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Exploring paleo food-webs in the European Early and Middle Pleistocene: A network analysis

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Food webs are networks of feeding (trophic) interactions among species. As any other network approach, research on food webs focuses its analysis on the structure of direct and indirect interactions among diverse species, rather than looking at the particularities of certain taxa. In recent times, scholars have collected an impressive amount of empirical food-web data to study present day terrestrial and aquatic habitats.More restrictively, this approach has also been applied to trophic interactions represented in the fossil record of extinct ecosystems. Nevertheless, to our knowledge, none of them has addressed the role played by the different Pleistocene hominin species as part of such food-webs. In this work, we aim at filling this gap by focusing on the Early and Middle Pleistocene paleo-communities in Western Eurasia. Our goal is to improve our understanding on changes experienced by large mammals' interactions during this period, and shed some light on the influence of and on Homo species of those changes.We have constructed up to 27 paleo food-webs from the archaeo-paleontological record of European assemblages, covering from the Middle Villafranchian to the Late Galerian. Only large mammals have been considered, including a couple of Homo species that are present in 8 food-webs. Then, we have developed a two-steps analysis. First, we have calculated the main structural features of all the networks, and have compared them across geographical areas, periods and cases with and without Homo species. Second, we have calculated different structural centrality measures in order to assess the relevance of Homo species in their corresponding food-webs.The obtained results show that the Pleistocene food webs under study shared basic features with modern food webs, although differences in the values of some parameters might be significant. Moreover, when comparing the networks across periods, we found a marked change that could be related to the Mid-Pleistocene Revolution. Finally, our results also highlight the trophic position of hominins in the web as a central species that channeled energy fluxes.
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EXPLORING PALEO FOOD-WEBS IN THE EUROPEAN EARLY AND
MIDDLE PLEISTOCENE: A NETWORK ANALYSIS
Lozano S.
1*
, Mateos A.
2
, Rodríguez J.
2
1
IPHES, Institut Català de Paleoecologia Humana i Evolució Social, Tarragona, Spain and Àrea
de Prehistòria, Universitat Rovira i Virgili (URV), Tarragona, Spain
2
National Research Center on Human Evolution (CENIEH), Paseo Sierra de Atapuerca, 3.
09002 Burgos (Spain)
* Corresponding author: S. Lozano (slozano@iphes.cat)
e-mail addresses: ana.mateos@cenieh.es (A. Mateos); jesus.rodriguez@cenieh.es (J. Rodríguez)
Abstract
Food webs are networks of feeding (trophic) interactions among species. As any other
network approach, research on food webs focuses its analysis on the structure of direct
and indirect interactions among diverse species, rather than looking at the particularities
of certain taxa. In recent times, scholars have collected an impressive amount of
empirical food-web data to study present day terrestrial and aquatic habitats.
More restrictively, this approach has also been applied to trophic interactions
represented in the fossil record of extinct ecosystems. Nevertheless, to our knowledge,
none of them has addressed the role played by the different Pleistocene hominin species
as part of such food-webs. In this work, we aim at filling this gap by focusing on the
Early and Middle Pleistocene paleo-communities in Western Eurasia. Our goal is to
improve our understanding on changes experienced by large mammals' interactions
during this period, and shed some light on the influence of and on Homo species of
those changes.
We have constructed up to 27 paleo food-webs from the archaeo-paleontological record
of European assemblages, covering from the Middle Villafranchian to the Late Galerian.
Only large mammals have been considered, including a couple of Homo species that are
present in 8 food-webs. Then, we have developed a two-steps analysis. First, we have
calculated the main structural features of all the networks, and have compared them
across geographical areas, periods and cases with and without Homo species. Second,
we have calculated different structural centrality measures in order to assess the
relevance of Homo species in their corresponding food-webs.
The obtained results show that the Pleistocene food webs under study shared basic
features with modern food webs, although differences in the values of some parameters
might be significant. Moreover, when comparing the networks across periods, we found
a marked change that could be related to the Mid-Pleistocene Revolution. Finally, our
results also highlight the trophic position of hominins in the web as a central species
that channeled energy fluxes.
Keywords: Paleo food-webs; Early and Middle Pleistocene; Macro-mammals; Homo
species
1
1. Introduction
Food webs are networks of feeding (trophic) interactions among species (Cohen et al.,
1990). As any other network approach, research on food webs focuses its analysis on
the structure of direct and indirect interactions among diverse species, rather than
looking at the particularities of certain taxa. In recent times, scholars have collected an
impressive amount of empirical food-web data to study present day terrestrial and
aquatic habitats (Martínez, 1991; Williams and Martínez, 2000; Dunne et al.,2002;
Stouffer et al., 2005; Pascual and Dunne, 2006; Brose et al, 2006). Moreover, there is an
increasing literature on the construction of theoretical models of food-web structure to
understand dynamics of ecological communities like, for instance, their robustness to
the extinction of certain species or the introduction of new ones (Allesina et al., 2008;
Stouffer and Bascompte, 2011; Stouffer et al., 2012; Capitán et al. 2013).
Beyond its application to study ecosystems in vivo, the ‘food web approach’ has also
been used to study trophic relationships as represented in the fossil record of extinct
ecosystems. Since the pioneering work by Dunne et al. (2008), which constructs and
analyses paleo food-webs from extraordinarily well preserved Cambrian records, some
authors have contributed other case studies (Maschner et al., 2009; Roopnarine and
Hertog, 2010; Lotze et al., 2011), and guidelines on how to deal with methodological
specificity of paleo food-webs (Roopnarine, 2009). Nevertheless, to our knowledge,
none of these works have applied food-web analysis to the fossil record in order to
address long-term ecological processes and, specifically, interactions of different Homo
species with other animal taxa along the first steps of human evolution. The closest
reference we have found, analyzes structural changes on seed-dispersal interactions
related to the late Quaternary megafaunal extinction in America (Pires et al., 2014).
The general objective of this article is, then, to explore the potential of food-webs
generated from paleontological fossil records as a valid methodological approach to
study dynamics in Pleistocene ecosystems. To this end, we have chosen as a case study
the late Early Pleistocene and the Middle Pleistocene in Western Eurasia. A major
climate and ecological event, known as the Mid-Pleistocene Revolution (MPR), driven
by variations in the orbital forcing of the climate cycles occurred within this period
(Maslin and Ridgwell, 2005). The effects of the MPR on the climate system were
particularly evident in the period from 1.0 Ma to 0.8 Ma, when a substantial increment
2
on global ice volume occurred at 0.94 Ma, the periodicity of the cycles changed from 41
ky to 100 ky and their amplitude increased (Head and Gibbard, 2005). These climate
changes promoted a drastic reorganization of the European ecosystems, that affected
both the fauna and the vegetation, and was characterized by an expansion of the open
environments (Bertini et al., 2010; Croitor and Brugal, 2010; Kahlke et al., 2011; Leroy
et al., 2011; Palombo, 2014a; Suc and Popescu, 2005). These environmental changes
undoubtedly affected the survival opportunities of the European humans because the
new environments provided different qualities and quantities of trophic resources
(Rodríguez et al., 2012; Palombo, 2014a). Within that framework, our goal is twofold.
First, to uncover possible changes on large mammals' trophic relationships along this
period. Second, to analyze the role (either passive or active) played by different
Pleistocene's Homo species in such changes.
2. Material and methods
2.1 Data compilation and network construction
A set of 27 European large mammal Local Faunal Assemblages (LFAs) dated from the
middle Villafranchian to the late Galerian was selected from the literature (See Table 1
and Figure 1). Five time periods, corresponding to the middle Villafranchian (2.6-1.8
Ma), late Villafranchian (1.8-1.2 Ma), early Galerian (1.2-0.78 Ma), middle Galerian
(0.78-0.0.5 Ma), and late Galerian-early Aurelian (0.5-0.3 Ma) (Palombo, 2014a) were
distinguished, and local faunas were assigned to one of them according to
biostratigraphic correlations and numerical ages provided by the original sources. Only
reasonably complete LFAs were included in the database. Although it is extremely
difficult to establish strong criteria to determine whether a LFA is reasonably complete,
we established a rule of thumb based on the analisys of 1,452 Pleistocene LFAs from
Europe. We selected faunas with a number of primary and secondary consumers above
the median of the 1,452 LFAs. Thus, we selected a number of faunal assemblages with
more than seven primary consumer species and more than four secondary consumers.
This is a conservative criterion, based on selecting the richest LFAs on the confidence
that they are reasonably complete, but it does not necessarily imply that poorer LFAs
3
are incomplete. The dataset includes only large mammals, defined as species weighing
more than 10 kg. This size is slightly below the threshold where predators shift from
small to large prey, which according to Carbone et al. (1999) is 21.5 kg. Setting the
threshold at 10 kg avoids excluding medium-sized carnivores that occasionally include
large prey in their diets.
Putative trophic relationships between the species in the LFAs were inferred on the
basis of the information available about the characteristics and behavior of the prey and
predators as explained in Rodríguez et al. (2012). Extrapolation of the behavior of
recent relatives (see references in Rodríguez et al. 2012), isotopic (Bocherens et al.,
2011; Feranec et al., 2010; García et al., 2009; Palmqvist et al., 2008), and
paleontological or zooarchaeological evidence was taken into account to infer the
trophic relationships. The evidence on the predatory behaviour and the potential prey of
Homotherium sp, Lynx issiodorensis, Lynx pardinus, Megantereon cultridens, Panthera
gombaszoegensis, Panthera pardus, Puma pardoides, Acinonyx pardinensis,
Chasmaporthetes lunensis, Pachycrocuta brevirostris, Crocuta crocuta, Pliocrocuta
perrieri, Canis arnensis, Canis etruscus, Canis mosbachensis, and Lycaon lycaonoides
was discussed in detail in Rodríguez et al. 2012. Here we review the information
available to infer the predatory behavior of the other species included in the present
work.
The lion (Panthera leo) arrived in Europe 0.7-0.6 Ma. to occupy the niche of a top
predator, able to kill very large prey (Croitor and Brugal, 2008). Modern lions are
certainly the best analog for the predatory behavior of Pleistocene P. leo. The sociability
of lions allow them to kill very large prey in group hunting. Their cursorial abilities and
social hunting make them very efficient in open country, while their strong constitution
makes them good ambush hunters (Turner, 2009). Mean prey size of recent lions is
around 130 kg (correcting by age and sex of the prey), but almost half of the prey weigh
around 70 kg, while 40% of the kills are around 220 kg and the rest correspond to prey
above 400 kg ( Rapson and Bernard, 2007). Megafauna species like rhinos (Brain et al.,
1999) or young elephants are opportunistically killed and there is practically not limit
for the smaller prey (Sunquist and Sunquist, 2009). Isotopic studies confirm the role of
Pleistocene lions as top predators, including in their diet significant amounts of
megafauna species (Bocherens et al., 2015).
4
A medium sized hyaenid attributed to the genus Hyaena is present in the Untermassfeld
LFA and some other Middle Pleistocene localities. It is usually identified as Hyaena
prisca, although Arribas and Garrido (2008) consider H. prisca a synonym of H.
brunnea (=Parahyaena brunnea). Both the recent stripped hyaena (Hyaena hyaena) and
the brown hyaena (H. brunnea) are omnivorous and extremely efficient scavengers.
They also consume significant amounts of vegetable matter and opportunistically kill
small mammals and other vertebrates (Holekamp and Kolowski, 2009, Burgener and
Gusset, 2003). Thus we consider than the European Hyaena was a scavenger, unable to
kill ungulates.
Two large social canid species were present in Europe during the Middle and Late
Pleistocene: Cuon alpinus and Canis lupus. The European representatives of the genus
Cuon are considered by some authors as subspecies of the recent species Cuon alpinus,
living in East Asia, while other specialists consider them a different species (Brugal and
Boudadi-Maligne, 2011). In any case, they were hypercarnivorous canids closely related
to the dhole (C. alpinus), which constitutes the better analog to infer their behavior.
Modern dholes are group hunters. Males weigh 15-20 kg and females 10-12 kg. They
hunt medium sized and large ungulates and occasionally eat carrion (Sillero-Zubiri,
2009). Preferred prey are in the size interval 15-50 kg and include fawns of Cervus
unicolor, and Axis axis together with adults of Muntiacus muntjak and Sus scrofa
(Andheria et al., 2007, Venkataraman et al., 1995, Wang and Macdonald, 2009). The
European Cuon was larger in size than the dhole, specially the middle Pleistocene forms
usually classified as Cuon priscus (Brugal and Boudadi-Maligne, 2011). European
dholes most likely preferred prey in the 10-45 kg weight interval, but cooperative
hunting allowed them to effectively kill larger prey. Species in the 45-90 kg interval,
and even in the 90-180 kg interval were likely killed, specially young and physically
depleted individuals. Carrion was probably also eaten.
The diet of extant wolves is extremely variable, but ungulates become their main prey
when available (Sillero-Zubiri, 2009, Ansorge et al., 2006). Pack hunting allows gray
wolves to kill large ungulates like red deers, bisons, moose, or horses (Garrot et al.,
2007, van Duyne et al., 2009). However, in Europe small ungulates are the preferred
prey (Ansorge et al., 2006, Okarma, 1995), while large ungulates seem to be the main
5
prey in North America (Milakovic and Parker, 2011). Isotopic evidence from the Late
Pleistocene site of Valdegoba suggest that aurochs were part of the diet of Pleistocene
wolves, while smaller prey like Castor fiber were negatively selected (Feranec et al.,
2010). Thus, we may assume for the Pleistocene wolfs hunting preferences more similar
to the Northamerican than to the European recent populations. Preferred prey size
would be in the interval 90-360 kg, while prey in the 10-90 kg and 360-1000 kg would
be hunted as secondary prey.
Ursids are, generally speaking, omnivorous species, although the diet of the recent
species ranges from strictly herbivorous in the giant panda (Ailuropoda melanoleuca) to
hypercarnivorous in the case of the polar bear (Ursus maritimus). Similarly, the diet of
the Pleistocene species of the genus Ursus may be classified as different degrees of
omnivory. Proportion of meat in the diet of recent bears varies between species and
populations but, as a general rule, larger animals and more northern populations include
a larger amount of meat in their diet. Scavenging is a common practice for all bears
although some species like brown bears (U. arctos) are also able to kill large ungulates
both fawns and adults (Garshelis, 2009). Six species in the genus Ursus have been
recorded in the set of 27 Pleistocene LFAs: U. etruscus, U. dolinensis , U. thibetanus,
U. deningeri, U. spelaeus and U. arctos.
Palmqvist et al. (2008) infer for U. etruscus a diet similar to the recent U. arctos, based
on their similar tooth morphology. Ursus etruscus was likely an omnivorous bear that
mainly relied on vegetable food on temperate environments. Likely, ungulates in the
10-360 kg. body weight interval were sporadically hunted and carrion opportunistically
consumed. The species U. dolinensis is a small-sized bear described on material from
Atapuerca Gran Dolina site (García and Arsuaga, 2001) that may be present also in
Untermassfeld (Kahlke and Gaudzinski, 2005). A diet similar to U. etruscus is assumed.
The lineage Ursus deningeri-Ursus spelaeus represents an evolutionary trend towards a
herbivorous specialization. Isotopic data on the population of the Sima de los Huesos
site suggest that the diet of U. deningeri included a large amount of vegetal matter (Gar-
cía et al., 2009). The herbivorous behavior of the cave bear (U. spelaeus) was initially
inferred on the basis of the morphology and wear pattern of its dentition (Kurten, 1958)
and it was eventually confirmed by ecomorphological studies(Van Hetheren et al.,
2014), and by isotopic analyses (Bocherens et al., 1994, 2014). Here we consider U.
6
spealeus a strictly herbivorous species, but it is admitted that U. deningeri was able to
sporadically kill medium sized ungulates. Isotopic analyses of subfossil brown bears
from the Alps show a mainly vegetarian diet (Bocherens et al., 2004). Bocherens et al.,
(2015) found isotopic evidence of a high consumption of mammoth meat by brown
bears at the Gravettiann site of Předmostí, although they interpret that mammoths were
mostly consumed as carrion. American grizzly bears (U. arctos horribilis) are able to
kill large ungulates like moose, red deers, or reindeers, although meat proportion in the
diet of recent european brown bears is in the range 9-15% (Bocherens, 2004). Concern-
ing the Asiatic black bear (U. thibetanus) we assume for the Pleistocene populations a
behavior similar to their living counterparts. Asiatic black bears eat large amounts of
vegetable food, including fruits in a large proportion, although small ungulates may
compose a sizable proportion of their diet in some areas (Garshelis, 2009). In our analy-
sis, we considered that Pleistocene brown bears and Asiatic black bears consumed all
other species as carrion, although they were also able to hunt small-sized ungulates.
Since cannibalism and inter-specific aggression between predators are widespread
behaviors (Azevedo et al., 2010; Balme and Hunter, 2013; Palomares and Caro, 1999),
although not very frequent, it has been assumed that all carnivore species practiced
cannibalism sporadically and that larger carnivores occasionally killed and consumed
smaller competitors.
Locality Land Mammal Age Reference
Swanscombe Lower
loam late Galerian / Aurelian (Ashton et al., 1994)
Heppenloch late Galerian / Aurelian (Koenigswald and Heinrich, 1999)
Atapuerca-Galería GIIb late Galerian (Rodríguez et al., 2011)
Caune de l'Arago late Galerian (Alberdi et al., 1997)
Atapuerca-Galería GIIa late Galerian (Rodríguez et al., 2011)
Hundsheim late Galerian (Koenigswald and Heinrich, 1999)
Mauer late Galerian Wagner et al. (2011)
Voigtstedt middle Galerian (Koenigswald and Heinrich, 1999)
Sussenborn middle Galerian (Koenigswald and Heinrich, 1999)
Slivia middle Galerian (Palombo et al., 2000-2002)
Atapuerca Dolina TD6 early Galerian (Rodríguez et al., 2011)
Kozarnika 12 early Galerian (Sirakov et al. 2010; Martínez-Navarro et al., 2012)
Untermassfeld early Galerian (Koenigswald and Heinrich, 1999)
Grotte du Vallonnet III early Galerian (Echassoux, 2004)
Pirro Nord late Villafranchian (Arzarello et al., 2007; Pavia et al., 2012)
7
Ceyssaguet 1 late Villafranchian
(Aouadi, 2001; Kaiser and Croitor, 2004; Tsoukala and Boni-
fay, 2004)
Fuente Nueva-3 late Villafranchian (Martínez-Navarro et al., 2010)
Venta Micena late Villafranchian (Duval et al., 2011; Palmqvist et al., 2010)
Barranco León V BL-D late Villafranchian (Toro-Moyano et al., 2013) (Martínez-Navarro et al., 2010)
Cueva Victoria late Villafranchian (Gibert, 1993; Madurell-Malapeira et al., 2014)
Casa Frata late Villafranchian (Palombo et al., 2000-2002)
Olivola late Villafranchian (Palombo et al., 2000-2002)
Fonelas P-1 middle Villafranchian (Arribas, 2008; Viseras et al., 2006)
Puebla de Valverde middle Villafranchian (Alberdi et al., 1997)
Saint-Vallier LD3 middle Villafranchian (Guérin, 2004)
Gerakarou middle Villafranchian (Palombo et al., 2006)
Seneze middle Villafranchian (Palombo and Valli, 2003-2004)
Table 1: The 27 palaeontological sites providing the empirical data from NQMDB (Neogene-Quaternary
Mammals Database).
The concrete locations of the paleontological sites providing the data are shown in
Figure 1.
Figure 1: Geographical distribution of the palaeontological sites providing the empirical data on trophic
relationships . 1: Swanscombe Lower loam; 2: Heppenloch ; 3: Atapuerca-Galería GIIb; 4: Caune de
l'Arago ; 5: Atapuerca-Galería GIIa; 6: Hundsheim ; 7: Mauer ; 8: Voigtstedt; 9: Sussenborn ; 10: Slivia ;
11: Atapuerca Dolina TD6; 12: Kozarnika 12; 13: Untermassfeld ; 14: Grotte du Vallonnet III; 15: Pirro
Nord ; 16: Ceyssaguet 1 ; 17: Fuente Nueva-3 ; 18: Venta Micena ; 19: Barranco León BL-D; 20: Cueva
Victoria ; 21: Casa Frata ; 22: Olivola ; 23: Fonelas P-1 ; 24: Puebla de Valverde ; 25: Saint-Vallier LD3;
26: Gerakarou ; 27: Seneze.
These data on trophic relations were used to generate one food-web per site.
Specifically, food-webs were constructed as (directed) graphs, where species were
8
represented by vertices and trophic relationships corresponded to arcs pointing to
predators (see figure 2 for clarifications). Notice that our nodes represent original and
not 'trophic species', as is usually done in food web analysis (Dunne, 2009).Trophic
species are equivalent trophic positions in a network that might be occupied by
several original species, provided that they share the same predators and prey. The
reason for such a choice is that we aim at focusing our study on the role of a specific set
of species, and in particular Homo.
Figure 2: Three examples of trophic relations as represented in a food web. Left: A feeds B (or, in other
words, B predates A); Centre: A and B feed (and predate) each other; Right: A feeds B, which also
practices cannibalism.
Both the construction of these paleo food webs and their analysis (subsections 2.2 and
2.3) were conducted using Python and the IGRAPH library of R statistical package (See
http://igraph.org/r/).
2.2 General structural analysis
Once the networks were constructed, we conducted a basic structural analysis in order
to get a general overview of the resulting paleo food-webs, and make a comparison
among them (across different periods and geographical regions) and with modern ones.
First, we calculated some simple structural measures typically applied to this sort of
networks (Dunne, 2009), namely:
S and L: Respectively the total number of species and relationships composing
a food-web.
C (L/S
2
): Connectance or density of trophic relationships in the network. It is
calculated as the total number of connections identified in the network over the
9
total possible existing ones. Consequently, its possible values are bounded
between 0 and 1.
L/S: Average number of connections per species (also referred to as average
degree in network analysis). This indicator provides information on
specialization. The more specialized the carnivores in the network (or the fewer
predators prey herbivores), the lower the value of L/S.
Path: Average path (geodesic) length or, in other words, the average number of
steps along the shortest paths for all possible pairs of network nodes It can be
understood as a global measure of trophic positions averaged across species in
the web (Williams and Martínez, 2000; Capitán et al., 2013).
Path_r: Average value of Path for n samples of an Erdös-Renyi random graph
(Bollobas, 2001) equivalent to the empirical food-web under study. Erdös-Renyi
graphs are regular random graphs where vertices are linked with a given
probability p. This regularity makes it easy to mathematically characterize this
sort of graphs and, as a consequence, they are commonly used as null models
to evaluate empirical features like the Path value. If Path and Path_r are
significantly different, we consider that this feature contains relevant particular
information of the food-web (usually related to functional aspects or formation
process).
CI (Clustering coefficient): Density of triads/triangles in the network (e.g. A-
>B->C->A). Its value is bounded between 0 and 1.
CI_r: Average value of CI for n samples of an Erdös-Renyi random graph. It is
also used as a null model to be compared to the CI calculated for the empirical
food-web.
2.3 Centrality of Homo species
Beyond the general characterization of paleo food-webs during the Pleistocene in
Western Eurasia, the second goal of this work is to assess the (structural) role played by
10
Homo species in that period. In food web analysis, species with a particularly large
impact are labelled as keystone species (Power et al, 1996).
In order to quantitatively identify and characterize keystone species, scholars have used
different sort of centrality measures (Estrada, 2007; Jordán, 2009). Two of the most
consolidated centrality measures applied to this end are the degree and betweeness
centralities (Freeman, 1979). The former, which corresponds to the number of
connections of a certain species, provides information on the diversity of direct trophic
relationships (specialists vs. generalists). The later is related to the intermediate position
of a certain species within the general energy flows among species as represented by the
food web.
For all the paleo food webs including Homo, we calculated these centrality measures
and compared the values across species in order to assess the relevance of Homo within
each food-web. Specifically, the centrality measures selected were: Betweeness, in-
degree (number of connections as predator), out-degree (number of connexions as a
prey) and total degree (the sum of both).
3. Results and Discussion
As a result of data collection and network construction tasks described in subsection
2.1, we obtained 27 paleo food-webs (17 corresponding to the Early Pleistocene and 10
to Middle Pleistocene). Among them, 8 cases include different Homo species as part of
the network. Figure 3 shows two examples of paleo food-web visualization, created by
means of the Gephi visualization software.
11
Figure 3: Two examples of paleo food-web visualization corresponding to Venta Micena (left) and
Atapuerca Galeria GIIa (right). Both figures were created using the Gephi network analysis tool
(http://gephi.github.io/)
3.1 General structural analysis
We calculated the structural measures introduced in subsection 2.2, and obtained the
results shown in Table 2. Networks are arranged according to the chronology of the
fossil assemblage considered in each case.
food web S C(L/S2) L/S Path Path_r
(n=100 |
n=1000)
CI CI_r
(n=100 |
n=1000)
CI/CI
_r
Presence of
Homo species
late Galerian-Aurelian
Swanscombe 17 0.15 2.53 1.16 2.71 | 2.71 0.31 0.26 | 0.26 1.19 x
Heppenloch 16 0.20 3.25 1.11 2.33 | 2.33 0.43 0.36 | 0.36 1.19
Caune de
l'Arago
19 0.27 5.05 1.17 1.95 | 1.95 0.55 0.45 | 0.45 1.22 x
Atapuerca-
Galería GIIa
13 0.28 3.61 1.12 2.04 | 2.03 0.55 0.46 | 0.46 1.19 x
Atapuerca-
Galería GIIb
13 0.21 2.77 1.11 2.32 | 2.32 0.39 0.37 | 0.36 1.08 x
Hundsheim 16 0.38 6.06 1.26 1.69 | 1.69 0.66 0.61 | 0.61 1.08
Mauer 21 0.32 6.81 1.18 1.75 | 1.75 0.62 0.53 | 0.54 1.17 x
middle Galerian
Voigtstedt 17 0.20 3.35 1.17 2.36 | 2.34 0.37 0.35 | 0.34 1.05
Sussenborn 23 0.22 5.09 1.16 2.06 | 2.06 0.48 0.39 | 0.39 1.23
Slivia 21 0.18 3.9 1.19 2.30 | 2.31 0.44 0.33 | 0.33 1.33
12
early Galerian
Grotte du
Vallonnet
17 0.24 4.12 1.08 2.08 | 2.09 0.57 0.41 | 0.41 1.39 x
TD6 14 0.29 4.07 1 1.93 | 1.93 0.56 0.49 | 0.49 1.14
Untermassfeld 24 0.29 6.96 1.25 1.81 | 1.81 0.65 0.49 | 0.49 1.33
late Villafranchian
Venta Micena 19 0.30 5.73 1.19 1.82 | 1.82 0.62 0.51 | 0.50 1.24
Pirro Nord 21 0.29 6.29 1.23 1.82 | 1.81 0.64 0.50 | 0.50 1.28
Cueva
Victoria
19 0.38 7.26 1.2 1.65 | 1.66 0.70 0.61 | 0.61 1.15
Ceyssaguet 1 15 0.37 5.6 1.22 1.71 | 1.71 0.70 0.61 | 0.60 1.16
Fuente Nueva-
3
16 0.26 4.25 1.3 2.02 | 2.01 0.54 0.45 | 0.45 1.2 x
Barranco León 13 0.30 3.92 1.23 1.95 | 1.94 0.57 0.49 | 0.50 1.14 x
Casa Frata 14 0.32 4.43 1.14 1.89 | 1.87 0.59 0.52 | 0.52 1.13
Olivola 18 0.33 5.94 1.17 1.77 | 1.77 0.66 0.55 | 0.55 1.2
middle Villafranchian
Fonelas P-1 21 0.35 7.43 1.09
2
1.70 | 1.69 0.67 0.58 | 0.58 1.15
Puebla de
Valverde
20 0.3 6 1.03 1.82 | 1.82 0.70 0.51 | 0.50 1.4
Saint Vallier 21 0.34 7.14 1.17 1.72 | 1.72 0.69 0.57 | 0.56 1.23
Gerakarou 16 0.30 4.87 1.17 1.87 | 1.87 0.56 0.51 | 0.51 1.09
Seneze 22 0.22 4.95 1.18 2.07 |2.065 0.49 0.39 | 0.39 1.25
Table 2: Structural features of the 27 food webs under study. Indices are defined in subsection 2.1.
Generally speaking, when comparing the obtained networks with modern food-webs
previously studied in the literature (Dunne, 2009), they show some differences that can
be explained from the nature of the scenarios under study or the characteristics of our
dataset. In particular, connectance values for our paleo food webs are higher than the
modern ones (which show an average of 0.11). This could be related to the highly
relevant presence of scavenging in our networks (far above the levels usually observed
in modern food webs). Actually, we re-calculated the connectance of the paleo food
webs once scavenging was subtracted, and found similar values to modern food webs.
CI (Clustering coefficient) values are also higher for our paleo food webs (both in
absolute terms and relatively as compared to CI_r). This could be related to a higher
number of trophic interactions among carnivore species. More carnivore species
competing for the same prey increases the number of triads when carnivores also
consume each other.
13
When we compare our networks across periods, we observe some trends that provide
clues about the transformations experimented by faunas along the Pleistocene (see
Figure 4). Specifically, connectance (usually related to structural stability of food webs)
shows a decreasing trend from the Villafranchian to the Galerian, which could be related
to the Mid-Pleistocene Revolution. Besides, CI values show two phases with a
transition between the early and the middle Galerian periods (Figure 4). Such a
transition correlated with a change on the number of carnivore species in the studied
food webs, which can be easily seen in Figure 3. The high predator/prey ratios in the
Villafranchian LFAs, evident in our food webs, is a well known phenomenon previously
pointed out by other authors (Raia et al. 2007, Croitor and Brugal, 2010, Rodríguez et
al. 2012). As mentioned above when comparing with modern food webs, a broader
presence of carnivore species could explain the higher CI values of the Villafranchian
and early Galerian food webs.
The MPR strongly affected the European large mammal fauna and, specifically, caused
a reorganization of the carnivore guild, with the disappearance of several
hypercarnivore species, the arrival of more versatile social predators and a decrease in
carnivore richness (Croitor and Brugal, 2010; Palombo, 2014a, Rodríguez et al. 2012).
Moreover, a change in the fauna of large herbivore mammals also occurred, with a
general trend towards an increase in body size. The new predators were unable to kill
the largest species and, as a consequence, much of this megafauna was free of predation
(Croitor and Brugal, 2010), and bottom up regulatory mechanisms gained more
relevance in the ecosystems (Raia et al., 2007, Rodríguez et al., 2012). The main effect
of all these changes on the food webs was to decrease the number of interactions. With
all this, the faunal turnover triggered a reorganization of the food webs, visible in the
decrease of the clustering coefficient (CI) and the connectance. Connectance is a key
feature of the food web related to its complexity (Dunne et al. 2002, Poisot and Gravel,
2014). Thus, one of the consequences of the MPR on the European ecosystems was a
simplification of the food webs, something that might have had an effect on their
stability.
Concerning the effect of the arrival of hominins on the European food webs, the two
late Villafranchian food webs that include Homo (Fuente Nueva 3 and Barranco Leon)
14
show values of connectance similar to other food webs of the same period. The
clustering coefficient of these two food webs is relatively low, but higher than in a
random food web of the same size (Table 2), In light of these results, the first European
hominins integrated in the existing food webs without inducing any significant
structural change on them. This is in agreement with marginal role for hominins in those
food webs, as has been proposed elsewhere (Rodríguez et al., 2012).
0.12 0.18 0.24 0.30 0.36
1.0 1.08 1.16 1.24 1.32
Conectance
Path length
Clustering
0.35 0.45 0.55 0.65 0.75
Villafranchian
Galerian
middle late
early
middle
0.5
0.6
0.7
0.8
0.9
1.0
1.1
1.2
1.3
1.4
1.5
1.6
1.7
1.8
1.9
2.0
2.1
2.2
2.3
2.4
2.5
2.6
Brunhes
Matuyama
Jaramillo
Olduvai
late
12 16 20 24 28
S
Arrival of Homo
Change
in Cyclicity
acheulean
“Pre-acheulean”
Ice Increase
Oldowan
Events
H. heidelbergensis
H. antecessor
Figure 4. Changes in food web parameters through time in relation to climate changes and some key
events in the human colonization on Europe.
3.2 Centrality of Homo species
The centrality values obtained for the 8 paleo food-webs including Homo species are
presented in Table 3. Not surprisingly, carnivores playing a double role as prey and
predators show the highest scores (i.e. they have more interactions and occupy
intermediate positions between 'purely prey' and 'purely predator' species). Among
them, Homo (independently of the concrete species) presents the highest value for all
cases except Barranco León and Mauer. This is explained by the generalist trophic be-
haviour of hominins and their role as both predator and prey. Focusing on
betweeness, in some cases (i.e. Swanscombe, Grotte du Vallonnet and Fuente Nueva-3)
15
Homo species present values several times higher than the following species. This result
suggests that, when present, hominins were a central element of the food web, and a
highly relevant one in channeling the energy fluxes.
Differences between Homo antecessor and Homo heidelbergensis, or between popula-
tions of Oldowan and Acheulean culture are not visible: This might be explained
in part because of the limited number of food webs including Homo that have been
analysed. Moreover, the analysis does not distinguish between hunting and scavenging
interactions while, these strategies to obtain meat might have a different relevance, for
late Villafranchian and Galerian populations Espigares et al., 2013; Huguet et al., 2013;
Saladié et al., 2011).
Apparently, hominins occupied a central position in the European food webs since their
arrival to the continent in the late Villafranchian. This result seems to be in contradiction
with the interpretations, mentioned above, of a small effect of the arrival of hominins to
Europe on the structure of food webs and of a marginal role played by hominins in the
community. However, these are two sides of the same medal. The late Villafranchian
hominin populations were likely opportunistic omnivores. They were a member of the
guild of secondary consumers, but a marginal one. Carrion was likely an important re-
source for hominins and this connected them to every species in the web. Moreover,
they were a suitable prey for many top predators, and this also increased the number of
their connections. It is also important to note that our analysis takes all interactions as
equal, whist in an actual food web they differ in intensity. Hominins were a central ele-
ment in the late Villafranchian food webs, but also redundant, since there are other
species with a similar number of connections: the scavenger Pachycrocuta brevirostris
and the omnivorous canid Canis mosbachensis. From this point of view, hominins can
not be considered a keystone species in those communities.
If attention is focused on the late Villafranchian food webs, betweeness is specially high
for Homo in Fuente Nueva-3, although moderate in Barranco Leon. Interestingly, the
species with the highest value of betweeness in Barranco Leon is Canis mosbachensis,
and the small canids of the line etruscus/mosbachensis are the species with the highest
value of betweeness in the late Villafarnchian localities were Homo is not present, (Pirro
Nord, Venta Micena, Cueva Victoria, Ceyssaguet and Olivola) (See Supplementary
16
Material). These canids had a diet similar to modern coyotes (Rodríguez et al., 2012 and
references therein), omnivorous social canids that eat invertebrates, small mammals,
ungulates and some fruits. Coyotes consume large mammals, usually as carrion, but
they also hunt opportunistically small ungulates especially fawns (Sillero-Zubiri, 2009).
It is tempting to establish a parallelism between the role played in the late Villafranchian
food webs by those omnivorous canids and the role played by the recently arrived ho-
minins. However, this does not imply that Canis etruscus/mosbachensis and Homo oc-
cupied similar niches, since both species coexisted in most Local Faunas. It only indi-
cates that both species occupied similar central positions in the food webs, due to their
omnivorous and opportunistic behavior.
Species Betweenness Connexions
(total)
Connexions
(as predator)
Connexions
(as prey)
Swanscombe
Canis lupus
Panthera leo
Ursus spelaeus
Macaca sylvanus
Capreolus capreolus
Trogontherium cuvieri
Dama dama
Sus scrofa
Homo sp.
Cervus elaphus
Bison priscus
Bos primigenius
Megaloceros giganteus
Equus ferus
Stephanorhinus hemitoechus
Stephanorhinus kirchbergensis
Elephas antiquus
1
0
0
0
0
0
0
0
7
0
0
0
0
0
0
0
0
15
16
2
3
3
3
3
2
20
2
3
3
3
3
2
2
1
12
14
0
0
0
0
0
0
17
0
0
0
0
0
0
0
0
3
2
2
3
3
3
3
2
3
2
3
3
3
3
2
2
1
Caune de l'Arago
Canis etruscus
Cuon priscus
Lynx pardinus
Panthera pardus
Panthera leo
Ursus deningeri
Rupicapra rupicapra
Homo heidelbergensis
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Rangifer tarandus
Ovis ammon
Bison priscus
Bos primigenius
Praeovibos priscus
Equus ferus
Stephanorhinus hemitoechus
4.28
4.28
0.2
0.5
2.03
2.03
0
5.66
0
0
0
0
0
0
0
0
0
0
24
21
7
15
21
21
6
24
4
3
4
5
5
6
6
4
5
5
19
15
1
10
16
16
0
19
0
0
0
0
0
0
0
0
0
0
5
6
6
5
5
5
6
5
4
3
4
5
5
6
6
4
5
5
17
Stephanorhinus kirchbergensis 0 6 0 6
Atapuerca-Galería GIIa
Canis lupus
Cuon alpinus
Lynx pardinus
Panthera leo
Hystrix vinogradovi
Homo sp.
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Bison sp.
Praemegaceros solilhacus
Equus ferus
Stephanorhinus hemitoechus
1
1.5
0
0
0
3.5
0
0
0
0
0
0
0
15
16
5
12
5
17
3
3
4
3
4
4
3
11
12
1
10
0
13
0
0
0
0
0
0
0
4
4
4
2
5
4
3
3
4
3
4
4
3
Atapuerca-Galería GIIb
Cuon alpinus
Lynx pardinus
Panthera leo
Hystrix vinogradovi
Homo sp.
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Equus hydruntinus
Bison sp.
Praemegaceros solilhacus
Equus ferus
Stephanorhinus hemitoechus
1.5
0
0
0
2.5
0
0
0
0
0
0
0
0
16
3
12
4
16
2
2
3
3
2
3
3
3
13
0
10
0
13
0
0
0
0
0
0
0
0
3
3
2
4
3
2
2
3
3
2
3
3
3
Mauer
Canis mosbachensis
Lynx issiodorensis
Panthera pardus
Pliocrocuta perrieri
Panthera leo
Homotherium sp.
Ursus tibethanus
Ursus deningeri
Capreolus capreolus
Castor fiber
Trogontherium cuvieri
Sus scrofa
Homo heidelbergensis
Cervus elaphus
Bison schoetensacki
Bison voigtstedtensis
Cervalces latifrons
Equus mosbachensis
Hippopotamus sp.
Stephanorhinus hundsheimensis
Elephas antiquus
6.18
1.71
0.30
1.93
0.43
2.41
2.69
6.18
0
0
0
0
6.18
0
0
0
0
0
0
0
0
29
12
15
22
22
26
28
29
7
6
8
6
28
5
7
5
7
7
5
7
5
21
4
7
14
15
19
21
21
0
0
0
0
21
0
0
0
0
0
0
0
0
8
8
8
8
7
7
7
8
7
6
8
6
7
5
7
5
7
7
5
7
5
Grotte du Vallonnet
Arvernoceros giulii
Bison schoetensacki
Dama vallonnetensis
Hemitragus bonali
Soergelia elisabethae
Sus sp.
Equus stenonis
Stephanorhinus hundsheimensis
Homo sp.
Mammuthus meridionalis
0
0
0
0
0
0
0
0
27.66
0
5
4
6
6
5
7
4
3
24
3
0
0
0
0
0
0
0
0
17
0
5
4
6
6
5
7
4
3
7
3
18
Hystrix refossa
Acinonyx pardinensis
Lynx issiodorensis
Pachycrocuta brevirostris
Panthera gombaszoegensis
Panthera pardus
Ursus etruscus
0
0
0
0
2.66
0.66
0
7
15
9
20
19
17
20
0
9
3
17
13
11
17
7
6
6
3
6
6
3
Fuente Nueva-3
Canis mosbachensis
Lycaon lycaonoides
Lynx sp.
Pachycrocuta brevirostris
Ursus sp.
Hystrix sp.
Metacervoceros rhenanus
Hemitragus albus
Homo sp.
Soergelia sp.
Equus altidens
Bison sp.
Praemegaceros verticornis
Hippopotamus antiquus
Stephanorhinus hundsheimensis
Mammuthus meridionalis
6.66
1.16
0.5
3.16
0.0
0.0
0.0
0.0
15.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
21
14
8
20
12
5
6
5
21
4
4
3
3
3
3
4
16
9
3
16
8
0
0
0
16
0
0
0
0
0
0
0
5
5
5
4
4
5
6
5
5
4
4
3
3
3
3
4
Barranco León
Canis mosbachensis
Lycaon lycaonoides
Pachycrocuta brevirostris
Ursus sp.
Metacervoceros rhenanus
Hemitragus albus
Homo sp.
Bison sp.
Praemegaceros verticornis
Equus stenonis
Equus suessenbornensis
Hippopotamus antiquus
Stephanorhinus hundsheimensis
6.83
0.33
2.83
0.0
0.0
0.0
4.0
0.0
0.0
0.0
0.0
0.0
0.0
18
10
17
11
5
5
17
3
3
4
3
3
3
13
5
13
7
0
0
13
0
0
0
0
0
0
5
5
4
4
5
5
4
3
3
4
3
3
3
Table 3: Centrality metrics for all species in paleo food webs including Homo. In all cases (except
Barranco León), we observe that the different Homo species show the highest values of betweeness and
(total) degree centralities.
4. Conclusions
Network analysis of putative food webs reveals itself as a powerful tool to address the
study of trophic relationship in past mammalian communities. The results presented
here show that the Pleistocene food webs of Europe shared basic features with modern
food webs, although differences in the values of some parameters might be significant.
Moreover, a marked change in the parameters that describe the food webs and related to
the Mid-Pleistocene Revolution challenges has been detected. Villafranchian food webs
19
were more complex, included more interactions than Galerian food webs. Our results
also highlight the trophic position of hominins in the web, and show them as a central
species that channeled energy fluxes.
Future extensions of the present work might deep into two main aspects already stressed
here, namely the comparison among different Homo species and the potential of our
dataset to show evidences of possible evolutionary changes of feeding relationships.
Following recent works in the literature, these aspects could be addressed by extending
comparisons with modern food webs to other structural features such as intervality .
This property relates to the number of 'niche' variables needed to reproduce food-web
structure (Stoufer et al, 2006; Capitan et al, 2013). By exploiting this particularity, we
might be able to determine whether different Homo species could roughly correspond to
the same niche (and, therefore, be considered as a single trophic species). Moreover,
intervality has already been applied to studies in other evolutionary contexts (Capitan et
al, 2015).
Acknowledgements
This research was supported byModelling human settlement, fauna and flora
dynamics in Europe during the Mid-Pleistocene Revolution (1.2 to 0.4 Ma) Project
(#1403), funded by the INQUA Humans and Biosphere Commission and by the
MINECO project CGL2012-38434-C03-02. S. L. is supported by the Ramón y Cajal
programme through the grant RYC-2012-01043.
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Figure captions
Figure 1: Geographical distribution of the palaeontological sites providing the
empirical data on trophic relationships . 1: Swanscombe Lower loam; 2: Heppenloch ;
3: Atapuerca-Galería GIIb; 4: Caune de l'Arago ; 5: Atapuerca-Galería GIIa; 6:
Hundsheim ; 7: Mauer ; 8: Voigtstedt; 9: Sussenborn ; 10: Slivia ; 11: Atapuerca Dolina
TD6; 12: Kozarnika 12; 13: Untermassfeld ; 14: Grotte du Vallonnet III; 15: Pirro
Nord ; 16: Ceyssaguet 1 ; 17: Fuente Nueva-3 ; 18: Venta Micena ; 19: Barranco León
BL-D; 20: Cueva Victoria ; 21: Casa Frata ; 22: Olivola ; 23: Fonelas P-1 ; 24: Puebla
de Valverde ; 25: Saint-Vallier LD3; 26: Gerakarou ; 27: Seneze.
Figure 2: Three examples of trophic relations as represented in a food web. Left: A
feeds B (or, in other words, B predates A); Centre: A and B feed (and predate) each
other; Right: A feeds B, which also practices cannibalism.
Figure 3: Two examples of paleo food-web visualization corresponding to Cueva
29
Victoria (left) and Atapuerca Galeria GIIa (right). Both figures were created using the
Gephi network analysis tool (http://gephi.github.io/)
Figure 4: Changes in food web parameters through time in relation to climate changes
and some key events in the human colonization on Europe.
Table 1: The 27 paleontological sites providing the empirical data from NQMDB
(Neogene-Quaternary Mammals Database.
Locality Land Mammal Age Reference
Swanscombe Lower loam late Galerian / Aurelian (Ashton et al., 1994)
Heppenloch late Galerian / Aurelian (Koenigswald and Heinrich, 1999)
Atapuerca-Galería GIIb late Galerian (Rodríguez et al., 2011)
Caune de l'Arago late Galerian (Alberdi et al., 1997)
Atapuerca-Galería GIIa late Galerian (Rodríguez et al., 2011)
Hundsheim late Galerian (Koenigswald and Heinrich, 1999)
Mauer late Galerian Wagner et al. (2011)
Voigtstedt middle Galerian (Koenigswald and Heinrich, 1999)
Sussenborn middle Galerian (Koenigswald and Heinrich, 1999)
Slivia middle Galerian (Palombo et al., 2000-2002)
30
Atapuerca Dolina TD6 early Galerian (Rodríguez et al., 2011)
Kozarnika 12 early Galerian (Sirakov et al. 2010; Martínez-Navarro et al., 2012)
Untermassfeld early Galerian (Koenigswald and Heinrich, 1999)
Grotte du Vallonnet III early Galerian (Echassoux, 2004)
Pirro Nord late Villafranchian (Arzarello et al., 2007; Pavia et al., 2012)
Ceyssaguet 1 late Villafranchian
(Aouadi, 2001; Kaiser and Croitor, 2004; Tsoukala and Bonifay,
2004)
Fuente Nueva-3 late Villafranchian (Martínez-Navarro et al., 2010)
Venta Micena late Villafranchian (Duval et al., 2011; Palmqvist et al., 2010)
Barranco León V BL-D late Villafranchian (Toro-Moyano et al., 2013) (Martínez-Navarro et al., 2010)
Cueva Victoria late Villafranchian (Gibert, 1993; Madurell-Malapeira et al., 2014)
Casa Frata late Villafranchian (Palombo et al., 2000-2002)
Olivola late Villafranchian (Palombo et al., 2000-2002)
Fonelas P-1 middle Villafranchian (Arribas, 2008; Viseras et al., 2006)
Puebla de Valverde middle Villafranchian (Alberdi et al., 1997)
Saint-Vallier LD3 middle Villafranchian (Guérin, 2004)
Gerakarou middle Villafranchian (Palombo et al., 2006)
Seneze middle Villafranchian (Palombo and Valli, 2003-2004)
Table 2: Structural features of the 27 food webs under study. Indices are defined in
subsection 2.1.
food web S C(L/S2) L/S Path Path_r
(n=100 |
n=1000)
CI CI_r
(n=100 |
n=1000)
CI/CI
_r
Presence of
Homo species
late Galerian-Aurelian
Swanscombe 17 0.15 2.53 1.16 2.71 | 2.71 0.31 0.26 | 0.26 1.19 x
Heppenloch 16 0.20 3.25 1.11 2.33 | 2.33 0.43 0.36 | 0.36 1.19
Caune de
l'Arago
19 0.27 5.05 1.17 1.95 | 1.95 0.55 0.45 | 0.45 1.22 x
Atapuerca-
Galería GIIa
13 0.28 3.61 1.12 2.04 | 2.03 0.55 0.46 | 0.46 1.19 x
31
Atapuerca-
Galería GIIb
13 0.21 2.77 1.11 2.32 | 2.32 0.39 0.37 | 0.36 1.08 x
Hundsheim 16 0.38 6.06 1.26 1.69 | 1.69 0.66 0.61 | 0.61 1.08
Mauer 21 0.32 6.81 1.18 1.75 | 1.75 0.62 0.53 | 0.54 1.17 x
middle Galerian
Voigtstedt 17 0.20 3.35 1.17 2.36 | 2.34 0.37 0.35 | 0.34 1.05
Sussenborn 23 0.22 5.09 1.16 2.06 | 2.06 0.48 0.39 | 0.39 1.23
Slivia 21 0.18 3.9 1.19 2.30 | 2.31 0.44 0.33 | 0.33 1.33
early Galerian
Grotte du
Vallonnet
17 0.24 4.12 1.08 2.08 | 2.09 0.57 0.41 | 0.41 1.39 x
TD6 14 0.29 4.07 1 1.93 | 1.93 0.56 0.49 | 0.49 1.14
Untermassfeld 24 0.29 6.96 1.25 1.81 | 1.81 0.65 0.49 | 0.49 1.33
late Villafranchian
Venta Micena 19 0.30 5.73 1.19 1.82 | 1.82 0.62 0.51 | 0.50 1.24
Pirro Nord 21 0.29 6.29 1.23 1.82 | 1.81 0.64 0.50 | 0.50 1.28
Cueva
Victoria
19 0.38 7.26 1.2 1.65 | 1.66 0.70 0.61 | 0.61 1.15
Ceyssaguet 1 15 0.37 5.6 1.22 1.71 | 1.71 0.70 0.61 | 0.60 1.16
Fuente Nueva-
3
16 0.26 4.25 1.3 2.02 | 2.01 0.54 0.45 | 0.45 1.2 x
Barranco León 13 0.30 3.92 1.23 1.95 | 1.94 0.57 0.49 | 0.50 1.14 x
Casa Frata 14 0.32 4.43 1.14 1.89 | 1.87 0.59 0.52 | 0.52 1.13
Olivola 18 0.33 5.94 1.17 1.77 | 1.77 0.66 0.55 | 0.55 1.2
middle Villafranchian
Fonelas P-1 21 0.35 7.43 1.09
2
1.70 | 1.69 0.67 0.58 | 0.58 1.15
Puebla de
Valverde
20 0.3 6 1.03 1.82 | 1.82 0.70 0.51 | 0.50 1.4
Saint Vallier 21 0.34 7.14 1.17 1.72 | 1.72 0.69 0.57 | 0.56 1.23
Gerakarou 16 0.30 4.87 1.17 1.87 | 1.87 0.56 0.51 | 0.51 1.09
Seneze 22 0.22 4.95 1.18 2.07 |2.065 0.49 0.39 | 0.39 1.25
Table 3: Centrality metrics for all species in paleo food webs including Homo. In all
cases (except Barranco León), we observe that the different Homo species show the
highest values of betweeness and (total) degree centralities.
Species Betweenness Connexions
(total)
Connexions
(as predator)
Connexions
(as prey)
Swanscombe
Canis lupus
Panthera leo
1
0
15
16
12
14
3
2
32
Ursus spelaeus
Macaca sylvanus
Capreolus capreolus
Trogontherium cuvieri
Dama dama
Sus scrofa
Homo sp.
Cervus elaphus
Bison priscus
Bos primigenius
Megaloceros giganteus
Equus ferus
Stephanorhinus hemitoechus
Stephanorhinus kirchbergensis
Elephas antiquus
0
0
0
0
0
0
7
0
0
0
0
0
0
0
0
2
3
3
3
3
2
20
2
3
3
3
3
2
2
1
0
0
0
0
0
0
17
0
0
0
0
0
0
0
0
2
3
3
3
3
2
3
2
3
3
3
3
2
2
1
Caune de l'Arago
Canis etruscus
Cuon priscus
Lynx pardinus
Panthera pardus
Panthera leo
Ursus deningeri
Rupicapra rupicapra
Homo heidelbergensis
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Rangifer tarandus
Ovis ammon
Bison priscus
Bos primigenius
Praeovibos priscus
Equus ferus
Stephanorhinus hemitoechus
Stephanorhinus kirchbergensis
4.28
4.28
0.2
0.5
2.03
2.03
0
5.66
0
0
0
0
0
0
0
0
0
0
0
24
21
7
15
21
21
6
24
4
3
4
5
5
6
6
4
5
5
6
19
15
1
10
16
16
0
19
0
0
0
0
0
0
0
0
0
0
0
5
6
6
5
5
5
6
5
4
3
4
5
5
6
6
4
5
5
6
Atapuerca-Galería GIIa
Canis lupus
Cuon alpinus
Lynx pardinus
Panthera leo
Hystrix vinogradovi
Homo sp.
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Bison sp.
Praemegaceros solilhacus
Equus ferus
Stephanorhinus hemitoechus
1
1.5
0
0
0
3.5
0
0
0
0
0
0
0
15
16
5
12
5
17
3
3
4
3
4
4
3
11
12
1
10
0
13
0
0
0
0
0
0
0
4
4
4
2
5
4
3
3
4
3
4
4
3
Atapuerca-Galería GIIb
Cuon alpinus
Lynx pardinus
Panthera leo
Hystrix vinogradovi
Homo sp.
Cervus elaphus
Dama clactoniana
Hemitragus bonali
Equus hydruntinus
Bison sp.
Praemegaceros solilhacus
Equus ferus
Stephanorhinus hemitoechus
1.5
0
0
0
2.5
0
0
0
0
0
0
0
0
16
3
12
4
16
2
2
3
3
2
3
3
3
13
0
10
0
13
0
0
0
0
0
0
0
0
3
3
2
4
3
2
2
3
3
2
3
3
3
33
Mauer
Canis mosbachensis
Lynx issiodorensis
Panthera pardus
Pliocrocuta perrieri
Panthera leo
Homotherium sp.
Ursus tibethanus
Ursus deningeri
Capreolus capreolus
Castor fiber
Trogontherium cuvieri
Sus scrofa
Homo heidelbergensis
Cervus elaphus
Bison schoetensacki
Bison voigtstedtensis
Cervalces latifrons
Equus mosbachensis
Hippopotamus sp.
Stephanorhinus hundsheimensis
Elephas antiquus
6.18
1.71
0.30
1.93
0.43
2.41
2.69
6.18
0
0
0
0
6.18
0
0
0
0
0
0
0
0
29
12
15
22
22
26
28
29
7
6
8
6
28
5
7
5
7
7
5
7
5
21
4
7
14
15
19
21
21
0
0
0
0
21
0
0
0
0
0
0
0
0
8
8
8
8
7
7
7
8
7
6
8
6
7
5
7
5
7
7
5
7
5
Grotte du Vallonnet
Arvernoceros giulii
Bison schoetensacki
Dama vallonnetensis
Hemitragus bonali
Soergelia elisabethae
Sus sp.
Equus stenonis
Stephanorhinus hundsheimensis
Homo sp.
Mammuthus meridionalis
Hystrix refossa
Acinonyx pardinensis
Lynx issiodorensis
Pachycrocuta brevirostris
Panthera gombaszoegensis
Panthera pardus
Ursus etruscus
0
0
0
0
0
0
0
0
27.66
0
0
0
0
0
2.66
0.66
0
5
4
6
6
5
7
4
3
24
3
7
15
9
20
19
17
20
0
0
0
0
0
0
0
0
17
0
0
9
3
17
13
11
17
5
4
6
6
5
7
4
3
7
3
7
6
6
3
6
6
3
Fuente Nueva-3
Canis mosbachensis
Lycaon lycaonoides
Lynx sp.
Pachycrocuta brevirostris
Ursus sp.
Hystrix sp.
Metacervoceros rhenanus
Hemitragus albus
Homo sp.
Soergelia sp.
Equus altidens
Bison sp.
Praemegaceros verticornis
Hippopotamus antiquus
Stephanorhinus hundsheimensis
Mammuthus meridionalis
6.66
1.16
0.5
3.16
0.0
0.0
0.0
0.0
15.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
21
14
8
20
12
5
6
5
21
4
4
3
3
3
3
4
16
9
3
16
8
0
0
0
16
0
0
0
0
0
0
0
5
5
5
4
4
5
6
5
5
4
4
3
3
3
3
4
Barranco León
Canis mosbachensis
Lycaon lycaonoides
Pachycrocuta brevirostris
Ursus sp.
Metacervoceros rhenanus
6.83
0.33
2.83
0.0
0.0
18
10
17
11
5
13
5
13
7
0
5
5
4
4
5
34
Hemitragus albus
Homo sp.
Bison sp.
Praemegaceros verticornis
Equus stenonis
Equus suessenbornensis
Hippopotamus antiquus
Stephanorhinus hundsheimensis
0.0
4.0
0.0
0.0
0.0
0.0
0.0
0.0
5
17
3
3
4
3
3
3
0
13
0
0
0
0
0
0
5
4
3
3
4
3
3
3
35

Supplementary resource (1)

... However, the Early Pleistocene paleocommunities do not fit the relationship observed in the present, although the single Middle Pleistocene paleocommunity that passed the completeness test does; therefore, it is tempting to relate this difference to the profound rearrangement of the European ecosystems caused by the Mid-Pleistocene Revolution (MPR; Palombo, 2017). It may be speculated that, during the Early Pleistocene, the ecosystems of Southern Europe were able to sustain high carnivoran richness, but low population densities, with a relatively low carrying capacity due to the specific structure of those mammal communities (Rodríguez et al., 2012;Lozano et al., 2016). According to this hypothesis, the relationship between species richness and productivity at an equilibrium state in those paleocommunities would be different from that observed in the present communities. ...
... Indeed, opportunism might have been the more successful strategy for the survival of hominins in the Early Pleistocene European ecosystems. Interestingly, the analysis of the structure of Early Pleistocene paleofood webs including Homo species by Lozano et al. (2016) suggests that hominins were a relevant species in channeling the energy fluxes. If hominins were opportunistic omnivores, they would have benefited from a low encounter rate with predators, while taking advantage of the abundant edible resources found in the carcasses abandoned in the landscape by Megantereon, opportunistically hunting ungulates, and complementing their diets with plant foods and other edible resources. ...
Article
Carrying capacity, the maximum biomass that an ecosystem can sustain over the long term, strongly influences several ecological processes and it is also one of the main determinants of biodiversity. Here, we estimate the carrying capacity (CC) of the late Early and early Middle Pleistocene ecosystems of Europe, using equations describing the relationship between CC and climatic variables observed in the present, as well as maps of inferred paleotemperature and paleoprecipitation. Maps of paleoclimate values were interpolated from the composite benthic stable oxygen isotope ratios and a transfer function was used to estimate ungulate carrying capacity (CCU) from the interpolated mean annual temperature and annual precipitation values. Carnivoran carrying capacity was subsequently estimated from ungulate carrying capacity and the effect of CC on the carnivoran faunas was analyzed in 12 paleocommunities from Southern Europe. Our results show that carnivoran species richness is strongly related to ungulate carrying capacity in recent ecosystems, but the late Early Pleistocene paleocommunities from Southern Europe included much richer carnivore guilds than would be expected for a recent community with a similar ungulate carrying capacity. Thus, those late Early Pleistocene ecosystems supported a high number of carnivoran species, but the carnivoran biomass they could support was relatively low. Consequently, carnivorans occurred at low densities in Southern Europe compared to the recent African savanna ecosystems, but likely also compared to coeval East African ecosystems. Consequently, the first Homo populations that arrived in Europe at the end of the late Early Pleistocene found mammal communities consisting of a low number of prey species, which accounted for a moderate herbivore biomass, as well as a diverse but not very abundant carnivore guild. This relatively low carnivoran density implies that the hominin-carnivore encounter rate was lower in the European ecosystems than in the coeval East African environments, suggesting that an opportunistic omnivorous hominin would have benefited from a reduced interference from the carnivore guild.
... Wolves are one of the most prominent carnivore taxa of the Northern Hemisphere, appearing in a number of ancient sites as a competitor with humans [1,2]. The genus Canis [3] has been most recently estimated to have emerged towards the Messinian stage of the Miocene, dated at approximately 5.7 Ma, with Bayesian inferred Highest Posterior Density (HPD) intervals between 8.5 and 4.0 Ma [4]. ...
... To this extent, some authors hypothesize the trophic pressure and competition for resources among these species [10,[12][13][14][15][16][17][18][19]. From a similar perspective, being a close competitor with large felids at the time, other studies hypothesize these canids to have had a dynamic role in complex food chains throughout the Pleistocene [1,2]. As of the Upper Palaeolithic, interactions between canid and hominin species begin to change, with possible evidence of domestication and collaboration as early as >30 Kya [20][21][22][23][24]. ...
Article
Full-text available
Human populations have been known to develop complex relationships with large carnivore species throughout time, with evidence of both competition and collaboration to obtain resources throughout the Pleistocene. From this perspective, many archaeological and palaeontological sites present evidence of carnivore modifications to bone. In response to this, specialists in the study of microscopic bone surface modifications have resorted to the use of 3D modeling and data science techniques for the inspection of these elements, reaching novel limits for the discerning of carnivore agencies. The present research analyzes the tooth mark variability produced by multiple Iberian wolf individuals, with the aim of studying how captivity may affect the nature of tooth marks left on bone. In addition to this, four different populations of both wild and captive Iberian wolves are also compared for a more in-depth comparison of intra-species variability. This research statistically shows that large canid tooth pits are the least affected by captivity, while tooth scores appear more superficial when produced by captive wolves. The superficial nature of captive wolf tooth scores is additionally seen to correlate with other metric features, thus influencing overall mark morphologies. In light of this, the present study opens a new dialogue on the reasons behind this, advising caution when using tooth scores for carnivore identification and contemplating how elements such as stress maybeaffecting the wolves under study.
... The alteration of habitat conditions is well known to deeply influence mammal communities which may develop new community structure and ways to exploit the available plant resources (DeMiguel et al., 2010;DeMiguel, 2016;Lozano et al., 2016;Palombo, 2016a). Herbivorous mammals, for example, are highly susceptible to variation in vegetal communities and, hence, their feeding strategies accurately reflect plant resource availability and environmental settings. ...
Article
The intra-montane Guadix-Baza Basin is one of the few continental basins in Europe that hosts a well-dated set of fossiliferous sites spanning from the latest Miocene to the late Middle Pleistocene. The Cúllar de Baza 1 (CB-1) represents a key site to investigate the effects of the Early-Middle Pleistocene Transition, considered a fundamental transformation in the Earth’s climate state. Our review and update of the large mammal assemblage, and particularly equids, is of paramount relevance to understand the systematic affinities and the evolution of the Early and Middle Pleistocene European horses. We confirm the occurrence of two different taxa, the medium sized Equus altidens and the larger E. suessenbornensis. Moreover, we illustrate that CB-1 is essential for the biochronological studies of the latest Early Pleistocene/Middle Pleistocene transition (Epivillafranchian/Galerian ELMA); in particular with regard to the Last Occurrences of the Etruscan rhino Stephanorhinus etruscus and the large deer Megaloceros savini and the First Occurrence of the water-rat Arvicola mosbachensis in the Iberian peninsula. Finally, a development of a mosaic environment characterised the CB-1 site contrasting with the conditions reported for other Iberian late Early and Middle Pleistocene localities.
... Palmqvist et al. (2008b) argued that C. mosbachensis body size and craniodental traits are more similar to modern jackals. Dental morphology points to an omnivorous diet for this canid (Palmqvist et al., 2008b;Lozano et al., 2016). On the other hand, Flower and Schreve (2014) stated that C. mosbachensis had a reduced crushing capability and potential increased slicing ability indicated by elongated upper carnassials implying a more carnivorous mode than C. etruscus and more dietary specialization than C. lupus. ...
Article
The northern coastal area of the Iberian Peninsula shows an excellent archaeo-paleontological record with a unique representation of Pleistocene mammalian fossils. While the Late Pleistocene is better recorded, the Middle Pleistocene record remains more fragmentary. The Punta Lucero site (Biscay) has yielded the most important fossil assemblage of the middle Middle Pleistocene for the northern Iberian Peninsula in both, number of identified specimens and taxonomic diversity. Punta Lucero constitutes a unique opportunity to evaluate Middle Pleistocene mammalian resource and habitat use, and trophic dynamics employing a combined approach: biogeochemical analysis and mathematical modeling. Stable isotope analysis points to resource partitioning between Punta Lucero cervids and bovids. Stable isotope analysis and trophic modeling evidence resource overlap and interspecific competition among predators, especially between the scimitar-toothed cat Homotherium latidens and the European jaguar Panthera gombaszoegensis. The trophic resource availability modeling assumes that Canis mosbachensis consumed a 20% of preys of more than 10 kg, mainly as carrion. Thus, while there would be a taxonomic overlap with those preys consumed by the large felids, the different strategy would have facilitated the coexistence of these canids with larger carnivores. Trophic modeling indicates a high competition among the predator guild. The potential presence of hominins in the area would have reached to an unsustainable situation. However, the potential presence of other prey species, such as Equus sp., would have made the ecosystem more sustainable. The methodology followed in this study highlights the potential of multidisciplinary approaches in the assessment of Pleistocene faunal dynamics.
... We reviewed all faunal lists and applied uniform taxonomic criteria (see Rodríguez et al., 2012 and references therein) to obtain a taxonomically consistent database. Our analysis was restricted to mammal species of more than 10 kg because they constitute the portion of the food web that allegedly included hominins (Binford, 1981(Binford, , 1985Marean, 1989;Díez et al., 1999;Gaudzinski and Roebroeks, 2000;Roebroeks, 2001;Speth, 2010;Saladié et al., 2011;Lozano et al., 2016). Primary consumer species included in this study belong to the families Bovidae, Castoridae, Cercopithecidae, Cervidae, Elephantidae, Equidae, Hippopotamidae, Hystricidae, Rhinocerotidae, and Suidae. ...
Article
Full-text available
Fossil remains and the technological complexes recorded in archaeological sites suggest that the human presence in Europe late in the early and middle Pleistocene was discontinuous. Moreover, competition for meat with other secondary consumers could have delayed the human dispersal through Europe. However, evaluation of the extent competition intensity among secondary consumers suggests this influenced the discontinuity of the human settlement of Europe between 1.1 and 0.2 Ma. Using a mathematical model, we estimate the amount of biomass available in a community for secondary consumers. The amount of available biomass is subsequently distributed among the guild of secondary consumers according to their requirements and prey preferences. Indexes that quantify the competition intensity among secondary consumers to compare the conditions in different paleoecosystems show that the competition intensity late in the early Pleistocene, early in the middle Pleistocene, and late in the middle Pleistocene does not support the view that an increase in competition intensity constrained the expansion of human populations early in the middle Pleistocene. Somewhat paradoxically, the lowest competition intensity is estimated to have occurred early in the middle Pleistocene, most likely because of an increase in the number of large herbivore species and a decrease in the number of secondary consumers. The early Pleistocene paleoecosystems supported higher competition intensity than the middle Pleistocene ecosystems, likely because of the different configuration in the food webs of these two periods (the early and middle Pleistocene).
... A sister volume, published in the Journal of Quaternary Sciences (volume 30, 7, 2015) is devoted to the chronological and palaeoenvironmental evidence from these earliest Acheulean sites . The shift to a 100 ka climatic cycle during the Mid Pleistocene Revolution led to the replacement of established widespread forests by mosaics of trees and more open environments, as well as the extension of grasslands into the higher latitudes, thereby opening or closing corridors for the dispersal of mammalian taxa (Guthrie, 1984;Almogi-Labin, 2011;Rodríguez et al., 2011;Abbate and Sagri, 2012;Martínez et al., 2014;Lozano et al., 2015;Markova and Vislobokova, 2015). However, the relationships between faunal turnovers across Eurasia and the onset of bifacial technology are not always easy to establish, due to a lack of clear mammalian dispersal events from Africa into Eurasia between 780 and 500 ka. ...
Article
Full-text available
Over the last few decades, several types of evidence such as presence of hominin remains, lithic assemblages, and bones with anthropogenic surface modifications have demonstrated that early human communities inhabited the European subcontinent prior to the Jaramillo Subchron (1.07–0.98 Ma). While most studies have focused primarily on early European lithic technologies and raw material management, relatively little is known about food procurement strategies. While there is some evidence showing access to meat and other animal-based food resources, their mode of acquisition and associated butchery processes are still poorly understood. This paper presents a taphonomic and zooarchaeological analysis of the Fuente Nueva-3 (FN3) (Guadix-Baza, Spain) faunal assemblage, providing a more in-depth understanding of early hominin subsistence strategies in Europe. The present results show that hominins had access to the meat and marrow of a wide range of animal taxa, including elephants, hippopotami, and small- and medium-sized animals. At the same time, evidence of carnivore activity at the site suggests that these communities likely faced some degree of competition from large predators when acquiring and processing carcasses.
Article
Full-text available
Anthropogenic pressures are causing a global decline in biodiversity. Successful attempts at biodiversity conservation requires an understanding of biodiversity patterns as well as the drivers and processes that determine those patterns. To deepen this knowledge, neoecologists have focused on studying present-day or recent historical data, while paleoecologists usually study long-term data through the composition of various biological proxies and environmental indicators. By establishing standard protocols or gathering databases, research infrastructures (RIs) have been instrumental to foster exchange and collaboration among scientists within neoecology (e.g. Global Information Biodiversity Facility or National Ecological Observatory Network) and paleoecology (e.g. Paleobiology Database, Neotoma Paleoecology Database or European Pollen Database). However, these two subdisciplines (and their RIs) have traditionally remained segregated although both provide valuable information that combined can improve our understanding of biodiversity drivers and underlying processes, as well as our predictions of biodiversity responses in the future. For instance, integrative studies between paleo- and neoecology have addressed the global challenge of biodiversity loss by validating climate and ecological models, estimating species fundamental niches, understanding ecological changes and trajectories, or establishing baseline conditions for restoration. Supporting and contributing to research infrastructures from both paleo- and neoecology, as well as their further integration, could boost the amount and improve the quality of such integrative studies. We argue this will enable improved capabilities to anticipate the impacts of global change and biodiversity losses. To boost such integration and illustrate our arguments, we (1) review studies integrating paleo- and neoecology to advance in the light of global changes challenge, (2) describe RIs developed in paleoecology, and (3) discuss opportunities for further integration of RIs from both disciplines (i.e. paleo- and neoecology).
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Representing data as networks cuts across all sub-disciplines in ecology and evolutionary biology. Besides providing a compact representation of the interconnections between agents, network analysis allows the identification of especially important nodes, according to various metrics that often rely on the calculation of the shortest paths connecting any two nodes. While the interpretation of a shortest paths is straightforward in binary, unweighted networks, whenever weights are reported, the calculation could yield unexpected results. We analyzed 129 studies of ecological networks published in the last decade that use shortest paths, and discovered a methodological inaccuracy related to the edge weights used to calculate shortest paths (and related centrality measures), particularly in interaction networks. Specifically, 49% of the studies do not report sufficient information on the calculation to allow their replication, and 61% of the studies on weighted networks may contain errors in how shortest paths are calculated. Using toy models and empirical ecological data, we show how to transform the data prior to calculation and illustrate the pitfalls that need to be avoided. We conclude by proposing a five-point check-list to foster best-practices in the calculation and reporting of centrality measures in ecology and evolution studies.
Preprint
Full-text available
1. Representing data as networks cuts across all sub-disciplines in ecology and evolutionary biology. Besides providing a compact representation of the interconnections between agents, network analysis allows the identification of especially important nodes, according to various metrics of network centrality. These centrality measures often rely on the calculation of the shortest path connecting any two nodes, and while the interpretation of a shortest paths is straightforward in binary, unweighted networks, whenever weights are accounted for, inconsistency between weight definition and shortest path interpretation could yield unexpected results. 2. Here we review 129 studies of ecological networks published in the last decade and making use of shortest paths. 3. We evidenced a methodological inaccuracy related to the edge weights used to calculate shortest paths (and related centrality measures) in ecological studies, particularly in interaction networks. Specifically, we found numerous studies in which the edge weights were not transformed prior to calculating shortest paths when the edge weights were proportional to the information flow between the nodes of the network at study. 49% of the studies do not report sufficient information on the calculation to allow their replication, and 61% of the studies on weighted networks may contain errors in how shortest paths are calculated. Using toy models and empirical ecological data, we show how to transform the data prior to calculation and illustrate the pitfalls that need to be avoided. 4. We conclude by proposing a five-point check-list to foster best-practices in the calculation and reporting of centrality measures in ecology and evolution studies.
Article
Ecomorphological and biogeochemical (trace element, and carbon, nitrogen, and oxygen isotope ratios) analyses have been used for determining the dietary niches and habitat preferences of large mammals from lower Pleistocene deposits at Venta Micena (Guadix-Baza Basin, Spain). The combination of these two approaches takes advantage of the strengths and overcome the weakness of both approaches. The range of δ 13 C collagen values for ungulate species indicates that C 3 plants were dominant in the diet of these mammals. δ 13 C collagen values vary among ungulates: perissodactyls have the lowest values and bovids the highest ones, with cervids showing intermediate values. The hypsodonty index measured in lower molar teeth and the relative length of the lower premolar tooth row indicate that the horse, Equus altidens , was a grazing species, whereas the rhino, Stephanorhinus etruscus , was a mixed feeder in open habitats. The similar δ 13 C collagen values shown in both perissodactyls does not reflect differences in feeding behavior with other ungulates, but rather a lower isotope enrichment factor in these monogastric herbivores than in ruminants, owing to their lower metabolic efficiency. The cervids Eucladoceros giulii and Dama sp. show low hypsodonty values, indicating that they were mixed feeders or browsers from forested habitats, an ecomorphologically based conclusion corroborated in the former by its low δ 15 N collagen content (canopy effect). Bovid species (Bovini aff. Leptobos, Soergelia minor , and Hemitragus albus ) presumably inhabited open environments, according to their comparatively high hypsodonty and δ 15 N collagen values. Carnivore species ( Homotherium latidens, Megantereon whitei, Pachycrocuta brevirostris, Canis falconeri , and Canis etruscus ) exhibit higher δ 15 N collagen values than ungulates. These results record the isotopic enrichment expected with an increase in trophic level and are also supported by low bone Sr.Zn ratios. The elevated δ 15 N collagen value for a sample of Mammuthus meridionalis , which came from an individual with unfused epiphyses, confirms that it was a suckling animal. The δ 15 N collagen value of the scimitar-cat H. latidens is well above that obtained for the young individual of Mammuthus , which indicates that juvenile elephants were an important part of its diet. The hippo, Hippopotamus antiquus , yielded unexpectedly high δ 15 N collagen values, which suggest feeding on aquatic, non-N 2 -fixing plants. The high δ 18 O hydroxyl values of bovids Hemitragus and Soergelia and of cervid Dama indicate that these ungulates obtained most of their water requirements from the vegetation. The megaherbivores and Eucladoceros exhibit the lowest δ 18 O hydroxyl values, which suggest increased water dependence for them. Paleosynecological analysis was based on the relative abundance of species of large mammals from different ecological categories, determined by feeding behavior and locomotion types. The comparison of the frequencies of such categories in Venta Micena with those found in modern African communities indicates that the composition of the paleocommunity closely resembles those of savannas with tall grass and shrubs. The net above-ground primary productivity estimated for the on-crop biomass of the mammalian species preserved in the fossil assemblage also yields a figure congruent with that expected for an open environment.
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The intuitive background for measures of structural centrality in social networks is reviewed and existing measures are evaluated in terms of their consistency with intuitions and their interpretability.