NOTES
Abstract: According to central place foraging theory, adult Patagonian gray foxes (Pseudoalopex ,griseus) behaving
efficiently should consume on the spot those food items too large to be carried and those too small to warrant being
carried to the den. Consequently, fox cubs should be provisioned with intermediate-sized items. We tested this
prediction by analyzing 96 fecal samples from adult foxes and 82 fecal samples from cubs belonging to three different
dens collected near Junin de los Andes in the province of Neuqudn, Argentina, from November 1994 to January 1995.
As predicted, adult foxes consumed carrion of large ungulates (large items) and arthropods and berries (small items)
significantly more often than cubs 416. Cubs ate more intemiediate-sized vertebrates, from lizards and birds to rodents
and hares. Medium-sized armadillos, which are difficult to handle and transport, were consumed only by adults. Cubs
ate some insects, which were probably captured by the cubs themselves near the den.
Résumé : D’après l’hypothdse de la quête de nourriture autour d’un point central, on peut penser que, pour étre
efficaces, les renards de Patagonie (Pseudoalopex griseus) consommeront sur place les alimenis trop gros pour être
transportés ou trop petits pour qu’il vaille Ia peine de les transporter. En poursuivant ce raisonnement, il est permis de
croire que la nourriture apportée aux jeunes renards dans Ia taniére sera constituée d’aliments de taille intermddiaire.
Nous avons éprouvé cette hypothèse en analysant 96 échantillons de feces d’adultes et 82 échantilLons de feces de
jeunes provenant de trois tanidres diffdrentes, prés de Junin de los Andes, province de Neuqudn, en Argentine, de
novembre 1994 a janvier 1995. Tel que prévu, les adultes ont consommé significativement plus souvent des charognes
de gros ongulés (aliments de grande taille) ainsi que des arthropodes et petits fruits (petits aliments) que les jeunes.
Les jeunes ont consommé plus de vertdbrés de taille intermédiaire, ldzards, oiseaux, rongeurs et liCvres. Lcs tatous de
taille moyeime, difficiles a manipuler et a transporter, ont dté consommds exclusivemer,t par des adultes. Les jeunes ont
mange des insectes qu’ils ont probablement attrapés eux-mémes aux abords de leur taniCre.
[Traduit par la Redaction]
Introduction
Central place foraging (CPF) theory predicts that a singleprey carrier behaving optimally should cosis’arne osi the spot
food items that it could not economically bring to its feeding
place (Orians and Pearson 1979; Schoener 1979). This themy, frequently used to analyze patterns of food collection by
nesting birds (e.g., Kacelnik 1984), may also be applied to
breeding foxes, which usually bring individual food items to
the den to feed their cubs (Lovari and Parigi 1995).
Since Murie (1936, 1944), several authors (Englund 1969;
Harris 1981; Rau et al. 1985) have claimed that adult red
Received December 15, 1997. Accepted July 31, 1998.
S.C. Zapata, A. Travaini, and M. Delibes? EstaciOn
Bioldgica de Doflana, Consejo Superior de Investigaciones
Cientificas, Pabelh5n de Peni, Avenida Ma. Luisa s.n., 41013
Sevilla, Spain.
‘Author to whom all correspondence should be addressed
(e-mail: decastro@ebd03.ebd.csic.es).
foxes (Vulpes vulpes) seem to prefer to carry to their cubs
bulkier prey items than those they consume themselves.
Likewise, it may be expected that very large food items,
such as ungulates taken as carrion, should also be consumed
on the spot, as they cannot be carried away. Hence, we predict that during the rearing period, adult foxes should consume either larger or smaller food items than their cubs,
which should be provisioned with intermediate-sized food
items.
To test our prediction, we studied the diets of adults and
cubs of the Patagonian gray fox (Pseudoalopex grireus).
This is a small fox (approximately 3 kg in the study area;
unpublished data) inhabiting plains, pampas, deserts, and
low mountains (Ginsberg and Macdonald 1990) from
Atacama (northern Chile) and Santiago del Estero (northeastern Argentina) to Tierra del Fuego (Cabrera 1958; Wilson and Reeder 1993). Its feeding habits have been studied
chiefly in Chile, where it is considered an opportunistic
feeder that hunts prey, mainly rodents, according to their
availability (Medel and Jaksic 1988). Up to now, detailed information on the diet of gray fox cubs in the den has been
Table 1. Frequency of occurrences of prey in the feces of adults
and cubs of the Patagonian gray fox (Pseudoalopex griseus).
Food item
Mammals
Order Xenarthra
Zaidyus pichiy (1.2)
Order Artiodactyla
Cervus elaphus (>20)
Ovis aries (>20)
Order Lagornorpha
Lepus europaeus (<3)
Order Rodeatia
Adults
(a = 96 fecal
samples)
Cubs
(it = 82 fecal
samples)
8
To reduce biases, diet results were expressed in two ways: (1) percent occurrence and (2) percent dry mass of each food type in feces. We assume that this provides a good representation (Corbett
1989) uf the food items consumed directly by adults or brought to
6
the den and consumed by the cubs.
10
24
1
Oryzomys longicaudarus
(0.03)
Auliscomys mkropus (0.07)
Eliginodontia typus (0.02)
!renornys tarsalis (0115)
Ph9llotis danvini (0.06)
Rèithrodon auritus (0.08)
Akodon sp. (0.03)
Geoxus valdivio.nus (0.03)
Galea musteloides (0.25)
Ctenomys haigi (0.15)
Unknown
Birds (<0.5)
Lizards (<0.05)
Arthropods (<0.01)
Berries (<0.01)
those of adults by their very small size (moreover, incorrect assignment of adult feces to cubs should be conservative, as our nul.t
hypothesis is that adults and cubs consume the same types of food
items).
The components of the feces were separated by Land. Mammals
were identified to the species level, based on hair and bone remains. Food items were arbitrarily assigned to three groups: large
and (or) difficult to carry (ungulates, armadillos), intermediatesized (hares, rodents, birds, reptiles), and small (insects, berries).
2
2
2
4
9
20
7
7
1
12
7
18
2
1
8
5
8
5
45
21
39
—
—
24
Total
177
128
Note: The numbers in parentheses show the approximate mass (kg) of
food items.
lacking, although Johnson and Franklin (1994) reported that
both parents provisioned pups with mice, hares, birds, and
duck eggs.
Study area and methods
‘The study was carried out from November 1994 to January 1995
on Catán-Lil ranch, 50 km northeast of Junin de Los Andes in the
province of Neuquén, Argentina (40°S, 71°W). The area belongs
to the Patagonian phytogeographic province Western District
(Cabrera 1976), and is characterized by great plains 800—900 m
high, dissected by steep, rugged valleys. The vegetation is a naixed
steppe of grass and shrubs dominated by Mullium spin osurn,
Senecio sp., Stipa sp., and Faa sp. The mammalian fauna is charac.teristic of the ch-y Patagonian shrub—steppe (Pearson and Pearson
1982), but introduced European brown hares (Lepus europaeus)
and, to a lesser extent, European red deer (Cervus elaphus) and
wild boar (Sus scrofa), are common. The annual mean temperature
is 17.4’C, and the annual mean rainfall is 360 mm, mostly falling
during winter (June—August).
Ninety-six fecal samples from adult foxes were collected in an
area of approximately 4000 ha, while 82 fecal samples from cubs
were collected in three different dens separated by more than 1 km
within the same area. Cubs were born in October, and in January
they were still living in the den or its surroundings (Johnson and
Franklin 1994), where their feces can be easily distinguished from
Results
Food items consumed by adult gray foxes in Catdn-Lil included mammals (at least 14 species), birds, reptiles, arthropods, and berries (Table 1). Rodents were the best represented
group (31.1% of all occurrences and 33% of dry mass in feces), followed by berries (22 and 22.3%, respectively) and
asthropods (25.4 and 13.7%, respectively). Carrion was represented by the remains of sheep, deer, and perhaps armadillos (8.5% of occurrences and 19.9% of dry mass overall).
Lagomorphs, birds, and lizards were of less importance (below 6% of occurrences and 7% of dry mass each).
The list of food items brought for cubs was less diverse,
including mammals (nine species), birds, reptiles, and arthropods (Table 1). As with adults, rodents were the main prey
of cubs (46.1% of all occurrences and 57.1% of dry mass in
feces). Lagomorphs (18.8 and 22%, respectively), birds (16.4
and 13.2%, respectively), and arthropods (18.8 and 7.7%, respectively) were the next most prevalent items in the diet.
No carrion or berries were detected in cubs.
Percent occurrence and percent dry mass in feces of small,
intermediate-sized, and large food items (as previously defined) differed in the diets of adults and cubs (0 test, p <
0.001) (Fig. 1). Cubs consumed more intermediate-sized
food items, including birds, rodents, aM lagomorphs, and
fewer large (ungulates) and small food items (berries and
arthropods). Interestingly, the medium-sized armadillo (Z2edyus pichiy), which is difficult to handle and carry away,
was eaten only by adults.
Discussion
We did not attempt to test CPF theory, but rather a specific prediction derived from it. An experimental testing of
CPF theory should consider the “currency” to be optimized
(for instance, the energetic value or the nutritious components of the food item as benefit, and the time (distance) or
energy needed to bring it to the feeding place as cost). We
have assumed that all types of food items had the same
probability of being found at every distance from the feeding place and that the size of a food item is a good estimator
of its. nutritional value and the energy needed to take it away
(Lindsironi 1994). Under these conditions, intermediatesized items should be brought to the den more often than
large or small items.
The results seem to confirm our prediction. However, the
predominance of intermediate-sized food items in the cubs’
diets may arise from a sampling bias because a prey items
that yield more remains (intermediate-sized rather than small
prey) can be handled for a longer time around the den
(Lloyd 1980). Nevertheless, such a bias should overestimate
the frequency of occurrence of large prey, contrary to our results. Lindstrom (1994) specifically addressed this point by
comparing the relationship between the frequencies of occurrence of large and small prey in the diets of adults and
cubs of the Swedish red fox over 3 years, concluding that
proportions were not consistent through the years and therefore the hypothesis of sampling bias was not supported.
Resolving at least two other methodological questions
could modify the interpretation of our results. On one hand,
medium-sized portions of large items, such as deer and
sheep, could be brought to the den. Again, ignoring this possibility is conservative, as it favours the null hypothesis of
similar diets in adult foxes and cubs. On the other hand,
cubs could be fed raw meat from large food items, leaving
no remains in seats. While we have confidence in our results
(usually it is possible to recognize significant amounts of ingested soft food in the feces; also, it is unlikely that no hair
will be found), this is a real possibility, although it is improbable,.
Undoubtedly the small Patagonian gray fox cannot carry
ungulates to the den (but see the previous paragraph) and
probably finds it difficult to carry hard-shelled armadillos in
its mouth. Also, it would be unprofitable to take small berries and insects to provision the cubs unless large amounts
of these foods were eaten and subsequently regurgitated, but
this behaviour is unfrequent in foxes (Lovari and Parigi
1995). However, insects were well represented in the feces
of the cubs, probably because they were able to capture insects themselves close to the den (Murie 1936).
Several authors have found differences in the size of food
items eaten by adults and cubs of the Holaretic red fox
Englund (1969) observed in Sweden that adult foxes carried
hares for feeding cubs at the den, while they themselves fed
on rodents (rodents are relatively small prey for the red fox,
which weighs about 6—7 kg, while they would be considered
medium-sized prey for the smaller- gray fox). In southern
Spain, adult red foxes consumed berries and insects but
provisioned their cubs with rabbits (Rau et al. 1985). Also,
in suburban London, adult foxes fed selectively on the
smaller food items obtained, carrying the larger ones to the
cubs (Harris 1981). In all these cases, adult foxes consumed
the smaller and less rewarding prey on the spot and fed their
cubs the rulatively bulky items that could be carried, which
is in accord with CPF theory.
However, Lovari and Parigi (1995) found that adult foxes
consumed large pheasants, but selected for their cubs small
and medium-sized passerines, probably because they are
easier to digest. This observation opens up the possibility of
alternative hypotheses (e.g., protein may be more important
than gross energy for the growing pups, or adults could select suitable partially succumbed prey for bringing to the
den in order to stimulate cubs to chase them).
In a review of the feeding ecology of the gray fox in
Chile, Medel and Jaksic (1988) found that rodents were the
principal component of the diet of this canid, followed by
birds and insects. Fruits, lagomorphs, and reptiles were
Fig. 1. Percent occurrence and percent dry mass of of large,
intermediate-sized, and small food items in the feces of adults
and cubs of the Patagcmian gray fox (Psendra1opex grisecs).
Armadillos are included in the first category because of the
difficulty of carrying them for a small fox.
food item
poorly represented, depending on region and season. During
the rearing period in our study area, the gray fox followed
this general pattern, although berries occurred in the feces of
adults of this species more often than in those of Chilean
gray foxes. In any case, dietary changes according to season
and geographic location must be expected in an opportunistic forager such as the gray fox.
Acknowledgements
We are grateful to 0. Ceballos, 13. Castillo, LA. Donázar,
M. Funes, F. Hiraldo, and 0. Monsalvo for help with the
fieldwork. 0. Alefiá permitted us to work on his land. A. del
Valle and the Centro de Ecologla Aplicada del Neuqudn (Argentina) provided us with logistic support and kind assistance. M.C. Blázquez, P. Ferreras, S. Lovari, F. Palomares,
E. Revilla, and J. Weaver improved earlier versions of the
manuscript. Financial support was provided by the Instituto
de Cooperacidn Iberoamericana, Ministerfo de Asuntos
Exteriores (Spain) through the Prograrna de Cooperacidn
Cicnt(flea con Iberoamérica. AT. has a postdoctoral fellowship from the Spanish Ministeria de Educacidn y Cultura.
References
Cabrera, A.L. 1958. Catálogo de los mamIferos de America del
Sur, 1. Metatheria, Unguiculata, Carnivora. Rev. Mus. Argent.
list. Nat. “Bernardino Rivadavia” Zool. 4: 1—307.
Cabrera, AL. W76. Territorios fitogeográficos de Ia Repdblica Argentina. In Enciclopedia Argentina Agricultura y Jardineria. 2nd
ed. Editorial Acme SACI, fluenos Aires.
Corbett, L.IC 1989. Assessing the diet of dingoes from feces: a
comparison of thee methods. 3. WildI. Manage. 53: 343—346.
Englund, 3. 1969. The diet of fox cubs (Vulpes vrdpes) in Sweden.
Viltrevy (Stockh.), 6: t—39
Ginsberg, .LR., and Macdonald, D.W. 1990. Foxes, wolves, jackals,
and dogs; an action plan for the conservation of eanids. International Union for Conservation of Nature and Natural Resources,
Gland, Switzerland.
Harris, S. 1981. The food of suburban foxes (Vulpes wipes), with
special reference to London. Mammal Rev. 4: 151—168.
Sohnson, WE., and Franklin, W.L. 1994. Conservation implications of South American grey fox (Dusicyon griseur)
socioecology in the Patagonia of southern Chile. Vida Silvestre
Neotr. 3: 16—23.
Kacelnik, A. 1984. Central place foraging in starlings (Siun,us
vuigaris). L Patch residence time. 1. Anita. Ecol. 53: 283—299.
Lindstrom, ER. 1994. Large prey for small cubs: on crucial resources of a boreal red fox population. Ecography, 17: 17—22.
Lloyd. 11.0. 1980. The red fox. B.’l’. Batsiord Ltd., London.
Lovari, S., and Parigi, L 1995. The red fox as a gamebird killer or
a considerate parent? Manimalia, 59: 455—459.
Medel, R.G., and Jaksic, F. 1988. Ecologia de los cinidos
sudatnericanos: usia revi.sidn. Rev. Chit. Rist. Nat. 61: 67—79.
Murie, A. 1936. Following fox trails. Misc. Publ. Mus. Zool. Univ.
Mich. 32: 1—45.
Murie, A. 1944. The wolves of Mount McKinley. Fauna of the national parks of the United States. Fauna Series No. 5. U.S. Government Printing Office, Washington, D.C.
Orians, G.H., and Pearson, N.E. 1979. On the theory of central
place foraging. In Analysis of ecological systems. Edited by D.J.
Horn, G.R. Stairs, and RI). Mitchell. Ohio State University
Press, Columbus. pp. 155—177.
Pearson, O.P., and Pearson, A.K. 1982. Ecology and biogeography
of the southern rainforest of Argentina. In Mammalian biology
of South America. Edited by A.M. Mares and H.H. Genoways.
Pymatunirtg Laboratory of Ecology, Pittsburgh. pp. 129—142.
Rau, J.R., Beltrdn, J.F., and Delibes, M. 1985. Can the increase of
fox density explain the decrease in lynx numbers at Doflana?
Rev. Ecol. Terre Vie, 40: 145—150.
Schoenex, T.W. 1979. Generality of the size-distance rtiation in
models of optimal feeding. Am. Nat. 114: 902—914.
Wilson, D.E., and Reeder, O.K 1993. Mammal species of the
world. 2nd ed. Smithsonian Institution Press, Washington, D.C.,
and London.
C 1998 NRC Canada