Paleobiology, 2021, pp. 1–17
DOI: 10.1017/pab.2021.30
Article
The taphonomic clock in fish otoliths
Konstantina Agiadi* , Michele Azzarone, Quan Hua, Darrell S. Kaufman,
Danae Thivaiou, and Paolo G. Albano
Abstract.—Paleobiological and paleoecological interpretations rely on constraining the temporal resolution
of the fossil record. The taphonomic clock, that is, a correlation between the alteration of skeletal material
and its age, is an approach for quantifying time-averaging scales.We test the taphonomic clock hypothesis
for marine demersal and pelagic fish otoliths from a 10–40m depth transect on the Mediterranean silici-
clastic Israeli shelf by radiocarbon dating and taphonomic scoring. Otolith ages span the last ∼8000 yr,
with considerable variation in median and range along the transect. Severely altered otoliths, contrary
to pristine otoliths, are likely to be older than 1000 yr. For pelagic fish otoliths, at 30m depth, taphonomic
degradation correlates positively with postmortem age. In contrast, no correlation occurs for demersal
fishes at 10 and 30m depth, mostly because of the paucity of very young pristine (<150 yr) otoliths, pos-
sibly due to a drop in production over the last few centuries. Contrary tomolluscan and brachiopod shells,
young otoliths at these depths are little affected and do not showa broad spectrumof taphonomic damage,
because those that derive from predation are excreted in calcium- and phosphate-rich feces forming an
insoluble crystallic matrix that increases their preservation potential. At 40m depth, all dated otoliths
are very young but rather damaged because of locally chemically aggressive sediments, thus showing
no correlation between taphonomic grade and postmortem age. Our results show that local conditions
and the target species population dynamics must be considered when testing the taphonomic clock
hypothesis.
Konstantina Agiadi, Michele Azzarone, and Paolo G. Albano†. Department of Palaeontology, University of Vienna,
Althanstrasse 14, A-1090, Vienna, Austria. E-mail: konstantina.agiadi@univie.ac.at, michele.azzarone2@unibo.it.
†Present address: Stazione Zoologica AntonDohrn, Villa Comunale, 80121Naples, Italy. E-mail: pgalbano@gmail.com
QuanHua. Australian Nuclear Science and TechnologyOrganisation, Kirrawee DC, NSW2232, Australia. E-mail:
qhx@ansto.gov.au
Darrell S. Kaufman. School of Earth and Sustainability, Northern Arizona University, Flagstaff, Arizona 86011,
U.S.A. E-mail: Darrell.Kaufman@nau.edu
Danae Thivaiou. Department of Historical Geology and Paleontology, Faculty of Geology and Geoenvironment,
National and Kapodistrian University of Athens, Panepistimioupolis 15784, Athens, Greece. E-mail: dthivaiou@
geol.uoa.gr
Accepted: 30 July 2021
*Corresponding author.
Introduction Experimental approaches as well as
The extent of time averaging in death and increasingly affordable geochronological
fossil assemblages is crucial for quantifying tools, including radiocarbon-calibrated amino
the temporal resolution of the fossil record. acid racemization (Allen et al. 2013) and rapid
One approach to quantify scales of time aver- radiocarbon dating (Bush et al. 2013), have
aging is the taphonomic clock: older skeletons allowed researchers to test rigorously the
show a higher degree of alteration because of taphonomic clock hypothesis by attempting to
the accrual of skeletal damage with increasing correlate the preservation state with post-
postmortem age (Powell and Davies 1990; Kid- mortem age in modern to Holocene assem-
well 1993). The taphonomic clock is useful for blages. At very short timescales, years to a
unmixing assemblages into cohorts of different few decades, the taphonomic clock works pre-
ages (Albano and Sabelli 2011; Belanger 2011; dictably: skeletal shell degradation is signifi-
Yanes 2012; Hassan et al. 2014; Tomašových cantly influenced by elapsed time-since-death
et al. 2017). (e.g., Callender et al. 1994, 2002; Powell et al.
© The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society. 0094-8373/21
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45,
subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
2 KONSTANTINA AGIADI ET AL.
2002, 2008, 2011; Klompmaker et al. 2017; Cris- experiments. Then, upon burial, skeletal loss
tini and De Francesco 2019). In the longest slows down in the sequestration zone (SZ)
experiment on molluscan shells, which lasted because of greater protection frommost drivers
13 yr, edge alteration showed the most dra- of alteration. These skeletons occasionally
matic increases with time, and most shells return to the TAZ, for example, as a result of
were discolored after just 2 yr (Powell et al. bioturbation, contributing to the long tail of
2011). Over timescales from decades to millen- old skeletons often observed in the age–
nia, correlative studies gave less straightfor- frequency distributions of surficial assem-
ward results: heavily damaged shells are blages (e.g., Kowalewski et al. 1998; Carroll
generally old, but young shells can also appear et al. 2003; Harnik et al. 2017; Ritter et al.
old and old shells can bewell preserved (Powell 2017; Tomašových and Kidwell 2017; Albano
and Davies 1990; Flessa et al. 1993; Kowalewski et al. 2020). The processes of destruction and
et al. 1994; Martin et al. 1996; Kidwell 1998; burial are stochastic (Olszewski 2004). A skel-
Carroll et al. 2003; Kidwell et al. 2005). When eton can be buried quickly, thus avoiding sig-
it comes to individual alteration variables, nificant degradation, and be re-exhumed
Powell and Davies (1990) found that only much later, contributing old shells in good
shell color could be used to confidently separ- preservation state, as observed empirically. In
ate old from young beached Donax bivalve contrast, a skeleton may remain at the sedi-
shells, which was confirmed with experimental ment–water interface longer, accruing signifi-
results by Powell et al. (2011). Similarly, Kowa- cant damage in a relatively short period of
lewski et al. (1994) found correlation only time. Therefore, correlative studies on skeletons
between bivalve shell luster and postmortem decades to millennia old may provide noisy
age when comparing shelly cheniers of ages data and show only moderate correlations.
spanning 70 to 5000 yr; other taphonomic vari- However, over very long timescales, even the
ables did not present significant correlations. more conservative taphonomic features show
Studying venerid bivalves, Flessa et al. (1993) a consistent trend of degradation with age.
found a moderately positive correlation The taphonomic clock proves useful in both
between preservation state and postmortem ecologic and paleontological applications. The
age on tidal flats in Mexico and reported that rapid loss of luster in shells enables discriminat-
the bivalve shell surface was modified early in ing fresh dead specimens from older ones; such
taphonomic history, whereas material loss fresh shells can be added to counts of living indi-
took place later on. Over even longer time- viduals, for example, to overcome the lowdetect-
scales, the taphonomic clock works unambigu- ability of most land snails (Cernohorsky et al.
ously: Pleistocene shells can be consistently 2010; Albano 2014). Additionally, even though
distinguished from modern shells (Frey and geochronological methods can nowadays rou-
Howard 1986; Henderson and Frey 1986; Flessa tinely be used to quantify time averaging in the
1993; Yanes 2012), suggesting that the tapho- Holocene, they are destructive methods. Despite
nomic clock is sensitive to age differences in continuous improvements that now enable dat-
the >104 yr range (Frey and Howard 1986; Kid- ing samples with less than 1mg mass (Bush
well 1993; Wehmiller et al. 1995). et al. 2013; Gottschalk et al. 2018; Bright et al.
The apparent inconsistency in the relation- 2021), whole small skeletons may be required,
ship between damage and age over different conflicting with other research needs.
timescales can be reconciled, considering that A major example of such small skeletal parts
such results derive from the two-phase process is fish otoliths. They are incremental structures
of taphonomic loss in surficial sediments in the inner ear of marine fishes that facilitate
(Tomašových et al. 2014, 2016). First, degrad- sound and balance perception (Schulz-Mirbach
ation of skeletal material occurs quickly in the et al. 2018). Due to their species-specificmorph-
taphonomically active zone (TAZ), so that ology, sagittal otoliths, which are aragonitic
even young skeletons may accrue significant (Degens et al. 1969), are valuable for recon-
damage (Carroll et al. 2003)—results consistent structing past fish faunas. Establishing the
with the strong correlation observed in taphonomic clock of otoliths is important,
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 3
because marine fish otoliths are commonly
used for studying fish evolutionary patterns
(e.g., Landini and Sorbini 2005), fish paleobio-
geography (e.g., Girone et al. 2006; Agiadi
et al. 2011, 2017, 2018; Aguilera et al. 2014;
Schwarzhans et al. 2020), and paleoenviron-
mental conditions, including paleoclimate and
paleodepth (Andrus et al. 2002; Girone 2005;
Price et al. 2009; Agiadi et al. 2010, 2020; Ber-
tucci et al. 2018; Jones andCheckley 2019; Sand-
weiss et al. 2020).
Studies on the taphonomy of otoliths are
scarce (Lin et al. 2019), and the taphonomic
clock has never been tested for these important
vertebrate skeletal elements. We here taphono-
mically scored and radiocarbon-dated otoliths
from a depth gradient encompassing different
grain sizes on a siliciclastic shallow shelf in
the eastern Mediterranean to test the hypoth-
esis that the accrual of damage correlates with
postmortem age. In addition, we compared
the results for the otoliths of anchovies with
those of gobies and congrids, taxa with differ-
ent lifestyles, to explore the role of these factors
in otolith preservation.
FIGURE 1. Location of the sampling stations off Ashqelon in
Materials and Methods southern Israel, Mediterranean Sea.
Study Area and Sampling.—The study area is
the Mediterranean coast of southern Israel off at 10 and 30m depths, respectively, to 2.4
Ashqelon (Fig. 1), which is an open shelf receiv- mm/yr at 40m (Goodman-Tchernov et al.
ing sediment input from the Nile (Inman and 2009; Albano et al. 2020).
Jenkins 1984). The deposition of fine-grained Otolith Specimens.—We scored and dated 77
sediment is limited above ∼35m depth by otoliths of two groups of fishes: pelagic fishes
strong wave-induced counterclockwise cur- that occupy the higher part of thewater column
rents from the Nile delta northward along the and travel some distance on a daily basis, spe-
Israeli coast (Golik 1993; Avnaim-Katav et al. cifically the codlet Bregmaceros nectabanus and
2015). The fair-weather wave base is located at the anchovy Engraulis encrasicolus (n = 25);
15–25m depth (Hyams-Kaphzan et al. 2008). and demersal fishes that live in/near the sea
We collected sediment samples using a Van bottom and do not migrate, namely the congrid
Veen grab (36.5 × 31.8 cm) onboard the RV Ariosoma balearicum and the gobies Gobius paga-
Mediterranean Explorer at 10, 30, and 40m nellus, Gobius auratus, Gobius cobitis, Gobius
depths (Supplementary Table S1) in autumn niger, Lesueurigobius friesii, and Lesueurigobius
2016. At each depth, we collected five replicate suerii (n = 52). These two groups of fishes
grab samples, sieved them with a 0.5-mm have otoliths with different shapes, thin and
mesh, and picked otoliths from all of them to elongate in anchovies and thick and square/
maximize sample size. The grab samples cap- oval-shaped in gobies and congrids. Because
tured the first 5–20 cm of sediment, depending predation may be relevant to otolith preserva-
on grain size, which correspond to the TAZ. tion and input to the seafloor (as is explained
The sedimentation rate varies strongly along in the “Discussion”), we note that anchovies
the transect, from 0.4 mm/yr and 0.2 mm/yr are preyed upon by pelagic and demersal
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
4 KONSTANTINA AGIADI ET AL.
fishes, gobies by larger pelagic and demersal University of Bern, as described by Gottschalk
fishes, and congrids by large pelagic fishes et al. (2018). The calibrated radiocarbon ages
and seabirds. The studied material is shown (Supplementary Table S2) were expressed in
in the Supplementary Table S2. The selection calendar years before 2016 (year of collecting).
of otoliths was random, from the subset of Details of the radiocarbon and calibration pro-
those larger than 0.5mg in mass, in order to cedures are available in the Supplementary
achieve radiocarbon dating. In the case of Material.
B. nectabanus, we dated both otoliths found at Data Analysis.—We described the age–fre-
the 40m station. All stations contained otoliths quency distributions of the otoliths based on
of both pelagic and demersal fishes (Agiadi and their range and median, and we computed
Albano 2020), but we dated anchovy otoliths Kolmogorov-Smirnov and Wilcoxon tests to
only from the 30m station, because they were compare their shapes and medians, respect-
most abundant there. ively. To investigate the overall preservation
Taphonomic Scoring Protocol.—We evaluated state of the otoliths, we described taphonomic
the preservation of the inner face of the otoliths damage with a univariate descriptor obtained
based on six alteration variables: completeness, by averaging the scores of all taphonomic vari-
translucency, bioerosion, edge preservation, ables and defined four grades: pristine (0–0.5),
dissolution, and ornamentation loss. All moderate (0.5–1.5), severe (1.5–2.5), and high
variables were scored on a scale from 0 to 3, (2.5–3.0). We plotted the distribution of ages
where 0 indicated a pristine otolith (zero dam- in relation to this univariate score with box
age) and 3 a strongly altered otolith (maximum plots and scatter plots, and then the distribu-
damage) (Fig. 2, Table 1). Completeness reflects tion of the univariate score in relation to the
the level of fragmentation of the otolith. Trans- sampling site. We tested for differences
lucency varies from almost fully translucent in among groupswith the Kruskal-Wallis analysis
pristine otoliths, to white semi-translucent and of variance and permutational multivariate
white–yellowish and opaque in very altered analysis of variance (PERMANOVA). Pairwise
otoliths. Bioerosion qualitatively measures the p-values were assessed with the Holm-
area of the otolith affected by microborers Bonferroni correction. In addition, we plotted
(mainly algae, fungi, and sponges). Edge pres- the range of ages for each of the taphonomic
ervation measures the degree of preservation variables and tested for correlation with the
of the edge profile of the otolith, in terms of ero- Spearman rank correlation coefficient.
sion or chipping. Dissolution reflects the alter- We then performed principal coordinate ana-
ation of the otolith as expressed by chalky or lysis (PCoA) on all the taphonomic variables to
grainy appearance and dense pitting of the sur- explore variation in multivariate alteration
face. Ornamentation loss indicates the preser- among the otoliths, usingManhattan distances.
vation status of the inner-face morphology of The distribution of the otoliths (distances
the otolith, specifically the morphology of the among specimens in the PCoA ordination
sulcus acusticus and the dorsal/ventral cristae space) reflected their differences inmultivariate
(if present in the target species originally). alteration that are independent of their ages. In
The complete taphonomic scoring results are addition, to identify the taphonomic variables
reported in Supplementary Table S2. that most affected the order of the specimens
Radiocarbon Dating.—The 77 dated otoliths along the first two PCoA axes, each alteration
belong to nine fish species. Of these, 75 were variable was represented as a vector, produced
dated by accelerator mass spectrometry by maximizing the correlation between the
(AMS) radiocarbon, using powdered carbonate scores of the alteration variables on each indi-
targets following the methodology of Bush vidual otolith and the corresponding ordin-
et al. (2013). They were prepared at the Nor- ation scores along each of the first two axes
thern Arizona University and measured at the using the envfit function of the vegan package
University of California at Irvine. The two oto- (Oksanen et al. 2015). Each vector had two com-
liths of B. nectabanus were dated using the ponents: the direction, which reflected the
gas-ion source of the MICADAS AMS at the highest rate of change in the score of a given
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 5
FIGURE 2. Otoliths of the anchovy Engraulis encrasicolus showing different degrees of degradation ranging from 0 (pristine)
to 3 (heavily degraded), details given in Table 1. The otolith specimens shown are from top to bottom: OT175, OT104,
OT112, OT192, OT174, and OT135 in the first column; OT181, OT101, OT136, OT183, OT109, and OT218 in the second col-
umn (full scores in Supplementary Table S3). Scale bar, 0.5mm.
taphonomic variable (from pristine to signifi- pelagic species at 30m depth, as this was the
cantly altered), and the length. The latter was only station from which we dated large subsets
scaled by correlating it with the first two ordin- of otoliths belonging to both groups. All statis-
ation axes. Thus, variables with longer vectors tical analyses were performed using R software
were more strongly correlated with ordination v. 3.6.1 (R Development Core Team 2019).
axes. We also measured the correlation
between the first ordination axis and age and
Results
between the first ordination axis and the tapho-
nomic variables with the Spearman rank correl- Age–Frequency Distributions.—The otolith
ation coefficient. Finally, we tested the effects of assemblage spans much of the Holocene with
age and water depth on multivariate alteration a range of 4–7961 yr and a median of 559 yr
with constrained analysis of principal coordi- (n = 77). The age ranges are markedly different
nates (CAP; Anderson and Willis 2003). at the three sites (Fig. 3). The dated otoliths
The analyses were performed for the whole are 144–1622 yr old (median = 561 yr, n = 20),
dataset, for each depth, and for demersal versus 6–7961 yr old (median = 735 yr, n = 47), and
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
6 KONSTANTINA AGIADI ET AL.
TABLE 1. Taphonomic variables and scoring. The higher the value, the greater the taphonomic alteration.
Taphonomic
variable Possible values
Completeness 0 = 95%–100% 1 = 75%–95% complete 2 = 50%–75% complete 3 = 25%–50% complete
complete
Translucency 0 = clear, 1 =white, translucent 2 =white, not 3 = yellow, not translucent
translucent translucent
Bioerosion 0 = no bioerosion 1 = 1/3 bioeroded 2 = 2/3 bioeroded 3 =more than 2/3
bioeroded
Edge 0 = sharp, pristine 1 = 1/3 eroded/chipped 2 = 2/3 eroded/ 3 =more than 2/3 eroded/
preservation chipped chipped
Dissolution 0 = absent 1 = patchy dissolution 2 = diffuse dissolution 3 = pervasive dissolution
Ornamentation 0 = pristine 1 = ornamentation mostly 2 = ornamentation 3 =massive loss (original
loss ornamentation preserved (>50%) but traces (<50% ornamentation mostly
worn preserved) erased)
4–174 yr old (median = 8 yr, n = 10) at 10, 30, significant relationship (slope of the taphonomic
and 40m, respectively. At the 30m depth, the score p = 0.0013; slope of depth p = 0.0003; but
demersal species’ (n = 22) range is 6–4950 yr note the low adjusted R2 = 0.22). The results for
with a median of 744 yr, whereas the pelagic the individual depths (Fig. 5B–D) showa signifi-
species’ (n = 25) range is 11–7961 yr old with a cant, albeit weak, correlation between age and
median of 678 yr; neither the shape of the mean alteration only at 30m (Spearman rho =
age–frequency distributions nor the medians 0.33, p = 0.022); at 10 and 40m, there is no such
of these two groups differ (shape: Kolmo- correlation (Table 2) due to the very similar
gorov-Smirnov, D = 0.23, p = 0.54; median: age ranges for the different taphonomic grades.
Wilcoxon W = 305.5, p = 0.52). Time averaging, In the 30m station assemblage, otoliths from
the temporal mixing of the otolith death assem- pelagic fishes show a monotonic increase of
blage, expressed in terms of interquartile range taphonomic damage with age (Spearman rho
is 156, 1499, and 18 yr at 10, 30, and 40m, = 0.65, p = 0.0005; Fig. 5F), in striking contrast
respectively. with demersal fishes, which show a negative
Relationship between Postmortem Age and nonsignificant correlation (Spearman rho =
Mean Univariate Preservation.—The median of −0.37, p = 0.09; Fig. 5E).
the univariate mean taphonomic grade does Relationship between Postmortem Age and
not differ among the stations (Kruskal Wallis Alteration Variables.—A significant correlation
test, χ2 = 2.07, p = 0.35; Fig. 4), but the station between otolith alteration variables and age is
at 40m (median age = 8 yr) is characterized by found only in some cases (Table 2). Specifically,
a lack of otoliths in pristine condition, a remark- completeness is the variable that most com-
able result considering the very young age of monly significantly correlates positively with
the assemblage. age, followed by translucency, but the correl-
For the entire assemblage, we observe a broad ation coefficients are always≤ 0.5. Even for
distribution of ages within each taphonomic individual alteration variables, the pristine
grade (Fig. 5A). Interestingly, otoliths graded grade encompasses a broad age range (Fig. 6
as pristine span almost the entire age range, in for the full dataset, Supplementary Figs. S1–
contrast to those of moderate, severe, and high S3 for each depth station). Nevertheless, for
taphonomic grade. Differences in taphonomic the otolith assemblage of the pelagic fishes at
grade among groups are not significant (Krus- 30m depth, all alteration variables positively
kal Wallis test, χ2 = 22.38, p = 0.049). Otolith and significantly correlate with age (Supple-
age correlates positively but weakly with mean mentary Figs. S4–S5).
alteration (Spearman rho = 0.25, p = 0.026). To Relationship between Postmortem Age and
factor out depth, a linear model, with the tapho- Multivariate Preservation.—Multivariate preser-
nomic score and depth as predictors and the vation does not differ among stations (PERMA-
log10-transformed age as response, suggests a NOVA, F = 0.768, p = 0.496). The first PCoA axis
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 7
FIGURE 3. Otolith age–frequency distributions across a depth gradient on the Mediterranean southern Israeli shelf. The
dashed lines indicate the median ages. A, Entire dataset; B–D, for the assemblages at 10, 30, and 40m depths, respectively;
E–F, only for the demersal and pelagic fishes, respectively, at 30m depth.
explains 56% of the variation in otolith alter- rarely orders otoliths according to their post-
ation of the full dataset and 78%, 60%, and mortem ages (Fig. 7). Accordingly, the Pearson
73% at 10, 30, and 40m depths, respectively. correlation between the first PCoA axis and
For pelagic fishes at 30m depth, the first postmortem age is weak and nonsignificant
PCoA axis explains 74% of the variation, but (6). Again, the pelagic assemblage at 30m
only 52% for the demersal fishes. This axis depth shows the highest correlation and the
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
8 KONSTANTINA AGIADI ET AL.
respectively (today down to ∼35m depth),
where fine-grained sediment originating from
the Nile is transported northward along the
Israeli coast (Hyams-Kaphzan et al. 2008;
Avnaim-Katav et al. 2015). At 40m, the otoliths
look much altered, notwithstanding their very
young age (4–174 yr). The same high alteration
versus young age was observed for molluscan
shells (Albano et al. 2020) and thus points to
aggressive conditions in the sediments, pos-
sibly due to higher organic matter content
and thus more acidic pore water. At the 30m
depth, the correlation between age and tapho-
nomic grade is positive and significant, and
particularly strong for pelagic fishes, for
which individual alteration variables also cor-
FIGURE 4. Mean taphonomic damage of the otoliths along
the depth gradient. The distribution of the univariate relate strongly with age (Table 2). In contrast,
taphonomic score does not differ among sites, but at the at 40m, the correlation is positive but not sig-
40m depth there is a lack of pristine otoliths, even though nificant. This latter result also derives from
the death assemblage is very young.
the combined high sedimentation rate and
aggressive conditions, which lead to a very lim-
p-value closest to 0.05. In the PCoAs with the ited age range spanning only 170 yr. In such a
best correlation between the first axis and post- short time frame, the stochastic processes of
mortem age (full dataset and 30m datasets; destruction and burial blur the taphonomic
Fig. 7A,F), the vectors of the alteration variables clock signal. In contrast, the otolith age range
increase along the first axis toward older oto- at 30m spans most of the Holocene (6–7961
liths. The correlation between the first PCoA yr), enabling a clearer signal. The different
axis and the individual alteration variables is taphonomic pathways caused by local condi-
strong (usually > to >> 0.5) and significant in tions lead to distinct taphofacies (Brett and
most cases (Table 3). The first CAP axis reflects Baird 1986; Speyer and Brett 1986; Best and
the increase in postmortem age (Fig. 8) with a Kidwell 2000a; Tomašových and Zuschin
weak relationshipwithmost alteration variables. 2009; Petró et al. 2018; Ritter et al. 2019).
When adding water depth as a factor, age and Importantly, variation in taphofacies may
depth diverge markedly, but most alteration occur over relatively small spatial and depth
variables (with the exception of translucency scales, as in our case study.
and completeness) show a greater relationship The Taphonomic Clock Is Influenced byOrganis-
with age, suggesting that each sampled station mal Life Histories.—In general, otolith input to
represents a different taphofacies. seafloor sediments depends on fish production,
as it is filtered through natural mortality and
predation (Fig. 9A). For any given species,
Discussion
under constant fish production, a mass mortal-
The Taphonomic Clock Depends on the Taphofa- ity event causes an increase in otolith input,
cies.—Local conditions (e.g., depth and type of whereas a change in its predator’s abundance
sediment) are the major drivers of the strength may cause a decrease or increase in otolith
of the taphonomic clock, as clearly shown by input depending on the type of predator. On
the different results at 30 and 40m depths. At one hand, variability in input rate generates
30m, the sedimentation rate is 0.2 mm/yr and age distributions that deviate from right-skewed
the substrate is muddy sand, whereas at 40m, exponential shapes, and unimodal distributions
the sedimentation rate is much higher, 2.4 as observed at 10 or 30m indicate a recent
mm/yr, and the substrate is muddy. The two decline in input rate of otoliths. Thus, to explain
depths are above and below the sand belt, differences between species in otolith input
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 9
FIGURE 5. Box plots of postmortem age (log10-transformed) vs. taphonomic alteration grade. A, Entire dataset; B–D, for the
assemblages at 10, 30, and 40m depths, respectively; E–F, only for the demersal and pelagic fishes, respectively, at 30m
depth. In most cases, young otoliths display the full range of taphonomic alteration, but at the 40m depth, pristine otoliths
are absent, notwithstanding the young age of the assemblage. A positive and significant correlation between taphonomic
damage and age is observed only at the 30m depth for pelagic fishes.
TABLE 2. Spearman correlation between alteration variables and age. Whereas this correlation is generally weak and
nonsignificant, the taphonomic alteration of the otoliths of pelagic species at the 30m depth correlates positively and
significantly with postmortem age. Bold text indicates statistically significant values.
−30m
Full dataset −10m −30m −40m demersal −30m pelagic
(n = 77) (n = 20) (n = 47) (n = 10) (n = 22) (n = 25)
rho p rho p rho p rho p rho p rho p
Completeness 0.38 0.0006 0.33 0.14 0.50 0.0002 0.00 1 −0.12 0.59 0.82 <<0.001
Translucency 0.25 0.03 0.07 0.74 0.33 0.02 −0.18 0.60 −0.11 0.61 0.57 0.002
Bioerosion 0.38 0.10 −0.01 0.95 0.06 0.61 0.23 0.51 −0.49 0.02 0.41 0.03
Edge preservation 0.11 0.18 −0.17 0.44 0.22 0.12 0.50 0.13 −0.33 0.13 0.50 0.009
Dissolution 0.45 0.08 −0.31 0.17 0.24 0.10 0.26 0.46 −0.10 0.65 0.42 0.03
Ornamentation 0.34 0.10 −0.29 0.19 0.20 0.16 0.62 0.053 −0.22 0.31 0.46 0.01
Mean taphonomic grade 0.25 0.026 −0.15 0.54 0.33 0.022 0.52 0.12 −0.37 0.09 0.65 0.0005
trends over time, we must consider how the and mixing affect the steepness of the age distri-
changes in the factors affecting fish production, butions, and these processes are controlled by
natural mortality, and predation (temperature, depth, substrate, currents and waves, sedimen-
oxygenation, substrate condition, depth) impact tation rate, bioturbation, bioerosion, pore-water
these species. On the other hand, disintegration chemistry, temperature, and water oxygenation
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
10 KONSTANTINA AGIADI ET AL.
FIGURE 6. Box plots that show the distribution of ages (log10-transformed) within alteration variable grades for the entire
dataset, all depths pooled together. A, Completeness; B, translucency; C, bioerosion; D, edge preservation; E, dissolution; F,
ornamentation loss. For all variables, pristine otoliths span a broad time range.
(Fig. 9B). Therefore, differences in the intrinsic Similarly, the otoliths of demersal fishes at 30m
properties of the otoliths of the compared spe- span 6 to 4950 yr, but only a few of them are a
cies may result in one or more of these factors few centuries old: only 2 (9%) of the dated oto-
preferentially preserving/disintegrating and/ liths are younger than 150 yr. The lack of young
or mixing the otoliths of one species. The final otoliths contrasts our expectation: taphonomic
shape of the age distributions is a combined loss may follow different models, but all
effect of input and preservation states (Tomašo- include a fast initial loss (e.g., exponential)
vých et al. 2016). Consequently, apart from oto- that leads to typical right-skewed age–fre-
lith inputs, we have to account for otolith quency distributions dominated by young oto-
intrinsic properties to estimate species temporal liths, with a tail of few old ones (Tomašových
resolutions in otolith death assemblages. et al. 2014, 2016; Albano et al. 2020). The rela-
Our investigation clearly shows that the tive rarity or absence of very young otoliths
taphonomic clock is influenced by the life his- likely derives from smaller or absent input
tories of the target species, such as temporal from the living assemblage (e.g., in Albano
variations in production and the fish lifestyle. et al. 2016; Tomašových and Kidwell 2017;
At the 10m depth, otolith ages range back to Tomašových et al. 2018), pointing to a decline
1622 yr, but the abundance of the demersal spe- of demersal species production at least locally
cies we dated shows a decline over the last few (the 10 and 30m stations are ∼2.5 km apart).
centuries, with no otoliths younger than 144 yr. Interestingly, this decline cannot be observed
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 11
FIGURE 7. Principal coordinate analysis (PCoA) of alteration variables. Thefirst PCoA axis hardly orders otoliths according
to their postmortem age. Abbreviations: BE: bioerosion; CO: completeness; DS: dissolution; EP: edge preservation; OL:
ornamentation loss; TR: translucency.
in the pelagic fishes we dated or in the infaunal demersal fish otoliths are unlikely. The lack of
bivalves Donax semistriatus and Corbula gibba at young otoliths at these depths implies that the
the same sites (Albano et al. 2020), suggesting assemblage lacks those most pristine, compact-
that extrinsic taphonomic processes such as ing the range of taphonomic damage to the
transport or preferential disintegration of altered end (only 2 [10%] and 1 [5%] otoliths
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
12 KONSTANTINA AGIADI ET AL.
TABLE 3. Correlation between principal coordinate analysis (PCoA) axis 1 and the alteration variables are strong and
significant in most cases, suggesting that the first ordination axis orders otoliths according to taphonomic condition. Bold
text indicates statistically significant values.
Entire dataset 10m 30m 40m 30m demersal 30m pelagic
Completeness 0.43 ( p < 0.0001) −0.38 −0.41 −0.70 −0.29 −0.66
( p = 0.0997) ( p = 0.0048) ( p = 0.0247) ( p = 0.1861) ( p = 0.0003)
Translucency 0.66 ( p < 0.0001) −0.72 −0.77 0.46 −0.70 −0.83
( p = 0.0003) ( p < 0.0001) ( p = 0.177) ( p = 0.0003) ( p < 0.0001)
Bioerosion 0.79 ( p < 0.0001) −0.86 −0.74 −0.78 −0.52 −0.83
( p < 0.0001) ( p < 0.0001) ( p = 0.0078) ( p = 0.0143) ( p < 0.0001)
Edge preservation 0.87 ( p < 0.0001) −0.77 −0.90 −0.90 −0.80 −0.93
( p < 0.0001) ( p < 0.0001) ( p = 0.0004) ( p < 0.0001) ( p < 0.0001)
Dissolution 0.73 ( p < 0.0001) −0.90 −0.74 −0.44 −0.47 −0.86
( p < 0.0001) ( p < 0.0001) ( p = 0.2072) ( p = 0.0261) ( p < 0.0001)
Ornamentation loss 0.83 ( p < 0.0001) −0.80 −0.80 −0.92 −0.76 −0.90
( p < 0.0001) ( p < 0.0001) ( p = 0.0001) ( p < 0.0001) ( p < 0.0001)
FIGURE 8. Constrained analysis of principal coordinates (CAP). A, CAP axis 1 reflects the increase in postmortem age,
which has a weak relationship with most alteration variables. B, When the depth factor is added, alteration variables
(with the exception of translucency and completeness) better align with age, suggesting that each station represents a dif-
ferent taphofacies.
were graded “pristine” at 10m and for the upon by larger fishes and by fishes and sea-
demersal fish assemblage at 30m, respectively, birds, respectively (Froese and Pauly 2021).
in contrast to 7 [28%] for the pelagic fish assem- There is thus potential for differential
blage at 30m; 5 [71%] of these are younger than out-of-habitat transport and alteration in the
55 yr), thus hindering significant correlations. predators’ digestive tracts (Jobling and Breiby
The fish lifestyle (e.g., demersal vs. pelagic) 1986). The different results in terms of both dir-
may also influence postmortem processes. Pre- ection and strength of the correlation between
dation is a significant cause of otolith input into age and alteration variables between demersal
the sediment, and predators differ between the (negative and nonsignificant) and pelagic
two lifestyles: pelagic species such as the (positive and significant) may point to such dif-
anchovies are preyed upon by pelagic and ferences, but the bias introduced by the lack of
demersal fishes, whereas demersal species young demersal fish otoliths hampers drawing
such as the gobies and the congrids are preyed any final conclusions.
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 13
FIGURE 9. Simplified model showing the factors affecting the fate of otoliths from fish death to otolith final burial. A, Bio-
logical processes. Fish otoliths are deposited on the seafloor either after the decomposition of the fish carcass (natural mor-
tality) or in predator feces (predation); the production of fish populations, which depends on temperature, substrate, water
oxygenation, and depth, determines the rate of otolith input in the sediment. B–D, Taphonomic processes. Once at the sedi-
ment–water interface, otoliths are vulnerable to taphonomic damage, but they quickly get mixed into the surficial sedi-
ments (B). In the taphonomic active zone (TAZ), abiotic (temperature, oxygenation, and pore-water chemistry) and
biotic (bioerosion) factors continue to affect otolith preservation/disintegration. In addition, they are mixed due to abiotic
(currents and waves) and biotic (bioturbation) factors. Otoliths remain in the TAZ for periods comparable to those of
similar-sized skeletal parts of other organisms, such as small bivalve shells (C). Otoliths get progressively deeper in the
sediment and into the sequestration zone (SZ) at rates depending on sea bottom depth and sedimentation rate. In the
SZ, loss occurs at a lower rate, and exhumation into the TAZ is still possible due to biological activity (e.g., of deep-
burrowing invertebrates), contributing to further mixing and the occurrence of very old otoliths in the surficial death
assemblage,which is retrieved from the TAZwith standard samplingmethods such as VanVeen grabs (D). E, Fossilization.
Once otoliths are buried deeper, they undergo diagenesis to form the fossil assemblage. For comparison (see “Discussion”),
C–E also show how burial–exhumation affects bivalve shells. Otolith and bivalve colors (C–E) indicate the level of alter-
ation (white: pristine; yellow: moderate; orange: strongly altered).
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
14 KONSTANTINA AGIADI ET AL.
Comparison with Other Taxa.—Taphonomic 1965; Schwarzhans et al. 2018) (Fig. 9). Carniv-
pathways, and thus the strength of the tapho- orous fishes produce feces rich in calcium and
nomic clock, depend on local extrinsic factors phosphate, which can form an insoluble crys-
for other taxa as well. For example, molluscan tallic calcium phosphate matrix that increases
shells show different preservation states and their preservation potential (Hollocher and
correlation between preservation state and Hollocher 2012). Therefore, otoliths may be ini-
postmortem age in siliciclastic versus carbonate tially protected from degradation in the TAZ,
sediments (Kidwell et al. 2005). Carbonate further explaining why some old otoliths are
areas in particular show a greater degree of bio- still taphonomically pristine. The passage
foulers and more acidic pore waters, leading to through the predator’s digestive tract affects
a faster accrual of damage and eventually shell otoliths due to the stomach acids at a level
loss (Best and Kidwell 2000a,b; Kidwell et al. depending on the kind of predator, the expos-
2005). Consistently, brachiopod shells collected ure time, and the otolith form and structure
along a narrow and shallow depth gradient on (Jobling and Breiby 1986). The residence time
a uniform mixed carbonate–siliciclastic shelf in the predator’s digestive system is not
did not show significant differences in tapho- expected to be sufficient for the complete disin-
nomic patterns (Carroll et al. 2003). Still, we tegration of the otoliths. Instead, gastric acid
show here that even within homogenous may etch an otolith uniformly, without obliter-
shelves in terms of sediment type, the occur- ating or enhancing its ornamentation, thus
rence of organic-rich versus organic-poor sedi- making it appear almost pristine, even though
ments at relatively close distances may lead to it has been somewhat reduced in size (Jobling
different pore-water acidity and thus affect and Breiby 1986).
the preservation state and the strength of its These results suggest that testing the hypoth-
correlation with age (like our stations at 30 esis of the taphonomic clock for any skeletal
and 40m depths, which are 6 km apart on a element requires a careful assessment of spatial
siliciclastic shelf). Indeed, that taphonomic heterogeneity in abiotic conditions and knowl-
pathways depend on the environment of edge of the temporal population dynamics of
deposition is also a clear result of short-term the target species and its specific life histories.
taphonomic experiments (e.g., Callender et al.
2002; Powell et al. 2011).
Previous correlative studies based on Holo- Conclusions
cene–Recent molluscan shells in shallow Estimating the age of fossils and the temporal
shelves, thus similar to our own study, often resolution of their assemblages is the first priority
showed only moderate correlation between in all paleontological and paleobiological investi-
preservation state and age (Powell and Davies gations. Our results indicate that the strength of
1990; Flessa et al. 1993; Kowalewski et al. the correlation between preservation state and
1994; Martin et al. 1996). In contrast, our case postmortem age of fish otoliths depends on
study shows that when an otolith death assem- local extrinsic conditions, such as sediment type
blage is not biased by strong variation in skel- and pore-water acidity, as well as on the target
etal production or under particularly species’ life history.Nevertheless, in optimal con-
aggressive sediment conditions, preservation ditions (i.e., chemically nonaggressive sediments,
state and age strongly correlate positively (our continuous species production), the taphonomic
results for pelagic species at the 30m depth; clock works predictably: old-looking otoliths in
Fig. 5F, Table 2, Supplementary Fig. S5). death assemblages recovered from shallow-
Under these conditions, the otolith taphonomic marine shelves are likely to be old; broken, opa-
clock works predictably. que, and largely dissolved or eroded otoliths
In contrast to molluscan shells that rapidly can be safely regarded as old (≥1000 yr in our
accrue damage, resulting in even young system), whereas pristine otoliths are unlikely
specimens appearing old, otoliths can be better to be old (older than 1000 yr here). Considering
preserved. At least some otoliths are the present results, we suggest that future work
deposited through predator feces (Martini should focus on evaluating the taphonomic
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 15
clock hypothesis in different settings, particularly Agiadi, K., C. Giamali, A. Girone, P. Moissette, E. Koskeridou, and
deeper marine as well as anoxic environments, V. Karakitsios. 2020. The Zanclean marine fish fauna and palaeo-environmental reconstruction of a coastal marine setting in the
where chemical processes may play a more eastern Mediterranean. Palaeobiodiversity and Palaeoenviron-
dominant role. ments 100:773–792.
Aguilera,O.,W. Schwarzhans,H.Moraes-Santos, andA.Nepomuceno.
2014. Before the flood: Miocene Otoliths from eastern Amazon Pira-
Acknowledgments bas Formation reveal a Caribbean-type fish fauna. Journal of South
American Earth Sciences 56:422–446.
This work was supported by the grants of the Albano, P. G. 2014. Comparison between death and living landmol-
Austrian Science Fund (FWF) P28983-B29 “His- lusk assemblages in six forested habitats in northern Italy. Palaios
29:338–347.
torical Ecology of Lessepsian Migration” (PI: Albano, P. G., and B. Sabelli. 2011. Comparison between death and
P.G.A.) and M2894-N “Deep-Time Climate living molluscs assemblages in a Mediterranean infralittoral off-
Change Impact on Marine Food Webs” (PI: shore reef. Palaeogeography, Palaeoclimatology, Palaeoecology
310:206–215.
K.A.), and by the Palaeontological Association Albano, P. G., N. Filippova, J. Steger, D. S. Kaufman, A. Tomašových,
Research Grant “Time Resolution of Fish M. Stachowitsch, and M. Zuschin. 2016. Oil platforms in the Per-
Death Assemblages on the Eastern Mediterra- sian (Arabian) Gulf: living and death assemblages reveal no effects.
Continental Shelf Research 121:21–34.
nean Shelf,” PA-RG201803 (to K.A.). This col- Albano, P. G., Q. Hua, D. Kaufman, A. Tomašových, M. Zuschin,
laboration was facilitated by a Short-Term and K. Agiadi. 2020. Radiocarbon dating supports bivalve-fish
Scientific Mission funded by the COST Action age coupling along a bathymetric gradient in high-resolution
paleoenvironmental studies. Geology 48:589–593.
CA15121 “Advancing Marine Conservation in Allen, A. P., M. A. Kosnik, and D. S. Kaufman. 2013. Characterizing
the European and Contiguous Seas.” The fun- the dynamics of amino acid racemization using time-dependent
ders had no role in study design, data collection reaction kinetics: a Bayesian approach to fitting age-calibration
models. Quaternary Geochronology 18:63–77.
and analysis, decision to publish, or preparation Anderson, M. J., and T. J. Willis. 2003. Canonical analysis of princi-
of themanuscript.We thank S. Szidat for dating pal coordinates: a useful method of constrained ordination for
the Bregmaceros otoliths with the MICADAS ecology. Ecology 84:511–525.
Andrus, C. F. T., D. E. Crowe, D. H. Sandweiss, E. J. Reitz, and C.
method, B. S. Galil and M. Zuschin for useful S. Romanek. 2002. Otolith Δ18O record of mid-Holocene sea sur-
discussion and support throughout the project, face temperatures in Peru. Science 295:1508–1511.
J. Steger for his help during sampling and Avnaim-Katav, S., O. Hyams-Kaphzan, Y. Milker, and
A. Almogi-Labin. 2015. Bathymetric zonation of modern shelf
material processing, and the three anonymous benthic foraminifera in the Levantine basin, eastern Mediterra-
reviewers for their insightful comments. nean Sea. Journal of Sea Research 99:97–106.
Belanger, C. L. 2011. Evaluating taphonomic bias of paleoecological
data in fossil benthic foraminiferal assemblages. Palaios 26:767–778.
Data Availability Statement Bertucci, T., O. Aguilera, C. Vasconcelos, G. Nascimento, G.Marques,
K. Macario, C. Queiroz de Albuquerque, T. Lima, and A. Belém.
Data available from the ZenodoDigital Reposi- 2018. Late Holocene palaeotemperatures and palaeoenvironments
tory: https://doi.org/10.5281/zenodo.5147991. in the southeastern Brazilian coast inferred from otolith geochemis-
try. Palaeogeography, Palaeoclimatology, Palaeoecology 503:40–50.
Best, M. M. R., and S. M. Kidwell. 2000a. Bivalve taphonomy in
References tropical mixed siliciclastic-carbonate settings. I. Environmental
Agiadi, K., and P. G. Albano. 2020. Holocene fish assemblages pro- variation in shell condition. Paleobiology 26:80–102.
vide baseline data for the rapidly changing eastern Mediterra- Best, M. M. R., and S. M. Kidwell. 2000b. Bivalve taphonomy in
nean. The Holocene 30:1438–1450. tropical mixed siliciclastic-carbonate settings. II. Effect of bivalve
Agiadi, K., M. Triantaphyllou, A. Girone, V. Karakitsios, and life habits and shell types. Paleobiology 26:103–115.
M. Dermitzakis. 2010. Paleobathymetric interpretation of the Brett, C. E., andG. C. Baird. 1986. Comparative taphonomy; a key to
fish otoliths from the Lower–Middle Quaternary deposits of paleoenvironmental interpretation based on fossil preservation.
Kephallonia and Zakynthos Islands (Ionian Sea, western Greece). Palaios 1:207–227.
Rivista Italiana Di Paleontologia e Stratigrafia 116:63–78. Bright, J., D. Kaufman, K. E. Whitacre, C. Ebert, J. R. Southon,
Agiadi, K., M. Triantaphyllou, A. Girone, and V. Karakitsios. 2011. P. G. Albano, C. Flores, T. K. Frazer, Q. Hua, M. Kowalewski,
The Early Quaternary palaeobiogeography of the eastern Ionian J. C. Martinelli, D. Oakley, W. G. Parker, M. Retelle, M. N. Ritter,
deep-sea teleost fauna: a novel palaeocirculation approach. Palaeo- M. M Rivadeneira, D. Scarponi, Y. Yares, M. Zuschin, and D.
geography, Palaeoclimatology, Palaeoecology 306:228–242. S. Kaufman. 2021. comparing rapid and standard
14C ages from
Agiadi, K., A.Antonarakou, G.Kontakiotis,N.Kafousia, P.Moissette, an Assortment of Biogenic carbonates. Radiocarbon 63:387–403.
J.-J. Cornée, E. Manoutsoglou, and V. Karakitsios. 2017. Connectiv- Bush, S. L., G. M. Santos, X. Xu, J. R. Southon, N. Thiagarajan,
ity controls on the Late Miocene eastern Mediterranean fish fauna. S. K. Hines, and J. F. Adkins. 2013. Simple, rapid, and cost effect-
14
International Journal of Earth Sciences 106:1147–1159. ive: a screening method for C analysis of small carbonate sam-
Agiadi, K., A. Girone, E. Koskeridou, P. Moissette, J.-J. Cornée, and ples. Radiocarbon 55:631–640.
F. Quillévéré. 2018. Pleistocene marine fish invasions and paleo- Callender, W. R., E. N. Powell, and G. M. Staff. 1994. Taphonomic
environmental reconstructions in the eastern Mediterranean. rates of molluscan shells placed in autochthonous assemblages
Quaternary Science Reviews 196:80–99. on the Louisiana continental slope. Palaios 9:60–73.
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
16 KONSTANTINA AGIADI ET AL.
Callender, W. R., G. M. Staff, K. M. Parsons-Hubbard, E. N. Powell, Inman, D. L., and S. A. Jenkins. 1984. TheNile littoral cell andman’s
G. T. Rowe, S. E. Walker, C. E. Brett, A. Raymond, D. D. Carlson, impact on the coastal zone of the southeastern Mediterranean.
S. White, and E. A. Heise. 2002. Taphonomic trends along a fore- Pp. 1600–1617 in 19th International Conference onCoastal Engineer-
reef slope: Lee Stocking Island, Bahamas. I. Location and water ing, Houston, Tex. https://doi.org/10.1061/9780872624382.110.
depth. Palaios 17:50–65. Jobling,M., andA. Breiby. 1986. The use and abuse of fish otoliths in
Carroll, M., M. Kowalewski, M. G. Simões, and G. A. Goodfriend. studies of feeding habits of marine piscivores. Sarsia 71:265–274.
2003. Quantitative estimates of time-averaging in terebratulid Jones, W. A., and D. M. Checkley. 2019. Mesopelagic fishes domin-
brachiopod shell accumulations from a modern tropical shelf. ate otolith record of past twomillennia in the Santa Barbara basin.
Paleobiology 29:381–402. Nature Communications 10:4564.
Cernohorsky, N. H., M. Horsak, and R. D. Cameron. 2010. Land Kidwell, S. M. 1993. Patterns of time-averaging in the shallow mar-
snail species richness and abundance at small scales: the effects ine fossil record. Short Courses in Paleontology 6:275–300.
of distinguishing between live individuals and empty shells. Kidwell, S. M. 1998. Time-averaging in the marine fossil record:
Journal of Conchology 40:233. overview of strategies and uncertainties. Geobios 30:977–995.
Cristini, P. A., and C. G. De Francesco. 2019. Taphonomic field Kidwell, S. M., M.M. R. Best, andD. S. Kaufman. 2005. Taphonomic
experiment in a freshwater shallow lake: alteration of gastropod trade-offs in tropical marine death assemblages: differential time
shells below the sediment–water interface. Journal of Molluscan averaging, shell loss, and probable bias in siliciclastic vs. carbon-
Studies 85:404–413. ate facies. Geology 33:729–732.
Degens, E. T., W. G. Deuser, and R. L. Haedrich. 1969. Molecular Klompmaker, A. A., R. W. Portell, and M. G. Frick. 2017. Compara-
structure and composition of fish otoliths. Marine Biology tive experimental taphonomy of eight marine arthropods indi-
2:105–113. cates distinct differences in preservation potential.
Flessa, K. W. 1993. Time-averaging and temporal resolution in Recent Palaeontology 60:773–794.
marine shelly faunas. Short Courses in Paleontology 6:9–33. Kowalewski, M., K. W. Flessa, and J. A. Aggen. 1994. Taphofacies
Flessa, K. W., A. H. Cutler, and K. H. Meldahl. 1993. Time and taph- analysis of recent shelly cheniers (beach ridges), northeastern
onomy: quantitative estimates of time-averaging and stratigraphic Baja California, Mexico. Facies 31:209.
disorder in a shallow marine habitat. Paleobiology 19:266–286. Kowalewski, M., G. A. Goodfriend, and K. W. Flessa. 1998. High-
Frey, R. W., and J. D. Howard. 1986. Taphonomic characteristics of resolution estimates of temporal mixing within shell beds: the
offshore mollusk shells, Sapelo Island, Georgia. Tulane Studies in evils and virtues of time-averaging. Paleobiology 24:287–304.
Geology and Paleontology 19. https://journals.tulane.edu/ Landini, W., and C. Sorbini. 2005. Evolutionary trends in the
tsgp/article/view/1054. Plio-Pleistocene ichthyofauna of theMediterranean basin: nature,
Froese, R., and D. Pauly, eds. 2021. FishBase. www.fishbase.org, timing and magnitude of the extinction events. Quaternary
version 02/2021. International 131:101–107.
Girone, A. 2005. Response of otolith assemblages to sea-level fluctua- Lin, C.H., B. deGarcia,M. E. R. Pierotti, A.H.Andrews, K.Griswold,
tions at the lower Pleistocene Montalbano Jonico Section (southern A. O’Dea. 2019. Reconstructing reef fish communities using fish
Italy). Bolletino della Societa Paleontologica Italiana 44:35–45. otoliths in coral reef sediments. PLoS ONE 14:e0218413.
Girone, A., D. Nolf, and H. Cappetta. 2006. Pleistocene fish otoliths Martin, R. E., J. F. Wehmiller, M. S. Harris, and W. D. Liddell. 1996.
from the Mediterranean basin: a synthesis. Geobios 39:651–671. Comparative taphonomyof bivalves and foraminifera fromHolo-
Golik, A. 1993. Indirect evidence for sediment transport on the con- cene tidal flat sediments, Bahia La Choya, Sonora, Mexico (nor-
tinental shelf off Israel. Geo-Marine Letters 13:159–164. thern Gulf of California): taphonomic grades and temporal
Goodman-Tchernov, B.N.,H.W.Dey, E.G.Reinhardt, F.McCoy, and resolution. Paleobiology 22:80–90.
Y. Mart. 2009. Tsunami waves generated by the Santorini eruption Martini, E. 1965. Die Fischfauna von Sieblos/Rhön (Oligozän).
reached eastern Mediterranean shores. Geology 37:943–946. Senckenbergiana Lethaea 46:291–314.
Gottschalk, J., S. Szidat, E. Michel, A. Mazaud, G. Salazar, Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre,
M. Battaglia, J. Lippold, and S. L. Jaccard. 2018. Radiocarbon D. McGlinn, P. R. Minchin, R.B. O’Hara, G. L. Simpson,
measurements of small-size foraminiferal samples with the P. Solymos, M. H. H Stevens, E. Szoecs, and H. Wagner. 2015.
mini carbon dating system (MICADAS) at the University of Vegan: community ecology package. https://cran.r-project.org/
Bern: implications for paleoclimate reconstructions. Radiocarbon web/packages/vegan, accessed 10 February 2021.
60:469–491. Olszewski, T. D. 2004. Modeling the influence of taphonomic
Harnik, P. G.,M. L. Torstenson, andM.A.Williams. 2017. Assessing destruction, reworking, and burial on time-averaging in fossil
the effects of anthropogenic eutrophication on marine bivalve life accumulations. Palaios 19:39–50.
history in the northern Gulf of Mexico. Palaios 32:678–688. Petró, S. M., M. N. Ritter, M. A. Gómez Pivel, and J. C. Coimbra.
Hassan, G. S., E. Tietze, P. A. Cristini, and C. G. De Francesco. 2014. 2018. Surviving in thewater column: defining the taphonomically
Differential preservation of freshwater diatoms and mollusks in active zone in pelagic systems. Palaios 33:85–93.
Late Holocene sediments: paleoenvironmental implications. Powell, E. N., and D. J. Davies. 1990. When is an “old” shell really
Palaios 29:612–623. old? Journal of Geology 98:823–844.
Henderson, S. W., and R. W. Frey. 1986. Taphonomic redistribution Powell, E. N., K. M. Parsons-Hubbard, W. R. Callender, G. M. Staff,
of mollusk shells in a tidal inlet channel, Sapelo Island, Georgia. G. T. Rowe, C. E. Brett, S. E. Walker, A. Raymond, D. D. Carlson,
Palaios 1:3–16. S. White, and E. A. Heise. 2002. Taphonomy on the continental
Hollocher, K., and T. C. Hollocher. 2012. Early process in the fossil- shelf and slope: two-year trends—Gulf of Mexico and Bahamas.
ization of terrestrial feces to coprolites, andmicrostructure preser- Palaeogeography, Palaeoclimatology, Palaeoecology 184:1–35.
vation. In: Vertebrate Coprolites. Bulletin of the New Mexico Powell, E. N., W. R. Callender, G. M. Staff, K. M. Parsons-Hubbard,
Museum of Natural History and Science 57:79–92. Albuquerque: C. E. Brett, S. E. Walker, A. Raymond, and K. A. Ashton-Alcox.
New Mexico Museum of Natural History & Science. 2008. Molluscan shell condition after eight years on the sea
Hyams-Kaphzan, O., A. Almogi-Labin, D. Sivan, and C. Benjamini. floor—taphonomy in the Gulf of Mexico and Bahamas. Journal
2008. Benthic foraminifera assemblage change along the south- of Shellfish Research 27:191–225.
eastern Mediterranean inner shelf due to fall-off of Nile-derived Powell, E. N., G. M. Staff, W. R. Callender, K. A. Ashton-Alcox, C..
siliciclastics. Neues Jahrbuch für Geologie und Paläontologie - E. Brett, K. M. Parsons-Hubbard, S. E. Walker, and A. Raymond.
Abhandlungen 248:315–344. 2011. Taphonomic degradation of molluscan remains during
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30
TAPHONOMIC CLOCK IN FISH OTOLITHS 17
thirteen years on the continental shelf and slope of the north- Speyer, S. E., and C. E. Brett. 1986. Trilobite taphonomy andMiddle
western Gulf of Mexico. Palaeogeography, Palaeoclimatology, Devonian taphofacies. Palaios 1:312–327.
Palaeoecology 312:209–232. Tomašových, A., and S. M. Kidwell. 2017. Nineteenth-century
Price, G. D., D. Wilkinson, M. B. Hart, K. N. Page, and S. T. Grimes. collapse of a benthic marine ecosystem on the open continental
2009. Isotopic analysis of coexisting Late Jurassic fish otoliths and shelf. Proceedings of the Royal Society of London B 284:20170328.
molluscs: implications for upper-ocean water temperature esti- Tomašových, A., and M. Zuschin. 2009. Variation in brachiopod
mates. Geology 37:215–218. preservation along a carbonate shelf-basin transect (Red Sea
R Development Core Team. 2019. R: a language and environment and Gulf of Aden): environmental sensitivity of taphofacies.
for statistical computing. Vienna, Austria: R Foundation for Stat- Palaios 24:697–716.
istical Computing. Tomašových, A., S. M. Kidwell, R. F. Barber, and D. S. Kaufman.
Ritter,M.N., F. Erthal,M.A.Kosnik, J. C.Coimbra, andD. S. Kaufman. 2014. Long-term accumulation of carbonate shells reflects a
2017. Spatial variation in the temporal resolution of subtropical 100-fold drop in loss rate. Geology 42:819–822.
shallow-water molluscan death assemblages. Palaios 32:572–583. Tomašových, A., S. M. Kidwell, and R. F. Barber. 2016. Inferring
Ritter,M.N., F. Erthal, and J. C. Coimbra. 2019. Depth as an overarch- skeletal production from time-averaged assemblages: skeletal
ing environmental variable modulating preservation potential and loss pulls the timing of production pulses towards the modern
temporal resolution of shelly taphofacies. Lethaia 52:44–56. period. Paleobiology 42:54–76.
Sandweiss, D. H., C. F. T. Andrus, A. R. Kelley, K. A. Maasch, E. Tomašových, A., J. Schlogl, A. Biron, N. Hudackova, and T. Mikus.
J. Reitz, and P. B. Roscoe. 2020. Archaeological climate proxies 2017. Taphonomic clock and bathymetric dependence of cephalo-
and the complexities of reconstructing Holocene El Niño in pod preservation in bathyal, sediment-starved environments.
coastal Peru. Proceedings of the National Academy of Sciences Palaios 32:135–152.
USA 117:8271–8279. Tomašových, A., I. Gallmetzer, A. Haselmair, D. S. Kaufman,
Schulz-Mirbach, T., M. Olbinado, A. Rack, A. Mittone, A. Bravin, R. M. Kralj, D. Cassin, R. Zonta, and M. Zuschin. 2018. Tracing the
R. Melzer, F. Ladich, and M. Heß. 2018. In-situ visualization of effects of eutrophication on molluscan communities in sediment
sound-induced otolith motion using hard X-ray phase contrast cores: outbreaks of an opportunistic species coincide with
imaging. Scientific Reports 8:3121. reduced bioturbation and high frequency of hypoxia in the Adri-
Schwarzhans, W. W., T. D. Murphy, and M. Frese. 2018. Otoliths in atic Sea. Paleobiology 44:575–602.
situ in the stem teleost Cavenderichthys talbragarensis (Woodward, Wehmiller, J. F., L. L. York, and M. L. Bart. 1995. Amino acid race-
1895), otoliths in coprolites, and isolated otoliths from the Upper mization geochronology of reworked Quaternary mollusks on
Jurassic of Talbragar, New SouthWales, Australia. Journal of Ver- U.S. Atlantic coast beaches: implications for chronostratigraphy,
tebrate Paleontology 38:e1539740. taphonomy, and coastal sediment transport. Marine Geology
Schwarzhans,W., K. Agiadi, andG. Carnevale. 2020. LateMiocene– 124:303–337.
Early Pliocene evolution of Mediterranean gobies and their envir- Yanes, Y. 2012. Shell taphonomy and fidelity of living, dead,
onmental and biogeographic significance. Rivista Italiana di Holocene, and Pleistocene land snail assemblages. Palaios
Paleontologia e Stratigrafia 126:657–724. 27:127–136.
Downloaded from https://www.cambridge.org/core. ANSTO Australian Nuclear Science and Technology Organisation, on 15 Dec 2021 at 06:27:45, subject to the
Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2021.30