FRFossil RecordFRFoss. Rec.2193-0074Copernicus PublicationsGöttingen, Germany10.5194/fr-21-1-2018Large dendrinids meet giant clam: the bioerosion trace fossil Neodendrina carnelia igen. et isp. n. in a Tridacna shell from Pleistocene–Holocene coral reef deposits, Red Sea, EgyptWisshakMaxmax.wisshak@senckenberg.dehttps://orcid.org/0000-0001-7531-3317NeumannChristianhttps://orcid.org/0000-0001-9630-9624Senckenberg am Meer, Marine Research Department, 26382 Wilhelmshaven,
GermanyMuseum für Naturkunde, Leibniz Institute for Evolution and
Biodiversity Science, 10115 Berlin, GermanyMax Wisshak (max.wisshak@senckenberg.de)10January20182111931July201723November201724November2017This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/This article is available from https://fr.copernicus.org/articles/21/1/2018/fr-21-1-2018.htmlThe full text article is available as a PDF file from https://fr.copernicus.org/articles/21/1/2018/fr-21-1-2018.pdf
The
rosette-shaped microboring trace fossil Neodendrina carnelia igen. et isp. n. – a large representative of the ichnofamily Dendrinidae – is
identified on the inner side of the giant clam Tridacna maxima from
Pleistocene to Holocene coral reef deposits of the El Quseir district at the
Egyptian Red Sea coast. The new dendritic bioerosion trace fossil is
diagnosed as a radial rosette comprised of a prostrate system of roofless
canals that ramify in a strictly dichotomous fashion forming intermittent
branches of uniform width and rounded terminations. The trace appears to be
rare, although in the type material it occurs in a cluster of more than a
hundred specimens. The location of traces on the interior surface of the
shell suggests that boring occurred post-mortem to the host. Its
record is presently restricted to shallow marine, euphotic, tropical coral
reef settings in the Western Indo-Pacific (Red Sea and Madagascar). The
biological identity of the trace maker cannot be resolved yet, but several
lines of reasoning allow speculations directed towards a complex attachment
scar, perhaps produced by a benthic foraminiferan or a macrophyte.
Introduction
The Dendrinidae are a diverse ichnofamily of dendritic and rosette-shaped
marine microboring trace fossils (Bromley et al., 2007) whose unknown trace
makers appear to have flourished particularly during the Devonian and the
Late Cretaceous (Wisshak, 2017). While they had been considered largely
extinct since the end-Cretaceous mass extinction event, a recent revision of
the group revealed that several members of the group still occur in modern
oceans, preferentially in temperate to polar waters (Wisshak, 2017).
In this study, we describe a new conspicuous dendrinid from a tropic coral
reef setting from the Pleistocene–Holocene of the north-eastern Red Sea
coast, El Quseir district, Egypt. In a single valve of the giant clam
Tridacna maxima (Röding, 1798), a large pelecypod common in
these settings, hundreds of specimens of this bioerosion trace fossil have
been recognized. Their unique habitus and branching pattern merits
establishment of a new ichnogenus, addressed as Neodendrina, in
reference to the type ichnogenus Dendrina Quenstedt, 1849 from the
Upper Cretaceous, which on first sight exhibits a remarkable similarity but
after closer examination reveals a quite distinct architecture.
The Pleistocene raised coral reef limestones exposed at the
type locality of Neodendrina carnelia igen. et isp. n. just south of the Carnelia Beach Resort,
located between El Quseir and Marsa Alam, exhibiting scleractinian corals as
primary reef builders (a) and giant clams Tridacna spp. weathering from the
carbonate–siliciclastic rocks (b) that mix with Holocene and
modern Tridacna valves, forming a highly time-averaged assemblage (c).
Geological context
Pleistocene raised coral reefs are a common feature along the Red Sea coast
of Egypt, forming terraces at different elevations above the present-day sea
level. Between El Quseir and Marsa Alam, three reefal units forming six
morphological terraces can be recognized (El-Sorogy, 1997). The reefs form
discontinuous strips which run parallel to the shore line, separated by
conglomerates, quartz sands and gravels. At the study area, the lithology of
the lowermost terrace represents a transition of mixed
carbonate–siliciclastic rocks with scleractinians as primary frame builders
(Fig. 1a). These Pleistocene reefal limestones are usually referred to as
the Samadai Formation (Philobbos et al., 1989) and are conformably overlain
by Pleistocene raised beaches and coral reefs (Kora et al., 2013, 2014).
Their age and diagenesis have been discussed by several workers during the last
decades (see Dullo, 1990; El Sorogy, 2002, for further references) and have
been a classical study area for palaeontological studies (see Kora et al.,
2014).
Among other fossils (Fig. 1a), the rocks contain numerous large molluscs with giant
clams (Tridacna spp.) and conchs (Lambis and Strombus spp.) being the most conspicuous. As the
poorly lithified sediments erode, exposed Tridacna valves accumulate in large
numbers on the surface (Fig. 1b). Here, they mix with subfossil (Holocene)
and modern Tridacna valves, forming a highly time-averaged assemblage (Fig. 1c).
This process was (and still is) promoted by active fishery of giant clams
by the native Bedouin population and their ancestors over the
course of the last > 125 000 years, producing huge piles of
discarded Tridacna shells along Red Sea beaches (e.g. Ashworth et al., 2004;
Benzoni et al., 2006; Richter et al., 2008).
Material and methods
One Tridacna maxima valve bearing the new bioerosional traces was sampled at a beach
deposit of the Red Sea, Egypt, 25 km south of El Quseir, between Ras Abu
Aweid and Mersa Um Gheig. Further, a query in the malacological collection
of the Museum für Naturkunde Berlin resulted in the recognition of one
additional Tridacnasquamosa valve from northern Madagascar bearing similar traces.
The two bivalve shells bearing the studied bioerosion traces were digitally
photographed with Nikon and Canon DSLRs, partly after coating with ammonium
chloride, and partly applying a Cognysis StackShot Macro Rail for extended
focal imaging with the software Helicon Focus Pro. Scanning electron
micrographs of the traces were produced with a Tescan VEGA3 XMU applying a
backscatter electron detector (BSE) after sputter coating with gold, except
for the holotype that was left untreated and was imaged in a low-vacuum
setting. In addition, a micro-CT scan of the holotype trace was performed
with a GE Phoenix nanotome X-ray tube at 90 kV and 150 µA,
generating 2500 projections with 750 ms per scan and effective voxel size of
4.6 µm. The cone beam reconstruction was performed using the GE
datos|x 2 reconstruction software and the data were visualized in
Volume Graphics Studio Max 3.0. For better spatial resolution of the CT
scans, the bivalve shell had to be cut into smaller blocks, some of the other
ones of which were used for vacuum cast embedding followed by dissolution of
the host substrate with hydrochloric acid (for details, see Wisshak, 2012),
yielding epoxy cast with the positive infills of the traces that were then
visualized with SEM after sputter coating with gold.
Morphometrical measurements were carried out using the measurements tool in
the VEGA SEM software, recording the maximum diameter of the trace, the
width of the individual galleries (up to five measurements per trace), the
branching angle of the dichotomous bifurcations (up to five measurements per
trace), the maximum number of subsequent bifurcations from the centre to the
periphery of the trace, and the number of peripheral gallery terminations.
This published work and the nomenclatural acts it contains were
registered in ZooBank on 5 October 2017 and have received the LSID number
EBD565C7-5042-47A9-8F1A-771ABBDCD1C0:
http://zoobank.org/references/EBD565C7-5042-47A9-8F1A-771ABBDCD1C0.
Systematic ichnology
Dendrinidae Bromley, Wisshak, Glaub & Botquelen, 2007Neodendrina igen. n.
Type ichnospecies: Neodendrinacarnelia isp. n.Etymology: Latinized from ancient Greek
(neos) and (dendron), referring to the parent
ichnofamily Dendrinidae and its type ichnogenus Dendrina, and making reference to
the fact that microborings of the new ichnogenus are among the few
dendrinids to also occur in modern seas.Diagnosis: Dendritic bioerosion trace in calcareous skeletal substrates,
forming a prostrate system of roofless canals that bifurcate dichotomously.Remarks: The dichotomous bifurcation pattern of Neodendrina igen. n. closely resembles
that of the ichnogenus Abeliella Mägdefrau, 1937, which is, however, found in a
different principal substrate type, namely fossil bone and teeth. Such
osteic substrates are considered as a principal substrate type for
bioerosion trace fossils at equal rank with xylic and lithic substrates,
thus justifying establishment of a separate ichnogenus (Höpner and
Bertling, 2017). The dichotomous nature of bifurcations shows some
similarity to Fascichnus bellafurcus (Radtke et al., 2010), originally established as Abeliella bellafurca by the
latter authors and transferred to Fascichnus by Wisshak (2017), which is much
smaller and shows a three-dimensional architecture. Another ichnogenus with
some similarity is Rhopalondendrina Wisshak, 2017, which differs by the presence of
a straight to arcuate entrance tunnel and the development of only a semi-circular
plexus of ramifying or anastomosing galleries. Neodendrina igen. n. differs from
the related ichnogenus Dendrina Quenstedt, 1849 by the lack of a tubular inlet
tunnel, and by the more regular bifurcation pattern of galleries that are
more constant in width. Apart from these distinctions, the main
morphological character that distinguishes Neodendrina igen. n. from Dendrina and most of the
other dendrinids is the roofless nature of the open galleries.
Neodendrinacarnelia isp. n.Figs. 2–4
Etymology: From Latin carnelia, meaning carnelian, red-coloured variety of chalcedony.
Referring to “Diving Carnelia”, a former scuba dive centre situated in the
direct vicinity of the type locality, and secondarily referring also to the
Red Sea.Diagnosis: Radial rosette nearly circular in outline, ramifying in a
strictly dichotomous fashion. Roofless canals with slight swellings but
relatively constant in width; terminations rounded. Particularly near the
centre of the trace, canals may be very shallow or discontinuous and then
appear as a series of pits.Description: The prostrate circular to oval rosette of the dendrinid
microboring is radiating from its centre in a strictly dichotomous pattern,
forming open canals of relatively constant width (within a trace and among
traces) and featuring rounded terminations (e.g. Figs. 2c–e, 3a–c). From the
roughly orthogonal individual points of bifurcation, the canals make a
slight turn in direction of the radial expansion of the trace, resulting in
an acute angle between two neighbouring branches (Fig. 3a–d). Particularly
in the centre of the trace, the canals may be either very shallow (at same
width than the deeper ones) or even discontinuous, i.e. no bioerosion
having taken place at these points (e.g. Figs. 2c–e, 3h, i, j). In the latter
case, the trace appears as an array of short grooves or pits, whereas
confined and shallow pits may also be found situated within the shallow
canals (Fig. 3h). The presence and degree of these different morphological
expressions varies markedly between different specimens, the by far most
common morphology being the deep and continuous canals. The surface texture
is smooth (Fig. 3e and k). The substrate surface in the direct vicinity of the
canals may either be a bit different in colour (Fig. 2b) or morphologically
slightly elevated (Fig. 4c). Several traces on the Tridacna shell that bears the
holotype contain authigenic gypsum crystals, calcite spar, and clay minerals
within the boring as well as on the surrounding shell surface (Fig. 3f–g).
Neodendrina carnelia igen. et isp. n. on the inner side of a Tridacnamaxima bivalve shell
from the Pleistocene–Holocene coral reef deposits in the Marsa Alam area,
Red Sea, Egypt. (a) Inner side of valve (left; prior to sectioning)
with hundreds of N. carnelia specimens, and outer surface (right) intensely bioeroded
by the sponge boring Entobia isp. (b) Section of the valve (MB.W 5640)
with the holotype (centre) and the paratypes (all other specimens) in
various ichnogenetic stages. (c) Close-up of the holotype trace.
(d–e) Respective micro-CT scan of the holotype in plan and angular
views as seen from inside the substrate.
SEM images (BSE detector) of Neodendrina carnelia igen. et isp. n. of the inner
side of a Tridacnamaxima bivalve shell from the Pleistocene–Holocene coral reef deposits
in the Marsa Alam area, Red Sea, Egypt. (a–c) Overview and
close-ups of the holotype. (d–e) Overview and close-up of an early
ichnogenetic stage. (f–g) Overview and close-up of a specimen with
authigenic gypsum crystals, calcite spar, and clay minerals within the
boring as well as on the host's shell surface. (h) Different
morphologies possibly developed in the trace, comprising deep open canals
(1), isolated deep pits (2), shallow open canals (3), pits in shallow canals
(4) and discontinuities (5). (i) Cross section of a trace showing
deep (1) and shallow (2) open canals. (j–k) Overview and detail of
an epoxy resin cast of a specimen, illustrating the smooth surface texture
and the high degree of microbioerosion in the surrounding (partly
mechanically removed to gain a view of the dendrinid).
Neodendrina carnelia igen. et isp. n. on the outer surface of a large recent
Tridacna squamosa valve from Nosy-Bé, northern Madagascar (ZMB/Mol 102671). (a) Shell
surface with various encrusters as well as bioerosion traces. (b) Close-up of a cluster of N. carnelia. (c) A large specimen with distinct
pitted arrays developed in most of the branches.
Morphometrical measurements obtained from 55 complete specimens on a single
Tridacna host shell, including the holotype and comprising a range of initial traces
to late ichnogenetic stages, show a maximum diameter of the rosette-shaped
trace ranging from 1025 to 3770 µm, with a mean of
1931 ± 651 µm (n=55), and individual galleries of relatively constant width
ranging from 59 to 153 µm, with a mean of 100 ± 16 µm (n=275). The angle of the dichotomous bifurcations ranges from 43 to
141∘ with a mean of 90 ± 15∘ (n=246) at the
branching points. One to six orders of bifurcations were observed (mean =
3 ± 1; n=55), leading to a number of peripheral gallery
terminations ranging from 4 to 43 (mean = 13 ± 7; n=55).Type material, locality and horizon: The holotype (Figs. 2b–e, 3a–c) is
preserved on a piece cut from a Tridacnamaxima (Röding, 1798)
shell, and is housed at the Museum für Naturkunde Berlin, Germany (MB.W
5640). All other specimens preserved on the same slab are defined as
paratypes (Fig. 2b). The type locality is 25 km south of El Quseir, between
Ras Abu Aweid and Mersa Um Gheig, just south of the former Carnelia Beach
Resort (25∘54′13′′ N, 34∘24′45′′ E). The type shell bed
is highly time averaged, and hence the exact age remains unresolved, either from the
reefal limestones of the Samadai Formation, Pleistocene, or from a late
Pleistocene to early Holocene archaeological shell midden, or (least likely)
from the recent reef top.Additional material: More than a hundred microboring specimens remained
preserved on the inner shell surface of the same Tridacnamaxima bivalve shell that bears
the holotype (Fig. 2a). In addition, a number of specimens were identified
on the outer surface of a large recent Tridacna squamosa de Lamarck, 1819 valve (Fig. 4) stored
at the Museum für Naturkunde Berlin, Germany (ZMB/Mol 102671),
originating from Nosy-Bé, northern Madagascar.Remarks: Spot checks of morphometrical measurements taken from the
additional Madagascar material plot in the range of the specimens from the
type material.
Further observations and discussion
The T. maxima shell that harbours the type material was bioeroded by different types
of bioeroders, both syn-vivo and post-mortem. All of the many N. carnelia igen. et isp. n. are
located on the inner surface of the host valve (Fig. 2a left), thus
indicating a post-mortem development (syn-vivo parasitism is very unlikely, considering their
occurrence also on the outside of the Madagascar specimen). The outer
surface, in contrast, was heavily infested by a bioeroding sponge that
produced Entobia isp. but did not form connections to the inner surface of the
valve (compare Fig. 2a left and right), thus indicating syn-vivo bioerosion. The
latter case probably also applies to some specimens of the bivalve
macroboring Gastrochaenolites isp. (e.g. Fig. 2a lower left) that enter the valve from the
outer surface. All other bioerosion traces developed post-mortem on the inner side of
the valve, as there are numerous traces of deep endolithic as well as
surficial attached foraminiferans (see e.g. Fig. 2b), or the endolithic
rhizoidal attachments Fascichnus grandis (Radtke, 1991) of the chlorophyte alga genus
Acetabularia (Radtke et al., 1997). The entire surface of the valve was densely
bioeroded by chlorophyte and cyanobacterial microendoliths (see e.g. Fig. 3c, e, g, j–k),
taking place both syn-vivo (outer surface) and post-mortem (both surfaces). The
overall trace fossil assemblage can be regarded as typical for
shallow-marine tropical reef settings.
The exact stratigraphic age of the type material cannot be pinned down with
certainty (see above) but is either Pleistocene or Holocene. The trace
definitively occurs also in modern seas, as indicated by the material from
Madagascar. Neodendrina carnelia igen. et isp. n. is a new member of the growing circle of known
extant dendrinids, which, according to the revision of the Dendrinidae by
Wisshak (2017), already includes six ichnospecies. The biogeographic
distribution at present is restricted to the tropical Western Indo-Pacific,
represented by the two known records from the Red Sea and Madagascar. With
respect to the (palaeo-)environmental setting, both records are from a
shallow-marine, euphotic, tropical coral reef.
The biological identity of the trace makers of all dendrinid microborings,
including the herein described N. carnelia igen. et isp. n., remains largely enigmatic.
Published interpretations in this respect are diverse, but the most likely
candidates are endolithic naked foraminiferans and micro-sponges, possibly
also hydroids and, in the case of the smallest forms, endolithic fungi or
microphytes (for a review, see Wisshak, 2017). As for N. carnelia igen. et isp. n., the presence of an epilithic part of the trace maker can be deduced from
the partly discontinuous open canals (e.g. Fig. 2b–d), and from the
observation that some of the traces appear to show somewhat of a “shadow”
surrounding the trace, expressed by a slightly darker colour of the shell
surface in the case of the holotype and neighbouring paratypes (Fig. 2b–c). This
phenomenon can best be explained by a lower degree of microbioerosion at the
place where the dendrinid trace maker was covering the substrate. This line
of reasoning is also supported by the presence of a slightly elevated
plateau surrounding the largest of the specimens on the Madagascar
Tridacna (see Fig. 4c). Furthermore, none
of the numerous studied specimens showed any signs of a partially
preserved or abraded roof, and a very homogenous abrasion that
could have resulted in an un-roofing of all of the numerous observed traces
on the concave inner side of the host shell is extremely unlikely. Hence, the
morphological feature of open canals is here regarded as the original and
intact morphology of the new dendrinid. Therefore, the fact that the canals
become very shallow (at constant width), or in places even discontinuous
(e.g. Fig. 3h), rather suggests continuity of the trace maker's soft body
with an alternation of epilithic and partly endolithic mode of progression.
With respect to indicative morphological characters that could help
identifying the trace maker, N. carnelia igen. et isp. n. has admittedly little to
offer. The absence of anastomoses and particularly the strictly dichotomous
bifurcation pattern are highly convergent characters that are developed in
algae, fungi, cyanobacteria, and other potential trace makers (see
discussion in Radtke et al., 2010). This suite of euendolithic
microborers can, however, most likely be excluded on grounds of the
comparatively large size of the dendrinid in question. Together with the
above proposed epilithic component, this raises the question of whether N. carnelia igen. et isp. n. could reflect a complex attachment scar of a larger trace maker
rather than the work of an euendolithic microborer. Matching epiliths could
perhaps be expected either among the benthic foraminiferans or in the form of
either a rhizoidal structure or etching of a hapteron of a macrophyte (for a
review, see Bromley and Heinberg, 2006). As for benthic foraminiferans,
many species are known to produce attachment scars or endolithic
microborings (for a recent review, see Walker et al., 2017), and at least
one modern dendrinid microboring was interpreted as
the work of a foraminiferan. This is Nododendrina europaea (Fischer, 1875), formerly Semidendrina pulchra Bromley et al., 2007 (for the revision, see Wisshak, 2017), which presumably is
produced by the foraminiferan Globodendrina monile Plewes et al., 1993. As for macrophytes,
various representatives of the large unicellular green algae of the genus
Acetabularia form rhizoidal bioerosion traces (Radtke et al., 1997) that are addressed
as Fascichnus grandis (Radtke, 1991). As outlined above, these traces also co-occur with N. carnelia
igen. et isp. n. on the very same Tridacna shell, and just like the new dendrinid,
these traces do bifurcate and have a smooth surface texture, but they are
much larger than morphologically similar cyanobacterial microborings. Unlike
N. carnelia igen. et isp. n. they are rather deeply penetrating, but this fact alone
does not justify ruling out the possibility that N. carnelia igen. et isp. n. might be
the work of a large chlorophyte alga within or similar to the genus
Acetabularia. Among the rhodophytes, many of the phaeophycean kelp and seaweeds attach
themselves to hard substrates by means of a holdfast or gripping hapteron.
According to Oliveira et al. (1989) the rhizoid's adhesive material is
composed of a glycoprotein or an acid–polysaccharide/protein complex. Some
representatives have been suspected or reported to etch carbonate substrates
(e.g. Emery, 1963; Barnes and Topinka, 1969; Warme, 1975; Radwanski, 1977),
but a detailed ichnological investigation and ichnotaxonomical treatment of
these attachment etchings is pending. In general, both chlorophytes and rhodophytes may exhibit a dichotomous branching pattern of their
endolithic or epilithic thalli (e.g. Sitte et al., 2002).
Last but not least, clues for the trace maker identity could be derived from
the observed abundance patterns of N. carnelia igen. et isp. n., which appears to be
fairly rare. This is suggested by the fact that this conspicuous and large
dendrinid has not been previously recognized, and considering that visual
inspection of hundreds, if not thousands, of further Tridacna valves at the type
locality did not yield a single additional record. In contrast, where it
occurs, it appears clustered in a remarkably high number of specimens on a
single host shell, as indicated by the T. maxima that bears the holotype in a
cluster together with hundreds of other specimens. Such clustering would be
in line with both a foraminiferan and a macrophyte trace maker, and is also
typical for several other dendrinid ichnotaxa, such as the aforementioned
S. pulchra or ichnospecies of the Cretaceous ichnogenus Dendrina. However, despite the
number of the above observations, the favoured options in respect to the
trace maker's biological identity remain highly speculative until evidence
from body fossils or organic remains in extant specimens of N. carnelia igen. et isp. n. can be identified.
The samples are reposited in museum collections (as specified in
the Systematic Ichnology section), and all necessary data can be found in the text.
Christian Neumann and editor Florian Witzmann work at the same
institution but do not collaborate scientifically, and the paper was accepted
on the basis of reviews from two outside reviewers. The authors declare no
other competing interests.
Acknowledgements
We gratefully acknowledge Kristin Mahlow (Museum für Naturkunde Berlin,
Germany) for taking care of the micro-CT scan, and Christine Zorn (Museum
für Naturkunde Berlin, Germany), who provided access to the malacological
collection and the Madagascar Tridacna specimen. Lydia Beuck (Senckenberg am Meer,
Wilhelmshaven, Germany) is thanked for fruitful discussion on the trace
maker identity, and Axel Munnecke (GeoZentrum Nordbayern, Erlangen, Germany)
for discussions on diagenetic phenomena. Funding for fieldwork was kindly
provided to M. Wisshak by André Freiwald (Senckenberg am Meer, Wilhelmshaven,
Germany). We are grateful to the reviewers Dirk Knaust (Statoil, Norway) and
Stjepko Golubic (Boston University, USA) for providing thorough and critical
reviews that helped improving the present contribution.
Edited by: Florian Witzmann
Reviewed by: Dirk Knaust and Stjepko Golubic
References
Ashworth, J. S., Ormond, R. F., and Sturrock, H. T.: Effects of reef-top
gathering and fishing on invertebrate abundance across take and no-take
zones, J. Exp. Mar. Biol. Ecol., 303, 221–242, 2004.
Barnes, H. and Topinka, J. A.: Effect of the nature of the substratum on the
force required to detach a common littoral alga, Am. Zool., 9, 753–758,
1969.
Benzoni, F., Ashworth, J. S., Addamo, A. M., Stefani, F., Mabrouk, A., and
Galli, P.: Artisanal fisheries and no-take zones in Nabq, Egypt: Effects on
molluscs and reef top benthic assemblages, in: Proceedings of the 10th
International Coral Reefs Symposium, Okinawa, Japan, 1362–1367, 2006.
Bromley R. G. and Heinberg C.: Attachment strategies of organisms on hard
substrates: A palaeontological view, Palaeogeogr. Palaeoclimatol.
Palaeoecol., 232, 429–453, 2006.Bromley R. G., Wisshak M., Glaub I., and Botquelen, A.: Ichnotaxonomic
review of dendriniform borings attributed to foraminiferans: Semidendrina igen. nov.,
in: Trace fossils: concepts, problems, prospects, edited by: Miller III, W.,
Elsevier, Amsterdam, 518–530, 2007.de Lamarck, J.-B. M.: Histoire naturelle des animaux sans vertèbres.
Tome sixième, 1re partie, published by the Author, Paris, vi + 343
pp., 1819.
Dullo, W. C.: Facies, fossil record, and age of Pleistocene reefs from the
Red Sea (Saudi Arabia), Facies, 22, 1–45, 1990.
El-Sorogy, A. S.: Progressive diagenetic sequence of Pleistocene coral reefs
in the area between Quseir and Mersa Alam, Red Sea coast, Egypt, Egypt J.
Geol., 41, 519–540, 1997.
El-Sorogy, A. S.: Paleontology and depositional environments of the
Pleistocene coral reefs of the Gulf of Suez, Egypt, N. Jahrb. Geol.
Paläont. Abh., 225, 337–371, 2002.
Emery, K. O.: Organic transportation of marine sediments, in: The sea,
edited by: Hill, M. N., Wiley, New York, 776–793, 1963.
Fischer, M. P.: D`un type de sarcodaires, J. Zool., 4,
530–533, 1875.
Höpner S. and Bertling M.: Holes in bones: ichnotaxonomy of bone
borings, Ichnos, 24, 259–282, 2017.
Kora, M., Salah, A., and Heba, E. D.: Microfacies and environmental
interpretation of the Pliocene-Pleistocene carbonates in the Marsa Alam
area, Red Sea coastal plain, Egypt, J. Environ. Sci., 42, 155–182, 2013.
Kora, M. A., Ayyad, S. N., and El-Desouky, H. M.: Pleistocene scleractinian
corals from Marsa Alam area, Red Sea Coast, Egypt: systematics and
biogeography, Swiss J. Palaeont., 133, 77–97, 2014.
Mägdefrau, K.: Lebensspuren fossiler “Bohr”-Organismen, Beiträge
zur naturkundlichen Forschung in Südwestdeutschland, 2, 54–67, 1937.Oliveira, L., Walker, D. C., and Bisalputra, T.: Ultrastructural,
cytochemical, and enzymatic studies on the adhesive “plaques” of the brown
algae Laminaria saccharina (L.) lamour. and Nereocystis luetkeana (nert.) post. et rupr. 1, Protoplasma, 104, 1–15,
1980.
Philobbos, E. R., El-Haddad, A. A., and Mahran, T. M.: Sedimentology of
syn-rift Upper Miocene (?)-Pliocene sediments of the Red Sea area: A model
from the environs of Marsa Alam, Egypt, Egypt. J. Geol., 33, 201–227, 1989.
Plewes, C. R., Palmer, T., and Haynes, J.: A boring foraminiferan from the
Upper Jurassic of England and Northern France, J. Micropalaeontol., 12,
83–89, 1993.
Quenstedt, F. A.: Petrefaktenkunde Deutschlands - Die Cephalopoden, Fues,
Tübingen, [text volume & atlas], 1849.
Radtke, G.: Die mikroendolithischen Spurenfossilien im Alt-Tertiär
West-Europas und ihre palökologische Bedeutung, Courier
Forschungsinstitut Senckenberg, 138, 1–185, 1991.Radtke, G., Gektidis, M., Golubic, S., Hofmann, K., Kiene, W. E., and Le
Campion-Alsumard, T.: The identity of an endolithic alga: Ostreobium brabantium Weber-van Bosse
is recognized as carbonate penetrating rhizoids of Acetabularia (Chlorophyta,
Dasycladales), Courier Forschungsinstitut Senckenberg, 201, 341–347, 1997.Radtke, G., Glaub, I., Vogel, K., and Golubic, S.: A new dichotomous
microboring: Abeliella bellafurca isp. nov., distribution, variability and biological origin,
Ichnos, 17, 25–33, 2010.
Radwański, A.: Present-day types of traces in the Neogene sequence;
their problems of nomenclature and preservation, in: Trace fossils 2, edited
by: Crimes, T, P. and Harper, J. C., Seel House Press, London, 227–164,
1977.
Richter, C., Roa-Quiaoit, H., Jantzen, C., Al-Zibdah, M., and Kochzius, M.:
Collapse of a new living species of giant clam in the Red Sea, Curr. Biol.,
18, 1349–1354, 2008.
Röding, P. F.: Museum Boltenianum sive catalogus cimeliorum e tribus
regnis naturæ quæ olim collegerat Joa. Fried Bolten, M. D. p. d. per
XL. annos proto physicus Hamburgensis. Pars secunda continens conchylia sive
testacea univalvia, bivalvia & multivalvia, Trapp, Hamburg, 199 pp.,
1798.
Sitte, P., Weiler, E., Kadereit, J. W., Bresinsky, A., and Körner, C.:
Lehrbuch der Botanik für Hochschulen. Begründet von E. Strasburger,
35th edition, Spektrum, Heidelberg, 1123 pp., 2002.Walker, S. E., Hancock, L. G., and Bowser, S. S.: Diversity, biogeography,
body size and fossil record of parasitic and suspected parasitic
foraminifera: a review, J. Foraminiferal Res., 47, 34–55, 2017.
Warme, J. E.: Borings as trace fossils, and the process of marine
bioerosion, in: The study of trace fossils, edited by: Frey, R. W., Springer,
New York, 181–227, 1975.
Wisshak, M.: Microbioerosion, in: Trace fossils as indicators of sedimentary
environments, edited by: Knaust, D. and Bromley, R. G., Elsevier, Amsterdam,
213–243, 2012.
Wisshak, M.: Taming an ichnotaxonomical Pandora's box: Revision of dendritic
and rosetted microborings (ichnofamily: Dendrinidae), European Journal of
Taxonomy, 390, 1–99, 2017.