J. Zool., Lond. (1977) 182, 343-351 Size variation of the fox, Vulpes vu&s in the palaearctic region today, and in Israel during the late Quaternary SIMON DAVIS Department of Zoology, The Hebrew University, Jerusalem (Accepted 9 November 1976) (With 3 figures in the text) Fox size variation, both today over a wide geographic range and during the late quaternary in Israel, was correlated with temperature changes. Competition with the related Asiatic jackal was not considered to have any effect on fox size; the degree of dwarfing of the fox was utilized in a speculative estimate of the Pleistocene-Holocene temperature rise. Contents Page Introduction. . . . . . . . . . . . . . . . . . . . . . 343 Material and methods .................. 344 Results ...................... 347 Discussion ...................... 349 Summary ...................... 350 References . . . . . . . . . . . . . . . . . . . . . . 350 Introduction Temperature is among several factors that influence body size in mammals, larger body size is selectively advantageous in cold climates; this is the basis of Bergmann’s rule, and has often been invoked (Rensch, 1959; Mayr, 1963). However it has been criticized, in particular by McNab (1971) for carnivores, who suggested that competition between closely related species is of greater importance, in regions of sympatry a size differential between species is selected for, this being known as “character displacement” (Brown & Wilson, 1956). The fox is distributed today throughout the palaearctic region of Europe, Asia (except the Tundra) and North Africa as well as North America (Ellerman & Morrison-Scott, 1966; Harrison, 1968). In Israel it is the most common carnivore both today and in fossil assemblages from prehistoric sites. Kurttn (1965) who studied the carnivore remains from upper Pleistocene and Holocene sites of Israel and Lebanon, discovered that most carnivores underwent considerable size changes during this time period. Since KurtCn’s work, much additional fossil material has been excavated, and in addition an analysis of size variation of the fox today over a wide geographical range, enables past size changes to be viewed in some kind of perspective. In this paper it is enquired whether or not size variation in the fox is more likely to be related to variation in external temperature or to size contrasts in sympatric species. 343
Transcript
J. Zool., Lond. (1977) 182, 343-351
Size variation of the fox, Vulpes vu&s in the palaearctic region today, and in Israel during the late Quaternary
SIMON DAVIS Department of Zoology, The Hebrew University, Jerusalem
(Accepted 9 November 1976)
(With 3 figures in the text)
Fox size variation, both today over a wide geographic range and during the late quaternary in Israel, was correlated with temperature changes. Competition with the related Asiatic jackal was not considered to have any effect on fox size; the degree of dwarfing of the fox was utilized in a speculative estimate of the Pleistocene-Holocene temperature rise.
Introduction Temperature is among several factors that influence body size in mammals, larger
body size is selectively advantageous in cold climates; this is the basis of Bergmann’s rule, and has often been invoked (Rensch, 1959; Mayr, 1963). However it has been criticized, in particular by McNab (1971) for carnivores, who suggested that competition between closely related species is of greater importance, in regions of sympatry a size differential between species is selected for, this being known as “character displacement” (Brown & Wilson, 1956).
The fox is distributed today throughout the palaearctic region of Europe, Asia (except the Tundra) and North Africa as well as North America (Ellerman & Morrison-Scott, 1966; Harrison, 1968).
In Israel it is the most common carnivore both today and in fossil assemblages from prehistoric sites. Kurttn (1965) who studied the carnivore remains from upper Pleistocene and Holocene sites of Israel and Lebanon, discovered that most carnivores underwent considerable size changes during this time period. Since KurtCn’s work, much additional fossil material has been excavated, and in addition an analysis of size variation of the fox today over a wide geographical range, enables past size changes to be viewed in some kind of perspective.
In this paper it is enquired whether or not size variation in the fox is more likely to be related to variation in external temperature or to size contrasts in sympatric species.
343
344 S . DAVIS
Material and methods Recent specimens of foxes were examined in the collections of the Tel Aviv University; the
Hebrew University, Jerusalem ; the Payne collection in the British School of Archaeology, Ankara ; the British Museum (Natural History) ; MusCe d’Anatomie Comparte, Paris ; the Harrison Zoological Museum, Sevenoaks, England, and the Staatesammlung, Munich. Measure- ments quoted in the literature were utilized for Holland (Hooijer, 1961); Greece-Neolithic to Helladic from Lerna, assumed equivalent to recent-(Gejvall, 1969) ; and for England, Germany and Finland (Kurt&, 1965).
The prehistoric sites from which fossil material was examined are shown in Table I. Cultural assignment, unless otherwise stated, follows Bar Yosef (1975), and radiocarbon dates, where available, are from Henry & Servello (1975).
TABLE I ~ _ _ _ _ _ _ _ _ ______~
Date in Years Collection Site Region Culture BP Reference
Geula cave Mount Carmel Mousterian 42,000 Wreschner (1964) HUJ Zool. Dept. Hayonim cave D West Galilee Aurignacian 25-24,000 Bar Yosef (pers. HUJ Zool. Dept.
Ein Gev 1 Sea of Galilee Kebaran 15,750 Stekelis &Bar Yosef HUJ Zool. Dept.
El Wad cave Bl and B2 Mount Carmel Natufian 12-10,300 Bate (1937) BMNH Hayonim terrace West Galilee Natufian 12-10,300 Henry &Davis HUJ Zool. Dept.
Jericho Jordan Valley Pre-Pottery 10,350- Clutton-Brock BMNH
comm.)
(1965)
(1 974)
Neolithic 8000 (1969)
The two osteometric parameters measured were the anteroposterior crown length of the lower carnassial (l .Ml) and the alveolar length of the lower molar tooth row (l.Ml-M3) (see von den Driesch, 1976). These parameters were chosen because isolated carnassials and mandibles, often with missing teeth, are the most frequently found and most easily identifiable elements, and
TABLE I1 Vulpes vulpes, recent and fossif measurements. (n refers to number of specimens, and S.E. to the
standard error of mean)
1.MI-Ms n Mean S.E.
RECENT Israel region
Galilee Mount Carmel and coastal plain Jerusalem area Sinai Dead sea basin H a l w a sands Central and southern Negev Central and southern Negev males Central and southern Negev females Northern Israel Negev and Sinai
Israel males Israel females Algeria Tunisia Cairo area Saudi Arabia, males and females Saudi Arabia, males Saudi Arabia, females Muscat & Oman Mesopotamia males and females Mesopotamia, males Mesopotamia, females Baluchistan Thar Parker, Sind males and females Thar Parker, Sind males Thar Parker, Sind females Himalayan foothills, males and females Himalayan foothills, males Himalayan foothills, females Himalayas Finland (Kurten, 1965) Germany (Kurten, 1965) England (Kurten, 1965) Holland, males and females (Hooijer, 1961) Holland, males (Hooijer, 1961) Holland, females (Hooijer, 1961) Northern Anatolia, Kizilcahaman Southern Anatolia, Karaman Greece, Lerna : Neolithic-Helladic
Cyprus Euphrates valley, northern Syria
FOSSIL Jericho Pre-Pottery Neolithic Hayonim terrace Natufian El Wad B1 and B2 Natufian Ein Gev 1 Kebaran Hayonim cave late Aurignacian Geula cave Mousterian Ksar Akil Lebanon “Main Wurm”
also because museum collections generally consist of skulls only. In the fossil material at hand long bones were so crushed that their lengths could not be measured.
Carnivores are characterized by relatively low crowned teeth, so that changes of crown length due to continual crown eruption or inter-dental abrasion, as in the artiodactyls (Grigson, 1974), do not occur, and the length of the crown remains constant throughout life. Fox lower molar
346 S . DAVIS
teeth, unlike the pre-molars, have no inter-dental spaces, so that age-dependant reduction of the length of the molar tooth row must be minimal.
For the recent material sex data are included where available, enabling an analysis of sexual dimorphism to be made for some areas (see Table I1 and Fig. 1). Fossil mandibles and teeth cannot be sexed, so that the material was generally lumped.
In Israel data were grouped according to local climatic regions, such as Galilee, the coastal
I M1-M3 ( m m )
N N N N N N w D Ln m
L M I (mm) - - - - -
N w P Ln m 1 I I
-% Hol land
-to
-9 - - - + - - - T h a r P a r k e r , Sind +to
- - - + - - - $0
FIG. I . Vulpes vulpes, recent. Plots of 1. MI-M, (broken lines), and I . M, (solid lines) showing the degree of sexual dimorphism. Measurements are in millemetres, graphics show meanh95 % confidence limits calculated from pooled standard deviation. (Bartlett’s test showed variances were homogenous (Sokal & Rohlf, 1969)).
plain, the Jerusalem hills, the Dead Sea basin, the Haluzza sands of the northern Negev and the Negev itself; outside Israel this was done according to geopolitical location.
To correlate size with temperature for foxes from different parts of the world, mean tempera- tures for the coldest month, January, and the hottest month, usually July or August, were taken from World Weather Records (1951-60).
SIZE VARIATION OF THE FOX 347
Analysis of variance was performed on Israeli samples, and temporally adjacent samples compared by use of the Student’s t test.
II
10.
Results Within Israel there are no significant differences (Analysis of variance at the 1 % level)
between the foxes of the different climatic regions. Specimens from the arid Negev are similar to those from the coastal plain, from cooler Jerusalem and from Galilee (Table 11).
Outside Israel there is little change in size throughout the Saharo-Arabian region, but moving northwards, an increase in size is encountered, which begins on ascending the Anatolian plateau, characterized by its greater altitude and lower mean temperature. A
- y = 44. 19 -0.107~ r = - 0 . 7 5
-5 0 5 10 15 20 o c
15
2 14 E
2 - 12
- - 13
I ’ .
A D
y - 5 0 . 1 3 - 0 . 1 2 O X r = - 0 . 8 0
15 2 0 25 3 0 3 5 40 OC
~ H J
L
I ?
K M
+R
34s S . DAVIS
I A B C D E F I
t 1
5 0 40 30 2 0 10 0 T i m e before present x lo3 years
FIG. 3. Vulpes vulpes, fossil specimens from Israel. Plot of 1. M,-M, (b) and 1. M, (c) against time, alongside the delta 180 graph (a) from the Greenland ice sheet (Dansgaard, Johnson et a/., 1969). Fox measurements are in millemetres, and graphics represent mean+95% confidence limits, for sample sizes see Table 11.
Sites: A, Geula cave, Mousterian; B, Hayonim cave, late Aurignacian; C, Ein Gev 1, Kebaran; D, El Wad cave B1 and €32 levels, Natufian; E, Hayonim terrace, Natufian; F, Jericho tell, pre-pottery Neolithic; I, Israel recent.
SIZE VARIATION OF THE FOX 349
further size increase is observed between foxes of England, Germany and Holland and those of Finland. Also eastwards, in the western Indian region, a clinal size increase can be observed: from the Thar desert of Sind (smallest) to the Baluchistan mountains and the Himalayan foothills of N.E. Punjab and to those from Tibet (largest). These size changes show a significant (Pt0.001) correlation with both mean January and July-August temperatures (Fig. 2). The correlation coefficients are -0.75 and -0.80 respectively.
Analysis of variance of fossil Israeli samples revealed a significant overall size change, (P<0.005) for length of M,-M, and P<O-OOl for length of M,). Recent males versus Ein Gev 1 and El Wad were significantly different (Student’s t test, Pt0.001), and so were Hayonim terrace and recent males (length of M, only). El Wad differs from Jericho pre- pottery Neolithic (l.Ml-M3 only; P<O.Ol). Figure 3 suggests a gradual size increase attaining a maximum about 15,000 years ago. Dwarfing commenced within the Natufian (10-1 1,000 years ago) and was completed by the pre-pottery Neolithic (about 9000 years ago), by which time the sizes were equivalent to recent Israeli specimens. This gradual increase followed by a sudden decrease closely agrees with KurtCn’s (1965) results. How- ever a more accurate location of the diminution can now be proposed. It is worth noting that the “Main Wurm” foxes from Ksar Akil, Lebanon, are larger than recent Israeli specimens, (Hooijer, 1961) again agreeing with the results presented here.
Discussion The problem is which of the two factors, temperature or character displacement affects
fox size both in the modern and the fossil Israeli samples. Whilst Kurtkn (1957, 1973) demonstrated correlation between latitude and body size in certain carnivores, Rosenzweig (1966, 1968) found that in addition to latitude and temperature, predator-predator competition was an important size determinant. According to McNab (1971) Bergmann’s effect in American carnivores is the exception rather than the rule.
In Israel the canid closest in size to the fox (apart from the Sand fox V. ruppelli which is limited to desert extremes) is the Asiatic jackal Canis aureus. If character displacement between fox and jackal does exist, one would expect some size change within the distribu- tion area of the fox to coincide with the jackal’s distribution: for example the observed differences between Israeli and Anatolian foxes (a similar differential is observed between Israeli and Turkish wolves) would have to be due to the presence of jackals in Israel and their absence from Anatolia. This is not the case, however, for jackals are reported from Anatolia (Kumerloeve, 1967; Harrison, 1968; Mendelssohn, pers. comm.) as well as Israel. In Europe, the jackal is limited to the Balkans, Romania and Hungary, and its distribution does not coincide with a size change of the fox; foxes from Germany, Holland and England being similar to those of Anatolia. Similarly some other factor must be responsible for the large size of the Finnish fox. Clinal size changes of the fox in southern Asia (Table 11) all occur within the jackal’s range of distribution (Ellerman & Morrison- Scott, 1966).
Within Israel, in spite of the variety of climatic and topographic regimes, no size variation is to be found, presumably due to the smallness of the area, so that Israeli foxes can be treated as a single population with respect to size,
Turning now from the recent to the Pleistocene, the most convincing evidence for some kind of extraneous factor is that other Israeli mammals such as Crocuta crocuta, Felis
350 S . DAVIS
silvestris and Canis lupus (KurtCn, 1965); Spalax ehrenbergi (Tchernov, 1968) and Gazella gazella (Davis, in prep.) all show significant dwarfing at the end of the Pleistocene. (In the gazelle this occurs within the Natufian.)
Evidence for a temperature increase at the end of the Pleistocene in Europe and north America is considerable (Butzer, 1971). Estimates for the Near East vary between 2-5" and 15"C, with most ranging between 5.0" and 7-0"C (Farrand, 1971 ; Gvirtzman, 1975). Dansgaard, Johnson et al. (1969) plotted delta Oxygen 18 isotope fluctuations in the Greenland ice sheet throughout the upper Pleistocene and Holocene, and these show some correlation with the fox changes (Fig. 3). Utilizing the fox data presented here, a specula- tive estimate of the Pleistocene-Holocene temperature change might be interpolated from Fig. 2, in which a 1 mrn diminution of the length of the lower carnassial is correlated with a temperature change of 8-9°C. Since fossil Israeli foxes show a 1 mm change in the length of M, from the Kebaran to the pre-pottery Neolithic periods, I suggest an 8-9°C tempera- ture elevation in Israel for that time period, i.e. around 11-12,OOO years ago.
Summary Fox mandible measurements from different parts of Israel showed that within this
region no significant size change could be observed. However, considering a wide geo- graphic range encompassing Europe, north Africa, the Middle East and N.W. India, fox size was found to decrease in correlation with mean January and July-August tempera- tures (r =-0-75 and 4 . 8 0 respectively).
The possibility that size change is due to character displacement by the jackal is con- sidered unlikely, since size changes of the fox are clinal and do not coincide with the jackal's distribution.
Fossil fox mandibles were examined from a series of prehistoric sites from the upper Pleistocene and Holocene in Israel. The fox increased in size, attaining a maximum towards the end of the Pleistocene, and dwarfing took place during or after the Natufian period, that is, at the end of the Pleistocene, as has been reported for several other mammals from this area. The order of magnitude of this dwarfing was observed to be equivalent to that correlated with a temperature change of 8-9°C in recent foxes, and a similar temperature change has therefore been suggested for the Pleistocene-Holocene boundary.
I owe my thanks to Prof. G. Haas, Prof. E. Tchernov, Dr Y . Heller, Dr U. Safriel and Prof. 0. Bar Yosef for their constructive criticism of this manuscript and for their encouragement. I thank S . Payne, J. Clutton-Brock, D. Harrison, F. Petter, F. Poplin and G. Heidemann for their hospitality while on a recent study tour of Turkish and European collections.
REFERENCES Bar Yosef, 0. (1975). The epipalaeolithic in Palestine and Sinai. In Problems in prehistory: North Africa and the
Bate, D. M. A. (1937). Palaeontology: the fossil fauna of the Wady el-Mughara caves. In The Stone Age of Mount
Brown, W. L. & Wilson, E. 0. (1956). Character displacement. Syst. Zool. 5: 49-64. Butzer, K. W. (1971). Environment and archaeology, an ecological approach to prehistory. 2nd ed. London : Methuen. Clutton-Brock, J. (1969). Carnivore remains from the excavations of the Jericho tell. In The domestication and
exploitation ofplants and animals: 337-345. Ucko, P. J. & Dimbleby, G. W. (Eds).London: G. Duckworth.
Levant: 363-378. Wendorf, F. & Marks, A. E. (Eds). Dallas: SMU Press.
Carmel Part 2: 137-240. Garrod, D. A. E. & Bate, D. M. A. (Eds). Oxford: Clarendon Press.
SIZE VARIATION O F T H E FOX 351
Dansgaard, W., Johnson, S. J., Msller, J. & Langway, C. C. (1969). One thousand centuries of climatic record
Driesch, A. von den (1976). Das vermessen von tierknochen aus vorund Friihgeschichtlichen siedlungen. Munich:
Ellerman, J. R. & Morrison-Scott, T. C. S. (1966). Check list of Palaearctic and Indian Mammals 1758-1946.
Farrand, W. R. (1971). Late Quaternary palaeoclirnates of the eastern Mediterranean area. In The late Cenozoic
Gejvall, N. G . (1969). Lerna I. The fauna. New Jersey: Athens & Princeton. Grigson, C. (1974). The craniology and relationships of four species of BOS. J. archaeol. Sci. 1: 353-379. Gvirtzman, G. (1975). Glacial features on Mt Herrnon and in Sinai and their bearing on the climate in the Levant
Harrison, D. L. (1968). The mammals of Arabia, 2. London: Ernest Benn. Henry, D. & Davis, S. (1974). The 1974 excavation of Hayonim terrace. A brief report. Paliorienf 2: 195-197. Henry, D. & Servello, F. (1975). A compendium of radiocarbon determinations derived from Near Eastern pre-
Hooijer, D. A. (1961). Fossil vertebrates of Ksar Akil, a Palaeolithic rock shelter in the Lebanon. Zool. Verh.,
Kumerloeve, H. (1967). Zur verbreitung Kleinasiatischer Raub- und Huftiere sowie einiger Grossnager. Saugetierk.
Kurtin, B. (1957). The bears and hyaenas of the interglacials. Quaternaria 4: 69-81. KurtCn, B. (1965). The carnivora of the Palestine caves. Acfa zool. fenn. 107: 1-74. KurtCn, B. (1973). Geographic variation in size in the Puma (Felis concolor). Commentat. biol. 63: 1-8. Mayr, E. (1963). Animal species and evolution. Cambridge, Mass. : Harvard University Press. McNab, B. (1971). On the ecological significance of Bergmann's rule. Ecology 52: 845-854. Rensch, B. (1959). Evolution above the species level. New York: Columbia University Press. Rosenzweig, M. L. (1966). Community structure in sympatric Carnivora. J. Mammal. 47: 602-612. Rosenzweig, M. L. (1968). The strategy of body size in mammalian carnivores. Am. Midl. Nut. 80: 299-315. Sokal, R. R. & Rohlf, F. J. (1969). Biometry, the principles and practise of statistics in biological research. San
Francisco: W. H. Freeman & Co. Stekelis, M. & Bar Yosef, 0. (1965). Un habitat du PalColithique supbieur a Ein Giiev, Israel. Note prkliminaire.
L' Anthropologie 69 : 176-1 83. Tchernov, E. (1968). Succession of rodent faunas during the upper pleistocene of Israel. Hamburg & Berlin: Paul
Parey. U.S. Department of Commerce, Environmental Science services Admin. World Weather Records, 1951-60.
Washington D.C. 2, Europe, (1966); 4, Asia, (1967); 5, Africa, (1967). Wreschner, E. (1964). Geulah cave, Haifa. Israel Explor. J. 14: 277-278.
from Camp Century on the Greenland Ice Sheet. Science, N. Y. 166: 377-381.
Institut fur Palaoanatomie. Universitat Miinchen.
London: British Museum (Natural History).
glacial ages: 529-564. Turekian, K. (Ed.) Yale: University Press.
during the last Glacial. (In Hebrew, English summary). Mitekufat Haeven 13: 8-20.
