Body sizes of carnivores commensal with humans have increased over the past 50 years

Authors


†Author to whom correspondence should be addressed. E-mail: yomtov@post.tau.ac.il

Summary

  • 1Improved nutrition may cause an increase in body size in animals, while increased ambient temperature may result in a decrease in body size, as expected from Bergmann's rule. In Israel, during the last 50 years both food availability for animals commensal with humans and ambient temperature have increased.
  • 2Using museum data, temporal changes in body size of five species of carnivorous mammals commensal with humans were examined.
  • 3An increase in body length was found in four species, and appears to be related to improved nutrition owing to a substantial increase in the amount of garbage and agricultural crops available to commensal mammals that has occurred since the establishment of the State of Israel in 1948.
  • 4The larger species were more affected than the smaller ones, apparently because of their higher position in the feeding hierarchy or because of having larger home ranges.
  • 5The increases are convergent with the increase in human body height observed during the past two centuries.
  • 6These changes illustrate the fast rate of animal response to changing environmental conditions.

Introduction

Temporal and spatial intraspecific variation in adult body size may be related to several factors, including nutrition and ambient temperature. Body size appears to be a function of how much time growing individuals have unhindered access to food of the highest quality (Geist 1987). Conditions experienced during early development affect growth and ultimately body size, and a range of related properties, including metabolism, survival and reproductive performance in many birds and mammals (Henry & Ulijaszek 1996; Lindstrom 1999). This is exemplified by the observations that during the last two centuries body height and weight in human populations have increased significantly (secular trend), predominantly in European and European origin populations (Ulijaszek et al. 1998). The prime determinants of this trend are considered to be improved nutrition and availability of public health services (Ulijaszek et al. 1998). Similar phenomena have been observed in animals. For example, in Harbour Porpoises (Phocoena phocoena G. Cuvier) increased prey availability (presumably due to hunting pressure and a decrease in population density) resulted in an increase in body length of calves and earlier sexual maturity of females (Read & Gaskin 1990).

Bergmann's rule is probably the best-known rule in zoogeography. It states that ‘In warm blooded animals, races from warm regions are smaller than races from cold regions’ (Mayr 1970). Bergmann's rule was interpreted as an adaptation to ambient temperature: the relatively larger body surface areas of the smaller races serve as efficient heat dissipators in warm climates, while relatively small body surface area of larger races may help in heat conservation in cold climates. Global mean surface temperatures have increased by 0·6 °C since the late nineteenth century (Intergovernmental Panel on Climate Change 1995). Recently it has been claimed that global warming has affected body size in several species of passerine birds (Yom-Tov 2001) and a rodent (Smith, Browning & Shepherd 1998). Although neither of these studies represents a controlled experiment, these trends are explained most parsimoniously by a correlation with recent climatic change (Hughes 2000).

Weight change in homoeothermic animals can occur rather rapidly, as reported for animals introduced into new environments. For example, within 100 years of its introduction into North America and New Zealand, the body size of the House Sparrow Passer domesticus correlated positively with seasonality and annual temperature range in both regions (Selander & Johnston 1967; Johnston & Selander 1971; Baker 1980; Lowther & Cink 1992). Similarly, within 50 years of its introduction into New Zealand, the body size of the Brushtail Possum Trichosurus vulpecula Lesson correlated with ambient temperature (Yom-Tov, Green & Coleman 1986) as it does in Australia from where it was introduced.

Sixteen species of wild mammalian predators presently occur in Israel, ranging in size from the 32 kg Striped Hyaena (Hyaena hyaena L.) to the 0·3 kg Marbled Polecat (Vormela peregusna Guldenstaedt) (Mendelssohn & Yom-Tov 1999). Five of these species (the Striped Hyaena, the Wolf Canis lupus L., the Golden Jackal Canis aureus L., the Red Fox Vulpes vulpes L. and the European Badger Meles meles L.) are commensal with humans, taking advantage of the large quantities of garbage that are not disposed of responsibly (or legally), road kills and agricultural crops and pests that thrive on these crops. Another anthropogenic food source is the carcasses of cattle, hens and turkeys that farmers dispose of in the many illegal garbage dumps that are common near agricultural settlements. Yom-Tov, Ashkenazi & Viner (1995) estimated that the total quantity of meat that farmers disposed of during 1993 in the Golan Heights alone was 1208 tonnes, composed of 42% turkeys, 32% cattle and 19% hens. Jackals and wolves also prey on calves (mainly jackals; Yom-Tov, Ashkenazi & Viner 1995), and wolves prey on cattle, mainly in the Golan Heights. The above food sources have enabled populations of commensal predators to increase appreciably during the last three decades.

Body size may decrease owing to global warming, as predicted by Bergmann's rule, or increase owing to anthropogenetic changes that increase food availability. The aim of this work was to examine whether the body size of five species of carnivores commensal with humans has undergone change during the second half of the twentieth century.

Methods

The Zoological Museum of Tel Aviv University (ZMTAU) hosts a collection of mammalian specimens from which I selected adult specimens of five species of common carnivores of which more than 60 specimens were collected throughout the second half of the 20th century: Wolf, Golden Jackal, Red Fox, European Badger and Striped Hyaena. Specimens were randomly collected for the museum at various times of the year throughout Israel, mostly from road kills and some shot by rangers of the Nature Reserve Authority of Israel as agricultural pests. At the university the taxidermists weighed these specimens to an accuracy of 10 g, and their body (snout to anus), tail (anus to end of tail), hind foot length and ear length were measured to an accuracy of 1 mm. Skulls that were not smashed were cleaned and preserved. Greatest skull length (GTL) was measured with callipers to an accuracy of 0·1 mm.

The museum also possesses specimens of carnivore species that are not commensal with humans. However, the number of specimens of such species is much smaller than those of commensal species, probably because commensal species are more abundant than others, and are more likely to be killed on roads or shot by rangers. Two non-commensal carnivores, the Caracal Caracal caracal Schreber and the Jungle Cat Felis chaus Guldenstaedt, are represented in the ZMTAU by about 40 specimens, and were included in the study.

Since males of the studied species are larger than females, and body size of some Israeli mammals is positively affected by latitude (as predicted by Bergmann's rule) as well as by month of collection (Mendelssohn & Yom-Tov 1999), all tests were carried out on the residuals of the measurements controlled for sex, latitude and month of collection. Multiple regressions were performed of body measurements vs. sex (dummy variable), latitude and month of collection and the residuals were calculated simultaneously. These residuals were run in simple regression models, with year as independent variable and residuals as dependent ones.

In order to test if body size increased in relation to ambient temperature, the above residuals were also run in simple regressions with mean minimum spring (April–June) temperature of the year of collection as independent variable. The reason for choosing mean minimum spring (April–June) temperature is that the main increase in ambient temperature during the last 50 years in Israel was in spring, with temperatures shown to increase by an average of 0·25 °C per decade (Ben-Gai et al. 1999).

Results and discussion

Year of collection was significantly and linearly related to residual body length of the Wolf, Golden Jackal, Striped Hyaena and European Badger, but not of the Red Fox (Fig. 1). Tail length, ear length and hind foot length, and GTL were not significantly correlated with year of collection in any of the species examined. None of the body measurements was significantly related to mean minimum spring (April–June) temperature of the year of collection. No significant relationships between body measurements (dependent variables) and year of collection or ambient temperature (independent variables) were found in the two non-commensal species (Caracal and Jungle Cat).

Figure 1.

The relationship between body length (in mm, controlled for sex, month of collection and latitude) and year of collection (50 = 1950, 100 = 2000) in the (a) Striped Hyaena (n = 38, r2 = 0·176, P = 0·0088; Y = −277·57 + 3·532 * year); (b) Wolf (n = 43, r2 = 0·160, P = 0·0079; Y = −247·39 + 3·123 * year); (c) Golden Jackal (n = 54, r2 = 0·094, P = 0·0241; Y = −115·78 + 1·599 * year); and (d) European Badger (n = 109, r2 = 0·061, P = 0·0094; Y = −0·15 + 0·002 * year). For the fox (not presented in the figure) n = 47, r2 = 0·002, P = 0·7416; Y = 9·74 − 0·131 * year.

The increases in body length in relation to year of collection appear to be related to improved nutrition, while ambient temperatures do not appear to affect it. This conclusion is supported by the fact that the two species of non-commensal carnivores examined did not increase in body size during the studied period. The amount of human-made food available for commensal carnivores in Israel increased considerably during the second half of the twentieth century. The number of settlements increased by 2·2-fold, and many small settlements and army camps have their own garbage dumps, where garbage is discarded without any further treatment. The human population has increased linearly by 7·7-fold and its living standard has increased by about 10-fold. The number of cattle, sheep and goats, hens and turkeys has increased linearly by 1·7, 1·8, 1·3 and 6·0-fold, respectively (Statistical Abstracts of Israel 1950–2000). Carcasses of livestock are commonly discarded (illegally) near many agricultural settlements, and are available to wild animals (Yom-Tov et al. 1995). The total cultivated area increased linearly by 2·6-fold until 1970 when it stabilized, while the total irrigated area increased linearly by 4·1-fold until stabilizing in 1980 (Statistical Abstracts of Israel 1950–2000). The irrigated areas have declined since 1992 by about 10% owing to shortage of water. All the studied carnivores apart from the badger feed at garbage dumps that are common near almost every settlement, while the badger, the fox and the jackal are omnivorous and often forage in and near agricultural fields, where they consume vegetables and their rodent and insect pests. All five species also feed on road kills.

Year of collection explained 0·2%, 6·1%, 9·4%, 16·0% and 17·6% of the variation in residual body length in the fox, badger, jackal, wolf and hyaena, respectively, and r2 values were significantly related to mean body length and weight of these species (for body length: n = 5, r2 = 0·972, P = 0·002; for body weight: n = 5, r2 = 0·858, P = 0·0238; Fig. 2). Similarly, the slopes of the regressions of body length and weight on year of collection are also positively related (for body length: n = 5, r2 = 0·911, P = 0·0115; for body weight: n = 5, r2 = 0·843, P = 0·0277). These relationships indicate that the larger the species, the more capable it is of exploiting the extra food provided by humans. This food generally comprises items large enough to be exploited by any of the studied species, but the larger species appear to have better access to it due to their larger body size and higher position in the food hierarchy. In garbage dumps and carnivore feeding stations there is a clear hierarchy, where larger species displace the smaller one (Y. Yom-Tov, personal observation). Another possible explanation for the relationship between body size and r2 values is the positive relationship between home range and body size. Larger species tend to have larger ranges, and are capable of exploiting more food sources than smaller ones. If these explanations are correct, they clarify why the relationship between year and residual body length was not significant in the smallest species, the Red Fox.

Figure 2.

The relationships between r2 values of residual body length and year of collection and body mass (a) and length (b) of the five species studied. For body length: n = 5, r2 = 0·972, P = 0·002; for body mass: n = 5, r2 = 0·858, P = 0·0238.

Among humans, secular trends in body height are generally associated with increase in body weight. In this study, a significant linear increase in residual body weight in relation to the year of collection was observed for the jackal and the badger until the 1990s, and no further increase was observed later (jackal: n = 40, r2 = 0·240, P = 0·0013; badger: n = 32, r2 = 0·174, P = 0·0177). No increase in residual body weight was observed in the other three species. The absence of such a trend in three species may be explained by the large variation in this parameter. Weight in wild animals fluctuates more than other body measurements, as it is affected by daily availability of food, and times of urination and defecation. In fact, in all five species studied the coefficient of variation of body weight was 2–2·3 times greater than that of body length, and 3·2–5·5 times greater than that of GTL. Hence, the chances of finding an increase in body weight are small.

The temporal trend in body weight in the jackal and the badger may be explained by the recent history of carnivore populations in Israel. In 1964 the Plant Protection Department (Ministry of Agriculture) carried out an extensive poisoning campaign against the Golden Jackal, which was blamed for the heavy damage caused to the plastic sheeting used to cover certain crops (Yom-Tov & Mendelssohn 1988). Tens of thousands of chick carcasses injected with fluoracetamid were distributed throughout the Mediterranean area of Israel, resulting in massive mortality among jackals as well as among other carnivores. However, within 20 years the populations of these species recovered to their former levels (Yom-Tov & Mendelssohn 1988). The jackals and badgers, whose diet is partly composed of vegetables and other crops, appear to have been more affected by the poisoning than the other three species. Moreover, individuals surviving after the poisoning campaign benefited from relative low population density and the resulting lack of competition from conspecifics until populations recovered in the 1980s. Like the other commensals they too benefited from the linear increase in food at garbage dumps and from livestock carcasses, but also from the increase in cultivated, and particularly irrigated, areas which increased linearly until the 1970s and 1980s, respectively, and then stabilized. It would thus appear that the increase in agricultural areas and the food associated with them enabled the increase in body length as well as in weight. As there was no further significant increase in cultivated areas after 1980, populations stabilized and competition became stronger, resulting in no further increase in body weight.

Acknowledgements

I am grateful to Arieh Landsman, and Tsila Shariv for their technical help, to Naomi Paz for editorial assistance and to Tamar Dayan, Eli Geffen, Avraham Hefetz and Johnathan Wright and two anonymous referees for advice and comments.

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