© 2004 Blackwell Publishing Ltd www.blackwellpublishing.com/geb

163

Global Ecology and Biogeography, (Global Ecol. Biogeogr.)

(2004)

13

, 163–176

RESEARCHPAPER

Blackwell Publishing, Ltd.

Body size structure in north-western Mediterranean Plio-Pleistocene mammalian faunas

Jesús Rodríguez*, María T. Alberdi*, Beatriz Azanza*† and José L. Prado‡

ABSTRACT

Aim

We investigated the patterns of body-size changes of the north-western Medi-terranean Plio-Pleistocene large mammal faunas (excluding rodents, bats, lagomorphsand insectivores) in order to identify the tempo and mode of the major shifts in bodysize distribution, and to put them in the context of Plio-Pleistocene environmentalchanges and the development of the Mediterranean climate.

Location

We analysed fossil faunas of Spain, France and Italy. A set of recentregional faunas from several macroclimatic regions was selected to serve as elementsfor comparison of the size distribution of past faunas, consisting of: Spain, Franceand Italy together, Florida, California, Central Chile, Indochina, India, Korea-Manchuria, Malawi, The Cape, North Africa, Turkey and Australia.

Methods

Mammal species were grouped into five body size categories for carni-vores and four categories for noncarnivore species. The number of species in eachsize category was computed and the resulting matrix of body weight classes

×

regionsand time intervals was used as an input matrix in a Correspondence Analysis.

Results

Recent and fossil faunas strongly differ in body size structure. The distri-bution of recent faunas within the CA seems to reflect both ecological and historicfactors, intertwined in a complex fashion. No clear relationship has been observedbetween body size structure and environmental factors. During the late Pliocene toearly Pleistocene there were only minor changes in the pattern of size distribution,although plant communities were in a transition process from subtropical forests toMediterranean woodlands and steppes. The major change in body size structure ofthe north-western Mediterranean fauna occurred at the Galerian, around 1 Ma ago.This marked the beginning of the modern fauna, and a general trend towards a largerbody size, reduction in the number of medium sized herbivores, and an increase oflarge herbivores and megaherbivores.

Main conclusions

The Plio-Pleistocene faunas lack modern analogues. The bodysize structure of mammalian regional faunas appears to be strongly dependent onhistorical factors. The only major shift in body size distribution occurred during thePlio-Pleistocene, in the late Villafranchian-Galerian transition, coincident with theonset of the Pleistocene high intensity glacial cycles.

Keywords

Body size structure, mammals, fossil faunas, Plio-pleistocene period, north-

western Mediterranean, species pool.

*Correspondence: Jesús Rodríguez,Departamento de Palaeobiología, MuseoNacional de Ciencias Naturales, CSIC. JoséGutiérrez Abascal, 2, 28006 Madrid, Spain.E-mail: jrm@mncn.csic.es.

*

Departamento de Palaeobiología, Museo Nacional

de Ciencias Naturales, CSIC. José Gutiérrez Abascal,

2, 28006 Madrid, Spain,

†

Area de Palaeontología,

Departamento de Ciencias de la Tierra, Univer-

sidad de Zaragoza, 50009 Zaragoza, Spain and

‡

INCUAPA, Departamento de Arqueología, F.C.S.

UNC. Del Valle 5737, B7400JWI-Olavarría,

Argentina. E-mail: jrm@mncn.csic.es (JR);

malberdi@mncn.csic.es (MTA)

INTRODUCTION

The late Cenozoic mammal record from the north-western Med-

iterranean area provides an opportunity to study the evolution

of the ecological features of regional faunas in relation to

environmental changes. The Neogene-Quaternary formations of

this region contain thick, especially well-exposed sedimentary

sequences that are abundant in mammalian fossils, making it

possible to document faunal changes with fine-tuned temporal

resolution.

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The Mediterranean region has been a single zoogeographical

province since the late Miocene (Bernor, 1984, 1986; Fortelius

et al

., 1996). Several major biotic crises have been identified in

this area from the late Miocene to the Holocene, based on

nonquantitative approaches (Aguirre

et al

., 1976; Azzaroli, 1983,

1996; Steininger

et al

., 1985; Azzaroli

et al

., 1988; Aguirre &

Morales, 1990; Sala

et al

., 1992; Torre

et al

., 1992; Rook & Torre,

1996). Azanza

et al

. (1999, 2000) discuss the dynamics of faunal

turnover in relation to the latest Cenozoic glacial trend. They

analyse the fossil record bearing in mind the different durations

of the intervals and the reliability of the record. From their anal-

ysis they found only four statistically significant events. The ‘Rus-

cinian mammal turnover pulse’ represents the first major biotic

event, which corresponds in time with the Messinian crisis. The

second biotic event corresponds to the so-called ‘

Equus

-elephant

event’ during the lower Villafranchian, which coincides with a

significant glacial trend. Although Azzaroli (1983) based his def-

inition of the alleged Wolf event on the massive expansion of

wolf-like dogs around 1.7 Ma, Azanza

et al.

(2000) failed to

identify any statistically significant faunal event at this time. The

third event was the ‘Galerian mammal turnover pulse’ around one

million years ago when glacial maxima became more extreme

with the development of massive Northern Hemisphere ice

sheets (Suc

et al

., 1995; Shackleton, 1996). This event coincides

with the arrival of

Homo antecessor

in the western Mediterranean

area (Azanza

et al

., 1999, 2000; Carbonell

et al

., 1995; Bermúdez

de Castro

et al

., 1997). Finally, in the fourth event, the western

Mediterranean fauna was affected by the worldwide Upper Pleis-

tocene megafaunal extinction that decimated European mega-

fauna (Stuart, 1991). This last event is considered by Azanza

et al

.

(1999, 2000) to be very different from the three previous events,

since it appears to constitute an extinction without replacement

process.

The composition of a regional fauna is the result of both

ecological and historical factors. Climatic events exert a great

influence throughout time on the biogeographical distribution

of mammalian species and, thus, influence the composition of

regional faunas. The distribution of body sizes in a mammalian

community, a taxon-free characterization, has been shown to be

useful in comparing communities from different time horizons

and geographical areas (Damuth, 1992). Body-size structure has

been used in studies of community evolution and in the inter-

pretation of ancient climate and vegetation (Andrews

et al

., 1979;

Van Couvering, 1980; Janis, 1982, 1984; Legendre, 1986; Van

Valkenburgh, 1988). The importance of body size as a major

aspect of the adaptive strategy of animals was recognized by

palaeontologists as early as the 19th century (e.g. Cope, 1887;

Depéret, 1909). Body size is the single most useful predictor of

the ecological characteristics and life history pattern of any

mammal species. It is one of the most important determinants

of body architecture and physiology (Schmidt-Nielsen, 1975;

Alexander

et al

., 1981; McNab, 1990), ecology (Hutchinson &

MacArthur, 1959; McNab, 1971; Damuth, 1981a, 1981b; Janis,

1986; Robinson & Redford, 1986) and social organization

(Jarman, 1974; Clutton-Brock

et al

., 1977; Eisenberg, 1981; Janis,

1982); it also influences the number of species found in a given

area (MacArthur & Wilson, 1967; Van Valen, 1973) and the prob-

ability of extinction (Diamond, 1984; Lessa

et al

., 1997). Thus

body size distribution is used in this paper to represent the eco-

logical structure of fossil and recent regional faunas. We restrict

our analysis to the size distribution of large-bodied mammal

faunas, since some of the time intervals studied lack a reliable

record of small mammals (Aguirre & Morales, 1990). We are aware

that this restriction limits the resolution of our analysis, and any

changes affecting micromammal communities will go unno-

ticed. However, many similar studies have proved that focusing

these types of analyses on macrofauna is a valid approach that

often renders interesting results (e.g. Vrba, 1995; Reed, 1998;

Bobe

et al

., 2002).

The aim of this paper is to compare the body size distribution

of the north-western Mediterranean large mammal faunas with a

selected sample of recent ones, and to interpret the similarities

and differences in the context of the known ecological character-

istics of past and present habitats. The influence of the develop-

ment of the Mediterranean climate on the body size distribution

of the regional species pool will also be evaluated.

MATERIALS AND METHODS

The current database was constructed from data obtained from

selected localities in Spain, France and Italy in previous studies,

and has been published elsewhere (Alberdi

et al

., 1997; Prado

et al

., in press). Small mammals (Chiroptera, Rodentia, Insec-

tivora, Lagomorpha and small marsupial species) were excluded

in order to standardize the analysis and allow more accurate

comparisons of the faunistic associations.

Study area

Although the north-western Mediterranean area is considered to

be a zoogeographical province, its environment and topography

are highly heterogeneous, with two clearly distinguishable

climatic zones. The southern zone (Iberian Peninsula, Italy and

southern France) is strongly influenced by the Mediterranean

climate regime of summer droughts and cool moist winters that

favours an abundance of evergreen shrubs and sclerophyllous

trees (Archibold, 1995). The northern zone, on the other hand

(northern France, and parts of northern Spain and northern

Italy) is characterized by more temperate conditions. These two

zones probably coexisted in the area during the entire period,

although the intensity of the climatic differences may have varied

during the period. It is likely that climatic differences were

greatest during the Pleistocene (Suc

et al

., 1995). Thus, the climate

factor does not affect our ability to compare intervals. The Med-

iterranean climate, which is included in the ‘sclerophyllous forest

of the winter rain regions’ biome (Walter, 1973), occurs in several

widely separated regions along the subtropical western margin of

continents between 30

°

and 40

°

latitude. The Mediterranean

zone of southern Africa is restricted to the rugged folded sand-

stones that form the mountainous rim around the Cape Province

(Archibold, 1995). There are also Mediterranean climates in Aus-

tralia (in the south-western coastal region and western Victoria),

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165

and in South America along the coastal lowlands and on the

west-facing slopes of the Andes, where the ‘matorral’ (shrub)

merges with alpine communities at about 2000 m elevation. In

North America, Mediterranean communities occur on the lower

slopes of the Sierra Nevada and in the hilly country throughout

much of California.

According to Walter’s classifications (Walter, 1973), the north-

ern half of the region considered in this paper, which corre-

sponds to France, northern Spain and northern Italy, belongs to

zonobiome VI — nemoral-broafleaf deciduous forests. This same

type of vegetation is found in eastern Asia and North America, as

well as in a small region of southern Chile. Unlike Mediterranean

regions, this area does not experience summer drought periods

and has slightly colder winter temperatures.

Time intervals

Different approaches may be used to analyse the evolution of

mammalian faunas over time. Some studies focus on the varia-

tions in structure of faunal assemblages from particular localities

arranged in a temporal sequence. This approach has been

followed by Montuire & Desclaux (1997), Montuire (1999)

and Montuire & Marcolini (2002) in three analyses of the Plio-

Pleistocene faunas from France, Spain and Italy, respectively.

When local faunas are analysed separately, it is implicitly assumed

that the local faunal assemblage (LFA) recorded in a locality is

representative of the entire community that lived during the time

of accumulation of the bones preserved in this locality. However,

taxonomical and anatomical compositions of some Spanish

Plio-Pleistocene LFAs have been subjected to highly variable

modifications by sedimentary and taphonomic processes (Pérez,

1990; Alcalá, 1994; Palmqvist

et al

., 1996; Alberdi

et al

., 2001; Pérez

& Soria, 1989–90). Thus, this approach requires a strict control

of the taphonomic processes involved in the accumulation of each

particular LFA. The use of LFAs as the unit of analysis is highly

sensitive to time- and space-averaging processes and may pro-

duce fossil assemblages that are composed of species that actually

did not coexist. It may be argued that the effect of space-averaging

may be minimized by comparing recent communities from

areas of adequate size, but it is usually impossible to comply with

this procedure, since the actual size of the area represented in a

fossil assemblage is rarely known.

An alternative approach is to divide a period into time inter-

vals and to use the faunal assemblages of these intervals as the

units of analysis, focusing attention on the study of regional

faunas rather than on communities. This approach may be seen as

an analysis at a different scale, and is as informative as other

approaches, if not more so. Many studies on recent faunas have

stressed the predominance of the regional species pool over the

local ecological conditions in shaping, or even determining, the

composition and diversity of local assemblages (Ricklefs &

Schluter, 1993).

Using generally recognized palaeontostratigraphical scales, as

other authors have done (e.g. Gunnell, 1994, 1997; Morgan

et al

.,

1995), poses several problems in our case. First, it is difficult

to correlate the biochronological scales proposed for the

Plio-Pleistocene formations of the north-western Mediterranean

because none of the scales covers the complete interval of time

analysed here, and the criteria used to define these scales differ

greatly. Secondly, the boundaries between these units are not

defined properly for the palaeoecological analysis of regional faunas.

Thirdly, this approach assumes that all taxa present in a single

unit occurred from the beginning to the end of that time interval.

Thus, if taxonomic turnover rates inside units are high, richness

could be overestimated by claiming that certain taxa coexisted

when they actually lived at different times (Alroy

et al

., 2001).

In order to eliminate these drawbacks, each time interval should

correspond to a block of coordinated stasis, i.e. intervals during

which no turnover occurred (Brett

et al

., 1996). Therefore, we

have used nine informal biochronological units (BUs) spanning

the last six million years (A to I) that have been substantiated by

multivariate procedures and have been published elsewhere

(Alberdi

et al

., 1997). These BUs cover the complete interval

considered in our study and they represent ‘

lapses of time during

which faunas have certain taxonomic homogeneity, the discontinu-

ity between them corresponding to faunal reconfigurations associ-

ated with major changes in environmental conditions

.’ (Azanza

et al

., 1999). Thus, BUs may be seen as blocks of coordinated

stasis, or periods of time when taxonomic turnover was close to

zero. The duration of these BUs was estimated from the available

dates for the particular localities, and ranged between 2.5 and

0.2 Ma. Interval A corresponds to the Turolian, interval B to the

Ruscinian, intervals C, D and E may be correlated to the Villf-

ranchian, F, G and H to the Galerian and, finally, interval I corre-

sponds to the Maspinian (Alberdi

et al

., 1997). All the rejoined

species or successive subspecies of a single species were removed

from the matrix so as not to give excessive weight to a species

with many subspecies.

Important fluctuations exist in the number of coexisting

species in different intervals (Azanza

et al

., 1999), a pattern that

may either reflect true richness changes or incomplete sampling.

Inferring the occurrence of taxa known from preceding and

succeeding intervals or ‘range-through’ taxa is a method usually

used to correct partially the underestimation of richness in a

particular interval. This method, known as the minimum census

technique (Rosenzweig & Taylor, 1980), is commonly applied in

analyses of mammalian richness (Stucky, 1990). When the pro-

portion of ‘range-through’ taxa is used as an estimate of the rela-

tive sampling quality of an interval, only intervals E and G yield

results that may indicate that species richness is underestimated

(Azanza

et al

., 1999, 2000). However, these two intervals corre-

spond to the late Villafranchian and the middle Galerian, and it is

well known that during the Pleistocene, short-term geographical

range fluctuations, closely related to climate oscillations, occurred

in cycles of 41,000 and 100,000 years. Thus, the absence of a spe-

cies may be due merely to shifts in its distribution in and out of

the study area and may not always indicate a poor record quality.

Body mass determinations

We have used body mass as a measurement of body size, according

to Gingerich

et al

. (1982), because its use facilitates comparison

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among animals of different head-and-body shape. We estimated

the body mass of fossil mammals mainly from dental measure-

ments, since teeth are usually preserved in relatively high num-

bers and most species are more easily identified by their teeth

than by postcranial elements.

The body masses of carnivores (Canidae, Ursidae, Mustelidae,

Felidae and Hyaenidae) were estimated from the lower carnassial

crown area using equations developed by Legendre & Roth

(1988). In the very few cases where the area of the lower carnas-

sial was unknown, body mass was estimated using the length of

M1 following the regression equation developed by Van Valken-

burgh (1990). The body masses of Proboscideans were taken

from Alcalá (1994) and Palmqvist

et al

. (1996). We used meas-

urements of leg bones for Equidae following Alberdi

et al

.

(1995). For the remaining Perissodactyla and Artiodactyla

species, body masses were calculated using dental measurements

and Janis’s equations (1990). For a discussion of the general

problems of using teeth to estimate body mass see Gould (1975),

Smith (1984, 1993) and Damuth (1990). See Prado

et al

. (in press)

for a detailed description of body mass estimations used in the

present analysis.

Body-size structure of faunas

Mammalian noncarnivore species were assigned to one of four

size categories, defined following Andrews

et al

. (1979), and

Owen-Smith (1988): small herbivores (N1), < 45 kg; medium

sized herbivores (N2), 45–360 kg; large herbivores (N3), 360–

1000 kg, and megaherbivores (N4), > 1000 kg. The number of

species in each size category, as well as the number of carnivores

was computed for each BU and recent fauna.

Palaeoecological studies analysing size distributions usually do

not consider carnivores (Legendre & Roth, 1988; Montuire &

Desclaux, 1997; Montuire, 1999; Montuire & Marcolini, 2002),

or they pool carnivores into the same size categories with non-

carnivores (Andrews, 1990; Rodríguez, 2001; Kovarovic

et al

.,

2002). Since it is presumed that the selective pressures that deter-

mine body size operate differently for predators than they do for

prey, we placed carnivores in a separate category for our analysis.

Carnivores were grouped into five size categories: < 1 kg, 1–5 kg,

5–10 kg, 10–45 kg, and > 45 kg. Since a strong relationship

exists between the size of a predator and the maximum size of its

prey (see data on Ewer, 1998), carnivores in the last size category

(> 45 kg) are able to prey on medium sized and large herbivores,

while megaherbivores are almost immune to predation. The first

four categories were defined mainly to visualize the effect of the

differential preservation probabilities of medium, small and very

small species.

The number of species (richness) in size categories N1, N2,

N3, N4 and the total number of carnivores (Nc) by BU and

recent fauna were used in the Correspondence Analysis (CA) using

STATISTICA data analysis software version 6. Correspondence

Analysis is an exploratory multivariate technique that sum-

marizes all the information between the similarities of a set of

cases (faunas) in a small number of dimensions (StatSoft, 2001).

CA has been widely used by ecologists as an ordination method

(Digby & Kempton, 1987) since it has the advantages over other

ordination methods of greater freedom from distortion, and

higher resistance to data noise, outliers and heterogeneity (Shi,

1993).

Comparisons with recent faunas

The patterns of body size distribution of recent mammalian

faunas from different geographical areas were explored in order

to evaluate the effects of climate and biogeography on body size

structure (Fig. 1, Table 1). Most palaeoecological analyses use the

patterns observed in recent faunas to interpret fossil assemblages,

assuming that they are independent of geographical or taxo-

nomic (but not historical) influences (Gunnell, 1994, 1997). We

looked for characteristics of body size distribution unique to

Mediterranean faunas in order to search for the origin of those

characteristics in the fossil assemblages. Since one of our aims

was to investigate the influence of the development of the Medi-

terranean-type climate on body size distribution of fossil faunas,

special care was taken to include recent faunas from every region

of the world that has a Mediterranean type climate (Chile,

California, SW Australia, The Cape, North Africa, and Turkey). The

Figure 1 Map of the 11 recent faunas usedfor comparison. See Table 1 for informationon the codes.

Body size in Mediterranean faunas

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167

faunas of Florida, Korea and Manchuria were included because it

has been suggested that, during some time-intervals, the vegeta-

tion of the western Mediterranean area was similar to the current

vegetation of these areas (Suc

et al

., 1995). During the Turolian,

the environment of Western Europe changed from tropical and

subtropical forest conditions to predominantly deciduous forests

and savannas (Fortelius

et al

., 1996). Thus, we have included in

our database four modern tropical faunas from Africa and

Southern Asia that correspond to zonobiome II and zonoecotone

II/III of Walter’s classification (deciduous tropical forests, dry

woodlands and savannas). Since the aim of this paper is to

analyse the evolution of body size structure in mammalian faunas

from a moderately wide geographical area, regional faunas have

been selected for comparison instead of species lists from indi-

vidual localities, which is the common practice in palaeoecological

studies focused on mammalian communities. The following cri-

teria were used while compiling the recent faunal lists: marsupi-

als weighing less than 1000 g, rodents, insectivores, lagomorphs

and Chiroptera, were excluded. Mammal species introduced by

humans in these areas were excluded but species present in the

Holocene that are now extinct, presumably by human influence,

were included.

The regions included in the analysis are very different in size

(Table 1). However, area and richness are not correlated in the

sample (Spearman’s

r

= 0.0714,

P

= 0.81,

n

= 13). The independ-

ence between area and species richness may seem unexpected,

but it reflects the fact that, at the planetary scale, other factors

(history and environment) are far more important than area in

determining species richness. The north-western Mediterranean

area and India are quite similar in size (Table 1), but the latter is

home to more than double the number of species than the

former (25 vs. 57). Moreover, Malawi, which is more than 10

times smaller than India, far exceeds this latter country in richness

(62 species).

RESULTS

The results of the Correspondence Analysis used to describe the

similarities and differences in size structure of the recent and fossil

faunas are shown in Fig. 2 and Table 2. The first three dimensions

explain 94.2% of the inertia. The first dimension distinguishes

faunas rich in medium-sized, large herbivores and megaher-

bivores from faunas richer in small herbivores (Table 2, Fig. 2),

while the second dimension separates faunas according to their

proportions of herbivores and carnivores. Finally, the third

dimension differentiates faunas rich in medium-sized herbivores

Table 1 Recent faunas used for comparison and ecological information about the selected areas

Code A T P D Vegetation Reference

North-western NWM 1,400,000 18.6–9.4 122–1081 0–4 Temperate forests, Mediterranean Schilling et al. (1987);

Mediterranean forests and shrublands Castells & Mayo (1993)

North Africa Naf 700,000 14.8–18.4 224–887 5 Mediterranean shrublands Grzimeck (1988)

Turkey Tur 850,000 19.5–8.3 113–2510 4 Mediterranean forests

and shrublands and steppes

Grzimeck (1988)

California state (USA) Cal 410,000 11.1–17.1 208–1210 5 Chaparral Hall (1981)

Central Chile Chi 350,000 12.4–14.3 490–722 5 Mediterranean shrubland Redford & Eisenberg (1989)

The Cape (Cedarberg) Cab 140,000 12.4–17.9 110–544 8 Fynbos Rautenbach & Nel (1980);

Grzimeck (1988)

Australia Aus 210,000 14.9–19.6 336–980 7–4 Heathlands Kikkawa et al. (1978)

Korea-Manchuria Kor 1,350,000 12.0–1.0 382–1398 0 Temperate forests Grzimeck (1988)

Florida state (USA) Flo 150,000 20.7–25.3 1004–1568 0 Mangroves and marshes Hall (1981)

Indochina Ino 1,900,000 28.1–23 1279–5435 5 Dipterocarp forests and savannas Corbert & Hill (1992)

India Ind 1,480,000 28–13 179–1617 7 Savannas and Tropical dry forests Le Berre (1991)

Malawi Mlw 119,000 22–25.8 1494–1024 3 Tropical woodlands and savannas Ansell & Doeset (1988)

Transvaal Trv 260,000 22.1–15.5 735–437 6 Tropical savannas and Rautenbach (1978)

(South Africa) grasslands

T, mean annual temperature in °C; P, annual precipitation in mm; D, length of the drought season in months. Climate data from Walter et al. (1975).

A, aproximate area of the region in km2.

Table 2 Results of the Correspondence Analysis used to describethe similarities and differences in size structure of recent and fossilfaunas. Size categories N1 ≤ 45 kg, N2 = 45–360 kg, N3 = 360–1000 kg,N4 ≥ 1000 kg, Nc = carnivores. Dim. 1, Dim. 2 and Dim. 3 are thecoordinates of the variables in the first three dimensions. Qualitymeasures the quality of the representation of each particular variablein the coordinate system defined by the three selected dimensions.Relative inertia is a measure of the relative contribution of eachvariable

Dim. 1 Dim. 2 Dim. 3 Quality Relative inertia

N1 −0.76 0.28 −0.02 1.00 0.42

N2 0.30 0.16 0.28 0.99 0.15

N3 0.55 0.31 −0.42 0.91 0.15

N4 0.55 0.47 −0.16 0.85 0.15

Nc −0.00 −0.29 −0.04 1.00 0.14

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from those faunas with a larger proportion of large herbivores

and megaherbivores (Figs 2 and 3). As a general trend, the size

structure of fossil faunas is entirely different from that of recent

faunas; with fossil faunas being richer in medium, large and very

large species.

The distribution of recent faunas seems to reflect both ecolo-

gical and biogeographical (historical) factors. Thus, the fauna

from El Cabo, a region with a Mediterranean-type climate, is

similar to other faunas from the same biogeographical region

(Malawi and Transvaal), and dissimilar to other Mediterranean

faunas. The extreme position of the fauna from Australia is

undoubtedly explained by its unique composition, due to the

singular history of this continent (Fig. 2). On the other hand, the

faunas from Chile, Korea and North Africa have very similar

structure and are not very different in size composition from

Western European communities, despite the fact that they are

located in different continents. However, none of the three

climatic variables considered in our database (mean annual

temperature, annual rainfall and length of the drought season) is

significatively correlated to the scores of the recent localities on

any of the three dimensions (Table 3). In summary, like other

recent authors (Hernández Fernández

et al

., 2003), we found

that body size distribution of recent faunas is influenced by both

historical factors and ecological factors. These factors are inter-

twined in complex fashion, making it impossible to establish a

clear relationship between the size structure of the faunas and

any one environmental factor.

With respect to the distribution of fossil faunas, there appear

to be proportionately more large and very large herbivores in

Late Villafranchian, and Early Galerian Faunas (E and F) than

there are in Turolian, Ruscinian and Maspinian faunas (Fig. 2).

However, these differences may be due, in part, to the fact that

the late Villafranchian and early Galerian BUs are the least rich in

terms of species samples (Fig. 3). Regional fossil faunas are

divided in two groups in dimension 3. The first group consists of

the oldest faunas (Turolian to late Villafranchian), while the

second group is composed of Galerian and Maspinian faunas

(Fig. 2). This separation reflects an important change in body

size distribution at the beginning of Galerian (interval F), when

large herbivore and megaherbivore species outnumbered middle-

sized herbivore species (Fig. 3). This new pattern of body size

distribution remains unchanged until the end of the Pleistocene,

when it was disrupted by the extinction of megafauna. Although

not detected in the CA, an earlier change in body size distribu-

tion occurred in interval D (Fig. 3), when the number of herbiv-

ore species of less than 45 kg dropped to only one. Moreover, this

species was a primate while in previous intervals this body-size

interval was filled with small bovids and cervids.

The relative abundance of small herbivores vs. carnivores

seems to separate tropical and temperate recent faunas in the sec-

ond dimension. Tropical faunas are rich in both small herbivores

Figure 2 Correspondence Analysis of the number of species persize category for recent and fossil faunas. Black dots: recent faunas;open dots: fossil faunas; crosses: variables. Codes for recent faunas asin Figure 1. Fossil faunas are grouped in nine biochronological units:A, Turolian; B, Ruscinian; C, D, E and F, Villafranchian; G and H,Galerian; and I, Maspinian (see text and Figure 4). Nc, total numberof carnivores; N1, number of small herbivores (< 45 kg); N2,number of medium sized herbivores (45–360 kg); N3, number oflarge herbivores (360–1000 kg); N4, number of megaherbivores(> 1000 kg).

Table 3 Kendall’s Tau rank correlations between the scores of therecent regional faunas on the 3 dimensions of CA and three climaticvariables

n = 13 D P T

Dim1 −0.37 0.00 −0.28

P 0.08 1.00 0.18

Dim2 0.32 −0.10 0.23

P 0.13 0.63 0.27

Dim3 0.21 −0.26 0.08

P 0.32 0.22 0.71

D, length of the drought season; P, annual rainfall; T, mean annualtemperature.

Body size in Mediterranean faunas

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169

and in carnivores. In contrast, temperate faunas are much richer

in carnivores than in small herbivores (Fig. 3). The position of

the fossil faunas in the second dimension is closer to recent trop-

ical faunas than to temperate faunas, due to the high proportion

of carnivores in recent temperate faunas, rather than to the pro-

portion of small herbivores (Figs 2 and 3). It should be noted

that, while it is well known that carnivores tend to be under-

represented in fossil assemblages (Rodríguez, 2001), the position of

the fossil faunas in the second dimension alone does not imply

that they are severely biased against carnivores (Fig. 3). As a mat-

ter of fact, except during the Villafranchian and Galerian, there

are similar numbers of carnivores in both fossil and recent

faunas. The CA reflects the differences and similarities between

the faunas based on the relative frequencies of each size category,

not on its absolute numbers. Therefore, the fossil faunas are

separated from the recent ones on the second dimension because

their proportion of carnivores is lower, despite their similar abso-

lute numbers. Furthermore, fossil faunas are richer than recent

ones in medium sized (10–45 kg) and very large carnivores (> 45 kg)

(Fig. 3). The abundance of large carnivores in the fossil faunas is

undoubtedly related to a higher proportion of large herbivores.

However, carnivores are probably underrepresented in the

fossil assemblages after all. As a matter of fact, the regional fossil

faunas of the nine time intervals have very few small carnivores

(< 5 kg) in comparison with recent faunas. Carnivore species

weighing less than 5 kg were recorded in only three BUs (C, H

and I). It is more likely that the paucity of small carnivores is due

to their lower preservation probabilities rather than to their true

absence in past faunas. Thus, a selective bias seems to exist in the

representation of small carnivores in the fossil faunas, but not in

the number of medium sized and large species (> 5 kg).

DISCUSSION

One of the most striking results of our analysis is that all regional

fossil faunas differ in body size composition from all recent

faunas. It may be asked whether this lack of recent analogues is a

consequence of an inadequate selection of recent faunas used for

comparison or is it due to the fact that regional fossil faunas

actually lack modern analogues. Results from other studies sup-

port the second explanation. An analysis comparing 6 Spanish

Pleistocene and 93 African, American and Eurasian recent local

faunas failed to find any recent analogue for the Pleistocene com-

munities (Rodríguez, 2001), and similar results were obtained by

Hernández Fernández

et al

., 2003) in their analysis of the

Miocene faunas from Spain.

Figure 3 Body size distribution in fossil andrecent faunas according to the size categoriesdefined in the text. Codes as in Figure 2.

J. Rodríguez

et al.

170

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As a general trend, fossil faunas are richer in large mammals

(N2, N3 and N4) and poorer in small herbivores (N1) than

recent faunas. Since a shift in body size composition occurred at

the end of the Villafranchian, fossil faunas may be classified into

two groups that differ in the proportion of medium-sized vs.

large herbivores and megaherbivores: the more ancient faunas

(Turolian, Ruscinian and Villafranchian) and the ‘modern’ faunas

(Galerian and Maspinian).

It is well-known that carnivores tend to be underrepresented

in fossil assemblages due to their lower population densities.

Comparison of the fossil and recent faunas demonstrates that a

severe bias exists due to the lack of small carnivores in all the

periods studied. The proportion of small carnivores in recent

faunas ranges from 30% to 90% of the total number of carni-

vores, being the modal value 50%. If we assume that the propor-

tion of small carnivores in the fossil faunas was similar to the

values observed in recent ones we should expect the total number

of carnivore species to be double the observed number. Thus,

fossil faunas, with the exception of the two poorest intervals (E

and F), would exceed recent faunas both in proportion and in

absolute number of carnivore species, reinforcing our conclusion

that recent analogues for fossil faunas do not exist.

At the end of the Turolian (MN13), faunistic exchanges took

place between Eurasia and Africa, classically interpreted as

dispersal events favoured by the Messinian salinity crisis (Aguirre

et al

., 1976; Hsü

et al

., 1977; Steininger

et al

., 1985; Cita

et al

.,

1996). However, some migrations occurred before the Messinian

salinity crisis and by other migration routes (Pickford

et al

.,

1995; Agustí & Llenas, 1996; Aguilar & Michaux, 1997; Garcés

et al

., 1998). The Messinian crisis, a time when thick evaporites

were deposited in an isolated and desiccated Mediterranean Sea,

occurred 5.9–5.4 Ma (Riding

et al

., 1998) and could have been

triggered in part by either glacio-eustatic changes related to

glacial trends (Kastens, 1992; Shackleton, 1996), or by tectonic

events (Krijgsman

et al

., 1999) or intraplate volcanism (Duggen

et al

., 2003). In any event, the causes and actual intensity of the

Messinian crisis are topics of heated debate. Some authors sug-

gest that the evaporites did not involve the desiccation of the

deep Mediterranean basin (Martínez del Olmo, 1996; Michalzik,

1997), while others propose that two different evaporite formation

events occurred (Clauzon

et al

., 1996).

During the Ruscinian, subtropical conditions predominated

that were characterized by seasonal rainfall. Subtropical to

meso-Mediterranean forests developed in the north, while Medi-

terranean steppes formed to the south of the north-western

Mediterranean area. These conditions heralded the beginning

of the double seasonality regime, and the temperature and

precipitation regimes that are typical of the Mediterranean cli-

mate (Suc

et al

., 1995). Strikingly, the ‘Ruscinian turnover’, that

Azanza

et al. (1999, 2000) associated with the first glacial pulse

at the Mio–Pliocene boundary, did not significantly alter the

size structure of the regional fauna, although richness in Bovidae,

Ursidae and Felidae increased (Azanza et al., 1999, 2000).

Although Fig. 3 shows that the Ruscinian was the richest period

of the entire sequence analysed, when standing richness (spe-

cies richness at the midpoint of a time interval) is taken into

account the richest interval corresponds to the early Villafranchian

(Azanza et al., 2000).

An important dispersal event in the early Villafranchian is the

so-called Equus-elephant event (Azzaroli, 1983; Steininger et al.,

1985; Azzaroli et al., 1988; Aguirre & Morales, 1990). Azanza

et al. (1999, 2000) confirmed that this dispersal event caused a

marked increase in standing richness due to the high number of

first appearances. Nevertheless, the influence of this event on the

size structure of the mammalian fauna seems to have been negli-

gible, although larger species of Equidae and Cervidae appeared

at this time, widening the range of body sizes for these families

(Prado et al. in press). According to Shackleton (1996), an impor-

tant climatic change took place between 3.0 and 2.6 Ma with the

onset of bi-polar glaciations (Fig. 4). This change produced cool

winters and generated a thermal seasonality, which between 3.5

and 2.6 Ma, supplanted the pre-existing moisture seasonality.

During this time interval, the modern Mediterranean climate began

in the region, and the modern Mediterranean floral assemblage

appeared (Suc et al., 1995). However, Correspondence Analysis

results suggest that the size structure of the early middle Villa-

franchian regional faunas remained close to those of the Turolian

and Ruscinian faunas (Figs 2 and 3).

The Wolf event described by Azzaroli (1983) in the Villafran-

chian (interval D) does not seem to coincide with any important

change in body size distribution of carnivore species, although it

coincides with a strong diminution in the number of small

herbivores (< 45 kg). As a matter of fact this size category is occu-

pied only by a primate (Macaca sp.) in the late Villafranchian (D-E),

due to the disappearance of small bovids from the regional fauna.

Intervals E and F, corresponding to late Villafranchian and

early Galerian, are separated from the rest of the intervals in the

Correspondence Analysis by the high proportion of large and

very large herbivores and by the scarcity of carnivores. Neverthe-

less, it is difficult to decide whether this pattern is a consequence

of bias against carnivores or if it is due to a true scarcity of pred-

ators during this period. In any event, it should be noted that, as

commented above, species richness may be underrepresented in

interval E. Azanza et al. (2000) found that species richness was

probably underestimated for interval G too. However, since there

is no evidence that this underrepresentation affected any size cat-

egory preferentially, it does not significatively bias our results. In

any event, the major differences in body size distribution among

the fossil faunas are caused by the proportion of medium-sized

vs. large herbivores and megaherbivores and are reflected in

Dimension 3 of the CA (Fig. 2). From the Turolian to the late

Villafranchian, medium-sized herbivores represent the most

abundant body size group, but they are outnumbered by the sum

of large herbivores plus megaherbivores during the Galerian and

Maspinian (Fig. 3).

This variation in body size structure may be related to the

environmental change that began in the late Villafranchian and

that increased during the Galerian. As discussed by Prado et al. (in

press) larger body size might be an advantage in fluctuating

environments, since larger mammals have more nutrient storage

capabilities in relation to energy expenditure per unit mass than

do smaller mammals. Although the general scenario of long

Body size in Mediterranean faunas

Global Ecology and Biogeography, 13, 163

–176, © 2004 Blackw

ell Publishing Ltd171

Figure 4 Summary of major trends in the body size structure of large mammal faunas expressed by the scores of the BUs in the three significant dimensions of the correspondence analysis. Climatetrends, faunal and vegetation events, and standing richness from the Plio-Pleistocene in the north-western Mediterranean area are included for comparison. Climatic trend is represented by thecomposite of the oxygen isotope record, δ18O (‰), from Shackleton (1996). Cyclity refers to the periodicity of the climate cycles. Standing richness is the number of species standardized at the midpointof the interval and the rate quotient is a measure of the intensity of turnover calculated as the ratio of the observed to the expected number of first or last occurrences, taking into account the standingrichness and the duration of the interval (from Azanza et al., 2000).

J. Rodríguez et al.

172 Global Ecology and Biogeography, 13, 163–176, © 2004 Blackwell Publishing Ltd

alternations of xeric-cool phases (glacials) and relatively humid-

warm phases (interglacials) began in the Villafranchian (interval

C), glacial maxima became more extreme between 1.07 and

0.99 Ma (at the beginning of interval F), with cycles of 100 ka

duration and the development of massive northern hemisphere

ice sheets (Fig. 4). The ‘Galerian mammal turnover pulse’, which

coincides with this climatic change, represents a major biotic

event in Europe and marks the onset of the modern Mediterra-

nean large-mammal fauna. At the Galerian, many of the lineages

that constitute the modern European mammal faunas appeared,

including humans (Carbonell et al., 1995; Bermúdez de Castro

et al., 1997; Oms et al., 2000). The present analysis confirms a

major shift in body size distribution of primary consumers at

interval F (Figs 2 and 3). The shift in body size distribution and

the coinciding increase in standing richness (Azanza et al., 1999,

2000) result from both an increase in body size of Bovidae and

Rhinocerotidae and a greater diversity of Cervidae. The number

of small- and medium-sized herbivores increased at the Galerian

with the appearance of Capreolus in interval F and new small and

medium-sized bovids (Rupicapra and Saiga) in interval H. At

the other end of the size distribution, new species of large-

bodied cervids (Megaloceros) and bovids (Bison, Bos and Ovibos)

appeared (Prado et al. in press). An increase in richness of Felidae

and Canidae is the most marked change for carnivores (Prado

et al. in press), although the change in body size distribution

of predators did not take place until interval G (Fig. 3). In

summary, this change in body size structure may be related

to the expansion of steppes during the now more intense glacial

periods and the development of new mammalian communities

characterized by the abundance of large and very large mammals

adapted to this new biome, the so called Mammoth steppe

(Guthrie, 1995).

A minor change in body size composition of mammalian fau-

nas occurred in the late Galerian and Maspinian (intervals H and

I), when the number of small carnivores increased, giving rise, in

turn, to an increase in standing richness (Azanza et al., 2000).

The high number of small carnivores in the Galerian and

Maspinian may be attributed to better current knowledge of this

group rather than to an actual increase in their numbers.

Finally, there is a marked change in body size composition

during the well-known extinction of megafauna (Stuart, 1991),

which occurred at the Pleistocene–Holocene boundary. This

moment is characterized by the absence of megaherbivores in the

recent fauna, and low numbers of large predators and large- and

medium-sized herbivores in comparison with the Maspinian

fauna. Whether this change was caused by sudden climatic

change or by intense human hunting has been the topic of heated

debate for decades (e.g. Stuart, 1991; Beck, 1996; Alroy, 2001;

Prado et al., 2001; Kerr, 2003) and is beyond the scope of this

paper.

A striking conclusion is that the shifts in the body size struc-

ture of the regional fauna do not always correlate with the

changes in vegetation. This results seems to indicate that the

changes in the body size structure are not mainly dependent on

environmental factors, or at least that other factors are highly

conditioning. Such factors may be of biogeographical-historical

character, highlighting again the importance of contingent

events on the composition of regional faunas.

Conclusions

The main change in the size distribution of the Plio-Pleistocene

north-western Mediterranean mammalian faunas occurred at

the early Galerian. This change is characterized by a dramatic

increase in the proportion of large and very large herbivores at

the expense of medium-sized herbivores. Medium-sized her-

bivores (45–360 kg) dominated the size distribution from the

Turolian to the late Villafranchian. From the late Pliocene to the

early Pleistocene (Villafanchian s.l.) a transition from subtropical

forests to Mediterranean forests and steppes occurred, producing

faunas dominated by large and very large herbivores in the

Galerian and Maspinian. However, the trend towards a fauna

composed of larger species began in the late Villafranchian, as

indicated by the absence of small herbivore species (< 45 kg) in

time intervals D and E. This shift in body size distribution of the

mammalian faunas at the late Villafranchian coincides broadly

with the Wolf-event detected by Azzaroli (1983) and with the

above mentioned environmental changes interpreted from data

on vegetation and geological indicators. It may be related to the

appearance of a new biome in Europe, the mammoth steppe,

caused by a change in the rate and intensity of the glacial cycles.

Finally, the comparison of recent faunas from several conti-

nents indicates that the size structure of a mammalian fauna is

clearly influenced by its biogeographical history. Since a direct

relationship between body size distribution and environmental

type is not observed in recent communities, it is difficult to use

body size to infer past environmental conditions. Body size com-

position of the present Mediterranean fauna differs greatly from

that of Pleistocene Mediterranean faunas. There are also major

differences in the ecological characteristics of the faunal assem-

blages. These differences should not be taken as evidence that

entirely different climates and environments existed in the

Pleistocene, but rather that these changes are the result of the

complex interaction of ecological and historical processes

and events (the extinction of megafauna being one of the

most significant). Since the Mediterranean climate has existed

since the early Villafranchian there is no reason to consider the

recent fauna ‘more typical’ of the Mediterranean climate than

Galerian or Maspinian faunas. After all, the body size distribu-

tion typical of the Galerian-Maspinian faunas lasted about

1 Ma in the region, whilst the recent distribution is only a few

millennia old.

ACKNOWLEDGEMENTS

The authors would like to thank C. Badgley, B. Sánchiz, M.

Hernández-Fernandez and E. Porter for critically reading and

improving the earlier drafts of this manuscript. This study was

supported by the following grants PB94-0071, PB97-1250 and

BTE2001-1684 of the DGICYT (Spain), Fundación Atapuerca to

JR and SECYT-UNC, PICT97-1166, and PIA-CONICET to JLP,

Argentina. Mr James Watkins corrected the English version.

Body size in Mediterranean faunas

Global Ecology and Biogeography, 13, 163–176, © 2004 Blackwell Publishing Ltd 173

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BIOSKETCHES

Jesús Rodríguez was awarded his doctorate from the

Universidad Autónoma de Madrid in 1997 for his

dissertation on the evolution of Pleistocene mammalian

communities in the Sierra de Atapuerca (Spain). The

focus of his research is on the factors that condition the

diversity and composition of past and present

mammalian communities.

María Teresa Alberdi, Beatriz Azanza and José Luis Prado are currently focusing their efforts

on projects dealing with the reconstruction of

palaeoenvironmental evolution and its influence on

evolutionary strategies, biogeographical distribution and

diversity changes of large mammal faunas during the last

8 Ma in the Western Mediterranean area, and its

correlation with the Southern Hemisphere. Dr Alberdi is a

Research Professor at CSIC, and Drs Azanza and Prado

are Professors of Palaeontology at the University of

Zaragoza and at the UNC, Buenos Aires, Argentina,

respectively.