VARIATION IN INCIDENCE OF MALE INFANTICIDE WITHIN ... - BioOne

Journal of Mammalogy, 87(1):35–40, 2006

VARIATION IN INCIDENCE OF MALE INFANTICIDE WITHIN SUBSPECIES OF PLAINS ZEBRA (EQUUS BURCHELLI) JAN PLUHAĆˇEK,* LUDEˇK BARTOSˇ,

AND JITKA

VICHOVA´

Ethology Group, Research Institute of Animal Production, Prague, P.O. Box 1, CZ-104 01 Praha 10-Uhrˇ´ıneˇves, Czech Republic (JP, LB, JV) Department of Zoology, Faculty of Science, Charles University, Vinicˇna´ 7, Praha 2, CZ-128 44, Czech Republic (JP)

Social organization seems to determine the occurrence of male infanticide in equids. Although, no information concerning social organization of the maneless zebra (Equus burchelli borensis) has been available, we presumed that the occurrence of infanticide would be the same across all subspecies of plains zebra. We examined the occurrence of this phenomenon in 9 herds of 4 subspecies: the maneless zebra, Grant’s zebra (E. burchelli boehmi), Chapmann’s zebra (E. b. chapmanni), and the Damara zebra (E. b. antiquorum) at 4 zoos. The probability of a foal’s death was affected by the presence of a new male and subspecies. Except for the maneless zebra, all subspecies showed existence of male infanticide. We found no occurrence of male infanticide in maneless zebras, which suggests a different social system. This would also support the subspecific status of the maneless zebra. Key words:

Equus burchelli, infanticide, infant mortality, maneless zebra, subspecies, zoo

over time, but the group male may be displaced by another male (Klingel 1974a, 1978). The group male sires all progeny (Rubenstein 1986). When a male in the harem is changed, the infanticide of dependent foals by the new male should be an advantageous reproductive strategy for him, because the mares will invest only in his own offspring (Pluhaćˇek and Bartosˇ 2000, 2005). In type II social organization, the only stable group is a female and her offspring (Klingel 1974b, 1977; Rubenstein 1986, 1993). No permanent bonds are maintained among adult individuals. Some of the males are territorial, maintaining their territories for years. Mating occurs mostly within these territories (Rubenstein 1986). Territorial males tolerate conspecifics of both sexes except other males during the time when females in estrus are present (Ginsberg and Rubenstein 1990; Klingel 1974b). So far as we know, infanticide has not been reported within these territorial equid species (Ebensperger 1998; van Schaik and Janson 2000). Free-ranging plains zebras form social organizations of type I (Klingel 1974a, 1978; Rubenstein 1986). Their social organization and social behavior are similar in all areas where they have been observed (Kenya, Tanzania, and Rwanda in eastern Africa; Malawi, Republic of South Africa, and Namibia in southern and southwestern Africa—Hack et al. 2002; Klingel 1969; Monfort and Monfort 1978). In Dutch and Australian zoos, captive plains zebra kept in large enclosures with many adults of both sexes showed the same social organization as

Male infanticide is defined as the killing of dependent young by an adult male of the same species. This phenomenon has been described in a few ungulate species such as red deer (Cervus elaphus—Bartosˇ and Madlafousek 1994), hippopotamus (Hippopotamus amphibius—Lewison 1998), Indian rhinoceros (Rhinoceros unicornis—Dinerstein et al. 1988), and in several equid species including feral horse (Equus caballus— Duncan 1982), Przewalski horse (E. przewalskii—Ryder and Massena 1988; Zharkikh 1999), and plains zebra (E. burchelli— Pluhaćˇek and Bartosˇ 2000, 2005). The occurrence of male infanticide in equids seems to be determined by the social organization of the species (Duncan 1982; Pluhaćˇek and Bartosˇ 2000; Rubenstein 1986). Freeranging equids exhibit 2 basic types of social organization and mating system (Klingel 1974a, 1978; Linklater 2000; Rubenstein 1986). Type I social organization is characterized by longterm, stable, nonterritorial groups composed of 1 or more adult males and 1 or more adult females and their offspring. Other males (in the case of mountain zebra [E. zebra], also subadult females) live in separate groups, referred to as a bachelor group. The adult females form a stable group and remain cohesive

* Correspondent: [email protected]

Ó 2006 American Society of Mammalogists www.mammalogy.org 35

36

Vol. 87, No. 1

JOURNAL OF MAMMALOGY

TABLE 1.—Environmental and social conditions of the 9 herds kept at 4 zoos in the Czech Republic where new male introductions took place. Subspecies

Zoo

Enclosure size (m2)

No. new males

Age of new males (years)

No. adult females

Age of females (years)

Age of foals (days)

Maneless zebraa Maneless zebra Maneless zebra Grant’s zebraa Chapmann’s zebra Chapmann’s zebra Chapmann’s zebra Damara zebra Damara zebra

Dvu˚r Kra´love´ Lesˇna´-Zlıń Lesˇna´-Zlıń Dvu˚r Kra´love´ Dvu˚r Kra´love´ Liberec Liberec Dvu˚r Kra´love´ Prague

1,350 400 2,200 800 1,750 1,695 1,425 360 (winter), 16,600 (summer) 1,400

4 2b 4b 2 1 3c 1c 4 4

415 410 314 416 4 413 9 510 48

17 23 2 56 4 34 4 15 24

214 612 313 315 67 223 415 524 217

199 1115 1204 1254 155 1164 1 1158 156

a b c

Managed by the same person over the entire breeding history. Two males were alternatively introduced into both herds. Total number of individual new males at Lesˇna´-Zlıń Zoo was 4. The same male was introduced alternatively into 2 herds. Total number of individual new males at Liberec Zoo was 3.

observed in the wild (Ford and Stroud 1993; Klingel 1969; Schilder 1992). Plains zebras form harems consisting of 1 adult male and 1–6 adult females. Within the range of the plains zebra, harem sizes tend to increase from south to north (Hack et al. 2002; Klingel 1969; Monfort and Monfort 1978; Neuhaus and Ruckstuhl 2002; Smuts 1976a, 1976b). Nevertheless, the social life of the northernmost subspecies, the maneless zebra (Equus burchelli borensis), is still unknown (for a review, see Hack et al. 2002). We presume that the mortality of foals of captive plains zebras will be higher in the presence of a new male than in his absence. If the social organization of all the subspecies is identical, then the occurrence of infanticide also would not differ among the subspecies, including the maneless zebra.

MATERIALS AND METHODS We collected data on zebras in 4 zoological gardens in the Czech Republic: Dvu˚r Kra´love´ nad Labem, Liberec, Lesˇna´-Zlıń, and Prague. Nine herds of 4 subspecies of plains zebra were available: Grant’s zebra (E. b. boehmi), Chapmann’s zebra (E. b. chapmanni), the Damara zebra (E. b. antiquorum), and the maneless zebra (E. b. borensis; all maneless zebras came from Karamoja region, Uganda). Grant’s zebras were kept only in 1 zoo; 3 other subspecies were kept in at least 2 zoos. Dvu˚r Kra´love´ Zoo keeps all 4 investigated subspecies. Detailed information on the size of enclosures, number and age of adult females, and age of foals at the time of introduction of a new male is given in Table 1. Adult animals included in the analyses were wild caught (6 males and 22 females) and zoo born (28 males and 57 females). Information on the number of generations in captivity was complete for 20 males and 41 females. They did not exceed the 4th captive generation. Almost no vegetation was present in the enclosures but food was available ad libitum and all mares were in good condition. Only the herd of Damara zebras in Dvu˚r Kra´love´ Zoo lived in a very large area, a grassy enclosure .16,000 m2 in which it lived from May to September. A winter enclosure for this herd was 360 m2 in size with no vegetation and with food provided ad libitum. For each foal we recorded date of birth, date of death (if it occurred), identity of dam and sire, subspecies, name of the zoo, and date of introduction of an unrelated stallion (a new male). Any foals injured by a new male that were in need of veterinary treatment and separated from the herd were regarded as dead in the analysis because these foals doubtless

would have died in the wild. The usual weaning age of 9 months (Smuts 1976b) was taken as the criterion for successful survival. The study was approved by the Institutional Animal Care and Use Committee of the Research Institute of Animal Science and was conducted in accordance with Czech Central Committee for Protection of Animals number 13803/2003-1020, and we also followed guidelines of the American Society of Mammalogists for the capture, handling, and care of mammals (Animal Care and Use Committee 1998). We analyzed the data using the SAS System V 9.1 (SAS Institute Inc., Cary, North Carolina). To assess the impact of the presence of a new male on mortality of foals, we applied an analysis of categorical repeated measurements based on the generalized estimating equation approach (Liang and Zeger 1986) using the GENMOD procedure (SAS Institute Inc.). The GENMOD procedure was designed to model the probability of death of the foals. To account for the repeated measures on the same individuals across the period of observation, the analysis was performed with the individual mare and stallion in the REPEATED statement. Explanatory variables were the classes: ‘new male’ (yes or no—new male present ¼ yes, new male absent ¼ no), ‘subspecies’ (Grant’s zebra, Chapmann’s zebra, Damara zebra, maneless zebra), and ‘zoo’ (Dvu˚r Kra´love´ nad Labem, Liberec, Lesˇna´-Zlıń, Prague). Both explanatory variables and interaction terms were tested, but are not reported unless they were statistically significant (P , 0.05). We analyzed only the data sets containing information on a foal’s mortality when a new male was present. We tested the differences in a foal’s mortality among zebra subspecies using Fisher’s exact probability tests. To resolve the multiple testing problem, the Fisher exact tests for 2-group comparisons adjusted by the permutation resampling method were applied (the CONTRAST statement, PROC MULTTEST, SAS Institute Inc.; Westfall et al. 1999).

RESULTS In total, we recorded data from about 394 foals born in all zoos investigated from 1973 to 2000. Almost two-thirds (259) of all foals were born at the Dvu˚r Kra´love´ Zoo and 65, 41, and 29 at the Liberec, Lesˇna´-Zlıń, and Prague zoos, respectively. The largest number of foals (129) was recorded for maneless zebras and .50 foals were recorded for each of the other subspecies. A new male was present in 89 cases. Ninety-six foals died within 9 months of birth and 30 of them during the presence of a new male in a herd.

February 2006

´ CˇEK ET AL.—INFANTICIDE IN PLAINS ZEBRA SUBSPECIES PLUHA

We did not find any case of male infanticide in maneless zebras, despite their having living conditions comparable to other herds. We recorded 3 or more infanticidal attacks in each of the other subspecies (Grant’s, Chapmann’s, and Damara zebras; Table 2). At least 1 infanticidal attack occurred in each zoo keeping these subspecies (Dvu˚r Kra´love´, Prague, and Liberec). The final logistic regression model fitting the probability of foal’s death contained the statistically significant effects of the class ‘new male’ (v2 ¼ 7.35, d.f. ¼ 1, P , 0.01) and the interaction between the ‘new male’ and ‘subspecies’ (v2 ¼ 12.67, d.f. ¼ 3, P , 0.01). None of the remaining factors, that is, subspecies and zoo, or interaction terms had any significant effect on the probability of mortality of foals. A higher probability of death of the foal was predicted when a new male was present than when he was absent (0.34 compared to 0.22). A significant interaction of new male and subspecies revealed that this relationship was valid in all tested subspecies except the maneless zebra, which showed the opposite. Next we analyzed only cases of mortality in situations where a new male was present. We divided all born foals into 2 groups. The 1st group included foals that died because of confirmed attacks by a new male and the 2nd group involved all other foals. The model revealed a statistically significant interaction between the number of foals attacked by a new male and subspecies (v2 ¼ 9.34, d.f. ¼ 3, P , 0.05). Although maneless zebras significantly differed from all other subspecies in number of foals attacked by a new male, no other difference was found (Fisher’s exact test, P-values adjusted for multiple comparisons by the permutation method, maneless versus Grant’s, v2 ¼ 6.63, d.f. ¼ 1, P , 0.05; maneless versus Chapmann’s, v2 ¼ 7.12, d.f. ¼ 1, P , 0.01; maneless versus Damara, v2 ¼ 10.49, d.f. ¼ 1, P , 0.01; maneless versus all others, v2 ¼ 8.55; d.f. ¼ 1; P , 0.01; Table 2).

DISCUSSION In contrast to our prediction, we found that subspecies of captive plains zebras differed in the incidence of male infanticide. Infanticide occurred in Grant’s, Chapmann’s, and Damara zebra kept in different zoos, but no case was recorded for the maneless zebra, although we analyzed the records of 3 maneless zebra groups kept in 2 different zoos (1 at Dvu˚r Kra´love´ Zoo and 2 at Lesˇna´-Zlıń Zoo). Moreover, we had available more new males and foals present in groups with new males in maneless zebras than in other zebra subspecies (Table 2). Maneless zebra males had a greater opportunity to be infanticidal than did males in other subspecies. Thus, we suggest that captive maneless zebras do not suffer from male infanticide or at least that this phenomenon is rare in captive populations of maneless zebras. Similarly, differences in the presence of male infanticide based on social organization between separate populations and subspecies were reported for wild Hanuman langurs (Semnopithecus entellus—Borries and Koenig 2000; Newton 1988) and for wild blue monkeys (Cercopithecus mitis—Butynski 1982, 1990). The zoo in which the zebras were housed did not affect the occurrence of infanticide. This means that living conditions

37

TABLE 2.—Summary of infanticidal attacks by subspecies (aligned according to their distribution in the wild from north to south) of plains zebra recorded at 4 Czech zoos (19 aborted or stillborn foals were not included in the total number of foals present).

Subspecies Maneless zebra Grant’s zebra Chapmann’s zebra Damara zebra

Total no. foals No. foals present with attacked by Total no. new male a new male new males 30 15 13 12

0 3 3 4

8 2 4 8

No. new males involved in infanticidal attempts 0 2 2 4

probably did not play a role in occurrence of male infanticide in the plains zebra. These results also support the view that male infanticide is probably an evolutionarily stable strategy for males whose genes are involved (van Schaik 2000). Our data are based on infanticide under captive conditions. That is always complicated by the possibility that the observed behavior does not reflect the behavior of wild animals. However, the results of our analyses are strengthened by the fact that some of the animals involved in infanticidal attacks were wild caught (male Damara zebra at Dvu˚r Kra´love´ Zoo; wildcaught adult females were present in herds of Damara zebras at Prague and Dvu˚r Kra´love´ zoos). Still we cannot fully reject the possibility that captive condition affected our results. Social organization is critically important for the incidence of male infanticide in equids (Duncan 1982; Pluhaćˇek and Bartosˇ 2000; Rubenstein 1986). Infanticide could be an advantageous reproductive strategy for males living in a type I social organization after male take over of a harem (Pluhaćˇek and Bartosˇ 2000). Infanticide has been reported for 3 equid species that form this type of social organization, including feral horses (Duncan 1982), captive Przewalski horses (Ryder and Massena 1988; Zharkikh 1999), and captive plains zebras (Pluhaćˇek and Bartosˇ 2000, 2005). It has been suggested that infanticide occurs in mountain zebras (Penzhorn 1985; Pluhaćˇek and Bartosˇ 2000). In contrast, male infanticide should be a disadvantageous reproductive strategy in the Asiatic wild ass (Equus hemionus), the African wild ass (E. africanus), and Grevy’s zebra (E. grevyi), which have type II social organization (Ginsberg 1989; Klingel 1974a, 1977; Moehlman et al. 1998; Rubenstein 1986). For example, social organization of Grevy’s zebras eliminates the possibility of infanticide or feticide in this species. After the 6th year of age, adult males hold territories, maintaining them for up to 7 years (Ginsberg 1989). These territories range in size from 2 to 12 km2 (Ginsberg 1989) and are situated along movement routes of females and near predator-free water sources or near areas of the highest biomass (Rubenstein 1986). Females range 10–15 km per day (Rubenstein 1986). Nonterritorial males copulate with the female only on rare occasions (Ginsberg and Rubenstein 1990; Klingel 1974b). Although all types of territories are visited by the females that wander daily, only those having just borne a foal stop ranging long distances and take up long-term (2- to 3-month) residence with a male, who is not necessarily the father of the foal (Rubenstein

38

Vol. 87, No. 1


1986). When females go to drink, they leave their foals, which are guarded by an adult, usually a territorial male (Becker and Ginsberg 1990). Although the gain associated with exclusive mating access to these females is reduced somewhat because the stallion protects another male’s offspring, infanticide is not favored (Rubenstein 1986). This anti-infanticidal strategy based on social organization is unique among mammals (Agrell et al. 1998; Ebensperger 1998; Hausfater and Hrdy 1984; van Schaik and Janson 2000). In 3 plains zebra subspecies (Grant’s, Chapmann’s, and Damara zebras) in which male infanticide was recorded in captivity, the social organization seems to be the same. As far as we know, the type of social organization in wild maneless zebras has not been described. This lack of existing data on its social organization led us to speculate that the social organization of the maneless zebra could differ from that of other subspecies of plains zebras. The harem size of plains zebras increases slightly from south to north (Hack et al. 2002). Maneless zebras occupy the northernmost parts of the plains zebra distribution (Groves and Bell 2004; Lo¨nnberg 1912; Østerballe 1997; Ziccardi 1959). Harems of maneless zebra might be larger than those of other plains zebras. Thus, for a new male it should be more difficult to attack a new foal within a larger harem. However, a study of the social system of wild maneless zebras is needed to confirm this. Variation of intraspecific social organization based on socioecology has been reported in ungulates such as the hippopotamus, pronghorn (Antilocapra americana), topi (Damaliscus lunatus), southern reedbuck (Redunca arundinum), mountain goat (Oreamnos americanus), and western roe deer (Capreolus capreolus—Lott 1991). In equids, the variation in social organization determined by different environmental conditions has been observed in Asiatic wild asses (Feh et al. 1994; Klingel 1977; Saltz et al. 2000), feral asses (E. asinus—Hoffmann 1983; Rudman 1998; Woodward 1979), and feral horses (Hoffmann 1983; Pacheco and Herrera 1997; Rubenstein 1981, 1986, 1993; but see Linklater 2000). Slight variation in terms of group size determined by resource availability was observed in Grevy’s zebras living under semicaptive conditions (Berger 1988). Thus, social flexibility is common in equids (Rubenstein 1993). The maneless zebra has not been accepted as a valid subspecies in most reviews. Usually, it is believed to belong to Grant’s zebra (Ansell 1971; Cabrera 1936; Duncan 1992; Groves 1974; Østerballe 1999; Rza˛sńicki 1951). The only nonmorphological study of taxonomy of plains zebras based on mitochondrial DNA did not included samples from the maneless zebra (Oakenfull et al. 2000). However, recent taxonomic revision of the plains zebra based on morphology showed that the maneless zebra differs from other zebras in several traits and that it should be a separate subspecies (Groves and Bell 2004), thus supporting suggestions of various authors (Dathe 1968; Dittrich 1966; Lo¨nnberg 1912; Ziccardi 1959). The maneless zebras in our study came from the same region (Karamoja, Uganda) as the samples of maneless zebras used in the morphological study of Groves and Bell (2004). Our behavioral results support the validity of the maneless zebra as a subspecies. If the maneless zebra is considered as a subspecies, then con-

servation efforts should be strengthened, because maneless zebra populations in southern Sudan, north Uganda, and northwestern Kenya are small and their numbers are decreasing (Hack et al. 2002).

ACKNOWLEDGMENTS We dedicate this paper to the memory of the late Ludeˇk J. Dobroruka. He will always be remembered for his dynamism and passion for ethology, conservation, and taxonomy of mammals, which inspired many Czech zoologists. He made various valuable comments on taxonomic aspects in early drafts of this paper. We thank the staff of Zoological Gardens at Dvu˚r Kra´love´, Liberec, Lesˇna´-Zlıń, and Prague for allowing us to analyze their records. Our thanks go to L. Cˇulı´k, D. Holecˇkova´, P. Moucha, I. Ma´slova´, K. Toma´sˇova´, and J. Va´hala of the Dvu˚r Kra´love´ Zoo; L. Melichar, J. Skrˇivańkova´, and D. Nejedlo of the Liberec Zoo; R. Horsky´, and T. Divı´lek of the Lesˇna´ Zoo; and M. Brtnicky´ and Z. Sˇ´ı sˇa of the Prague Zoo, in particular for all their data and suggestions. Our thanks to J. Ka´lnova´, D. Sparandara, T. DeVries, O. Abonyi, R. Kotrba, and J. L. A. Panama´ for their comments and improving the language. S. Lhota’s helpful comments also are acknowledged. The study was supported by grants from the Grant Agency of the Czech Republic (523/03/H076) and from the Ministry of Agriculture of the Czech Republic (MZE 0002701402).

LITERATURE CITED ANIMAL CARE AND USE COMMITTEE. 1998. Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. Journal of Mammalogy 79:1416–1431. AGRELL, J., J. O. WOLFF, AND H. YLONEN. 1998. Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83: 507–517. ANSELL, W. F. H. 1971. Order Perissodactyla. Pp. 1–14 in The mammals of Africa (J. Meester and H. W. Setzer, eds.). Smithsonian Institute Press, Washington, D.C. BARTOSˇ, L., AND J. MADLAFOUSEK. 1994. Infanticide in a seasonal breeder: the case of red deer. Animal Behaviour 47:217–219. BECKER, C. D., AND J. R. GINSBERG. 1990. Mother–infant behaviour of wild Grevy’s zebra: adaptations for survival in semidesert East Africa. Animal Behaviour 40:1111–1118. BERGER, J. 1988. Social systems, resources and phylogenetic inertia: an experimental test and its limitations. Pp. 157–186 in The ecology of social behaviour (C. Slobodchikoff, ed.). Academic Press, London, United Kingdom. BORRIES, C., AND A. KOENIG. 2000. Infanticide in hanuman langurs: social organization, male migration, and weaning age. Pp. 99–122 in Infanticide by males and its implications (C. P. van Schaik and C. H. Janson, eds.). Cambridge, University Press, Cambridge, United Kingdom. BUTYNSKI, T. M. 1982. Harem-male replacement and infanticide in the blue monkey (Cercopithecus mitis stuhlmanni) in the Kibale Forest, Uganda. American Journal of Primatology 3:1–22. BUTYNSKI, T. M. 1990. Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. Ecological Monographs 60:1–26. CABRERA, A. 1936. Subspecific and individual variation in the Burchell zebras. Journal of Mammalogy 17:89–112. DATHE, H. 1968. Zum Vorkommen ma¨hnenloser Zebras. Zoologische Garten 35:67–68.

February 2006

´ CˇEK ET AL.—INFANTICIDE IN PLAINS ZEBRA SUBSPECIES PLUHA

DINERSTEIN, E., C. WEMMER, AND H. MISHRA. 1988. Adoption in greater one-horned rhinoceros (Rhinoceros unicornis). Journal of Mammalogy 69:813–814. DITTRICH, L. 1966. Ma¨hnenlose Zebras in Zoo Hanover. Saügertierkundliche Mitteilungen 14:100–104. DUNCAN, P. 1982. Foal killing by stallion. Applied Animal Ethology 8:567–570. DUNCAN, P. 1992. Zebras, asses and horses. An action plan for the conservation of wild equids. International Union for the Conservation of Nature and Natural Resources (IUCN), Cambridge, United Kingdom. EBENSPERGER, L. A. 1998. Strategies and counterstrategies to infanticide in mammals. Biological Reviews 73:321–346. FEH, C., T. BOLDSUKH, AND C. TOURENQ. 1994. Are family groups in equids a response to cooperative hunting by predators? The case of mongolian kulans (Equus hemionus luteus Matschie). La Terre et la Vie 49:11–20. FORD, J. C., AND P. C. STROUD. 1993. Captive management strategies for natural behaviour of Chapman‘s zebra Equus burchelli chapmani at Werribee Zoological Park. International Zoo Yearbook 32:1–6. GINSBERG, J. R. 1989. The ecology of female behaviour and male reproductive success in the Grevy’s zebra, Equus grevyi. Pp. 89– 110 in Symposia of the Zoological Society of London (P. A. Jewell and G. M. O. Maloiy, eds.). Clarendon Press, Oxford, United Kingdom. GINSBERG, J. R., AND D. I. RUBENSTEIN. 1990. Sperm competition in zebra mating behavior. Behavioral Ecology and Sociobiology 26: 427–434. GROVES, C. P. 1974. Horses, asses and zebras in the wild. David and Charles, London, United Kingdom. GROVES, C. P., AND C. H. BELL. 2004. New investigations on the taxonomy of the zebras genus Equus, subgenus Hippotigris. Mammalian Biology 60:182–197. HACK, M. A., R. EAST, AND D. I. RUBENSTEIN. 2002. Status and action plan for the plains zebra (Equus burchelli). Pp. 43–60 in Status survey and conservation action plan. Equids: zebras, asses and horses (P. D. Moehlman, ed.). International Union for the Conservation of Nature and Natural Resources (IUCN), Gland, Switzerland. HAUSFATER, G., AND S. B. HRDY. 1984. Infanticide: comparative and evolutionary perspectives. Aldine Publishing Company, New York. HOFFMANN, R. 1983. Social organisation patterns of several feral horse and feral ass populations in central Australia. Zeitschrift fu¨r Saügertierkunde 48:124–126. KLINGEL, H. 1969. The social organization and population ecology of the plains zebra, Equus quagga. Zoologica Africana 4:249–263. KLINGEL, H. 1974a. A comparison of the social behaviour of the Equidae. Pp. 124–132 in The papers of an international symposium on the behaviour of ungulates and its relation to management (V. Geist and F. Walther, eds.). International Union for the Conservation of Nature and Natural Resources (IUCN), Morges, Switzerland. KLINGEL, H. 1974b. Soziale Organisation und Verhalten des GrevyZebras (Equus grevyi). Zeitschrift fu¨r Tierpsychologie 36:36–70. KLINGEL, H. 1977. Observations on social organization and behaviour of African and Asiatic wild asses (Equus africanus and E. hemionus). Zeitschrift fu¨r Tierpsychologie 44:323–331. KLINGEL, H. 1978. La vie sociale des ze`bres et des antilopes. La Recherche 86:112–120. LEWISON, R. 1998. Infanticide in the hippopotamus: evidence for polygynous ungulates. Ethology, Ecology and Evolution 10: 277–286.

39

LIANG, K. Y., AND S. L. ZEGER. 1986. Longitudinal data analysis using generalized linear models. Biometrika 73:13–22. LINKLATER, W. L. 2000. Adaptive explanation in socio-ecology: lessons from the Equidae. Biological Reviews 75:1–20. LO¨NNBERG, E. 1912. Mammals collected by the Swedish zoological expedition to British East Africa, 1911. Kunglasse Svenska Vetenskapsakademiens Handlingar 48:5. LOTT, D. 1991. Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge, United Kingdom. MOEHLMAN, P. D., L. E. FOWLER, AND J. H. ROE. 1998. Feral asses (Equus africanus) of Volcano Alce´do, Galapagos: behavioral ecology, spatial distribution, and social organisation. Applied Animal Behaviour Science 60:197–210. MONFORT, A., AND N. MONFORT. 1978. Structure et re´partition des populations de ze`bres (Equus burchelli) du Parc de l’Akagera (Rwanda). Mammalia 42:315–322. NEUHAUS, P., AND K. E. RUCKSTUHL. 2002. The link between sexual dimorphism, activity budgets, and group cohesion: the case of the plains zebra (Equus burchelli). Canadian Journal of Zoology 80: 1437–1441. NEWTON, P. 1988. The variable social organization of Hanuman langurs (Presbytis entellus), infanticide, and the monopolization of females. International Journal of Primatology 9:59–77. OAKENFULL, E. A., H. N. LIM, AND O. A. RYDER. 2000. A survey of equid mitochondrial DNA: implications for the evolution, genetic diversity and conservation of Equus. Conservation Genetics 1:341–355. ØSTERBALLE, R. 1997. European studbook on maneless zebra (Equus burchelli borensis). Givskud Zoo, Givskud, Denmark. ØSTERBALLE, R. 1999. European monitor studbook on maneless zebra (Equus burchelli borensis). Givskud Zoo, Givskud, Denmark. PACHECO, M. A., AND E. A. HERRERA. 1997. Social structure of feral horses in the llanos of Venezuela. Journal of Mammalogy 78: 15–22. PENZHORN, B. L. 1985. Reproductive characteristics of a free-ranging population of Cape mountain zebra. Journal of Reproduction & Fertility 73:51–57. PLUHAĆˇEK, J., AND L. BARTOSˇ. 2000. Male infanticide in captive plains zebra (Equus burchelli). Animal Behaviour 59:689–694. PLUHAĆˇEK, J., AND L. BARTOSˇ. 2005. Further evidence for male infanticide and feticide in captive plains zebra, Equus burchelli. Folia Zoologica 54:258–262. RUBENSTEIN, D. I. 1981. Behavioral ecology of island feral horses. Equine Veterinary Journal 13:27–34. RUBENSTEIN, D. I. 1986. Ecology and sociality in horses and zebras. Pp. 282–302 in Ecological aspects of social evolution (D. I. Rubenstein and R. V. Wrangham, eds.). Princeton University Press, Princeton, New Jersey. RUBENSTEIN, D. I. 1993. The ecology of social behaviour in horses, zebras and asses. Physiology and Ecology (Japan) 29:13–28. RUDMAN, R. 1998. The social organisation of feral donkeys (Equus asinus) on a small Caribbean island (St. John, US Virgin Islands). Applied Animal Behaviour Science 60:211–228. RYDER, O. A., AND R. MASSENA. 1988. A case of male infanticide in Equus przewalskii. Applied Animal Behaviour Science 21:187–190. RZA˛SŃICKI, A. 1951. Zebras and quaggas. Annales Musei Zoologici Polonici 14:203–251. SALTZ, D., M. ROWEN, AND D. I. RUBENSTEIN. 2000. The effect of spaceuse patterns of reintroduced Asiatic wild ass on effective population size. Conservation Biology 14:1852–1861. SCHILDER, M. B. H. 1992. Stability and dynamics of group composition in a herd of captive plains zebra. Ethology 90:145–154.

40


SMUTS, G. L. 1976a. Population characteristics of Burchell’s zebra (Equus burchelli antiquorum, H. Smith, 1841) in the Kruger National Park. South African Journal of Wildlife Research 6:99–112. SMUTS, G. L. 1976b. Reproduction in the zebra mare Equus burchelli antiquorum from the Kruger National Park. Koedoe 19: 89–132. VAN SCHAIK, C. P. 2000. Infanticide by male primates: the sexual selection hypothesis revisited. Pp. 27–60 in Infanticide by males and its implications (C. P. van Schaik and C. H. Janson, eds.). Cambridge University Press, Cambridge, United Kingdom. VAN SCHAIK, C. P., AND C. H. JANSON (EDS.). 2000. Infanticide by males and its implications. Cambridge University Press, Cambridge, United Kingdom.

Vol. 87, No. 1

WESTFALL, P. H., R. D. TOBIAS, D. ROM, R. D. WOLFINGER, AND Y. HOCHBERG. 1999. Multiple comparisons and multiple tests using the SAS system. SAS Institute Inc., Cary, North Carolina. WOODWARD, S. L. 1979. The social system of feral asses. Zeitschrift fu¨r Tierpsychologie 49:304–316. ZHARKIKH, T. L. 1999. The cases of infanticide in the Przewalskii horses in Askajnia-Nova. Vestnik Zoologii Supplement 11:80–82. ZICCARDI, F. 1959. Zebra senza criniera dell’Oltregiuba. Supplemento alle Ricerche di Zoologica applicata alla Caccia 2:293–299.

Submitted 15 April 2005. Accepted 21 July 2005. Associate Editor was Nancy G. Solomon.