Prado 2014

Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology
journal homepage: www.elsevier.com/locate/palaeo
Plio-Pleistocene fossil record of large predators in Iberia: Diversity, home
range and climatic change
José L. Prado a,⁎, Beatriz Azanza b, Juan L. Cantalapiedra c, María T. Alberdi c
a
b
c
INCUAPA, UE CONICET-UNICEN, Del Valle 5737, B7400JWI Olavarría, Argentina
Departamento de Ciencias de la Tierra, Facultad de Ciencias, Instituto Universitario de Ciencias Ambientales (IUCA), Universidad de Zaragoza, 50009 Zaragoza, Spain
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2, 28006 Madrid, Spain
a r t i c l e
i n f o
Article history:
Received 31 May 2013
Received in revised form 14 February 2014
Accepted 18 February 2014
Available online 28 February 2014
Keywords:
Home range-size
Diversity
Mammals
Carnivores
Miocene–Pleistocene
Iberia
a b s t r a c t
We investigated the patterns of change in diversity and home range-size structure of the latest Miocene–
Pleistocene Iberian carnivores to recognize the tempo and mode of the major shifts, and place them in the
context of late Cenozoic climatic changes. The database consists of 36 selected and taxonomically revised faunal
lists. A general pattern of carnivore diversity from Iberia shows three maxima in diversity that can be correlated
with major global changes. The ﬁrst coincides with the glacial trend during Pliocene, starting at 2.7–2.6 Ma, with
the onset of glacial cycles of 41 ka; second maximum happened at the beginning of the Middle Pleistocene and
can be correlated with the switch at 1 Ma; third maximum in diversity occurs at the end of Middle Pleistocene,
when the amplitude of interglacials shifted from cooler to warmer interglacials. The most signiﬁcant shifts in
Carnivora diversity and home range-size patterns were linked to dispersal phases that were tracked by a renovation of the carnivore guild. From the patterns in home range-size structure it seems that some multifaceted, and
not always straight, interactions exist between ecological and climatic change and shifts in home range-size. The
onset of the Holocene home range-size structure in Iberian carnivores traces back to a high diversity pulse at
the end of the Middle Pleistocene.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Iberian Cenozoic basins provide one of the richest and most valuable
records of fossil mammals and continental environments. They represent exceptional opportunities to evaluate the ecological and evolutionary responses of mammals to climatic change over a scale of millions of
years (Azanza et al., 1999, 2000; van Dam et al., 2006). This information
is crucial for connecting the dynamics of biotic change from the ecological to the evolutionary scales, and for investigating the processes affecting ecosystems (Badgley et al., 2008).
Living Iberian carnivores inhabit the Mediterranean biome but it is
unclear when the assembly of their ecological structure took place and
whether this is related to the establishment of the Mediterranean climate. Some evidence suggests that the Mediterranean biome began
during the Late Pliocene when xerophytic plants ﬁrst appeared
(Suc et al., 1995), coincident with the initiation of northern hemisphere
glaciations (Sosdian and Rosenthal, 2009). During the Late Pliocene the
global temperature gradually dropped. Between 2.8 and 2.6 Ma seasonality of the North Paciﬁc, as well as the glacial activity of the Greenland,
⁎ Corresponding author. Tel.: +54 2284 450331x209.
E-mail addresses: [email protected] (J.L. Prado), [email protected] (B. Azanza),
[email protected] (J.L. Cantalapiedra), [email protected] (M.T. Alberdi).
http://dx.doi.org/10.1016/j.palaeo.2014.02.023
0031-0182/© 2014 Elsevier B.V. All rights reserved.
Scandinavian and North American ice sheets, increased (Flesche Kleiven
et al., 2002; Haug et al., 2005). Around 2.6 Ma ago, glacial/interglacial alternations were initiated in the northern hemisphere. All of these climatic changes had signiﬁcant ecological consequences. Seasonality
became marked, while successive cycles throughout the 2.6–1.8 Ma interval produced progressively cooler and somewhat drier conditions in
western Eurasia. The Early Pleistocene transition reinserted a further
drop in temperature, as climatic cycling remained dominated by the
41 ka periodicity. The cycles of cool and temperate climatic events became more clearly deﬁned and regular. Final shaping of the Mediterranean landscapes took place throughout the Middle Pleistocene, a highly
dynamic period of climatic ﬂuctuations. During the transition between
1.2 and 0.7 Ma the ﬂora was not altered by any important event (Suc
and Popescu, 2005). This time span represents the ﬁnal phase of the
interval dominated by 41 ka periodicity in the global climatic record.
During the 0.9–0.4 Ma interval the climatic cycling switched from
41 ka periodicity to that governed by orbital eccentricity cycles with
100 ka periodicity (Lisiecki and Raymo, 2005). The amplitude of ﬂuctuations exacerbated glacial phenomena, increasing both seasonality and
aridity over northern and middle latitudes of the northern hemisphere.
The Pliocene–Pleistocene large predatory mammals of Iberia have
been investigated to analyze ecological and evolutionary responses to
climatic events. In large terrestrial mammals, the dominant reaction to
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
climate change seems to have been habitat tracking (Azzaroli et al.,
1988; Aguirre and Morales, 1990; Azanza et al., 1999, 2000; Torre
et al., 2001; Kahlke et al., 2011; Raia et al., 2012). Inﬂuenced by the
Mio-Pleistocene climatic oscillations, newcomers migrated into Iberia
mainly from central and southern Europe across the Pyrenees. Some
mammals, could also have crossed from Africa over the Gibraltar Strait
(O'Regan, 2008; Carbonell et al., 2010; Geraads, 2010; O'Regan et al.,
2011). Indeed, faunal interchanges occurred between North Africa and
Iberia at the end of Miocene (Aguilar and Michaux, 1997; Agustí et al.,
2006) and were tentatively related to the strait closure as a consequence of the Messinian Desiccation Event (Krijgsman et al., 1999).
Iberia attracted a great variety of animals by acting as either a colonizing
bridge, or a refuge for temperate taxa during the late Pleistocene glaciations (O'Regan et al., 2011). These dispersal events most probably
caused changes in the ecology and evolution of carnivore guilds. Species
respond in different ways to climatic change. Biotic interactions such us
competition between predators and prey may have been disrupted as
a response to this change (Meloro et al., 2007). Our focus here is on
patterns of community change related to these events.
The ability of a species to colonize an empty habitat patch is
constrained by the distance moved by dispersers (Bowman et al.,
2001). The resource distribution and abundance have an important inﬂuence on the manner in which space is used by mammals thus
constraining the home range size (HR-size) (Gittleman and Harvey,
1982). Therefore, patterns of change in the HR-size structure throughout the record can provide important understandings into the ecological
and evolutionary responses of mammals to new ecological conditions. A
number of previous studies offered two possible explanations for
changes in HR-size (Hutchinson, 1959; MacArthur, 1972): (a) Competitive size displacement, because sound theoretical reasons exist for
expecting interspeciﬁc competition to be important in shaping communities by determining which species, and how many, can coexist, and
(b) environmental disturbances, that remove key organisms or inﬂuence the availability of space or food by changing the physical environment. However, what happens over evolutionary time scales is less
understood.
In this study we evaluate the variations in origination and extinction
rates, diversity, and inferred HR-size structure across the late Miocene
to Pleistocene times (around 5 to 0.001 Ma). Our aim is to answer the
following questions: (1) what are the overall trends in diversity over
time? (2) Is the inferred change in HR-size structure (i.e. the arrangement between the home range of carnivore guild) concentrated in a
particular biochronological unit and do these changes occur during signiﬁcant climatic change? If so, do patterns or gradients exist that explain
a relationship between climatic changes? What are the reasons for
these patterns? (3) Are the species with a larger HR-size within each
lineage those that colonized other areas? We seek to understand how
the assemblages of large predatory mammals that occurred in Iberia
are distributed in time, and the ways these assemblages were inﬂuenced by dispersal and environmental constraints, as well as intra
guild interactions. Addressing these questions will allow us to recognize
the causes behind the observed ecological and evolutionary patterns,
which is also essential for a better understanding of the origin of the
Mediterranean biome.
2. Methods
2.1. Study area
Iberia has a temperate climate. It is geographically and topographically very variable due to the presence of a jagged coastline, an interior
central plateau and many relatively young mountain ranges, which are
often moderate in elevation in a global context. During glacial periods,
central and northern European mammals are known to have migrated
south to Mediterranean refuges (Hewitt, 2000; Waltari et al., 2007).
The great majority of the “cold taxa” that arrived to Iberia are recorded
405
in localities found today in the modern wet Iberia zone (Álvarez-Lao and
García, 2010). Data from these localities are not included to avoid an
ecological mixture between taxa from the Atlantic and Mediterranean
realms. Thus, our study is limited to the evolution of large predatory
guilds in Mediterranean Iberia. Fig. 1 shows the location of the localities
where recorded.
2.2. Material and data quality
We analyzed the variations of diversity and HR-size structure of
Iberian large predatory mammals though time. Larger predators achieve
a higher net gain rate by concentrating on large prey. We followed the
criterion set by Carbone et al. (2007), who identiﬁed that the change
in dietary strategy (the switch from small to large prey) occurs at a
body weight of 14.5 kg. We restrict our study to species of the three
families that include top terrestrial predators: Canidae, Felidae and
Hyaenidae. Ursidae are excluded due to their omnivorous feeding behavior that rarely includes meat.
The database consists of selected and taxonomically updated faunal
lists of large predatory mammals by time intervals that have been compiled from previous analyses on the Plio-Pleistocene mammals of the
Northwestern Mediterranean region (Alberdi et al., 1997; Azanza
et al., 1999, 2000; Palombo et al., 2009). To eliminate the edge effects
when only a discrete part of the fossil record is investigated (Foote,
2000), we have extended our database in both directions, toward the
latest Miocene and the Holocene to recent times.
We have used thirteen informal biochronological units (BUs) spanning the last seven million years that have been used in previous paleoecological works (Palombo et al., 2009). These BUs have been
substantiated by multivariate procedures (Azanza et al., 1999) and
they represent periods ‘of time during which faunas have certain taxonomic homogeneity, the discontinuity between them corresponding to
faunal reconﬁgurations associated with major changes in environmental conditions’ (Azanza et al., 1999). Thus, each time interval would correspond to a block of coordinated stasis, i.e. an interval during which no
turnover occurred or its rate is low (Brett et al., 1996; Raia et al., 2005,
2007, 2009). It is expected that if the taxonomic turnover rates inside
units are low or null, the diversity should not be greatly overestimated
by claiming that certain taxa coexisted when they actually lived at
different times (Alroy et al., 2001). The boundaries between BUs are estimated by using present day Spanish localities for calibration (see Fig. 2
and Table 1). Only the estimated duration of two BUs (R and V1 intervals) are longer than the canonical span time (500 ka) suggested
by Maas et al. (1995), whereas the durations of the other intervals are
either less than, or at least equal to, 400 ka.
The quality of the fossil data is crucial for validating results and conclusions, because the ﬂuctuating frequencies of coexisting species may
reﬂect actual changes in diversity or may depend simply on sampling
bias. Sampling adequacy was explored using the completeness indices
(CI = [(Nt/(Nt + Nrt)] × 100 and CIbda = [(Nbda/Nbda + Nrt)] × 100 proposed by Maas et al. (1995). These indices are based on the proportion
of Lazarus taxa, or range-through taxa (whose presence can be inferred
because the species is preserved before and after the interval) supposing that their existence is mainly a consequence of deﬁcient sampling.
The number of Lazarus taxa (Nrt) are counted and added to the actual
taxa present before, during, and after an interval (Nbda) in the more conservative index (CIbda) or to the actual total number of taxa (Nt) in the
more generous CI index. We use as a cut-off the threshold the value of
70% suggested by Maas et al. (1995). The values of the completeness indices are affected by BU duration, because increasing the length of a
time span means that it can potentially include a more extensive fossil
record, which moreover reduces the number of Lazarus taxa. To normalize the values of both indices, they were divided by the duration of the
corresponding BU. As a cut-off, we use the threshold the value of 0.14
that results from dividing the minimum acceptable index value of 70%
by the span time (500 ka) suggested by Maas et al. (1995).
406
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
20,23,26
36
35
Atlantic-Mediterranean
present-day boundary
30
Madrid
10
27
31
8
33
24
29
2
1,6
7,14
9
12
19
16,17,18
4
21
25
22
11, 32
15,28
13
3
34
5
1- El Arquillo
2- Las Casiones
3- Venta del Moro
4- Librilla
5- Alcoy
6- La Gloria 4
7- La Calera
8- Layna
9- Las Higueruelas
10- Villarroya
11- Huélago
12- El Rincón
13- Almenara-Casablanca
14- La Puebla de Valverde
15- Fonelas 1
16- Venta Micena
17- Fuente Nueva 1, 3
18- Barranco León 5
19- Quibas
20- Atapuerca TE
21- Cueva Victoria
22- Huéscar-1
23- Atapuerca TD
24- Vallparadís
25- Cúllar de Baza-1
26- Atapuerca SH
27- Ambrona
28- La Solana del Zamborino
29- Aridos
30- Pinilla del Valle
31- Cueva del Congosto
32- La Carigüela
33- Cueva de Los Casares
34- Cova Negra
35- Villacastín
36- Cueva de los Torrejones
Fig. 1. Geographical distribution of the selected latest Miocene to Pleistocene mammal localities in Spain.
2.3. Taxon-free characterization
2.4. Diversity, evolutionary rates and home range
For each species, we compiled data of its presence in time intervals,
body-size, diet and preferred habitat. We used body-mass as a measurement of body-size as it facilitates evaluation among animals with different head and body shapes (Gingerich et al., 1982). Data were collected
from previous works (Prado et al., 2004; Rodríguez et al., 2004) that estimated body mass of fossil species from dental metrics using available
allometric equations (Legendre and Roth, 1988; Van Valkenburgh,
1990).
By using a taxon-free characterization, species were assigned to several ecological categories according to diet and preferred habitat. Data
were collected from the exhaustive review of Palombo et al. (2009)
and Alberdi et al. (2012).
Large Predators were assigned to the following trophic categories:
Paleodiversity refers to the richness of species, measured as the total
number of taxa in a time interval. Following Foote (2000) we counted
for each BU the number of species that exist only in that interval or singletons (NFL); those that originate before the interval but go extinct
within it (NbL); those that originate in the interval and persist beyond
it (NFt); and those that originate before the interval and persist beyond
it (Nbt). We use the standard range-through census technique to minimize preservational and sampling biases (see above), thus Nbt includes
both the number of Lazarus taxa or range through species (Nrt) and the
number of species actually preserved before, during and after the interval (Nbda). Based on these metrics, we estimated origination, extinction
and turnover rates (Foote, 2000). To assess the signiﬁcance of these evolutionary rates we bootstrapped our dataset with replacement 1000
times, using the temporal ranges of the species as the sampling unit.
The average rate from the simulations was considered the best ﬁt-rate
and ± 1 standard deviation of the values around the each mean was
used to deﬁne the uncertainty of the estimate (Finarelli and Badgley,
2010). Results are summarized in Tables 3 and 4.
The HR-size of fossil species can be estimated using allometric equations. The relationship between HR-size and body size (or body weight,
BW) has been stated by McNab (1963) using the allometric equation
HR = a · BWb. Among terrestrial mammals, carnivore guilds have
the broadest range of HR-sizes. Some of the variation in the HR-size
of Carnivora can be explained by diet. McNab (1963) considered
two categories: hunters and croppers, the former having a greater allometric coefﬁcient. (a) This is attributed to the relatively low density of their preferred food items. Meat is a scarce food resource
compared with fruit, foliage or insects. Previous studies, such us
that by Gittleman and Harvey (1982), have established that carnivorous species have larger HR-size than herbivorous species of similar
body mass, and that the distribution of food resources is more homogeneous for herbivores than for carnivores. However, other studies
- Carnivore (C): including hypercarnivores with a diet consisting of at
least 70% ﬂesh meat (Van Valkenburgh, 1988), bone-eaters, bonecrushers and scavenging bone-crackers.
- Carnivore–Omnivore (OM): including ﬂesh-eaters (with a diet of
less than 10% ﬂesh), taxa feeding on invertebrates, and occasionally
fruit.
As for preferred habitat, three major ecological categories were
retained:
- Forest dwellers (FH): including taxa inhabiting forest, closed woodland, bushland, Mediterranean ‘macchia’, open woodland and miscellaneous woodland.
- Ubiquitous (MXH): including more ﬂexible taxa that could live in
scrublands or woodland, as well as in an open landscape, or at the
edge of both.
- Open habitats dwellers (OH): including taxa inhabiting grassland,
steppe or savanna.
Diversity
Turnover
407
Habitat Preference
Climatic Trend
Lisiecki & Raymo 2005
Intervals
Myr
Land
Mammal ages
Geomagnetic
Polarity
Scale
MN "zones"
Geochronolgy
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
Cumulative
diversity
Boundary
crossers
Estimated Mean
Standing Diversity
Per-taxon rates
Turnover
forest
mixed
habitat
open
habitat
δ 18(O‰)
600-
800-
G2
100 ka
400-
Glacial maxima
GALLERIAN
Bruhnes
late
middle
200-
1000-
G1
16
2000-
2200-
V3
2400-
V2
2600-
2800-
3000-
V1
Kaena
41 ka
1800-
V4
Glacial trend
17
VILLAFRANCHIAN
Gauss
late
1400-
1600-
Olduvai
2
3
V5
No Antartic Ice
Matuyama
1200-
early
PLEISTOCENE
3.0-
Jaramillo
3.5-
1
4.0-
0-
A3
AURELIAN A2
A1
G3
4.5-
5.0-
0
3200-
Mammoth
19-23 ka
3400-
3600-
4
Gilbert
Nunivak
Sidufjall
14
4200-
R
4400-
4600-
4800-
5
Thvera
0
latest
MIOCENE
13
latest
TUROLIAN
4
8
Nt = Nft+Nbt
0
Large predators
p (origination)
Carnivorans
q (extinction)
5
0
50
10
Nsd = (Nb+Nt)/2
T
6
"Golden age"
4000-
Cochiti
early
3800-
RUSCINIAN
PLIOCENE
15
0
4
8
p = (Nft/Nsd)/Dt
q = (Nbl/Nsd)/Dt
5000-
5200-
-4
0
4
TI = (Nt-Nb)/Nsd/Dt
0
100
50
100
percentage of taxa
Fig. 2. Carnivoran standing diversity, turnover and habitat preferences over the end of the Miocene to Holocene in Spain. Unequal time intervals correspond to the 13 informal
biochronological units recognized by Palombo et al. (2009). Each faunal complex was placed at the mid-point of the considered time interval. The uncertainty of the estimate diversity
and evolutionary rates was assessed bootstrapping the dataset with replacement 1000 times, using the temporal ranges of the species as the sampling unit. The average rate from the simulations was considered the best ﬁt-rate and bootstrapped conﬁdence intervals are ±1 standard deviation of the values around the each mean.
(Kelt and Van Vuren, 1999) defend that scaling relations of HR-size
are not statistically different between carnivorous and herbivorous
or omnivorous species. Among terrestrial mammals, carnivore guilds
have the broadest range of HR-sizes. Also resource distribution and
abundance has an important inﬂuence on the HR-size (Gittleman
and Harvey, 1982).
As a proxy for HR-size of fossil species we used three different estimations based on allometric relationships (HR = a · BMb where BM is
the body mass). Allometric equations were implemented from data of
living species that were arranged following taxonomic, habitat preference (forest dwellers, ubiquitous and open landscape dwellers) and trophic categories (carnivore and omnivore). These category-speciﬁc
regressions (Table 2) were applied to fossil species using body mass
estimates. As a consequence, for each fossil species we obtained three
different estimations of HR-size dependent on its inclusion in each of
the three categories considered.
Table 1
Age and duration of the informal biochronological units (BUs) for the latest Miocene to Pleistocene in Spain and main localities used in the calibration.
BU
T
R
V1
V2
V3
V4
V5
G1
G2
G3
A1
A2
A3
Latest Turolian
Ruscinian
Villafranchian 1
Villafranchian 2
Villafranchian 3
Villafranchian 4
Villafranchian 5
Galerian 1
Galerian 2
Galerian 3
Aurelian 1
Aurelian 2
Aurelian 3
Lower age
Upper age
Mid-point age
Duration
Main localities
6.6
5.40
3.40
2.70
2.40
2.05
1.60
1.15
0.95
0.70
0.50
0.40
0.15
5.40
3.40
2.70
2.40
2.05
1.60
1.15
0.95
0.70
0.50
0.40
0.15
0.01
6.00
4.40
3.05
2.55
2.23
1.83
1.38
1.05
0.83
0.60
0.45
0.28
0.08
1.20
2.00
0.70
0.30
0.35
0.45
0.45
0.20
0.25
0.20
0.10
0.25
0.14
Venta del Moro, El Arquillo, Las Casiones
Alcoy, La Gloria 4, Layna
Villarroya
El Rincón 1, Huélago
La Puebla de Valverde, Almenara-Casablanca
Fonelas P-1
Fuente Nueva 1, 3, Venta Micena, Atapuerca TE, Barranco León
Cueva Victoria, VallParadís inf.
Atapuerca TD-4-6, Huéscar 1, Vallparadís sup.
Cúllar Baza 1, Atapuerca SH
Ambrona
Atapuerca TD10-11, Pinilla, La Carigüela
Cova Negra, Villacastín, Valdegoba
408
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
Table 2
Regression statistics for the home-range size based on systematics, and trophic and habitat
preferences of living carnivores. FH: forest dwellers; MXH: Ubiquitous habitat; OH: Open
landscape dwellers; C: Carnivore; OM: Carnivore–Omnivore.
FH
MXH
0H
C
OM
Canidae
Felidae
Hyaenidae
Slope
Intercept
R
R2
Standard error
p
1.014
1.074
1.144
1.068
0.982
1.987
0.9
2.227
−2.046
−3.097
−3.174
−2.189
−3.032
−10.688
−0.889
−15.042
0.851
0.694
0.846
0.836
0.818
0.805
0.591
0.863
0.724
0.481
0.715
0.699
0.669
0.649
0.35
0.745
1.23109
1.76074
1.80722
1.4208
1.2054
1.3225
1.38613
1.3215
p
p
p
p
p
p
p
p
b
b
b
b
b
b
b
N
0.01
0.01
0.05
0.01
0.01
0.01
0.05
0.05
3. Results
3.1. Data quality
Fig. 3 shows the values of the completeness indices for the large
predators compared with that of other large mammals. The more conservative CIbda index has a value below 70% in three BUs: V2, V4 and
A1, whereas if the more generous CI index is used, the quality of the record is only deﬁcient in two (V2 and A1 BUs), indicating that data from
these BUs should be treated (Maas et al., 1995). Nonetheless, when the
database of all large mammals is considered, the values of CI index for all
BUs are close to or above this threshold. When the values of both indices
are normalized by the BU duration, none of these BUs are below the
threshold. Only the Ruscinian BU now appears below the cutoff line because its estimated duration is well over 500 ka, but a value 100 for the
CI index was obtained. Consequently, we consider that diversity was not
greatly underestimated.
3.2. Paleodiversity
The diversity trends (Nt and Nsd) show three maxima (Fig. 2), with
peaks at the Plio-Pleistocene boundary (V2 to V3 BUs), at the beginning
of the Middle Pleistocene (G1 BU) and at the Middle–Late Pleistocene
boundary (A1 to A2 BUs). The ﬁrst and third maxima could prove
even more important because the diversity of the V2 and A1 BUs
could be underestimated according with CI index.
Despite these ﬂuctuations, diversity increases during the PlioPleistocene but in large predators it increases much more moderately
than in other carnivores. It should be noted that the lowest diversity is
recorded during the Early Pliocene (R BU), despite the fact of it being,
by far, the longest BU. This could be the result of inadequate sampling,
but it occurs after the Mio-Pliocene transition, one of the most relevant
extinction events in Iberia, when all the Turolian large predators became extinct (Alberdi et al., 2012).
Cumulative richness also reﬂects this general increase, but shows a
break in the trend of the curve at the beginning of the Villafranchian
(V1–V2 BUs).
These trends roughly correlate with the general global climate signal
(Lisiecki and Raymo, 2005, see Fig. 2). The cumulative curve the general
trend of the temperature curve. The ﬁrst maximum is coincident with
the onset of Northern Hemisphere Glaciations and the following decrease in diversity began when glacial–interglacial cycles of 41 ka had
clearly started. The second is coincident with the intensiﬁcation of
glacial cycles that change from a duration of 41 ka to 100 ka; and the
third maximum is during the Middle Pleistocene, a warm period
(Holstein stage) between the Mindel and Riss glaciations.
The ﬁrst and third maxima occur without a large turnover rate. By
contrast, the second maximum at the beginning of the Middle Pleistocene occurs at the time of an important turnover when the records
show a high extinction rate (the “Galerian turnover” sensu Azanza
et al., 2000).
In a previous study, we found a rough correlation between diversity
trends and shifts in the percentage of carnivores in each of the habitat
categories (Palombo et al., 2009). Croitor and Brugal (2010), and Torre
et al. (2001) also obtained similar results. This rough correspondence
should be explained as an ecological response, given that the relative increase of ubiquitous taxa, which occurred during the Pleistocene, could
be related to the environmental ﬂuctuations associated with the glacial
cycles, as ubiquitous taxa are expected to be better able to adapt to environmental changes. With few variations this pattern is maintained in
the present analysis (Fig. 2).
3.3. Patterns of HR-size changes
The HR size quantiﬁes the inherent ability of the animal to move.
Consequently, dispersal distance and HR-size covary across mammal
species when considered independently of body mass (Bowman et al.,
2002). Fig. 4 documents the patterns of HR-size change over time. The
Canidae were represented in Iberia by 14 species in six genera. Fig. 4
shows that HR-size decreases during the Pliocene. This trend is clearly
independent of the method of HR-size estimation used. The canid
species were distributed into two groups of HR-size, distinctly by the
predicted boundary of 14.5 kg. The species with carnivorous diets
have a larger HR-size than the omnivorous species. When the HR-size
was inferred using the allometric equation based on diet, the gap between the two groups was magniﬁed. The upper limit for omnivores
corresponds to the HR-size estimation for 14.5 kg in the omnivore equation. In turn, the lower limit for carnivores corresponds to the HR-size
estimation for 14.5 kg in the carnivore equation. Consequently, the differentiation between carnivores and omnivores implies a large jump in
HR-size. This jump appears in the lower Pleistocene when hypercarnivorous Canidae spread into Eurasia (called ‘the Wolf event’,
Sardella and Palombo, 2007).
Table 3
Diversity and turnover data performed on the taxa per BUs matrix in Table 4. Biochronological units as in Table 1.
Species richness
Singletons (NFL)
Only cross bottom boundary (NbL)
Only cross top boundary (NFt)
Cross both boundaries (Nbt)
Range-through (Nrt)
Bottom-crossers (Nb)
Top-crossers (Nt)
Estimated mean standing diversity (Nsd)
Originations
Extinctions
Per-taxon origination rate (p)
Per-taxon extinction rate (q)
R
V1
V2
V3
V4
V5
G1
G2
G3
A1
A2
A3
5
2
0
3
0
0
0
3
1.5
5
2
0.5
0.2
7
0
0
4
3
0
3
7
5
4
0
0.816
0
7
0
0
0
7
5
7
7
7
0
0
0
0
9
0
2
2
5
0
7
7
7
2
2
0.635
0.635
10
2
5
1
2
1
7
3
5
3
7
0.667
1.556
8
0
0
5
3
0
3
8
5.5
5
0
1.389
0
8
0
4
0
4
0
8
4
6
0
4
0
2.5
5
0
3
1
1
0
4
2
3
1
3
0.8
2.4
5
0
0
3
2
0
2
5
3.5
3
0
3
0
5
0
0
0
5
3
5
5
5
0
0
0
0
6
1
0
0
5
0
5
5
5
1
1
0.667
0.667
5
0
2
0
3
0
5
3
4
0
2
0
2.857
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
409
Table 4
Biochronological distribution; and habitat preference, diet and body mass for each fossil taxa. FH: forest dwellers; MXH: Ubiquitous habitat; OH: Open landscape dwellers; HY:
hypercarnivores; CA/SC: bone-crushers and scavenging bone-crackers; CIO: Carnivore–Insectivore–Omnivore C: Carnivore; OM: Carnivore–Omnivore. Biochronological units as in Table 1.
Body
mass
(kg)
Biochronological unit
Taxa
T
R
V1
V2
V3
V4
V5
G1
G2
G3
A1
A2
A3
H
Habitat
Diet
Large size
Acinonyx pardinensis
Adcrocuta eximia
Amphimachairodus giganteus
Canis accitanus
Canis etruscus
Canis lupus
Canis mosbachensis
Caracal/Lynx depereti-issiodorensis
Chasmaporthetes lunensis
Crocuta crocuta
Cuon alpinus
Eucyon adoxus
Eucyon debonisi
Homotherium latidens
Hyaena/Parahyaena cf. brunnea
Hyaenictitherium /Thalassictis hyaenaoides
Hyaenictitherium wongii / Thalassictis hipparionum
Lycaon/Canis (Xenocyon) falconeri
Lycaon/Canis (Xenocyon) lycaonoides
Lynx pardina spelaea
Megantereon cultridens
Megantereon whitei
Metailurus parvulus
Pachycrocuta brevirostris
Panthera ex gr. gombaszoegensis
Panthera leo spelaea
Panthera pardus
Paramachairodus maximiliani
Paramachairodus orientalis
Pliocrocuta perrieri
Pliocrocuta pyrenaica
Puma pardoides
OH
MXH
MXH
OH
MXH
MXH
MXH
FH
OH
MXH
MXH
MXH
MXH
MXH
MXH
MXH
MXH
OH
OH
FH
FH
MXH
FH
MXH
FH
OH
FH
MXH
MXH
MXH
MXH
FH
HY
CA/SC
HY
CIO
CA/SC
CA/SC
CA/SC
HY
HY
CA/SC
HY
CIO
CIO
HY
CA/SC
CA/SC
CA/SC
HY
HY
HY
HY
HY
HY
CA/SC
HY
HY
HY
HY
HY
CA/SC
CA/SC
HY
C
C
C
OM
C
C
C
C
C
C
C
OM
OM
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
60.2
58.7
215
16.5
23.8
43
16.5
24.3
68.4
52
17.9
12.6
21.1
188
43.4
19.8
16
40
29.7
14.1
62
100
33.5
75.8
64.7
180
48
71.6
65.5
47.7
35.2
38
Small size
Felis attica
Felis silvestris silvestris
Nyctereutes donnezani
Nyctereutes megamastoides
Plioviverrops faventinus
Vulpes alopecoides
Vulpes praeglacialis
Vulpes vulpes
MXH
FH
FH
FH
FH
OH
OH
MXH
HY
HY
CIO
CIO
CIO
CIO
CIO
CIO
C
C
OM
OM
OM
OM
OM
OM
12.7
4.7
7.1
7.7
3.4
5
5.2
7.3
The Felidae were represented in Iberia by 17 species in eleven genera. The Felidae HR-size structure is quite different from that for the
Canidae. There are four groups of HR-size that can be clearly distinguished in the Middle to Late Pleistocene. The groups are less differentiated in the Late Miocene. During the Late Pliocene the intermediate
range of HR-sizes overlaps. The appearances of new species during the
Lower Pleistocene begin a competitive displacement in each group.
The Hyaenidae were represented in Iberia by 10 species in eight
genera (Fig. 4). The patterns for the Hyaenidae seem to be more similar
to those of the Canidae than the Felidae. The distribution of HR-size is
limited by diet, but this pattern was obtained before the hyaenids
arrived in Iberia and omnivorous species are only occasionally present.
4. Discussion
The beginning of the Pliocene epoch at 5.3 Ma saw something of a
comeback towards more forested conditions in the northwestern
Mediterranean after Messinian aridiﬁcation. During the Ruscinian, subtropical conditions predominated that were characterized by seasonal
rainfall. Subtropical to meso-Mediterranean forests developed in the
north, while Mediterranean steppes formed to the south of the
northwestern Mediterranean area. These conditions heralded the
beginning of the double seasonality regime, and the temperature and
precipitation regimes that are typical of the Mediterranean climate
(Suc et al., 1995).
A concomitant shift in the composition of the large mammalian
fauna is detected, a point emphasized by Azanza et al. (2000) who called
it the ‘Ruscinian-turnover’. None of the eleven carnivore species present
during the Late Miocene in the Iberian basins crossed the Mio-Pliocene
boundary. Only Plioviverrops faventinus, a small hyaena with a mongoose like insectivore/omnivore morphology (Turner et al., 2008),
seems to have survived this event but this taxon is not recorded in Iberia
before the Pliocene. Among large predators, there appears to be both a
radiation of canids and the full emergence of bone-cracking hyaenas
leading to an organized guild of large carnivores in Europe.
The ﬁrst record of Canidae in Eurasia is “Canis” cipio, only occasionally recorded in Iberia during the latest Miocene. Around 7.2 to 5.3 Ma
ago, the genus Eucyon was ﬁrst recorded as E. debonisi (Montoya et al.,
2009; Rook, 2009). The genus Eucyon probably dispersed again to Iberia
at the end of the Early Pliocene (Sotnikova and Rook, 2010). The replacement of E. debonisi by E. adoxus implied a decrease in the Eucyon
HR-size during the Pliocene (Fig. 4). There was further diversiﬁcation
CI index
Large predators
Quality cutoff value (70%)
CI
CIbda
6
5
4
3
2
1
0
Large predators
Quality cutoff value (0.14)
6
5
4
3
2
1
Time (Myr)
0
120
110
100
90
80
70
60
60
40
30
20
10
0
0,8
0,7
0,6
0,5
0,4
0,3
0,2
0,1
0,0
G1
G2
G3
A1
A2
A3
V5
V4
V3
V2
V1
R
T
G1
G2
G3
A1
A2
A3
V5
Intervals
CI / duration
0,8
0,7
0,6
0,5
0,4
0,3
0,2
0,1
0,0
V4
R
T
CI index
CI / duration
120
110
100
90
80
70
60
60
40
30
20
10
0
V1
Intervals
V3
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
V2
410
Large mammals
Quality cutoff value (70%)
CI
CIbda
6
5
4
3
2
1
0
3
2
1
0
Large mammals
Quality cutoff value (0.14)
6
5
4
Time (Myr)
Fig. 3. Quality assessment of the large predator and large mammal data from the early Pliocene to Pleistocene in Spain: a line-diagram of completeness values corresponding to each faunal
complex. The 70% cut-off line corresponds to the value considered by Maas et al. (1995) as a useful ad hoc cut-off point for their data, where higher values indicate reasonably adequate
sampling.
within the group of small HR-size with the record of the genus
Nyctereutes and later with the genus Vulpes. These taxa are small
predators that persisted in the omnivore niche. The major change in
the patterns of canids HR-size happened during the Early Pleistocene
when the glacial–interglacial cycles were established. HR-size analysis
indicated the appearance of a new large HR-size group. This change is related to the modiﬁcation in carnivore niche. These canids comprise
coyote-like and hypercarnivores (Table 4). The dispersal of hypercarnivorous canids during the Early Pleistocene is testiﬁed to by increasing fossil evidences and it is worth noting that both large wild dogs
(Lycaon falconeri in Martínez-Navarro and Rook, 2003) and wolf-like
canids (Canis etruscus) appeared in Iberia. In France, wolves could have
appeared as early as the Late Pliocene (Lacombat et al., 2008). However
the main increase in their presence did not take place before 2 Ma. This
episode (the so-called “Wolf Event”; Torre et al., 2001; Sardella and
Palombo, 2007) is an important part of a faunal renewal related to climatic and environmental. Even C. accitanus, a coyote-like dog, enlarged
the HR-size of the omnivore canids at this interval. The circumstance
that wolves and large hypercarnivorous canids progressively dispersed
into Iberia and occupied new niches that became available may be related to the widespread occurrence of open habitats (Fig. 2). By increasing
HR-size, canids could have extended their feeding range. However,
it should be taken into account that the development of predator size
is likely to be induced by changes in prey size, and a major trend toward
larger size has been documented for large herbivores (Prado et al.,
2004; Rodríguez et al., 2004). The diversity of canids declines at
the end of the Middle Pleistocene when the modern lineages (Vulpes
vulpes and Canis lupus) appear. Only the diversity occasionally increases
with the intermittent presence of Cuon alpinus during the Late
Pleistocene.
By contrast, the most strictly carnivorous taxa in the order, the felids,
develop up to four different HR-sizes (Fig. 4). The smallest HR-size is
only present through the latest Miocene and from the latest Middle to
Late Pleistocene. Drastic reductions in diversity occur during the Early
Pliocene when machairodontine felids become rare elements in local
faunas and the remains are so scarce that a taxonomic assignment
below the family level is not possible. In contrast diversity during the
Late Pliocene is very high. The intermediate range of HR-sizes is very
close between them. This time was characterized by a predominately
open and mixed habitat. For instance, in present-day African landscape,
most of the large living predators abound in open savannas and savannas–woodlands (variable mixtures of trees, grassland, and bushland) that are coincident with the highest ungulate densities. During
the Plio-Pleistocene, Rodríguez et al. (2004) show an increase in body
size of ungulates, where none of the herbivores occupied the small
size range. This pattern indicates a close ﬁt in size between the predator
and its preys. The appearances of new species during the Early Pleistocene seem to better delimited the felid niches and after the wolf event
four set of HR-size appear clearly separated. We hypothesized that
competitive interactions could be the principal mechanism to explain
HR-size changes.
The Hyaenidae species were more diverse through the Late Miocene.
Together with a precocious bone eating Hyaenidae, Adcrocuta eximia,
two thalassictine forms were recorded during the latest Miocene. The
thalassictine group is basically canid-like in ecomorphology and determines the general trend towards hypercarnivory which hyaenid evolution follows (Werdelin and Solounias, 1991). All these taxa disappeared
at the end of the Miocene and were replaced by a completely new
hyaenid fauna. The hunting hyaena forms show a decline in diversity,
which is strongly associated with the invasion of Eurasia by dogs (family
Canidae) in the Late Miocene–Early Pliocene. Nevertheless the only
hunting hyaena Chasmaportetes lunensis persisted through the Pliocene
but its disappearance in the Early Pleistocene occurred in coincidence
with the ‘wolf event’. Chasmaportetes lunensis was the only cursorily
hyaena adapted to open habitat (Turner et al., 2008). The appearance
of Pliocrocuta at the R BU followed by the giant Pachycrocuta during
the Late Pliocene and Early Pleistocene shows how hyaenas were able
to make a living from scavenging when necessary. In this group, the
bone-cracking component of the dentition is established at the expense
of the shearing element (Palmqvist et al., 2011). The marked seasonality
that characterized temperate Europe for most of the Pleistocene, with
cooler and drier conditions than those of tropical Africa, made the availability of large ungulate carcasses for scavenging a key resource for hyaenas (Turner, 1992). Living hyaenas possess a range of strategies that
affect several features of their skeletal morphology (Werdelin and
Solounias, 1991; Turner et al., 2008). The wolf event did not exemplify
any signiﬁcant change despite the immigration of Pachycrocuta
brevirostris, the largest true hyaena ever recorded. Only one form of
hyaenid was recorded after this moment and persisted to the latest
Pleistocene.
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
0
diet
0
1
1
1
2
2
2
3
3
3
4
4
4
5
5
5
6
6
1
10
100
1000 10000
CA
7
0.01
0.1
1
10
100
0.01
0
0
0
1
1
1
2
2
2
3
3
3
6
100
V4
V3
V2
3
V1
4
OH MXH FH
R
OM
5
6
7
0.01
0.1
1
10
T
100
1000 10000
0
0
1
1
2
2
3
3
4
4
5
5
OM
CA
6
1
10
100
1000 10000
0.01
0.1
1
10
0.01
0.1
1
10
100
1000 10000
100
1000 10000
6
7
7
0.1
1000 10000
7
0.01
CA
2
Hyaenidae
1
1000 10000
A3
A2
A1
G3
G2
G1
V5
14.5 Kg threshold
0
10
100
6
7
7
1
10
?
5
CA
6
OM
5
0.1
1
?
5
0.01
0.1
4
4
4
?
Time (Ma.)
1000 10000
FH
MXH
OH
0.1
FH
MXH
OH
0.01
Felidae
6
7
7
habitat
FH
MXH
OH
taxonomy
OM
Canidae
0
411
0.01
0.1
1
10
100
1000 10000
LOG Home Range size (Km2)
Fig. 4. Home range size (expressed in logarithms) of selected species of Canidae, Felidae and Hyaenidae over the end of the Miocene to Pleistocene in Spain. The symbols are plotted at the
mid-point of the time interval. Vertical axis represents time from past to present.
5. Conclusions
The analysis of Iberian Carnivora diversity trends shows that the assumption of a direct effect by climate change is partially supported by
the data. There are three diversity maxima that can be correlated with
main global changes. The ﬁrst maximum is at the Plio-Pleistocene
boundary, which coincides with the beginning of the Pliocene glacial
trend at 2.7–2.6 Ma. The onset of 41 ka glacial cycles is consistent with
the diversity reduction during the Early Pleistocene. This event marks
the beginning of accelerating turnover rates (stemming from
alternating speciation and extinction pulses) that remained high until
the Holocene. The second maximum occurred at the beginning of the
Middle Pleistocene. These diversity changes can be associated with the
onset of the 100 ka glacial cycles at 1.0 Ma. A third maximum occurred
at the end of the Middle Pleistocene, when the glacial maxima became
warmer.
During this span of time only a few carnivore species were specialized; many others were ubiquitous or generalist taxa and occupied
broad niches (Palombo et al., 2009). This circumstance favored the
survival of a great number of taxa during main environmental changes.
Likening diversity trends and shifts in the percentage of species in each
of the habitat categories, it seems that tendencies in diversity are roughly associated with the variations of the relative abundance of forest habitat throughout time. This coarse correspondence should be explained
as an ecological response, assuming that the forest dwelling species
had narrower environmental tolerance. The relative expansion of
412
J.L. Prado et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 399 (2014) 404–413
ubiquitous taxa during the Pleistocene could be linked to the environmental variations correlated with the glacial cycles, in keeping with
their broader environmental tolerance.
From the patterns in HR-size it seems that some complicated, and
not always straight, relationships exist between environmental variations and changes in HR-size as ungulate fauna show (Azanza et al.,
1999). During the Pliocene, the conditions were predominately subtropical, but the glacial trend at the Plio-Pleistocene boundary anticipated the temperature, precipitation and seasonality regime that are
typical of the Mediterranean climate. Our analysis conﬁrms that this
event altered signiﬁcantly only the HR-size structure of the Iberian
canids regarding the massive dispersal of carnivorous canids in the socalled ‘Wolf Event’. The pattern suggests that the canids that gradually
dispersed into Iberia did not occupy preexistent niches, but entered
new ones that became vacant because of the climatic and environmental change. Among felids, the appearances of new species seem to begin
a competitive size displacement that might have caused the main
HR-size changes in coincidence with the second and third maxima.
This pattern seems to reﬂect a closer ﬁt between prey and predator.
Consequently, the organization of guilds seems to be more narrowly
associated to the time and mode of dispersal events than to the major
climatic variations. The Holocene HR-size structure of the Carnivora
was acquired during the third maximum at the end of the Middle
Pleistocene.
Acknowledgments
The authors would like to thank Jon Baskin for critically reading and
improving the earlier drafts of the manuscript. The manuscript was greatly improved by thoughtful review from Pasquale Raia and two anonymous referees. Stefan Gabriel and Dan Rafuse revised the English text
and Mauricio Antón facilities the life carnivorous reconstruction in highlights ﬁgure. Funding was provided by a Projects CGL2007-60790/BTE
and CGL2010-19116/BOS from the Dirección General de Investigación
Cientíﬁca y Técnica of Spain and Projects AECID A/023681/09 and
A/030111/10; grants from the Universidad Nacional del Centro de la provincial de Buenos Aires (http://www.unicen.edu.ar) and the Project
ANPCYT (http://www.agencia.gov.ar) PICT 11-0561, Argentina. The
funders had no role in study design, data collection and analysis, decision
to publish, or preparation of the manuscript.
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