Professional Documents
Culture Documents
James L. Hayward
a
*, Kristin M. Dickson
b
, Susan R. Gamble
c
, Adam W. Owen
d
and Kimberly C. Owen
e{
a
Department of Biology, Andrews University, Berrien Springs, MI 49104, USA;
b
Emory University Psychiatry and Behavioral Sciences,
Tufts House, Suite 218, 2004 Ridgewood Dr, Atlanta, GA 30322, USA;
c
Department of Internal Medicine, Yale School of Medicine,
Residency Training Programs, P.O. Box 208030, New Haven, CT 06520, USA;
d
Central Maine Pain and Headache Center, 10 Minot
Avenue, Auburn, ME 04210, USA;
e
Central Maine Medical Center, 300 Main St., Lewiston, ME 04240, USA
(Received 27 May 2010; nal version received 3 June 2010)
Dinosaur eggshell is abundant in the fossil record but only during the last several decades has this reproductive product been
considered more than a novelty. Recent work has provided evidence that both whole eggs and fragmented eggshell represent a
rich source of information related to paleoecology and dinosaur reproductive biology. In this paper, we report the effects of
environmental variables on modern eggshell fragment orientation. Non-transported eggshell fragments at hatching and
predation sites favoured concave-up over concave-down orientations. Trampled fragments and fragments transported by
wind and water favoured concave-down over concave-up orientations. Although differences in orientation between non-
transported and transported eggshell fragments were usually obvious and signicant under the chosen experimental
conditions, paleontologists are cautioned to interpret the taphonomy at fossil eggshell sites with care and within their
sedimentological context.
Keywords: dinosaur; eggshell; experiments; taphonomy; transport
Introduction
Dinosaur eggshell is abundant in the fossil record but only
recently has this reproductive product been considered a
valuable source of information. Whole fossil eggs and egg
clutches are the most exciting discoveries of this type and
have yielded spectacular insights into the lives of the
animals that produced them (Carpenter et al. 1994;
Carpenter 1999). Recent experimental work has demon-
strated, however, that even fragmented eggshell contains a
wealth of paleoecological information.
Dinosaurs, like modern birds, laid eggs with brittle
calcitic shells. The shells of theropod dinosaurs consisted
of at least two structural layers (Mikhailov et al. 1996;
Mikhailov 1997; Zelenitsky et al. 2002). Some theropods,
like some birds, appeared to nest in colonies (Carpenter
1999), laid their eggs in rimmed nests located on the ground
(Horner 1982; Varricchio et al. 1997; Chiappe et al. 2004)
and apparently brooded or protected their eggs by covering
them with their bodies (Norell et al. 1995; Varricchio et al.
1997; Clark et al. 1999). Dinosaur eggshell was subject to
fragmentation by hatching and predation, transport by wind
and water and alteration by trampling and weathering just
like modern avian eggshell. Thus, taphonomic processes
affecting modern avian eggshell can serve as useful
analogues to processes inuencing ancient dinosaur
eggshell (Hayward et al. 2000).
The bowl-like shape of eggshell fragments, like that of
bivalve shells (Clifton and Boggs 1970), is subject to
physical forces that inuence resting orientation patterns.
An understanding of these patterns holds promise for
increasing our understanding of eggshell paleoenviron-
ments and transport processes (Hayward et al. 1997, 2000).
Here, we report a series of observations and experiments
designed to provide insight into what eggshell fragment
orientation concave surface up or down can provide
regarding taphonomic factors impinging on dinosaur
eggshell. Specically, we test the null hypothesis that
hatching, post-hatching trampling, predation and transport
in a wind tunnel, ume and natural stream lead to 1:1 ratios
of concave surface up and down orientations of eggshell
fragments.
Previous work
To place our study in context, we rst review the small
number of previously published studies in experimental
eggshell taphonomy.
ISSN 0891-2963 print/ISSN 1029-2381 online
q 2011 Taylor & Francis
DOI: 10.1080/08912963.2010.499170
http://www.informaworld.com
*Corresponding author. Email: hayward@andrews.edu
Email: kristin.dickson@gmail.com
Email: susan.gamble@yale.edu
Email: adamowen33@hotmail.com
{
Email: kimcso@hotmail.com
Historical Biology
Vol. 23, No. 1, March 2011, 513
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Early motivation for experimental eggshell taphonomy
was provided by the 18 May 1980 eruption of Mount St.
Helens, Washington. This event buried an entire nesting
colony of ring-billed and California gulls (Larus
delawarensis and L. californicus) 1 day before the onset
of hatching (Hayward et al. 1982). One year later, entire
clutches of desiccated ring-billed gull eggs were found
buried beneath the ash (Hayward et al. 1989). Structural
features of fresh eggshell and eggshell buried beneath the
ash for 1 year and 7 years were compared and the results
demonstrated rapid corrosion by the acidic ash (Hayward
et al. 1991).
Carpenter (1982) discussed the effect of local pHon the
preservation potential of dinosaur eggshell and found that
in 60 days acids produced by decaying vegetation
dissolved the broken edges of chicken eggshell fragments.
Clayburn et al. (2004) examined this effect further, along
with that of temperature, in controlled experiments with
glaucous-winged gull (L. glaucescens) eggshell fragments.
Treatment in buffered solutions of varying pH and
temperature for up to 42 days resulted in corrosion and
pitting of the outer surface and corrosion on the
mammillary layer of the inner surface. Fragment mass,
surface area and thickness decreased in response to
decreased pH and increased temperature and exposure
time. Similarly, Smith and Hayward (2010) inoculated
sterile glaucous-winged gull eggshell fragments in sterile
soil with bacteria isolated from eggshell on the surface of
the nesting colony. Over a 10-week period, eggshell protein
concentration declined, soil calcium concentration
increased and eggshell corrosion patterns similar to those
seen in naturally weathered eggshell appeared.
Horner (1994) reported a study of bone and eggshell
distributions at colonies of American white pelicans
(Pelecanus erythrorhynchos), double-crested cormorants
(Phalacrocorax auritus) and various species of gulls. He
noted that colony surfaces were littered with juvenile
bones and carcasses but that none of the remains were
from adults. Similarly, Hayward et al. (2000) analysed
bone, mollusc shell and eggshell fragment distributions on
the surface of a glaucous-winged gull (L. glaucescens)
colony. Approximately 4 weeks after the time of hatching,
eggshell fragment densities were signicantly higher close
to nests than further away, but this was not true for bones
and mollusc shells. Weathering of gull eggshells, placed
on the colony surface in an exclosure which prohibited
disturbance by colony residents, was followed for 2 years.
Within 1 week, shrinking membranes detached from the
inner surface of the shells and precipitated fragmentation.
After 1 year, some of the membranes were still present but
had changed colouration, as had the outer shell surfaces.
After 2 years, membranes and shell inner surfaces were
coated with unicellular green algae. Hatched and predated
eggshell could be distinguished on the basis of the fracture
patterns.
Soja et al. (2004, 2005) and Soja (2008) carried out
burial experiments with infertile ostrich, emu (Dromaius
novaehollandiae), chicken (Gallus gallus) and alligator
(Alligator mississippiensis) eggs. Extensive fractures
developed across the surface of many eggs, the shells of
which were held together by the inner shell membrane.
Sediment ltered into eggs with fractured shells and
replaced the soft contents after it had drained away. The
sediment prevented further collapse of the shell, thus
increasing its fossilisation potential. Holes and depressed
features in some buried specimens were similar to
holes interpreted as hatching windows in some dinosaur
eggs, suggesting the importance of caution when interpret-
ingthese openings infossil specimens. Scavengers removed
over two-thirds of the eggs at one of the burial sites.
The impact of high temperatures on eggshell, as might
have been experienced during wildres (Wolbach et al.
1988; Scott et al. 2000), was explored by Janssen and
Hayward (2006). Ostrich (Struthio camelus) and glaucous-
winged gull eggshell fragments were heated to temperatures
up to 8508C for various lengths of time. A series of dramatic
colour changes, similar to those reported for conodonts
(Epstein et al. 1977), began to occur at about 2008C.
Reverse curling of eggshell was observed at temperatures
above 6008C. Thermogravimetric analysis showed a
negligible decrease in mass below 2008C, attributable to
water loss, but sharp decreases in mass occurred at about
7108C for both types of eggshell. The remaining CaO
residue represented 55% of the original mass.
Tokaryk and Storer (1991) demonstrated that eggshell
could be transported great distances in simulated uvial
systems without signicant damage. Hayward et al. (1997)
showed that whole chicken eggs were readily recruited
into the sea by rising tides. Fresh eggs rolled along the
benthic surface; simulated incubated eggs, which were less
dense, oated out to sea (see also Schafer 1972). Eggs
placed on the subtidal benthic surface accumulated
epibiont loads and by 44 days were partially buried by
sediment. When lowered to a depth of 626 m in the Pacic
Ocean, fresh chicken eggs withstood hyperbaric pressures
of 62 atmospheres without cracking or breakage.
Methods
In each section below, eggshell fragment orientation
refers to whether the concave surfaces of horizontally
positioned fragments were facing up concave up, or facing
down, concave down. Following each treatment, most
fragments assumed an unambiguously horizontal position;
thus, only horizontally positioned fragments were counted.
Means are reported with standard deviations (^SD), and all
statistical tests were carried out at the 0.05 level of
signicance. Table 1 summarises the observations and
experiments reported, and Figure 1 illustrates the range of
eggshell fragment sizes used in the transport experiments.
J.L. Hayward et al. 6
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Fragment orientation at hatching sites
On 7 July 2004 on the Protection Island National Wildlife
Refuge, Jefferson County, Washington, orientations of
eggshell fragments in 12 glaucous-winged gull (L.
glaucescens) nest cups in which all chicks had hatched
were determined and compared against the null prediction
of a 1:1 ratio using a chi-square test.
Twelve fertile domestic chicken eggs were obtained
from Town Line Poultry Farm, Zeeland, Michigan. Eggs
(mean length 55.5 ^ 1.53 mm; mean width 43.0 ^
1.04 mm) were incubated at 398C in an incubator with an
automatic egg turner. Just prior to the estimated time of
hatching (21 days post-laying), each egg was singly placed
in the centre of a circular cardboard arena, 33 cm in
diameter, 28 cm tall and with a sand-covered base. As soon
as hatching was complete, the chick was removed from the
arena without disturbing the eggshell fragments, and
fragment orientations for all arenas were determined and
compared against the null prediction of a 1:1 ratio using a
chi-square test.
Fragment orientation at egg predation sites
On 7 July 2004, orientations of glaucous-winged gull
eggshell fragments were determined at four egg cannibal
(Hayward et al. 2000) territories on the Protection Island
colony. Stolen eggs at such territories were transported
there whole by the cannibals, and then broken and the
contents devoured. Likewise, on 2 July 2004, orientations
of glaucous-winged gull eggshell fragments were deter-
mined at 10 sites where bald eagles (Haliaeetus
leucocephalus) had preyed on glaucous-winged gull eggs
on the Protection Island colony. These sites occurred in the
immediate vicinity (,2 m) of the predated gull nests
where the eggs had been broken into and the contents
devoured. In each case, orientations were determined and
compared against the null prediction of a 1:1 ratio using a
chi-square test.
Fragment orientation after trampling by chicks
Four domestic chicks from the hatching experiment were
placed in a single arena, shaped as a half circle,
radius 50 cm, with a sand-covered base. One hundred
and twenty crushed chicken eggshell fragments of mixed
diameters were placed concave up on the surface of the
Figure 1. Range of chicken eggshell fragment sizes used in the
transport experiments. A United States 25-cent coin is shown for
scale. Dimensions refer to diameters.
Table 1. Summary of observations and experiments. Type of observation or experiment, total number of eggshell fragments counted in
the observation or included in the experiment and total number of fragments included in the data analysis for that observation or
experiment (i.e. fragments in an unambiguously horizontal position and therefore countable) are listed. Gull refers to glaucous-winged
gull (L. glaucescens) and Chicken and chick refer to domestic fowl (Gallus gallus).
Observation or experiment Fragments included Fragments counted
Hatching sites (gull and chicken eggshell)
Gull (12 nest sites) 145 145
Chicken (9 hatch sites) 220 220
Predation sites (gull eggshell)
Gull egg cannibal (4 sites) 629 629
Eagle predation on gull eggs (10 sites) 557 557
Chick trampling (chicken eggshell)
Initially concave up 120 99
Initially concave down 120 84
Wind tunnel transport (chicken eggshell)
Small fragments
Initially concave up 50 50
Initially concave down 50 50
Large fragments
Initially concave up 50 50
Initially concave down 50 50
Flume transport (chicken eggshell)
Initially concave up 30 30
Initially concave down 30 30
Natural stream transport (chicken eggshell)
Medium fragments (initial orientation random) 355 338
Half shells (initial orientation random) 50 23
Historical Biology 7
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sandy base. Chicks were provided with food and water and
allowed to move freely about the arena for 36 h, after
which they were removed. After chick removal, the
orientations of fragments were determined. The exper-
iment was repeated, except that 120 eggshell fragments
were initially placed concave down. A McNemar test for
signicance of change (Zar 1999; Berenson et al. 2005)
was used to test the null prediction that fragments in both
experiments showed no change in orientation as a result of
treatment.
Fragment transport in a wind tunnel
Transport experiments were conducted using a wind
tunnel 5.7 mm long and 18 cm wide with 26 cm high sides.
The top of the tunnel was covered with glass and the oor
was covered with dry, levelled sand. A squirrel cage fan
served as a wind source. A bafe made of stacked plastic
tubes 15.5 cm long and 3.2 cm in diameter was placed
between the fan and the tunnel to minimise turbulence.
The tunnel was marked at 10-cm intervals. Wind velocity
was measured with a Turbo Meter
TM
electronic wind
speed indicator (Davis Instruments Corp.) which averaged
to 8.2 m/s at the proximal end and 3.8 m/s at the distal end
of the tunnel.
Fifty small (diameter < 2.0 cm) and 50 large
(diameter < 3.7 cm) eggshell fragments were placed
concave up 2 cm in front of the fan bafe, two to four
at a time to avoid fragment collisions. After smoothing
the sand with a straight edge, the fan was turned on and
run for 15 s, after which distance from the starting
point was determined. The experiment was repeated
with each fragment initially placed concave down.
McNemar tests were used to test the null prediction that
fragments showed no change in orientation as a result of
treatment.
Fragment transport in a laboratory ume
Chicken eggshell fragments, 2.55.0 cm in diameter,
were experimentally transported in a Hydraulic Demon-
stration Channel, Model A-8 (Engineering Laboratory
Design, Inc.). In this device, water stored in a reservoir
could be pumped through a ume with transparent sides,
2.20 m long, 0.15 m wide and 0.3 m deep. To minimise
turbulence, water entered the channel through a cross-
section of tubular bafes constructed from stacked 1.27-
diameter PVC pipes 10 cm long. A segment of the channel
with the least turbulence, 90 cm long, was selected as the
working distance for the experiment. The eggshell release
point was located at the proximal end of the working
distance. During each experiment, water depth and tank
slope were maintained at 20 cm and 08, respectively.
Experiments were conducted at two water velocities
determined at the release point as 25 and 30 cm/s using a
Global Flow Probe
TM
FP101-FP-201 (Global Water
Instrumentation, Inc.).
Thirty fragments each underwent two experimental
runs, one initially concave up and the other initially
concave down. The smooth plastic substrate of the ume
channel was made rough by completely covering it with an
asphalt shingle. Before release, each fragment was
submerged and placed entirely on the rough substrate
with its front edge at the release point. Final fragment
orientation was determined once the fragment reached the
end of the working distance. The shingle was then
removed and the experiment was repeated with only the
smooth substrate of the ume channel. McNemar tests
were used to test the null prediction that fragments in
both experiments showed no change in orientation as a
result of treatment.
Fragment transport in a natural stream
Pieces of crushed chicken eggshells were divided into two
categories: fragments .11 mm, n 355 and half shells,
n 50. On 12 September 1996, these samples were
released in mass beneath the waters surface in Lemon
Creek, Berrien County, Michigan, 0.5 km upstream from
where the creek enters the St. Joseph River. Water depth
ranged from 5 to 30 cm; ow rates (measured with a
Global Flow Probe
TM
) ranged from 15 to 45 cm/s.
The nal distributions of eggshell fragments and half
shells were determined at least 6 days later by
positioning a 1-m
2
steel grid with sixteen 0.0625-m
2
quadrants on the benthic surface at increasing distances
downstream from the release point until no eggshell was
observed. Eggshell fragments within each quadrant were
viewed through the bottom of an empty 1.5-litre beaker
pushed below the waters surface. Buried fragments were
exposed by gently disturbing the surface sediment.
Fragment and half shell orientations were determined and
compared against the null prediction of a 1:1 ratio using
chi-square tests.
Results
Fragment orientation at hatching sites
In the 12 glaucous-winged gull nests, 145 eggshell
fragments (