Linking diet switching to reproductive performance across populations of two critically endangered mammalian herbivores
Kawecki, T. J. Adaptation to Marginal Habitats. Annu. Rev. Ecol. Evol. Syst. 39, 321–342 (2008).
Google Scholar
Holt, R. D. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proc. Natl Acad. Sci. 106, 19659–19665 (2009).
Google Scholar
Pulliam, H. Sources, sinks, and population regulation. Am. Nat. 132, 652–661 (1988).
Google Scholar
Kendall, B. E., Fox, G. A., Fujiwara, M. & Nogeire, T. M. Demographic heterogeneity, cohort selection, and population growth. Ecology 92, 1985–1993 (2011).
Google Scholar
Britnell, J. A., Zhu, Y., Kerley, G. I. H. & Shultz, S. Ecological marginalization is widespread and increases extinction risk in mammals. Proc. Natl Acad. Sci. 120, e2205315120 (2023).
Google Scholar
Hardie, D. C. & Hutchings, J. A. Evolutionary ecology at the extremes of species’ ranges. Environ. Rev. 18, 1–20 (2010).
Google Scholar
Kaszta, Ż., Cushman, S. A. & Macdonald, D. W. Prioritizing habitat core areas and corridors for a large carnivore across its range. Anim. Conserv. 23, 607–616 (2020).
Google Scholar
Pironon, S. et al. Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biol. Rev. 92, 1877–1909 (2017).
Google Scholar
Santini, L., Pironon, S., Maiorano, L. & Thuiller, W. Addressing common pitfalls does not provide more support to geographical and ecological abundant-centre hypotheses. Ecography 42, 696–705 (2019).
Google Scholar
Johnston, A. S. A. et al. Predicting population responses to environmental change from individual-level mechanisms: towards a standardized mechanistic approach. Proc. R. Soc. B Biol. Sci. 286, 20191916 (2019).
Google Scholar
New, L. F. et al. Modelling the biological significance of behavioural change in coastal bottlenose dolphins in response to disturbance. Funct. Ecol. 27, 314–322 (2013).
Google Scholar
Grueter, C. C. et al. Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am. J. Phys. Anthropol. 140, 700–715 (2009).
Google Scholar
Kitaysky, A. S., Kitaiskaia, E. V., Piatt, J. F. & Wingfield, J. C. A mechanistic link between chick diet and decline in seabirds? Proc. R. Soc. B Biol. Sci. 273, 445–450 (2006).
Google Scholar
Ingala, M. R., Becker, D. J., Bak Holm, J., Kristiansen, K. & Simmons, N. B. Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats. Ecol. Evol. 9, 6508–6523 (2019).
Google Scholar
Faith, J. T. Palaeozoological insights into management options for a threatened mammal: southern Africa’s Cape mountain zebra (Equus zebra zebra). Divers. Distrib. 18, 438–447 (2012).
Google Scholar
Hecker, L. J., Edwards, M. A. & Nielsen, S. E. Assessing the nutritional consequences of switching foraging behavior in wood bison. Ecol. Evol. 11, 16165–16176 (2021).
Google Scholar
Jesmer, B. R., Kauffman, M. J., Murphy, M. A. & Goheen, J. R. A test of the niche variation hypothesis. a Rumin. Herbiv. J. Anim. Ecol. 89, 2825–2839 (2020).
Google Scholar
Staver, A. C. & Hempson, G. P. Seasonal dietary changes increase the abundances of savanna herbivore species. Sci. Adv. 6, eabd2848 (2020).
Google Scholar
Schoener, T. W. Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2, 369–404 (1971).
Google Scholar
Kartzinel, T. R., Hsing, J. C., Musili, P. M., Brown, B. R. P. & Pringle, R. M. Covariation of diet and gut microbiome in African megafauna. Proc. Natl Acad. Sci. 116, 23588–23593 (2019).
Google Scholar
Marshall, A. J., Boyko, C. M., Feilen, K. L., Boyko, R. H. & Leighton, M. Defining fallback foods and assessing their importance in primate ecology and evolution. Am. J. Phys. Anthropol. 140, 603–614 (2009).
Google Scholar
Altmann, S. A. Fallback foods, eclectic omnivores, and the packaging problem. Am. J. Phys. Anthropol. 140, 615–629 (2009).
Google Scholar
Kartzinel, T. R. & Pringle, R. M. Multiple dimensions of dietary diversity in large mammalian herbivores. J. Anim. Ecol. 89, 1482–1496 (2020).
Google Scholar
Iason, G. R. & Villalba, J. J. Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance–tolerance continuum. J. Chem. Ecol. 32, 1115–1132 (2006).
Google Scholar
Cooper, S. M., Owen-Smith, N. & Bryant, J. P. Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna. Oecologia 75, 336–342 (1988).
Google Scholar
Owen-Smith, N., Chafota, J. & Rachlow, J. Selective feeding by a megaherbivore, the African elephant (Loxodonta africana). J. Mammal. 93, 698–705 (2012).
Google Scholar
Abraham, J. O., Hempson, G. P. & Staver, A. C. Drought-response strategies of savanna herbivores. Ecol. Evol. 9, 7047–7056 (2019).
Google Scholar
Lea, J., Kerley, G., Hrabar, H., Barry, T. & Shultz, S. Recognition and management of ecological refugees: a case study of the Cape mountain zebra. Biol. Conserv. 203, 207–215 (2016).
Google Scholar
Kaczensky, P. et al. Stable isotopes reveal diet shift from pre-extinction to reintroduced Przewalski’s horses. Sci. Rep. 7, 5950 (2017).
Google Scholar
Ferreira, S. M., Roex, Nle & Greaver, C. Species-specific drought impacts on black and white rhinoceroses. PLoS ONE 14, e0209678 (2019).
Google Scholar
Mackie, R. I. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr. Comp. Biol. 42, 319–326 (2002).
Google Scholar
Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).
Google Scholar
Hanning, I. & Diaz-Sanchez, S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome 3, 51 (2015).
Google Scholar
Li, H. et al. Diet diversity is associated with beta but not alpha diversity of pika gut microbiota. Front. Microbiol. 7, 1169 (2016).
Google Scholar
Tracy, C. R. et al. The importance of physiological ecology in conservation biology. Integr. Comp. Biol. 46, 1191–1205 (2006).
Google Scholar
Li, Y. et al. Characterization of intestinal microbiota and fecal cortisol, T3, and IgA in forest musk deer (Moschus berezovskii) from birth to weaning. Integr. Zool. 16, 300–312 (2021).
Google Scholar
Antwis, R. E., Edwards, K. I., Unwin, B., Walker, S. L. & Shultz, S. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome 7, 1–12 (2019).
Google Scholar
Jiménez, R. R. & Sommer, S. The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers. Conserv. 26, 763–786 (2017).
Google Scholar
Barelli, C. et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci. Rep. 5, 14862 (2015).
Google Scholar
Whitecross, M. A., Witkowski, E. T. F. & Archibald, S. Savanna tree-grass interactions: a phenological investigation of green-up in relation to water availability over three seasons. South Afr. J. Bot. 108, 29–40 (2017).
Google Scholar
Adole, T., Dash, J. & Atkinson, P. M. Large-scale prerain vegetation green-up across Africa. Glob. Change Biol. 24, 4054–4068 (2018).
Google Scholar
Archibald, S. & Scholes, R. J. Leaf green-up in a semi-arid African savanna -separating tree and grass responses to environmental cues. J. Veg. Sci. 18, 583–594 (2007).
Hesla, B. I., Tieszen, H. L. & Boutton, T. W. Seasonal water relations of savanna shrubs and grasses in Kenya, East Africa. J. Arid Environ. 8, 15–31 (1985).
Google Scholar
Shorrocks, B. & Bates, W. Biology of African Savannahs Second Edition. (Oxford University Press, Oxford, 2014).
Milligan, P. D. et al. Mutualism disruption by an invasive ant reduces carbon fixation for a foundational East African ant-plant. Ecol. Lett. 24, 1052–1062 (2021).
Google Scholar
Pansu, J. et al. The generality of cryptic dietary niche differences in diverse large-herbivore assemblages. Proc. Natl Acad. Sci. 119, e2204400119 (2022).
Google Scholar
Buk, K. G. & Knight, M. H. Seasonal diet preferences of black rhinoceros in three arid South African National Parks. Afr. J. Ecol. 48, 1064–1075 (2010).
Google Scholar
Cerling, T. E. et al. Stable isotope ecology of black rhinos (Diceros bicornis) in Kenya. Oecologia 187, 1095–1105 (2018).
Google Scholar
Adcock, K., Amin, R. & Khayale, C. Habitat Characteristics and Carrying Capacity Relationships of 9 Kenyan Black Rhino Areas. (Kenya Wildlife Service, 2007).
Emslie, R., Amin, R. & Kock, R. Guidelines for the in Situ Re-Introduction and Translocation of African and Asian Rhinoceros. (IUCN Species Survival Commission, 2009).
Sundaresan, S. R., Fischhoff, I. R., Hartung, H. M., Akilong, P. & Rubenstein, D. I. Habitat choice of Grevy’s zebras (Equus grevyi) in Laikipia, Kenya. Afr. J. Ecol. 46, 359–364 (2008).
Google Scholar
Kartzinel, T. R. et al. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc. Natl Acad. Sci. USA 112, 8019–8024 (2015).
Google Scholar
Landman, M., Schoeman, D. & Kerley, G. Shift in black rhinoceros diet in the presence of elephant: evidence for competition? PLoS ONE 8, e69771 (2013).
Google Scholar
Barbosa, E. R. M. et al. Short-term effect of nutrient availability and rainfall distribution on biomass production and leaf nutrient content of Savanna tree species. PLoS ONE 9, e92619 (2014).
Google Scholar
Rubanza, C. D. K., Shem, M. N., Bakengesa, S. S., Ichinohe, T. & Fujihara, T. The content of protein, fibre and minerals of leaves of selected Acacia species indigenous to north-western Tanzania. Arch. Anim. Nutr. 61, 151–156 (2007).
Google Scholar
Abdulrazak, S. A., Fujihara, T., Ondiek, J. K. & Ørskov, E. R. Nutritive evaluation of some Acacia tree leaves from Kenya. Anim. Feed Sci. Technol. 85, 89–98 (2000).
Google Scholar
Tan, J. et al. in Advances in Immunology (ed. Alt, F. W.) Vol. 121. 91–119 (Academic Press, 2014).
Debruyne, L., Gevers, D. & Vandamme, P. Taxonomy of the Family Campylobacteraceae. in Campylobacter (eds. Nachamkin, I., Szymanski, C. M. & Vandamme, P.) 1–25 (John Wiley & Sons, Ltd, 2008).
Reese, A. T. & Dunn, R. R. Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. MBio 9, e01294–18 (2018).
Google Scholar
Russell, W. & Duthie, G. Plant secondary metabolites and gut health: the case for phenolic acids. Proc. Nutr. Soc. 70, 389–396 (2011).
Google Scholar
Odadi, W. O., Young, T. P. & Okeyo-Owuor, J. B. Effects of Wildlife on Cattle Diets in Laikipia Rangeland, Kenya. Rangel. Ecol. Manag. 60, 179–185 (2007).
Google Scholar
Cerling, T. E., Wittemyer, G., Ehleringer, J. R., Remien, C. H. & Douglas-Hamilton, I. History of animals using isotope records (HAIR): a 6-year dietary history of one family of African elephants. Proc. Natl Acad. Sci. 106, 8093–8100 (2009).
Google Scholar
MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).
Google Scholar
Crego, R. D. et al. Moving through the mosaic: identifying critical linkage zones for large herbivores across a multiple‐use African landscape. Landsc. Ecol. 36, 1325–1340 (2021).
Google Scholar
O’Neill, H. M. K., Durant, S. M., Strebel, S. & Woodroffe, R. Fencing affects African wild dog movement patterns and population dynamics. Oryx 56, 128–136 (2022).
Google Scholar
Harvey Sky, N. et al. Female reproductive skew exacerbates the extinction risk from poaching in the eastern black rhino. Proc. R. Soc. B Biol. Sci. 289, 20220075 (2022).
Google Scholar
Birkett, A. The impact of giraffe, rhino and elephant on the habitat of a black rhino sanctuary in Kenya. Afr. J. Ecol. 40, 276–282 (2002).
Google Scholar
Joppa, L. & Pfaff, A. High and far: biases in the location of protected areas. PLoS ONE 4, e8273 (2009).
Google Scholar
Venter, O. et al. Bias in protected-area location and its effects on long-term aspirations of biodiversity conventions. Conserv. Biol. 32, 127–134 (2018).
Google Scholar
Kerley, G., Beest, M., te, Cromsigt, J. P. G. M., Pauly, D. & Shultz, S. The Protected Area Paradox and refugee species: the giant panda and baselines shifted towards conserving species in marginal habitats. Conserv. Sci. Pract. 2, e203 (2020).
Google Scholar
Pearman, P. B., Guisan, A., Broennimann, O. & Randin, C. F. Niche dynamics in space and time. Trends Ecol. Evol. 23, 149–158 (2008).
Google Scholar
Sexton, J. P., McIntyre, P. J., Angert, A. L. & Rice, K. J. Evolution and ecology of species range limits. Annu. Rev. Ecol. Evol. Syst. 40, 415–436 (2009).
Google Scholar
Britnell, J. A. et al. Species stereotypes as a result of unconscious research biases compromise conservation efficacy. Biol. Conserv. 261, 109275 (2021).
Google Scholar
Kavwele, C. M., Kimanzi, J. K. & Kinyanjui, M. J. Impacts of bush encroachment on wildlife species diversity, composition, and habitat preference in Ol Pejeta Conservancy, Laikipia, Kenya. Int. J. Ecol. 2017, 1–6 (2017).
Giesen, W., Giesen, P. & Giesen, K. Habitat Changes at Lewa Wildlife Conservancy, Kenya. From Cattle Ranch to Conservation Area: Effects of Changing Management on Habitat from 1962–2006. (Lewa Wildlife Conservancy, 2007).
Winowiecki, L. A., Vågen, T.-G., Kinnaird, M. F. & O’Brien, T. G. Application of systematic monitoring and mapping techniques: assessing land restoration potential in semi-arid lands of Kenya. Geoderma 327, 107–118 (2018).
Google Scholar
Odadi, W. O., Fargione, J. & Rubenstein, D. I. Vegetation, wildlife, and livestock responses to planned grazing management in an African pastoral landscape. Land Degrad. Dev. 28, 2030–2038 (2017).
Google Scholar
Funk, C. et al. The climate hazards infrared precipitation with stations—a new environmental record for monitoring extremes. Sci. Data 2, 150066 (2015).
Google Scholar
Funk, C. Climate Hazards Group [Data set]. (2015).
Birkett, A. & Stevens‐Wood, B. Effect of low rainfall and browsing by large herbivores on an enclosed savannah habitat in Kenya. Afr. J. Ecol. 43, 123–130 (2005).
Google Scholar
Meshesha, D. T., Ahmed, M. M., Abdi, D. Y. & Haregeweyn, N. Prediction of grass biomass from satellite imagery in Somali regional state, eastern Ethiopia. Heliyon 6, e05272 (2020).
Google Scholar
USGS. USGS FEWS NET Data Portal. (2020).
Owen-Smith, R. Megaherbivores: The Influence of Very Large Body Size on Ecology. (Cambridge University Press, Cambridge, 1992).
Law, P. R., Fike, B. & Lent, P. C. Mortality and female fecundity in an expanding black rhinoceros (Diceros bicornis minor) population. Eur. J. Wildl. Res. 59, 477–485 (2013).
Google Scholar
Garnier, J., Bruford, M. & Goossens, B. Mating system and reproductive skew in the black rhinoceros. Mol. Ecol. 10, 2031–2041 (2001).
Google Scholar
Cain, B. et al. Sex‐biased inbreeding effects on reproductive success and home range size of the critically endangered black rhinoceros. Conserv. Biol. 28, 594–603 (2014).
Google Scholar
Rubenstein, D. I. et al. The state of Kenya’s Grevy’s zebras and reticulated giraffes: Results of the Great Grevy’s Rally 2018. (The Great Grevy’s Rally, 2018).
Pauli, J. N., Whiteman, J. P., Riley, M. D. & Middleton, A. D. Defining noninvasive approaches for sampling of vertebrates. Conserv. Biol. 24, 349–352 (2010).
Google Scholar
Murphy, M. A. et al. An evaluation of long-term preservation methods for brown bear (Ursus arctos) faecal DNA samples. Conserv. Genet. 3, 435–440 (2002).
Google Scholar
Blekhman, R. et al. Common methods for fecal sample storage in field studies yield consistent signatures of individual identity in microbiome sequencing data. Sci. Rep. 6, 31519 (2016).
Google Scholar
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).
Google Scholar
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).
Google Scholar
Posit Team. RStudio: Integrated Development for R. Posit Software (Posit Team, 2023).
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2022).
Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
Google Scholar
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41, D590–D596 (2013).
Google Scholar
Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42, D643–D648 (2014).
Google Scholar
Gill, B. A. et al. Plant DNA-barcode library and community phylogeny for a semi-arid East African savanna. Mol. Ecol. Resour. 19, 838–846 (2019).
Google Scholar
Gill, B. A. et al. DS-UHURUR2 [Data set]. BOLD (2021).
McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
Google Scholar
Deagle, B. E. et al. Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Mol. Ecol. 28, 391–406 (2019).
Google Scholar
Littleford-Colquhoun, B. L. et al. The precautionary principle and dietary DNA metabarcoding: commonly used abundance thresholds change ecological interpretation. Mol. Ecol. 31, 1615–1626 (2022).
Google Scholar
Littleford-Colquhoun, B. L., Sackett, V. I., Tulloss, C. V. & Kartzinel, T. R. Evidence-based strategies to navigate complexity in dietary DNA metabarcoding: a reply. Mol. Ecol. 31, 5660–5665 (2022).
Google Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Google Scholar
Holst, K. K. & Budtz-Jørgensen, E. Linear latent variable models: the lava-package. Comput. Stat. 28, 1385–1452 (2013).
Google Scholar
Barnett, D. J., Arts, I. C. & Penders, J. microViz: an R package for microbiome data visualization and statistics. J. Open Source Softw. 6, 3201 (2021).
Google Scholar
Wright, E. S. Using DECIPHER v2.0 to analyze big biological sequence data in R. R. J. 8, 352 (2016).
Google Scholar
Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).
Google Scholar
Revell, L. J. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 2, 217–223 (2012).
Liu, C., Cui, Y., Li, X. & Yao, M. microeco: an R package for data mining in microbial community ecology. FEMS Microbiol. Ecol. 97, fiaa255 (2021).
Google Scholar
Lozupone, C. & Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2005).
Google Scholar
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
Google Scholar
link