A new taphonomic bioerosion in a Miocene lakeshore environment
M. Dolores Pesquero
a,b,
⁎, Carmen Ascaso
c
, Luis Alcalá
a
, Yolanda Fernández-Jalvo
b
a
Fundación Conjunto Paleontológico de Teruel-Dinópolis, Avda. Sagunto s/n, 44002 Teruel, Spain
b
Museo Nacional de Ciencias Naturales (CSIC), C/José Gutiérrez Abascal 2, 28006 Madrid, Spain
c
Instituto de Recursos Naturales, Centro de Ciencias Medioambientales (CSIC), C/Serrano 115-bis, 28006 Madrid Spain
abstract article info
Article history:
Received 14 October 2009
Received in revised form 7 May 2010
Accepted 28 May 2010
Available online 9 June 2010
Keywords:
Miocene
Microboring
Bacteria
Aquatic ecosystems
Concud
Teruel
Spain
This study describes a new type of taphonomic alteration of fossil bone that occurred in a continental carbonate
palaeolake environment at the reference Spanish Miocene site of Cerro de la Garita (Concud, Teruel). Scanning
electron microscopy showed this type of alteration to be characterized by microtunnels that penetrate inward
from the bone surface and by a branching-meandering arrangement of microchannels on the bone surface.
These microtunnels had a highly electron dense inner wall, seen as a characteristic rim in transverse section.
Microspheres were seen inside the microtunnels. Both this electron dense layer and these microspheres were
found to be composed of calcium phosphate. These taphonomic modifications bear some similarities to, but
also differs from, those caused by bacterial attack on bone and enamel in marine and terrestrial environments,
suggesting the present process to be a new type of bioerosion. The microspheres inside the microtunnels were
similar in size, shape and composition to the fossilized bacteria covering fossils from Fossil-Lagersttäten
palaeolake sites, such as Libros (Teruel, Spain) and Messel (Germany). Under the transmission electron
microscope these structures showed an apparent cell wall, suggesting them to be fossilized coccoid bacteria.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
1.1. Microboring and activity of microorganisms
Wedl (1864) was the first to describe microboring affecting the
bone structure, a phenomenon he attributed to fungal attack. Hackett
(1981) distinguished four types of microscopic focal destruction
(MFD) of such bone which he divided into three non-Wedl-types
(linear longitudinal, lamellate and budded foci) and one Wedl-type.
Hackett (1981) attributed the first three types to bacterial activity and
described the areas so attacked to be surrounded by zones of
remineralization. Hedges et al. (1995) proposed an index of histolog-
ical destruction (the Oxford Histology Index, OHI) for describing the
overall extent to which the histological integrity of post-mortem bone
attacked in this way is lost, from stage 0 (with no original histological
features identifiable other than Haversian canals) to stage 5 (with less
than 5% of bone affected by bacterial attack). The distribution of
modifications affecting the bone matrix made by indigenous bacteria
during decay is conditioned by the histological microstructure of the
bone in question (Bell, 1990; Jans et al., 2002, 2004; Turner-Walker
and Jans, 2008). However, the marks left by bacteria in non-Wedl
alteration may appear dispersed, independent of the vascular or cell
network; such bacterial activity is post-depositional or post-skeleto-
nization (i.e., appearing after the soft tissues have disappeared) (Bell
and Elkerton, 2008; Fernández-Jalvo et al., 2010).
The most commonly observed type of non-Wedl microbial bone
deterioration in terrestrial environments involves discrete zones that
in backscattered scanning electron microscopy (BSE-SEM) are seen to
contain small pores and thin channels 0.1–1.0 μm in diameter
(Hackett, 1981; Bell, 1990; Bell et al., 1991, 1996; Turner-Walker et
al., 2002; Jans, 2005). These zones are often surrounded by an electron
dense region marking the limit of the affected area. Jackes (1990)
hypothesized that this was due to coccoid bacteria removing collagen
from the solubilized compactum and then reprecipitating bone
mineral in a more dense form. Using the scanning electron microscope
(SEM), Jackes et al. (2001) showed a rim surrounding the destructive
foci to be much more electron dense than unaltered bone. These
authors indicated these rims to contain more mineral (a higher
percentage of Ca + P) and less organic matter (collagen) than the
surrounding unaltered bone.
The remaining type of microscopic focal destruction in post-mortem
bones (i.e., Wedl microscopic focal destruction) involves microboring
similar to that seen by Wedl (1864). Roux (1887) agreed with Wedl that
this bioerosion was the product of fungal activity and assigned such
microborings to the ichnogenus Mycelites ossifragus. Arnaud et al.
(1978) sectioned medieval human bones from a shipwreck and
observed microboring similar to this Wedl type alteration. However,
these authors were unable to find any microorganism inside the
microtunnels that might have given rise to them. Ascenzi and Silvestrini
(1984) extended the study to experimental work and analysed both
medieval and modern human bones collected from sea water using the
Palaeogeography, Palaeoclimatology, Palaeoecology 295 (2010) 192–198
⁎ Corresponding author. Fundación Conjunto Paleontológico de Teruel-Dinópolis,
Avda. Sagunto s/n, 44002 Teruel, Spain. Fax: +34 978 617 638.
E-mail address: pesquero@fundaciondinopolis.org (M.D. Pesquero).
0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2010.05.037
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