Revealing kleptoparasitic and predatory tendencies in an African mammal community using camera traps: a comparison of spatiotemporal approaches

Camera trap data are increasingly being used to characterise relationships between the spatiotemporal activity patterns of sympatric mammal species, often with a view to inferring inter-specific interactions. In this context, we attempted to characterise the kleptoparasitic and predatory tendencies of spotted hyaenas Crocuta crocuta and lions Panthera leo from photographic data collected across 54 camera trap stations and two dry seasons in Tanzania's Ruaha National Park. We applied four different methods of quantifying spatiotemporal associations, including one strictly temporal approach (activity pattern overlap), one strictly spatial approach (co-occupancy modelling), and two spatiotemporal approaches (co-detection modelling and temporal spacing at shared camera trap sites). We expected a kleptoparasitic relationship between spotted hyaenas and lions to result in a positive spatiotemporal association, and further hypothesised that the association between lions and their favourite prey in Ruaha, the giraffe Giraffa camelopardalis and the zebra Equus quagga, would be stronger than those observed with non-preferred prey species (the impala Aepyceros melampus and the dikdik Madoqua kirkii). Only approaches incorporating both the temporal and spatial components of camera trap data resulted in significant associative patterns. The latter were particularly sensitive to the temporal resolution chosen to define species detections (i.e. occasion length), and only revealed a significant positive association between lion on spotted hyaena detections, as well as a tendency for both species to follow each other at camera trap sites, during the dry season of 2013, but not that of 2014. In both seasons, observed spatiotemporal associations between lions and each of the four herbivore species considered provided no convincing or consistent indications of any predatory preferences. Our study suggests that, when making inferences on inter-specific interactions from camera trap data, due regards should be given to the potential behavioural and methodological processes underlying observed spatiotemporal patterns.

[1]  H. Jane Brockmann,et al.  Kleptoparasitism in birds , 1979, Animal Behaviour.

[2]  A. Sih The Behavioral Response Race Between Predator and Prey , 1984, The American Naturalist.

[3]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[4]  Kay E. Holekamp,et al.  A seasonal feast: long-term analysis of feeding behaviour in the spotted hyaena (Crocuta crocuta) , 1999 .

[5]  David L. Smith,et al.  The use of photographic rates to estimate densities of tigers and other cryptic mammals , 2001, Animal Conservation.

[6]  J. Laundré,et al.  Wolves, elk, and bison: reestablishing the "landscape of fear" in Yellowstone National Park, U.S.A. , 2001 .

[7]  H. Hofer,et al.  The response of spotted hyaenas to long‐term changes in prey populations: functional response and interspecific kleptoparasitism , 2002 .

[8]  J. Andrew Royle,et al.  ESTIMATING SITE OCCUPANCY RATES WHEN DETECTION PROBABILITIES ARE LESS THAN ONE , 2002, Ecology.

[9]  Kate E. Jones,et al.  Body mass of late Quaternary mammals , 2003 .

[10]  J. Nichols,et al.  Investigating species co-occurrence patterns when species are detected imperfectly , 2004 .

[11]  Craig Packer,et al.  Planning for success: Serengeti lions seek prey accessibility rather than abundance , 2005 .

[12]  G. Kerley,et al.  Prey preferences of the lion (Panthera leo) , 2005 .

[13]  Gerald Kastberger,et al.  Competitive interactions between spotted hyenas and lions in the Etosha National Park, Namibia , 2005 .

[14]  M. Hayward Prey preferences of the spotted hyaena (Crocuta crocuta) and degree of dietary overlap with the lion (Panthera leo) , 2006 .

[15]  D. MacKenzie Modeling the Probability of Resource Use: The Effect of, and Dealing with, Detecting a Species Imperfectly , 2006 .

[16]  Matt W. Hayward,et al.  Activity patterns of reintroduced lion Panthera leo and spotted hyaena Crocuta crocuta in the Addo Elephant National Park, South Africa , 2007 .

[17]  Yoan Dinata,et al.  Estimating occupancy of a data deficient mammalian species living in tropical rainforests: Sun bears in the Kerinci Seblat region, Sumatra , 2007 .

[18]  K. Holekamp,et al.  Interspecific competition influences reproduction in spotted hyenas , 2008 .

[19]  Michelle Thorn,et al.  Estimating Brown Hyaena Occupancy Using Baited Camera Traps , 2009 .

[20]  R. Slotow,et al.  Temporal Partitioning of Activity in Large African Carnivores: Tests of Multiple Hypotheses , 2009 .

[21]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[22]  M. Linkie,et al.  Estimating overlap of daily activity patterns from camera trap data , 2009 .

[23]  Byron J. T. Morgan,et al.  Design of occupancy studies with imperfect detection , 2010 .

[24]  Robert M Dorazio,et al.  A new parameterization for estimating co-occurrence of interacting species. , 2010, Ecological applications : a publication of the Ecological Society of America.

[25]  J. Ahumada,et al.  Community structure and diversity of tropical forest mammals: data from a global camera trap network , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  G. Guillera‐Arroita,et al.  Species Occupancy Modeling for Detection Data Collected Along a Transect , 2011 .

[27]  Martin S. Ridout,et al.  Assessing tiger–prey interactions in Sumatran rainforests , 2011 .

[28]  L. Silveira,et al.  Using occupancy models to investigate space partitioning between two sympatric large predators, the jaguar and puma in central Brazil , 2012 .

[29]  D. Dawson,et al.  Occupancy in continuous habitat , 2012 .

[30]  Jaguar and Puma Activity Patterns and Predator‐Prey Interactions in Four Brazilian Biomes , 2013 .

[31]  Daniel Fortin,et al.  Moving to stay in place: behavioral mechanisms for coexistence of African large carnivores. , 2013, Ecology.

[32]  R. Courtois,et al.  Multi-trophic resource selection function enlightens the behavioural game between wolves and their prey. , 2013, The Journal of animal ecology.

[33]  D. Macdonald,et al.  Activity patterns and temporal avoidance by prey in response to Sunda clouded leopard predation risk , 2013 .

[34]  Aaron P. Wagner,et al.  Occupancy patterns and niche partitioning within a diverse carnivore community exposed to anthropogenic pressures , 2013 .

[35]  Paul D. Meek,et al.  "Which camera trap type and how many do I need?" A review of camera features and study designs for a range of wildlife research applications , 2013 .

[36]  D. Macdonald,et al.  Risk avoidance in sympatric large carnivores: reactive or predictive? , 2013, The Journal of animal ecology.

[37]  R. Kays,et al.  Quantifying levels of animal activity using camera trap data , 2014 .

[38]  M. Lewis,et al.  A unifying framework for quantifying the nature of animal interactions , 2014, Journal of The Royal Society Interface.

[39]  J. Marcus Rowcliffe,et al.  Food acquisition and predator avoidance in a Neotropical rodent , 2014, Animal Behaviour.

[40]  G. Roemer,et al.  The application of occupancy modeling to evaluate intraguild predation in a model carnivore system , 2014 .

[41]  Trisalyn A Nelson,et al.  A critical examination of indices of dynamic interaction for wildlife telemetry studies. , 2014, The Journal of animal ecology.

[42]  Richard Bischof,et al.  Being the underdog: an elusive small carnivore uses space with prey and time without enemies , 2014 .

[43]  D. Macdonald,et al.  Using Landscape and Bioclimatic Features to Predict the Distribution of Lions, Leopards and Spotted Hyaenas in Tanzania's Ruaha Landscape , 2014, PloS one.

[44]  Lael Parrott,et al.  Spatio-temporal dynamics in the response of woodland caribou and moose to the passage of grey wolf. , 2014, The Journal of animal ecology.

[45]  T. Caro,et al.  Cheetahs and wild dogs show contrasting patterns of suppression by lions. , 2014, The Journal of animal ecology.

[46]  Theodore R. Simons,et al.  Performance of species occurrence estimators when basic assumptions are not met: a test using field data where true occupancy status is known , 2015 .

[47]  Damon B. Lesmeister,et al.  Spatial and Temporal Structure of a Mesocarnivore Guild in Midwestern North America , 2015 .

[48]  David W. Macdonald,et al.  Random versus Game Trail-Based Camera Trap Placement Strategy for Monitoring Terrestrial Mammal Communities , 2015, PloS one.

[49]  Sunarto Sunarto,et al.  Cat coexistence in central Sumatra: ecological characteristics, spatial and temporal overlap, and implications for management , 2015 .

[50]  J. Cusack,et al.  Conservation of snow leopards: spill-over benefits for other carnivores? , 2015, Oryx.

[51]  Erin M. Bayne,et al.  REVIEW: Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes , 2015 .

[52]  Tavis D. Forrester,et al.  Cats are Rare Where Coyotes Roam , 2015 .

[53]  E. Revilla,et al.  The Lion King and the Hyaena Queen: large carnivore interactions and coexistence , 2015, Biological reviews of the Cambridge Philosophical Society.

[54]  Craig J. Tambling,et al.  Temporal shifts in activity of prey following large predator reintroductions , 2015, Behavioral Ecology and Sociobiology.

[55]  D. Macdonald,et al.  Regional variation of the manifestation, prevalence, and severity of giraffe skin disease: A review of an emerging disease in wild and captive giraffe populations , 2016 .

[56]  D. Macdonald,et al.  Reactive responses of zebras to lion encounters shape their predator–prey space game at large scale , 2016 .