Introduction
The genus Crassostrea Sacco (1897) comprises numerous commercially
exploited species. The modes of growth and population structures of extant
Crassostrea species are of paramount importance for oyster fishery
(FAO, 2015). Consequently, a wealth of data exists on the ontogeny, biology
and ecological requirements. These data, in turn are a valuable base for the
interpretation of the autecology of fossil congeners. Extant
Crassostrea are sessile bivalves adapted to estuarine and intertidal
environments where they have to cope with high environmental stress. Whilst
physicochemical stress is managed by genetic response (Zhang et al., 2012),
the formation of thick shells is a strategy against predation (Lombardi et
al., 2013; Robinson et al., 2014). The largest and fastest growing
Crassostrea species flourished during the Miocene and Early Pliocene
and became replaced by comparatively smaller and thinner species thereafter
(Kirby and Jackson, 2004). Among these, Crassostrea gryphoides (von
Schlotheim, 1813) is the largest, attaining shell lengths of up to 80 cm and
individual ages of more than 40 years (Harzhauser et al., 2010). The
Pleistocene–Holocene extirpation of large and thick-shelled
Crassostrea species was explained by a shift from shallow-marine
towards estuarine–intertidal habitats to escape from predation (Kirby, 2000,
2001). At least for C. gryphoides this model does not fit because
the oyster lived as secondary soft-bottom dweller in the intertidal zone of
estuaries along the circum-Tethyan coasts (Laurain, 1980; Schultz, 2001;
Mandic et al., 2004). This species evolved during the Late Oligocene in the
European Paratethys Sea and became ubiquitous in the Paratethys Sea, the
proto-Mediterranean Sea and the eastern Atlantic throughout the Early to Late
Miocene. It might even have entered the Indian Ocean during the Miocene
(Newton and Smith, 1912) and reached the North Sea during the Middle Miocene
(Schultz, 2001). Pliocene records from the eastern Atlantic and North Africa,
however, may need verification (see Schultz, 2001 for a detailed list of
occurrences). This species became extinct around the Miocene/Pliocene
boundary or with the onset of the Pliocene cooling 3 Ma ago at the latest.
Studies on growth in fossil Crassostrea species (and other oysters)
and the resulting carbonate production were published by Chinzei (1982, 1986,
1995), Chinzei and Seilacher (1993), Kirby (2001) and Kirby and
Jackson (2004). These studies are based on collection material comparing
species and specimens from different stratigraphic horizons. No study,
however, tried to capture the size and age structures of a fossil
Crassostrea reef, presumably representing a real population of
coeval specimens. The lack of such studies is clearly linked to the fact that
fossil shell beds usually represent time-averaged assemblages (Kidwell, 1986,
1991), which only vaguely reflect original community structures. Although
some in situ preserved fossil Crassostrea reefs are known (e.g.,
Hoşgör, 2008; Ragaini and Di Celma, 2009; Chinzei, 2013) no
population data exist, which would allow a comparison with modern oyster
reefs. Herein, we analyze an Early Miocene Crassostrea shell bed
covering an area of 459 m2, which is permanently exposed at a
geopark in Austria. The shells are concentrated in a sheet-like, ca. 20 cm thickness
layer, which was formed by a major storm or tsunami, amalgamating a single
oyster reef in an event bed (Fig. 1a–c). Although the hydrodynamic process
will have biased the original structure to some degree, our data suggest that
no out-of-habitat transport occurred and the shell bed still reflects the
original composition and thus the population structure of an oyster reef from
the onset of the Miocene Climatic Optimum (Zachos et al., 2008; Goldner et
al., 2014).
Part of the digital surface model of the shell bed; the white cross
indicates the area, within which all objects were digitally outlined and
evaluated. It contains 1121 complete shells of C. gryphoides and
7047 fragments of that species (a). Outcrop pictures of the shell
bed illustrating the density and extent of the shell bed (b–c),
(b) width ca. 2 m; (c) see workers as scale.
Crassostrea reefs flourished during the Miocene within the tropical reef belt (Mandic
et al., 2004) but were also successful in more northern latitudes (Wiedl et
al., 2013; Harzhauser et al., 2010). Therefore, the main purpose of this
paper is to quantify the growth performance of the Miocene giant oyster and
to reveal its significance as part of the Miocene “carbonate factory”.
Moreover, we test whether size–frequency data deduced from fossil oyster shells
allow a comparison with community structures of extant Crassostrea reefs.
A taxonomic note
Although the type of Crassostrea gryphoides (von Schlotheim, 1813)
was described from the mid-Miocene of Romania, the name is also used in
biological literature for an extant backwater species from India and Pakistan
(Newton and Smith, 1912; Chatterji et al., 1985; Nagi et al., 2011; Afsar et
al., 2014; Trivedi et al., 2015). The taxonomic status of the extant species
is unclear; based on molecular data, Reece et al. (2008) considered C.
“gryphoides” to be closely related with C. belcheri
(Sowerby, 1871), whilst molecular data of Trivedi et al. (2015) suggest a
close relation with C. cuttackensis (Newton and Smith, 1912), which
was originally described as subspecies of C. gryphoides. Whatever
the taxonomic and systematic status of the recent species may be, it is most
probably not conspecific with the European fossil species. It differs in its
more regular and elongate-ovoid outline (Durve and Bal, 1960), in the short and
bean-shaped adductor muscle scar (Durve, 1974; Siddiqui and Ahmed, 2002) and in
it being more inequivalved. Overall, the recent species is clearly smaller with
the largest specimen documented so far attaining 508 mm in length (Mahar and
Awan, 2012) but usually ranging around 50–120 mm (Chatterji et al., 1985;
Nagi et al., 2011).
Nevertheless, the Miocene species is closely related to the extant
Asian-Pacific Crassostreinae species, which show a large genetic difference
from Atlantic species (Littlewood, 1994; Ó Foighil et al. 1995; Wang et
al., 2004; Ren et al., 2010; Salvi et al., 2014). The Asian-Pacific group
(e.g., C. gigas, C. plicatula, C. ariakensis) and
Atlantic group (e.g., C. virginica, C. rhizophorae,
C. gasar) differ considerably in mitochondrial genes, nuclear genome
and chromosome structures (Wang et al., 2004; Ren et al., 2010; Salvi et al.,
2014). The divergence between both groups seems to have happened already in
Cretaceous times and the diversification of the Asian-Pacific group started
during the Eocene (Ren et al., 2014). Based on this genetic evidence and
biogeographic separation, Salvi et al. (2014) introduced the genus
Magallana Salvi et al. (2014) for the Asian-Pacific
species group with Ostrea gigas Thunberg (1793) as type species.
Salvi et al. (2014), however, did not provide a formal “description or
definition that states in words characters that are purported to
differentiate the taxon” (ICNZ Art. 13.1.1). The authors only refer to a
description of the type species. Therefore, Magallana is formally
unavailable (see also Marshall, 2015) and we use Crassostrea in its
traditional sense.
Geological setting and paleoenvironment
The investigated oyster shell bed was excavated at Stetten in Lower Austria
(48∘22′03.33 N, 16∘21′33.22 E). It is part of the about
600 m thick lower Miocene (upper Burdigalian = Karpatian regional stage)
siliciclastic succession of the Korneuburg Basin, which is a 20 km long and
7 km wide halfgraben within the Alpine–Carpathian thrust-belt (Fig. 2)
(Wessely, 1998). The basin fill is dominated by an alternation of shoreface
and tidal flat deposits, which were formed in an embayment of the Paratethys
Sea (Zuschin et al., 2014). More than 650 species-level taxa have been
described from the area (Sovis and Schmid, 1998, 2002) and the
paleoenvironments are well understood (Harzhauser et al., 2002; Zuschin et
al., 2014). The oyster reef flourished in an estuary fringed by salt marshes,
Taxodiaceae swamps and scattered Avicennia mangroves (Harzhauser et
al., 2002; Kern et al., 2010). The pollen record of the Stetten section
documents a warm subtropical climate with marked seasonality (Kern et al.,
2010). A warm and wet summer season with ca. 204–236 mm precipitation
during the wettest month was alternating with a rather dry winter season with
precipitation of ca. 9–24 mm during the driest month. The mean annual
temperature ranged between 15.7 and 20.8 ∘C, with about 9.6–13.3 ∘C during the cold season and 24.7–27.9 ∘C during the
warmest month. These data suggest similarities with the modern “Cwa”
climate of Köppen (1936). Today this climate covers parts of northern India
extending into southeastern Asia (southern Nepal, Myanmar, northern Thailand)
to East China and in central/south Africa (eastern Angola, Zambia, northern
Zimbabwe, northern Mozambique) (Peel et al., 2007; Kern et al., 2010). The
distinct seasonality was also revealed in sclerochronologic analysis of one
of the Crassostrea shells collected from the shell bed (Harzhauser
et al., 2010). This shell exhibits a regular annual rhythm of at least 11
seasons with a temperature range of 9.8 ∘C. Thus, the paleoclimatic
and paleoenvironmental frame of the C. gryphoides shell bed is
comparable to the settings of modern Crassostrea reefs in the
subtropical parts of the Asian Pacific.
Geographic position of the Stetten site within the Korneuburg
Basin north of Vienna in Austria; shaded areas represent pre-Miocene
basement; dashed lines are major faults (modified from Dellmour and
Harzhauser, 2012).
The fossil shell bed was excavated in a 3-month campaign by the Natural
History Museum Vienna in 2008. The oyster bed was covered by up to 10 m
of silty sand and clay, which was successively removed. Due to the
largely unconsolidated state of the surrounding silty sand, the excavation
of the shell bed could be done manually with steel gravers and brushes; no
water or any chemicals were added and all shells and fragments remained in
their original position. The oyster shells themselves are well preserved and
robust. Therefore, no artificial fragmentation occurred during the
excavation.
Examples of the data acquisition: orthophoto and digital surface
model (DSM) are used to define shell outlines manually. Together with
various attributes, such as degree of fragmentation and taxon ID, these data
are georeferenced in an ArcGIS database. Yellow lines in the DSM are
examples of center lines.
Originally, the shell bed was nearly flat at the time of deposition but has
now an undulate surface due to postsedimentary tectonic activity. This tectonic
phase occurred during the Middle Miocene at least 1–2 million years after
deposition and caused a tilting of the units of ca. 25∘ in the western
direction. During that tilting, a NW–SE trending fault system developed that
caused the current relief. Locally, the displacement by the faults is in the
range of a few centimeters.
Harzhauser et al. (2015) describe the complex taphonomy of the shell bed,
which was formed by a tsunami or an exceptional storm and represents an event
deposit sensu Einsele et al. (1991) and Kidwell (1991). As discussed by
Harzhauser et al. (2015), the assemblage is not monospecific but contains
about 46 molluscan species of which Crassostrea gryphoides
predominates in individual numbers (79.4 %). The species, such as the
potamidid gastropod Ptychopotamides papaveraceus and the venerid
bivalve Venerupis basteroti, lived partly within the oyster reef or
were admixed from adjacent mudflats and shallow sublittoral habitats. As
shown by Harzhauser et al. (2015), the fossil bed is parautochthonous.
Although the oyster shell bed is clearly not in situ but reworked, the
original community structure still seems to be reflected, which is the basic
working hypothesis of this paper. Lack of sorting is indicated by the
accumulation of very small and very large shells. Similarly, the equal
contribution by left and right valves points to the preservation of the
primary composition and contradicts the hypothesis of hydrodynamic sorting
and selective transport. Despite the bias of post-event processes, when the
exhumed shells were exposed for a few years on the seafloor, the rapid
subsequent burial preserved most of the original distribution patterns.
Materials and methods
Data acquisition by terrestrial laser scanning and orthophotos
Terrestrial laser scanning has triggered a revolution in topographic terrain
capturing, especially in the generation of digital terrain models. Methods
for generating such models from laser scanning data are discussed by Kraus
and Pfeifer (2001) and references therein. Terrestrial laser scanning was
applied to document the site as georeferenced 3-D point cloud (Otepka et al.,
2013). A Faro Focus Laser scanner with a nominal point measurement accuracy
of 1 mm (SD) in each coordinate and a sampling distance of
approximately 1 mm was used. The individual point clouds of each scan were
transformed first into one common coordinate system and then georeferenced by
control points to Universal Transverse Mercator (UTM) coordinates (resolution
below 2 mm). A robust filter (pre-processing) was applied to reduce
measurement noise while preserving surface structures like sharp edges
(Nothegger and Dorninger, 2009). The surface triangulation is based on the
Poisson surface reconstruction method (Kazhdan et al., 2006). The points of
this triangulation are used for interpolating a regular grid of heights above
the plane of the shell bed using the scientific software OPALS (Pfeifer et
al., 2014). In addition, a Canon 60D with a Canon EF 20 mm f2.8 was used to
capture more than 300 photos from a moving platform. The camera was placed
approximately orthogonal to the fossil bed. From the photos with a nominal
ground resolution of approximately 0.6 mm per pixel an orthophoto mosaic was
generated with a resolution of 0.5 mm per pixel. To detect patterns in the
distribution and composition of shells two transects (N–S, W–E) were
defined, each represented by 42 m2 with a central overlap (Fig. 1). All
objects within this area were manually outlined on the digital surface model
and cross-checked based on the high-resolution orthophotos (Fig. 3).
Models of six shells based on high-resolution laser scanning data of
shells from the collections of the Natural History Museum. These specimens
document the broad range of morphologies and were used for volume
calculations; L = left shell, R = right shell.
Manual outlines are vector data sets in the form of manually digitized polygons
representing the boundaries of the identified specimens. They are created as
thematic layer in an ArcGIS environment. The polygon is defined by features
such as points (i.e., vertices connected with lines). Each polygon is a 2-D
visual representation of the manually digitized specimen from the adequate
orthophoto and its corresponding digital surface model. Further, manually
digitized data are organized into a table. This tabular structure has its
elements, i.e., numerical and descriptive attributes. For instance, numerical
attributes are ID, length, orientation, etc. Descriptive attributes are
taxon, side (left, right, unknown), state of preservation (complete, low,
moderate, high fragmented), etc.
The outline data are composed of about 1000 virtual points (nodes) on
average per object and are also stored in the georeferenced ArcGIS database.
These allow an automatic calculation of the surface area of each object by
using the Calculate Geometry tool.
Size–frequency diagrams for center line length and area data (log
transformed) with cohorts (dashed lines) as detected by mixture analysis
(a, b). Box-plot illustrating the strongly right-skewed distribution
for fragments (n=7047) and a clear separation from the size distribution
pattern of complete shells (n=1121) (c).
In total, 10 284 objects were defined. Of these, 8168 objects were
identified as Crassostrea gryphoides of which 1121 are complete
shells (see supplementary table); 86 % of the specimens display various
degrees of fragmentation and are excluded from the size–frequency analysis.
Four categories of fragmentation were used: complete shells are fully
preserved or display only minor damage, which might have occurred already
during the life of the animal (n=1121). The category “low fragmentation”
comprises shells in which not more than 1/2 of the assumed length is
missing (n=951). Moderate fragmentation is defined by representing at
least 1/2 of the original shell lengths (n=1638). The category “high
fragmentation” comprises 4458 specimens of strongly damaged shells
representing less than 1/4 of the complete shell. Note that the attribute
fragmentation does not contain any information on abrasion. The fragments
usually show sharp fractures, and therefore the main cause for fragmentation
seems to be predatory and hydrodynamic breakage. The ratio between left and
right valves is balanced (0.98). The distribution of the shells is not
uniform, occasionally featuring areas of higher shell densities, which seem
to reflect former colony-like concentrations.
Shell length and area
Crassostrea gryphoides shows a very broad range of morphologies,
ranging from elongate shells to strongly curved and sigmoidal shapes
(Fig. 4). Therefore, measuring shell length as a straight line, as done in
other extant and fossil Crassostrea species, is inadequate. To
overcome this problem, we evaluated shell length based on the 2-D center
line. Center line length is the term used in photogrammetry and aims for
capturing the real shell length as far as possible. Here it is an imaginary
curved line spanning the maximum length of the shell. The advantage of this
method is that the center line will approximate the “real” lengths of the
curved and irregularly shaped shells much better than any manual attempt in
the field.
For the automatic determination of the center line we used the shell margins,
which comprise about 1000 points on average. For easier calculation the
outline point number was reduced to 100 and then filtered to points with
close to even spacing. In the next step, a Delaunay triangulation was
calculated between the filtered outline points (Delaunay, 1934), constrained
by the edges between the outline points. To find the center line for each
oyster outline, the Voronoi diagram was formed (Voronoi, 1908) from the
triangulation. The edges between neighboring Voronoi vertices within the
boundary are the medial axis transform (MAT) for the oyster outline
(Aichholzer et al., 1996). The longest 2-D path in this tree was found using
Dijkstra's algorithm between MAT end points (Kirk, 2015).
The center line lengths of 1121 complete Crassostrea shells, rounded
to the nearest mm, range from 48 to 602 mm with a mean of 237 mm (σ= 89 mm) (Fig. 5a). The data distribution displays a positive skewness of
0.52 and the Shapiro–Wilk test excludes normal distribution for raw data and
log10-transformed measurements. Area data range from 1708 to 56 755 mm2
with a mean of 16 983 mm2 (σ= 8414 mm2) (Fig. 5b). These
data show also a positive skewness (0.83) and normal distribution is rejected
by the Shapiro–Wilk test.
Based on the manual outlines, the exposed shell area can be deduced directly.
Area data are slightly underestimated because shells are not always exposed
parallel to the bedding plane but may be somewhat oblique. Despite the fact
that area data are somewhat biased by oblique shells, the correlation between
center line lengths and areas is highly significant (raw data: r=0.92, p<0.001; log10-transformed: r=0.93, p<0.001)
(Fig. 6).
Regression analysis revealing a significant correlation between
length and area of complete shells.
Length–frequency data
Non-normal distribution of length–frequencies is a common pattern in extant
Crassostrea reefs (e.g., Coakley, 2004; Baqueiro Cárdenas and
Aldana Aranda, 2007; Harding et al., 2008; Nurul Amin et al., 2008; Ross and
Luckenbach, 2009; Goslier et al., 2014). It results from seasonal and/or
annual recruitment with distinct cohorts (sensu Powell et al., 2006, 2015;
Southworth et al., 2010). For instance, the (sub)tropical C. madrasensis and C. rhizophorae display a distinct annual
recruitment peak (Nurul Amin et al., 2008; Mancera and Mendo, 1996). In
multiannual communities this results in a right-skewed distribution due to
the loss of old specimens by natural mortality and shell loss. For extant
Crassostrea reefs, the analysis of the cohorts is routinely
performed using Bhattacharya's model or the EM-Algorithm of Dempster et
al. (1977), which tries to detect normal distributions within the
length–frequency data. Consequently, in order to test for cohort mixing,
lengths of C. gryphoides were subjected to mixture analysis, a
maximum-likelihood method for estimating the parameters of two or more
univariate normal distributions, based on a pooled univariate sample (Hammer,
2015). Statistical analyses were performed in PAST versions 2.17c and 3.06
(Hammer et al., 2001). Akaike's information criterion (AIC) was used to test
the goodness of fit of the maximum likelihood estimates to the
length–frequency data.
In log10-transformed length frequency diagrams, the maximum likelihood based
analysis reveals lowest AIC values for four or five cohorts. Similarly,
log-transformed area data have lowest AIC values if four or five cohorts are
detected. The assumption of more groups does not lower the AIC, or the computed
cohorts comprise unrealistic narrow cohort ranges, which are nested within
larger ones.
Growth model
Kirby et al. (1998), Kirby (2000, 2001) and Kirby and Jackson (2004) used
ligamental increments of fossil and recent Crassostrea species to
estimate individual life spans, assuming that increments are formed annually.
The ligamental area of these Crassostrea species is typically
structured by alternating transversal, growth ridges and furrows, oriented
perpendicular to growth direction, corresponding to phases of rapid and low
calcification. The specimens from the Stetten site lack such well-defined
ridges. In all specimens of C. gryphoides analyzed by Harzhauser et
al. (2010) for stable isotopes, the counting of increments would have
resulted in a large overestimation of the life spans. Similarly, Alam and
Das (1999) documented a clear misfit between growth increments and age for
the extant C. madrasensis. Therefore, we restrict our age estimates
solely to growth rates of C. gryphoides deduced from stable isotope
profiles published by Harzhauser et al. (2010). According to these authors, a
shell from Stetten attained 43 cm in length at an age of 11 years and the
second one from a slightly younger horizon was 63 cm long at an age of 16
years. These values document an average growth rate of ∼ 3.9 cm per
year and might serve as a base for rough age estimates for the complete adult
shells from the Stetten shell bed.
For juvenile shells, this estimate would be wrong due to the non-linear mode
of growth known from extant Crassostrea species, which show very
high initial growth rates (Kennedy et al., 1996). Similarly, growth rates of
Crassostrea gryphoides seem to decline in very old and large
specimens as shown for a 78 cm long and 41-year-old shell from the upper
Langhian of Austria (Harzhauser et al., 2010). To cope with the non-linear
growth, growth curves of extant Crassostrea species are routinely
calculated with the von Bertalanffy equation (von Bertalanffy, 1934). This
equation is SLt= SLmax(1-e-k(t-t0)), where SLt is
shell length at time t, SLmax is the asymptotic shell length,
t0 is the size at time 0, and k is a rate constant. Herein, we used the
length of the center line of each shell as SLt as this measure captures
the real growth length of the partly strongly curved or sigmoid specimens.
For SLmax we used the size-to-age data of the 78 cm long shell,
which is the largest individual known so far.
Ratio between chalky and foliate layers
The calcitic Crassostrea shells consist of two structures: thin but
densely spaced foliate layers separated by thick layers of light-weight
chalky material (Stenzel, 1971; Higuera-Ruiz and Elorza, 2009). This fast
growing structure is interpreted to be a major adaptive advantage of
Crassostrea to impede drilling predation and to prevent from sinking
in the soft bottom (Seilacher, 1984; Chinzei, 1995; Kirby, 2001; Vermeij,
2014). In fossil shells the chalky layer is completely recrystallized and has
the same density as the foliate layer. Nevertheless, it is optically easily
recognized by its lighter color and the nearly opaque appearance. A polished
longitudinal section of an articulated C. gryphoides shell
(providing data for left and right shells) was scanned and the ratio between
both shell structures was quantified by image analysis (Fig. 7). This method
is only an approximation to the true value, as the ratio may vary locally
(Durve and Bal, 1960; Chinzei, 1995), but it is clearly an improvement
compared to former studies that used only linear transects or sectors within
the shell (Durve and Bal, 1960; Chinzei, 1995; Kirby, 2001).
Longitudinal section through C. gryphoides from the oyster reef site showing
the high amount of chalky layers (gray) and the low amount of foliate layers
(black).
The image analysis of the cross-section documents proportions of 64 chalky to
36 % foliate layers for the right shell and of 61 to 39 % for the
left shell. The density of the chalky layer when wet ranges around
1.15–1.32 g cm-3 (Chinzei, 1995) and the density of the foliate layer
ranges around 2.2–2.5 g cm-3 (Chinzei, 1995; Yoon et al., 2003) and
has a clear upper limit by the density of calcite (2.7 g cm-3). Using
1.2 for the chalky layer and 2.2 g cm-3 for the foliate
layer as rough estimates, mean density results in 1.84 and
1.81 g cm-3 for the right and left valves, respectively. Shell density
in Crassostrea species is independent of age and size (Lombardi et
al., 2013) and therefore the density estimates can be applied to the entire
data set.
Shell volume
The volume of nine individual shells was determined using close-range laser
scanning technology, which provides high-resolution models with sub-mm
resolution. The specimens were selected from the collections of the Natural
History Museum and vary in center length from 141 to 406 mm; four of these
shells represent left–right shell pairs of an individual (Fig. 4). The data
were captured with a measuring arm (METRIS MCA, 3600 M7). A hand-help
triangulation laser scanner (a laser plane and a camera) was mounted at the
end of two arms of fixed length with flexible joints. The laser scanner takes
measurements with a maximum scan rate of 80 stripes per second with a
strip-width of about 200 mm; the camera has a resolution of 1000 dots per
strip.
In the first step, more than half of each shell was scanned and in the second
step the other half. The overlap between both parts was more than 70 %,
which was sufficient for successful registration of the scanned parts. During
this registration process, the geometric transformation is determined, which
puts the two 3-D laser point clouds together based on the points in the
overlapping part. This procedure is done using the iterative closest point
(ICP) algorithm (Glira et al., 2015). The resulting point cloud is analyzed
in order to reduce noise and thus improve the surface description. Outliers
(wrongly determined points not on the surface) were manually eliminated.
Additionally, the raw point cloud (over 1.5 million points per shell) was
uniformly sub-sampled to allow interactive handling. The final resolution is
better than 0.18 mm (i.e., around 25 points per mm2). For volume
calculation the point cloud has to be transformed into a closed mesh.
Remaining holes, non-manifold surfaces and additional not connected
components were identified and removed. Finally, the surface area of the mesh
and its volume were computed using the algorithm of Mirtich (1996).
Based on the nine measured shells a relation between center line length and
volume can be deduced. The largest shell measured is 406 mm long but no
empirical volume data are available for larger shells, because these cannot
be removed from the site. Therefore, the von Bertalanffy equation would not
be applicable for shells larger than ∼ 40 cm. Consequently, we chose a
logistic function to approximate the inverse von Bertalanffy equation: ϑ=3.2439E061+118.86e-0.0099889SL,
where v is the volume in mm3 and SL the center line length in mm
(Fig. 8). Applying this equation to all shells results in a total volume of
393 273 cm3 with a mean shell volume of 350.8 cm3 (σ=313.7). These values do not change significantly if a non-linear Gompertz
growth model is assumed as frequently done for Crassostrea (Lopes et
al., 2013; Ginger et al., 2013). The respective equation ϑ=1.978E08e-9.1404e0.0013762χ results in a total volume of
398 474 cm3. Applying the above-discussed average shell gravity of
1.82 g cm-3 results in a total carbonate mass of ∼ 715 kg
(logistic) to ∼ 725 kg (Gompertz) for all 1121 shells. Thus, based on
the age models of the shells, the annual carbonate production per shell can
be calculated, which ranges from 74 (σ=2.9) (Gompertz)
to 83 g yr-1 (σ=2.8) (logistic), accounting for
∼ 150 g yr-1 per living oyster individual (i.e., two valves).
Logistic function showing the relation between center line length
and shell volume based on empirical measurements of nine shells (dots);
L = left shell, R = right shell; shell pairs are linked; numbers
correspond to specimens illustrated in Fig. 4.
Age–frequency data and box-plot of the shells based on center length
data transformed with the von Bertalanffy growth equation. Four cohorts are
detected by mixture analysis (a). Combined effect of natural
mortality and shell loss based on an exponential decay equation derived from
the amplitudes of detected cohorts (dashed lines represent 95 %
confidence intervals) (b).
Discussion
From lengths to cohorts
Based on the assumption that the size–frequency groups represent age classes
it is apparent to establish length-at-age relationships. Applying the von
Bertalanffy equation to the length data reveals a strongly right-skewed
distribution with 50 % of the shells ranging between 3 and 6 years
(Fig. 9a). The frequency of specimens between 6 and 9 years decreases rapidly
and the contribution by shells older than 9 years is subordinate although
outliers with up to 16 years occur. Again the non-normal distribution of the
von Bertalanffy growth model data suggests cohort mixing and the mixture
analysis assumes at least four significant cohorts with low AIC value. Due to
the rareness of large and aged shells, the fourth cohort displays a rather
low amplitude and we assume that at least two natural cohorts may be
amalgamated in this group. This suggests that more or less continuous recruitment
accentuated by very successful settlement peaks every 2 or 3 years.
Similarly, comparable patterns in extant Crassostrea reefs are
linked to fluctuating mortality rates and changing recruitment success
(Southworth et al., 2010). The data show that old and large shells are rare.
The reason for this may be a generally high mortality during the early years
of growth, resulting in low survival rates and few old specimens. The high
amount of fragments of large shells, however, suggests that a distinctly
higher proportion of large shells existed but became successively destroyed.
Comparison of von Bertalanffy growth model of Crassostrea gryphoides with selected fossil and extant Crassostrea species. 1:
C. titan (Conrad, 1853), Miocene, California, USA (Kirby, 2001); 2:
C. madrasensis (Preston, 1916), recent, Bangladesh (Nurul Amin et
al., 2008); 3: C. virginica (Gmelin, 1791), recent and Pleistocene
Virginia, USA (Kirby, 2001; Powell et al., 2011); 4: C. corteziensis
(Hertlein, 1951), recent, Mexico (Chávez-Villalba et al., 2005); 5:
C. gigas (Thunberg, 1793), recent, Marennes-Oleron, France (Berthome
et al., 1986).
Shell loss and mortality
The rapid decline of old shells is a combination of two processes. First,
natural mortality will result in a tail of large shells. Second, shells of
died-off Crassostrea are known to have surprisingly short half-lives
ranging from a few years to a few decades (Powell et al., 2006, 2015; Waldbusser
et al., 2011). Natural degradation processes, such as fragmentation,
dissolution and hydrodynamic export may account for 30 % loss of shells
per year (Southworth et al., 2010). The high amount of fragments with sharp
edges suggests that fragmentation is a major factor in our case. The
importance of hydrodynamic export cannot be evaluated due to the limited
outcrop area. Dissolution, however, is a minor factor as the well-preserved
shell-surfaces lack any signs of chemical degradation. Based on the declining
amplitudes of the cohorts the total shell loss can be computed as an exponential
decay function (Fig. 9b) revealing initial half-lives of less than 4 years.
The high proportion of fragmented, abraded and/or bioeroded oyster shells
(fragments: n=7047) would balance the “missing frequencies” easily. We
have no evidence for age-specific shell destruction and assume that all age
classes were equally affected by fragmentation.
Overall, under the environmental conditions as present in the Early Miocene
estuary, a died-off Crassostrea gryphoides reef would have been
fully degraded within 1 or 2 decades if not buried below the
taphonomically active zone (Olszewski, 2004). The high sedimentation rates in
the rapidly subsiding basin with rates (0.6 m kyr-1, Zuschin et al.,
2014), warranted a rapid burial of the reef, thus capturing the population
structure.
Crassostrea as carbonate factory?
The image-analysis-based estimation of chalky and foliate layers shows that
the values for chalky layers are slightly lower than reported for other
fast-growing Crassostrea species. The volume of chalky layers in
left shells of the extant Crassostrea “gryphoides”
(sensu Newton and Smith, 1912) is ∼ 70% (Durve and Bal, 1960). The
shells of the Miocene Crassostrea titan (Conrad, 1853) and
C. gravitesta (Yokoyama, 1926) were reported to comprise even up to
∼ 90 % of chalky deposits (Chinzei, 1995; Kirby, 2001) but this may
be a slight overestimation, neglecting the high amount of dense calcite in
the hinge areas. A re-evaluation of the illustrated specimen of C. gravitesta in Chinzei (1995) using our method reveals a somewhat lower but
still high value of 77 % chalky layer. The gravity of the fast-growing
C. titan, C. gravitesta and C. cahobasensis (Pilsbry and
Brown, 1917) was estimated to range around 1.35–1.40 g cm-3 (Chinzei,
1995; Kirby and Jackson, 2004). These values are very close to the empirical
data on the fast growing C. ariakensis (Fujita, 1913)
(1.44 ± 0.12 g cm-3) measured by Lombardi et al. (2013).
Slightly higher values are given for C. gigas
(1.63 ± 0.35 g cm-3, mean = 1.58) by Chinzei (1995).
Generally, species with low amounts of chalky layer have much higher
densities; e.g., C. virginica shells range around
2.18–2.35 g cm-3 (Kirby and Jackson, 2004; Lombardi et al., 2013).
Our gravity estimate of ∼ 1.82 g cm-3 for C. gryphoides
is thus somewhat higher than expected for such a growth type. In fact, large
parts of the shells are very light-weighed and fit well to the patterns
discussed by Chinzei (1995) and Kirby (2001). The main difference is the
large proportion of heavy shell material in the huge umbos and hinges.
A comparison of the growth curve of C. gryphoides with the von
Bertalanffy growth models of fossil and extant Crassostrea species
(Fig. 10) reveals this oyster to be an outstandingly fast growing species. Thus,
C. gryphoides was an important carbonate producer in Neogene
estuaries and lagoons where it lived as a secondary soft-bottom dweller in
dense colonies in a mixed mode of shell-supported reclining and mud sticking
(sensu Seilacher et al., 1985; Seilacher and Gishlick, 2014). Therefore,
dense populations with more than 100 individuals per m2 can be expected.
Even within the shell bed, which is clearly not in situ, the average density
is 129 shells (∼ 64 individuals) per m2 (including also moderately
fragmented shells). This would point to a hypothetic annual carbonate
production of up to 15 kg m-2 with the oyster reef. Although this
calculation is just a very rough estimate, it indicates that the carbonate
production is in the range of fast growing coral reefs with productions of
6–10 kg m-2 yr-1 (Montaggioni, 2005; Jones et al., 2015). A
major difference, however, is the rapid shell loss in Crassostrea
reefs, which prevents the formation of rigid and stable structures comparable
to coral reefs.
Conclusions
Crassostrea gryphoides was the fastest growing and largest
Crassostreinae species known so far. Despite the fact that this species
could attain outstanding individual ages of four decades (Harzhauser et al.,
2010), the bulk of specimens analyzed herein lived less than 10 years,
typically growing up to about 300 mm in length.
The non-normal distribution in the size, area and age–frequency data are best
explained by the presence of distinct recruitment cohorts, comparable to
modern oyster reefs. About four cohorts are detected by mixture analysis and
the rapidly decreasing amplitudes of frequency of these cohorts is
interpreted to reflect the combined effect of mortality, the declining life
expectancy with age, and the shell loss by biotic and physical factors. As no
accumulation of large and aged shells occurred, whilst the amount of
fragments is high, we assume that shell loss is an important factor to
explain the strongly right-skewed distribution. Shell half-lives ranged
around 2–4 years and within less than 2 decades the seemingly rigid and
persisting structure of a Crassostrea gryphoides reef could have
been completely degraded. This may explain the rareness of in situ C. gryphoides reefs in the fossil record although the shells are frequent and
ubiquitous.
The significant growth rate is clearly boosted by the formation of up to 64 % percentage of fast-growing and lightweight chalky material. The
subtropical climate with warm winter temperatures above ca. 10 ∘C and
the nutrient-rich setting in an estuary will additionally have supported the
excessive growth.
Due to its fast growth and large shells, the carbonate production of
C. gryphoides is outstanding. Dense colonies might have produced
around 15 kg m-2 yr-1 of carbonate, which is within the range of
fast growing coral reefs. Therefore, this oyster may have been a major
carbonate producer in the circum-Tethyan area throughout the Miocene. In
contrast to coral reefs, however, the high shell loss rates did not allow stable persistent structures to
form.
Information about the Supplement
Supplement Table: Center line length and area data for 1121 complete
shells of Crassostrea gryphoides. Age, volume and carbonate mass data are derived from the
equations discussed in the text.