The Trace-Fossil Record of Organism–Matground Interactions in Space and Time

Abstract

Coarse-grained, incised-valley-fill (IVF) deposits of the Kings River alluvial fan, located southeast of Fresno, California, strongly influence local recharge and groundwater flow, and thus contaminant transport, within the alluvial-fan aquifer. Alluvial-fan sequence stratigraphic concepts provide a framework for predicting the geometry and internal facies associations of the IVF and surrounding depositional sequences. Three-dimensional Markov chain models of spatial variability of facies distributions were developed for each sequence and the uppermost IVF. Facies distributions in individual sequences were simulated separately to avoid geostatistical correlation across unconformity boundaries. These individual realizations were combined to produce a final, three-dimensional, multi-scale model of aquifer hydrofacies distributions.
Modeling of groundwater flow and solute transport within this stratigraphic framework indicates that the coarse-grained IVF significantly influences groundwater flow and contaminant transport in several ways. First, the high degree of gravel/sand body connectivity within the IVF results in rapid groundwater flow relative to the surrounding, generally finer-grained fan deposits. Second, the coarse-grained nature and relatively high hydraulic conductivity of these sediments enhances vertical flow and recharge. Finally, modeling indicates that groundwater and contaminants generally flow from the IVF deposits into the adjacent alluvial-fan deposits. Thus, the IVF not only results in rapid downward and horizontal movement of contaminants but also routes non-point-source contaminants into adjacent deposits. This significantly increases the vulnerability of aquifer sediments adjacent to the IVF to contamination.

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THE TRACE-FOSSIL RECORD OF ORGANISM–MATGROUND INTERACTIONS
IN SPACE AND TIME
LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
Department of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon, Saskatchewan,
S7N 5E2, Canada
e-mail: luis.buatois@usask.ca
ABSTRACT:Organism–matground interactions reflect two somewhat interrelated aspects: (1) the environmental restriction of microbial mats through
geologic time and (2) the evolutionary changes in benthic faunas. The history of such interactions may be subdivided into six phases: (1) Ediacaran, (2)
Cambrian, (3) Ordovician, (4) Silurian to Permian, (5) Early Triassic, and (6) Middle Triassic to Holocene. Widespread matgrounds in both shallow- and
deep-marine deposits during the Ediacaran provided substrates that were available for benthic colonization and the development of various interactions.
The most abundant ichnofossils in Ediacaran rocks are very simple grazing trails (Helminthopsis ichnoguild), representing grazing of organic matter
concentrated within microbial mats below a thin veneer of sediment. In shallow-marine environments, interactions were also evidenced by the mollusk-like
Kimberella and associated scratch marks (Radulichnus) preserved on microbial mats. Interactions are also indicated for vendozoans, as reflected by
serially repeated resting traces of Dickinsonia and the related genus Yorgi a preserved on biomats. By the latest Ediacaran, simple burrow systems
(treptinids) also occur in association with matgrounds. The replacement of matgrounds by mixgrounds was arguably the most significant change at the
ecosystem scale in the history of marine life. By the Early Cambrian, branched burrow systems became more complex and common, resulting in
increasing disruption of matgrounds in nearshore and offshore settings. While matgrounds were widespread in supratidal and upper- to middle-intertidal
environments during most of the early Paleozoic, lower-intertidal deposits were already intensely bioturbated by the late Early Cambrian. The diachronic
nature of the Agronomic Revolution is evident in the deep sea, where microbial matground ecosystems persisted during most, if not all, of the Cambrian.
In addition to the Helminthopsis ichnoguild, Cambrian deep-marine ichnofaunas also consist of arthropod trackways and sophisticated feeding strategies
represented by different Oldhamia ichnospecies, revealing complex architectural designs by undermat miners. In contrast, in deep-marine Lower
Ordovician deposits, microbial textures are rare and patchy and typically not associated with trace fossils. Biomats persisted into the late Paleozoic in the
innermost, freshwater region of estuarine systems, as well as in fluvio-lacustrine deposits, glacial lakes, and fjords. Ichnofaunas dominated by very shallow
tier structures, such as arthropod trackways and grazing trails, locally associated with matgrounds, were common in these deposits. The widespread
development of matgrounds after the end-Permian mass extinction sets the stage for the reappearance of feeding strategies linked to the exploitationof
biomats. However, subsequent faunal recovery and deep and pervasive bioturbation resulting from the establishment of the Modern evolutionary fauna led
to increased restriction of microbial mats. Analysis of ichnofaunas in matgrounds provides evidence of the temporal and environmental restriction of
biomats and allows a better understanding of animal–matground interactions, as well as of preservational biases in the trace-fossil record.
KEY WORDS:trace fossils, microbial mats, evolutionary paleoecology, matgrounds, mixgrounds
INTRODUCTION
The study of trace fossils provides information on organism–substrate
interactions (Bromley 1996). Ichnologic research has focused on
biogenic structures emplaced in softgrounds, firmgrounds, and hard-
grounds. However, during the last decade a number of studies have
started to explore the interactions between organisms and microbial
matgrounds (Gehling 1999; Seilacher 1999, 2007; Buatois and Ma
´ngano
2003, 2004; Seilacher et al. 2005; Ma
´ngano and Buatois 2007; Baucon
2008; Gehling and Droser 2009; Mata and Bottjer 2009). The aim of this
article is to analyze how these interactions have changed in the different
ecosystems through geologic time. In order to evaluate these changes,
information derived from ichnologic studies in rocks of different ages
and depositional environments needs to be integrated with sedimentary
facies analysis. Conceptually, organism–matground interactions reflect
two somewhat interrelated aspects: (1) the environmental restriction of
microbial mats through geologic time and (2) the evolutionary changes
in benthic faunas. Comparative analysis of ichnofaunas in matgrounds
provides evidence of the temporal and environmental restriction of
biomats and allows a better understanding of animal–matground
interactions, as well as of preservational biases in the trace-fossil record.
THE ICHNOGUILD CONCEPT
The ichnoguild concept, proposed by Bromley (1990, 1996), is
central to the present study. An ichnoguild reflects three parameters: (1)
bauplan, (2) food source, and (3) use of space (Bromley 1990, 1996).
With respect to bauplan, trace fossils are categorized as permanent to
semi-permanent burrows produced by stationary organisms or
transitory structures made by vagile animals. Food source is evidenced
by trophic analysis of biogenic structures, including categories such as
microbial feeding, detritus feeding, deposit feeding, suspension
feeding, gardening, and chemosymbiosis. Use of space is equivalent
to the vertical position within the substrate recorded by the tiering
structure. Ichnoguilds are named after their dominant ichnotaxa.
Ichnoguilds are essential tools with which to understand the adaptive
strategies displayed by benthic organisms, as reflected by the trace-
fossil record. Recognition and comparison of ichnoguilds from specific
ecosystems through geologic time become particularly useful in
evolutionary paleoecology (Buatois and Ma
´ngano 2003). In this study,
the ichnoguild concept is used to assess the interactions of benthic
fauna and microbial mats through geologic time.
CHANGES OF ORGANISM–MATGROUND
INTERACTIONS THROUGH GEOLOGIC TIME
In this section we review the record of organism–matground
interactions through time based on trace-fossil data. The history of
such interactions may be subdivided into six phases: (1) Ediacaran, (2)
Cambrian, (3) Ordovician, (4) Silurian to Permian, (5) Early Triassic,
and (6) Middle Triassic to Holocene.
Microbial Mats in Siliciclastic Depositional Systems Through Time
SEPM Special Publication No. 101, Copyright Ó2011
SEPM (Society for Sedimentary Geology), ISBN 978-1-56576-314-2, p. 15–28.
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Phase 1 (Ediacaran): Matground-Dominated Ecosystems
Microbial mats were widespread in both shallow- and deep-marine
deposits during the Ediacaran, providing substrates that were available
for benthic colonization and the development of various interactions
(Gehling 1999; Seilacher 1999, 2007; Seilacher et al. 2005; Gehling
and Droser 2009). Significant evidence indicates that prior to the
Ediacaran, microbial matgrounds were also dominant in marine
ecosystems (Noffke et al. 2006, 2008; Noffke 2010). However, no
convincing trace fossils have been recorded in pre-Ediacaran rocks
(Jensen et al. 2006), indicating that biofilms remained unexploited
(Phase 0). Ediacaran rocks contain a rather unusual suite of structures,
including wrinkled surfaces, ripple patches, palimpsest ripples, and
elephant skin structures, all indicative of sediment stabilization by
microbial binding (Seilacher and Pflu¨ger 1994, Seilacher 1999, Droser
et al. 2005, Gehling et al. 2005, Bottjer and Clapham 2006, Dornbos et
al. 2006, Ma
´ngano and Buatois 2007, Callow and Brasier 2009,
Gehling and Droser 2009).
According to Seilacher (1999), four major categories of organism–
microbial mat interactions were established during the Ediacaran: mat
encrusters (attached to the microbial mats), mat scratchers/grazers
(organisms grazing on the microbial mats), mat stickers (organisms
growing inside of the mats), and undermat miners (those that
constructed tunnels below the mat). Mat encrusters (e.g., Charnio-
discus) and mat stickers (e.g., Cloudina) are essentially represented by
body fossils. On the other hand, evidence of the activity of undermat
miners and mat scratchers/grazers is preserved in the ichnologic record.
The most common trace fossils in Ediacaran rocks are by far very
simple grazing trails, such as Helminthoidichnites (Fig. 1A),
Helminthopsis (Fig. 1B), and Gordia. These trails are preserved either
as negative or positive hyporeliefs/epireliefs and are commonly
associated with microbial mats, representing grazing of organic matter
concentrated within microbial mats below a thin veneer of sediment
(Gehling 1999). Another ichnogenus that commonly occurs in
association with matgrounds is Archaeonassa (Fig. 1C), which is
preserved at the top of beds as a negative furrow flanked by levees
(Jensen 2003). These grazing trails commonly crosscut corrugated
surfaces resulting from microbial activity without producing signifi-
cant disruption. Collectively these trails have been included in the
Helminthopsis ichnoguild, which consists of transitory, near-surface to
very shallow-tier, mat-grazer structures produced by vagile vermiform
animals (Buatois and Ma
´ngano 2003).
Although the Helminthopsis ichnoguild has been recorded for the
most part in shallow-marine deposits, it is also present in deep-marine
rocks. In particular, MacNaughton et al. (2000) documented the
presence of Helminthoidichnites tenuis in deep-marine deposits of the
Ediacaran Gametrail and Blueflower formations of the Canadian
Mackenzie Mountains. These authors documented the association of
this grazing trail with pustular microbial textures (see also Narbonne
and Aitken [1990]).
While organism–matground interactions in the Ediacaran deep sea
were restricted to simple grazing, the situation in coeval shallow-
marine ecosystems was slightly more complex. In addition to the
Helminthopsis ichnoguild, interactions in shallow-marine environ-
ments were also evidenced by the mollusk-like Kimberella and
associated scratch marks (Radulichnus) produced by its paired radular
teeth and preserved on microbial mats (Seilacher et al. 2005) (Fig. 2).
The close association among the body fossil Kimberella,the
ichnogenus Radulichnus, and microbial mats has been documented
in Ediacaran rocks from both the Ediacara Member of the Flinders
Ranges in southern Australia (Gehling et al. 2005) and the Ust Pinega
Formation of the White Sea in Russia (Fedonkin 2003, Fedonkin et al.
2007). These occurrences illustrate the presence of the Radulichnus
ichnoguild, which consists of transitory, surface mat-scratcher
structures produced by vagile mollusk-like animals.
The vermiform grazing trails and the scratch marks produced by
mollusk-like organisms record matground feeding by metazoans.
However, interactions are also indicated for the so-called vendozoans,
as reflected by serially repeated resting traces of Dickinsonia and the
related genus Yorgia preserved on matgrounds from both the White Sea
and South Australia (Ivantsov and Malakhovskaya 2002, Fedonkin
2003, Gehling et al. 2005, Sperling and Vinther 2010). The
ichnotaxonomic affi nity of the dickinsonid trace fossils is still
uncertain. They have been attributed to the recently proposed
ichnogenus Musculopodus (Getty and Hagadorn 2008), but dick-
insonid trace fossils differ from the type specimens of this ichnotaxon,
and,therefore, they best represent a new, still-unnamed ichnogenus. A
different interpretation, however, has been put forward by McIlroy et
al. (2009), who, based on experimental work, suggested that the
passive movement of dead organisms upon a microbial mat may have
produced multiple impressions of body tissues mimicking a trace
fossil.
The discussed interactions are typical of the lower Ediacaran trace-
fossil zone defined by Jensen (2003). The age of this interval is
approximately 560–550 Ma (Martin et al. 2000, Jensen et al. 2006).
However, by the latest Ediacaran some evolutionary innovations in the
benthic fauna resulted in new types of interactions between animals
and matgrounds. These changes are reflected in the upper Ediacaran
trace-fossil zone of Jensen (2003), the age of which ranges,
approximately, between 550 and 542 Ma (Grotzinger et al. 1995,
Jensen et al. 2006). This zone includes the oldest branching burrow
systems (Treptichnus-like, Streptichnus) as well as three-lobate trace
fossils similar to Curvolithus (Jensen et al. 2000, Jensen and Runnegar
2005). In particular, this zone is well represented in the Urusis
Formation of the Nama Group in Namibia.
Specifically, burrow systems that closely resemble Treptichnus have
been recorded in the Huns Member of the Urusis Formation (Jensen et
al. 2000). The age of this unit is constrained between 548 and 545 Ma
(Grotzinger et al. 1995, Jensen et al. 2000). An even more complex
form, Streptichnus narbonnei, is present in the Spitzkop Member, the
uppermost unit of the Urusis Formation (Jensen and Runnegar 2005).
The trace-fossil–bearing strata occur above a tuff dated 543.3 Ma
(Grotzinger et al. 1995, Narbonne et al. 1997). The appearance of
branched burrow systems (treptinids) represents a major innovation
with respect to trace-fossil morphologic patterns and signals an
incipient exploitation of the infaunal ecospace by the end of the
Ediacaran. However, these structures are relatively uncommon, and
simple grazing trails continued to be dominant in Ediacaran deposits.
Treptinids occur in the same layers as the Helminthopsis ichnoguild, in
association with matgrounds. Although no clear evidence exists that
treptinids exploited microbial matgrounds, their patchy and low-
density occurrence prevent significant disruption of these matground-
dominated ecosystems.
Phase 2 (Cambrian): The Agronomic Revolution
The replacement of matgrounds by mixgrounds (the ‘‘Agronomic
Revolution’’ of Seilacher [1999] and the ‘‘Cambrian Substrate
Revolution’’ of Bottjer et al. [2000]) was arguably the most significant
change at the ecosystem scale in the history of marine life. By the Early
Cambrian, branched burrow systems became more complex and
common, as illustrated by the abundance of Treptichnus pedum (Jensen
2003). Together with this ichnospecies, the appearance of much more
complex and large grazing trace fossils (e.g., Psammichnites) resulted
in increasing disruption of matgrounds in nearshore and offshore
settings (Buatois and Ma
´ngano 2004, Seilacher et al. 2005). Later in
the Early Cambrian, the presence of vertical dwelling structures
(Skolithos,Diplocraterion,Arenicolites) of suspension feeders and
passive predators marks the appearance of deep bioturbation in high-
energy settings. All of these evolutionary changes were leading to the
16 LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
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FIG. 1.—The Helminthopsis ichnoguild and Ediacaran shallow-marine microbial mats. (A) Helminthoidichnites tenuis (Ht) associated with
patches of wrinkle marks indicative of microbial mats. Arondegas Formation, Vanrhynsdorp Group, Arondegas Farm, South Africa. Scale bar
is 1 cm. (B) Helminthopsis tenuis in unusually coarse-grained sandstone Ediacara Member, Rawnsley Quartzite, Pound Subgroup, Flinders
Ranges, southern Australia. Coin is 1.9 cm. (C) Archaeonassa fossulata. Ediacara Member, Rawnsley Quartzite, Pound Subgroup, Flinders
Ranges, southern Australia. Scale bar is 1 cm.
THE TRACE-FOSSIL RECORD OF ORGANISM–MATGROUND INTERACTIONS IN SPACE AND TIME 17
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establishment of the mixed layer, resulting in increased rates of
diffusion, particle mixing, and bioirrigation (Aller 1982, McIlroy and
Logan 1999, Droser et al. 2004, Ma
´ngano and Buatois 2007, Callow
and Brasier 2009, Desjardins et al. 2010).
As a result of matground restriction, spatial heterogeneity increased
in Early Cambrian shallow-marine environments, where patches of
microbial mats coexisted with adjacent, intensely bioturbated mix-
ground sediments (Bailey et al. 2006). In these biomat patches, the
Helminthopsis ichnoguild persisted, representing ‘‘islands’’ of micro-
bial matground-dominated conditions. Even some of the Early
Cambrian large grazing trails may have been produced by organisms
targeting concentration of food resources in microbial mats (Hagadorn
et al. 2000). Although the undermat mining trace Oldhamia is
dominant in Cambrian deep-marine environments, this ichnogenus is
also present, albeit rarely, in shallow-marine offshore deposits.
Examples include Oldhamia alata (Fig. 3A, B) and Oldhamia
geniculata, both known from shallow-marine deposits (Buatois and
Ma
´ngano 2004, 2012; Seilacher et al. 2005; Buatois et al. 2007;
Almond et al. 2008). In addition to Oldhamia, undermat miners are
also represented by tiny branching burrow systems included in the
ichnogenus Pilichnus (Fig. 4; Buatois and Ma
´ngano 2012). As is the
case for its deep-marine counterparts, shallow-marine representatives
occur in direct association with wrinkle marks and corrugated surfaces,
indicating exploitation of microbial mats (Figs. 3A, B, 4).
In addition to spatial heterogeneity within environments, the
Agronomic Revolution was diachronic along the depositional profile.
Offshore deposits (i.e., below the fair-weather wave base but above the
storm wave base) tend to be more intensely bioturbated than do those
formed in adjacent shelf environments (i.e., below the storm wave
base). In addition, while matgrounds were widespread in supratidal and
upper- to middle-intertidal environments during most of the early
Paleozoic, lower-intertidal deposits were already intensely bioturbated
by the late Early Cambrian. Treptichnus pedum was not restricted to
offshore settings but rather extended into tidal-flat environments in the
earliest Early Cambrian, albeit coexisting with matgrounds (Buatois et
al. 2007, Almond et al. 2008). Deep burrows of Skolithos and
Syringomorpha forming pipe-rock occur in high-energy sand-flat
areas, revealing colonization of a relatively deep infaunal ecospace by
endobenthic organisms in these lower-intertidal areas. In short,
ichnologic information indicates that the Agronomic Revolution was
not restricted to shoreface and offshore environments (Ma
´ngano and
Buatois 2004a).
However, microbial matgrounds persisted in more proximal
intertidal areas well into the Late Cambrian (Hagadorn et al. 2002,
Hagadorn and Belt 2008). These deposits contain a wide variety of
microbially induced structures that allowed preservation of medusa
body fossils and a peculiar suite of trace fossils consisting of the giant
mollusk-like trail Climactichnites, its associated resting trace Muscu-
lopodus, and the arthropod trackway Protichnites, among other
ichnotaxa (Yochelson and Fedonkin 1993; Hagadorn et al. 2002;
Bottjer and Hagadorn 2007; Getty and Hagadorn 2008, 2009;
Hagadorn and Belt 2008; Seilacher 2008). The presence of these
mollusk-like and arthropod trace fossils reveals an interesting
combination of relict Ediacaran styles of interaction together with
the appearance of Cambrian styles of interaction. The Climactichnites
ichnoguild consists of transitory, surface mat-grazer structures
produced by vagile mollusk-like animals, representing a Cambrian
FIG. 2.—Radular marks attributed to the ichnogenus Radulichnus (Ra)
associated with the producer, the protomollusk Kimberella
quadrata (Ki). Note also the presence of Dickinsonia (Di). Ediacara
Member, Rawnsley Quartzite, Pound Subgroup, Flinders Ranges,
southern Australia. Scale bar is 5 cm.
FIG. 3.—The Oldhamia ichnoguild in Lower Cambrian shallow-marine
microbial mats (Puncoviscana Formation of Quebrada del Toro,
northwest Argentina). (A) General view of a surface with several
specimens of Oldhamia alata associated with corrugated surfaces
and wrinkle marks. Scale bar is 1 cm. (B) Close-up showing wing-
like spreite of O. alata and corrugated surfaces. Scale bar is 1 cm.
18 LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
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equivalent of the Radulichnus ichnoguild. Interestingly, the restricted
temporal distribution of Climactichnites (Late Cambrian) indicates that
its disappearance may have been linked to the expansion of the
Agronomic Revolution into upper- and middle-intertidal deposits.
In contrast, the presence of arthropod trackways is a clear signature
of the Cambrian explosion (Seilacher et al. 2005, Jensen et al. 2006).
Similar Cambrian trackways have been included in the Diplichnites
ichnoguild by Buatois and Ma
´ngano (2003). This ichnoguild consists
of vagile, surface to near-surface structures produced by arthropods. As
noted by these authors, the food source in this ichnoguild is unclear
because trophic types are difficult to infer from trackways. However, in
the case of these Cambrian tidal-flat deposits, both Climactichnites and
Protichnites are directly associated with structures indicative of
microbial stabilization, such as domal sand buildups (Bottjer and
Hagadorn 2007, Hagadorn and Belt 2008), indicating that exploitation
of the matgrounds may have been the adopted feeding strategy. The
Helminthopsis ichnoguild also occurs in these matground-dominated
settings, as illustrated by grazing trails crosscutting breached ripple
surfaces (Planolites in Hagadorn and Belt [2008]). Interestingly, areas
of this Late Cambrian tidal flat dominated by biofilms coexisted with
others displaying burrows of infaunal organisms (e.g., Skolithos). The
localized persistence of matgrounds in shallow-marine environments is
consistent with the sporadic preservation of Ediacaran-type fossils in
Cambrian rocks (e.g., Hagadorn et al. 2000). This fact indicates a
gradual closure of this taphonomic window during the Ediacaran–
Cambrian transition (Gehling et al. 1998, Jensen et al. 1998).
The diachronic nature of the Agronomic Revolution is particularly
evident in the deep sea, where microbial matground ecosystems
persisted during most, if not all, of the Cambrian. In addition to
elements of the Helminthopsis ichnoguild (Figs. 5A, B, 6B), Cambrian
deep-marine ichnofaunas also manifest more sophisticated feeding
strategies represented by different Oldhamia ichnospecies, revealing
complex architectural designs by undermat miners (Seilacher 1999,
Buatois and Ma
´ngano 2003) (Fig. 6A–D). The Oldhamia ichnoguild
consists of semi-permanent, very shallow-tier, undermat-miner
structures produced by stationary vermiform organisms. This ichno-
guild is typically represented by several Oldhamia ichnospecies that
have been recorded in Cambrian deep-sea rocks of North America
(Churkin and Brabb 1965, Hofmann and Cecile 1981, Lindholm and
Casey 1990, Sweet and Narbonne 1993, Hofmann et al. 1994), South
America (Buatois and Ma
´ngano 2003), Europe (Crimes and Crossley
1968), and Africa (El Hassani and Willefert 1990). The combination of
matground-dominated ecology and the evolutionary innovations of the
Cambrian explosion allowed more complex interactions to develop.
These are illustrated by the sophisticated feeding patterns displayed by
Oldhamia, which are far more complex than those revealed by
Ediacaran trace fossils. Cambrian deep-marine deposits commonly
contain arthropod trackways of the Diplichnites ichnoguild. These
trackways are commonly associated with corrugated surfaces indica-
tive of microbial mats, but direct exploitation of biomats has not yet
been documented.
Phase 3 (Ordovician): The Expansion of the Agronomic
Revolution into Deep Water
By the Ordovician, mixgrounds were fully established in shallow-
marine environments, and matground-dominated ecosystems became
essentially restricted to stressed environments characterized by the
suppression of bioturbation (Hagadorn and Bottjer 1999, Ma
´ngano and
Droser 2004, Mata and Bottjer 2009). Locally, microbial patches still
FIG. 4.—Pilichnus cf. dichotomus, tunnels by undermat miners in
Lower Cambrian shallow-marine microbial mats (Puncoviscana
Formation of Quebrada del Toro, northwest Argentina). Scale bar is
1 cm.
FIG. 5.—The Helminthopsis ichnoguild in Lower Cambrian deep-marine microbial mats (Puncoviscana Formation of San Antonio de Los Cobres,
northwest Argentina). (A) General view of Helminthopsis tenuis associated with wrinkle marks. (B) Close-up of a meander. Coin is 1.8 cm.
THE TRACE-FOSSIL RECORD OF ORGANISM–MATGROUND INTERACTIONS IN SPACE AND TIME 19
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persisted in areas adjacent to mixgrounds. In a study on the Lower
Ordovician shallow-marine deposits of France, Noffke (2000) reported
that matground formation was inhibited in high-energy sandy bars
colonized by Daedalus halli. However, in this succession matgrounds
persisted under less energetic conditions, even in the presence of
superficial to shallow-tier grazers, documenting the local persistence of
a mat-grazing ichnoguild. Further restriction is evidenced by the Late
Ordovician, with the presence of microbial mats represented by
FIG. 6.—The Oldhamia ichnoguild in Lower Cambrian deep-marine microbial mats (Puncoviscana Formation of San Antonio de Los Cobres,
northwest Argentina). All scale bars are 1 cm. (A) Oldhamia flabellata associated with wrinkle marks and mini-ripples. (B) Oldhamia
flabellata cross-cutting Helminthoidichnites tenuis. (C) Palimpsest ripples on top of layer indicating development of a microbial mat. (D)
Poorly preserved specimen of Oldhamia isp. at the base of the layer shown in A indicating mining below the mat.
20 LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
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millimeter ripples in dysaerobic laminated fine-grained deposits
containing Chondrites, an ichnogenus characteristic of oxygen-
depleted environments (Osgood 1970).
In addition, the Early Ordovician represents a turning point in the
evolutionary history of deep-marine environments (Buatois et al.
2009). Trace-fossil data indicate that the colonization of the deep sea
was a protracted process, which lagged behind colonization of
nearshore and offshore substrates (Ma
´ngano and Buatois 2007). While
mat grazers and undermat miners were widespread in the deep sea
during the Ediacaran to Cambrian, microbial mats display an
increasingly patchy distribution in the Early Ordovician, and the
Oldhamia ichnoguild essentially disappeared (Buatois et al. 2009).
The appearance of ichnofaunas containing an increasing number of
graphoglyptids indicates a replacement of strategies linked to
exploitation of microbial mats by farming of bacteria and trapping of
microorganisms. While graphoglyptids were apparently rare, poorly
diverse in terms of morphologic patterns, and geometrically simpler in
Tremadocian turbidites (Buatois et al. 2009), Arenigian deep-marine
deposits contain much more varied graphoglyptid patterns, including
guided meanders, networks, and radial structures (Crimes et al. 1992).
A further increase in diversity and complexity of graphoglyptids has
been recorded in the Late Ordovician–Early Silurian (Orr 2001,
Ma
´ngano and Droser 2004, Uchman 2004).
Phase 4 (Silurian–Permian): Restriction of Microbial
Matgrounds to Marginal-Marine and
Continental Environments
Available information indicates that animal–matground interactions
became extremely uncommon in both shallow- and deep-marine
environments during the rest of the Paleozoic as a result of the
restriction of biomats to stressed environments. Pflu¨ ger (1999)
provided one of the most detailed studies of the role of microbial
binding in shallow-marine environments in this time span. He
documented a wide variety of structures indicative of microbial
matgrounds (e.g., ‘‘Manchuriophycus,’’ palimpsest ripples) in a
Silurian storm-dominated succession of Lybia. Although trace fossils
do occur in this succession, they are typically absent or rare in the
matground layers. Pflu¨ger (1999) noted that this succession encom-
passes a range of redox conditions, from fully aerobic nearshore
sandstone to anoxic shelf graptolite-bearing black shale. In this
succession, trace fossils (e.g., Gyrochorte,Arthrophycus,Cruziana,
Skolithos,Diplocraterion) and matgrounds tend to be mutually
exclusive. Very rarely, Gyrochorte and Skolithos intersect matground
surfaces (Pflu¨ ger 1999; Fig. 5C). Although Skolithos most likely
descend from a stratigraphically higher colonization surface, Gyro-
chorte may represent exploitation of the microbial mat. More
commonly, particularly in the dysaerobic facies, is the alternation of
layers with microbial mats and layers with trace fossils, reflecting
fluctuations in oxygen content. In any case, the example from the
Silurian of Lybia indicates that temporal alternation of matgrounds and
mixgrounds, rather than spatial heterogeneity, characterizes these
storm-dominated shallow-marine settings.
In contrast to fully marine environments, biomats persisted well into
the late Paleozoic in the innermost, freshwater region of estuarine
systems, as well as in fluvio-lacustrine, glacio-lacustrine, and fjord
deposits. In these settings, trace fossils are dominantly parallel to the
bedding plane, with little disturbance of the primary sedimentary fabric
(Buatois and Ma
´ngano 1993; Buatois et al. 1997, 1998a; Ma
´ngano and
Buatois 2004b; Netto et al. 2009). Ichnofaunas dominated by very
shallow tier structures, such as arthropod trackways and grazing trails,
locally associated with corrugated surfaces of microbial matground
origin were common in these deposits. The combination of a diverse
arthropod benthic fauna and microbial binding of the substrate resulted
in the spectacular preservation of a wide variety of arthropod trackways
and resting traces, particularly in Carboniferous tidal rhythmites
formed in the innermost zone of estuaries.
The Carboniferous Buildex Quarry ichnofauna of eastern Kansas,
containing the monuran insect resting trace Tonganoxichnus (Fig. 7A,
B); various trackways, such as Stiaria (Fig. 7C) and Diplichnites;
grazing trails such as Helminthopsis; and the feeding burrow
Treptichnus bifurcus (Fig. 7D), represents one of the best-known
examples of ichnofaunas in tidal rhythmites (e.g., Buatois et al. 1997,
1998b; Ma
´ngano et al. 1997). In particular, the ichnospecies
Tonganoxichnus ottawensis is thought to record the ability of these
insects to perform successive lateral jumps, with a pivot point at the
posterior tail-like extension (Fig. 7B). Tonganoxichnus ottawensis
most likely represents jumping in connection with a defensive strategy
or raking the microbial mat with a feeding purpose (e.g., Ma
´ngano et
al. 1997). Similar ichnofaunas have been detected in other late
Paleozoic fluvio-estuarine transition deposits of North America
(Archer and Maples 1984, Rindsberg 1990, Ma
´ngano et al. 2001,
Lucas and Lerner 2005, Minter and Braddy 2009). In addition to the
Diplichnites,Helminthopsis, and Treptichnus ichnoguilds, the Tonga-
noxichnus ichnoguild, consisting of transitory, surface mat-scratcher
structures produced by vagile apterygote insects, represents a novel
interaction.
Interactions between arthropods and microbial mats are also evident
in Carboniferous–Permian glacially related deposits of Gondwana (see
Buatois et al. [2010] for review of these ichnofaunas). In particular,
glacial lake and fjord deposits of the Parana
´Basin in southern Brazil
contain abundant grazing trails and arthropod trackways in direct
association with structures indicative of microbial binding, such as
wrinkle marks (e.g., Netto et al. 2009). The Diplichnites and
Helminthopsis ichnoguilds are dominant in these freshwater settings,
revealing arthropod exploitation of food resources in microbial mats.
Netto et al. (2009) noted that microbial mats frequently are the initial
colonizers of barren habitats, such as those in subpolar regions, and
that cyanobacteria play an important role in biomass production in
these extreme environments. These authors also attributed some of
these trackways to millipedes and stressed that in modern environments
these arthropods live on the surface of wet substrates, feeding on
decaying vegetation or grazing on microbial mats.
Microbial stabilization enhancing preservation of trace fossils was
not exclusive of freshwater to transitional terrestrial to freshwater
settings but also played a major role in the preservation of biogenic
structures in eolian deposits. Seilacher (2008) stressed the importance
of microbial participation (bioglues) in the preservation of delicate
arthropod and vertebrate trackways on eolian-dune deposits. This is
clearly illustrated by the wide variety of vertebrate and arthropod
trackways (e.g., Octopodichnus,Paleohelcura) in Permian eolian
deposits of the western United States (e.g., Brady 1947, Sadler 1993,
Braddy 1995, Hunt and Lucas 2007).
Phase 5 (Lower Triassic): Matground-Dominated
Ecosystems in the Aftermath of the End-Permian
Mass Extinction
The end-Permian mass extinction was the largest of the entire
Phanerozoic, displaying the greatest ecologic severity in both marine
and continental environments, with estimations of up to 96% of species
becoming extinct (Raup 1979, Hallam and Wignall 1997, Benton
2003, McGhee et al. 2004, Erwin 2006). While pre-extinction marine
deposits are intensely bioturbated and contain a wide variety of trace
fossils, ichnofaunas from the lowermost Triassic strata (immediate
post-extinction aftermath) are typically monospecific and consist of
opportunistic ichnotaxa, typically small Planolites (e.g., Twitchett and
Wignall 1996, Twitchett 1999, Pruss and Bottjer 2004, Twitchett and
THE TRACE-FOSSIL RECORD OF ORGANISM–MATGROUND INTERACTIONS IN SPACE AND TIME 21
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FIG. 7.—Trace fossils in Upper Carboniferous fluvio-estuarine microbial mats (Tonganoxie Sandstone of Buildex Quarry, eastern Kansas, United
States). All scale bars are 1 cm. (A) Tonganoxichnus buildexensis. Note spectacular preservation of morphologic details, allowing
reconstruction of the latero-ventral anatomy of the monuran insect producer. The anterior region is characterized by the presence of a frontal
pair of maxillary palp impressions, followed by a head impression and three pairs of conspicuous thoracic appendage imprints symmetrically
opposite along a median axis. The posterior region commonly exhibits numerous delicate chevron-like markings, recording the abdominal
appendages, and a thin, straight, terminal extension. (B) Tonganoxichnus ottawensis. Note fan-like arrangement of mostly bifid scratch marks
at the anterior area, recording the head and thoracic-appendage backstrokes against the sediment. The posterior area displays chevron-like
markings or small subcircular impressions recording the abdominal appendages of the animal, ending in a thin, straight, terminal extension.
Specimens display lateral repetition and are commonly grouped into twos or threes, with a fix point at the posterior-most tail-like structure. (C)
Treptichnus bifurcus associated with corrugated surfaces indicative of a microbial mat. (D) Stiaria intermedia and corrugated surface.
22 LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
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Barras 2004, Fraiser and Bottjer 2009). Interestingly, proliferation of
structures indicative of microbial mats (e.g., wrinkle marks) during the
post-extinction aftermath provides further evidence of suppressed
bioturbation and environmental stress (Pruss et al. 2004, 2005). Pruss
et al. documented widespread wrinkle marks in offshore hummocky
cross-stratified sandstone in the Lower Triassic strata of both the
western United States and Italy. In addition, they documented various
ichnotaxa in these deposits, including Asteriacites,Rhizocorallium,
Planolites, and Gyrochorte. All of these ichnotaxa are shallow-tier
trace fossils causing little disturbance to the primary sedimentary
fabric. Even typically deeper-tier trace fossils, such as Thalassinoides,
occupy anomalously shallow-tier positions (less than 5 cm) in Lower
Triassic rocks (Pruss and Bottjer 2004). The association of some of
these trace fossils with biomats indicates that exploitation of microbial
mats may have reappeared as a common feeding strategy during the
Early Triassic.
Phase 6 (Middle Triassic to Holocene): The Restriction of
Matgrounds to Extreme Environments
With the gradual recovery of benthic faunas after the end-Permian
mass extinction and the establishment of the Modern evolutionary
fauna, mixgrounds became dominant in all but the most extreme
environments. In most of these settings, such as the anoxic zones of the
deep sea or hypersaline lagoons and lakes, no interactions between the
benthic fauna and the microbial substrate occur simply because these
environments are too extreme for colonization by trace-making
organisms. However, interactions locally persisted in intertidal zones
and lake-margin settings.
DISCUSSION
Organism–matground interactions reflect a subtle balance between
two mutually exclusive situations: (1) a world completely dominated by
microbial mats in the absence of benthic bioturbators and (2) substrates
in which the activity of benthic bioturbators prevents the establishment
of matgrounds. However, the shift from matgrounds to mixgrounds
implies a transition during which matgrounds coexist with benthic
organisms, allowing for a number of interactions, essentially reflecting
feeding of biomat organic matter by epifaunal grazers and undermat
miners (Fig. 8). In addition, the presence of matgrounds enhances the
preservation potential of delicate trace fossils, allowing for the
‘‘unlocking’’ of delicate morphologic features of the producers and
their associated behaviors.
Animal–matground interactions are key to understanding the
similarities between Ediacaran–earliest Cambrian marine ichnofaunas
and late Paleozoic continental to transitional ichnofaunas. Both
ichnofaunas consist of tiny grazing trails (e.g., Helminthopsis,
Helminthoidichnites,Gordia) produced by epifaunal or very shallow
infaunal organisms and very shallow-tier feeding burrows of infaunal
animals (e.g., Treptichnus,Oldhamia). Although many of these
structures are attributed to worm-like animals, arthropods become
one of the most important producers during Phanerozoic times. In fact,
delicate preservation of trackways (e.g., Diplichnites,Stiaria) and
resting/feeding traces (e.g., Tonganoxichnus) is possible through the
mediation of a microbial mat. These trace fossils are typically
associated with structures indicative of microbial mats, such as
corrugated surfaces and wrinkle marks.
This recurrent association reveals the establishment of a number of
epifaunal to shallow-tier ichnoguilds reflecting grazing and mining of
the biomats. Mid- to deep-tier trace fossils as well as sediment
bulldozers are characteristically absent. The key to understanding
similarities between apparently unrelated ichnofaunas resides in the
idea that the initial exploitation of underutilized ecospace is linked to a
number of temporarily recurrent interactions between organisms and
matgrounds, the preservation of which is mediated by a peculiar set of
taphonomic conditions (Buatois and Ma
´ngano 2011).
CONCLUSIONS
Organism–matground interactions since the Ediacaran reflect two
somewhat interrelated aspects: (1) the environmental restriction of
microbial mats through geologic time and (2) the evolutionary changes
in benthic faunas. The history of such interactions may be subdivided
into six phases: (1) Ediacaran, (2) Cambrian, (3) Ordovician, (4)
Silurian to Permian, (5) Early Triassic, and (6) Middle Triassic to
Holocene.
The Ediacaran (Phase 1) was characterized by the presence of
widespread matgrounds in both shallow- and deep-marine deposits,
allowing for the development of various interactions between
organisms and biomats. The most common interaction was represented
by the Helminthopsis ichnoguild, which consists of transitory, near-
surface to very shallow-tier, mat-grazer structures produced by vagile
vermiform animals, and this ichnoguild occurs in both shallow- and
deep-marine deposits. In addition, the Radulichnus ichnoguild,
consisting of transitory, surface mat-scratcher structures produced by
vagile mollusk-like animals, was present in shallow-marine environ-
ments. Interactions are also indicated for vendozoans, as reflected by
serially repeated resting traces of Dickinsonia and the related genus
Yorgia preserved on biomats.
The Cambrian (Phase 2) replacement of matgrounds by mixgrounds
represents a major change in the nature and abundance of organism–
matground interactions. Evolutionary changes conducive to the
establishment of the mixed layer resulted in increased rates of
diffusion, particle mixing, and bioirrigation, with the corresponding
restriction of the matground-dominated ecosystem. Spatial heteroge-
neity increased in Early Cambrian shallow-marine environments,
where patches of microbial mats coexisted with adjacent, intensely
bioturbated mixground sediments. In these biomat patches, the
Helminthopsis ichnoguild persisted, representing ‘‘islands’’ of micro-
bial matground-dominated conditions. In upper-intertidal deposits, the
Climactichnites ichnoguild, consisting of transitory, surface mat-grazer
structures produced by giant vagile mollusk-like animals, may be
understood as a Cambrian equivalent of the Radulichnus ichnoguild.
Microbial matground ecosystems persisted during most, if not all, of
the Cambrian in the deep sea. In addition to elements of the
Helminthopsis ichnoguild, Cambrian deep-marine ichnofaunas also
reveal more sophisticated feeding strategies represented by the
Oldhamia ichnoguild, which consists of semi-permanent, very
shallow-tier, undermat-miner structures produced by stationary
vermiform organisms. The Diplichnites ichnoguild, consisting of
vagile, surface to near-surface structures produced by arthropods,
signals the appearance of new tracemakers in both shallow- and deep-
marine environments.
During the Ordovician (Phase 3), mixgrounds were fully established
in shallow-marine environments, and matground-dominated ecosys-
tems became essentially restricted to stressed environments character-
ized by the suppression of bioturbation. However, microbial patches
displaying grazing trace fossils locally persisted in areas adjacent to
mixgrounds. In the deep sea, microbial mats display an increasingly
patchy distribution in the Early Ordovician, with graphoglyptids
replacing the Oldhamia ichnoguild and gradually rising in dominance,
reaching relatively high diversity levels by the end of the Ordovician.
Animal–matground interactions became extremely uncommon in
both shallow- and deep-marine environments during the Silurian–
Permian (Phase 4) as a result of the restriction of biomats to stressed
environments. However, the combination of a diverse arthropod
benthic fauna and microbial binding of the substrate resulted in the
spectacular preservation of a wide variety of arthropod trackways and
resting traces in the innermost zone of estuaries, fluvio-lacustrine
THE TRACE-FOSSIL RECORD OF ORGANISM–MATGROUND INTERACTIONS IN SPACE AND TIME 23
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FIG. 8.—Summary of animal–matground interactions in space and time. Fluvio-estuarine refers to marginal-marine environments located in the
inner tide–influenced but freshwater portion of estuaries. Tidal-flat environments occur between high- and low-tide lines, while subtidal refers
to environments below the low-tide line. The shoreface is located below the low-tide line and above the fair-weather wave base in wave-
dominated shorelines. The offshore occurs below the fair-weather wave base and above the storm wave base. The shelf is located between the
storm wave base and the slope break. The slope is the high-gradient area extending between the shelf edge and the base of the slope. In this
context, deep marine refers to settings seaward of the base of the slope. During pre-Ediacaran times (Phase 0), matgrounds dominated in
almost every environment, but no metazoan trace fossils are known. During the Ediacaran (Phase 1), microbial mats were widespread in
24 LUIS A. BUATOIS AND M. GABRIELA MA
´NGANO
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environments, glacial lakes, and fjords, particularly during the
Carboniferous–Permian. Infaunal bioturbation in these low-energy
freshwater settings was uncommon until the Permian. In addition to the
Diplichnites and Helminthopsis ichnoguilds, the Tonganoxichnus
ichnoguild, consisting of transitory, surface mat-scratcher structures
produced by vagile apterygote insects, represents a novel interaction in
continental and transitional environments.
Proliferation of microbial mats during the Early Triassic post-
extinction aftermath (Phase 5) provides further evidence of suppressed
bioturbation and environmental stress. This marks the reappearance of
ichnofabrics dominated by shallow-tier trace fossils, somewhat
reminiscent of those from the early Paleozoic. The association of
some of these trace fossils with biomats indicates that exploitation of
microbial mats may have been a common feeding strategy during the
Early Triassic.
With the gradual recovery of benthic faunas since the Middle
Triassic (Phase 6), mixgrounds became dominant in all but the most
extreme environments. Organism–matground interactions locally
persisted in intertidal zones and lake-margin settings.
ACKNOWLEDGMENTS
Discussions with John Almond, Jim Gehling, So¨ren Jensen, and
Dolf Seilacher have always been both enjoyable and illuminating.
Brenda Kirkland, an anonymous reviewer, and editor Henry Chafetz
provided valuable comments. Financial support for this study was
provided by Natural Sciences and Engineering Research Council
(NSERC) Discovery Grants 311727-05/08 and 311726-05/08, award-
ed to authors Ma
´ngano and Buatois, respectively.
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