Craig Packer

A canine distemper virus epidemic in Serengeti lions ( Panthera leo )

CANINE distemper virus (CDV) is thought to have caused several fatal epidemics in canids within the Serengeti–Mara ecosystem of East Africa, affecting silver-backed jackals (Canis mesomelas) and bat-eared foxes (Otocyon megalotis) in 1978 (ref. 1), and African wild dogs (Lycaon pictus) in 1991 (refs 2, 3). The large, closely monitored Serengeti lion population4,5 was not affected in these epidemics. However, an epidemic caused by a morbillivirus closely related to CDV emerged abruptly in the lion population of the Serengeti National Park, Tanzania, in early 1994, resulting in fatal neurological disease characterized by grand mal seizures and myoclonus; the lions that died had encephalitis and pneumonia. Here we report the identification of CDV from these lions, and the close phylogenetic relationship between CDV isolates from lions and domestic dogs. By August 1994, 85% of the Serengeti lion population had anti-CDV antibodies, and the epidemic spread north to lions in the Maasai Mara National reserve, Kenya, and uncounted hyaenas, bat-eared foxes, and leopards were also affected.

Why Lions Form Groups: Food is Not Enough

Extensive observations of foraging female lions reveal that two group sizes maximize foraging success during the season of prey scarcity: one female and five or six females. Foraging success does not vary significantly with group size when prey is abundant. Female lions live in fission-fusion social units (prides) and forage only with members of their own pride. If lion grouping patterns were primarily related to group-size-specific feeding efficiency, females in prides containing fewer than five females should forage alone when prey is scarce, whereas females in larger prides should forage alone or in groups of five or six. However, extensive data on the grouping patterns of radio-collared females show that females in small prides most commonly forage in as large a group as possible, even at the expense of foraging efficiency. Females in large prides most often forage in intermediate group sizes of four or five. However, mothers keep their cubs in a creche and form highly stable maternity groups that are effective in defending the cubs against infanticidal males. Most large prides contain a creche involving four or five mothers, and in the absence of a creche, large prides show no preference for any group size. Females also compete aggressively against neighboring prides, and larger groups successfully repel smaller ones in territorial disputes. Small prides appear to be excessively gregarious in order to compete against larger neighboring prides.

Reproductive and genetic consequences of founding isolated lion populations

Species survival is critically dependent on reproductive performance, a complex physiological process under rigorous genetic control. Classical studies of inbreeding in laboratory animals and livestock have shown that increased homozygosity can adversely affect spermatogenesis, ovulation and perinatal mortality and morbidity1–3. For wild populations, the consequences of inbreeding depression have not been examined intensively, although our recent studies of the African cheetah revealed a striking degree of genetic uniformity4,5 combined with an extremely high incidence of structurally abnormal spermatozoa (>70%) in captive6 as well as free-ranging7 males. In this study, we report definitive evidence that the reproductive function of free-ranging mammals can be impaired as a result of demographic contraction followed by inbreeding. In an examination of three distinct lion populations (two from the Serengeti ecosystem in East Africa and a third descended from lions in the Gir Forest of western India), a direct correlation was observed between genetic variability and two physiological traits, incidence of abnormal sperm and circulating testosterone, a critical hormone for spermatogenesis.

Reproductive cessation in female mammals

In female mammals, fertility declines abruptly at an advanced age. The human menopause is one example, but reproductive cessation has also been documented in non-human primates, rodents, whales, dogs, rabbits, elephants and domestic livestock. The human menopause has been considered an evolutionary adaptation assuming that elderly women avoid the increasing complications of continued childbirth to better nurture their current children and grandchildren. But an abrupt reproductive decline might be only a non-adaptive by-product of life-history patterns. Because so many individuals die from starvation, disease and predation, detrimental genetic traits can persist (or even be favoured) as long as their deleterious effects are delayed until an advanced age is reached, and, for a given pattern of mortality, there should be an age by which selection would be too weak to prevent the onset of reproductive senescence,,. We provide a systematic test of these alternatives using field data from two species in which grandmothers frequently engage in kin-directed behaviour. Both species show abrupt age-specific changes in reproductive performance that are characteristic of menopause. But elderly females do not suffer increased mortality costs of reproduction, nor do post-reproductive females enhance the fitness of grandchildren or older children. Instead, reproductive cessation appears to result from senescence.

Transmission Dynamics and Prospects for the Elimination of Canine Rabies

Rabies has been eliminated from domestic dog populations in Western Europe and North America, but continues to kill many thousands of people throughout Africa and Asia every year. A quantitative understanding of transmission dynamics in domestic dog populations provides critical information to assess whether global elimination of canine rabies is possible. We report extensive observations of individual rabid animals in Tanzania and generate a uniquely detailed analysis of transmission biology, which explains important epidemiological features, including the level of variation in epidemic trajectories. We found that the basic reproductive number for rabies, R0, is very low in our study area in rural Africa (∼1.2) and throughout its historic global range (<2). This finding provides strong support for the feasibility of controlling endemic canine rabies by vaccination, even near wildlife areas with large wild carnivore populations. However, we show that rapid turnover of domestic dog populations has been a major obstacle to successful control in developing countries, thus regular pulse vaccinations will be required to maintain population-level immunity between campaigns. Nonetheless our analyses suggest that with sustained, international commitment, global elimination of rabies from domestic dog populations, the most dangerous vector to humans, is a realistic goal.

Cooperation in male lions: kinship, reciprocity or mutualism?

Playback experiments simulating the presence of intruder male lions elicited cooperative behaviour of male coalitions resident with prides of females. Resident males approached the broadcast roars on all occasions when more than one male was present for the experiment, and only failed to approach in three of eight cases when a single male faced the roars of three intruders. Three routes to cooperation were tested: kinship, reciprocity and mutualism. These results suggest that approaching the roars of strange males is a cooperative behaviour, and that this cooperation is not conditional on either the kinship or the behaviour of a males companions. Cooperation in male lions instead appears to be based on mutualism.

A comparative analysis of non-offspring nursing

Abstract Information on the incidence of non-offspring nursing in 100 mammalian species was assembled from the literature and from a questionnaire survey. A comparative analysis of these data revealed several factors that influence the occurrence of non-offspring nursing across species. The incidence of nonoffspring nursing is increased by captivity. In field studies, it is more common in species that have larger litters and there are several important differences in the context of non-offspring nursing between monotocous taxa (where females typically give birth to a single young) and polytocous taxa (where females routinely give birth to multiple young). In monotocous species, non-offspring nursing is associated with high levels of ‘milk theft’ by parasitic infants; and is more common in species where females continue nursing after they have lost their own young. In polytocous species, non-offspring nursing is not associated with ‘milk theft’ and is most common in species that live in small groups. These results are discussed in terms of the costs to females of tolerating non-offspring nursing.

Group hunting behaviour of lions : a search for cooperation

Abstract The participation of individual African lions, Panthera leo , during 64 communal hunts of four prey species was measured to quantify the extent to which lions cooperate and the factors affecting the degree of cooperation. The extent of individual participation in communal hunts varied significantly. Finite mixture models were used to determine the probability that each lions behaviour belonged to each of three strategies: ‘refraining’ (non-participation in hunts), ‘conforming’ (active participation in groups in which all individuals behaved similarly) and ‘pursuing’ (active participation in groups where individual behaviour varies). Our analysis reveals two important trends. First, males refrain more and pursue less than females. Second, refraining during a group hunt is more common during hunts of prey that appear to be easier to capture: lions are more likely to refrain during hunts of wart hog, Phacochoerus aethiopicus , and less likely to refrain during hunts of zebra, Equus burchelli , and buffalo, Syncerus caffer . Of the alternatives considered, the data indicate that refraining is ‘cheating’ and that lions exhibiting this strategy are thus exploiting the hunting behaviour of their companions. These results are discussed in the framework of a recent game-theoretical model of cooperative hunting.

Sustainable trophy hunting of African lions

In most species, sport hunting of male trophy animals can only reduce overall population size when the rate of removal of males is so high that females can no longer be impregnated. However, where males provide extensive paternal care, the removal of even a few individuals could harm the population as a whole. In species such as lions, excessive trophy hunting could theoretically cause male replacements (and associated infanticide) to become sufficiently common to prevent cubs reaching adulthood. Here we simulate the population consequences of lion trophy hunting using a spatially explicit, individual-based, stochastic model parameterized with 40 years of demographic data from northern Tanzania. Although our simulations confirm that infanticide increases the risk of population extinction, trophy hunting could be sustained simply by hunting males above a minimum age threshold, and this strategy maximizes both the quantity and the quality of the long-term kill. We present a simple non-invasive technique for estimating lion age in populations lacking long-term records, and suggest that quotas would be unnecessary in any male-only trophy species where age determination could be reliably implemented.

Viruses of the Serengeti: Patterns of Infection and Mortality in African Lions

Summary 1. We present data on the temporal dynamics of six viruses that infect lions (Panthera leo) in the Serengeti National Park and Ngorongoro Crater, Tanzania. These populations have been studied continuously for the past 30 years, and previous research has documented their seroprevalence for feline herpesvirus, feline immunodeficiency virus (FIV), feline calicivirus, feline parvovirus, feline coronavirus and canine distemper virus (CDV). A seventh virus, feline leukaemia virus (FeLV), was absent from these animals. 2. Comprehensive analysis reveals that feline herpesvirus and FIV were consistently prevalent at high levels, indicating that they were endemic in the host populations. Feline calici‐, parvo‐ and coronavirus, and CDV repeatedly showed a pattern of seroprevalence that was indicative of discrete disease epidemics: a brief period of high exposure for each virus was followed by declining seroprevalence. 3. The timing of viral invasion suggests that different epidemic viruses are associated with different minimum threshold densities of susceptible hosts. Furthermore, the proportion of susceptibles that became infected during disease outbreaks was positively correlated with the number of susceptible hosts at the beginning of each outbreak. 4. Examination of the relationship between disease outbreaks and host fitness suggest that these viruses do not affect birth and death rates in lions, with the exception of the 1994 outbreak of canine distemper virus. Although the endemic viruses (FHV and FIV) were too prevalent to measure precise health effects, there was no evidence that FIV infection reduced host longevity.