Habitat-related microgeographic body size variation in two
Mediterranean populations of red fox (Vulpes vulpes)
C. Gorta’ zar1,2*, A. Travaini3,4 and M. Delibes3
1
SEDIFAS Wildlife Diagnostic Service, Facultad de Veterinaria, Universidad de Zaragoza, c.I Miguel Servet 177, E-50.013 Zaragoza, Spain
Ebronatura S.L., Co Cabezo’ n s.n., E-50.730 El Burgo de Ebro, Spain
3
Estacio’ n Biolo’ gica de Don ana (CSIC), Avda. Ma Luisa s.n., E-41.013 Sevilla, Spain
4
Universidad Nacional de la Patagonia Austral, Centro de Investigaciones de Puerto Deseado, Almte. Brown y Colo’ n s.n., Puerto Deseado
9050, Santa Cruz, Argentina
2
Abstract
The habitat-related microgeographical body size variations in red foxes Vulpes vulpes living in two
separated areas of Mediterranean Spain, the Central Ebro Valley (CEV) and Don ana National Park
(DNP) are analysed. In both areas, samples taken from good and bad fox-habitats were compared
regarding body weight and head and body length. In the Ebro Valley, foxes collected in the good habitat
were heavier (14%, P < 0.001 for males; 9%, P < 0.01 for females) and larger (4%, P < 0.01 for males; 1%,
P < 0.05 for females) than those collected in the bad habitat. In Don ana, males from the good habitat were
19% heavier (P < 0.01) and 3% longer (P < 0.05) than those from the poorer one. The average weight and
size of DNP vixens did not show significant differences, although both are higher in the good habitat. It is
shown that body size of adult foxes can vary, linked to habitat change even across short geographic
distances. Some tentative explanations for these results are discussed.
Key words: despotic distribution, red fox, body size, Spain, variation, Vulpes vulpes
INTRODUCTION
Size is one of the most significant characteristics of any
animal, as it is related to its life-history patterns,
comparative physiology, ecology and behaviour
(Calder, 1984). Consequently, the study of body size
variation has received considerable attention.
Frequently, geographic variation in body size has
been interpreted as a long-term adaptation to environmental conditions (e.g. the so-called ecogeographical
rules, which linked size differences to latitudinal or
climatic gradients; Mayr, 1956; Geist, 1987). However,
there is increasing evidence of high intraspecific body
size variation over the short-term, in space (e.g.
Ulfstrand et al., 1981) as well as in time (e.g. Kruuk &
Parish, 1983). These differences are usually related to
food availability (Rosatte, Power & MacInnes, 1991),
prey size (King, 1991) and character displacement associated to intragremial competition (Fuentes & Jaksic,
1979; Palomares & Caro, in press).
Here we analyse the microgeographical body size
variations in red foxes Vulpes vulpes living in two
*All correspondence to present address: Dr C. Gorta’ zar, Instituto de
Investigacio’ n en Recursos Cinege’ ticos IREC (CSIC-UCLM-JCCLM)
P.O. Box 535, E-13.080 Ciudad Real, Spain
unrelated areas of Mediterranean Spain. Our aim is to
prove that the average body size of adult foxes can vary,
linked to habitat change even across short geographic
distances, and to discuss some tentative explanations for
our results. If the average body size of foxes varies
widely in the short-term, some traditional long-term
adaptive interpretations based on this character (e.g.
Davis, 1977) should be taken with caution.
STUDY AREA AND METHODS
We have replicated our observations in 2 areas
separated by about 900 km. In each area, 2 contiguous
but a priori different-quality habitats were distinguished.
Foxes are generalists and very catholic feeders, eating
carrion, garbage, vertebrates, insects and fruits (Harris
& Lloyd, 1991). Hence, we assume that crude productivity may be a good estimator of food availability, and
therefore of habitat quality.
The first area is the Central Ebro Valley (CEV;
41°30’N, 01°00’W), with a continental Mediterranean
climate (rather rainy and cold winters and hot and dry
summers). Most of this area is a low-productive semiarid steppe devoted to cereal cultures, but along the
main rivers there are irrigated high-productive ‘Vegas’
Table 1. Body weight (g) and head and body length (mm) of adult red foxes sampled in the Central Ebro Valley and in Donana
National Park. The table shows for each class the average ± sE and the sample size (in parentheses)
Central Ebro Valley
Body weight (g)
Head and body length (mm)
Males
Females
Males
Females
Donana National Park
Good habitat
Bad habitat
Good habitat
Bad habitat
6907 ± 220 (21)
5833 ± 247 (23)
701 ± 7.11 (29)
661 ± 7.74 (24)
6043 ± 101 (81)
5223 ± 81 (103)
674 ± 4.63 (98)
641 ± 3.59 (128)
6600 ± 176 (30)
5130 ± 143 (20)
714 ± 6.03 (30)
663 ± 5.30 (20)
5539 ± 144 (28)
4703 ± 150 (29)
690 ± 7.04 (29)
652 ± 5.41 (29)
where most of the human population is concentrated.
Plots of land are smaller and crops more diverse in the
Vegas, and cereal and Leguminosae production per
hectare is 3 times higher here than in the semi-arid
steppe (Diputacio’ n General de Arago’ n, 1997). Moreover, in both habitats, the main biomass intake of foxes
is garbage and carrion of domestic livestock (Gorta’ zar,
1997), and most villages and livestock breeding facilities
are placed in the Vegas (Diputacio’ n General de Arago’ n,
1982). Fish, another important food item in spring, is
only available in the Vegas (Gorta’ zar, 1997). Therefore,
we compare body size of foxes captured in the Vegas
(assumed to be the ‘good habitat’) and in the steppe
(‘bad habitat’).
The second area is the Donana National Park (DNP;
37°00’N, 06°30’W), with a sub-humid Mediterranean
climate (rainy and mild winters and hot and dry
summers). About one-half of the area is a low marsh
flooded during the winter, and the other half is a scrubland on sandy dunes (mostly fixed). This scrubland can
be divided into dry pure Mediterranean and humid,
more Atlantic scrubland. Pure Mediterranean scrubland
includes a 3200 ha patch of pine Pinus pinea plantation
with a high stem density and very low productivity. The
second one includes a highly productive ecotone between
the marsh and the uplands, locally called ‘Vera’. Annual
grass productivity in Donana (estimated as dry
weight I ha) is between 10 and 30 times higher in the
humid than in the dry scrubland (Lazo, 1992). In
addition, the Donana foxes eat European rabbits
Oryctolagus cuniculus when available (Fedriani, 1996),
and rabbit abundance is about 6 times higher in the
humid scrubland (Moreno & Villafuerte, 1995). Carrion
is another important food item (Fedriani, 1996). Sources
of carrion (free ranging cows, red deer, Cervus elaphus
and Dama dama, and wild boar, Sus scrofa) are from 10
to 20 times more abundant in the humid scrubland and
the Vera (R. Soriguer, pers. comm.). Hence, we compare
body size of foxes captured in the humid scrubland and
the Vera (assumed to be the ‘good habitat’) and in the
dry scrubland and pine plantation (‘bad habitat’).
Fox carcasses in CEV were collected from hunters
from 1989 to 1996. In DNP, foxes were trapped in
control programs between 1988 and 1994. All foxes
were aged by counts of cementum annuli in premolars
and by cursory examination of complete dentition,
which was enough to distinguish young individuals
(Zapata, Travaini & Delibes, 1995).
Total body mass (g) and head and body length
(maximum length from the tip of the snout to the dorsal
edge of the perineum, in mm) were recorded for each
carcass. To eliminate age-specific variation, only foxes
older than 12 months were considered, as age-related
changes in body size after the first autumn of life are
insignificant in the species (Cavallini, 1995). Data on body
mass of pregnant or lactating females were not included.
All data sets were tested for normal distribution
(Kolmogorov—Smirnoff test; Zar, 1984). Mean body
measurements were then compared using Student’s
t-test (Zar, 1984).
RESULTS
A total of 391 adult red foxes (179 in CEV and 112 in
DNP) were weighed and measured for this study, but
not all data could be obtained from all the carcasses.
The results are shown in Table 1.
In the Ebro Valley, male foxes collected in the good
habitat (‘Vegas’) were on average 14% heavier (t = 5.53,
100 d.f., P < 0.001) and 4% longer (t = 3.31, 125 d.f.,
P < 0.01) than those collected in the bad habitat (dry
steppe). Also, females from the irrigated land were 9%
heavier (t = 3.22, 124 d.f., P < 0.01) and 1% longer
(t = 2.20, 150 d.f., P < 0.05) than those collected in the
steppe.
In Donana, males from the good habitat (‘Vera’) were
on average 19% heavier (t = 2.82, 56 d.f., P < 0.01) and
3% longer (t = 2.40, 57 d.f., P < 0.05) than those from
the pine plantation. The average weight and size of
females did not show significant differences, although
both were higher in the good habitat of the DNP.
DISCUSSION
Our results consistently show that foxes of the more
productive habitats are bigger and heavier than those
living in the poorer habitats. This is especially clear for
males. Interestingly, in each study area the two distinguished habitats are contiguous, without any barriers
preventing the rather mobile foxes from migrating
between them. Individuals from both study areas and all
four habitats were collected in the same period, and the
seasonal distribution of the sampling effort was similar
in each, avoiding biases resulting from seasonal weight
changes. Thus, the observed differences are considered
genuinely habitat-related.
Unpublished data of the authors suggest higher fat
deposits in foxes from good habitats in CEV (Gorta’ zar,
1997) and DNP (Travaini, 1994). Even though more fat
may not necessarily indicate better condition (Prestrud
& Nilssen, 1992), higher food-availability andIor lower
energy expenditure in the apparently better habitats
of both areas could partially explain the observed
differences in body weight, but not in size.
Several, not mutually exclusive, hypotheses could be
applied to explain the size variation on a microgeographical scale. Most of them have been used to justify size
variation in canids or other carnivores.
Character-displacement due to intraguild competition
(Dayan et al., 1989) is difficult to assess, but does not
explain the repeated pattern we found in CEV and
DNP. In Donana, the size of the red fox may be
influenced by the presence of the Iberian lynx Lynx
pardinus, which lives only in the wet scrubland and
occasionally kills foxes (Palomares et al., 1996).
However, there are no lynxes in the Ebro Valley, where
potential competitors of foxes coincide in the good and
in the bad habitat.
In addition, body size could be influenced by differential prey size (Schmitz & Lavigne, 1987). European
rabbits O. cuniculus are the biggest common prey of the
fox in both areas, but they are mainly eaten in the bad
habitat in CEV (Gorta’ zar, 1997) and in the good
habitat in DNP (Delibes et al., 1992). Hence, in our
areas prey size does not seem to be a good candidate to
explain the habitat-related size differences.
A third possibility is that size variations reflect
differences in food availability (Geist, 1987; Geffen
et al., 1992), especially during the first months of life, or
differences in population density (Cavallini, 1995).
Foxes in suboptimal habitats would be smaller because
they receive less food while growing. However, this
implies some kind of phylopatry (foxes growing in the
best habitats remain in these habitats) and radiotracking data suggest that juvenile foxes (especially
males) disperse tens of kilometres through different
habitats, in CEV (Gorta’ zar, 1990) as well as in DNP
(J. M. Fedriani, pers. comm.).
Finally, a fourth possibility related to social dominance probably represents the more compatible
explanation of our results. Larger individuals can be
expected to dominate over smaller conspecifics in resource contests (Dawkins & Krebs, 1978), and hence
larger foxes will be able to defend territories in optimal
habitats, relegating small ones to inferior quality habitats. This is the main prediction of the ideal despotic
distribution (Fretwell & Lucas, 1970). Note that since
territorial contests in the red fox are conducted mainly
between males (Macdonald, 1983), interhabitat size
differences for this reason are to be expected mainly in
this sex; this is the pattern observed in both study areas.
Additionally, size plasticity is usually higher in males, as
maximum size of females is probably set by the energy
requirements of reproduction (Moors, 1980; Powell &
King, 1997).
More research is needed to prove that a despotic
distribution (i.e. social dominance combined with
differential food availability) is the cause of the microgeographic size variation of red foxes. Anyhow, the high
plasticity in body size found, and also detected in other
animals such as birds (Ulfstrand et al., 1981; Bost,
Jouventin & Pincson-du-Sel, 1992) and reptiles (Roughgarden & Fuentes, 1977), emphasizes the importance of
considering small geographical scales in the study of
body size variation, and advises against making some
general inferences about the effects of long-term
selection.
Acknowledgements
We thank the staff of the Donana Biological Reserve
and that of DNP for their general assistance. We also
acknowledge Dr J. Aldama, Dr P. Ferreras, R. Laffitte,
A. Donaire and F. Ayala for their field assistance, while
S. Zapata performed several histological age estimations. Funds were provided by the Instituto para la
Conservacio’ n de la Naturaleza (ICONA) and Direccio’ n
General de Ciencia y Tecnologia; Project PB90-1018
(AT, MD), and by the Direccio’ n General del Medio
Natural, Gobierno de Arago’ n (CG). Dr R. Villafuerte
and Dr J. C. Blanco provided ideas for the discussion.
REFERENCES
Bost, C. A., Jouventin, P. & Pincson-du-Sel, N. (1992). Morphometric variability on a microgeographical scale in two inshore
seabirds. J. Zool. (Lond.) 226: 135—149.
Calder, W. A., III. (1984). Size, function and life history. Cambridge, MA: Harvard University Press.
Cavallini, P. (1995). Variation in the body size of the red fox. Ann.
Zool. Fenn. 32(4): 421—427.
Davis, S. (1977). Size variation of the fox, Vulpes vulpes, in the
Palearctic Region today, and in Israel during the late Quaternary. J. Zool. (Lond.) 182: 343—351.
Dawkins, R. & Krebs, J.R. (1978). Animal signals: information
or manipulation? In Behavioural ecology: an evolutionary
approach: 282—315. Krebs, J. R. & Davies, N. B. (Eds).
Oxford: Blackwell.
Dayan, T., Tchernov, E., Yom Tov, Y. & Simberloff, D. (1989).
Echological character displacement in Saharo-Arabian Vulpes:
outfoxing Bergmann’s rule. Oikos 55: 263—272.
Delibes, M., Ferreras, P., Travaini, A. & Laffitte, R. (1992).
Evolucio‘i n de las poblaciones de carni’voros del Parque Nacional
de Donana. Sevilla: ICONA. Unpublished report.
Diputacio’ n General de Arago’ n (1982). Estudio de reconocimiento
territorial de Arago‘i n. Zaragoza: Centro de Estudios de Ordenacio’ n del Territorio, D.G.A.
Diputacio’ n General de Arago’ n (1997). Anuario estadi’stico agrario
de Arago‘i n 1996. Zaragoza: Departamento de Agricultura y
Medio Ambiente, D.G.A.
Fedriani, J. M. (1996). Dieta anual del zorro, Vulpes vulpes, en
dos ha’ bitats del Parque Nacional Donana Donana, Acta Vert.
23: 143—152.
Fretwell, S. D. & Lucas, H. L. (1970). On territorial behaviour
and other factors influencing habitat distribution in birds.
I. Theoretical development. Acta Biotheor. 19: 16—36.
Fuentes, E. R. & Jaksic, F. M. (1979). Latitudinal size variation of
Chilean foxes: tests of alternative hypotheses. Ecology 60:
43—47.
Geffen, E., Hefner, R., MacDonald, D. W. & Ucko, M. (1992).
Morphological adaptations and seasonal weight changes in
Blanford’s fox, Vulpes cana. J. Arid Environ. 23: 287—292.
Geist, V. (1987). Bergmann’s rule is invalid. Can. J. Zool. 65:
1035—1038.
Gorta’ zar, C. (1990). Medidas de control para las poblaciones de
zorro: Implicaciones en la sanidad y la predacio‘i n de la fauna
silvestre. Diputacio’ n General de Arago’ n. Unpublished report.
Gorta’ zar, C. (1997). Ecologi’a y patologi’a del zorro en el
Valle Medio del Ebro. PhD thesis, University of Zaragoza,
Spain.
Harris, S. & Lloyd, H. G. (1991). Fox Vulpes vulpes. In The
handbook of British mammals: 351—367. Corbett, G. B. &
Harris, S. (Eds). Oxford: Blackwell.
King, C. M. (1991). Body size—prey size relationships in European
stoats Mustela erminea: a test case. Holarctic Ecol. 14: 173—185.
Kruuk, H. & Parish, T. (1983). Seasonal and local differences in
the weight of European badgers (Meles meles) in relation to
food supply. Z. Sa” ugetierkd. 48: 45—50.
Lazo, A. (1992). Socioecologi’a del ganado bovino asilvestrado de la
Reserva Biolo‘i gica de Donana. PhD thesis, University of Sevilla,
Spain.
Macdonald, D. W. (1983). The ecology of carnivore social behavior. Nature 301: 379—384.
Mayr, E. (1956). Geographical character gradients and climatic
adaptation. Evolution 10: 105—108.
Moors, P. J. (1980). Sexual dimorphism in the body size of
mustelids (Carnivora): the roles of food habits and breeding
systems. Oikos 34: 147—158.
Moreno, S. & Villafuerte, R. (1995). Traditional management of
scrubland for the conservation of rabbits Oryctolagus cuniculus
and their predators in Donana National Park, Spain. Biol.
Conserv. 73: 81—85.
Palomares, F. & Caro, T. M. (In press). Interspecific killing
among mammalian carnivores. Am. Nat. 153.
Palomares, F., Ferreras, P., Fedriani, J. M. & Delibes, M. (1996).
Spatial relationships between Iberian lynx and other carnivores
in an area of south-western Spain. J. appl. Ecol. 33: 5—13.
Powell, R. A. & King, C. M. (1997). Variation in body size, sexual
dimorphism and age-specific survival in stoats, Mustela erminea
(Mammalia: Carnivora), with fluctuating food supplies. Biol. J.
Linn. Soc. 62: 165—194.
Prestrud, P. & Nilssen, K. (1992). Fat deposition and seasonal
variation in body composition of arctic foxes in Svalbard.
J. Wildl. Manage. 56: 221—233.
Rosatte, R. C., Power, M. J. & MacInnes, C. D. (1991). Ecology
of urban skunks, raccoons, and foxes in metropolitan Toronto.
In Wildlife conservation in metropolitan environments: 31—38.
Adams, L. W. & Leedy, D. L. (Eds). Columbia: NIUW
Symposium Serie 2. National Institute for Urban Wildlife.
Roughgarden, J. D. & Fuentes, E. (1977). The environmental
determinants of size in solitary populations of West Indian
Anolis lizards. Oikos 28: 44—51.
Schmitz, O. J. & Lavigne, D. M. (1987). Factors affecting body
size in sympatric Ontario canis. J. Mamm. 68: 92—99.
Travaini, A. (1994). Demografi’a de la Poblacio‘i n de zorros (Vulpes
vulpes) del Parque Nacional de Donana. PhD thesis, University
Auto’ noma de Madrid, Spain.
Ulfstrand, S., Alatalo, R. V., Carlson, A. & Lundberg, A. (1981).
Habitat distribution and body size of the great tit Parus ma]or.
Ibis 123: 494—499.
Zapata, S. C., Travaini, A. & Delibes, M. (1995). Comparacio’ n
entre varias tecnicas de estimacio’ n de la edad en zorros, Vulpes
vulpes, de Donana (sur de la Peninsula Ibe’ rica). Donana Acta
Vert. 22: 29—50.
Zar, J. H. (1984). Biostatistical analysis. New Jersey: Prentice-Hall.