Physiological and life history strategies of a fossil large mammal in a resource-limited environment

Abstract

Because of their physiological and life history characteristics, mammals exploit adaptive zones unavailable to ectothermic reptiles. Yet, they perform best in energy-rich environments because their high and constant growth rates and their sustained levels of resting metabolism require continuous resource supply. In resource-limited ecosystems such as islands, therefore, reptiles frequently displace mammals because their slow and flexible growth rates and low metabolic rates permit them to operate effectively with low energy flow. An apparent contradiction of this general principle is the long-term persistence of certain fossil large mammals on energy-poor Mediterranean islands. The purpose of the present study is to uncover the developmental and physiological strategies that allowed fossil large mammals to cope with the low levels of resource supply that characterize insular ecosystems. Long-bone histology of Myotragus, a Plio-Pleistocene bovid from the Balearic Islands, reveals lamellar-zonal tissue throughout the cortex, a trait exclusive to ectothermic reptiles. The bone microstructure indicates that Myotragus grew unlike any other mammal but similar to crocodiles at slow and flexible rates, ceased growth periodically, and attained somatic maturity extremely late by approximately 12 years. This developmental pattern denotes that Myotragus, much like extant reptiles, synchronized its metabolic requirements with fluctuating resource levels. Our results suggest that developmental and physiological plasticity was crucial to the survival of this and, perhaps, other large mammals on resource-limited Mediterranean Islands, yet it eventually led to their extinction through a major predator, Homo sapiens.

Full text

Physiological and life history strategies of a fossil
large mammal in a resource-limited environment
Meike Ko
¨hler
1,2
and Salvador Moya
`-Sola
`
1
Catalan Institute for Research and Advanced Studies, Catalan Institute of Paleontology, Autonomous University of Barcelona, 08193 Bellaterra, Spain
Edited by Paul E. Olsen, Columbia University, Palisades, NY, and approved October 2, 2009 (received for review January 2, 2009)
Because of their physiological and life history characteristics, mam-
mals exploit adaptive zones unavailable to ectothermic reptiles.
Yet, they perform best in energy-rich environments because their
high and constant growth rates and their sustained levels of rest-
ing metabolism require continuous resource supply. In resource-
limited ecosystems such as islands, therefore, reptiles frequently
displace mammals because their slow and flexible growth rates
and low metabolic rates permit them to operate effectively with
low energy flow. An apparent contradiction of this general prin-
ciple is the long-term persistence of certain fossil large mammals
on energy-poor Mediterranean islands. The purpose of the present
study is to uncover the developmental and physiological strategies
that allowed fossil large mammals to cope with the low levels of
resource supply that characterize insular ecosystems. Long-bone
histology of Myotragus, a Plio-Pleistocene bovid from the Balearic
Islands, reveals lamellar-zonal tissue throughout the cortex, a trait
exclusive to ectothermic reptiles. The bone microstructure indi-
cates that Myotragus grew unlike any other mammal but similar to
crocodiles at slow and flexible rates, ceased growth periodically,
and attained somatic maturity extremely late by ⬇12 years. This
developmental pattern denotes that Myotragus, much like extant
reptiles, synchronized its metabolic requirements with fluctuating
resource levels. Our results suggest that developmental and phys-
iological plasticity was crucial to the survival of this and, perhaps,
other large mammals on resource-limited Mediterranean Islands,
yet it eventually led to their extinction through a major predator,
Homo sapiens.
islands 兩artiodactyl 兩paleohistology 兩growth rate 兩metabolism
Energy availability is a key factor in the evolution of physio-
logical and life history strategies of organisms. Therefore,
much interest has recently been shown in the ecophysiological
adaptations of vertebrates endemic to ecosystems with low
energy f lux (1). Ectotherms, although frequently thought of as
primitive (2), are actually specialists in coping with low levels of
available energy (3, 4). Ectotherm vertebrates have slow and
flexible growth rates and a notable physiological plasticity, which
allows a close matching of their energy requirements to prevail-
ing resource conditions (3, 5, 6). Endotherms, instead, typically
have high and steady growth rates and a constant thermometa-
bolic regime, and they depend on high and continuous food
intake to maintain their elevated metabolism (7). Therefore, in
environments such as islands, where resource bases are narrow
and resource availability is unpredictable (1), reptiles frequently
replace mammals (8, 9).
Certain mammals, however, were dominant faunal elements
on Mediterranean islands, where they persisted for long time
periods, some of them over millions of years (10). This is
particularly perplexing in the case of insular dwarf mammals
such as elephants, deer, and hippos, which should be expected to
have even higher resource requirements than small mammals
because of the scaling of metabolic rate with body mass. Un-
surprisingly, therefore, hypotheses aimed to explain the evolu-
tion of dwarfism and gigantism on islands (the Island Rule) (11)
traditionally evoked resource availability as the driving force
behind these, often dramatic, changes in body size (8, 9). More
recently, however, several studies drew attention to the tight
correlation between body size and life history traits, suggesting
that not body size itself but fitness-related life history traits were
the chief goal of selection on islands (12, 13). Thus, it has been
argued that dwarfing is a corollar y of selection for an increase
in production rate in low-mortality environments (12–15)
through an increase in growth rate (14) and a decrease in age at
maturity (14, 15). This contrasts with a model that predicts shifts
in adult body size in function of the magnitude of adaptive
changes in growth rate and age at maturity in response to
resource availability and extrinsic mortality (16). For environ-
ments such as islands, where resources are scarce and extrinsic
mortality is low, this model predicts a decrease in adult body size
through a decrease in growth rate, associated to an increase in
age at maturity (16). Data that might provide empirical support
for any of these essentially theoretical approaches, however, are
scarce and come from observations on small extant vertebrates
only (see ref. 16 for a more comprehensive review), because
almost all large insular mammals went extinct following human
settlement (1). The only way to reconstruct the physiological and
life history strategies of dwarfed insular mammals, hence, is the
study of their fossil remains. Myotragus, a dwarf bovid from the
Plio-Pleistocene of Majorca (Balearic Islands, Spain), is partic-
ularly suitable for this purpose because it evolved under known
selective pressures (chronically low resource levels and lack of
predators) (10, 17) in a completely isolated ecosystem, condi-
tions that closely resemble experiments on natural populations
but at a timescale that only the fossil record can provide.
Physiological and life history strategies of fossil vertebrates are
recorded in their hard tissues. Long-bone tissues of slow and
flexibly growing ectotherms and fast and constantly growing
endotherms differ substantially. Ectotherms are characterized
by lamellar-zonal bone throughout the cortex. This bone is
formed in a periodic manner whereby the deposition of lamellar
(parallel-fibered) bone (18, 19) cyclically comes to a halt. These
seasonal pauses in bone formation are recorded in the bone
tissue as growth rings or lines of arrested growth (LAGs)
(20–22). Endotherms are characterized by uninterrupted
(azonal) fast growing fibrolamellar tissue throughout the cortex
and a thin outer cortical layer (OCL) of slow growing lamellar
bone deposited after attainment of somatic/sexual maturity (21,
23, 24). LAGs, if present, appear near the periosteum in the OCL
(21, 23). An ‘‘intermediate’’ pattern, the fibrolamellar-zonal
complex (25) composed of alternating zones of fibrolamellar
tissue and LAGs, can be observed in extinct tetrapods only
(dinosaurs and nonmammalian therapsids) (24, 25). Fossil evi-
dence indicates that fast and uninterrupted growth has been
acquired independently by birds and mammals (21). The capa-
Author contributions: M.K. designed research; M.K. performed research; M.K. and S.M.-S.
analyzed data; and M.K. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Freely available online through the PNAS open access option.
1M.K. and S.M.-S. contributed equally to this work.
2To whom correspondence should be addressed. E-mail: meike.kohler@icrea.es.
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bility to stop growth periodically is therefore considered to be a
plesiomorphic trait reflecting an intermediate physiological con-
dition (20) that has been lost in modern vertebrates (20, 24) or
is simply a phylogenetic legacy (26).
Results
Ontogenetic Stages of Bone Tissue. Our descriptions of bone tissues
of Myotragus are based on the typological classification estab-
lished by de Ricqle`s (ref. 18; see also ref. 19). Thin sections from
an ontogenetic series of 57 long bones of Myotragus reveal that
the primary bone tissue consists of zonal bone throughout (Fig.
1A,C,E, and F; Fig. 2 B–E), comparable to that of crocodiles
(compare Fig. 1 Band D). LAGs appear as simple (Fig. 1 A,E,
and F), double, or even triple rest lines (Fig. 2 B–E). They are
spaced fairly homogeneously throughout the cortex (Fig. 2C). In
older individuals, LAGs are closer spaced the more they ap-
proach the periosteal surface (Fig. 1 A), indicating that growth
rate decreased with age. At an early ontogenetic stage (Figs. 1 F
and 2B), fibrolamellar-zonal (23) tissue or lamellar bone with
primary osteons (LPO) prevails, alternating with annuli of
lamellar nonvascular bone (LNV) with f lattened osteocytes and
LAGs (Fig. 2 Band D). Vascularization is moderate with an
essentially circumferential orientation of the channels. Early
remodeling becomes manifest at the inner medullary sur face
(erosion of innermost primary tissue and deposition of inner
circumferential layers, first Haversian systems) (Figs. 1Fand
2B). The primary bone pattern of this early ontogenetic stage
indicates a moderately rapid rate of bone deposition interrupted
by low rates of bone deposition and growth arrest. It sharply
contrasts with the early ontogenetic stage of other bovids (here
Gazella borbonica, Fig. 1I), which is characterized by an azonal
fibro-lamellar complex (FLC) throughout the cortex deposited
Fig. 1. Micrographs of long bone tissues. (A)Myotragus balearicus (IPS 44929; entire section through cortical wall), adult distal tibia with completely fused
epiphysis, 11 lines of arrested growth (LAGs), some Haversian systems. (B) Crocodile (IPS 4913, Eocene, Spain; entire section through cortical wall), adult femur.
Observe the similarities with Myotragus (A) in the spacing of growth lines. (C)M. balearicus (IPS 44923c), subadult tibia, annuli (bars) interrupting FLC and LPO
bone. (D) Crocodile gen. et sp. indet. (IPS 4930-h, Eocene, Spain), proximal femur with alternating lamellar annuli and fibrolamellar zones. (E)M. balearicus (IPS
44929), complete tibia with alternating LAGs, lamellar annuli, and fibrolamellar zones (elongated vascular channels, red). Note the resemblances with crocodile
(D). (F)M. balearicus (IPS 26158-1), very tiny humerus of ⬇4-cm length, FLC bone, one LAG (yellow arrowhead), two generations of endosteal bone (white
arrowheads). (G) Cervid gen. et sp. indet. (IPS 3811-f, Pleistocene, Spain), adult distal tibia with completely fused epiphysis. Densely vascularized FLC tissue is
shown with alternating formation of radial, concentric, and irregular oriented channels and one isolated LAG (arrowhead). Compare with the almost nonvascular
zonal bone of Myotragus (E). (H)Gazella borbonica (IPS 26760-c, Pliocene, Spain), adult proximal femur with uninterrupted FLC bone. Compare with the zonal
bone of adult Myotragus (E). (I)G. borbonica (IPS 26780, Pliocene, Spain) juvenile distal femur without epiphysis. Loosely formed azonal tissue of FLC type is shown
with rounded osteocytes. Compare with the more compact and organized bone with flattened osteocytes and advanced remodeling of juvenile Myotragus (F).
Periosteal surface is shown in all micrographs at lower left (left in Aand B). (Aand B) Transmitted light; (C–Eand G–I) polarized light with 1
␭
filter; (F) circularly
polarized light. (Aand B) are composed of various micrographs. (Scale bars: Aand D–I, 200
␮
m; B, 1,000
␮
m; C, 100
␮
m.)
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during uninterrupted fast growth. At a later juvenile stage (Fig.
2Cand E), alternating LNV and LPO bone becomes predom-
inant and vascularization decreases. Equidistant LAGs embed-
ded in LNV tissue with f lattened osteocytes (annuli) denote that
growth slowed down and ceased periodically. Haversian systems
become increasingly abundant throughout the inner half of the
cortex. Older individuals (Fig. 1 E) show very slow growing
lamellar-zonal bone in which nonvascular annuli (LNV) and/or
LAGs alternate with poorly vascularized zones (LNV/LPO)
throughout cortex. This pattern of bone microstructure is fre-
quent among wild alligators (27) (compare Fig. 1 Band D), but
contrasts with the presence of fast growing fibrolamellar bone
(FLC) throughout the cortex in other artiodactyls (here adult G.
borbonica, Fig. 1H, and adult Cervus indet., Fig. 1G). None of the
Myotragus specimens available for sectioning shows a distinct
OCL that might indicate a rather abrupt onset of somatic
maturity and/or sexual maturity as in other mammals. Instead,
some of the specimens simply show an increasingly closer spacing
of LAGs toward the outer cortex, a trait that characterizes
crocodiles but not mammals (compare Fig. 1Awith Eocene
crocodile, Fig. 1B). Table 1 summarizes the main histological
traits of Myotragus in comparison with the bone microstructure
of crocodiles and large mammals.
Skeletochronology. Skeletochronology is consistent with the slow
and variable-rate growth pattern deduced from the long-bone
tissue. The earliest ontogenetic stage available for sectioning is
a very tiny and immature humerus without epiphyses (IPS
26158–1, length ⬇4 cm; Fig. 1F). The tissue consists largely of
FCL with longitudinal and circular osteons, although at the
middle of the bone wall the tissue is more compact and of LPO
type. Two clearly distinguishable generations of endosteal bone
are deposited along the medullary cavity. At the periosteum, one
LAG is observable followed by a thin annulus and, most periph-
erally, by FLC tissue, indicating that the individual resumed
growth after the unfavorable season but died shortly after at the
age of somewhat more than 1 year. A small proximal femur
without epiphysis (IPS 26444e; Fig. 2 Ab,B, and D) shows FLC
bone around the medullary cavity followed by LPO and LNV
bone. Erosion is observable along the medullar y cavity and some
Haversian systems are scattered over the inner bone wall. At the
middle of the bone wall there is a double LAG embedded in
lamellar (LNV) annuli with f lattened osteocytes, followed by
alternating LPO/LNV bone. This tissue indicates that the indi-
vidual recovered a faster growth rate after a period of slow
growth and growth arrest. Age at death, hence, was at ⬇2 years.
A slightly larger immature femur (IPS 26324, Fig. 2Ac) that still
lacks epiphyses, trochanter major, and trochanter minor shows
little vascularized primary tissue of LPO type throughout. It
presents two LAGs, large erosion cavities on the inner cortical
(medullary) surface, endosteal bone, and more extensive Hav-
ersian remodeling, providing a minimum age of almost 3 years.
We found a similar tissue pattern with two LAGs in a similar-
sized humerus without epiphyses (IPS 26430). A minimum of six
LAGs has been observed in a tibia of only two-thirds the size of
a fully grown tibia in which the proximal epiphysis is not
completely fused (IPS 44923-c), providing a minimum age of 7
years. Seven LAGs and, hence, a minimum age of close to 8
years, correspond to a juvenile femur of nearly adult size that still
lacks both proximal and distal epiphyses and that shows an initial
fusion of the trochanter major (IPS 26321; Fig. 2 Ad,C, and E).
The primary bone largely consists of LNV tissue type; LAGs are
mostly double or triple. Haversian systems invaded the inner
cortical wall, and erosion and formation of endosteal bone along
the medullary cavity are advanced. The presence of a minimum
of 11 LAGs in fully grown individuals with epiphyses completely
or almost completely fused (Fig. 1 A, IPS 44929) denotes that
Myotragus grew for at least 12 years before it attained skeletal/
sexual maturity, more than sixfold the time of bovids of similar
body mass (28) and even longer than large males of highly
dimorphic Bison, which stop somatic growth at 7 years (29).
Discussion
The peculiar bone histology of Myotragus provides direct evi-
dence of the developmental and growth strategy and indirect
evidence regarding the physiology of this insular dwar f mammal.
The presence of lamellar-zonal bone throughout the cortex
indicates that Myotragus grew at slow and variable rates and
ceased growth cyclically, which was associated with an important
delay in the attainment of skeletal (sexual) maturity. Consistent
with life history theory (30), the extended juvenile development
of Myotragus was associated with an extended life span as
indicated by the elevated number of very old individuals in the
fossil assemblages (10). Our empirical finding, hence, does not
support the prediction that life history traits of insular dwarfs
Fig. 2. Growth series for three aged femora and micrographs of their
sections. (A) Growth series of femora from the smallest juvenile (a, gray dot;
mbcn7160) to a large adult individual (e, gray dot; mbcn7260) [logarithmic
regression of anterior–posterior diameter (DAP) against transversal diameter
(DT) at midshaft]. Sectioned specimens (red dots) provided ages of 2 (b, IPS
26444e), 3 (c, IPS 26324), and 8 (d, IPS 26321) years. Note the surprisingly small
size at 2 and 3 years. (Scale bar, 10 cm.) (B) Section through cortical wall of IPS
26444e (femur in Ab) with a double LAG (arrowhead) in the central cortical
wall, embedded in LNV annuli. Bone tissue is of FLC type close to the medullary
cavity and of LPO type before and after the annuli. (C) Section through cortical
wall of IPS 26321 (femur in Ad) with seven LAGs (arrowheads). Their regular
distances and their presence only on the central cortex suggest that there
might have been more LAGs that have been deleted by microbial attack (dark
clouds) and remodeling; Haversian systems (red) scattered throughout inner
cortex; erosion and endosteal bone surrounding medullary cavity. (D) Higher
magnification of IPS 26444-e-1 (femur in Ab) showing the double LAG em-
bedded in LNV tissue with flattened osteocytes. (E) Higher magnification of
IPS 26321 (femur in Ad) showing multiple LAGs embedded in LNV tissue with
flattened osteocytes. (Scale bars: Band C, 500
␮
m; Dand E, 100
␮
m.) Cis
composed of multiple micrographs.
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accelerate to increase reproductive investment (12–15), but
instead lends support to the model that predicts a shift in life
history traits toward the slow end of the slow–fast continuum
with a delay in age at maturity and an extended life span (16).
True zonal bone with growth marks deposited seasonally
throughout ontogeny is a general ectotherm characteristic (20).
In ectotherms, the bone matrix consists of slow growing lamellar
bone (LNV, LSV, LPO). However, cyclically interrupted fast
growing fibrolamellar bone (fibrolamellar-zonal complex, ref.
25) has been found in many dinosaur taxa, in basal birds (20, 31)
and in nonmammalian therapsids (24), leading to an ongoing
controversy over whether zonal bone indicates an intermediate
physiological condition along the transition between poikilo-
thermic ectothermy and homeothermic endothermy (20) or
whether it merely represents the ghost of past physiologies (26).
Inferences about the physiologies of these extinct vertebrate
groups, however, remain conjectural because they do not have
living equivalents. Our finding of true lamellar-zonal bone in a
fossil representative of phylogenetically modern mammals,
hence, may shed some light on the physiological correlates of
zonal bone.
Ungulates, like other endotherms, are characterized by azonal
fast growing bone tissue and a thin outer cortical layer that may
contain several grow th lines. Sporadically, a single, isolated LAG
has been observed within the fast growing fibrolamellar bone of
cervids (23, 26) (see also Fig. 1G). The occasional presence of
LAGs in these large endothermic (nonhibernating and nones-
tivating) mammals led some (26) to conclude that such growth
lines reflect phylogenetic legacy rather than a physiological
response to environmental cycles or stresses. Nevertheless, ev-
idence is accumulating that certain ungulates significantly re-
duce endogenous heat production to cope with energetically
challenging situations (food shortage, harsh climatic conditions)
(32). Thus, seasonal fluctuations in metabolic rate and in body
temperature (heterothermy) have been described for ungulates
with a winter nadir in northern species (32–34) and with a
summer nadir in desert species (35, 36). Taking into account
these recent advances in ungulate physiology, the zonal bone of
Myotragus quite likely reflects seasonal fluctuations in metabolic
rate and/or body temperature over an extended juvenile period
in response to fluctuating resource conditions on the island.
Insular ecosystems are intrinsically resource limited (1, 8, 9,
16, 37) because their limited landmass can support only a limited
number of primary producers, which in turn affects the energy
flow at higher trophic levels. Therefore, energy-poor islands are
depauperate in competitors and predators (8, 9). Under these
conditions, the pivotal achievements of endothermy—(i) sus-
tained aerobic capacities (7), (ii) an enhanced behavioral rep-
ertoire (7), (iii) high growth rates (38), and (iv) high reproductive
rates (38)—are not only dispensable but the elevated metabolic
rate to fuel these activities is also incompatible with the low
insular resource bases. Therefore, insular endotherms should be
expected to reduce these expensive traits. Indeed, among extant
birds and mammals, small-island endemics have lower basal
metabolic rates than their continental counterparts (8, 9, 39),
whereas heterothermic small mammals such as dormice were
dominant faunal elements in the fossil record of Mediterranean
islands (10).
Majorca was such a resource-poor island, which is evidenced
by nutrition-related malformations and other symptoms of star-
vation and undernourishment in fossil endemic populations (10),
as well as by the low species diversity and the absence of
predators (10). In agreement with the reasoning given above,
Myotragus not only decreased aerobic capacities (low-gear loco-
motion) (40) and behavioral traits (reduction of brain and sense
organs) (41) but also flexibly synchronized growth rates and
metabolic needs to the prevailing resource conditions as do
ectothermic reptiles. Our present study, hence, provides evi-
dence that in energy-poor environments where reptiles usually
replace mammals, selection for energy saving may be so impe-
rious that mammals may revert to some ectotherm-like state that
includes both physiological and developmental plasticity. Com-
pletely unexpected, this reversal is possible even in large mam-
mals of phylogenetically modern groups such as bovids.
The reptile-like physiological and life history traits found in
Myotragus were certainly crucial to their survival on a small
island for the amazing period of 5.2 million years, more than
twice the average persistence of continental species (42). There-
fore, we expect similar physiological and life history traits to be
present in other large insular mammals such as dwarf elephants,
hippos, and deer. However, precisely because of these traits (very
tiny and immature neonates, low growth rate, decreased aerobic
capacities, and reduced behavioral traits), Myotragus did not
survive the arrival of a major predator, Homo sapiens, some
3,000 years ago.
Materials and Methods
Materials. Fossil material is as follows: Myotragus, Plio-Pleistocene of Majorca,
Spain (Cova de Llenaire, Es Bufador, Son Apats, Cova de Moleta, Avenc de
Ne` cora); crocodile (genus and species indet.), Eocene (Lutetian), La Boixedat
Table 1. Main histological traits of crocodiles, large mammals, and Myotragus
Histological traits Crocodiles Myotragus Large mammals
Inner and central cortex
Primary bone Zonal, LNV, LSV, and FLC Zonal, LNV, LPO, and FLC Azonal, FLC through LPO
Annuli Present Present Absent
Resting lines (LAGs) Cyclically throughout cortex Cyclically throughout
cortex
Rare, near periosteum
Outer cortical pattern in adults Increasingly closer spacing of
LAGs
Increasingly closer spacing
of LAGs
OCL
Vascularization Sparse to avascular Sparse to avascular Densely vascularized
Orientation of vascular
channels
Mostly longitudinal Longitudinal and
concentric
Irregular, variable, increasingly
organized with age
Remodeling Little, in females extensive during
egg-shell formation
Extensive Extensive
Erosion and endosteal bone Rare From an early age onward At subadult age
Haversian systems Rare Frequent Extensive
Bone microstructure of Myotragus is essentially similar to that of crocodiles in tissue pattern, periodicity of bone formation, transition to slower bone
formation at skeletal/sexual maturity, and degree and pattern of vascularization. It resembles, however, other large mammals in pattern and rate of remodeling.
LNV, lamellar nonvascular bone; LSV, lamellar bone with simple vascular canals; LPO, lamellar bone with primary osteons; FLC, fibrolamellar complex (18, 19).
Trait description for crocodiles and large mammals is modified from refs. 21, 23, and 27.
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(Huesca, Spain); G. borbonica, Middle Pliocene, Layna (Spain); cervid (genus
and species indet.), Upper Pliocene, Vilarroya (Spain). Specimens labeled IPS
are housed at the Institut Catala` de Paleontologia, Universitat Auto`noma de
Barcelona, Bellaterra, Spain. Specimens labeled mbcn are housed at the
Museu Balear de Cie` ncies Naturals, So´ller, Majorca (Spain).
To avoid irreversible damaging of valuable material, we preferred frag-
mented specimens for sectioning (except for IPS 44923-c, IPS 26158–1, IPS
26324, and IPS 26321). Slices were made at midshaft following standard
procedures (21, 23) and examined under transmitted light and under polar-
ized and circularly polarized light with a 1
␭
filter. Micrographs (Figs. 1 C–Iand
2B,D, and E) were taken on slices previously moistened with a drop of alcohol
(98%) on their uncovered surface (a common procedure in petrography and
crystallography). This procedure emphasizes the original tissue structure
where this is affected by microbial attack or diagenetic processes, without
damaging the fossil. Micrographs were taken with a polarization microscope
(Leica DM 2500 P).
Age Assessment. There is a general agreement that growth marks represent
annual cycles (21, 22, 25). We estimated the age of individuals by counting
cortical growth rings in histological sections of each specimen. Estimation of
the number of lost or masked growth marks was not possible because removal
of inner cortical bone starts at early ontogenetic stages. Therefore, estimated
ages are minimum ages.
ACKNOWLEDGMENTS. We thank A. de Ricqle` s, A. Chinsamy-Turan, and M.
Sander for helpful comments on the micrographs; L. Demetrius for construc-
tive discussions on the manuscript; two anonymous referees; L. Celia` for
assistance in the collections of the Catalan Institute of Paleontology; C.
Constantino for access to the collections of the Museu Balear de Cie` ncies
Naturals (So´ ller, Spain); and R. García and A. García for technical help. This
work was supported by the Spanish Ministry of Science and Innovation
(CGL2008–06204/BTE) and by the National Science Foundation (RHOI-
Hominid-NSF-BCS-0321893).
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