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Criteria for identifying bone modification by termites in the fossil record
Lucinda R. Backwell
a,
⁎, Alexander H. Parkinson
a
, Eric M. Roberts
b
,
Francesco d'Errico
c,d
, Jean-Bernard Huchet
e,f
a
Bernard Price Institute for Palaeontological Research, School of Geosciences, and Institute for Human Evolution, University of the Witwatersrand, Private Bag 3, WITS 2050, Johannesburg,
South Africa
b
School of Earth and Environmental Science, James Cook University, Townsville, Qld 4811, Australia
c
CNRS UMR 5199 PACEA, Université Bordeaux 1, Avenue des Facultés, F-33405 Talence, France
d
Department of Archaeology, History, Cultural Studies and Religion, University of Bergen, Postbox 7805, 5020, Bergen, Norway
e
Muséum National d'Histoire Naturelle, UMR 7209 du CNRS, Archéozoologie, Archéobotanique: sociétés, pratiques et environnements, and Origine,
Structure et Evolution de la Biodiversité (OSEB), Département Systématique et Evolution, Entomologie, 55 rue Buffon, 75005 Paris, France
f
Laboratoire d'Anthropologie (A3P), UMR 5199, PACEA, Université Bordeaux 1, Avenue des Facultés, 33405 Talence, France
abstractarticle info
Article history:
Received 10 November 2011
Received in revised form 17 March 2012
Accepted 23 March 2012
Available online 30 March 2012
Keywords:
Taphonomy
Ichnology
Insect damage
Cave deposit
Fossil
Bone modification
Three geographically dispersed Middle and Later Stone Age cave sites in South Africa, and a Middle Stone Age
cave site in Ethiopia, share a similar taphonomic signature that includes destruction of bones associated with
variable forms of star shaped features, clusters of microscopically visible sub-parallel striations, edge gnawing,
pits, and etching of the bone surface. Similar traces preserved on Plio-Pleistocene fauna are interpreted by
different authors as the possible work of termites or ants. Considering that ambiguity exists in the interpretation
of these traces and that there are no modern examples available for comparison, we set out to create a reference
collection of bones modified by southern African termites. Here we present the results of an actualistic
experiment conducted with the harvester termite: Trinervitermes trinervoides (Sjöstedt) (Isoptera: Termitidae)
in the Sterkfontein Valley, South Africa. Results show that within six months all bones were approximately half
covered with a dark surface residue, had an etched surface appearance and recorded boreholes and destruction,
particularly of less dense elements and epiphyses. Star-shaped marks, edge gnawing, and clusters of sub-parallel
striationson the periosteal surfacewere faint after six months,but became clearly visibleand more plentiful after
12 months, a finding attributed to the termites being more active in austral autumn and spring. This result
demonstrates the pertinence of insect modification studies to our understanding of regional palaeoenvironment,
palaeoecology and palaeoclimate. This experiment has demonstrated that T. trinervoides can destroy bone in all
stages of preservation, favouring fresh thin cortical and spongy bone with meat and marrow. The presence of
appreciable quantitiesof calcium carbonate in termite mounds suggests that termites may be drawn to dolomitic
cave sites and the calcium-rich bones they contain to satisfy their mineral requirements. They thereforehave the
potential to bias taxonomic and element representation, minimum number of individuals, and age profiles in a
faunal assemblage, andmay account in part forthe patchy preservation of faunalremains, including hominins, in
fossil deposits, and/orthe lack of bone artefacts at some Middle Stone Age cavesites preserving longsequences of
occupation.
© 2012 Elsevier B.V. All rights reserved.
1. Introduction
As primary accumulators and modifiers of bone assemblages in
caves, hyaenas, leopards, humans and porcupines have received a great
deal of attention by taphonomists. A good number of actualistic and
experimental bone modification studies have been conducted (e.g.
Binford, 1981; Brain, 1981; Haynes, 1983; Shipman and Rose, 1983;
Behrensmeyer et al., 1986; Brain, 1993; Blumenschine, 1995; Capaldo,
1997; LeMoine, 1997; Domínguez-Rodrigo, 1999; Denys, 2002; Brain,
2004; Njau and Blumenschine, 2006; Domínguez-Rodrigo et al., 2007,
2010; Fernández-Jalvo and Andrews, 2011), and new analytical
techniques have been developed for the microscopic analysis and
identification of agents responsible for alterations to bone (e.g. Shipman,
1981; Olsen and Shipman, 1988; Kaiser and Katterwe, 2001; d'Errico
and Backwell, 2009). Actualistic research has contributed a great deal to
the identification of diagnostic criteria, and has shown that the damage
caused by some agents may be mimicked by others (e.g. Brain, 1967;
Potts and Shipman, 1981; d'Errico et al., 1984; Shipman and Rose, 1984;
Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
⁎Corresponding authorat: Bernard Price Institute for Palaeontological Research, School
of Geosciences and Institute for Human Evolution, University of the Witwatersrand,
Private Bag3, WITS 2050, Johannesburg, South Africa.Tel.: + 27 11 7176672; fax: +27 11
7176694.
E-mail addresses: lucinda.backwell@wits.ac.za (L.R. Backwell),
alexhp@vodamail.co.za (A.H. Parkinson), eric.roberts@jcu.edu.au (E.M. Roberts),
f.derrico@pacea.u-bordeaux1.fr (F. d'Errico), huchet@mnhn.fr (J.-B. Huchet).
0031-0182/$ –see front matter © 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2012.03.032
Contents lists available at SciVerse ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology
journal homepage: www.elsevier.com/locate/palaeo
Andrews and Cook, 1985; Haynes, 1988; Fiorillo, 1989; Haynes, 1991;
Lyman, 1994; d'Errico and Villa, 1997; Villa and d'Errico, 2001; Backwell
and d'Errico, 2004). While taphonomic research on the effects of large
mammals, birds, water, sediment, wind, and stone has contributed
greatly to our understanding of faunal accumulations and site forma-
tion processes, relatively little attention has been paid to terrestrial
invertebrates as potential modifiers of modern and fossil bone. This is
surprising given that a variety of insect taxa are known to modify
bones with their mandibles, including the larvae of some beetles
(Dermestidae, Tenebrionidae, Scarabaeoidea) (McFarlane, 1971; Coe,
1978; Hefti et al., 1980; Kitching, 1980), moths (Tineidae) (Hill, 1980),
and several distinct families of termites (Termitidae, Mastotermitidae,
Rhinotermitidae) (Derry, 1911; Thorne and Kimsey, 1983; Watson and
Abbey, 1986; Wylie et al., 1987; Huchet et al., 2011). In addition, insects
and their traces have longbeen used by forensic scientists to reconstruct
length of carcass exposure and the chronology of taphonomic events, as
well as gather information on season, palaeoenvironment and palaeo-
climate (Laudet and Antoine, 2004; Bader et al., 2009).
1.1. Contextual information
Our research interest in insect modification of bones developed
mostly out of a need to identify the taphonomic agent responsible for
microscopic star shaped marks and other traces observed on fossils
from four geographically dispersed Middle and Later Stone Age cave
sites in Africa (Fig. 1). A cursory analysis of potentially worked bone
and some associated faunal remains from the Middle Stone Age
(MSA) sites of Sibudu, Plovers Lake and Porc Epic Cave, and the Later
Stone Age (LSA) site of Jubilee Shelter revealed a similar suite of
modifications reminiscent of insect gnawing. Pieces from Sibudu Cave
near the KwaZulu–Natal coast, from a Howiesons Poort layer aged
64.7±1.9 ka (Wadley, 2007; Jacobs et al., 2008a,b; d'Errico et al.,
2012), show traces of destruction, boring, edge gnawing (Fig. 2A),
and clusters of star-shaped marks (Fig. 2B) and sub-parallel striations
(Fig. 2C). A human tibia and associated fauna from Plovers Lake Cave,
situated in the Sterkfontein Valley, from deposits aged between
62.9 ±1.3 and 88.7± 1.6 ka (Churchill, pers. comm.), also preserves
clusters of star-shaped marks (Fig. 3A, B) and sub-parallel striations
(Fig. 3C). Fragmented remains from Jubilee Shelter in the Magaliesburg
northwest of Johannesburg, radiocarbon dated to 1350±120–8500±
240 BP (Wadley and Verhagen, 1986; Wadley, 1989), preserves star-
like features (Fig. 3D1, E1, 2) and edge gnawing (Fig. 3D1, 2). A second
hominin distal element, a fibula, records star shaped marks, surface pits
and edge gnawing (Fig. 4). This piece comes from the MSA site of Porc
Epic Cave, Dire Dawa in east-central Ethiopia. Associated with a human
jaw fragment showing modern features, it is tentatively attributed to
the Late Pleistocene (Assefa, 2006),possibly 77,000 to 61,000 BP (Clarke
et al., 1984). Fossil remains from the four localities thus share a similar
taphonomic signature that includes variable forms of edge gnawing,
star-shaped features and clusters of sub-parallel striations on the
periosteum. A review of the literature in search of comparative material
showed similar traces preserved on Plio-Pleistocene fauna. Star shaped
marks and clusters of sub-parallel striations on remains from East Africa
(Laetoli, Kaiser, 2000,Fig. 5A1, 2; Fejfar and Kaiser, 2005) and Eastern
Europe (Fejfar and Kaiser, 2005: 10) are interpreted as the work of
termites. However, Sands (in Hill, 1987)putsforwardthealternative
idea that the modifications on the Laetoli fauna (Fig. 5B), as well as
the modifications observed on modern bones in Kenya attributed
by Behrensmeyer (1978) to termites, may have been the work of
subterranean safari ants. Ants as collectors and modifiers of small
vertebrates is well documented by Shipman and Walker (1980),who
observed this behaviour amongst harvester ants in Kenya, where they
supplement their granivorous diet with the meat of small animals.
When it comes to identifying insect traces in the South African
archaeological record, our reference is limited to contributions by
ichnologists working on Cenozoic–Mesozoic fossils from South America,
North America and Eurasia (e.g. Tobien, 1965; Thenius, 1979, 1988a,b;
Rogers, 1992; Martin and West, 1995; Laws et al., 1996; Hasiotis and
Fiorillo, 1997; Rogers and Roberts, 1997; Hasiotis et al., 1999; Paik,
2000; Hasiotis, 2004; Laudet and Antoine, 2004; Tapanila et al., 2004;
Fejfar and Kaiser, 2005; Roberts et al., 2007; Britt et al., 2008; Bader
et al., 2009), and confounded by their differing interpretations; a
problem shared with the marks on Plio-Pleistocene fauna from East
Africa. Apart from a human skeleton from Peru (Huchet et al., 2011),
which preserved termite specimens in the matrix surrounding bone
(Scheffrahn and Huchet, 2010), the actualistic studies conducted by
Watson and Abbey (1986) on termites in Australia, and Roberts et al.
(2003) on dermestid beetles in North America, interpretations of
termite and other insect damage have been mostly based on a mac-
roscopic analysis, and did not seek to understand the development in
time of the phenomenon. The earliest report of termite modification of
bones in the palaeoanthropological record pertains to Egyptian and
Nubian graves that preserved mummies with skulls encrusted with
matrix, showing extensive signs of tunnelling that resulted in parts of
the cranium being destroyed (Derry, 1911). The impact of termites on
cranial material has been reported for China (Light, 1929), Australia
(Wood, 1976; Wylie et al., 1987), Kenya (Behrensmeyer, 1978), Panama
(Thorne and Kimsey, 1983)andPeru(Huchet et al., 2011). Post cranial
modification is also documented (Behrensmeyer, 1978; Thorne and
Kimsey, 1983; Wylie et al., 1987; Tappen, 1994; Kaiser, 2000; Brain,
2004; Fejfar and Kaiser, 2005; Huchet et al., 2011), with termites having
completely destroyed some skeletons (Wylie et al., 1987; Guapindaia,
2008). Freymann et al. (2007) report modern termites of the genus
Odontotermes as optionally keratophagous, i.e. hoof eating. The research
of Watson and Abbey (1986) grew out of their discovery of termite
damage to bones in aboriginal cave burials. Their results confirmed
bone modification by termites in cave settings, and showed that
they favoured fresh and weathered bone over diagenetically altered
(fossilized) material. A preference for fresh bone was also observed on
modern carcasses consumed by Neotropical termites (Thorne and
Kimsey, 1983), showing that their activities are widespread. They occur
Fig. 1. Map of Africa showing sites mentioned in the text. The asterisk marks the spot
where the experiment was conducted, in savanna grassland near to the early hominin
sites of Malapa and Gladysvale Cave in the Sterkfontein Valley, South Africa.
73L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
in caves in semi-arid grassland environments and at tropical open air
localities.
1.2. Research background
Termites as agents of post-depositional disturbance at African
open air sites were recognized over twenty years ago by McBrearty
(1990), who showed how their nest building activities can profound-
ly affect the interpretation of site formation processes. Termites were
found to produce pseudofacts that may resemble hearths, and to
concentrate or disperse lithics, thereby affecting temporal resolution.
Concentrated lines of stones were observed across landscapes more
than 500 m in length, where extensive termite activity had produced
a widespread uniform mantle of loamy topsoil. The stone artefacts
had become concentrated at a consistent depth due to this activity,
giving a false impression of an ancient land surface or living floor. The
site of Gombe (Kalina) Point in the Democratic Republic of the Congo
(formerly Zaire) provides another example of lithic migration caused
by termites. Even though distinct artefactual units were discernible,
and the site yielded a series of internally consistent radiocarbon
dates, refitting experiments demonstrated that 39 sets of stone
artefacts from different cultural levels, vertically separated by as
much as 1 m, were joinable (Cahen, 1976, 1978). This is attributed by
McBrearty (1990) to the unconsolidated sediments associated with
termite nests, which are in a constant state of collapse, resulting in
artefacts moving down in the soil profile. A scenario of migrating
lithics caused by termite activity does not pertain to the South African
cave sites discussed here, which record clearly defined and undis-
turbed microstratigraphy (Wadley and Jacobs, 2006; Wadley, 2007;
Jacobs et al., 2008a,b), nor the East African Porc Epic cave site, which
apparently showed clearly demarcated MSA deposits (Clarke et al.,
1984). However, the effect of termite gnawing on bones in different
cultural horizons appears to be a valid concern, because unrecognised
bone destruction by termites would influence interpretations of the
fossil record. Whereas termites may destroy bone through gnawing,
they have also been found to contribute to local bone preservation by
Fig. 2. Selection of modified bones from Sibudu Cave, including a flake from HP layers showing boring and marked destruction of the bone (A1) associated with clusters of star-like
featuresand edge gnawing (A2). A wedge made on a largebovid mandible fragment, from a HP layeraged 64.7± 1.9 ka shows star-shaped marks around nutrientforamina and evidence
of edge gnawing (B). An awl made on a bird radius, from the same HP layer, shows clusters of individual sub-parallel striations and pits (C). Scales in black=10 mm, scales in
white= 1 mm.
74 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
raising the local pH (Lee and Wood, 1971). This was observed at an
Iron Age graveyard in Zimbabwe, where human skeletons were
preserved in the alkaline sediments beneath a termite mound, but not
in the surrounding acidic soil (Watson, 1962, 1969). The presence of
appreciable quantities of calcium carbonate in termite mounds in
Equatorial Africa is reported by Milne (1947,inWatson, 1974), who
found a termite mound with 7% calcium carbonate, and estimated that
it contained about two tonnes of calcium carbonate, excluding the hard
limestone (53% CaCO
3
) base of the mound. The soil underneath one
termite mound in an area of non-calcareous soil was found to have a
mean of 1.7% calcium carbonate to a depth of 6 m, or about 20 tonnes of
calcium carbonate. While the calcium carbonate in termite mounds
may help to preserve bones locally, termite activity ultimately
accelerates bone dissolution through increasing soil porosity and
microbial activity (McBrearty, 1990). In light of the fact that termites
may be extremely destructive to modern and fossil fauna in cave sites,
and considering that ambiguity exists in the interpretation of similar
star-shaped traces in the palaeontological literature, our goal isto create
a reference collection of bones modified by southern African in-
vertebrates, starting with termites. We aim to systematically document
for comparative purposes the type, distribution and frequency of
macro- and microscopic modifications, establish diagnostic criteria for
the identification of the different trace makers, ascertain whether they
favour certain types of bones in specific states of preservation, measure
Fig. 3. Human tibia from Plovers Lake Cave (A), aged 62.9 ±1.3–88.7 ±1.6 ka, showing clusters of star-shaped marks associated with destruction of the bone (A1, 2), and etching of
the periosteal surface (A1). Associated faunal remains (B, C) record star-shaped marks (B) and clusters of individual sub-parallel striations (C). Flakes from the LSA site of Jubilee
Shelter (D, E), radiocarbon dated to 1350 ± 120–8500 ± 240 BP, show star-shaped marks (D1, E1, 2) and edge gnawing (D1, 2). Specimen scales in black = 10 mm. Scales in
A1=10 mm, A2 =5 mm, B-D= 1mm, E2i=2 mm.
75L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
their potential impact on a faunal assemblage, and explore their
forensic potential as palaeoenvironmental indicators. Here we present
the results of an actualistic experiment conducted with termites, and
discuss how our findings relate to similar traces described in the
literature and observed on archaeological remains from South African
cave sites.
2. Materials and method
2.1. Experimental protocol
The bone modification experiments were conducted in the field in
a savanna grassland environment (Mucina and Rutherford, 2006)at
an elevation of 1401 m above sea level, near the early hominin sites
of Gladysvale (Berger, 1993; Berger et al., 1993; Lacruz et al.,
2002, 2003; Pickering et al., 2007) and Malapa (Berger et al., 2010;
Dirks et al., 2010), on the John Nash Nature Reserve (S25°53.910′
E27°45.618′) in the Sterkfontein Valley, South Africa (Fig. 1). The
experiment was set up in March 2007. After six months, at the end of
winter, half of the specimens were removed, and after one year the
experiment was concluded. Winter temperatures for this period
ranged between 5.83 and 20.05 °C, and summer temperatures 13.15–
22.64 °C. Winter rainfall averaged 8.3 mm, while precipitation in
summer was 106.33 mm. Thirty-four bone specimens of varying type
and in different states of preservation (Fig. 6) were inserted directly
into seven Trinervitermes trinervoides (Termitidae: Nasutitermitinae)
mounds at the start of summer. Each termite mound was assigned a
reference letter from A to G and given a GPS coordinate. A hacksaw
blade was used to remove a neat wedge from the nest, producing a
window approximately 100 cm
2
(Fig. 7A, B). Pre-selected bone
specimens were inserted into the mound and the snug-fitting segment
quickly replaced so that worker termites could seal the structure before
outside factors, particularly ants, temperature and humidity, could
negatively affect the nest. The specimens were sourced from chicken
(Gallus domesticus), sheep (Ovis aries) and medium- and large-sized
bovid skeletal remains (following Brain, 1981). Fresh bones were
purchased from a local butchery, while fossil specimens came from
ex situ contexts at Gladysvale Cave. Following Behrensmeyer (1978),
weathered medium and large-size bovid remains, otherwise unmodi-
fied, were found in the field, and drawn from un-catalogued specimens
in the modern mammal collection housed at the Bernard Price Institute
for Palaeontological Research at the University of the Witwatersrand.
Each specimen was numbered from 1 to 34, identified to taxon and
skeletal element (Table 1) and photographed. The level of conservation
for each specimen was recorded as being complete, a shaft fragment, or
a proximal epiphysis. The dominant bone type was noted as thin
cortical (diaphyses), cancellous/spongy (epiphyses, ribs, spinous pro-
cess), thin cortical with cancellous bone, thick cortical, or compact bone
(referring here to bovid carpals and phalanges). Furthermore, the
condition of each specimen was recorded as being fossilised, dry
Fig. 4. Insect traces recorded on a hominin fibula from the MSA site of Porc Epic Cave in Ethiopia, showing surface pits (1, 2), multiple parallel striations (2) and star shaped marks
(3, 4) in the bracketed area. Specimen scale =10 mm, close ups =1 mm.
Fig. 5. Insect traces recorded on Plio-Pleistocene fauna from Laetoli showing star-shaped marks (A1) and clusters of sub-parallel striations (A2) interpreted as termite damage
(from Kaiser, 2000, courtesy of the Entomological Society of America), and clusters of star-like marks (B) posited to be ant damage (Sands in Hill, 1987, with the permission of
Oxford University Press). Scales in A =5 mm, B =10 mm.
76 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
displaying weathering stage 1 or 2 (following Behrensmeyer, 1978),
fresh but dry, fresh with meat, fresh with marrow, fresh with meat and
marrow, or fresh with meat and fur, also referred to as tissue and hide.
After a period of six months, which coincided with austral summer, the
site was revisited and 12 specimens were removed from three mounds
(B, D, F) using a geological pick. It was noted that the termites were
small, non-aggressive and appeared to be slightly disoriented. After one
year, the site was revisited and the 21 remaining specimens were
retrieved from moundsA, C, E and G (Fig. 7C). During this winter period
the termites appeared to be much larger (the size of harvester ants,
which have a body length ranging from 5 to 12 mm), and much more
active. When the bone specimens were removed from the mounds they
were heavilyencrusted with mound matrix (Fig. 7D), and one specimen
was never located. The encrusted bones were cleaned in the lab using
cold water and a very soft paint brush, and air dried under a lamp.
2.2. Analytical protocol
Each specimen was analysed and photographed at magnifications
between 7 and 50 times under reflected light using an Olympus SZX 16
Multifocus microscope fitted with a digital camera. Qualitative and
quantitative information on specimen morphometrics and taphonomic
alteration was recorded for each specimen in an Excel spreadsheet for
later analysis using StatView. Once all of the specimens had been
analysed, examples of the types of features observed were moulded
using Coltene President light body dental elastomer, and cast in resin
(Araldite M resin). Transparent replicas of the traces were viewed and
photographed under transmitted light using the same Olympus SZX 16
microscope system, and studied using a JEOL JSM-840 Scanning
Electron Microscope (SEM) at magnifications between 130 and 270 x.
In an attempt to understand better the mandibular mechanics behind
the traces, three specimens of Trinervitermes trinervoides workers were
also studied using SEM. Striations associated with six distinct bone
modification features were measured and counted using analySIS getIT
image processing software linked to the Multifocus microscope. A total
of 281 striations were measured, comprising two star shaped marks
(with a total of 138 striations), and four clusters of sub-parallel
striations (with a total of 143 striations). The data were analysed and
a Mann–Whitney Utest was applied to establish whether a difference
exists between the populations of striations comprising the two
features.
3. Results
Results show that Trinervitermes trinervoides, the most widely dis-
tributed termite found in southern Africa (Uys, 2000), do modify bone in
Fig. 6. Selectionof specimen types and statesof preservation chosenfor the experiment prior to insertion in the mounds(named A to F) and grouped here accordingly. (A1) specimen 11,
a fossilisedmedium sized bovidrib fragment; (A2) specimen 10, a weathered largebovid vertebral spine fragment;(A3) specimen 19, a fresh large bovidrib fragment; (B1) specimen 8, a
fossilisedmedium sized bovidlong bone flake; (B2) specimen7, a weathered mediumsized bovid long bone flake;(B3) specimen 9, a fresh Ovis tibia flake; (C1) specimen14, a weathered
medium sizedbovid proximal metapodial; (C2)specimen 13, a fresh mediumsized bovid proximalmetapodial with hide;(C3) specimen 12, a freshOv isproximal tibia; (D1) specimen6,
a fossilised large bovid long bone flake; (D2) specimen 5, a weathered large bovid long bone flake; (D3) specimen 4, a dry large bovid long bone flake; (D4) specimen 20, a fresh large
bovid longbone flake; (E1) specimen15, weatheredbird humerus; (E2) specimen 22, freshbird humerus; (F1)specimen 3, a fossilised mediumsized bovid 2nd phalanx;(F2) specimen 2,
a dry medium sized bovid 1st phalanx; (F3) specimen 1, medium sized bovid 1st and 2nd phalanges with hide. Scale= 10 mm. See Table 1 for details on specimens.
77L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
a number of ways. All 33 specimens used in the experiment displayed
one or more types of damage. Eight overarching types of bone
modification were observed: destruction, bore holes, etched surface
texture, surface pits, star shaped marks, clusters of sub-parallel striations,
parallel striations and the presence of a surface residue (Table 2). While
thepresenceofresidueisnotabonemodification type, but rather a
Fig. 7. Eric Roberts setting up the experiment in a T. trinervoides termite nest (A) on a nature reserve in the Sterkfontein Valley, South Africa. Bones of varying type and state of
preservation were inserted directly into each mound (B) and the segment of removed nest quickly replaced. Fernando Abdala recovering specimens one year later (C).
Experimental bones removed from mounds were heavily encrusted with nest matrix (D). Scale =5 cm.
Table 1
Experimental protocol.
Condition Spec. no. Taxon Element Conservation Bone type Mound Time
Weathered* 10 Indet. Large bovid Spinous process Shaft fragment Spongy A 12
Weathered* 14 Indet. Med. Bovid Metapodial Prox. epiphysis Thin cort. and spongy D 6
Weathered* 15 Gallus domesticus Humerus Complete Thin cortical F 6
Weathered** 5 Indet. Large bovid Longbone Shaft fragment Thick cortical C 12
Weathered** 7 Indet. Med. Bovid Longbone Shaft fragment Thin cortical B 6
Fossil 3 Indet. Med. Bovid 2nd phalanx Complete Compact E 12
Fossil 6 Indet. Large bovid Longbone Shaft fragment Thick cortical C 12
Fossil 8 Indet. Med. bovid Longbone Shaft fragment Thin cortical B 6
Fresh dry 2 Indet. Med. Bovid 1st phalanx Complete Compact E 12
Fresh dry 4 Indet. Large bovid Longbone Shaft fragment Thick cortical C 12
Fresh with marrow 18 Indet. Med. Bovid Tibia Shaft fragment Thin cortical F 6
Fresh with marrow 25 Gallus domesticus Humerus Shaft fragment Thin cortical B 6
Fresh with marrow 27 Gallus domesticus Humerus Shaft fragment Thin cortical A 12
Fresh with marrow 28 Gallus domesticus Humerus Shaft fragment Thin cortical B 6
Fresh with marrow 29 Ovis aries Tibia Shaft fragment Thin cortical E 12
Fresh with meat 12 Indet. Med. Bovid Tibia Prox epiphysis Thin cort. and spongy D 6
Fresh with meat 19 Indet. Large bovid Rib Shaft fragment Spongy A 12
Fresh with meat 20 Indet. Large bovid Longbone Shaft fragment Thick cortical C 12
Fresh with meat and fur 1a Ovis aries 1st phalanx Complete Compact E 12
Fresh with meat and fur 1b Ovis aries 1st phalanx Complete Compact E 12
Fresh with meat and fur 1c Ovis aries 2nd phalanx Complete Compact E 12
Fresh with meat and fur 1d Ovis aries 2nd phalanx Complete Compact E 12
Fresh with meat and fur 13 Indet. Med. Bovid Metapodial Prox. Epiphysis Thin cort. and spongy D 6
Fresh with meat and fur 34 Ovis aries Carpal Complete Compact D 6
Fresh with meat and fur 35 Ovis aries Carpal Complete Compact D 6
Fresh with meat and marrow 22 Gallus domesticus Humerus Complete Thin cortical F 6
Fresh with meat and marrow 23 Gallus domesticus Humerus Complete Thin cortical A 12
Fresh with meat and marrow 24 Gallus domesticus Humerus Complete Thin cortical B 6
Fresh with meat and marrow 30 Ovis aries Tibia Shaft fragment Thin cortical G 12
Fresh wet 9 Indet. Med. Bovid Tibia Shaft fragment Thin cortical B 6
Fresh wet 31 Ovis aries Tibia Shaft fragment Thin cortical G 12
Fresh wet 32 Ovis aries Tibia Shaft fragment Thin cortical G 12
Fresh wet 33 Ovis aries Tibia Shaft fragment Thin cortical G 12
Abbreviations: Spec. no. (specimen number), Time (months), weather stage 1 (*), weathering stage 2 (**) after Behrensmeyer (1978), indet. (indeterminate), med. (medium), prox.
(proximal), cort. (cortical).
78 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
feature, it is included with the other criteria because it is associated with
the destruction of bone. The bone modification features are presented
from the most to the least visible. Four of the modification features are
macroscopically observable (with the naked eye). These include bone
destruction, bore holes, an etched surface appearance and the presence
of residue. Surface pits and star shaped marks are considered as
intermediate between macro- and microscopic levels of observation,
while parallel and sub-parallel striation marks are only seen with the aid
of a microscope. Macroscopically visible modifications are presented in
Table 3, while features considered as intermediate and microscopically
visible are presented in Table 4. Both tables have been ordered according
to the condition of the specimen prior to termite alteration, as presented
in the experimental protocol in Table 1. The location of modifications is
recognised as being on the interior or body of the periosteum, medulla,
edges and ends of specimens.
3.1. Macroscopically visible modifications
3.1.1. Destruction (Table 3,Fig. 8A, B)
A total of 16 specimens showed signs of destruction, with bone
removal occurring on nearly half (47%) of the sample. Four of the eight
specimens with a medulla displayed destruction. Destruction of the
periosteum, on the body of a piece away from an edge, was present on
12 out of 16 specimens (75%). After six months destruction was
recorded on four indeterminate medium bovid long bone fragments
(specimens 7, 9, 14, 18), and three complete Gallus domesticus humeri
(specimens 15, 22, 24), distributed over three mounds (B, D, F). After
12 months destruction was record on two Ovis aries (specimens 1a, 31),
one indeterminate medium bovid (specimen 3) and five indeterminate
large-size bovid long bone shaft fragments (specimens 4, 6, 10, 19, 20),
and one G. domesticus (specimen 23) humerus, distributed over four
mounds (A, C, E, G). Overall, destruction occurred equally on complete
and fragmented specimens; however, thin cortical bone was more
affected, with ten of the 16 specimens (63%) showing destruction to
originally fresh bone, while only four weathered (25%) and two fossil
specimens (12%) showed this modification. Destruction was found in
combination with parallel striations (edge gnawing) on 12 specimens,
an etched surface appearance on 11 specimens, star shaped marks and
clusters of sub-parallel striations on seven specimens and on four
specimens with bore holes and surface pits. Refer to Table 1 for
specimen descriptions.
3.1.2. Bore holes (Table 3,Fig. 8C, D)
Eight bore holes were recorded on four specimens recovered from
four mounds, representing 12% of the sample. They always occurred on
the ends of specimens. After six months two complete G. domesticus
humeri, originally with meat and marrow, were recovered from two
different mounds (specimen 22 from mound F and specimen 24 from
mound B). The one humerus had only a single bore hole, while the
other displayed four, the highest number recorded on any specimen.
After twelve months an additional complete G. domesticus humerus
(specimen 23) was recovered from mound A, originally with meat
and marrow, along with a fossilised complete 2nd phalanx of an
indeterminate medium-sized bovid (specimen 3 from mound E). The
G. domesticus humerus had only a single bore hole, while the fossilised
Table 2
Types of bone modification caused by termites.
Modification type Description and level of observation Fig. no.
Destruction Obliteration of bone. Macroscopically visible. 8A, B
Bore holes Semi-circular holes that penetrate outer cortical lamella and/or cancellous bone through to the medullary cavity. Boreholes typically
range between 3.41 and 4.20 mm in length and between 2.83 and 2.64 mm in width, though one borehole measures 6.09 by 3.06 mm.
These features are macroscopically visible.
8C, D
Etched appearance Removal of outer lamellae to expose underlying bone structure. Macroscopically visible. 8E, F
Surface residue Dark brown to black coating that discolours the bone and is associated with destruction and etching of the bone surface. Macroscopically
visible.
8G, H
Surface pits Semi-circular depressions nested in bone that exhibit radially arranged edge gnawing comprising overlapping individual sub- and parallel
striations. The lengths of pits range between 1.97and 3.63 mm, and the widths between 1.54 and 3.09 mm. Surface pits are intermediately
visible. At 25× magnification the internal morphology of pits show indistinct and randomly oriented gnaw marks.
9A, B
Star shaped marks Numerous sometimes overlapping individual striations/grooves radially arranged around a cavity with smooth walls, though at 50×
magnification very faint scratch marks may be observed where the cavity wall meets the periosteal surface of the bone. The striations
constituting the star shaped marks have a u-shaped profile and smooth internal morphology. Striations average 518 μm in length. Star
shaped marks are intermediately visible.
9C, D
Parallel striations Multiple relatively parallel striations located along and oriented perpendicular to broken edges or ends. Also referred to as edge gnawing.
They have a u-shaped profile and smooth internal morphology. Microscopically visible.
9E, F
Sub-parallel striations Clusters of randomly oriented sub-parallel striations located mainly on the periosteum or body of specimens, away from edges. They have
a u-shaped profile and smooth internal morphology. Striations average 599 μm in length. Microscopically visible.
9G, H
Table 3
Description of macroscopically visible features.
Destruction Bore holes Etched-like surface Surface residue Spec.
Location No. Location % Location % No.
peri. na Peri. 41-60 All over 41–60 10
peri. na na na Peri. 21–40 14
peri. na Peri. > 80 All over 41–60 15
na na Peri. 41–60 Med. 21–40 5
peri. na Peri. 41–60 Peri. b20 7
peri. 2 Peri. >80 All over 41–60 3
peri. na na na All over 61–80 6
na na Peri. 21–40 All over 61–80 8
na na Peri. 21–40 Ends b20 2
med. na Med. >80 Peri. 41–60 4
med. na na na All over 21–40 18
na na Med. >80 All over 21–40 25
na na Peri. > 80 All over >80 27
na na Peri. > 80 All over >80 28
na na Med. 61–80 Peri. 21–40 29
na na Peri. 21–40 All over 41–60 12
peri. na Peri. > 80 All over 21–40 19
peri. na Med. 61–80 All over 41–60 20
peri. na na na All over 41–60 1a
na na na na All over 41–60 1b
na na Peri. b20 All over 41–60 1c
na na Peri. b20 All over 41–60 1d
na na Peri. b20 Peri. b20 13
na na na na Peri. b20 34
na na na na Peri. b20 35
peri. 1 Peri. >80 All over 41–60 22
peri. 1 Peri. >80 Peri. b20 23
peri. 4 Peri. >80 All over 41–60 24
na na Peri. 61–80 Peri. 21–40 30
med. na na na All over 41–60 9
med. na Peri. 41–60 Peri. 21–40 31
na na Peri. 21–40 All over 41–60 32
na na Med. 61–80 Peri. 21–40 33
Abbreviation: Spec. (specimen), No. (number), % (area cover), peri. (periosteum), med.
(medulla).
79L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
2nd phalanx recorded one on both ends. Boreholes typically range
between 3.41 and 4.20 mm in length and between 2.83 and 2.64 mm in
width, though one borehole measures 6.09 by 3.06 mm. Bore holes
were found in combination with destruction and an etched surface
texture on all four specimens, with star shaped marks and sub-parallel
striations on three specimens, and with parallel striations on two
specimens. Refer to Table 1 for specimen descriptions.
3.1.3. Etched surface texture (Table 3,Fig. 8E, F)
Twenty-five specimens (75%) displayed varying degrees of an
etched surface texture. The etched appearance was recorded as faintly
visible on three specimens, moderately visible on five and clearly visible
on 17. In all instances, this etched surface texture was recorded on the
periosteum, and in five cases also occurred in the medullary cavity.
Three specimens recorded etching on b20% of the surface area, four
specimensrecorded damage in therange 21–40% surface cover, another
four in the range 41–60%, and four more in the range 61–80%. Ten
specimens (nearly half) exhibited an etched appearance on more
than 80% of the bone piece. After six months four indeterminate
medium-sized bovid specimens (specimens 7, 8, 12, 13) and four Gallus
domesticus humeri (specimens 15, 22, 24, 28)were retrieved from three
mounds (B, D, F). After twelve months 16 bones were retrieved from
four mounds(A, B, C, E), including seven of Ovis aries (specimens 1c, 1d,
29, 30, 31, 32, 33), two of an indeterminate medium-sized bovid
(specimens 2, 3), five of an indeterminate large-sized bovid (specimens
4, 5, 10, 19, 20) and two G. domesticus long bones (specimens 23, 27). In
sum, an etched appearance was apparent after six months, and more
than three quarters (76%) of the etched pieces were from originally
fresh bone. After one year it was considerably higher, with 85% of all
specimensexhibiting etching. Four specimens were weathered and two
were fossils. The majority of etched pieces were thin cortical or spongy
bone. Two of the three thick cortical bone specimens were etched in the
medullary cavity. An etched surface texture was found in association
with parallel striations on 18 of the 25 specimens, destruction on 11
specimens, sub-parallel striations on ten specimens, star shaped marks
on nine, surface pits on five, and bore holes on four specimens. Refer to
Table 1 for specimen descriptions.
3.1.4. Surface residue (Table 3,Fig. 8G, H)
The presence of a surfaceresidue and associated burned-like surface
discolouration was recorded on every specimen to a varying degree.
The percentage of total surface area affected was recorded as either
0–20% (6 specimens), 21–40% (8 specimens), 41–60% (15 specimens),
61–80% (2 specimens) or> 80% (2 specimens). No dominant location
could be established for this feature as the distribution of the residue
and discolouration was widespread and random.
3.2. Intermediate modifications
3.2.1. Surface pits (Table 4,Fig. 9A, B)
Surface pits were recorded on six specimens from three mounds
(B, E, F). Pits occurred primarily on the ends of complete bones, on the
outer periosteum in areas away from the edge, and on the medullary
wall in a single case. After six months three specimens recovered from
two mounds had pits (specimens 7 and 24 from moundB and specimen
15 from mound F). Three specimens (1a,1b, 2) recovered from a single
mound (E) showed surface pits after twelve months. The lengths of pits
range between 1.97 and 3.63 mm, and the widths between 1.54 and
3.09 mm. Surface pits were found in combination with star shaped
marks on five specimens, with sub-parallel striations, destruction and
Table 4
Description of intermediate and microscopically visible features.
Intermediate Microscopic
Surface Pits Star-shaped marks Parallel striations Sub-parallel striations Spec.
Loc. No. Loc. Vis. % Loc. Vis. % Loc. Vis. % No.
na na Peri. Clear 21–40 Ed. & en. Clear b20 Peri. Clear 21–40 10
na na na na na Edge Faint b20 Peri. Faint b20 14
Peri. 1 Peri. Faint b20 na na na Peri. Faint b20 15
na na na na na Ed. & en. Clear >80 Peri. Mod. b20 5
Med. 2 na na na Ed. & en. Faint 21–40 Med. Mod. b20 7
na na Peri. Mod. 21–40 na na na Peri. Mod. b20 3
na na Med. Faint b20 Ed. & en. Clear 21–40 na na na 6
na na na na na Edge Faint b20 na na na 8
Peri. 1 Peri. Clear 21–40 End Faint b20 Peri. Faint b20 2
na na na na na Ed. & en. Clear 61–80 na na na 4
na na na na na Ed. & en. Clear b80 na na na 18
na na na na na na na na na na na 25
na na na na na Ed. & en. Clear 21–40 na na na 27
na na na na na End Clear 21–40 na na na 28
na na na na na Ed. & en. Clear 41–60 na na na 29
na na na na na na na na na na na 12
na na na na na na na na na na na 19
na na na na na Edge Mod. b20 na na na 20
Peri. 2 Peri. Clear b20 End Faint 41–60 na na na 1a
Peri. 1 Peri. Faint b20 End Faint 21–40 na na na 1b
na na Peri. Clear 21–40 End Faint 41–60 na na na 1c
na na Peri. Clear 21–40 End Faint 21–40 na na na 1d
na na na na na End Faint b20 Peri. Faint b20 13
na na na na na na na na na na na 34
na na na na na na na na na na na 35
na na na na na na na na na na na 22
na na Peri. Mod. b20 End Clear b20 Peri. Faint b20 23
Peri. 2 Peri. Faint b20 Ed. & en. Faint b20 Peri. Faint b20 24
na na na na na Edge Faint b20 na na na 30
na na na na na Edge Clear b20 na na na 9
na na na na na Edge Mod. b20 na na na 31
na na na na na Edge Mod. b20 na na na 32
na na na na na na na na na na na 33
Abbreviation: Spec. (specimen), No. (number), Loc. (location), % (area cover), Vis. (visibility), peri. (periosteum), med. (medulla), mod. (moderate), ed. & en. (edge and end).
80 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
an etched surface texture on four specimens, parallel striations in three
cases and bore holes in a single instance. Refer to Table 1 for specimen
descriptions.
3.2.2. Star shaped marks (Table 4,Fig. 9C, D)
Eleven specimens (33%) were found to display star shaped marks,
which occurred on the periosteum away from an edge, and in one case
on the medullary wall. In five instances they were considered clearly
visible, in two cases moderate, and in four faintly visible. In five
instances they were randomly scattered across 21–40% of the surface
area, and in seven instances were recorded as singularly occurring
modifications covering b20% of the available surface. Scanning electron
microscopy revealed individual striations (grooves) constituting the
star shapes to be smooth-sided and featureless, unlike stone tool-
generated marks with their characteristic internal microstriations
(Potts and Shipman, 1981; Shipman, 1981; Shipman and Rose, 1983,
1984; Shipman, 1988). While they appear at low magnification to
radiate neatly from the centre, at high magnification, some individual
striations become difficult to distinguish, because they overlap and/or
cross-cut one another.
Fig. 8. Experimental bones from termite mounds showing destruction or obliteration on (A) specimen 23, a Gallus domesticus humerus retrieved after one year, and (B) specimen 22,
aG. domesticushumerus retrievedafter six months.Bore holes on (C) specimen 24, a freshG. domesticus humerusretrieved aftersix months, and (D) specimen22, a G. domesticus humerus
retrieved after six months. An etchedsurface appearance on (E) specimen 28, a G. domesticus humerus flake retrieved after six months, and (F) specimen 12, an Ovis tibia fragment that
originally had flesh attached and was retrieved after six months. Surface residue on(G) specimen 10, a large bovid vertebral spine that originally showed weathering stage 1, retrieved
after one year,and (H) specimen 22, a G. domesticus humerus retrieved aftersix months. Note the furrowsand recessed areas associated with the residueafter only six months.Specimens
in A, B, C, D, E and H originally had flesh and marrow. Scales= 1 mm unless indicated otherwise. See Table 1 for details on the specimens.
81L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
After six months, star shaped marks were recorded on one in-
determinate medium-sized bovid (specimen 7) and two G. domesticus
long bones (specimens 15, 24), distributed over three mounds (B, E, F).
After 12 months star shaped marks were recorded on four O. aries
(specimens 1a, 1b, 1c, 1d), two indeterminate medium-size bovid
(specimens 2, 3), two indeterminate large-size bovid fragments
(specimens 6, 10) and one G. domesticus long bone (specimen 23),
retrieved from a further three mounds (A, C, E). Star shaped marks were
found in combination with parallel striations on nine specimens, with
an etched surface texture on eight specimens, with destruction on
seven, sub-parallel striations on six, surface pits on five, and with bore
holes on three specimens. Refer to Table 1 for specimen descriptions.
3.3. Microscopic modifications
3.3.1. Parallel striations (Table 4,Fig. 9E, F)
Multiple parallel striations situated perpendicular to and located
along broken edges or ends were recorded on 24 specimens (73%),
primarily on the periosteal surface. After six months, parallel
striations were recorded on six indeterminate medium-sized bovid
(specimens 7, 8, 9, 13, 14, 18), and two Gallus domesticus long bones
(specimens 24, 28), distributed over three mounds (B, D, F). After
12 months ten specimens, observed at relatively low magnification
(7–20 times), recorded clearly visible striations, while three were
considered moderately visible, and ten faint. Twelve specimens (36%)
Fig. 9. Bones retrieved from termite mounds after one year showing (A, B) surface pits on specimen 1a. Note the randomlyoriented gnawing, as opposed to distinct striation marks
in the base of the pit; star-shaped marks comprising individual striations radially arranged around a smooth-walled central cavity are preserved on (C) specimen 1c, and (D)
specimen 10, shown here as a resin replica observed under transmitted light; edge gnawing comprising multiple approximately parallel individual striations is recorded on (E)
specimen 10, and (F) a resin replica of specimen 18; clusters of individual sub-parallel striations on the periosteum, away from an edge, are recorded on (G) specimen 29, and (H) a
resin replica of specimen 10. Scales =1 mm unless indicated otherwise. See Table 1 for details on the specimens.
82 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
showed percentage edge damage in the range 0–20%, six in the range
21–40%, three in the range 41–60%, one in the range 61–80%, and two
in the range 80–100%. Parallel striations were recorded on eight Ovis
aries (specimens 1a, 1b, 1c, 1d, 29, 30, 31, 32), one indeterminate
medium-size bovid (specimen 2), five indeterminate large-size bovid
(specimens 4, 5, 6, 10, 20) and two G. domesticus long bones
(specimens 23, 27), distributed over four mounds (A, C, E, G). Parallel
striations were found in combination with an etched surface texture
on 18 specimens, with destruction on 12, star shaped marks on nine,
with sub-parallel striations on eight, with surface pits on five, and
with bore holes on two specimens. Refer to Table 1 for specimen
descriptions.
3.3.2. Sub-parallel striations (Table 4,Fig. 9G, H)
Ten specimens (33%) from six mounds (A, B, C, D, E, F) displayed
clusters of sub-parallel striations, in nine cases on the periosteum and
once in the medullary cavity. In six instances the striations were
considered as only faintly visible, even microscopically, while in three
instances they were moderately visible, and only once were they
considered as clearly visible, on a weathered piece after 12 months.
These clusters of striations did not cover any significant amount of the
total available surface area, with nine of the ten specimens recording
b20% surface cover, and one specimen 21–40%. After six months, sub-
parallel striations were faintly visible on three indeterminate medium-
size bovid (specimens 7, 13, 14) and two Gallus domesticus long bones
(specimens 15, 24), retrieved from three mounds (B, D, F). After twelve
months, sub-parallel striations were more clearly observed on two
indeterminate medium-size bovid phalanges (specimens 2, 3), two
large-size bovid shaft fragments (specimens 5, 10), and one G.
domesticus long bone (specimen 23), retrieved from three mounds (A,
C, E). In sum, although not readily visible, after 12 months clusters of
sub-parallel striations were found to occur on all types of bone in equal
proportion on pieces in different stages of preservation, from fresh with
meat and marrow to completely fossilised. Sub-parallel striations were
found in combination with an etched surface texture on nine specimens,
with parallel striations in eight, with star shaped marks in six, with
destruction on seven, with surface pits on four, and with bore holes on
three specimens. Refer to Table 1 for specimen descriptions.
3.3.3. Striation length
Measurement of the length of 281 striations, constituting two star
shaped marks and four clusters of sub-parallel striations, showed that of
the 138 striations associated with star shaped marks, the shortest was
171 μm, and the longest 832 μm. The mean average was 518 μmwitha
standard deviation of 137 μm. The shortest sub-parallel striation was
244 μm, and the longest 889 μm. The mean average was 599 μm, with a
standard deviation of 97.2 μm.
AMann–Whitney Utest produced a Z-value of −6.248 and a P-value
of b0.0001, indicating that a significant difference exists between the
length of the striations comprising the two features, with sub-parallel
striations markedly longer than those of star shaped marks. This is
possibly because star shaped marks radiate around a well-defined
central cavity that provides anchorage for one half of the mandible,
while the other half excavates the bone using an inward gesture, as
suggestedbytwoTrinervitermes trinervoides worker mandibles ob-
served using SEM, which show signs of wear damage on the medial side
of the apical tooth (Fig. 10). In accordance with observations by
Weesner (1987), the mandibles are asymmetrical, with a single apical
tooth responsible for the production of individual striations, augmented
by two or three marginal teeth.
4. Discussion
This experiment has demonstrated that Trinervitermes trinervoides,a
variety of termite similar in size to a sugar ant, certainly do destroy
bone, with pre-fossilised material showing the most destruction. This
finding is in accordance with Watson and Abbey (1986) for Australian
termites. Thin cortical bone was more affected than thick cortical or
compact bone. Destruction was apparent on half of the specimens
within six months, by which time bird bone epiphyses were completely
destroyed. Fresh bone with remnants of meat and marrow were
favoured, though all bones at all stages of preservation recorded all of
the eight features after 12 months, mainly on the periosteal surface.
Fig. 11 shows the percentage of modifications recorded on all ex-
perimental specimens after six and 12 months. As pre- and post-
depositional destroyers of bone in cave deposits, termites have the
potential to bias taxonomic and element representation, minimum
number of individuals, and age profiles in fossil faunal assemblages,
resulting in a lack of small vertebrate and juvenile remains.
Fig. 10. Scanning electron micrographs of a T. trinervoides mandible (A) and a close up view of the worn apical cusp showing where it contacted the bone (B). Scale A = 100 μm,
scale B =10 μm.
Fig. 11. Type and percentage of modification observed on all specimens used in the
experiment after six and 12 months.
83L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
4.1. Plio-Pleistocene record of insect traces for South Africa
Evidence of destruction on MSA fauna at Plovers Lake Cave in the
Sterkfontein Valley warrants further taphonomic investigation of
fauna from other early hominin sites in the region. At present, the
identification of termite damage on faunal remains from Swartkrans is
based solely on the recognition of boreholes (Newman, 1993, 2004),
which according to our study are relatively rarely produced; only four
of the 33 specimens analysed recording this feature after one year.
Forty-one of the 147,311 fossil bone pieces analysed from Members 1,
2, 3 and 5 show circular holes that vary in diameter from 2 to 5 mm,
and may penetrate for up to 1 cm. The walls of borings are described as
smooth, while their bases are rounded. It has been surmised that
smaller holes and tunnels were made by termites, while larger
examples were the work of beetle or moth larvae (Newman, 1993,
2004). As noted by Newman (1993, 2004), such insects were
obviously occasionally active on the floor of the cave during the
accumulation periods of all Members investigated. Traces of insect
burrowing and boring are reported on eight of the 33,421 specimens
studied by Pickering (1999) from Sterkfontein Member 5, and one
hominin vault fragment (Stw 545) from Member 4, although there is
no description of the modifications, extent of damage or identification
of the putative agents. Kitching (1980) identified fossil puparial casts
and burrows of blow-fly (Calliphoridae), as well as dung balls and
dung beetle (Scarabaeidae) burrows, carrion beetle (Trogidae) puparial
casts, and dermestid beetle boring (Dermestidae) in bovid long bones
from the Lower Phase I (Member 3) through to Upper Phase I (Member
4) breccias at Makapansgat (3–1 My). Fossilised pupae similar to
material described by Kitching as dermestid beetles is noted by Berger
and Lacruz (2003) in the deposits at Motsetse (c.1.64–1.0 Ma), also in
the Sterkfontein Valley, and Brink (1987) has documented hornmoth
(Ceratophaga vastella) marks on numerous bovid horncores in the Old
Collection of the Florisbad faunal assemblage, dated to c. 400–100 ka.
Apart from the few other authors that have cited the presence of insect
bone modification in fossil localities, there remains a paucity of data on
the type and extent of insect damage in the southern African fossil
record.
4.2. Termite foraging on bone and seasonality
Six out of eight bore holes recorded in this study were either on the
proximal and/or distal ends of complete Gallus domesticus humeri, and
they were produced on two specimens within six months. The only
other specimen with bore holes is a fossilised complete 2nd phalanx of
an indeterminate medium-size bovid, which has a bore hole on both
ends. Evidence of borings on bones in different stages of preservation,
and the discovery of two small mammal bones in one termite mound,
which had not been placed there by us, suggests that termites select
bones at different diagenetic stages for consumption of various trace
elements (calcium, phosphorous, nitrogen), proteins and lipids. The
etched surface appearance on three quarters of thesample is caused by
the saliva- or faecal rich material produced by the termites, and found
lining the inner walls of the galleries inside the mound. Manifest as a
dark, patchy residue, it creates an acid-etched appearance as the
underlying bone structure is exposed. The high degree of etching and
destruction recorded on bird and bovid epiphyses demonstrates the
marked effect of the pH and chemical composition of the termite
secretion on less dense bone. Trinervitermes trinervoides forage in the
open in a radiusof ~ 8.25 m from the mound, witha colony exploiting an
area of approximately 214 m
2
annually (Adam et al., 2008). However,
other termite taxa create galleries on and around the food source
(Bignell, 2010), a feature that may prove useful in the identification of
fossil species. The residue is also associated with the darkening of the
bone surface, almost to the point that some specimens appear burned.
While the residue may not survive in the fossil record, the effects may
be preserved in the form of etching, pinprick holes (exposed underlying
Haversian canals and nutrient foramina), broad furrows and subtle
recesses on the bone surface. Surface pits were found primarily on
complete specimens. Five of the six pits occur on the periosteal face of
four unfossilised sheep and bovid phalanges and the diaphyses of
chicken humeri. Two surface pits were recorded on a specimen that also
displays four bore holes (specimen 24, retrieved after six months). Pits
are markedly smaller than boreholes, yet the length-width ratio of
surface pits to boreholes is relatively consistent, suggesting that pits
represent incipient boreholes. Considering that both features occur
predominantly on complete freshspecimens, it would appear that apart
from providing a source of calcium carbonate, termites also consume
bones for their protein and marrow lipid content.
Of the eight features associated with termites, the most distinctive
and diagnostic are those produced by the mandibles of workers,
including multiple parallel striations (edge gnawing), clusters of sub-
parallel striations, and star shaped marks on the bone surface.
Multiple parallel striations are clearly visible on the edges and/or
ends of most specimens in all states of preservation after 12 months,
while clusters of sub-parallel striations occur on a third of specimens,
on the periosteal surfaces of fresh and weathered bone in equal
proportions, where they are generally faint, situated on an anatomical
ridge or rough area away from an edge. After 12 months star shaped
marks were clearly observed on bovid and sheep phalanges and
the diaphyses of complete bird humeri, all in different states of
preservation. Star shaped marks and pits produced by termites may
prove to be the most diagnostic of the eight features identified, based
on a smooth central cavity that lacks or has very faint mandible marks,
associated with radially arranged individual u-shaped grooves/
striations that have a smooth internal morphology. Star shaped
marks, clusters of sub-parallel striations, multiple parallel striations,
surface pits and borings all result from gnawing on edges, elevated
areas or around vascular canals on the surfaces of bone, sites that
provide traction for the apical teeth of the mandible. Even though the
various modification categories are quite distinct, star shaped marks
and surface pits likely represent incipient boreholes in search of lipids,
while early forms of destruction take the form of clusters of sub-
parallel striations and star shaped features.
The increase in number and intensity of bone modifications from
the 6 to 12 month collections appears to be a function of seasonality.
It has been shown that Trinervitermes trinervoides do not forage
during the South African winter months of June, July and August, and
that little foraging takes place during the peak summer months
(Adam et al., 2008). Increased activity occurs in autumn (April) and
spring (October), with foraging rates recorded as being significantly
higher at temperatures ranging between 13 and 25 °C. The life cycle
of termites depends largely upon the environment they inhabit; in
semi-arid regions termite colonies usually produce winged repro-
ductive alates at the start of the rainy season, while in the tropics
their dispersal can occur throughout the year (Martius et al., 1996).
Once they disperse, the alates mate and establish a new colony,
producing first workers that build the mound, forage for food and
tend to the young, and later soldiers to defend the colony (Uys, 2000;
Bignell, 2010). This implies that the destruction rate of bone is also
seasonal, associated with the life cycle of the termite. This is
supported by Fig. 12, which shows the increased percentage of
bones with gnaw marks after twelve months. These findings highlight
the contribution of insect modification studies to our understanding
of regional palaeoenvironment, palaeoecology and palaeoclimate. The
insect traces documented here provide an excellent source of data
on past temperature and moisture regimes, and demonstrate the
potential of these features as indicators of seasonality. Based on the
results of the termite experiment, it would appear that bones from
MSA layers at Sibudu, Plovers Lake and Porc Epic caves, and LSA layers
at Jubilee Shelter record the same suite of modifications, namely
destruction of bone associated with an etched surface appearance,
occasional bore holes and pits, numerous variably star-shaped marks,
84 L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
with striations radially arranged around smooth-walled central
cavities or nutrient foramina, individual parallel striations (edge
gnawing) and clusters of individual sub-parallel striations on the
periosteum. It is noteworthy that of the relatively few bones studied
in the course of identifying potentially human modified bone from
these sites, two of the specimens studied are artefacts from HP layers,
and another two are the distal elements of hominins. Termites may
thus account, in part, for the sparse and patchy faunal record, which
may be absent at sites with long occupation sequences, and the lack
of MSA bone tools at some sites, when others preserve collections of a
range of organic remains. In the case of Sibudu Cave, termite gnawing
on HP artefacts aged 64.7±1.9 ka suggests an optimal foraging
temperature of between 13 and 25 °C, or at least within a range of
6–33 °C at this time, based on the finding that T. trinervoides do not
forage outside of this range (Adam et al., 2008). The traces recorded on
faunal remains from Plio-Pleistocene deposits in East Africa appear to
parallel those recorded on bones used in the termite experiment. Most
notably, the clusters of variably star-shaped marks comprising radially
arranged individualstriationswith a smooth central pit, clusters ofsub-
parallel striations on the periosteum away from edges, and an etched
surface appearance. Similar features, interpreted as termite damage,
have recently been reported on bones from a late Pleistocene site
in Argentina (Pomi and Tonni, 2011). Our interpretation of traces
recorded on the fossil remains discussed here are preliminary, based on
a‘best fit’comparative approach with known termite damage. We do
not yet know how ants modify bone, so cannot exclude them as the
agent responsible for the marks. Ongoing research on bone modifica-
tion by ants, cockroaches, millipedes, snails and other invertebrates
associated with the decomposition and burial process aims to establish
criteria for the identification of the various trace makers at a macro and
microscopic scale, discuss how they impact a faunal assemblage, the
implications they may have for interpreting site formation processes,
and their potential as palaeoenvironmental indicators.
5. Conclusion
The most widely distributed and most common termite species in
southern Africa, Trinervitermes trinervoides, has been shown to modify
bone in a characteristic manner. All experimental bones analysed
bear one or more macro- and microscopic surface modifications that
include star shaped marks, clusters of sub-parallel striations, surface
pits, multiple parallel incisions along edges, boreholes, destruction of
bone, and etching of the outer cortical lamellae associated with
surface residue. This experiment has demonstrated that T. trinervoides
can destroy bone in all stages of preservation, favouring fresh thin
cortical and spongy epiphyseal bone with meat and marrow. The role
of termites as modifiers and destroyers of bones at all stages of
preservation, from fleshed to fossilised, is generally not considered by
researchers working on Plio-Pleistocene and younger cave deposits. A
cursory analysis of faunal remains from four geographically dispersed
MSA and LSA cave sites in sub-Saharan Africa show that many pieces
have been modified by termites. Analysis of potentially worked bone
and some associated faunal remains from Sibudu, Plovers Lake, Porc
Epic and Jubilee shows that of the relatively few specimens analysed,
those recording insect damage include rare hominin remains and
bone artefacts. The presence of appreciable quantities of calcium
carbonate in termite mounds in Equatorial Africa suggests that
termites may be drawn to dolomitic cave sites and the calcium-rich
bones they contain to satisfy their mineral requirements. A prefer-
ence for fresh bone with meat and marrow and evidence of boring
unrelated to pupation, suggests that in addition to providing calcium
and other trace elements, like harvesting ants, bones are consumed
for their protein and lipid content. The dark residue recorded on all
specimens used in the experiment warrants further investigation. It
appears to be saliva or faecal rich material produced by the termites,
with a pH and chemical composition that negatively affects the
structural integrity of bone. In T. trinervoides, bone modification
intensity appears to be correlated with seasonality (humidity and
temperature), with increased activity during autumn and spring.
Termite activity may thus account for the patchy distribution of bone
preserved in cave deposits, as well as an absence of fossil fauna and
organic artefacts at a site, whether resulting from destruction of bone
through foraging, or dissolution caused by termite secretions and/or
increased soil porosity. As pre- and post-depositional modifiers of
bone, termites have the potential to bias taxonomic and element
representation, minimum number of individuals, and age profiles in
fossil faunal assemblages.
Acknowledgements
We dedicatethis paper to the memory of J.A.L. (Tony) Watson, who
recognised the potential impact of termites on fossil remains in cave
contexts, and pioneered actualistic research on the effects of insects on
bone. We thank Michael Lenz of CSIRO Entomology in Canberra,
Fig. 12. Type and percentage of modification observed on bones with different densities after six and 12 months.
85L.R. Backwell et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 337–338 (2012) 72–87
Australia, for his assistance in accessing Watson's archived photo-
graphs. The Entomological Society of America and Oxford University
Press kindly permitted the reproduction of previously published
images. The South African Weather Service provided data on precipi-
tation and temperature. We are grateful to the Nash family for allowing
us to conduct the experiment on their land, and to their farm manager,
Hennie Visser for facilitating the study. We thank Christine Steininger
of the Bernard Price Institute for Palaeontological Research for provid-
ing unprovenienced fossil specimens from Gladysvale Cave for the
experiment, and Michael Witcombof the Microscopy and Microanalysis
Unit at the University of the Witwatersrand for his assistance in viewing
specimens. Our thanks also go to Zelalem Assefa and Jonas Beyene for
helpful discussions, the Ethiopian authorities for giving us access to the
Porc Epic material, and the Italian Embassy in Addis Ababa for facili-
tating the stay of one of us (FD) there. We thank the reviewers for their
useful comments and suggestions, and Fernando Abdala for correcting
the final version of the manuscript. This research was funded by grants
from the South African National Research Foundation (NRF Thuthuka,
Women in Research) and the University Research Office of the
University of the Witwatersrand awarded to Lucinda Backwell, and to
Alexander Parkinson by the Palaeontology Scientific Trust, and the
University of the Witwatersrand in the form of a Postgraduate Merit
Award. Francesco d'Errico acknowledges financial support from the
European Research Council (FP7/2007/2013)/ERC Grant TRACSYMBOLS
n°249587).
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