic energy, 3) time of exposure to subaerial con-ditions, 4) temperature, 5) substrate type, and 6) food supply(Desjardins et al., 2012a). These controls operate in differentways across the tidal-flat area. Because of the variableimpact of these limiting factors, very few species are able toinhabit the entire tidal range, resulting in a zonational distri-bution of organisms across the intertidal area (Reise, 1985).In the upper-intertidal zone, environmental conditions areextreme and characterized by high temporal instability andunpredictability. As a result, communities tend to show lowdiversity. In contrast, middle- to lower-intertidal zones areless stressful settings, resulting in high diversity and includ-ing species that are adapted to utilize the resources of specif-ic microhabitats (Sanders, 1968, 1969; Slobodkin andSanders, 1969). In particular, lower-intertidal communitiesresemble adjacent subtidal communities (Schäfer, 1972;Reise, 1985; Swinbanks and Murray, 1981).

The sedimentological characteristics of tidal-flat depositshave been summarized elsewhere (e.g., Klein, 1971, 1977;Dalrymple, 2010; Flemming, 2012), and their ichnologicalaspects have received attention as well (e.g., Frey et al.,1987a, b; Mángano et al., 2002; Mángano and Buatois,2004a; Buatois and Mángano, 2011a; Desjardins et al.,2012a). Therefore, only a brief summary is provided here.The mud flat (upper zone of the tidal flat) is dominated bydeposition of fine-grained sediment, with mud depositionrecording suspension fallout, clay flocculation and biodeposi-tion in the form of the production of fecal pellets and pseudo-feces (de Boer, 1998; Augustinus, 2002; Potter et al., 2005;Chang et al., 2007; Flemming, 2012). Mud-flat deposits typ-ically consist of laminated or massive mudstone with someintercalation of siltstone and very fine-grained sandstone, dis-playing lenticular bedding. Although modern mud flats areintensely bioturbated by the activity of polychaetes, gas-tropods and bivalves (Schäfer, 1972; Reineck and Singh,1980), limited lithological contrast commonly precludespreservation and visualization of biogenic structures, withindistinct mottled texture being common (Mángano et al.,2002). Elements of the Cruziana Ichnofacies may be pre-served where lithological interfaces (e.g., exceptional stormbeds) are available (e.g., Mángano et al., 2002).

The mixed flat consists of middle-intertidal area, whichrepresents the transition between sand flats (<5% mud con-

158

MÁNGANO and BUATOIS

tent) and mud flats (>95% mud content), recording sedimen-tation from traction alternating with fallout from suspension(Flemming, 2012). Mixed-flat deposits consist of thinlyinterbedded wave- and current-ripple crosslaminated, veryfine-grained sandstone and massive or parallel-laminatedmudstone, typically displaying flaser and wavy bedding.Wrinkle marks, relict troughs, flat-topped ripples andwashout structures are common locally. The degree of bio-turbation is typically moderate (Reineck and Singh, 1980),and the presence of interbedded sandstone and mudstoneenhances preservation of elements of the CruzianaIchnofacies (Mángano et al., 2002; Buatois and Mángano,2011a; Desjardins et al., 2012a).

The sand flat constitutes the lower intertidal zone of thetidal flat, and is dominated by bedload transport of sand-sizedsediment. In settings typified by high current speeds, two-dimensional and three-dimensional dunes are the dominantmigrating bedforms (Dalrymple and Rhodes, 1995; Boyd etal., 2006; Dalrymple, 2010). Resultant deposits consist oftrough and planar crossbedded, coarse- to fine-grained sand-stone and medium- to very fine-grained sandstone; upper-flow regime parallel lamination is common (Dalrymple et al.,1990; Dalrymple and Choi, 2007; Dalrymple, 2010).Bioturbation intensity tends to be low, and the SkolithosIchnofacies is dominant in these high-energy deposits(Mángano et al., 2002; Buatois and Mángano, 2011a;Desjardins et al., 2012a). In lower energy settings, ripples arethe dominant bedforms, and deposits tend to consist of cur-rent- and wave-rippled, crosslaminated, very fine- and fine-grained sandstone. Mudstone drapes are common, typicallyforming flaser bedding. As the case of the mixed flat, wrinklemarks, relict troughs, flat-topped ripples and washout struc-tures may be present. Although the energy gradient increasesfrom the upper- to the lower-intertidal zone, many sand flatsrecord moderate levels of energy. In these cases, intensity ofbioturbation may be quite high and a wide variety of biogenicstructures, representing the Cruziana Ichnofacies rather thanthe Skolithos Ichnofacies, is recorded.

TIDAL-FLAT ICHNOFAUNAS

THROUGH GEOLOGIC TIME

Evolutionary aspects of tidal flats through thePhanerozoic have been discussed previously (Mángano etal., 2002; Buatois and Mángano, 2011a). Additional studieson the evolution of intertidal biotas have focused on thebody-fossil record, providing further information on tempo-ral trends (Johnson and Baarli, 2012). However, a compre-hensive analysis of tidal-flat ichnofaunas through time is notyet available.

Tidal flats are formed in a wide variety of physiograph-ic settings, such as fluvio-estuarine transitions, restricted

bays, estuaries, deltas and open-marine shorelines. Whereastidal flats in fluvio-estuarine transitions are dominated byterrestrial to freshwater ichnofaunas, those associated withbays, estuaries and deltas typically contain depauperatebrackish-water ichnofaunas, and tidal flats directly connect-ed with the open sea tend to display more diverse ichnofau-nas illustrating the Cruziana Ichnofacies (Mángano andBuatois, 2004a). This paper focuses on this latter type oftidal-flat ichnofaunas, in which environmental stress is notcontrolled by freshwater dilution. Changes of freshwater andbrackish-water ichnofaunas through time have beenaddressed elsewhere (Buatois et al., 1998, 2005). Tidal flatsin estuarine and deltaic settings are typically characterizedby low-diversity ichnofaunas (see McIlroy, 2004, 2007;McIlroy et al., 2005 for exceptions). From an evolutionaryperspective, they are assessed within the framework of thebrackish-water model because they represent adaptations tosettings in which salinity dilution plays the major controllingrole (Buatois et al., 2005).

In this section, we have subdivided the ichnologicalrecord of tidal flats in five main evolutionary phases. Thisframework may help to address the problem of faunalturnovers in intertidal settings through the Phanerozoic andto evaluate the notion that tidal flats may have served as sitesof evolutionary innovations.

PHASE 1 (EARLIEST CAMBRIAN): THE INITIAL

INVASION BY ANIMALS

The Precambrian biologic record of tidal flats is domi-nated by extensive microbial matgrounds (e.g., Noffke et al.,2006, 2008). However, by the earliest Cambrian (Fortunian),an initial colonization of tidal flats by animals took place.Monospecific occurrences of Treptichnus pedum occur inmiddle- to lower-intertidal deposits of the VanrhynsdorpGroup in South Africa (Buatois et al., 2013; Fig. 1A‒C) andthe Nama Group in Namibia (Geyer and Uchman, 1995).Upper intertidal settings may have represented the landwardboundary for the T. pedum producer (Buatois et al., 2013).Microbially induced sedimentary structures are locally pres-ent in these deposits. These occurrences suggest that T.pedum was produced by an opportunist organism adapted tostressful conditions (Geyer, 2005). The presence ofTreptichnus pedum in Fortunian tidal-flat deposits records anincipient colonization of the intertidal realm at the dawn ofthe Cambrian explosion.

PHASE 2 (CAMBRIAN–ORDOVICIAN): THE

ARTHROPOD EXPANSION

The ichnologic record of early Paleozoic tidal flats isquite extensive. The rest of the Cambrian and the Ordovicianreflect the appearance of a unique cast of characters in inter-

TRACE FOSSIL OF TIDAL FLATS THROUGH THE PHANEROZOIC

159

tidal settings. Particularly in northeastern North America,Cambrian (Stage 2 to Furongian) tidal-flat deposits are char-acterized by a peculiar ichnofossil suite consisting of thegiant locomotion trail Climactichnites and its related restingtrace Musculopodus (Logan, 1860; Seilacher, 1977, 2008;Yochelson and Fedonkin, 1993; Hagadorn et al., 2002;Hagadorn and Belt, 2008; Getty and Hagadorn, 2008, 2009;Seilacher and Hagadorn, 2010). Associated paired scratchmarks arranged in meandering patterns, included in theichnogenus Radulichnus, are present as well although not inassociation with Climactichnites (Seilacher, 1977; Seilacherand Hagadorn, 2010). These ichnofaunas are present on sur-faces containing a wide variety of microbially induced sedi-mentary structures. The plasticity of the microbially bindedsubstrate, played a significant role in the preservation of del-icate morphologic details. This assemblage is temporallyrestricted because Climactichnites and Musculopodus areonly known from the Middle to Late Cambrian (Series 3 toFurongian).

Although once attributed to the activity of a representa-tive of an unknown phylum (Yochelson and Fedonkin,1993), Climactichnites is now regarded as produced by alarge (up to 32 cm wide and 75 cm long), shallow-tier prim-itive mollusc or mollusc-like organism that employed mus-cular waves generated along the sole of a flexible foot aslocomotion mechanism (Getty and Hagadorn, 2009;Seilacher and Hagadorn, 2010). The presence in thesedeposits of cylindrical pellets resembling those of modernmolluscs is consistent with this interpretation (Seilacher andHagadorn, 2010). In the same vein, Radulichnus scratchmarks are regarded as produced by rows of paired radularteeth rasping through a resistant microbial mat (Seilacher,1977; Seilacher and Hagadorn, 2010). The producer ofClimactichnites and related ichnotaxa probably inhabited thelower-intertidal sand flat on a more permanent basis, insteadof exploring the intertidal zone for short periods of time(Getty and Hagadorn, 2008, 2009). This trace-fossil suiteseems to record the locomotion of organisms that may havetraversed the intertidal area under subaerial as well as sub-aqueous conditions (Getty and Hagadorn, 2008, 2009).

Shallow-tier arthropod trackways (Protichnites,Diplichnites), trails (Cruziana) and resting traces(Rusophycus) are also present in these Cambrian tidal flats(MacNaughton et al., 2002; Hagadorn and Seilacher, 2009;Collette and Hagadorn, 2010; Collette et al., 2010, 2012;Hagadorn et al., 2011). Their environmental range over-lapped, in part, with that of Climactichnites, but arthropod-generated structures were not restricted to sand flats; rather,they occupied middle- to upper-intertidal flats and coastaleolian dunes as well (MacNaughton et al., 2002; Hagadorn etal., 2011; Collette et al., 2012). Although some of the

160


Figure 1. Treptichnus pedum in Fortunian tidal-flat depositsof the Kalk Gat Formation, Vanrhynsdorp Group, creek nearKalk Gat Noord Farm, South Africa. A) General view of sev-eral specimens. Scale bar is 5 cm; B) Close-up of long andwinding specimens. Scale bar is 1 cm long; C) Close-up of aspecimen locally showing the typical branching pattern ofthis ichnospecies. Scale bar is 5 cm long.

Protichnites specimens were regarded as produced byeurypterid-like arthropods carrying mollusc shells (i.e., her-mit arthropods; Hagadorn and Seilacher, 2009), this hypoth-esis has been challenged more recently in favour of euthycar-cinoids (Collette et al., 2012), which is actually in line withthe original interpretation proposed for some of these arthro-pod trackways (MacNaughton et al., 2002). In addition,euthycarcinoid body fossils occur at the end of Cruziana-liketrails (Collette et al., 2010; Collette and Hagadorn, 2010).

In any case, the most widespread group of trace fossils inlower Paleozoic tidal flats are those produced by trilobitesand trilobite-like organisms, represented by Rusophycus (Fig.2A and D) and Cruziana (Fig. 2B and E‒G), as well as by thetrackways Diplichnites (Fig. 2C) and Dimorphichnus (e.g.,Driese et al., 1981; Durand, 1985; Astini et al., 2000;Mángano et al., 2001; Mángano and Buatois, 2004b;Desjardins et al., 2012b; Mángano et al., 2013a, 2014).Cruziana and Rusophycus attributed to olenellid trilobiteshave been recorded in Early Cambrian tidal-flat deposits ofboth the Argentinean Precordillera (Astini et al., 2000) andthe North American Appalachians (Mángano et al., 2014),both being part of the same continent at that time (Thomasand Astini, 1996, 2003). Rusophycus leifeirikssoni (Fig. 2A)commonly forms clusters in Lower to Middle Cambrianmixed- to sand-flat deposits, where it crosscuts shallower tierarthropod structures and horizontal burrows, sharing a mid-tier position with the sea-anemone burrow Bergaueria andlarge Rusophycus isp. (Mángano and Buatois, 2003a, 2004b).Shallow tiers are typically colonized with Cruziana problem-atica (Fig. 2B), Rusophycus carbonarius, Diplichnites isp.(Fig. 2C), Dimorphichnus isp., Helminthoidichnites tenuis,Helminthopsis isp. and Planolites isp., reflecting the activitiesof arthropods and worm-like organisms (Mángano andBuatois, 2003a, 2004b; Desjardins et al., 2012b; Mángano etal., 2013a). Upper Cambrian tidal-flat deposits show similartiering patterns, but with Cruziana omanica and Cruzianasemiplicata (Fig. 2E) recording shallow tiers, and clusters ofRusophycus latus (Fig. 2D) occupying mid-tier positions(Mángano et al., 1996). Lower to Middle Ordovician tidal-flat deposits are dominated by trilobite trace fossils as well. Afaunal turnover in trilobite faunas of olenids by asaphids isreflected by the ichnologic record, with the appearance of therugosa group (C. rugosa rugosa, C. rugosa furcifera and C.rugosa goldfussi), locally displaying the typical ‘bathtub mor-phology’ (Mángano et al., 2001; Mángano and Buatois,2003b; Fig. 2F and G). Shallow-tier Dimorphichnus isp.,recording feeding activities of arthropods on fresh organicdetritus or scrapping microbial mats, are also typically part ofthese associations. Upper Ordovician intertidal ichnofaunasare poorly known, but a general review of Ordovician ichno-faunas has suggested that trilobite trace fossils became lessabundant by the Late Ordovician (Mángano and Droser,2004).

In addition to shallow-tier arthropod and mollusc-liketrace fossils, deep-tier intertidal habitats (up to 40 cm deep)were colonized, with Skolithos linearis (Fig. 3A),Arenicolites isp. (Fig. 3B) and Diplocraterion parallelum(Fig. 3C) being common in both Cambrian and Ordoviciansand-flat deposits (Goodwin and Anderson, 1974; Cornish,1986; Simpson, 1991; Skoog et al., 1994; Mángano et al.,1996, 2001; Mángano and Buatois, 2004b; Desjardins et al.,2012b). These dwelling structures reflect the activity of sus-pension-feeding worm-like organisms feeding on particlessuspended in the water column or passively preying on otherorganisms. In some cases, the density of these structures isquite high, resulting in the production of piperock (Simpson,1991; Skoog et al., 1994; Mángano and Buatois, 2004b). Thedeep tier was also colonized with Syringomorpha nilssoni(Fig. 3E) and Syringomorpha isp. (Fig. 3D), which seems tobe restricted to the Cambrian. The functional significance ofSyringomorpha is not completely clear, but it may representfeeding, linked to the exploitation of microbial films on coat-ed sand grains and interstitial meiofauna (Mángano andBuatois, 2004b).

PHASE 3 (SILURIAN‒DEVONIAN):

DIVERSIFICATION AND FAUNAL TURNOVER

Evaluating the ichnologic record of Silurian‒Devoniantidal-flat ichnofaunas is not straightforward because,although some studies are available (e.g., Kumar, 1978;Miller 1979, 1991; Miller and Johnson, 1981; Narbonne,1984; Theron and Loock, 1988; Davies et al., 2006;Poschmann and Braddy, 2010; Bradshaw, 2010), an intertidalorigin has not been convincingly demonstrated in all cases.However, the emerging picture is one of rapid diversificationand faunal change, with a number of ichnotaxa appearing forthe first time in tidal-flat settings, resulting in trace-fossilassemblages that have little in common with those of theCambrian‒Ordovician. A moderately diverse trace-fossilassemblage is present in Silurian intertidal carbonates, com-prising dominantly shallow-tier ichnotaxa, such asPalaeophycus, Polarichnus, Petalichnus, Cochlichnus,Gordia, Cruziana, and Rusophycus, together with mid-tierrepresentatives including Bergaueria and Helicodromitesand some deep-tier ichnotaxa, such as Chondrites, Skolithos,Arenicolites and Diplocraterion (Narbonne, 1984).Arthropod trackways are known from a number of coastalSilurian‒Devonian deposits, but it is not completely clear, iftrue tidal-flat facies are represented, and these ichnofaunasmay even represent attempts to colonize adjacent subaeriallyexposed settings (e.g., Trewin and McNamara, 1995;Draganits et al., 2001; Davies et al., 2006). Eurypterid track-ways included in Palmichnium pottsae and the bivalve tracefossils Lockeia siliquaria and Protovirgularia dichotomahave been documented in Devonian tidal-flat deposits, andmay record the work of a lower intertidal community


161

162


Figure 2. Trilobite trace fossils in Cambrian‒Ordovician tidal-flat deposits. A) Clusters of Rusophycus leifeirikssoni, Lowerto Middle Cambrian Campanario Formation, Angosto del Morro de Chucalezna, northwest Argentina. Hammer is 33.5 cmlong; B) Cruziana problematica displaying a scribbling pattern, Lower to Middle Cambrian Campanario Formation,Purmamarca, northwest Argentina. Scale bar is 2 cm long; C) Diplichnites isp., Lower to Middle Cambrian CampanarioFormation, Angosto del Moreno, northwest Argentina. Scale bar is 1 cm long; D) Rusophycus latus, Upper Cambrian Pico deHalcón Member of the Santa Rosita Formation, Quebrada del Salto Alto, northwest Argentina. Scale bar is 2 cm long; E)

Cruziana semiplicata and associated synaeresis cracks, Furongian (Upper Cambrian) Pico de Halcón Member of the SantaRosita Formation, Quebrada del Salto Alto, northwest Argentina. Scale bar is 1 cm long; F) Cruziana rugosa, Floian–Darriwilian Mojotoro Formation, Quebrada del Gallinato, northwest Argentina. Coin is 1.8 cm wide; G) Cross section ofCruziana rugosa showing ‘bathtub morphology’, Floian–Darriwilian Mojotoro Formation, Quebrada del Gallinato, northwestArgentina. Coin is 1.8 cm wide.


163

Figure 3. Deep-tier vertical burrows in Cambrian sand-flat deposits, Lower to Middle Cambrian Campanario Formation,northwest Argentina. A) Bedding plane view of a high-density association of Skolithos linearis on a rippled sandstone surface.Angosto de Perchel. Lens cap diameter is 5.5 cm; B) Arenicolites isp. Angosto de Perchel. Lens cap diameter is 5.5 cm; C)

Bedding plane view of a high-density association of Skolithos linearis and Diplocraterion parallelum. Quebrada de Moya.Scale bar is 1 cm long; D) Syringomorpha isp. piperock. Angosto del Morro de Chucalezna. Lens cap is 5.5 cm; E)

Syringomorpha nilssoni, displaying the classic J-shaped morphology and associated spreite. Cordón de Alfarcito. Coin is 1.8cm wide.

(Poschmann and Braddy, 2010). In the Devonian, the ichno-genera Zoophycos and Spirophyton are known from extreme-ly shallow water, possibly occurring in intertidal areas (e.g.,Miller 1979, 1991; Miller and Johnson, 1981; Theron andLoock, 1988).

PHASE 4 (CARBONIFEROUS‒PERMIAN): SETTING

THE STAGE FOR THE MODERN FAUNA

Late Paleozoic tidal-flat ichnofaunas are well known,particularly in the North American midcontinent (e.g., Millerand Knox, 1985; Martino, 1989; Rindsberg, 1994; Greb andChesnut, 1994; Mángano et al., 1998, 2002; Mángano andBuatois, 2004a). As a result, a detailed picture on the evolu-tionary significance of these ichnofaunas can be reconstruct-ed (Mángano et al., 1998, 2002). Tidal flats developed undermoderate- to high-energy conditions contain trace-fossilsuites similar to those of the early Paleozoic, and are domi-nated by Diplocraterion polyupsilon, Diplocraterion isp.,Skolithos isp., Conichnus conicus and Rosselia isp. (Masonand Christie, 1986; Wescott and Utgaard, 1987). This trace-fossil suite represents mid- to relatively deep-tier (up to 11cm deep) colonization by an infauna comprising suspensionfeeders, passive predators and detritus feeders.

However, it is in those tidal flats, formed under low-energy conditions, where a higher diversity of biogenicstructures is present, developing a more complex infaunaltiering structure (Mángano et al., 2002; Mángano andBuatois, 2004a). These tidal-flat deposits are dominated by awide variety of shallow-tier and, to a lesser extent, mid-tierstructures produced by bivalves (Lockeia ornata, L. siliquar-ia, Protovirgularia bidirectionalis, P. rugosa, Solemyatubaisp.) (Fig. 4A‒C), ophiuroids (Asteriacites lumbricalis,Pentichnus pratti) (Fig. 4D), arthropods (Cruziana problem-atica, Cruziana isp., Rusophycus isp.), sea anemones(Conichnus conicus), molluscs or mollusc-like organisms(Psammichnites grumula, P. implexus, P. plummeri) (Fig. 4Eand G), gastropods or flatworms (Curvolithus simplex, C.multiplex; Fig. 4F), worm-like animals (Nereites cambrensis,N. imbricata, N. jacksoni, N. missouriensis, Palaeophycustubularis, Parahaentzschelinia ardelia, Phycodes palmatus,Phycodes isp., Phycosiphon incertum, Planolites beverleyen-sis, Rosselia socialis, Skolithos isp., Teichichnus rectus,Trichophycus isp.; Fig. 4H and I), and worm-like organismsor crustaceans (Arenicolites isp., Diplocraterion isp.,Halopoa isp., Rhizocorallium irregulare) (Mángano et al.,2002; Mángano and Buatois, 2004a).

Bivalve-produced trace fossils are extremely commonand important components in late Paleozoic tidal-flat com-munities (e.g., Rindsberg, 1994; Mángano et al., 2002;Mángano and Buatois, 2004a). Particularly significant is theoccurrence of large specimens of Lockeia siliquaria in the

same tidal-flat deposits bearing the anomalodesmatanWilkingia (Mángano et al., 1998). This association suggestsrelatively deep burrowing by siphon-feeding infaunalbivalves in Carboniferous tidal flats (Mángano et al., 1998).In addition, Protovirgularia dichotoma (in a wide range ofpreservational variants) and Lockeia ornata record the activ-ities of protobranch bivalves in organic-rich, mixed- to sand-flat facies (Mángano et al., 1998).

PHASE 5 (MESOZOIC‒CENOZOIC): INFAUNAL-

IZATION AND THE ROLE OF CRUSTACEANS

Post-Paleozoic tidal-flat ichnofaunas are relatively welldocumented (e.g., Häntzschel and Reineck, 1968;MacKenzie, 1972, 1975; Carter, 1975; Sellwood, 1975;Pollard and Steel, 1978; Ireland et al., 1978; Chamberlain,1980; Richards, 1994; Weissbrod and Barthel, 1998;Zonneveld et al., 2001, 2012; Bromley and Uchman, 2003;Baucon and Avanzini, 2008; Šimo and Olšavsky, 2007;Carmona et al., 2008; Knaust, 2010; Fernández and Pazos,2013). However, with more studies there is a strong possibil-ity that this phase may be further subdivided. Mesozoic andCenozoic intertidal ichnofaunas are different from theirPaleozoic counterpart, but are quite similar to recent exam-ples, underscoring that the origin of modern tidal-flat faunasis firmly rooted in the Mesozoic Marine Revolution. EarlyTriassic tidal-flat ichnofaunas are sparse, most likely reflect-ing the impact of the end-Permian mass extinction on benth-ic faunas (e.g., Twitchett and Barras, 2004), althoughSkolithos isp., Diplocraterion isp., Diplocraterion paral-lelum, Arenicolites isp. and Rhizocorallium isp. are known inLower Triassic tidal-flat deposits (Richards, 1994; Šimo andOlšavsky, 2007). Lower Triassic vertical burrows are consid-erably shallower than their older or younger counterparts,suggesting that the deep infaunal ecospace was essentiallyempty or underutilized during the aftermath of the end-Permian extinction event (Twitchett and Barras, 2004).

Contrastingly, Middle Triassic to Neogene tidal-flat ich-nofaunas tend to be dominated by abundant mid- to deep-tiertrace fossils, mostly produced by decapod crustaceans, andto a lesser extent, polychaetes and bivalves. Common mid- todeep-tier elements are Thalassinoides suevicus,Ophiomorpha nodosa, Ophiomorpha isp., Arenicolites isp.,Diplocraterion habichi, D. luniforme, D. parallelum (Fig.5A and B), Polykladichnus irregularis, Skolithos linearis,Conichnus conicus, Cylindrichnus concentricus, Asterosomaisp., Rhizocorallium isp. (Fig. 5C) and Zoophycos-like struc-tures (Häntzschel and Reineck, 1968; MacKenzie, 1972,1975; Carter, 1975; Sellwood, 1975; Ireland et al., 1978;Chamberlain, 1980; Weissbrod and Barthel, 1998;Zonneveld et al., 2001, 2012; Baucon and Avanzini, 2008Carmona et al., 2008). Sediment reworking by deep- to mid-tier crustaceans, as well as polychaetes and bivalves, may

164



165

Figure 4. High-diversity trace-fossil association in tidal-flat deposits of the Upper Carboniferous Stull Shale Member, KanwakaFormation, Waverly site, Kansas, USA. A) Protovirgularia bidirectionalis; B) Lockeia ornata intergrading with Protovirgulariarugosa; C) Lockeia siliquaria; D) Asteriacites lumbricalis; E) Psammichnites implexus; F) Curvolithus simplex. Lens cap is 5.5cm wide; G) Psammichnites grumula; H) Nereites missouriensis; I) Nereites imbricata. All scale bars are 1 cm long.

have led to the obliteration of shallower tiers in post-Paleozoic tidal flats (Mángano et al., 2002).

Shallow-tier trace fossils, such as Planolites isp.,Archaeonassa fossulata, Kouphichnium isp., Asteriaciteslumbricalis, Gyrochorte comosa and Curvolithus simplex, arepresent as well, but are clearly less common (Häntzschel andReineck, 1968; Fernández and Pazos, 2013). Interestingly, inmany cases preservation of these shallow-tier trace fossils isapparently linked to the role of microbial mats. Microbiallyinduced sedimentary structures, such as wrinkle marks, arecommon in Jurassic tidal-flat deposits of Germany containinga relatively wide variety of shallow-tier trace fossils producedby xiphosurids, mollusks, flatworms, polychaetes and ophi-uroids (Häntzschel and Reineck, 1968). Preservation ofxiphosurid trace fossils assigned to the ichnogenusKouphichnium in Cretaceous tidal-flat deposits of Argentinawas allowed by microbial binding and biostabilization of the

sediment (Fernández and Pazos, 2013). The very shallow-tiertrace fossil Archaeonassa fossulata occurs in ripple patches inCretaceous tidal-flat deposits of Colorado (Schieber, 2007;(Fig. 6A‒D). This ichnotaxon may represent matground graz-ing of a microbially enriched surface.

DISCUSSION: SECULAR CHANGES

IN TIDAL-FLAT BIOTURBATION

TRENDS IN ICHNOFAUNAL COMPOSITION AND

INFAUNAL TIERING

A comparative analysis of intertidal ichnofaunas,through the Phanerozoic, provides useful information forunderstanding the importance of tidal flats as sites of evolu-tionary innovations and the impact of faunal turnovers inintertidal ecosystems (Fig. 7). The history of tidal-flat colo-nization by metazoans encompasses evolutionary changes

166


Figure 5. U-shaped burrows in Cretaceous sand-flat deposits, Dakota Group, Alameda Avenue, Colorado, USA. A) Cross sec-tion of deep-tier Diplocraterion parallelum; B) Bedding-plane view of several specimens of Diplocraterion parallelum; C)

Bedding-plane view of Rhizocorallium isp. All scale bars are 5 cm long.

spanning the whole of the Phanerozoic. Early Paleozoic tidalflats, and particularly Cambrian ones, are anactualistic(Mángano and Buatois, 2004b). The initial colonization ofintertidal areas by the Treptichnus pedum producer (Buatoiset al., 2013) was followed by the establishment of a ratherpeculiar, large mollusc-like and arthropod (e.g., euthycarci-noid, trilobite) fauna, displaying variable degrees of adapta-tion to withstand the harsh conditions of the intertidal setting(MacNaughton et al., 2002; Mángano and Buatois, 2004b;Mángano et al., 2014). Generally, intertidal communities inthe Cambrian were only incipiently developed. Most trace-fossil assemblages are paucispecific and involved surficial orshallow-tier structures (with the exception of some mid-tierRusophycus and deep-tier vertical burrows). Intertidal ichno-faunas were dominated by migrants (i.e., horizontal migra-tion related to tidal cycles) and explorers (coming from thesea and searching for food in eolian dunes adjacent to thetidal flat). Early Paleozoic tidal flats were unique in terms offood supply, predator pressures and role of microbial bind-ing, among other factors (Mángano and Buatois, 2004b;Buatois and Mángano, 2011a). In contrast to modern tidalflats, which are characterized by abundant food supply com-

ing from a wide variety of sources (including terrestriallyderived organic particles), early Paleozoic intertidal trophicwebs were essentially based on a marine nutrient source andautochthonous production. Modern tidal-flat animals areexposed to a double set of predators, being preyed on bymarine organisms during submergence and by terrestrialorganisms during emergence. On the contrary, Cambrian‒Ordovician intertidal communities developed in the absenceof continental predators, allowing tidal flats to function asrefuges from marine predators (Mángano and Buatois,2004b; Mángano et al., 2014). Finally, early Paleozoic tidal-flat sediments were commonly stabilized by microbial mats,allowing for a different set of taphonomic rules to be in place(Buatois and Mángano, 2011b).

Despite these differences, early Paleozoic tidal flats mayhave resembled their modern counterparts in being sites ofreproduction, protection, and feeding. Four main alternativehypotheses have been proposed to explain trilobite incur-sions to intertidal areas (Mángano and Buatois, 2004b;Mángano et al., 2014). One of these hypotheses involvedreproduction (trilobite nurseries), whereas the other three


167

Figure 6. Trace fossils in microbial mats in Cretaceous sand-flat deposits, Dakota Group, Alameda Avenue, Colorado, USA.A) General view of ripple patches. Scale bar is 1 m long; B) Close-up of ripple patches. Scale bar is 1 m long; C) Generalview of Archaeonassa fossulata in ripple patches. Scale bar is 15 cm long; D) Close-up of Archaeonassa fossulata. Scale baris 5 cm long.

underscore the importance of tidal flats as feeding grounds(trilobite pirouette, hunting burrow, and microbial gardenhypotheses). The trilobite nursery hypothesis suggests thatsome trilobites used the intertidal areas to nest, in analogywith modern limulids. This hypothesis is supported by theoccurrence of mid-tier Rusophycus clusters in Lower toMiddle Cambrian tidal-flat deposits (Fenton and Fenton,1937; Mángano et al., 1996; Mángano and Buatois, 2004b;Fig. 2A). This behaviour is consistent with the activities ofseveral modern organisms, including both invertebrates (e.g.,limulids, crabs) and vertebrates (e.g., fish, turtles), whichnest in tidal flats and return to subtidal environments afterbirth (Reise, 1985). The absence of terrestrial predators in theearly Paleozoic may have made tidal flats a protected settingfor eggs and juvenile individuals.

The trilobite pirouette hypothesis is based on the inter-pretation that some trilobite trails showing circular and scrib-

bling patterns may record grazing activity rather than purelocomotion (Seilacher, 1970; Neto de Carvalho, 2006; Fig.2B). This interpretation was originally based on observationsin offshore deposits, but has been expanded to accommodateincursions in tidal flats (Mángano and Buatois, 2004b). Inthis scenario, shallow-marine trilobites foray into intertidalzones to browse for organic detritus.

The hunting burrow hypothesis envisages trilobite aspredators on vermiform infauna. It is based on the interpre-tation of some deep Rusophycus dispar oriented with its axisparallel to subparallel to Palaeophycus as reflecting preda-tion on worms (Jensen, 1990). In these examples, the wormburrows closely follow the curvature of the Rusophycus,being commonly in contact with only one of its lobes. Thishas been proposed based on observations in shallow-subtidaldeposits (Jensen, 1990). Although similar behaviour may beexpected in intertidal environments, no examples are known.

168


Figure 7. Evolutionary changes of tidal-flat ichnofaunas. Microbial mats decreased in abundance through the Paleozoic, butreappeared in prolific numbers in the Early Triassic. Skolithos piperock, which records colonization of deep tiers in the earlyPaleozoic, became less abundant during the mid- to late Paleozoic. As a result of the end-Permian mass extinction, depth ofbioturbation decreased dramatically in the Early Triassic, but subsequently experienced a remarkable increase during the restof the Mesozoic and the Cenozoic. The importance of ecosystem engineers increased through geologic time, playing a majorrole on modifying the tidal-flat landscape, with the establishment of an incipient mounded microtopography generated bybivalves during the late Palaeozoic, but particularly in the Mesozoic and Cenozoic due to the activity of major bioturbators,such as decapod crustaceans (e.g., callianassids) and polychaetes (e.g., arenicolids), which significantly altered the sedimen-tary surface.

The microbial garden hypothesis involves trilobites vis-iting the tidal flat to feed from the thick microbial mat andenriched microbial resources resulting from infaunal activityof benthic organisms (Mángano and Buatois, 2004b;Mángano et al., 2014). This hypothesis is consistent with thefact that in modern tidal flats, bacteria and the activity of theinfauna (e.g., polychaetes, tellinid bivalves, crustaceans) isconducive to an increase in nutrients, promoting an upwarddiffusion of nutrients, and enhancing microbial growth(Reise, 1985, 2002).

Regardless of the underlying explanation, ichnologicevidence clearly supports trilobite incursions ontoCambrian‒Ordovician tidal flats, demonstrating that theCambrian evolutionary fauna was not exclusive of offshoresettings, but was able to explore and use the resources of theintertidal area (Mángano et al., 2014). In addition, the pres-ence of deep vertical burrows, such as Skolithos andDiplocraterion, points to a significant landward expansion ofthe Agronomic Revolution (Mángano and Buatois, 2004b).

The ichnologic record of Silurian‒Devonian tidal flatsreveals a faunal turnover apparently associated with rapiddiversification. A new cast of characters appeared by themiddle Paleozoic, including the significant participation ofeurypterids and bivalves. Diversification continued into thelate Paleozoic, as recorded by the presence of highly diversetrace-fossil assemblages in Carboniferous tidal flats. Middle,and particularly late, Paleozoic, tidal-flat ichnofaunas arequite different from those of early Paleozoic intertidal set-tings in that trilobite-dominated communities were replacedby bivalve-dominated communities. This faunal replacementis consistent with body-fossil data, as revealed by the corre-spondence between Sepkoski’s evolutionary faunas and localmarine communities (Sepkoski and Miller, 1985). Temporalchanges in environmental distribution of each of these com-munities display onshore‒offshore expansions, with trilo-bite-rich communities being replaced and displaced by mol-lusc-rich communities in shallow-marine settings throughoutthe Paleozoic (Sepkoski and Miller, 1985).

Mantle fusion and siphon formation were regarded asthe key features leading to the Mesozoic infaunal bivalveradiation (Stanley, 1968, 1972). Siphons and ventral mantlefusion allow sealing of the mantle cavity, promoting rapidfoot extrusion and ejection of water that fluidizes the sedi-ment around the shell (Trueman, 1966; Trueman et al., 1966;Stanley, 1970; Seilacher and Seilacher, 1994). In turn, deepinfaunalization has been interpreted as a co-evolutionaryresponse to high predation pressure (Vermeij, 1987).Absence of ventral mantle fusion and true siphons charac-terises sluggish shallow burrowers, a trait regarded as typicalof Paleozoic bivalves (Stanley, 1972). However, the associa-tion of large, relatively deep-tier Lockeia siliquaria and the

anomalodesmatan Wilkingia in Carboniferous tidal flats mayrecord an early appearance of an evolutionary innovation.Wilkingia exhibits an elongate shell and relatively deep pal-lial sinus, suggesting a mode of life adapted for siphon feed-ing, and setting the stage for the Modern evolutionary fauna(Mángano et al., 1998). In short, integration of ichnologicand body-fossil data suggests incipient exploitation of thedeep infaunal ecospace by siphonate bivalves before theMesozoic marine revolution, indicating a modification to theecospace colonization patterns derived from Bambachianmegaguilds (Mángano et al., 1998). In any case, although thedeep infaunal ecospace was occupied by the late Paleozoic,Carboniferous‒Permian tidal-flat ichnofaunas are dominatedby a high diversity of shallow-tier trace fossils, showing thatdeep-tier bivalves did not obliterate shallowly emplacedstructures.

Deep-tier suspension-feeding and predator structuresproduced by worm-like organisms persisted in high-energyintertidal areas (typically, sand flats exposed to high energywaves and currents) during the Paleozoic as revealed by thepresence of low-diversity suites of simple and U-shaped ver-tical burrows. However, decrease in the degree and depth ofbioturbation since the middle Paleozoic is apparent, as indi-cated by the decline in Skolithos piperock (Droser, 1991). Thereasons for this pattern are unclear, but major roles may havebeen played by the radiations of predators contributing to adecline in large sessile suspension-feeders (McIlroy andGarton, 2004) and greater spatial competition for the infaunalecospace, resulting from diversification established cladesduring the Ordovician radiation (Desjardins et al., 2010).

Post-Paleozoic intertidal deposits are typically dominat-ed by deep- to mid-tier crustacean structures, together withpolychaete and bivalve trace fossils (Mángano et al., 2002).Shallow-tier trace fossils tend to be particularly abundant insediments that have been stabilized by microbial binding. Theemergence of a tidal-flat community of modern aspect tookplace during the Mesozoic‒Cenozoic evolutionary phase. Theimportance of crustaceans, as well as polychaetes and modernbivalves, as key bioturbators in tidal flats cannot be overem-phasized, as revealed by observations in recent intertidal envi-ronments (e.g., Howard and Dörjes, 1972; Possey et al., 1991;Dittmann, 1996; Curran and Martin, 2003; DeWitt et al.,2003; Atkinson and Taylor, 2003; Kinoshita et al., 2003;Papaspyrou et al., 2005; Koo et al., 2007; Volkenborn et al.,2007, 2009; D’Andrea and DeWitt, 2009).

THE ROLE OF ECOSYSTEM ENGINEERING

The colonization of tidal flats can be understood as asteady increase in the importance of ecosystem engineering(Fig. 7). Undoubtedly, the Cambrian explosion itself wasassociated with ecosystem engineering (Erwin and Tweedt,


169

2012; Mángano and Buatois, 2014). Although the appear-ance of Treptichnus pedum in the Fortunian represents anincipient colonization of the infaunal ecospace, its impact ontidal-flat ecosystems may have been relatively limited. Amajor shift in benthic ecologic structure took place later inthe Cambrian (Agronomic Revolution of Seilacher, 1999).This second phase in the colonization of tidal flats was sig-naled by the establishment of a suspension-feeder infauna,increased complexity of the trophic web, coupling of benthosand plankton, and reorganization of the infaunal ecospace(Mángano and Buatois, 2004b, 2014). It is this second phasethat actually resulted in the establishment of a mixgroundecology (Mángano and Buatois, 2014). Skolithos piperock insand-flat deposits reveals high-density populations of sus-pension feeders, which may have moved and processed largeamounts of material, playing a major role in nutrient cycling,such as regeneration of nitrogen and phosphorus to the watercolumn, as observed in modern suspension-feeding commu-nities (Dame et al., 2001; Newell et al., 2005). Intense activ-ity of photosynthetic bacteria and infaunal burrowing inearly Paleozoic tidal flats may have promoted an unusualconcentration of organic detritus, microfauna and meiofauna,ultimately causing the immigration of other megafauna to theshore (microbial garden hypothesis of Mángano and Buatois,2004b). In modern environments, it has been noted that up toa tenfold increase of bacterial abundance can occur alongburrow walls (Papaspyrou et al., 2005). In this scenario,Syringomorpha may represent a feeding strategy linked tothe exploitation of microbial films on sand grains and meio-fauna in well-oxygenated sand flats characterized by abun-dant nutrients and water percolation.

Increased importance of ecosystem engineers in tidalflats is envisaged for the middle, and particularly, the latePaleozoic, mostly related to the activity of infaunal bivalves.High degrees of spatial heterogeneity have been extensivelydocumented in late Paleozoic tidal flats, most likely reflect-ing a complex partitioning of energy resources (Mángano etal., 2002). Whereas mobile, mostly detritus-feeder infaunaand epifauna, whose feeding and excreting activities mayprovide abundant particles in suspension, qualify as substratedestabilizers, sedentary infaunal organisms that build mucus-lined tubes reduce re-suspension and erosion, representingsediment stabilizers (Reise, 1985; Widdows and Brinsley,2002; Volkenborn et al., 2009). In Carboniferous tidal flats,the U-shaped, lined bivalve burrow Protovirgularia bidirec-tionalis may have acted as a sediment stabilizer, as suggest-ed by its preferential concentration in small mounds, whichresulted from trapping of the tide-transported sediment, cre-ating a patchy microtopography on the tidal-flat surface(Mángano et al., 2002). In contrast, structures produced bymobile detritus-feeding nuculanid bivalves, such asProtovirgularia rugosa and Lockeia ornata, were in all prob-ability sediment destabilizers (Mángano et al., 2002).

Overall, the emerging picture by the end of the Paleozoic isone of a significant role played by ecosystem engineers, par-ticularly in shaping, at least in part, the tidal-flat surface.

This tendency accentuated in the Mesozoic with the riseto dominance of the Modern Fauna. Not only efficient mod-ern bivalves, but also crustaceans (e.g., callianassids) andpolychaetes (e.g., arenicolids) were probably instrumental inproducing changes in geochemical gradients and in shapingthe tidal-flat landscape. Evidence of ecosystem engineeringin the Mesozoic is provided by the presence of fecal castingsdirectly associated with vertical burrows in Jurassic rippledsandstones, defining a distinctive pit-and-mound microto-pography (Mángano et al., 2013b). These structures are iden-tical to those produced by the lugworm Arenicola marina inmodern tidal flats. Burrowing by Arenicola marina activelymodifies the physical environment, resulting in the provisionof microhabitats within the burrow and changes of microto-pography, that in turn, further control the distribution of ben-thic biota (Volkenborn et al., 2009). As noted above, bivalvesare important ecosystem engineers in tidal flats. For exam-ple, the infaunal detritus feeder Macoma balthica is thoughtto be responsible for an upward diffusion of nutrients byextending its inhalant siphon up to the sediment surface(Schäfer, 1972). Fecal pellets released from the exhalentsiphon provide an organic substrate for heterotrophs, andexcreted metabolites generate important amounts of nutri-ents, therefore enhancing microbial growth and promotingthe establishment of bacteria-feeding benthos (Reise, 1985).Crustaceans undoubtedly have played a major role as ecosys-tem engineers since the Mesozoic decapod radiation (Förster,1985; Feldmann, 2003). Its paramount role as ecosystemengineers in modern tidal flats is well documented (e.g.,Posey et al., 1991; Dittmann, 1996; Curran and Martin,2003; Kinoshita et al., 2003; Koo et al., 2007; D’Andrea andDeWitt, 2009). For example, burrowing by the callianassidshrimp Glypturus acanthochirus profoundly affects the inter-tidal landscape by creating a widespread mounded topogra-phy (Curran and Martin, 2003). These mounds are stabilizedby microbial activity, making them highly resistant to ero-sion. In turn, the cohesive substrate is appropriate for colo-nization by the shrimp Upogebia vazquezi and the fiddlercrab Uca major (Curran and Martin, 2003).

TRENDS IN ALPHA AND GLOBAL ICHNODIVER-

SITY: THE ROLE OF TAPHONOMIC BIASES

Trends in ichnodiversity in tidal-flat settings do not dis-play a straightforward increase in trace-fossil richnessthrough time. However, global ichnodiversity and alphaichnodiversity (sensu Buatois and Mángano, 2013) displayparallel trajectories through the entire Phanerozoic. Bothglobal ichnodiversity and alpha ichnodiversity steadilyincreased through the Paleozoic. However, ichnodiversity of

170


Mesozoic‒Cenozoic tidal flats decreased with respect toPaleozoic levels. This pattern can be interpreted as a tapho-nomic bias. High diversity of shallow-tier trace fossils in thePaleozoic resulted from enhanced preservation due to theabsence of intense deeper tier infaunal reworking. In con-trast, post-Paleozoic tidal flats are characterized by the activ-ity of key bioturbators resulting in the dominance of deep- tomid-tier-dominated ichnofabrics (Mángano et al., 2002;Buatois and Mángano, 2011a).

CONCLUSIONS

1) Tidal-flat colonization can be summarized as five mainevolutionary phases:

i) the initial invasion by animals (earliest Cambrian),ii) the arthropod exploration (Cambrian‒Ordovician), iii) diversification and faunal turnover (Silurian‒

Devonian), iv) setting the stage for the Modern Fauna (Carboni-

ferous‒Permian), and v) infaunalization and the role of crustaceans

(Mesozoic‒Cenozoic).

2) An incipient colonization of tidal flats took place in theFortunian as indicated by the presence of monospecificsuites of Treptichnus pedum. This was followed by theestablishment of an intertidal fauna dominated by mol-lusc-like animals, euthycarcinoids and trilobites. EarlyPaleozoic tidal flats were markedly anactualistic,reflecting reduced predation pressures, absence of ter-restrially derived food and microbial binding. The rest ofthe Paleozoic was characterized by faunal replacementsand a continuous increase in ichnodiversity, with theinvasion of new tracemakers. The association of largedeep-tier Lockeia siliquaria and the anomalodesmatanWilkingia in Carboniferous tidal-flat deposits suggestsrelatively deep burrowing by siphon-feeding infaunalbivalves, well before the advent of the Mesozoic marinerevolution. Mesozoic‒Cenozoic tidal-flat ichnofaunasare dominated by deep-tier bioturbators, particularlycrustaceans, as well as polychaetes and bivalves. Therole of ecosystems engineers increased through thePhanerozoic, reaching a peak during this latter phasewith active modification of the intertidal landscape byinfaunal bioturbators.

3) Global ichnodiversity and alpha ichnodiversity steadilyincreased through the Paleozoic. However, both alphaand global ichnodiversity show a decrease by theMesozoic‒Cenozoic in comparison with Paleozoic lev-els. This pattern most likely reflects a preservationalbias, resulting from increased shallow-tier destructionby deep- to mid-tier key bioturbators in post-Paleozoictimes.

ACKNOWLEDGMENTS

Financial support for this study was provided by NaturalSciences and Engineering Research Council (NSERC)Discovery Grants 311727-05/08 and 311726-05/08/13awarded to Mángano and Buatois, respectively. AndrewRindsberg helped us to improve the manuscript through acareful revision and Margaret Bradshaw provided valuableinsights into the Devonian of Antarctica.

REFERENCES

Astini, R.A., Mángano, M.G. and Thomas, W.A., 2000, Elicnogénero Cruziana en el Cámbrico Temprano de laPrecordillera Argentina: El registro más antiguo deSudamérica. Revista de la Asociación GeológicaArgentina, v. 55, p. 111-120.

Atkinson, R.J.A. and Taylor, A.C., 2003, Aspects of the biol-ogy and ecophysiology of thalassinidean shrimps inrelation to their burrow environment, in Tamaki, A., ed.,Proceedings of the Symposium on “Ecology of LargeBioturbators in Tidal Flats and Shallow SublittoralSediments – From Individual Behavior to their Role asEcosystem Engineers”, p. 45-52.

Augustinus, P., 2002, Biochemical factors influencing depo-sition and erosion of fine-grained sediment, in Healy, T.,Wang, Y. and Healy, J.A., eds., Muddy Coasts of theWorld: Processes, Deposits, and Function. Proceedingsin Marine Science, no. 4, p. 203-228.

Baucon, A. and Avanzini, M., 2008, Zoophycos-like struc-tures associated with dinosaur tracks in a tidal-flat envi-ronment: Lower Jurassic (Southern Alps, Italy). StudiTrentini di Scienze Naturali, Acta Geologica, v. 83, p.123-131.

Bromley, R.G. and Uchman, A., 2003, Trace fossils from theLower and Middle Jurassic marginal marine deposits ofthe Sorthat Formation, Bornholm, Denmark. Bulletin ofthe Geological Society of Denmark, v. 52, p. 185-208.

Boyd, R., Dalrymple, R.W. and Zaitlin, B.A., 2006,Estuarine and incised-valley facies models, inPosamentier, H.W. and Walker, R., eds., Facies ModelsRevisited. SEPM Special Publication 84, p. 175-240.

Bradshaw, M.A., 2010, Devonian trace fossils of the HorlickFormation, Ohio Range, Antarctica: Systematic descrip-tion and palaeoenvironmental interpretation. Ichnos, v.17, p. 58-114.

Buatois, L.A. and Mángano, M.G., 1993, Ecospace utiliza-tion, paleoenvironmental trends and the evolution ofearly nonmarine biotas. Geology, v. 21, p. 595-598.

Buatois, L.A. and Mángano, M.G., 2011a, Ichnology:Organism-substrate Interactions in Space and Time.Cambridge University Press, 358 p.

Buatois, L.A. and Mángano, M.G., 2011b, The trace-fossilrecord of organism-matground interactions in space and


171

time, in Noffke, N. and Chafez, H., eds., Microbial Matsin Siliciclastic Sediments. SEPM Special Publication101, p. 15-28.

Buatois, L.A. and Mángano, M.G., 2013, Ichnodiversity andichnodisparity: Significance and caveats. Lethaia, v. 46,p. 281-292.

Buatois, L.A., Mángano, M.G., Genise, J.F. and Taylor, T.N.,1998, The ichnologic record of the invertebrate invasionof nonmarine ecosystems: evolutionary trends in eco-space utilization, environmental expansion, and behav-ioral complexity. Palaios, v. 13, p. 217-240.

Buatois, L.A., Gingras, M.K., MacEachern, J., Mángano,M.G., Zonneveld, J.-P, Pemberton, S.G., Netto, R.G. andMartin, A.J., 2005, Colonization of brackish-water sys-tems through time: Evidence from the trace-fossilrecord. Palaios, v. 20, p. 321-347.

Buatois, L.A., Almond, J. and Germs, G.J.B., 2013, Environ-mental tolerance and range offset of Treptichnus pedum:Implications for the recognition of the Ediacaran-Cambrian boundary. Geology, v. 41, p. 519-522.

Carmona, N.B., Buatois, L.A., Mángano, M.G. and Bromley,R.G., 2008, Ichnology of the lower Miocene ChenqueFormation, Patagonia, Argentina: Animal-substrateinteractions and the Modern evolutionary fauna.Ameghiniana, v. 45, p. 93-122.

Carter, C.H., 1975, Miocene-Pliocene beach and tidaldeposits, southern New Jersey, in Ginsburg, R.N., ed.,Tidal Deposits. A Casebook of Recent Examples andFossil Counterparts. Springer-Verlag, New York, p. 109-116.

Chamberlain, C.K., 1980, Depositional environment of theDakota Formation at Denver (Stop 4), in Basan, P.B.,Chamberlain, C.K., Fischer, W.A. and Scott, R.W., eds.,Trace Fossils of Nearshore Environments of Cretaceousand Ordovician Rocks, Front Range, Colorado. GuideBook for SEPM Field Trip no. 1, p. 30-41.

Chang, T.S., Flemming, B.W. and Bartholomä, A., 2007,Distinction between sortable silts and aggregates inmuddy intertidal sediments of the East Frisian WaddenSea, southern North Sea. Sedimentary Geology, v. 202,p. 453-463.

Collette, J.H. and Hagadorn, J.W., 2010, Three-dimensional-ly preserved arthropods from Cambrian lagerstätten ofQuébec and Wisconsin. Journal of Paleontology, v. 84,p. 646-667.

Collette, J.H., Hagadorn, J.W. and Lacelle, M.A., 2010, Deadin their tracks – Cambrian arthropods and their tracesfrom intertidal sandstones of Québec and Wisconsin.Palaios, v. 25, p. 475-486.

Collette, J.H., Gass, K.C. and Hagadorn, J.W., 2012,Protichnites eremita unshelled? Experimental model-based neoichnology and new evidence for aEuthycarcinoid affinity for this ichnospecies. Journal ofPaleontology, v. 86, p. 442-454.

Cornish, F.G., 1986, The trace-fossil Diplocraterion; evi-dence of animal-sediment interactions in Cambrian tidaldeposits. Palaios, v. 5, p. 478-491.

Crimes, T.P., 1974, Colonization of the early ocean floor.Nature, v. 248, p. 328-330.

Curran, H.A. and Martin, A.J., 2003, Complex decapod bur-rows and ecological relationships in modern andPleistocene intertidal carbonate environments, SanSalvador Island, Bahamas. Palaeogeography, Palaeocli-matology, Paleoecology, v. 192, p. 229-245.

Dalrymple, R.W., 2010, Tidal Depositional Systems, inJames, N. and Dalrymple, R., eds., Facies Models. 4thEdition. Geological Association of Canada, p. 201-231.

Dalrymple, R.W. and Choi, K., 2007, Morphologic faciestrends through the fluvial-marine transition in tide-dom-inated depositional systems: A schematic framework forenvironmental and sequence-stratigraphic interpretation.Earth-Science Reviews, v. 81, p. 135-174.

Dalrymple, R.W. and Rhodes, R.N., 1995, Estuarine dunesand bars, in Perillo, G.M.E., ed., Geomorphology andSedimentology of Estuaries. Elsevier, Amsterdam,Developments in Sedimentology, v. 53, p. 359-406.

Dalrymple, R.W., Knight, R.J., Zaitlin, B.A. and Middleton,G.V., 1990, Dynamics and facies model of a macrotidalsand-bar complex, Cobequid Bay-Salmon River estuary(Bay of Fundy). Sedimentology, v. 37, p. 577-612.

Dame, R.F., Bushek, D. and Prins, T.C., 2001, Benthic sus-pension feeders as determinants of ecosystem structureand function in shallow coastal waters, in Reise, K., ed.,Ecological Comparisons of Sedimentary Shores.Ecological Studies, v. 151, p. 11-37.

D’Andrea, A.F. and DeWitt, T.H., 2009, Geochemicalecosystem engineering by the mud shrimp Upogebiapugettensis (Crustacea: Thalassinidae) in Yaquina Bay,Oregon: Density-dependent effects on organic matterremineralization and nutrient cycling. Limnology andOceanography, v. 54, p. 1911-1932

Davies, N.S., Sansom, I.J. and Turner, P., 2006, Trace fossilsand paleoenvironments of a Late Silurian marginal-marine/alluvial system: the Ringerike Group (LowerOld Red Sandstone), Oslo region, Norway. Palaios, v.21, p. 46-62.

Desjardins, P.R., Mángano, M.G., Buatois, L.A. and Pratt,B.R., 2010, Skolithos pipe rock and associated ichnofab-rics in the Fort Mountain Formation, Gog Group:Colonization trends and environmental controls in anEarly Cambrian subtidal sandbar complex. Lethaia, v.43, p. 507-528.

Desjardins, P.R., Buatois, L.A. and Mángano, M.G., 2012a,Tidal flat and subtidal sand bodies, in Knaust, D. andBromley, R.G., eds., Trace Fossils as Indicators ofSedimentary Environments. Developments in Sedimen-tology, Elsevier, v. 64, p. 529-562.

172


Desjardins, P.R., Buatois, L.A., Pratt, B.R. and Mángano,M.G., 2012b Forced-regressive tidal flats: response tofalling sea level in tide-dominated settings. Journal ofSedimentary Research, v. 82, p. 149-162.

de Boer, P.L., 1998, Intertidal sediments: Composition andstructure, in Eisma, D., ed., Intertidal Deposits: RiverMouths, Tidal Flats and Coastal Lagoons. CRC Press,Boca Raton, p. 912-921.

Dewitt, T.H., D’Andrea, A.F., Brown, C.A., Griffen, B.D.and Eldridge, P.M., 2003, Impact of burrowing shrimppopulations on nitrogen cycling and water quality inwestern North American temperate estuaries, in Tamaki,A., ed., Proceedings of the Symposium on “Ecology ofLarge Bioturbators in Tidal Flats and ShallowSublittoral Sediments – From Individual Behavior totheir Role as Ecosystem Engineers”, p. 107-118.

Dittmann, S., 1996, Effects of macrobenthic burrows oninfaunal communities in tropical tidal flats. MarineEcology and Progress Series, v. 134, p. 119-130.

Draganits, E., Braddy, S.J. and Briggs, D.E.G., 2001, AGondwanan coastal arthropod ichnofauna from theMuth Formation (Lower Devonian, northern India):Paleoenvironment and tracemaker behavior. Palaios, v.16, p. 126-147.

Driese, S.G., Byers, C.W. and Dott, R.H., Jr., 1981, Tidaldeposition in the basal Upper Cambrian Mt. SimonFormation in Wisconsin. Journal of SedimentaryResearch, v. 51, p. 367-381.

Droser, M.L., 1991, Ichnofabric of the Paleozoic Skolithosichnofacies and the nature and distribution of theSkolithos piperock. Palaios, v. 6, p. 316-325.

Durand, J., 1985, Le Gres Armoricain. SédimentologieTraces fossiles. Milieux de dépôt: Centre Armoricaind'Étude structurale des Socles, Mémoires et Documents,v. 3, p. 1-150.

Erwin, D.H. and Tweedt, S., 2012, Ecological drivers of theEdiacaran-Cambrian diversification of Metazoa.Evolutionary Ecology, v. 26, p. 417-433.

Feldmann, R.M., 2003, The Decapoda: new initiatives andnovel approaches. Journal of Paleontology, v. 77, p.1021-1039.

Fenton, C.L. and Fenton, M.A., 1937, Trilobite “nests” andfeeding burrows. American Midland Naturalist, v. 18, p.446-451.

Fernández, D. and Pazos, P., 2013, Xiphosurid trackways ina Lower Cretaceous tidal flat in Patagonia: Palaeoeco-logical implications and the involvement of microbialmats in trace-fossil preservation. Palaeogeography,Palaeoclimatology, Palaeoecology, v. 375, p. 16-29.

Flemming, B.W., 2012, Siliciclastic back-barrier tidal flats,in Davis, R.A., Jr. and Dalrymple, R.W., eds., Principlesof Tidal Sedimentology. Springer-Verlag, Dordrecht, p.231-267.

Förster, R., 1985, Evolutionary trends and ecology ofMesozoic decapod crustaceans. Transactions of theRoyal Society of Edinburgh, v. 76, p. 299-304.

Frey, R.W., Hong, J.S., Howard, J.D., Park, B.K. and Han,S.J., 1987a, Zonation of benthos on a macrotidal flat,Inchon, Korea. Senckenbergiana Maritima, v. 19, p.295-329.

Frey, R.W., Howard, J.D. and Hong, J.S., 1987b, PrevalentLebensspuren on a modern macrotidal flat, Inchon,Korea: Ethological and environmental significance.Palaios, v. 2, p. 571-593.

Getty, P.R. and Hagadorn, J.W., 2008, Reinterpretation ofClimactichnites Logan 1860 to include subsurface bur-rows, and erection of Musculopodus for resting traces ofthe trailmaker. Journal of Paleontology, v. 82, p. 1161-1172.

Getty, P.R. and Hagadorn, J.W., 2009, Palaeobiology of theClimactichnites tracemaker. Palaeontology, v. 52, p.753-778.

Geyer, G., 2005, The Fish River Subgroup in Namibia:stratigraphy, depositional environments and theProterozoic-Cambrian boundary problem revisited.Geological Magazine, v. 142, p. 465-498.

Geyer, G. and Uchman, A., 1995, Ichnofossil assemblagesfrom the Nama Group (Neoproterozoic-LowerCambrian) in Namibia and the Proterozoic-Cambrianboundary problem revisited. Beringeria Special Issue, v.2, p. 175-202.

Goodwin, P.W. and Anderson, E.J., 1974, Associated physi-cal and biogenic structures in environmental subdivisionof a Cambrian tidal sand body. Journal of Geology, v. 82,p. 779-794.

Gould, S.J., 1987, Time’s Arrow Time’s Cycle. HarvardUniversity Press, Cambridge, Massachusetts, 222 p.

Greb, S.F. and Chesnut, D.R., Jr., 1994, Paleoecology of anestuarine sequence in the Breathitt Formation(Pennsylvanian), central Appalachian Basin. Palaios, v.9, p. 388-402.

Hagadorn, J.W. and Belt, E.D., 2008, Stranded in UpstateNew York: Cambrian Scyphomedusae from the PotsdamSandstone. Palaios, v. 23, p. 424-441.

Hagadorn, J.W. and Seilacher, A., 2009, Hermit arthropods500 million years ago? Geology, v. 37, p. 295-298.

Hagadorn, J.W., Dott, R.H. and Damrow, D., 2002, Strandedon an Upper Cambrian shoreline: Medusae from centralWisconsin. Geology, v. 30, p. 147-150.

Hagadorn, J.W., Collette, J.H. and Belt, E.D., 2011, Eolian-aquatic deposits and faunas of the Middle CambrianPostdam Group. Palaios, v. 26, p. 314-334.

Häntzschel, W. and Reineck, H.E., 1968, Fazies-Untersuchungen im Hettangium von Helmstedt(Niedersachsen). Mitteilungen aus dem GeologischenStaatsinstitut in Hamburg, v. 37, p. 5-39.


173

Howard, J.D. and Dörjes, J., 1972, Animal-sediment rela-tionships in two beach-related tidal flats; Sapelo Island,Georgia. Journal of Sedimentary Petrology, v. 42, p.608-623.

Ireland, R.J., Pollard, J.E., Steel, R.J. and Thompson, D.B.,1978, Intertidal sediments and trace fossils from theWaterstones (Scythian-Anisian?) at Daresbury,Cheshire. Proceedings of the Yorkshire GeologicalSociety, v. 41, p. 399-436.

Jensen, S., 1990, Predation by early Cambrian trilobites oninfaunal worms - evidence from the Swedish MickwitziaSandstone. Lethaia, v. 23, p. 29-42.

Johnson, M.E. and Baarli, B.G., 2012, Development of inter-tidal biotas through Phanerozoic times, in Talent, J.A.,ed., Earth and Life. Global Biodiversity, ExtinctionIntervals and Biogeographic Perturbations ThroughTime. Springer Science, Berlin, p. 63-128.

Kinoshita, K., Wada, M., Kogure, K. and Furota, T., 2003,Mud shrimp burrows as dynamic traps and processors oftidal-flat materials. Marine Ecology Progress Series, no.247, p. 159-164.

Klein, G. de V., 1971, A sedimentary model for determiningpaleotidal range. Geological Society of AmericaBulletin, v. 82, p. 2585-2592.

Klein, G. de V., 1977, Clastic Tidal Facies. CEPCO,Champaign, Illinois, 149 p.

Knaust, D., 2010, Remarkably preserved benthic organismsand their traces from a Middle Triassic (Muschelkalk)mud flat. Lethaia, v. 43, p. 344-356.

Koo, B.J., Kwon, K.K. and Hyun, J.H., 2007, Effect of envi-ronmental conditions on variation in the sediment-waterinterface created by complex macrofaunal burrows on atidal flat. Journal of Sea Research, v. 58, p. 302-312.

Kumar, A., 1978, Some trace fossils from Clinton RedSandstone (Early Silurian) from Harrisburg area,Pennsylvania, and their environmental significance.Journal of the Palaeontological Society of India, v. 21-22, p. 29-32.

MacEachern, J.A., Bann, K.L., Pemberton, S.G. and Gingras,M.K., 2007, The ichnofacies paradigm: High-resolutionpaleoenvironmental interpretation of the rock record, inMacEachern, J.A., Bann, K.L., Gingras, M.K. andPemberton, S.G., eds., Applied Ichnology. Society forSedimentary Geology Short Course Notes, v. 52, p. 27-64.

MacKenzie, D.B., 1972, Tidal sand flat deposits in LowerCretaceous Dakota Group near Denver, Colorado. TheMountain Geologist, v. 9, p. 269-277.

MacKenzie, D.B., 1975, Tidal sand flat deposits in LowerCretaceous Dakota Group near Denver, Colorado, inGinsburg, R.N., ed., Tidal Deposits. A Casebook ofRecent Examples and Fossil Counterparts. Springer-Verlag, New York, p. 116-126.

MacNaughton, R.B., Cole, J.M., Dalrymple, R.W., Braddy,S.J., Briggs, D.E.G. and Lukie, T.D., 2002, First steps on

land: Arthropod trackways in Cambrian-Ordovicianeolian sandstone, southeastern Ontario, Canada.Geology, v. 5, p. 391-394.

Mángano, M.G. and Buatois, L.A., 2003a, Rusophycusleifeirikssoni en la Formación Campanario:Implicancias paleobiológicas, paleoecológicas y pale-oambientales, in Buatois, L.A. and Mángano, M.G., eds.,Icnología: Hacia una convergencia entre geología ybiología. Publicación Especial de la AsociaciónPaleontológica Argentina, v. 9, p. 65-84.

Mángano, M.G. and Buatois, L.A., 2003b, Trace Fossils, inBenedetto, J.L., ed., Ordovician Fossils of Argentina.Universidad Nacional de Córdoba, Secretaría de Cienciay Tecnología, p. 507-553.

Mángano, M.G. and Buatois, L.A., 2004a, Ichnology ofCarboniferous tide-influenced environments and tidalflat variability in the North American Midcontinent, inMcIlroy, D., ed., The Application of Ichnology toPalaeoenvironmental and Stratigraphic Analysis.Geological Society, Special Publication 228, p. 157-178.

Mángano, M.G. and Buatois, L.A., 2004b, Reconstructingearly Phanerozoic intertidal ecosystems: Ichnology ofthe Cambrian Campanario Formation in northwestArgentina, in Webby, B.D., Mángano, M.G. and Buatois,L.A., eds., Trace Fossils in Evolutionary Palaeoecology.Fossils and Strata, v. 51, p. 17-38.

Mángano, M.G. and Buatois, L.A., 2007, Trace fossils inevolutionary paleoecology, in Miller, W. III, ed., TraceFossils. Elsevier, p. 391-409.

Mángano, M.G. and Buatois, L.A., 2012, A multifacetedapproach to ichnology. Ichnos, v. 19, p. 121-126.

Mángano, M.G. and Buatois, L.A., 2014, Decoupling ofbody-plan diversification and ecological structuring dur-ing the Ediacaran-Cambrian transition: Evolutionaryand geobiological feedbacks. Proceedings of the RoyalSociety, Biological Sciences, no. 281.

Mángano, M.G. and Droser, M.L., 2004, The ichnologicrecord of the Ordovician radiation, in Webby, B.D.,Paris, F., Droser, M.L. and Percival, I.G., eds., The GreatOrdovician Biodiversification Event. ColumbiaUniversity Press, New York, p. 369-379.

Mángano, M.G., Buatois, L.A. and Aceñolaza, G.F., 1996,Trace fossils and sedimentary facies from an EarlyOrdovician tide-dominated shelf (Santa RositaFormation, northwest Argentina): Implications for ich-nofacies models of shallow marine successions. Ichnos,v. 5, p. 53-88.

Mángano, M.G., Buatois, L.A., West, R.R. and Maples, C.G.,1998, Contrasting behavioral and feeding strategiesrecorded by tidal-flat bivalve trace fossils from theUpper Carboniferous of eastern Kansas. Palaios, v. 13,p. 335-351.

Mángano, M.G., Buatois, L.A. and Moya, M.C., 2001,Trazas fósiles de trilobites de la Formación Mojotoro

174


(Ordovícico inferior-medio de Salta, Argentina):Implicancias paleoecológicas, paleobiológicas y bioes-tratigráficas. Revista Española de Paleontología, v. 16,p. 9-28.

Mángano, M.G., Buatois, L.A., West, R.R. and Maples, C.G.,2002, Ichnology of a Pennsylvannian equatorial tidalflat: The Stull Shale Member at Waverly, EasternKansas. Kansas Geological Survey Bulletin, no. 245, p.1-133.

Mángano, M.G., Buatois, L.A., Hofmann, R., Elicki, O. andShinaq, R., 2013a, Exploring the aftermath of theCambrian Explosion: The evolutionary significance ofmarginal- to shallow-marine ichnofaunas of Jordan.Palaeogeography, Palaeoclimatology, Palaeoecology, v.374, p. 1-15.

Mángano, M.G., Piñuela, L., García-Ramos, J.C., Buatois,L.A., Rodríguez-Tovar, F.J. and Volkenborn, N., 2013b,Exceptional preservation of Upper Jurassic fecalmounds and the fossil record of ecosystem engineers.XII International Ichnofabric Workshop.

Mángano, M.G., Buatois, L.A., Astini, R. and Rindsberg,A.K., 2014, Trilobites in early Cambrian tidal flats andthe landward expansion of the Cambrian explosion.Geology, v. 42, p. 143-146.

Martino, R.L., 1989, Trace fossils from marginal marinefacies of the Kanawa Formation (MiddlePennsylvanian), West Virginia. Journal of Paleontology,v. 63, p. 389-403.

Mason, T.R. and Christie, A.D.M., 1986, Palaeoenviron-mental significance of the ichnogenus DiplocraterionTorell from the Permian Vryheid Formation of the KarooSupergroup, South Africa. Palaeogeography, Palaeocli-matology, Palaeoecology, v. 52, p. 249-265.

McIlroy, D., 2004, Ichnofabrics and sedimentary facies of atide-dominated delta: Jurassic Ile Formation of KristinField, Haltenbanken, Offshore Mid-Norway, in McIlroy,D., ed., The Application of Ichnology to Palaeoenviron-mental and stratigraphic analysis. Geological Society,London, Special Publications, 228, p. 237-272.

McIlroy, D., 2007, Ichnology of a macrotidal tide-dominateddeltaic depositional system: Lajas Formation, NeuquénProvince, Argentina, in Bromley, R.G., Buatois, L.A.,Mángano, M.G., Genise, J.F. and Melchor, R.N., eds.,Sediment-Organism Interactions; A MultifacetedIchnology. SEPM Special Publication, v. 88, p. 195-211.

McIlroy, D. and Garton, M., 2004, A worm’s eye view of theearly Palaeozoic sea floor. Geology Today, v. 20, p. 224-230.

McIlroy, D., Flint, S., Howell, J.A. and Timms, N., 2005,Sedimentology of the tide-dominated Jurassic LajasFormation, Neuquén Basin, Argentina, in Veiga, G.D.,Spalletti, L.A., Howell J.A. and Schwarz, E., eds., TheNeuquén Basin, Argentina: A Case Study in Sequence

Stratigraphy and Basin Dynamics. Geological Society,London, Special Publications, 252, p. 83-107.

Miller, M.F., 1979, Paleoenvironmental distribution of tracefossils in the Catskill deltaic complex, New York State.Palaeogeography, Palaeoclimatology, Palaeoecology, v.28, p. 117-141.

Miller, M.F., 1991, Morphology and paleoenvironmental dis-tribution of Paleozoic Spirophyton and Zoophycos:implications for the Zoophycos ichnofacies. Palaios, v.6, p. 410-425.

Miller, M.F. and Johnson, K.G., 1981, Spirophyton in allu-vial-tidal facies of the Catskill deltaic complex: Possiblebiological control of ichnofossil distribution. Journal ofPaleontology, v. 55, p. 1016-1027.

Miller, M.F. and Knox, L.W., 1985, Biogenic structures anddepositional environments of a Lower Pennsylvaniancoal-bearing sequence, northern Cumberland Plateau,Tennessee, U.S.A., in Curran, H.A., ed., BiogenicStructures: Their Use in Interpreting DepositionalEnvironments. Society of Economic Paleontologists andMineralogists, Special Publication, v. 35, p. 67-97.

Narbonne, G.M., 1984, Trace fossils in Upper Silurian tidalflat to basin slope carbonates of Arctic Canada. Journalof Paleontology, v. 58, p. 398-415.

Neto de Carvalho, C., 2006, Roller coaster behavior in theCruziana rugosa Group from Penha Garcia (Portugal):Implications for the feeding program of trilobites.Ichnos, v. 13, p. 255-265.

Newell, R.I.E., Holyoke, R.R. and Cornwell, J.C., 2005,Influence of eastern oysters on nitrogen and phosphorusregeneration in Chesapeake Bay, USA., in Dame, R.F. andOleni, S., eds., The Comparative Roles of Suspension-feeders in Ecosystems. NATO Science Series, IV, Earthand Environmental Sciences, no. 47, p. 93-120.

Noffke, N., Eriksson, K.A., Hazen, R.M. and Simpson, E.L.,2006, A new window into Early Archean life: Microbialmats in Earth's oldest siliciclastic tidal deposits (3.2 GaMoodies Group, South Africa). Geology, v. 34, p. 252-256.

Noffke, N., Beukes, N., Bower, D., Hazen, R.M. and Swift,D.J.P., 2008, An actualistic perspective into Archeanworlds – (cyano-)bacterially induced sedimentary struc-tures in the siliciclastic Nhlazatse Section, 2.9 GaPongola Supergroup, South Africa. Geobiology, v. 6, p.5-20.

Orr, P.J., 2001, Colonization of the deep-marine environmentduring the early Phanerozoic: The ichnofaunal record.Geological Journal, v. 36, p. 265-278.

Papaspyrou, S., Gregersen, T., Cox, R.P., Thessalou-Legaki,M., Kristensen, E., 2005, Sediment properties and bac-terial community in burrows of the ghost shrimpPestarella tyrrhena (Decapoda: Thalassinidea). AquaticMicrobial Ecology, v. 38, p. 181-190.


175

Pollard, J.E. and Steel, R.J., 1978, Intertidal sediments in theAuchenhew Beds (Triassic) of Arran. Scottish Journal ofGeology, v. 14, p. 317-328.

Poschmann, M. and Braddy, S.J., 2010, Eurypterid track-ways from Early Devonian tidal facies of Alken an derMosel (Rheinisches Schiefergebirge, Germany). Palaeo-biology and Palaeoenvironments, v. 90, p. 111-124.

Potter, P.E., Maynard, J.B. and Depetris, P.J., 2005, Mud andMudstone: Introduction and overview. Springer-Verlag,Berlin, 297 p.

Posey, M.H., Dumbauld, B.R. and Armstrong, B.A., 1991,Effects of a burrowing mud shrimp, Upogebia pugetten-sis (Dana), on abundances of macro-infauna. Journal ofExperimental Marine Biology and Ecology, v. 148, p.283-294.

Reineck, H.-E., 1967, Layered sediments of tidal flat beach-es, and shelf bottoms of the North Sea, in Lauff, G.H.,ed., Estuaries. American Association for the Advance-ment of Science, Special Publication, no. 83, p. 191-206.

Reineck, H.-E. and Singh, I.B., 1980, DepositionalSedimentary Environments. 2nd edition. Springer-Verlag, Berlin, 551 p.

Reise, K., 1985, Tidal Flat Ecology. An experimentalapproach to species interactions. Ecological Studies, no.54. Springer-Verlag, Berlin, Heidelberg, 191 p.

Reise, K., 2002, Sediment mediated species interactions incoastal waters. Journal of Sea Research, v. 48, p. 127-141.

Richards, M.T., 1994, Transgression of an estuarine channeland tidal flat complex: the Lower Triassic of Barles,Alpes de Haute, Provence, France. Sedimentology, v.41, p. 55-82.

Rindsberg, A.K., 1994, Ichnology of the UpperMississippian Hartselle Sandstone of Alabama, withnotes on other Carboniferous formations. GeologicalSurvey of Alabama Bulletin, no. 158, p. 1-107.

Sanders, H.L., 1968, Marine benthic diversity: A compara-tive study. American Naturalist, v. 102, p. 243-282.

Sanders, H.L., 1969, Marine benthic diversity and the stabil-ity-time hypothesis. Brookhaven Symposia on Biology,no. 22, p. 71-81.

Schäfer, W., 1972, Ecology and Palaeoecology of MarineEnvironments. Chicago University Press, Chicago, 568 p.

Schieber, J., 2007, Ripple patches in the Cretaceous DakotaSandstone near Denver, Colorado, a classical locality formicrobially bound tidal sand flat, in Schieber, J., Bose,P.K., Eriksson, P.G., Banerjee, S., Sarkar, S., Altermann,W. and Catuneanu, O., eds., Atlas of Microbial MatFeatures Preserved within the Siliciclastic Rock Record.Atlases in Geology, no. 2, p. 22-224.

Seilacher, A., 1970, Cruziana stratigraphy of “non fossilifer-ous” Palaeozoic sandstones, in Crimes, T.P. and Harper,J.C., eds., Trace Fossils 2. Geological Journal SpecialIssue, no. 3, p. 447-476.

Seilacher, A., 1974, Flysch trace fossils: Evolution of behav-ioural diversity in the deep-sea. Neues Jahrbuch fürGeologie und Palaontologie, Monatshefte, 1974, p. 233-245.

Seilacher, A., 1977, Evolution of trace fossil communities, inHallam, A., ed., Patterns of Evolution. Elsevier,Amsterdam, p. 359-376.

Seilacher, A., 2008, Biomats, biofilms, and bioglue as preserva-tional agents for arthropod trackways. Palaeogeography,Palaeoclimatology, Palaeoecology, v. 270, p. 252-257.

Seilacher, A. and Hagadorn, J.W., 2010, Early molluscanevolution: Evidence from the trace-fossil record.Palaios, v. 25, p. 565-575.

Seilacher, A. and Seilacher, E., 1994, Bivalvian trace fossils:A lesson from actuopaleontology. Courier Forschung-sinstitut Institut Senckenberg, v. 169, p. 5-15.

Sellwood, B.W., 1975, Lower Jurassic tidal-flat deposits,Bornhom, Denmark, in Ginsburg, R.N., ed., TidalDeposits. A Casebook of Recent Examples and FossilCounterparts. Springer-Verlag, New York, p. 93-104.

Sepkoski, J.J., Jr. and Miller, A.I., 1985, Evolutionary faunasand the distribution of Paleozoic benthic communities inspace and time, in Valentine, J.W., ed., PhanerozoicDiversity Patterns: Profiles in Macroevolution.Princeton University Press, p. 153-190.

Šimo, V. and Olšavsky, M., 2007, Diplocraterion parallelumTorell, 1870, and other trace fossils from the LowerTriassic succession of the Drienok Nappe in the WesternCarpathians, Slovakia. Bulletin of Geosciences, v. 82, p.165-173.

Simpson, E.L., 1991, An exhumed, Lower Cambrian tidalflat: the Antietam Formation, central Virginia, U.S.A., inSmith, D.G., Reinson, G.E., Zaitlin, B.A. and Rahmani,R.A., eds., Clastic Tidal Sedimentology. CanadianSociety of Petroleum Geologists, Memoir 16, p. 123-134.

Skoog, S.Y., Venn, C. and Simpson, E.L., 1994, Distributionof Diopatra cuprea across modern tidal flats: implica-tions for Skolithos. Palaios, v. 9, p. 188-201.

Slobodkin, L.B. and Sanders, H.L., 1969, On the contribu-tion of environmental predictability to species diversity.Brookhaven Symposia on Biology, no. 22, p. 82-95.

Stanley, S.M., 1968, Post-Paleozoic adaptative radiation ofinfaunal bivalve molluscs - A consequence of mantlefusion and siphon formation. Journal of Paleontology, v.42, p. 214-229.

Stanley, S.M., 1970, Relation of shell form to life habits ofthe Bivalvia (Mollusca). Geological Society of America,Memoir 25, p. 1-269.

Stanley, S.M., 1972, Functional morphology and evolutionof byssally attached bivalve mollusks. Journal ofPaleontology, v. 46, p. 165-212.

Straaten, L.M.J. van., 1954, Composition and structure ofrecent marine sediments in the Netherlands. LeidseGeologische Mededelingen, v. 19, p. 1-110.

176


Swinbanks, D.D. and Murray, J.W., 1981, Biosedimentolog-ical zonation of Boundary Bay tidal flats, Fraser RiverDelta, British Columbia. Sedimentology, v. 28, p. 201-237.

Theron, J.N. and. Loock, J.C., 1988, Devonian deltas of theCape Supergroup, South Africa. Devonian of the World.Proceedings of the 2nd International Symposium on theDevonian System — Memoir 14, Volume I: RegionalSyntheses, South America and Southern Africa, p. 729-740.

Thomas, W.A. and Astini, R.A., 1996, The ArgentinePrecordillera: A traveler from the Ouachita embaymentof North American Laurentia. Science, v. 273, p. 752-757.

Thomas, W.A. and Astini, R.A., 2003, Ordovician accretionof the Argentine Precordillera terrane to Gondwana: Areview. Journal of South American Earth Sciences, v. 16,p. 67-79.

Trewin, N.H. and McNamara, K.J., 1995, Arthropods invadethe land: Trace fossils and palaeoenvironments of theTumblagooda Sandstone (?late Silurian) of Kalbarri,Western Australia. Transactions of the Royal Society ofEdinburgh: Earth Sciences, v. 85, p. 177-210.

Trueman, E.R., 1966, Bivalve molluscs: Fluid dynamics ofburrowing. Science, v. 152, p. 523-525.

Trueman, E.R., Brand, A.R. and Davis, P., 1966, The effectof substrate and shell shape on the burrowing of somecommon bivalves. Proceedings of the MalacologicalSociety of London, v. 37, p. 97-109.

Twitchett, R.J. and Barras, C.G., 2004, Trace fossils in theaftermath of mass extinction events, in McIlroy, D., ed.,The Application of Ichnology to Palaeoenvironmentaland Stratigraphic Analysis. Geological Society SpecialPublication 228, p. 397-418.

Uchman, A., 2003, Trends in diversity, frequency and com-plexity of graphoglyptid trace fossils: Evolutionary andpalaeoenvironmental aspects. Palaeogeography, Palaeo-climatology and Palaeoecology, v. 192, p. 123-142.

Uchman, A., 2004, Phanerozoic history of deep-sea tracefossils, in McIlroy, D., eds., The Application ofIchnology to Palaeoenvironmental and StratigraphicAnalysis. Geological Society Special Publication 228, p.125-139.

Vermeij, G.J., 1987, Evolution and Escalation. An EcologicalHistory of Life. Princeton University Press, Princeton,544 p.

Volkenborn, N., Hedtkamp, S.I.C., van Beusekom, J.E.E. andReise, K., 2007, Effects of bioturbation and bioirrigationby lugworms (Arenicola marina) on physical and chem-ical sediment properties and implications for intertidalhabitat succession. Estuarine, Coastal and Shelf Science,v. 74, p. 331-343.

Volkenborn, N., Robertsom, D.M. and Reise, K., 2009,Sediment destabilizing and stabilizing bio-engineers ontidal flats: cascading effects of experimental exclusion.Helgoland Marine Research, v. 63, p. 27-35.

Weimer, R.J., Howard, J.D. and Lindsay, D.R., 1981, Tidalflats and associated tidal channels, in Scholle, P.A. andSpearing, D., eds., Sandstone DepositionalEnvironments. American Association of PetroleumGeologists, Memoir 31, p. 191-245.

Weissbrod, T. and Barthel, W.K., 1998, An early Aptian ich-nofossil assemblage zone in southern Israel, Sinai andsouthwestern Egypt. Journal of African Earth Sciences,v. 26, p. 225-239.

Wescott, W.A. and Utgaard, J.E., 1987, An UpperMississippian trace-fossil assemblage from the TarSprings Sandstone, southern Illinois. Journal ofPaleontology, v. 61, p. 231-241.

Widdows, J. and Brinsley, M., 2002, Impact of biotic andabiotic processes on sediment dynamics and the conse-quences to the structure and functioning of the intertidalzone. Journal of Sea Research, v. 48, p. 143-156.

Yochelson, E.L. and Fedonkin, M.A., 1993, Paleobiology ofClimactichnites, an enigmatic Late Cambrian fossil.Smithsonian Contributions to Paleobiology, no. 74, p. 1-34.

Zonneveld, J.-P., Gingras, M.K. and Pemberton, S.G., 2001,Trace fossil assemblages in a Middle Triassic mixed sili-ciclastic-carbonate marginal marine depositional sys-tem, British Columbia. Palaeogeography, Palaeoclima-tology, Palaeoecology, v. 166, p. 249-276.

Zonneveld, J.-P., Zaim, Y., Rizal, Y., Ciochon, R.L., BettisIII, Aswan, E.A. and Gunnell, G.F., 2012, Ichnologicalconstraints on the depositional environment of theSawahlunto Formation, Kandi, northwest OmbilinBasin, west Sumatra, Indonesia. Journal of Asian EarthSciences, v. 45, p. 106-113.


177