GeolCarp_Vol70_No1_3

GEOLOGICA CARPATHICA

, FEBRUARY 2019, 70, 1, 3–13

doi: 10.2478/geoca-2019-0001

www.geologicacarpathica.com

Changes in the composition of trace fossil assemblages

across the Paleocene–Eocene transition in

the north-western Tethys (Untersberg section, Austria)

ALFRED UCHMAN



, HANS EGGER

and FRANCISCO J. RODRÍGUEZ-TOVAR

Institute of Geological Sciences, Jagiellonian University, Gronostajowa 3a; 30387 Kraków, Poland;



alfred.uchman@uj.edu.pl

Geological Survey of Austria, Neulinggasse 38, 1030 Vienna, Austria

Department of Stratigraphy and Paleontology, University of Granada, 18002 Granada, Spain

(Manuscript received August 7, 2018; accepted in revised form January 11, 2019)

Abstract: The Untersberg section (Northern Calcareous Alps, Austria) provides an expanded and biostratigraphically

well constrained deep-sea record of the Paleocene–Eocene transition in the north-western Tethyan realm. At the base of

the Eocene, massive carbonate dissolution and a shoaling of the calcite compensation depth (CCD) by at least 1 km is

recorded by 5.5 m-thick red claystone, which is intercalated into a grey marlstone succession. Previous studies documented

the benthic foraminifera extinction event (BEE) in this claystone. Now biodeformational structures and trace fossils were

investigated in this interval to evaluate the impact of the extinction event on the macrobenthic tracemaker fauna. Using

the stratigraphic distribution pattern of trace fossils, the lowermost Eocene claystone can be subdivided into three parts:

(1) the lower part shows a trace fossil assemblage consisting of Chondrites isp., Planolites isp., Thalassinoides isp., and

Zoophycos isp., (2) the middle part is characterized by primary sedimentary lamination and exceedingly rare ichnofossils,

and (3) the upper part shows a less abundant and less diverse trace fossil assemblage than the lower part, indicating a slow

recovery of the macrobenthic tracemaker community. This pattern demonstrates that macrobenthic communities were

severely affected by the ecological perturbations in the earliest Eocene. The change in sediment colouration towards red

colour in the middle part of the Paleocene–Eocene transition at the Untersberg section, together with decrease in

bioturbation degree indicate that oxygen consumption was rather reduced during the PETM, and the loss in bioturbation

is thus unrelated to oxygen limitation. Trace fossils can be used to improve the resolution of the benthic extinction

interval and provide an excellent proxy for the precise determination of timing of the climax of this global event.

Keywords: North-western Tethys, Eastern Alps, Paleocene–Eocene boundary, benthic extinction event, trace fossils.

Introduction

At the Paleocene–Eocene boundary (P–E boundary), around

56 Ma ago, an increase in Earth’s atmospheric temperature

by 5–8 ºC occurred (Kennett & Stott 1991; Sluijs et al.

2007; McInerney & Wing 2011). This hyperthermal event

(The Paleo cene–Eocene Thermal Maximum; PETM) is asso-

ciated with a massive perturbation of the global carbon cycle,

as indicated by a negative carbon isotope excursion (CIE)

in marine and terrestrial settings with a magnitude between

2.4 ‰ and 7 ‰ (e.g., Handley et al. 2008; McCarren et al.

2008). This is interpreted as the result of a massive release of

isotopically light carbon into the carbon cycle sourced by

a release of methane hydrates (Dickens 1999, 2011) or by

a major emission of volcanic gases (Gutjahr et al. 2017).

Based on X-ray fluorescence core-scanning of precessional

cycles the duration of the whole event is estimated approxi-

mately as 170 ka (Röhl et al. 2007).

The CIE is associated with severe carbonate dissolution and

a shoaling of the calcite compensation depth (Egger et al.

2005; Zachos et al. 2006; Penman et al. 2014) as well as

an increase in terrigenous input into marginal ocean basins,

which led to enhanced surface productivity in marginal ocean

settings (e.g., Egger et al. 2003; Thomas 2007; Speijer et al.

2012). The ecological perturbations at the P–E boundary also

affected deep-sea microfaunal biota and caused the global

extinction of 35–50 % of benthic foraminifera species within

the first 10 kyr of the Eocene (Benthic Foraminiferal Extinction

Event, BEE; Thomas 1998, 2003; Alegret et al. 2009a, b).

The benthic foraminifera assemblages at the top of the BEE-

interval show the predominance of opportunistic species

(Arreguín-Rodríguez et al. 2018). Several causes have been

proposed to explain the mass extinction, including low oxy-

genation, carbonate corrosion, changes in oceanic produc tivity

and increasing temperatures of deep ocean waters (Giusberti

et al. 2016 for a review).

McInerney & Wing (2011) stressed that benthic macroin-

vertebrate assemblages were not affected by the perturbations

during the BEE. However, effects on macrofossil communities

are indicated by the composition of trace fossil assemblages,

which reflect very well the activities of macrofaunas, even if

they are not preserved as body fossils (Nicolo 2008; Nicolo et

al. 2010; Cumming & Hodgson 2011a, b; Rodríguez-Tovar et

al. 2011a). The PETM seems to have had minor long-lasting

evolutionary impacts on benthic macrofauna inhabiting shelf

environments (Ivany et al. 2018). However, the effects of

UCHMAN, EGGER and RODRÍGUEZ-TOVAR

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, 2019, 70, 1, 3–13

the PETM event on microbenthic fauna in bathyal and deep-

sea environment remain poorly explored.

In the latest years, ichnological analysis has been revealed

as a tool for the interpretation of major bioevents, such as

those associated with the Frasnian–Famennian boundary

(Stachacz et al. 2017), the T-OAE (Rodríguez-Tovar & Uchman

2010; Rodríguez-Tovar & Reolid 2013; Reolid et al. 2014;

Miguez-Salas et al. 2017; Rodríguez-Tovar et at. 2017),

the Cenomanian–Turonian boundary (Uchman et al. 2008,

2013a, b; Rodríguez-Tovar et al. 2009a, b; Monaco et al. 2012,

2016b), the latest Hauterivian (Rodríguez-Tovar & Uchman

2017), the Paleocene–Eocene (Rodríguez-Tovar et al. 2011a),

and, especially the Cretaceous–Paleogene (K–Pg) boundary

(Rodríguez-Tovar & Uchman 2004a, b, 2006, 2008; Rodríguez-

Tovar et al. 2004, 2006, 2010, 2011b, 2016; Rodríguez-Tovar

2005; Kędzierski et al. 2011; Sosa-Montes de Oca et al. 2013,

2016, 2017; Alegret et al. 2015; Monaco et al. 2015; Labandeira

et al. 2016; Łaska et al. 2017; Lowery et al. 2018).

In this paper we present a high resolution trace fossil record

for the Paleocene–Eocene transition at a section in the north-

western Tethys and demonstrate that macrobenthic communi-

ties there were severely affected by the ecological perturbations

during the BEE.

Material and methods

The Untersberg section is located southwest of Salzburg

(Austria) in a forested stream gorge (47°44’21” N, 12°59’09” E)

in the Northern Calcareous Alps, which form a 500 km-long

fold and thrust belt on the north-eastern margin of the Alps

(Fig. 1). The P–E boundary lays within the Nierental Formation

(upper Santonian–Lutetian) of the Gosau Group and accumu-

lated in a lower bathyal slope environment at a paleodepth of

about 2000 m in the north-western Tethyan realm (Egger et al.

2005). General plate tectonic reconstructions by the ODSN

Plate Tectonic Reconstruction Service (http://www.odsn.de)

suggest a position of this section at a paleolatitude of c. 44° N

in the early Paleogene.

Thanetian and Ypresian deposits consist essentially of marl-

stone, displaying CaCO

contents between 40–50 wt. %. Within

the dominantly marlstone succession, a 5.5 m-thick inter-

calation of red and green claystone and marly claystone indi-

cates the CIE, which is used to recognize the P–E boundary.

At Untersberg, the CIE was associated with a shallowing of

the calcite compensation depth by at least one kilometre

(Egger et al. 2005).

High-resolution planktonic biostratigraphy of the section

was presented in Egger et al. (2005). Calcareous nannoplank-

ton assemblages of the entire now studied section indicate

the Discoaster multiradiatus Zone (Zone NP9) in the zonation

scheme of Martini (1971). Beneath the claystone the zonal

marker fossil co-occurs with common fasciculithids (F. tym

paniformis, F. involutus, F. schaubii). Close to the base of

the claystone the first specimens of Rhomboaster cuspis were

found, a species, which is indicative for the upper part of Zone

NP9. Above the claystone, which is devoid of calcareous

plankton, R. cuspis co-occurs with Discoaster araneus and

D. mahmoudii. The stratigraphic ranges of both species are

restricted to the CIE interval within the Zone NP9 (see Egger

et al. 2005, 2017). Planktonic foraminifera assemblages from

the base of the section contain Morozovella subbotinae and

were assigned to the Morozovella velascoensis Zone (Zone P5

of Berggren & Pearson 2005 and Wade et al. 2011). The clay-

stone contains an agglutinated fauna dominated by Glomospira

spp. The marlstone overlying the claystone is also assigned to

Zone P5.

Bioturbation structures, consisting of biodeformational

structures and trace fossils (Uchman & Wetzel 2011), were

studied directly on parting surfaces in the field during “bed-

by-bed” inspection and sampling. In the laboratory, the sam-

ples were polished mechanically in different plains with use of

abrasive paper. Features of ichnofabrics have been observed

on the polished and wet surfaces of collected rock samples.

Their visibility on photo-images was intensified using Adobe®

Photoshop® software. Collected specimens are housed in

the Nature Education Centre of the Jagiellonian University

(CEP) — Museum of Geology, labelled as Ft.

Results

Trace fossil assemblage

In general, the trace fossil assemblage of the Untersberg

section is poorly diverse and consists only of four ichnotaxa

(Fig. 2): Chondrites isp., Planolites isp., Thalassinoides isp.,

and Zoophycos isp. They are mostly visible in cross section

which precludes determinations at the ichnospecies level for

most of them.

Chondrites isp. was observed as patches of circular to ellip-

tical cross sections and short segments, occasionally with

branches, 0.4–2 mm wide (Figs. 3A–F and 4B). They are cross

sections of root-like burrow systems. Smaller forms, with bur-

rows less than 1 mm in diameter (Fig. 3A), probably belong to

Ch. intricatus and the larger forms (Fig. 3B) to Ch. targionii

(for morphometric parameters of Chondrites see Uchman 1999;

Uchman et al. 2012). Chondrites is a deep-tier trace fossil that

was most likely produced in dysaerobic conditions by chemo-

symbiotic organisms (Seilacher 1990; Fu 1991).

Planolites isp. is represented by circular or elliptical spots or

bars, which 1.4–4 mm wide (Fig. 3C, E). They represent hori-

zontal/oblique, straight, simple flattened cylinders without

any wall. Planolites is a pascichnion produced by several

different soft-bodied invertebrates in marine and non-marine

environments (Pemberton & Frey 1982; Keighley & Pickerill

1995).

Thalassinoides isp. is visible as circular or oval spots and

bars, 4–21 mm wide (Fig. 3C–E), which represent straight,

horizontal to oblique, locally vertical, branched cylinders.

Thalassinoides is a domichnial (i.e. dwelling) and fodinich-

nial (i.e. feeding) structure produced by arthropods, mostly

TRACE FOSSILS ACROSS THE PALEOCENE–EOCENE TRANSITION (UNTERSBERG SECTION, AUSTRIA)

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Hanken 2003) invertebrates of unknown origin, which ingest

organic detritus and accumulate fecal pellets in a subsurface

structure (Löwemark et al. 2006). Recent studies can be found

in Löwemark (2012, 2015), Kotake (2014), Zhang et al.

(2015a, b), Dorador et al. (2016), and Monaco et al. (2016a).

A large unidentified burrow was observed in the field (level

of sample Ft10) as an oval spot, 20–30 mm wide. Its ichnota-

xonomic affinity remains unknown, but Scolicia (an irregular

echinoid burrow) or a larger Thalassinoides can be assumed.

Trace fossil abundance and distribution

In modern oceans, bioturbated pelagic sediments show

a subdivision into two parts: (1) the up to 10 cm thick, smooth

near-surface mixed layer, where the majority of burrowing

organisms occur (Boudreau 1998, 2004), and (2) the under-

lying more consolidated transitional layer, which is affected

only by deep burrowing organisms (Ekdale & Berger 1978;

Berger et al. 1979; Bromley 1990, 1996). The interpretation of

trace fossil assemblages is mainly based on the preservation of

burrows, the cross-cutting relationship and their tiering

arrangement in the sediment. As a general rule, traces with

sharp outlines were produced deeper, and later, in more com-

pacted sediment than less distinct traces. Deeper traces cross

cut more shallow traces.

The trace fossil distribution pattern at the Untersberg sec-

tion shows a clear three-fold subdivision (Fig. 2). The highest

abundance and diversity of trace fossils was recognized in

the lower part of the section (0–2.40 m), where Chondrites isp.,

Planolites isp., Thalassinoides isp., Zoophycos isp., and large

unidentified burrows occur. All ichnotaxa show a more or less

consistent record, with the exception of Zoophycos and

the undeterminable large burrows, which are restricted to a few

horizons. These horizons indicate an episodic increase in

nutrients on the sea-floor (Löwemark 2015). The major part of

the deposits consists of grey and greenish grey mudstone with

occasional presence of red coloured spots and layers. This

mottled mudstone is attributed to near-surface mixed layer

bioturbation. Local exclusive presence of disrupted primary

lamination suggests that the uppermost part of the mixed layer

was temporarily bioturbated.

The middle part of the section (2.40–4 m) consists of

non-calcareous red coloured mudstone, which predominantly

shows disrupted primary lamination indicating very shallow

burrowing. Chondrites isp., Planolites isp., and Thalassinoides

isp. are the only trace fossils, which are exceedingly rare in

this interval. Around 3.10 m from the base, a 0.3 m thick layer

does not possess any indicators of bioturbation and displays

undisturbed sedimentary lamination.

In the upper part of the section (4–7.50 m) the same trace

fossil genera occur as in the middle part but with a significant

increase in abundance and stratigraphic persistence. Chondrites

shows a more or less consistent record, and Thalassinoides is

common, while Planolites occurs only sporadically. A 5 cm

thick unbioturbated layer with primary lamination occurs at

4.60 m of the logged section and records another short hostile

episode negatively affecting bioturbation producing macro-

benthos. In some intervals trace fossils are not recognized but

unrecognizable bioturbation structures are there.

Discussion

Previous studies (Egger et al. 2005, 2017) revealed a num-

ber of environmental changes associated with the Paleocene–

Eocene transition at the Untersberg section: (1) a shoaling

of the calcite compensation depth by at least 1 km indicated

by a lithological shift from marlstone to clayey mudstone,

(2) an increase in bottom water oxygenation indicated by a shift

from grey to red sediment colours, (3) enhanced continental

run-off indicated by an almost 50 % increase in the input of

terrigenous quartz and feldspar into the basin, (4) an increase

in plankton productivity indicated by increased numbers of

radiolarian casts, (5) acidification of surface waters indicated

by the occurrences of irregularly shaped discoasterids (D. ara

neus Bukry, and D. mahmoudii Bown), and (6) a change to

unfavourable ecological conditions at the sea-floor indicated

by a depauperation of agglutinated foraminifera assemblages,

which consist essentially of Glomospira spp. As we demon-

strate above, hostile conditions on the sea-floor also affected

macrobenthic communities.

The primary sedimentary lamination in the middle part of

the Paleocene–Eocene transition at the Untersberg section

reveals the absence of a bioturbating benthic macrofauna.

A similar red laminated horizon is recorded at the Paleocene–

Eocene interval at the Zumaia section at the Bay of Biscay,

Spain (Rodríguez-Tovar et al. 2011a). In contrast to laminated

horizons at other PETM sections (Dee Marl in Nicolo 2008;

Nicolo et al. 2010) the Untersberg and Zumaia sections display

red rock colours, which suggest oxic conditions on the sea-

floor (Rodríguez-Tovar et al. 2011a; Wetzel & Uchman 2018

and references therein). Consequently, we assume that oxy-

genation of deep-sea waters was not the critical factor for

the collapse of the benthic ecosystem there.

The red sediment colour indicates that all decomposable

organic matter enclosed had been decomposed prior to burial

and/or the input of organic matter was very low, thus mini-

mizing the potential for oxygen consumption by decaying

organic matter (in contrast to the interval before and after

the PETM event). Such oligotrophic sediment will not attract

burrowing organisms. However, low organic matter content

in red mudstones does not necessarily reflect a low primary

content of organic matter as shown for some of the so-called

variegated shales in the Carpathians on the basis of ichno-

logical analysis, where red turbiditic mudstones are deeply

bioturbated and relatively higher primary organic matter

content by oxidation and consumption by organisms (Wetzel

& Uchman 2018). At many sites, variegated shales are inten-

sively bioturbated (Leszczyński & Uchman 1993). Therefore,

it is unlikely that oligotrophic conditions caused the disap-

pearance of the benthic community at the Untersberg and

Zumaia sections.

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In the Untersberg section, abundant radiolarian casts sug-

gest high surface water productivity, which was probably trig-

gered by the enhanced terrigenous input into the ocean during

the Paleocene–Eocene transition. This increased continental

run-off is documented in many sections on a global scale and

is attributed to hydrological changes and to a sea level fall at

the Benthic Foraminiferal Extinction Event (see Pujalte et al.

2016). This seems to be contradictory to the notion of oligo-

trophic conditions on the sea-floor during that time. However,

Ma et al. (2014) suggested that an increase in surface water

productivity may not necessarily result in high carbon burial

in the sediments if the sinking particulate matter is efficiently

regenerated by increased bacterial activity and converted to

dissolve inorganic and organic carbon. This process can be

stimulated by high seawater temperatures. Climate model

simu lations indicate that mid- and high-latitude sea-surface

temperatures (SST) met or exceeded modern tropical tempera-

tures at the P–E boundary, and predict tropical SSTs higher

than 35 °C (see Frieling et al. 2017, for a review).

The complex interaction of variable limiting factors

According to the above, other environmental changes than

changes in oxygen concentration could have a major relevance

during the Paleocene–Eocene transition at the Untersberg sec-

tion. Thus, other reasons for the benthic crisis can be taken

into consideration:

• As deep sea burrowing organisms are well adapted to a life

below the CCD, the carbonate solution cannot be a factor

influencing the distribution of trace fossils. However,

the presence of calcium carbonate in sediments influences

the shear strength and may positively influence the preser-

vation of trace fossils (Ekdale et al. 1984). Nevertheless,

any influence of this factor is not observed at the Untersberg

section.

• A significant increase in deep-sea water temperature during

the Paleocene–Eocene transition, even by 15 °C compared

to the present, was postulated by Brass et al. (1982) and

Shackleton (1986). Bowen et al. (2006) estimated an increase

in the temperature in the deep sea by c. 4–5 °C and the ocean

surface waters at all latitudes by c. 5–9 °C. Such warming

could be responsible for a collapse of benthic ecosystems

dominated by groups adapted to cold waters.

• Low sedimentation rates, which are important factors con-

trolling the deposition of the oceanic red beds (Wang et al.

2005) negatively impact the burial of organic matter.

Therefore, it is very probable that burial of particulate

organic matter was very low in the red sediments of

Fig. 4. Primary lamination and bioturbation structures from the Fürstenbrunn section: A — Bioturbation structures, sample Ft18, horizontal

section; B — Horizontal lamination in the lower part of bed and with Chondrites isp. (Ch) in the upper part, sample Ft4, vertical section;

C — Interrupted horizontal lamination, sample Ft25, vertical section; D — Horizontal lamination, sample Ft29, vertical section. Scale bar is 1 cm.

UCHMAN, EGGER and RODRÍGUEZ-TOVAR

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the Untersberg section. For the Zumaia section, Rodríguez-

Tovar et al. (2011a) suggested that food for burrowing

organisms just concentrated in the shallowest sediment

depths, with deeper depths being food-depleted. However, it

is an open question whether this extreme situation, where

the food is completely absent in most of the sediment,

indeed leads to very limited bioturbation. There are no

recent equivalents of such conditions.

• Some authors assumed (e.g., Brass et al. 1982) that hypersa-

line bottom-water changed ecological conditions at the floor

of the deep-sea across the Paleocene–Eocene transition.

This would have a severe effect on macrobenthic life, even

if oxygen was available. However, no evidence of hyper-

salinity, such as evaporitic minerals, was found in the inves-

tigated section or elsewhere.

• Another scenario will be the presence of methane clathrates,

which will be dissociated with increasing bottom water tem-

perature. With increasing temperature, dissociation of

oceanic methane caused the enormous increase in the light

carbon isotopes characteristic for CIE and causing further

warming (e.g., Dickens 2000). The methane can saturate

pore waters and prevent functioning of burrowing

macroorganisms.

Thus, a single and conclusive interpretation of lacking bio-

turbation structures during the PETM at the Unterberg section

is difficult, and a complex scenario, with the interrelation of

several factors, is possible.

Conclusion

Ichnological analysis conducted at the Paleocene–Eocene

transition at the Untersberg section reveals a complex scenario

of environmental changes negatively affecting the macro-

benthic tracemaker community. The occurrence of laminated

oceanic red beds suggests that the extinction of the macro-

benthic tracemaker community in the earliest Eocene was not

generated by dysoxic or suboxic bottom waters. The distinct

change from grey to red sediment colours at the onset of

the extinction event, rather indicates that bottom-water oxy-

gen concentrations increased. This change is interpreted as

the result of an efficient regeneration of organic matter by

increased bacterial activity in the water column due to a signi-

ficant increase in water temperature and/or reduced export of

organic matter to sediment leading to low nutrient levels on

the sea floor.

Regardless of the scenario behind the severe crisis in

the burrowing activity, the occurrence of laminated red sedi-

ments confines the stratigraphic position of the PETM, with

unprecedented precision.

Acknowledgements: A.U. got additional support from

the Jagiellonian University (DS funds). Funding by RT was

provided by Project CGL2015-66835-P (Secretaría de Estado

de I+D+I, Spain), Research Group RNM-178 (Junta de

Andalucía), and Scientific Excellence Unit UCE-2016-05

(Universidad de Granada). The paper benefited from reviews

by Adam Tomašových (Bratislava, Slovakia), Vladimír

Šimo (Bratislava, Slovakia), and Michelle Zill (Riverside,

California, U.S.A.).

References

Alegret L., Ortiz S. & Molina E. 2009a: Extinction and recovery of

benthic foraminifera across the Paleocene–Eocene Thermal

Maximum at the Alamedilla section (Southern Spain). Palaeo

geogr. Palaeoclimatol. Palaeoecol. 279, 186–200.

Alegret L., Ortiz S., Orue-Etxebarria X., Bernaola G., Baceta J.I.,

Monech S., Apellániz E. & Pujalte V. 2009b: The Paleocene–

Eocene Thermal Maximum: new data on microfossil turnover at

the Zumaia section, Spain. Palaios 24, 318–328.

Alegret L., Rodríguez-Tovar F.J. & Uchman A. 2015: How bioturba-

tion obscured the Cretaceous–Palaeogene boundary record.

Terra Nova 27, 225–230.

Arreguín-Rodríguez G.J., Thomas E., D’haenens S., Speijer R.P. &

Alegret L. 2018: Early Eocene deep-sea benthic foraminiferal

faunas: Recovery from the Paleocene Eocene Thermal Maxi-

mum extinction in a greenhouse world. PLoS ONE 13, 2,

e0193167.

Berger W.H., Ekdale A.A. & Bryant P.P. 1979: Selective preservation

of burrows in deep-sea carbonates. Marine Geol. 32, 205–230.

Berggren W.A. & Pearson P.N. 2005: A revised tropical to subtropical

Paleogene planktonic foraminiferal zonation. J. Foram. Res. 35,

279–298.

Boudreau B.P. 1988: Mean mixed depth of sediments: The wherefore

and the why. Limnol. Oceanogr. 43, 524–526.

Boudreau B.P. 2004: What controls the mixed-layer depth in deep-sea

sediments? The importance of particulate organic carbon flux.

Limnol. Oceanogr. 49, 620–622.

Bowen G.J., Bralower T.J., Delaney M.L., Dickens G.R., Kelly D.C.,

Koch P.L., Kump L.R., Meng J., Sloan L.C., Thomas E.,

Wing S.L. & Zachos J.C. 2006: Eocene hyperthermal event

offers insight into greenhouse warming. EOS 87, 165–169.

Brass G.W., Southam J.R. & Peterson W.H. 1982: Warm saline

bottom water in the ancient ocean. Nature 296, 620–623.

Bromley R.G. 1990: Trace fossils: biology and taphonomy. Unwin

Hyman, London, 1–280.

Bromley R.G. 1996: Trace fossils: biology, taphonomy and applica-

tions, 2

ed. Chapman and Hall, London, 1–361.

Bromley R.G. & Hanken N.-M. 2003: Structure and function of large,

lobed Zoophycos, Pliocene of Rhodes, Greece. Palaeogeogr.

Palaeoclimatol. Palaeoecol. 192, 79–100.

Cummings J.P. & Hodgson D.M. 2011a: Assessing controls on the

distribution of ichnotaxa in submarine fan environments, the

Basque Basin, Northern Spain. Sediment. Geol. 239, 162–187.

Cummings J.P. & Hodgson D.M. 2011b: An agrichnial feeding

strategy for deep-marine Paleogene Ophiomorpha group trace

fossils. Palaios 26, 212–224.

Dickens G.R. 1999: The blast in the past. Nature 401, 752–755.

Dickens G.R. 2000: Methane oxidation during the late Palaeocene

thermal maximum. Bull Soc. Géol. France 171, 37–49.

Dickens G.R. 2011: Down the Rabbit Hole: toward appropriate dis-

cussion of methane release from gas hydrate systems during the

Paleocene-Eocene thermal maximum and other past hyperther-

mal events. Climate of the Past 7, 831–846.

Dorador J., Wetzel A. & Rodríguez-Tovar F.J. 2016: Zoophycos in

deep-sea sediments indicates high and seasonal primary produc-

tivity: ichnology as a proxy in palaeoceanography during gla-

cial–interglacial variations. Terra Nova 28, 323–328.

TRACE FOSSILS ACROSS THE PALEOCENE–EOCENE TRANSITION (UNTERSBERG SECTION, AUSTRIA)

GEOLOGICA CARPATHICA

, 2019, 70, 1, 3–13

Egger H., Fenner J., Heilmann-Clausen C., Rögl F., Sachsenhofer R.F.

& Schmitz B. 2003: Paleoproductivity of the northwestern

Tethyan margin (Anthering section, Austria) across the Paleo-

cene–Eocene transition. Geol. Soc. Amer. Spec. Paper 369,

133–146.

Egger H., Homayoun M., Huber H., Rögl F. & Schmitz B. 2005:

Early Eocene climatic, volcanic, and biotic events in the north-

western Tethyan Untersberg section, Austria. Palaeogeogr.

Palaeoclimatol. Palaeoecol. 217, 243–264.

Egger H., Briguglio A. & Rögl F. 2017: Eocene Stratigraphy of the

Reichenhall Basin (Eastern Alps, Austria, Germany). Newsletter

on Stratigraphy 50, 341–362.

Ekdale A.A. 1992: Muckraking and mudslinging: the joys of

deposit-feeding. In: Maples C.G. & West R.R. (Eds.): Trace

fossils. Short Courses in Paleontology 5, 145–171.

Ekdale A.A. & Berger W.H. 1978: Deep-sea ichnofacies: modern

organism traces on and in pelagic carbonates of the western

equatorial Pacific. Palaeogeogr. Palaeoclimat. Palaeoecol. 23,

268–278.

Ekdale A.A. & Lewis D.W. 1991: The New Zealand Zoophycos revi-

sited. Ichnos 1, 183–194.

Ekdale A.A., Bromley R.G. & Pemberton S.G. 1984: Ichnology: the

use of trace fossils in sedimentology and stratigraphy. Society of

Economic Paleontologists and Mineralogists (SEPM) Short

Course 15, 1–317.

Frey R.W., Curran A.H. & Pemberton G.S. 1984: Trace making acti-

vities of crabs and their environmental significance: the ichno-

genus Psilonichnus. J. Paleontol. 58, 333–350.

Frieling J., Gebhardt H., Huber M., Adekeye O.A.,Akande S.O.,

Reichart G.-J., Middelburg J.J., Schouten S. & Sluijs A. 2017:

Extreme warmth and heat-stressed plankton in the tropics during

the Paleocene-Eocene Thermal Maximum. Science Advances 3,

http://advances.sciencemag.org.

Fu S. 1991: Funktion, Verhalten und Einteilung fucoider und

lophocteniider Lebensspuren. Courier Forsch. Senckenberg

135, 1–79.

Giusberti L., Boscolo Galazzo F. & Thomas E. 2016: Variability in

climate and productivity during the Paleocene-Eocene Thermal

Maximum in the western Tethys (Forada section). Climate of the

Past 12, 213–240.

Gutjahr M., Ridgwell A., Sexton P.F., Anagnostou E., Pearson P.N.,

Pälike H., Norris R.D., Thomas E. & Foster G.L. 2017: Very

large release of mostly volcanic carbon during the Palaeocene–

Eocene Thermal Maximum. Nature 548, 7669, 573.

Handley L., Pearson P.N., McMillan I.K. & Pancost R.D. 2008: Large

terrestrial and marine carbon and hydrogen isotope excursions in

a new Paleocene/Eocene boundary section from Tanzania. Earth

Planet. Sci. Let. 275, 17–25.

Ivany L.C., Pietsch C., Handley J.C., Lockwood R., Allmon W.D. &

Sessa J.A. 2018: Little lasting impact of the Paleocene–Eocene

Thermal Maximum on shallow marine molluscan faunas. Science

Advances 4, 9, eaat5528.

Keighley D.G. & Pickerill R.K. 1995: The ichnotaxa Palaeophycus

and Planolites: historical perspectives and recommendations.

Ichnos 3, 301–309.

Kennett J.P. & Stott L.D. 1991: Abrupt deep-sea warming, palae-

oceanographic changes and benthic extinctions at the end of the

Palaeocene. Nature 353, 225–229.

Kędzierski M., Rodríguez-Tovar F.J. & Uchman A. 2011: Vertical dis-

placement and taphonomic filtering of nannofossils by bioturba-

tion in the Cretaceous-Palaeogene boundary section at Caravaca,

SE Spain. Lethaia 44, 321–328.

Kotake N. 2014: Changes in lifestyle and habitat of Zoophycos pro-

ducing animals related to evolution of phytoplankton during the

Late Mesozoic: geological evidence for the ‘benthic-pelagic

coupling model. Lethaia 47, 165–175.

Labandeira C.C., Rodríguez-Tovar F.J. & Uchman A. 2016:

The end-

Cretaceous extinction and ecosystem change.

In: Mángano G.M. & Buatois L. (Eds.): The Trace-Fossil Record

of Major Evolutionary Events. Topics in Geobiology 40,

265–300.

Łaska W., Rodríguez-Tovar F.J. & Uchman A. 2017: Evaluating

macrobenthic response to the Cretaceous-Palaeogene event:

a high-resolution ichnological approach at the Agost section

(SE Spain). Cretaceous Res. 70, 96–110.

Leszczyński S. & Uchman A. 1993: Biogenic structures of organic-

poor sediments: examples from the Paleogene variegated shales,

Polish Outer Carpathians. Ichnos 2, 267–275.

Löwemark L. 2012: Ethological analysis of the trace fossil Zoophycos:

hints from the Arctic Ocean. Lethaia 45, 290–298.

Löwemark L. 2015: Testing ethological hypotheses of the trace fossil

Zoophycos based on Quaternary material from the Greenland

and Norwegian Seas. Palaeogeogr. Palaeoclimatol. Palaeoecol.

425, 1–13.

Löwemark L., Lin H.-L. & Sarnthein M. 2006: Temporal variations of

the trace fossil Zoophycos in a 425 k.a. long sediment record

from the South China Sea: implications for the ethology of the

Zoophycos-producer. Geol. Mag. 143, 105–114.

Lowery C.M. [and 37 coauthors] 2018: Rapid recovery of life at

ground zero of the end-Cretaceous mass extinction. Nature 558,

288–291.

Ma Z., Gray E., Thomas E., Murphy B., Zachos J. & Paytan A. 2014:

Carbon sequestration during the Palaeocene-Eocene Thermal

Maximum by an efficient biological pump. Nature Geosci. 7,

382–388.

Martini E. 1971: Standard Tertiary and Quaternary calcareous nanno-

plankton zonation. In: Farinacchi A. (Ed.): Proceedings II

Planktonic Conference. Technoscienza, Roma, 739–785.

McCarren H., Thomas E., Hasegawa T., Röhl U. & Zachos J.C. 2008:

Depth-dependency of the Paleocene–Eocene Carbon Isotope

Excursion: paired benthic and terrestrial biomarker records

(Ocean Drilling Program Leg 208, Walvis Ridge). Geochem.

Geoph. Geosyst. 9, Q10008.

McInerney F.A. & Wing S.L. 2011: The Paleocene-Eocene Thermal

Maximum: a perturbation of Carbon cycle, climate, and bio-

sphere with implications for the future. Ann. Rev. Earth Planet

Sci. 39, 489–516.

Miguez-Salas O., Rodríguez-Tovar F.J. & Duarte L.V. 2017: Selec-

tive incidence of the Toarcian oceanic anoxic event on macroin-

vertebrate marine communities: a case from the Lusitanian ba-

sin, Portugal. Lethaia 50, 548–560.

Monaco P., Rodríguez-Tovar F.J. & Uchman A. 2012: Ichnological

analysis of lateral environmental heterogeneity within the

Bonarelli Level (uppermost Cenomanian) in the classical

localities near Gubbio, Central Apennines, Italy. Palaios 27,

48–54.

Monaco P., Rodríguez-Tovar F.J. & Uchman A. 2015: A delayed re-

sponse of the trace fossil community at the Cretaceous-Paleo-

gene boundary in the Bottaccione section, Gubbio, Central Italy.

Geobios 48, 137–145.

Monaco P., Bracchini L., Rodríguez-Tovar F.J. & Uchman A. &

Coccioni R. 2016a: Evolutionary trend of Zoophycos morpho-

types from Upper Cretaceous–Lower Miocene in the type pela-

gic sections of Gubbio, central Italy. Lethaia 50, 41–57.

Monaco P., Rodríguez-Tovar F.J. & Uchman A. 2016b: Environmental

fluctuations during the latest Cenomanian (Bonarelli level) in

the Gubbio area (central Italy) based on an ichnofabric approach.

Geol. Soc. Am. Spec. Pap. 524, 97–103.

Nicolo M.J. 2008: Multiple early Eocene hyperthermal events: Their

lithologic expressions and environmental consequences. Unpub

lished PhD Thesis, Rice University, http://scholarship.rice.edu/

handle/1911/26797.

UCHMAN, EGGER and RODRÍGUEZ-TOVAR

GEOLOGICA CARPATHICA

, 2019, 70, 1, 3–13

Nicolo M.J., Dickens G.R. & Hollis C.J. 2010: South Pacific interme-

diate water oxygen depletion at the onset of the Paleocene–

Eocene thermal maximum as depicted in New Zealand margin

sections. Paleoceanography 25, PA4210.

Olivero D. & Gaillard C. 1996: Paleoecology of Jurassic Zoophycos

from south-eastern France. Ichnos 4, 249–260.

Pemberton G.S. & Frey R.W. 1982: Trace fossil nomenclature and the

Planolites–Palaeophycus dilemma. J. Paleont. 56, 843–881.

Penman D.E., Hönisch B., Zeebe R.E., Thomas E. & Zachos J.C.

2014: Rapid and sustained surface ocean acidification during the

Paleocene–Eocene Thermal Maximum. Paleoceanography 29,

357–369.

Pujalte V., Robador A., Payro A. & Samsó J.M. 2016: A siliciclastic

braid delta within a lower Paleogene carbonate platform (Ordesa–

Monte Perdido National Park, southern Pyrenees, Spain): Re-

cord of the Paleocene–Eocene Thermal Maximum perturbation.

Palaeogeogr. Palaeoclimat. Palaeoecol. 459, 453–470.

Reolid M., Mattioli E., Nieto L.M. & Rodríguez-Tovar F.J. 2014:

The Early Toarcian Oceanic Anoxic Event in the External Sub-

betic (South Iberian Palaeomargin, westernmost Tethys): geo-

chemistry, nannofossils and ichnology. Palaeogeogr. Palaeo

climatol. Palaeoecol. 411, 79–94.

Rodríguez-Tovar F.J. 2005: Fe-oxide spherules infilling Thalassi

noides burrows at the Cretaceous–Paleogene (K–Pg) boundary:

evidence of a near contemporaneous macrobenthic colonization

during the K–Pg event. Geology 33, 585–588.

Rodríguez-Tovar F.J. & Reolid M. 2013: Environmental conditions

during the Toarcian Oceanic Anoxic Event (T-OAE) in the

western

most Tethys: influence of the regional context on

a global phenomenon. Bull. Geosci. 88, 697–712.

Rodríguez-Tovar F.J. & Uchman A. 2004a: Trace fossils after the K–T

boundary event from the Agost section, SE Spain. Geol. Mag.

141, 429–440.

Rodríguez-Tovar F.J. & Uchman A. 2004b: Ichnotaxonomic analysis

of the Cretaceous/ Palaeogene boundary interval in the Agost

section, south east Spain. Cretaceous Res. 25, 647–655.

Rodríguez-Tovar F.J. & Uchman A. 2006: Ichnological analysis of the

Cretaceous- Palaeogene boundary interval at the Caravaca sec-

tion, SE Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 242,

313–325.

Rodríguez-Tovar F.J. & Uchman A. 2008: Bioturbational disturbance

of the Cretaceous- Palaeogene (K-Pg) boundary layer: implica-

tions for the interpretation of the K-Pg boundary impact event.

Geobios 41, 661–667.

Rodríguez-Tovar F.J. & Uchman A. 2010: Ichnofabric evidence for

the lack of bottom anoxia during the Lower Toarcian Oceanic

Anoxic Event in the Fuente de la Vidriera section, Betic Cordil-

lera, Spain. Palaios 25, 576–587.

Rodríguez-Tovar F.J. & Uchman A. 2017: The Faraoni event (latest

Hauterivian) in ichnological record: The Río Argos section of

southern Spain. Cretac. Res. 79, 109–121.

Rodríguez-Tovar F.J., Martínez-Ruiz F. & Bernasconi S.M. 2004:

Carbon isotope evidence of the Cretaceous-Palaeogene macro-

benthic colonization at the Agost section (southeast Spain).

Palaeogeogr. Palaeoclimatol. Palaeoecol. 203, 65–72.

Rodríguez-Tovar F.J., Martínez-Ruiz F. & Bernasconi S.M. 2006:

Use of high resolution ichnological and stable isotope data

for assessing completeness of the K–Pg boundary section,

Agost, Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 237,

137–146.

Rodríguez-Tovar F.J., Uchman A. & Martín-Algarra A. 2009a:

Oceanic anoxic event at the Cenomanian-Turonian boundary

interval (OAE-2): ichnological approach from the Betic Cordil-

lera, southern Spain. Lethaia 42, 407–417.

Rodríguez-Tovar F.J., Uchman A.,Martín-Algarra A. & O’Dogherty L.

2009b: Nutrient spatial variation during intrabasinal upwelling

at the Cenomanian-Turonian oceanic anoxic event in the

westernmost Tethys: an ichnological and facies approach.

Sediment. Geol. 215, 83–93.

Rodríguez-Tovar F.J., Uchman A., Molina & E. Monechi S. 2010:

Bioturbational redistribution of Danian calcareous nannofossils

in the uppermost Maastrichtian across the KPg boundary at

Bidart, SW France. Geobios 43, 569–579.

Rodríguez-Tovar F.J., Uchman A., Alegret L. & Molina E. 2011a:

Impact of the Paleocene–Eocene Thermal Maximum on the

macrobenthic community: Ichnological record from the Zumaia

section, northern Spain. Mar. Geol. 282, 178–187.

Rodríguez-Tovar F.J., Uchman A., Orue-Etxebarria X., Apellaniz E.

& Baceta J.I. 2011b: Ichnological analysis of the Bidart and

Sopelana Cretaceous/Paleogene (K/Pg) boundary sections

(Basque Basin,WPyrenees): refining eco-sedimentary environ-

ment. Sediment. Geol. 234, 42–55.

Rodríguez-Tovar F.J., Uchman A., M’Hamdi A., Riahi S. &

Ismail-Lattrache K.B. 2016: Ichnological record of palaeoenvi-

ronment from the Cretaceous-Paleogene boundary interval at

El Kef, Tunisia: the first study of old and new sections at the

stratotype area. J. Afr. Earth Sci. 120, 23–30.

Rodríguez-Tovar F.J., Miguez-Salas O. & Duarte L. 2017: Toarcian

Oceanic Anoxic Event induced unusual behavior and palaeobio-

logical changes in Thalassinoides tracemakers. Palaeogeogr.

Palaeoclimatol. Palaeoecol. 485, 46–56.

Röhl U., Westerhold T., Bralower T.J. & Zachos J.C. 2007: On the

duration of the Paleocene–Eocene thermal maximum (PETM).

Geochem. Geoph. Geosyst. 8, doi:10.1029/2007GC001784.

Schlirf M. 2000: Upper Jurassic trace fossils from the Boulonnais

(northern France). Geol. Palaeontol. 34, 145–213.

Seilacher A. 1967: Bathymetry of trace fossils. Mari. Geol. 5,

413–428.

Seilacher A. 1990: Aberration in bivalve evolution related to photo-

and chemosymbiosis. Hist. Biol. 3, 289–311.

Shackleton N.J. 1986: Paleogene stable isotope events. Palaeogeogr.

Palaeoclimatol. Palaeoecol. 57, 91–102.

Sluijs A., Bowen G.J., Brinkhuis H., Lourens L.J. & Thomas E. 2007:

The Palaeocene–Eocene Thermal Maximum super greenhouse:

biotic and geochemical signatures, age models and mechanisms

of global change. In: Williams M., Haywood A.M., Gregory F.J.

& Schmidt D.N. (Eds.): Deep-time perspectives on climate

change: marrying the signal from computer models and biologi-

cal proxies. The Micropalaeont. Soc., Geol. Soc., London Spec.

Publ. 2, 323–349.

Sosa-Montes de Oca C., Martínez-Ruiz F. & Rodríguez-Tovar F.J.

2013: Bottom-water conditions in a marine basin after the Creta-

ceous–Paleogene impact event: timing the recovery of oxygen

levels and productivity. PLoS One 8, 12, e82242.

Sosa-Montes de Oca C., Rodríguez-Tovar F.J. & Martínez-Ruiz F.

2016: Geochemical and isotopic characterization of trace fossil

infillings: new insights on tracemaker activity after the K–Pg

impact event. Cretaceous Res. 57, 391–401.

Sosa-Montes de Oca C., Rodríguez-Tovar F.J. & Martínez-Ruiz F.

2017: Paleoenvironmental conditions across the Cretaceous–

Paleogene transition at the Apennines sections (Italy): an inte-

grated geochemical and ichnological approach. Cretaceous Res.

71, 879–894.

Speijer R.P., Scheibner C., Stassen P. & Morsi A.-M.M. 2012:

Response of marine ecosystems to deep-time global warming:

a synthesis of biotic patterns across the Paleocene–Eocene

thermal maximum (PETM). Austrian J. Earth Sci. 105,

6–16.

Stachacz M., Uchman A. & Rodríguez-Tovar F.J. 2017: Ichnological

record of the Frasnian–Famennian boundary interval: two exam-

ples from the Holy Cross Mts (Central Poland). Int. J. Earth Sci.

106, 157–170.

TRACE FOSSILS ACROSS THE PALEOCENE–EOCENE TRANSITION (UNTERSBERG SECTION, AUSTRIA)

GEOLOGICA CARPATHICA

, 2019, 70, 1, 3–13

Thomas E. 1998: The biogeography of the late Paleocene benthic

foraminiferal extinction. In: Aubry M.-P., Lucas S.G. & Berggren

W.A. (Eds.): Late Paleocene–Early Eocene biotic and climatic

events in the marine and terrestrial records. Columbia University

Press, New York, 214–243.

Thomas E. 2003: Extinction and food at the seafloor: A high-resolu-

tion benthic foraminiferal record across the Initial Eocene

Thermal Maximum, Southern Ocean Site 690. In: Wing S.L.,

Gingerich P.D., Schmitz B. & Thomas E. (Eds.): Causes and

consequences of globally warm climates in the Early Paleogene.

Geol. Soc. Amer. Spec. Publ. 369, 319–332.

Thomas E. 2007: Cenozoic mass extinctions in the deep sea: what

perturbs the largest habitat on Earth? In: Monechi S., Coccioni R.

& Rampino M.R. (Eds.): Large ecosystem perturbations: causes

and consequences. Geol. Soc. Amer. Spec. Papers 424,1–23.

Uchman A. 1999: Ichnology of the Rhenodanubian Flysch (Lower

Cretaceous–Eocene) in Austria and Germany. Beringeria 25,

65–171.

Uchman A. & Wetzel A. 2011: Deep-sea ichnology: the relationships

between depositional environment and endobenthic organisms.

In: Hüneke H. & Mulder T. (Eds.): Deep-sea sediments. Develop.

Sediment. 63, 517–556.

Uchman A., Bąk A. & Rodríguez-Tovar F.J. 2008: Ichnological record

of deep-sea palaeoenvironmental changes around the Oceanic

Anoxic Event 2 (Cenomanian–Turonian boundary): an example

from the Barnasiówka section, Polish Outer Carpathians.

Palaeogeogr. Palaeoclimatol. Palaeoecol. 262, 61–71.

Uchman A., Caruso C. & Sonnino M. 2012: Taxonomic review of

Chondrites affinis (Sternberg, 1833) from Cretaceous–Neogene

offshore-deep-sea Tethyan sediments and recommendation for

its further use. Riv. Ital. Paleont. Strat. 118, 313–324.

Uchman A., Rodríguez-Tovar F.J., Machaniec E. & Kędzierski M.

2013a: Ichnological characteristics of Late Cretaceous

hemipelagic and pelagic sediments in a submarine high

around the OAE-2 event: a case from the Rybie section, Polish

Carpathians. Palaeogeogr. Palaeoclimatol. Palaeoecol. 370,

222–231.

Uchman A., Rodríguez-Tovar F.J. & Oszczypko N. 2013b: Excep-

tionally favourable life conditions for macrobenthos during the

Late Cenomanian OAE-2 event: ichnological record from the

Bonarelli Level in the Grajcarek Unit, Polish Carpathians.

Cretaceous Res. 46, 1–10.

Wade B.S., Pearson P.N., Berggren W.A. & Pälike H. 2011: Review

and revision of Cenozoic tropical planktonic foraminiferal bio-

stratigraphy and calibration to the geomagnetic polarity and

astronomical time scale. EarthSci. Rev. 104, 111–142.

Wang C., Hu X., Sarti M., Scott R.W. & Li X. 2005: Upper Creta-

ceous oceanic red beds in southern Tibet: a major change from

anoxic to oxic, deep-sea environments. Cretaceous Res. 26,

21–32.

Werner F. & Wetzel W. 1982: Interpretation of biogenic structures in

oceanic sediments. Bull. Inst. Géol. Bassin d’Aquitaine 31,

275–288.

Wetzel A. & Uchman A. 2018: The former presence of organic matter

caused its the later absence of organic matter: Burn-down of

organic matter in oceanic red beds enhanced by bioturbation

(Eocene Variegated Shale, Carpathians). Sedimentology 65,

1504–1519.

Zachos J.C., Schouten S., Bohaty S., Quattlebaum T., Sluijs A.,

Brinkhuis H., Gibbs S.J. & Bralower T.J. 2006: Extreme warm-

ing of mid-latitude coastal ocean during the Paleocene–Eocene

Thermal Maximum: inferences from TEX86 and isotope data.

Geology 34, 737–740.

Zhang L.J., Shi G.R. & Gong Y.M. 2015a: An ethological interpreta-

tion of Zoophycos based on Permian records from south China

and southeastern Australia. Palaios 30, 408–423.

Zhang L.J., Fan R.Y. & Gong Y.M. 2015b: Zoophycos macroevo-

lution since 541 Ma. Nature, Sci. Rep. 5, 14954, 1–10.