Asynchronous food-web pathways could buffer the response of Serengeti predators to El Niño Southern Oscillation.

Understanding how entire ecosystems maintain stability in the face of climatic and human disturbance is one of the most fundamental challenges in ecology. Theory suggests that a crucial factor determining the degree of ecosystem stability is simply the degree of synchrony with which different species in ecological food webs respond to environmental stochasticity. Ecosystems in which all food-web pathways are affected similarly by external disturbance should amplify variability in top carnivore abundance over time due to population interactions, whereas ecosystems in which a large fraction of pathways are nonresponsive or even inversely responsive to external disturbance will have more constant levels of abundance at upper trophic levels. To test the mechanism underlying this hypothesis, we used over half a century of demographic data for multiple species in the Serengeti (Tanzania) ecosystem to measure the degree of synchrony to variation imposed by an external environmental driver, the El Niño Southern Oscillation (ENSO). ENSO effects were mediated largely via changes in dry-season vs. wet-season rainfall and consequent changes in vegetation availability, propagating via bottom-up effects to higher levels of the Serengeti food web to influence herbivores, predators and parasites. Some species in the Serengeti food web responded to the influence of ENSO in opposite ways, whereas other species were insensitive to variation in ENSO. Although far from conclusive, our results suggest that a diffuse mixture of herbivore responses could help buffer top carnivores, such as Serengeti lions, from variability in climate. Future global climate changes that favor some pathways over others, however, could alter the effectiveness of such processes in the future.

Conserving large populations of lions - the argument for fences has holes.

Packer et al. reported that fenced lion populations attain densities closer to carrying capacity than unfenced populations. However, fenced populations are often maintained above carrying capacity, and most are small. Many more lions are conserved per dollar invested in unfenced ecosystems, which avoid the ecological and economic costs of fencing.

Social 'meltdown' in the demise of an island endemic: Allee effects and the Vancouver Island marmot.

1. More than 75 years have passed since W.C. Allee proposed that breakdowns in sociality may shift animal populations to inverse density dependence at small sizes and thereby hasten spirals to extinction. Despite decades of attention, empirical evidence of this 'Allee effect' in wild populations remains scarce. 2. Here, we report on findings from a multi-year study of the population ecology and behaviour of the critically endangered Vancouver Island marmot (Marmota vancouverensis) and present quantitative evidence of an Allee effect and highlight the mechanisms that drive it. 3. The V.I. marmot is a large, social rodent endemic to Vancouver Island, Canada, and its population has declined by 80-90% since the 1980s. The species currently is represented in the wild by roughly 200 individuals. 4. This study compared characteristics of contemporary V.I. marmots (2002-2005) with (i) animals in the same population at an earlier time period (1973-1975) and (ii) congeners. Specifically, data on time allocation, social activity and ranging behaviour of animals in colonies in the late stages of decline were compared with historical data collected from colonies under more stable demographic conditions. 5. We found that contemporary V.I. marmots had home ranges that were 10-60x larger than historic animals and congeners, interacted with conspecifics at 10% of the historic rate, devoted 10x more time to anti-predator vigilance, and abandoned the bi-modal activity patterns previously described for this and other marmot species. Contemporary marmots also showed an 86% decline in feeding rate, and entered hibernation on average 20 days later than animals in historic populations. 6. Combined with results showing reduced per capita survival and reproduction in contemporary marmots, these findings suggest a strong role for Allee effects in the current plight of the Vancouver Island marmot. A positive link between aspects of fitness and population size emphasizes the need to identify threshold colony sizes and densities necessary to promote recovery. We discuss this and other implications of this species' social 'meltdown'.

Herbivores, resources and risks: alternating regulation along primary environmental gradients in savannas.

Herbivores are regulated by predation under certain environmental conditions, whereas under others they are limited by forage abundance and nutritional quality. Whether top-down or bottom-up regulation prevails depends both on abiotic constraints on forage availability and body size, because size simultaneously affects the risk of predation of herbivores and their nutritional demands. Consequently, ecosystems composed of similar species can have different dynamics if they differ in resource supply. Here, we use large herbivore assemblages in African savanna ecosystems to develop a framework that connects environmental gradients and disturbance patterns with body size and trophic structure. This framework provides a model for understanding the functioning and diversity of ecosystems in general, and unifies how top-down and bottom-up mechanisms depend on common underlying environmental gradients.

Serengeti birds maintain forests by inhibiting seed predators.

Of fundamental interest in conservation ecology are the regulatory mechanisms that maintain communities. We document a mechanism that maintains forests in the Serengeti ecosystem, Tanzania, and the destabilization when disturbance opens forest canopy. Forest birds, by consuming seeds, protected them from beetle attack. Consumption increased the germination rate and the density of seedlings and recruits, which was sufficient to maintain the forest. Opening of the canopy resulted in loss of birds, increased beetle attack, and loss of germination. Thus, frugivorous birds are necessary for the maintenance of forests. Their absence could have resulted in the observed forest decline since 1966.

Long-term ecosystem dynamics in the Serengeti: lessons for conservation.

Data from long-term ecological studies further understanding of ecosystem dynamics and can guide evidence-based management. In a quasi-natural experiment we examined long-term monitoring data on different components of the Serengeti-Mara Ecosystem to trace the effects of disturbances and thus to elucidate cause-and-effect connections between them. The long-term data illustrated the role of food limitation in population regulation in mammals, particularly in migratory wildebeest and nonmigratory buffalo. Predation limited populations of smaller resident ungulates and small carnivores. Abiotic events, such as droughts and floods, created disturbances that affected survivorship of ungulates and birds. Such disturbances showed feedbacks between biotic and abiotic realms. Interactions between elephants and their food allowed savanna and grassland communities to co-occur. With increased woodland vegetation, predators' capture of prey increased. Anthropogenic disturbances had direct (hunting) and indirect (transfer of disease to wildlife) effects. Slow and rapid changes and multiple ecosystem states became apparent only over several decades and involved events at different spatial scales. Conservation efforts should accommodate both infrequent and unpredictable events and long-term trends. Management should plan on the time scale of those events and should not aim to maintain the status quo. Systems can be self-regulating through food availability and predator-prey interactions; thus, culling may not be required. Ecosystems can occur in multiple states; thus, there may be no a priori need to maintain one natural state. Finally, conservation efforts outside protected areas must distinguish between natural change and direct human-induced change. Protected areas can act as ecological baselines in which human-induced change is kept to a minimum.

Understanding ecosystem dynamics for conservation of biota.

1. Ecosystems have higher-order emerging properties that can affect the conservation of species. We identify some of these properties in order to facilitate a better understanding of them. 2. Nonlinear, indirect effects of food web interactions among species can produce counterintuitive changes in populations. 3. Species differ in their roles and linkages with other species in the system. These roles are a property of the system. Such differences in roles influence how we conserve individual species. 4. Ecosystems operate at a multitude of interacting spatial and temporal scales, which together structure the system and affect the dynamics of individual populations. 5. Disturbance also structures an ecosystem, producing both long-term slow changes and sudden shifts in ecosystem dynamics. 6. Ecosystems therefore can have multiple states, determined both by disturbance regimes and biotic interactions. Conservation should recognize a possible multiplicity of natural states while avoiding aberrant (human-induced) states. 7. Ecosystem processes are influenced by the composition of the biota they contain. Disturbances to the biota can distort processes and functions, which in turn can endanger individual species. 8. The goal of ecosystem conservation is the long-term persistence of the biota in the system. There are two paradigms: community-based conservation (CBC) and protected area conservation. Both have their advantages but neither is sufficient to protect the biota on its own. 9. CBC is required to conserve the majority of the world's biota not included in protected areas. However, current CBC methods favour a few idiosyncratic species, distort the species complex, and ignore the majority. More comprehensive methods are required for this approach to meet the goal of ecosystem conservation. 10. Protected areas are essential to conserve species unable to coexist with humans. They also function as ecological baselines to monitor the effects of humans on their own ecosystems. 11. However, protected areas suffer from loss of habitat through attrition of critical areas. Thus, renewal (addition) of habitat is required in order to achieve the long-term persistence of biota in functioning ecosystems. Identification of minimum habitat areas and restoration of ecosystems become two major priorities for future research.

Bushmeat hunting, wildlife declines, and fish supply in West Africa.

The multibillion-dollar trade in bushmeat is among the most immediate threats to the persistence of tropical vertebrates, but our understanding of its underlying drivers and effects on human welfare is limited by a lack of empirical data. We used 30 years of data from Ghana to link mammal declines to the bushmeat trade and to spatial and temporal changes in the availability of fish. We show that years of poor fish supply coincided with increased hunting in nature reserves and sharp declines in biomass of 41 wildlife species. Local market data provide evidence of a direct link between fish supply and subsequent bushmeat demand in villages and show bushmeat's role as a dietary staple in the region. Our results emphasize the urgent need to develop cheap protein alternatives to bushmeat and to improve fisheries management by foreign and domestic fleets to avert extinctions of tropical wildlife.

Mammal population regulation, keystone processes and ecosystem dynamics.

The theory of regulation in animal populations is fundamental to understanding the dynamics of populations, the causes of mortality and how natural selection shapes the life history of species. In mammals, the great range in body size allows us to see how allometric relationships affect the mode of regulation. Resource limitation is the fundamental cause of regulation. Top-down limitation through predators is determined by four factors: (i). body size; (ii). the diversity of predators and prey in the system; (iii). whether prey are resident or migratory; and (iv). the presence of alternative prey for predators. Body size in mammals has two important consequences. First, mammals, particularly large species, can act as keystones that determine the diversity of an ecosystem. I show how keystone processes can, in principle, be measured using the example of the wildebeest in the Serengeti ecosystem. Second, mammals act as ecological landscapers by altering vegetation succession. Mammals alter physical structure, ecological function and species diversity in most terrestrial biomes. In general, there is a close interaction between allometry, population regulation, life history and ecosystem dynamics. These relationships are relevant to applied aspects of conservation and pest management.

Patterns of predation in a diverse predator-prey system.

There are many cases where animal populations are affected by predators and resources in terrestrial ecosystems, but the factors that determine when one or the other predominates remain poorly understood. Here we show, using 40 years of data from the highly diverse mammal community of the Serengeti ecosystem, East Africa, that the primary cause of mortality for adults of a particular species is determined by two factors--the species diversity of both the predators and prey and the body size of that prey species relative to other prey and predators. Small ungulates in Serengeti are exposed to more predators, owing to opportunistic predation, than are larger ungulates; they also suffer greater predation rates, and experience strong predation pressure. A threshold occurs at prey body sizes of approximately 150 kg, above which ungulate species have few natural predators and exhibit food limitation. Thus, biodiversity allows both predation (top-down) and resource limitation (bottom-up) to act simultaneously to affect herbivore populations. This result may apply generally in systems where there is a diversity of predators and prey.

Protected areas as biodiversity benchmarks for human impact: agriculture and the Serengeti avifauna.

Protected areas as biodiversity benchmarks allow a separation of the direct effects of human impact on biodiversity loss from those of other environmental changes. We illustrate the use of ecological baselines with a case from the Serengeti ecosystem, Tanzania. We document a substantial but previously unnoted loss of bird diversity in agriculture detected by reference to the immediately adjacent native vegetation in Serengeti. The abundance of species found in agriculture was only 28% of that for the same species in native savannah. Insectivorous species feeding in the grass layer or in trees were the most reduced. Some 50% of both insectivorous and granivorous species were not recorded in agriculture, with ground-feeding and tree species most affected. Grass-layer insect abundance and diversity was much reduced in agriculture, consistent with the loss of insectivorous birds. These results indicate that many species of birds will become confined to protected areas over time. We need to determine whether existing protected areas are sufficiently large to maintain viable populations of insectivorous birds likely to become confined to them. This study highlights the essential nature of baseline areas for assessing causes of change in human-dominated systems and for developing innovative strategies to restore biodiversity.

Complex numerical responses to top-down and bottom-up processes in vertebrate populations.

Population growth rate is determined in all vertebrate populations by food supplies, and we postulate bottom-up control as the universal primary standard. But this primary control system can be overridden by three secondary controls: top-down processes from predators, social interactions within the species and disturbances. Different combinations of these processes affect population growth rates in different ways. Thus, some relationships between growth rate and density can be hyperbolic or even have multiple nodes. We illustrate some of these in marsupial, ungulate and rabbit populations. Complex interactions between food, predators, environmental disturbance and social behaviour produce the myriad observations of population growth in nature, and we need to develop generalizations to classify populations. Different animal groups differ in the combination of these four processes that affect them, in their growth rates and in their vulnerability to extinction. Because conservation and management of populations depend critically on what factors drive population growth, we need to develop universal generalizations that will relieve us from the need to study every single population before we can make recommendations for management.

Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments.

Predator-prey studies in semi-arid eastern Australia demonstrated that populations of rabbits (Oryctolagus cuniculus) could be regulated by predators. The functional, numerical and total responses of foxes (Vulpes vulpes) to rabbits and the numerical response of feral cats (Felis catus) to rabbits, are described. Measurement of the rabbit component of foxes' stomach contents indicates a Type III functional response. The size of the fox population in summer was dependent on the availability of rabbits over the immediately preceding rabbit breeding season but there appeared to be no density-dependent aggregation of young foxes in areas of surplus food. The total response of foxes, estimated using the short-term numerical response of dispersing foxes, was directly density-dependent for low rabbit densities and inversely density-dependent for high rabbit densities. Two states are possible with this form of total response: a state with low rabbit densities regulated by predators and a state with high rabbit densities which occurs when rabbits escape predator regulation. The boundary between regulation and non-regulation by predators was demonstrated by a predator-removal experiment. In the treated areas, predators were initially culled and rabbits increased to higher densities than in an untreated area where predators were always present. When predators were allowed back into the treated areas, rabbit populations continued to increase and did not decline to the density in the untreated area. This is the critical evidence for a two-state system. When predators were present, rabbits could be maintained at low densities which were in the density-dependent part of the total response curve for foxes. Exceptionally high rabbit recruitment, or artificially reduced predation, could result in rabbits escaping predator-regulation. Under these circumstances, rabbits could move into the inversely density-dependent region of the total response curve for foxes.

Does competition regulate ungulate populations? Further evidence from Serengeti, Tanzania.

Changes in populations of several ungulate species in the Serengeti-Mara region of East Africa over the past 30 years suggest several hypotheses for their regulation and coexistence. Recent censuses in the 1980s have allowed us to test the hypotheses that: (1) there was competition between wildebeest (Connochaetes taurinus) and Thomson's gazelle (Gazella thomsoni). This predicted that gazelle numbers should have declined in the 1980s when wildebeest were food limited. Census figures show no change in gazelle numbers between 1978 and 1986, a result contrary to the interspecific competition hypothesis; (2) wildebeest and African buffalo (Syncerus caffer) populations were regulated by intraspecific competition for food. Since both populations reached food limitation in the 1970s, the hypothesis predicted that the populations should have been stable in the 1980s. The results confirm these predictions for wildebeest and the buffalo population in the Mara reserve. In the Serengeti the buffalo population declined 41% over the period 1976-1984. The decline was not evenly distributed over the park, some areas showing an 80-90% decline, others no change or an increase in numbers. The decline was associated with proximity to human habitation; (3) an outbreak of the viral disease, rinderpest, in 1982 may have been the cause of the drop in buffalo population. Blood serum samples to measure the prevalence of antibodies were collected from areas of decreasing, stable and increasing populations. If rinderpest was the cause of decrease there should be a negative relationship between the prevalence of rinderpest and the instantaneous rate of increase (r). The results showed no relationship. We conclude that rinderpest was not the major cause of the drop in buffalo numbers. Elephant (Loxodonta africana) numbers dropped 81% in Serengeti in the period 1977-1986. In the Mara there was little change. The evidence suggests that extensive poaching in northern and western Serengeti during 1979-1984 accounted for the drop in both elephant and buffalo numbers.

An antifeedant in balsam poplar inhibits browsing by snowshoe hares.

The 'plant defense guild' hypothesis for the evolution of plant secondary chemicals predicts that plant species defend themselves against generalist herbivores such as the snowshoe hare (Lepus americanus) in the Canadian boreal forest by evolving unique antifeedant chemicals. Plant species may coevolve in an ecosystem by presenting an array of chemicals to herbivores. We report further evidence for this idea from the presence of 2,4,6-trihydroxydihydrochalcone in the CH2Cl2 extracts of Populus balsamifera juvenile twigs. These extracts, added to rabbit chow, were offered to hares in choice tests. The bioassay established that the chemical acted as an antifeedant for hares.

Can predation cause the 10-year hare cycle?

We relate causes of mortality of snowshoe hares to density of hares over an 8-year period that included a peak in numbers. We then use simulation modeling to examine whether these density-dependent relationships could produce changes in hare density similar to those observed in our study are in Yukon, Canada.Predation during winter was the largest source of mortality for snowshoe hares at Kluane, Yukon during 1978-84. There was a one-year lag in the response of winter predation mortality rate to hare density. There was a two-year lag in the response of winter mortality not caused by predators to hare density.A simple simulation model with density-dependent predation produced 8-11 year cycles only within a narrow range of parameters that are inconsistent with data from the Kluane region. However, a simulation model that predicted winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, produced 8-11 year cycles within the range of parameter values measured in our study. Yet another simulation model that predicted both summer and winter mortality rates using a delayed density-dependent numerical response and a Type II functional response by predators, did not produce 8-11 year cycles within the range of parameter values measured in our study. Lack of data on juvenile mortality may be one reason for this result.

Population regulation of Serengeti Wildebeeest: a test of the food hypothesis.

The food hypothesis proposes that density dependent mortality regulates populations through food shortage. For Serengeti wildebeest, we found an empirical relationship between dry season adult mortality rate, density and food supply. This relationship predicted that: (1) the population would stabilize between 1.0 and 1.5 million animals, (2) dry season mortality would be density dependent and sufficient to account for the levelling off of this large ungulate population. Recent observations have tested and confirmed these predictions.

Do plant secondary compounds determine feeding preferences of snowshoe hares?

We investigated the food preferences of captive snowshoc hares (Lepus americanus) in winter to test three hypotheses proposed to explain food choices by hares: (1) that food choice is related to the protein content of twigs; 92) that defensive chemicals present in twigs are negatively correlated with hare food preferences; and (3) that hares eat less-preferred but protein-rich twigs when their diet is buffered by large amounts of palatable food. Hares exhibited striking and consistent preferences for different species and, in general, preferred mature twigs to juvenile growth stages. Preferences across species among mature twigs were not, however, the same as preferences for juvenile growth stages across species. None of the three hypotheses adequately explained food choice by hares. Hares did not (1) select twigs that were high in protein content. They also did not (2) consistently select twigs that were low in resins or phenols. Finally (3), hares generally ate less, not more of non-preferred twigs in the presence of a protein and energy rich alternative food, commercial rabbit chow. Food preferences of hares must presumably have some chemical basis, but no simple theory has yet explained what this is. We suggest that hares may not be under severe dietary constraints imposed by chemical defenses in winter.

Does competition or facilitation regulate migrant ungulate populations in the Serengeti? A test of hypotheses.

Interspecific competition and facilitation have both been proposed as processes promoting species separation and co-existence in African ungulates. In one group of grazers on the Serengeti plains, comprising wildebeest (Connochaetes taurinus), zebra (Equus burchelli), and Thomson's gazelle (Gazella thomsoni), these processes have also been suggested to regulate the populations. Censuses of these populations over 20 years have shown changes that allow a test of which, if either, process regulates population numbers. Wildebeest numbers have levelled off as a result of intraspecific competition for food following a five-fold increase due to release from disease and an increase in food supply. Zebra numbers have remained stationary throughout the same period. Gazelle numbers have declined in the last 10 years. These results are contrary to the facilitation hypothesis, which predicts that wildebeest numbers should not have increased if those of zebra did not, and that gazelle numbers should have increased since the wildebeest population increased. The gazelle results are consistent with the interspecific competition hypothesis, but the zebra results are contrary to it. We propose an alternative hypothesis that predation regulates the zebra population, and we suggest ways of testing this.