Predation strongly limits demography of a keystone migratory herbivore in a recovering transfrontier ecosystem

Abstract Large herbivore migrations are imperiled globally; however the factors limiting a population across its migratory range are typically poorly understood. Zambia's Greater Liuwa Ecosystem (GLE) contains one of the largest remaining blue wildebeest (Connochaetes taurinus taurinus) migrations, yet the population structure, vital rates, and limiting factors are virtually unknown. We conducted a long‐term demographic study of GLE wildebeest from 2012 to 2019 of 107 collared adult females and their calves, 7352 herd observations, 12 aerial population surveys, and concurrent carnivore studies. We applied methods of vital rate estimation and survival analysis within a Bayesian estimation framework. From herd composition observations, we estimated rates of fecundity, first‐year survival, and recruitment as 68%, 56%, and 38% respectively, with pronounced interannual variation. Similar rates were estimated from calf‐detections with collared cows. Adult survival rates declined steadily from 91% at age 2 years to 61% at age 10 years thereafter dropping more sharply to 2% at age 16 years. Predation, particularly by spotted hyena, was the predominant cause of death for all wildebeest ages and focused on older animals. Starvation only accounted for 0.8% of all unbiased known natural causes of death. Mortality risk differed substantially between wet and dry season ranges, reflecting strong spatio‐temporal differences in habitat and predator densities. There was substantial evidence that mortality risk to adults was 27% higher in the wet season, and strong evidence that it was 45% higher in the migratory range where predator density was highest. The estimated vital rates were internally consistent, predicting a stable population trajectory consistent with aerial estimates. From essentially zero knowledge of GLE wildebeest dynamics, this work provides vital rates, age structure, limiting factors, and a plausible mechanism for the migratory tendency, and a robust model‐based foundation to evaluate the effects of potential restrictions in migratory range, climate change, predator–prey dynamics, and poaching.

[1]  I. Douglas‐Hamilton,et al.  Cameras replace human observers in multi‐species aerial counts in Murchison Falls, Uganda , 2020, Remote Sensing in Ecology and Conservation.

[2]  S. Creel,et al.  Response of wildebeest (Connochaetes taurinus) movements to spatial variation in long term risks from a complete predator guild , 2019, Biological Conservation.

[3]  Benjamin J. Goodheart,et al.  What explains variation in the strength of behavioral responses to predation risk? A standardized test with large carnivore and ungulate guilds in three ecosystems , 2019, Biological Conservation.

[4]  S. Creel,et al.  Foraging investment in a long‐lived herbivore and vulnerability to coursing and stalking predators , 2018, Ecology and evolution.

[5]  S. Creel.  The control of risk hypothesis: reactive vs. proactive antipredator responses and stress-mediated vs. food-mediated costs of response. , 2018, Ecology letters.

[6]  S. Creel,et al.  Boots on the ground: in defense of low-tech, inexpensive, and robust survey methods for Africa’s under-funded protected areas , 2018, Biodiversity and Conservation.

[7]  N. Schumaker,et al.  Spatial Demographic Models to Inform Conservation Planning of Golden Eagles in Renewable Energy Landscapes , 2017, Journal of Raptor Research.

[8]  S. Creel,et al.  The relationship between direct predation and antipredator responses: a test with multiple predators and multiple prey. , 2017, Ecology.

[9]  M. Becker,et al.  Using dogs to find cats: detection dogs as a survey method for wide-ranging cheetah , 2017 .

[10]  S. Creel,et al.  Risky times and risky places interact to affect prey behaviour , 2017, Nature Ecology & Evolution.

[11]  S. Creel,et al.  Ecological and anthropogenic effects on the density of migratory and resident ungulates in a human‐inhabited protected area , 2017 .

[12]  L. Hayes,et al.  A synopsis of long-term field studies of mammals: achievements, future directions, and some advice , 2017, Journal of Mammalogy.

[13]  Benjamin A. Staton,et al.  From sequential to integrated Bayesian analyses: Exploring the continuum with a Pacific salmon spawner-recruit model , 2017 .

[14]  S. Creel,et al.  Spatial and temporal avoidance of risk within a large carnivore guild , 2016, Ecology and evolution.

[15]  S. Creel,et al.  Spotted hyaena survival and density in a lion depleted ecosystem: The effects of prey availability, humans and competition between large carnivores in African savannahs , 2016 .

[16]  W. Link,et al.  Tarangire revisited: Consequences of declining connectivity in a tropical ungulate population , 2016 .

[17]  J. Moore,et al.  Estimating Limit Reference Points for Western Pacific Leatherback Turtles (Dermochelys coriacea) in the U.S. West Coast EEZ , 2015, PloS one.

[18]  N. Pettorelli,et al.  Developing fencing policies for dryland ecosystems , 2015 .

[19]  Han Olff,et al.  Why are wildebeest the most abundant herbivore in the Serengeti , 2015 .

[20]  David W. Macdonald,et al.  Collapse of the world’s largest herbivores , 2015, Science Advances.

[21]  M. Becker,et al.  Human encroachment into protected area networks in Zambia: implications for large carnivore conservation , 2015, Regional Environmental Change.

[22]  M. Los Huertos,et al.  Estimating environmental conditions affecting protozoal pathogen removal in surface water wetland systems using a multi-scale, model-based approach. , 2014, The Science of the total environment.

[23]  T. Morrison,et al.  Connectivity and bottlenecks in a migratory wildebeest Connochaetes taurinus population , 2014, Oryx.

[24]  N. T. Hobbs,et al.  Integrating population- and individual-level information in a movement model of Yellowstone bison. , 2014, Ecological applications : a publication of the Ecological Society of America.

[25]  Fred G.R. Watson,et al.  Spatial patterns of wire-snare poaching: Implications for community conservation in buffer zones around National Parks , 2013 .

[26]  J. Gaillard.  Assessing fitness consequences of migratory tactics requires long-term individually based monitoring. , 2013, Ecology.

[27]  Rémi Choquet,et al.  A semi‐Markov model to assess reliably survival patterns from birth to death in free‐ranging populations , 2011 .

[28]  J. Fieberg,et al.  Estimating age-specific hazards from wildlife telemetry data , 2011, Environmental and Ecological Statistics.

[29]  Robert D. Holt,et al.  Predicted Impact of Barriers to Migration on the Serengeti Wildebeest Population , 2011, PloS one.

[30]  J. Hopcraft,et al.  Herbivores, resources and risks: alternating regulation along primary environmental gradients in savannas. , 2010, Trends in ecology & evolution.

[31]  F. Messier,et al.  Demography and population viability of polar bears in the Gulf of Boothia, Nunavut , 2009 .

[32]  J. Berger,et al.  Global decline in aggregated migrations of large terrestrial mammals , 2009 .

[33]  John M. Fryxell,et al.  Opposing Rainfall and Plant Nutritional Gradients Best Explain the Wildebeest Migration in the Serengeti , 2009, The American Naturalist.

[34]  Murdoch K. McAllister,et al.  A sequential Bayesian methodology to estimate movement and exploitation rates using electronic and conventional tag data: application to Atlantic bluefin tuna (Thunnus thynnus) , 2009 .

[35]  B. Elderd,et al.  Bias in population growth rate estimation: sparse data, partial life cycle analysis and Jensen's inequality , 2008 .

[36]  Murdoch K. McAllister,et al.  Combining multiple Bayesian data analyses in a sequential framework for quantitative fisheries stock assessment , 2008 .

[37]  Brian J. Smith,et al.  boa: An R Package for MCMC Output Convergence Assessment and Posterior Inference , 2007 .

[38]  D. Doak,et al.  The need for integrative approaches to understand and conserve migratory ungulates. , 2007, Ecology letters.

[39]  Tony O’Hagan.  Bayes factors , 2006 .

[40]  G. Caughley,et al.  Wildlife Ecology, Conservation and Management , 2006 .

[41]  Craig J. Tambling,et al.  Modelling wildebeest population dynamics: implications of predation and harvesting in a closed system , 2005 .

[42]  A. Sinclair,et al.  Can parks protect migratory ungulates? The case of the Serengeti wildebeest , 2004 .

[43]  J. Berger,et al.  The Last Mile: How to Sustain Long‐Distance Migration in Mammals , 2004 .

[44]  Dennis L. Murray,et al.  Assessing differential prey selection patterns between two sympatric large carnivores , 2003 .

[45]  Elisa Lee,et al.  Statistical Methods for Survival Data Analysis: Lee/Survival Data Analysis , 2003 .

[46]  L. Eberhardt.  A PARADIGM FOR POPULATION ANALYSIS OF LONG‐LIVED VERTEBRATES , 2002 .

[47]  Han Olff,et al.  Global environmental controls of diversity in large herbivores , 2002, Nature.

[48]  D. Doak,et al.  Long-term impacts of the Exxon Valdez oil spill on sea otters, assessed through age-dependent mortality patterns. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Ray Hilborn,et al.  Food regulates the Serengeti wildebeest: a 40‐year record , 1999 .

[50]  Toni K. Ruth,et al.  Winter Prey Selection by Wolves and Cougars in and Near Glacier National Park Montana , 1999 .

[51]  E. Milner‐Gulland,et al.  The ecology and management of the Saiga antelope in Kazakhstan , 1998 .

[52]  Peter Arcese,et al.  Serengeti II : dynamics, management, and conservation of an ecosystem , 1996 .

[53]  A. Sinclair,et al.  Population Consequences of Predation-Sensitive Foraging: The Serengeti Wildebeest , 1995 .

[54]  M. Mills,et al.  Predator--Prey Relationships: The Impact of Lion Predation on Wildebeest and Zebra Populations , 1992 .

[55]  John M. Fryxell,et al.  Why are Migratory Ungulates So Abundant? , 1988, The American Naturalist.

[56]  J. M. Fryxell,et al.  Seasonal migration by white‐eared kob in relation to resources , 1988 .

[57]  C. Attwell.  Population ecology of the blue wildebeest Connochaetes taurinus taurinus in Zululand, South Africa , 1982 .

[58]  A. Sinclair,et al.  Does competition or facilitation regulate migrant ungulate populations in the Serengeti? A test of hypotheses , 1982, Oecologia.

[59]  M. Friedman.  Piecewise Exponential Models for Survival Data with Covariates , 1982 .

[60]  J. Eisenberg,et al.  Serengeti: Dynamics of an Ecosystem , 1980 .

[61]  W. Siler.  A Competing‐Risk Model for Animal Mortality , 1979 .

[62]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[63]  S. Mazzuco,et al.  Measures and Models of Mortality , 2018 .

[64]  R. Estes.  The Gnu's World , 2014 .

[65]  M. Becker,et al.  Estimating past and future male loss in three Zambian lion populations , 2013 .

[66]  Peter A Vesk,et al.  A predictive model of avian natal dispersal distance provides prior information for investigating response to landscape change. , 2012, The Journal of animal ecology.

[67]  R. Holt,et al.  Grazers, browsers, and fire influence the extent and spatial pattern of tree cover in the Serengeti. , 2009, Ecological applications : a publication of the Ecological Society of America.

[68]  R. Estes,et al.  WCS Working Paper No. 37 - Status of the wildebeest (Connochaetes taurinus) in the wild, 1967-2005 , 2009 .

[69]  Claire N. Gower,et al.  Chapter 16 Wolf Prey Selection in an Elk-Bison System: Choice or Circumstance? , 2008 .

[70]  J. Berry,et al.  Aspects of wildebeest Connochaetes taurinus ecology in the Etosha National Park - a synthesis for future management , 1997 .

[71]  P. Boveng,et al.  MODELING AGE‐SPECIFIC MORTALITY FOR MARINE MAMMAL POPULATIONS , 1991 .

[72]  C. Whyte,et al.  Blue wildebeest population trends in the Kruger National Park and the effects of fencing , 1988 .

[73]  C. Attwell.  Reproduction and population ecology of the blue wildebeest Connochaetes taurinus taurinus in Zululand. , 1977 .

[74]  D. K. Andere.  The dynamics of pasture use by wildebeest (and cattle) in the Amboseli Basin , 1975 .

[75]  G. Schaller.  The Serengeti Lion: A Study of Predator-Prey Relations , 1972 .

[76]  L. Talbot,et al.  The wildebeest in Western Masailand, East Africa. , 1963 .