Diverse effects of the common hippopotamus on plant communities and soil chemistry

Abstract

The ecological importance of the common hippopotamus (Hippopotamus amphibius) in aquatic ecosystems is becoming increasingly well known. These unique megaherbivores are also likely to have a formative influence on the terrestrial ecosystems in which they forage. In this study, we employed a novel exclosure design to exclude H. amphibius from experimental plots on near-river grasslands. Our three-year implementation of this experiment revealed a substantial influence of H. amphibius removal on both plant communities and soil chemistry. H. amphibius significantly reduced grassland canopy height, increased the leafiness of common grasses, reduced woody plant abundance and size, and increased the concentrations of several soil elements. Many of the soil chemistry changes that we experimentally induced by exclusion of H. amphibius were mirrored in the soil chemistry differences between naturally occurring habitats of frequent (grazing lawns) and infrequent (shrub forest) use by H. amphibius and other grazing herbivores. In contrast to existing hypotheses regarding grazing species, we found that H. amphibius had little effect on local plant species richness. Simultaneous observations of exclosures designed to remove all large herbivores revealed that H. amphibius removal had ecologically significant impacts, but that the removal of all species of large herbivores generated more pronounced impacts than the removal of H. amphibius alone. In aggregate, our results suggest that H. amphibius have myriad effects on their terrestrial habitats that likely improve the quality of forage available for other herbivores. We suggest that ongoing losses of this vulnerable megaherbivore are likely to cause significant ecological change.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Augustine DJ, McNaughton SJ (2006) Interactive effects of ungulate herbivores, soil fertility, and variable rainfall on ecosystem processes in a semi-arid savanna. Ecosystems 9:1242–1256

    CAS  Article  Google Scholar 

  2. Bakker ES, Gill JL, Johnson CN et al (2016) Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation. Proc Natl Acad Sci 113:847–855. https://doi.org/10.1073/pnas.1502545112

    CAS  Article  PubMed  Google Scholar 

  3. Barnosky AD, Koch PL, Feranec RS et al (2004) Assessing the causes of late pleistocene extinctions on the continents. Science 306:70–75. https://doi.org/10.1126/science.1101476

    CAS  Article  PubMed  Google Scholar 

  4. Barnosky AD, Lindsey EL, Villavicencio NA et al (2016) Variable impact of late-quaternary megafaunal extinction in causing ecological state shifts in North and South America. Proc Natl Acad Sci 113:856–861. https://doi.org/10.1073/pnas.1505295112

    CAS  Article  PubMed  Google Scholar 

  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  6. Belsky AJ (1992) Effects of grazing, competition, disturbance and fire on species composition and diversity in grassland communities. J Veg Sci 3:187–200. https://doi.org/10.2307/3235679

    Article  Google Scholar 

  7. Boisserie J-R, Fisher RE, Lihoreau F, Weston EM (2011) Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea, Cetancodonta, Cetartiodactyla). Biol Rev 86:601–625. https://doi.org/10.1111/j.1469-185X.2010.00162.x

    Article  PubMed  Google Scholar 

  8. Caylor KK, Gitonga J, Martins DJ (2017) Mpala research centre meteorological and hydrological dataset [Datafile]. Mpala Research Centre, Laikipia

    Google Scholar 

  9. Cerling TE, Harris JM, Hart JA et al (2008) Stable isotope ecology of the common hippopotamus. J Zool 276:204–212. https://doi.org/10.1111/j.1469-7998.2008.00450.x

    Article  Google Scholar 

  10. Chao A, Chiu C-H, Jost L (2014) Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annu Rev Ecol Evol Syst 45:297–324. https://doi.org/10.1146/annurev-ecolsys-120213-091540

    Article  Google Scholar 

  11. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  12. Cromsigt JPGM, te Beest M (2014) Restoration of a megaherbivore: landscape-level impacts of white rhinoceros in Kruger National Park, South Africa. J Ecol 102:566–575. https://doi.org/10.1111/1365-2745.12218

    Article  Google Scholar 

  13. Cromsigt JPGM, Veldhuis MP, Stock WD et al (2017) The functional ecology of grazing lawns: how grazers, termites, people, and fire shape HiP’s savanna grassland mosaic. In: Cromsigt JPGM, Archibald S, Owen-Smith N (eds) Conserving Africa’s mega-diversity in the Anthropocene: the Hluhluwe-iMfolozi Park story. Cambridge University Press, Cambridge, UK, pp 135–160

    Google Scholar 

  14. Dahnke W, Johnson GV (1990) Testing soils for available nitrogen. In: Westerman RL (ed) Soil testing and plant analysis. Soil Science Society of America Inc, Madison, pp 128–139

    Google Scholar 

  15. de Boer WF, Van Oort JWA, Grover M, Peel MJS (2015) Elephant-mediated habitat modifications and changes in herbivore species assemblages in Sabi Sand, South Africa. Eur J Wildl Res 61:491–503. https://doi.org/10.1007/s10344-015-0919-3

    Article  Google Scholar 

  16. Detling JK, Painter EL (1983) Defoliation responses of western wheatgrass populations with diverse histories of prairie dog grazing. Oecologia 57:65–71

    CAS  Article  Google Scholar 

  17. Eldridge DJ, Bowker MA, Maestre FT et al (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis: synthesizing shrub encroachment effects. Ecol Lett 14:709–722. https://doi.org/10.1111/j.1461-0248.2011.01630.x

    Article  PubMed  PubMed Central  Google Scholar 

  18. Eltringham SK (1974) Changes in the large mammal community of Mweya Peninsula, Rwenzori National Park, Uganda, following removal of hippopotamus. J Appl Ecol 11:855. https://doi.org/10.2307/2401750

    Article  Google Scholar 

  19. Eltringham SK (1999) The hippos: natural history and conservation. Princeton University Press, Princeton

    Google Scholar 

  20. Frank DA, Groffman PM, Evans RD, Tracy BF (2000) Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands. Oecologia 123:116–121

    CAS  Article  Google Scholar 

  21. Georgiadis NJ, McNaughton SJ (1988) Interactions between grazers and a cyanogenic grass, Cynodon plectostachyus. Oikos 51:343. https://doi.org/10.2307/3565316

    Article  Google Scholar 

  22. Gill JL (2014) Ecological impacts of the late quaternary megaherbivore extinctions. New Phytol 201:1163–1169. https://doi.org/10.1111/nph.12576

    Article  PubMed  Google Scholar 

  23. Gosling CM (2014) Biotic determinants of heterogeneity in a South African savanna. University of Groningen, PhD

    Google Scholar 

  24. Gregory NC, Sensenig RL, Wilcove DS (2010) Effects of controlled fire and livestock grazing on bird communities in East African savannas. Conserv Biol 24:1606–1616. https://doi.org/10.1111/j.1523-1739.2010.01533.x

    Article  PubMed  Google Scholar 

  25. Hempson GP, Archibald S, Bond WJ et al (2015) Ecology of grazing lawns in Africa: African grazing lawns. Biol Rev 90:979–994. https://doi.org/10.1111/brv.12145

    Article  PubMed  Google Scholar 

  26. Hess AN, Hess RJ, Hess JLM et al (2014) American bison influences on lepidopteran and wild blue lupine distribution in an oak savanna landscape. J Insect Conserv 18:327–338. https://doi.org/10.1007/s10841-014-9640-x

    Article  Google Scholar 

  27. Hobbs NT (1996) Modification of ecosystems by ungulates. J Wildl Manag 60:695. https://doi.org/10.2307/3802368

    Article  Google Scholar 

  28. Johnson CN, Rule S, Haberle SG et al (2016) Geographic variation in the ecological effects of extinction of Australia’s Pleistocene megafauna. Ecography 39:109–116. https://doi.org/10.1111/ecog.01612

    Article  Google Scholar 

  29. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373. https://doi.org/10.2307/3545850

    Article  Google Scholar 

  30. Kanga EM, Ogutu JO, Piepho H-P, Olff H (2013) Hippopotamus and livestock grazing: influences on riparian vegetation and facilitation of other herbivores in the Mara Region of Kenya. Landsc Ecol Eng 9:47–58. https://doi.org/10.1007/s11355-011-0175-y

    Article  Google Scholar 

  31. Karki JB, Jhala YV, Khanna PP (2000) Grazing lawns in Terai Grasslands, Royal Bardia National Park, Nepal. Biotropica 32:423. https://doi.org/10.1646/0006-3606(2000)032%5b0423:GLITGR%5d2.0.CO;2

    Article  Google Scholar 

  32. Kimuyu DM, Sensenig RL, Riginos C et al (2014) Native and domestic browsers and grazers reduce fuels, fire temperatures, and acacia ant mortality in an African savanna. Ecol Appl 24:741–749

    Article  Google Scholar 

  33. Knapp AK, Blair John M, Briggs John M et al (1999) The keystone role of bison in North American tallgrass prairie Bison increase habitat heterogeneity and alter a broad array of plant, community, and ecosystem processes. Bioscience 49:39–50

    Article  Google Scholar 

  34. Lewison RL, Carter J (2004) Exploring behavior of an unusual megaherbivore: a spatially explicit foraging model of the hippopotamus. Ecol Model 171:127–138. https://doi.org/10.1016/S0304-3800(03)00305-3

    Article  Google Scholar 

  35. Lewison R, Oliver W (IUCN SSC Hippo Specialist Subgroup) (2008) Hippopotamus amphibius. The IUCN red list of threatened species. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T10103A3163790.en. Accessed 6 Jan 2017

  36. Lock JM (1972) The effects of hippopotamus grazing on grasslands. J Ecol 60:445. https://doi.org/10.2307/2258356

    Article  Google Scholar 

  37. McCauley DJ, Dawson TE, Power ME, et al (2015) Carbon stable isotopes suggest that hippopotamus-vectored nutrients subsidize aquatic consumers in an East African river. Ecosphere 6:art52. https://doi.org/10.1890/es14-00514.1

    Article  Google Scholar 

  38. McCauley DJ, Hardesty-Moore M, Halpern BS, Young HS (2016) A mammoth undertaking: harnessing insight from functional ecology to shape de-extinction priority setting. Funct Ecol. https://doi.org/10.1111/1365-2435.12728

    Article  Google Scholar 

  39. McNaughton SJ (1976) Serengeti migratory wildebeest: facilitation of energy flow by grazing. Science 191:92–94

    CAS  Article  Google Scholar 

  40. McNaughton SJ (1983) Serengeti grassland ecology: the role of composite environmental factors and contingency in community organization. Ecol Monogr 53:291–320. https://doi.org/10.2307/1942533

    Article  Google Scholar 

  41. McNaughton SJ (1984) Grazing lawns: animals in herds, plant form, and coevolution. Am Nat 124:863–886

    Article  Google Scholar 

  42. McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–294. https://doi.org/10.2307/1942578

    Article  Google Scholar 

  43. Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416. https://doi.org/10.1080/00103628409367568

    CAS  Article  Google Scholar 

  44. Olivier RCD, Laurie WA (1974) Habitat utilization by hippopotamus in the Mara River. Afr J Ecol 12:249–271

    Article  Google Scholar 

  45. Owen-Smith NR (1988) Megaherbivores. Cambridge University Press, Cambridge

    Google Scholar 

  46. Painter EL, Detling JK, Steingraeber DA (1993) Plant morphology and grazing history. Vegetatio 106:37–62

    Article  Google Scholar 

  47. Person BT, Herzog MP, Ruess RW et al (2003) Feedback dynamics of grazing lawns: coupling vegetation change with animal growth. Oecologia 135:583–592

    Article  Google Scholar 

  48. Pringle RM (2008) Elephants as agents of habitat creation for small vertebrates at the patch scale. Ecology 89:26–33

    Article  Google Scholar 

  49. Ripple WJ, Newsome TM, Wolf C et al (2015) Collapse of the world’s largest herbivores. Sci Adv 1:e1400103–e1400103. https://doi.org/10.1126/sciadv.1400103

    Article  PubMed  PubMed Central  Google Scholar 

  50. Ross D, Ketterings Q (1995) Recommended soil tests for determining exchange capacity. In: Sims JT, Wolf A (eds) Recommended soil testing procedures for the northeastern United States. Northeastern Regional Bulletin #493. Ag Experiment Station, University of Delaware, Newark, pp 62–69

  51. Ruess RW, Seagle SW (1994) Landscape patterns in soil microbial processes in the Serengeti National Park, Tanzania. Ecology 75:892–904. https://doi.org/10.2307/1939414

    Article  Google Scholar 

  52. Schulte E, Hopkins B (1996) Estimation of soil organic matter by weight loss-on ignition. In: Magdoff FR, Tabatabai MA, Hanlon EA Jr (eds) Soil organic matter: analysis and interpretation. (ed) Special publication No. 46. Soil Sci. Soc. Am., Madison, WI, pp 21–32

  53. Sensenig RL, Demment MW, Laca EA (2010) Allometric scaling predicts preferences for burned patches in a guild of East African grazers. Ecology 91:2898–2907

    Article  Google Scholar 

  54. Sensenig RL, Kimuyu DK, Ruiz Guajardo JC et al (2017) Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species. Ecology 98:1455–1464

    Article  Google Scholar 

  55. Singer FJ, Schoenecker KA (2003) Do ungulates accelerate or decelerate nitrogen cycling? For Ecol Manag 181:189–204. https://doi.org/10.1016/S0378-1127(03)00133-6

    Article  Google Scholar 

  56. Smith FA, Doughty CE, Malhi Y et al (2016a) Megafauna in the Earth system. Ecography 39:99–108. https://doi.org/10.1111/ecog.02156

    Article  Google Scholar 

  57. Smith FA, Hammond JI, Balk MA et al (2016b) Exploring the influence of ancient and historic megaherbivore extirpations on the global methane budget. Proc Natl Acad Sci 113:874–879. https://doi.org/10.1073/pnas.1502547112

    CAS  Article  PubMed  Google Scholar 

  58. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246. https://doi.org/10.1641/0006-3568(2001)051%5b0235:MFATSO%5d2.0.CO;2

    Article  Google Scholar 

  59. Stock WD, Bond WJ, van de Vijver CADM (2010) Herbivore and nutrient control of lawn and bucnh grass distributions in a Southern African savanna. Plant Ecol 206:15–27

    Article  Google Scholar 

  60. Subalusky AL, Dutton CL, Rosi-Marshall EJ, Post DM (2015) The hippopotamus conveyor belt: vectors of carbon and nutrients from terrestrial grasslands to aquatic systems in sub-Saharan Africa. Freshw Biol 60:512–525. https://doi.org/10.1111/fwb.12474

    CAS  Article  Google Scholar 

  61. Verweij RJT, Verrelst J, Loth PE et al (2006) Grazing lawns contribute to the subsistence of mesoherbivores on dystrophic savannas. Oikos 114:108–116

    Article  Google Scholar 

  62. Waldram MS, Bond WJ, Stock WD (2008) Ecological engineering by a mega-grazer: white rhino impacts on a South African savanna. Ecosystems 11:101–112. https://doi.org/10.1007/s10021-007-9109-9

    Article  Google Scholar 

  63. Young TP, Patridge N, Macrae A (1995) Long-term glades in Acacia bushland and their edge effects in Laikipia, Kenya. Ecol Appl 5:97–108. https://doi.org/10.2307/1942055

    Article  Google Scholar 

  64. Young HS, McCauley DJ, Helgen KM et al (2013) Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101:1030–1041. https://doi.org/10.1111/1365-2745.12096

    Article  PubMed  PubMed Central  Google Scholar 

  65. Zhao W, Chen S-P, Han X-G, Lin G-H (2009) Effects of long-term grazing on the morphological and functional traits of Leymus chinensis in the semiarid grassland of Inner Mongolia, China. Ecol Res 24:99–108. https://doi.org/10.1007/s11284-008-0486-0

    Article  Google Scholar 

Download references

Acknowledgements

For invaluable field support and advice we thank Douglas Branch, Jennifer Guyton, Francis Joyce, Margaret Kinnaird, Peter Lokeny, John Naisikie Mantas, Matthew Snider, the Kenya Wildlife Service, the Kenya National Commission for Science, Technology and Innovation, the Mpala Research Centre, National Museums of Kenya, Tristan Nuñez, Everlyn Ndinda, Noelia Solano, Hillary Young, Truman Young, Michelle and Ian Warrington. We also thank three anonymous reviewers for valuable feedback that greatly improved this manuscript. Funding for this work was provided by the National Science Foundation (IRFP OISE #1064649 and DEB #1146247).

Author information

Affiliations

Authors

Contributions

DJM, JSB, JMG, MO, WDN, TED, MEP, and JN conceived and designed the experiments. DJM and LFH conducted fieldwork. DJM and SIG analyzed the data. DJM and SIG wrote the manuscript; all other authors edited the manuscript.

Corresponding author

Correspondence to Douglas J. McCauley.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Communicated by Joanna E. Lambert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 9371 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McCauley, D.J., Graham, S.I., Dawson, T.E. et al. Diverse effects of the common hippopotamus on plant communities and soil chemistry. Oecologia 188, 821–835 (2018). https://doi.org/10.1007/s00442-018-4243-y

Download citation

Keywords

  • Exclosure
  • Grazing lawn
  • Megaherbivore
  • Vegetation structure
  • Nutrient cycling