Abstract
Hippopotami (hippos) are ecosystem engineers that subsidize aquatic ecosystems through the transfer of organic matter and nutrients from their terrestrial grazing, with potentially profound effects on aquatic biogeochemistry. We examined the influence of hippo subsidies on biogeochemical cycling in pools of varying hydrology and intensity of hippo use in the Mara River of Kenya. We sampled upstream, downstream, and at the surface and bottom of pools of varying volume, discharge, and hippo numbers, both before and after flushing flows. The product of hippo number and water residence time served as an index of the influence of hippo subsidies (hippo subsidy index, HSI) on aquatic biogeochemistry. Low-HSI hippo pools remained oxic between flushing flows and could be a source or sink for nutrients. High-HSI hippo pools quickly became anoxic between flushing flows and exported nutrients and byproducts of anaerobic microbial metabolism, including high concentrations of total ammonia nitrogen, hydrogen sulfide, and methane. Medium-HSI hippo pools were more similar to high-HSI hippo pools but with lower concentrations of reduced substances. Episodic high discharge events flushed pools and reset them to the oxic state. Transitions from oxic to anoxic states depended on water residence time, with faster transitions to anoxia in pools experiencing smaller flushing flows. Frequent shifts between these alternative oxic and anoxic states create heterogeneity in space and time in pools as well as in downstream receiving waters. In river systems where the influence of hippos on water quality is a concern, maintaining the natural flow regime, including flushing flows, ameliorates impacts of hippos.
Similar content being viewed by others
References
APHA. 2006. Standard methods for the examination of water & wastewater. Washington, DC: American Public Health Association.
Atkinson CL, Capps KA, Rugenski AT, Vanni MJ. 2016. Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev 92:2003–23.
Bartzke GS, Ogutu JO, Mukhopadhyay S, Mtui D, Dublin HT, Piepho H-P. 2018. Rainfall trends and variation in the Maasai Mara ecosystem and their implications for animal population and biodiversity dynamics. PLoS One 13:e0202814.
Bastviken D. 2009. Methane. In: Likens GE, Ed. Encyclopedia of inland waters. Oxford: Academic Press. p 783–805.
Burkholder J, Libra B, Weyer P, Heathcote S, Kolpin D, Thorne PS, Wichman M. 2007. Impacts of waste from concentrated animal feeding operations on water quality. Environ Health Perspect 115:308–12.
Burkholder JM, Mallin MA, Glasgow HB, Larsen LM, McIver MR, Shank GC, Deamer-Melia N, Briley DS, Springer J, Touchette BW, Hannon EK. 1997. Impacts to a coastal river and estuary from rupture of a large swine waste holding lagoon. J Environ Qual 26:1451–66.
Chew Shit F, Ho L, Ong Tan F, Wong Wai P, Ip Yuen K. 2005. The African Lungfish, Protopterus dolloi, detoxifies ammonia to urea during environmental ammonia exposure. Physiol Biochem Zool 78:31–9.
Conley DJ, Carstensen J, Vaquer-Sunyer R, Duarte CM. 2009. Ecosystem thresholds with hypoxia. Hydrobiologia 629:21–9.
Dawson J, Pillay D, Roberts PJ, Perissinotto R. 2016. Declines in benthic macroinvertebrate community metrics and microphytobenthic biomass in an estuarine lake following enrichment by hippo dung. Sci Rep 6:37359.
Dutton CL, Subalusky AL, Hamilton SK, Bayer EC, Njoroge L, Rosi EJ, Post DM. 2020. Data for: alternative biogeochemical states of river pools mediated by hippo use and flow variability. Mendeley Data.
Dutton CL, Subalusky AL, Hamilton SK, Rosi EJ, Post DM. 2018. Organic matter loading by hippopotami causes subsidy overload resulting in downstream hypoxia and fish kills. Nat Commun 9:1951.
Ehrenfeld JG. 2010. Ecosystem consequences of biological invasions. In: Futuyma DJ, Shafer HB, Simberloff D, Eds. Annual review of ecology, evolution, and systematics, Vol. 41. Palo Alto: Annual Reviews. p 59–80.
Ellis PS, Shabani AMH, Gentle BS, McKelvie ID. 2011. Field measurement of nitrate in marine and estuarine waters with a flow analysis system utilizing on-line zinc reduction. Talanta 84:98–103.
Eltschlager KK, Hawkins JW, Ehler WC, Baldassare F. 2001. Technical measures for the investigation and mitigation of fugitive methane hazards in areas of coal mining. Washington, DC: U.S. Department of the Interior.
Friedrich J, Janssen F, Aleynik D, Bange HW, Boltacheva N, Çagatay MN, Dale AW, Etiope G, Erdem Z, Geraga M, Gilli A, Gomoiu MT, Hall POJ, Hansson D, He Y, Holtappels M, Kirf MK, Kononets M, Konovalov S, Lichtschlag A, Livingstone DM, Marinaro G, Mazlumyan S, Naeher S, North RP, Papatheodorou G, Pfannkuche O, Prien R, Rehder G, Schubert CJ, Soltwedel T, Sommer S, Stahl H, Stanev EV, Teaca A, Tengberg A, Waldmann C, Wehrli B, Wenzhöfer F. 2014. Investigating hypoxia in aquatic environments: diverse approaches to addressing a complex phenomenon. Biogeosciences 11:1215–59.
GLOWS. 2007. Water quality baseline assessment report (WQBAR), Mara River Basin, Kenya-Tanzania. Miami: Global Water for Sustainability Program, Florida International University.
Golterman HL, Clymo RS. 1969. Methods for chemical analysis of fresh waters. Oxford: International Biological Programme by Blackwell Scientific.
Groffman PM, Baron JS, Blett T, Gold AJ, Goodman I, Gunderson LH, Levinson BM, Palmer MA, Paerl HW, Peterson GD, Poff NL, Rejeski DW, Reynolds JF, Turner MG, Weathers KC, Wiens J. 2006. Ecological thresholds: the key to successful environmental management or an important concept with no practical application? Ecosystems 9:1–13.
Hamilton SK, Ostrom NE. 2007. Measurement of the stable isotope ratio of dissolved N2 in 15 N tracer experiments. Limnol Oceanogr Methods 5:233–40.
Holgerson MA, Raymond PA. 2016. Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat Geosci 9:222.
Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70.
Hooda PS, Edwards AC, Anderson HA, Miller A. 2000. A review of water quality concerns in livestock farming areas. Sci Total Environ 250:143–67.
Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35.
Hosomi M, Sudo R. 1986. Simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulfate digestion. Int J Environ Stud 27:267–75.
Jäntti H, Hietanen S. 2012. The effects of hypoxia on sediment nitrogen cycling in the Baltic Sea. Ambio 41:161–9.
Kanga EM, Ogutu JO, Olff H, Santema P. 2011. Population trend and distribution of the Vulnerable common hippopotamus Hippopotamus amphibius in the Mara Region of Kenya. Oryx 45:20–7.
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.
Kilham P. 1982. The effect of hippopotamuses on potassium and phosphate ion concentrations in an African Lake. Am Midl Nat 108:202–5.
Kitchell JF, O’Neill RV, Webb D, Gallepp GW, Bartell SM, Koonce JF, Ausmus BS. 1979. Consumer regulation of nutrient cycling. BioScience 29:28–34.
Lewison RL, Oliver W, Subgroup ISHS. 2008. Hippopotamus amphibius. The IUCN Red List of Threatened Species 2008: e.T10103A3163790.
Loong AM, Tan JYL, Wong WP, Chew SF, Ip YK. 2007. Defense against environmental ammonia toxicity in the African lungfish, Protopterus aethiopicus: bimodal breathing, skin ammonia permeability and urea synthesis. Aquat Toxicol 85:76–86.
Lovley DR, Phillips EJP. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–40.
LVBC, Wwf-Esarpo. 2010. Assessing reserve flows for the Mara River, Kenya and Tanzania. Kisumu: Lake Victoria Basin Commission of the East African Community.
Masese FO, Abrantes KG, Gettel GM, Bouillon S, Irvine K, McClain ME. 2015. Are large herbivores vectors of terrestrial subsidies for riverine food webs? Ecosystems 18:686–706.
McCauley DJ, Dawson TE, Power ME, Finlay JC, Ogada M, Gower DB, Caylor K, Nyingi WD, Githaiga JM, Nyunja J, Joyce FH, Lewison RL, Brashares JS. 2015. Carbon stable isotopes suggest that hippopotamus-vectored nutrients subsidize aquatic consumers in an East African river. Ecosphere 6:1–11.
McCauley DJ, Graham SI, Dawson TE, Power ME, Ogada M, Nyingi WD, Githaiga JM, Nyunja J, Hughey LF, Brashares JS. 2018. Diverse effects of the common hippopotamus on plant communities and soil chemistry. Oecologia 188:821–35.
McClain ME. 2013. Balancing water resources development and environmental sustainability in Africa: a review of recent research findings and applications. Ambio 42:549–65.
McClain ME, Subalusky AL, Anderson EP, Dessu SB, Melesse AM, Ndomba PM, Mtamba JOD, Tamatamah RA, Mligo C. 2014. Comparing flow regime, channel hydraulics, and biological communities to infer flow–ecology relationships in the Mara River of Kenya and Tanzania. Hydrol Sci J 59:801–19.
McNeil BI, Sasse TP. 2016. Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle. Nature 529:383.
Mermillod-Blondin F, Rosenberg R. 2006. Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquat Sci 68:434–42.
Mnaya B, Mtahiko MGG, Wolanski E. 2017. The Serengeti will die if Kenya dams the Mara River. Oryx 51:581–3.
Murphy J, Riley JP. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27:31–6.
Mwanake RM, Gettel GM, Aho KS, Namwaya DW, Masese FO, Butterbach-Bahl K, Raymond PA. 2019. Land use, not stream order, controls N2O concentration and flux in the Upper Mara River Basin, Kenya. J Geophys Res Biogeosci 124:3491–506.
Naiman RJ. 1988. Animal Influences on Ecosystem Dynamics. BioScience 38:750–2.
Naqvi SWA, Bange HW, Farias L, Monteiro PMS, Scranton MI, Zhang J. 2010. Marine hypoxia/anoxia as a source of CH4 and N2O. Biogeosciences 7:2159–90.
Osborn SG, Vengosh A, Warner NR, Jackson RB. 2011. Methane contamination of drinking water accompanying gas-well drilling and hydraulic fracturing. Proc Natl Acad Sci 108:8172–6.
R Core Team. 2018. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Rabalais NN. 2002. Nitrogen in aquatic ecosystems. AMBIO: A Journal of the Human Environment 31: 102-112.
Randall DJ, Tsui TKN. 2002. Ammonia toxicity in fish. Mar Pollut Bull 45:17–23.
Schmitz OJ, Wilmers CC, Leroux SJ, Doughty CE, Atwood TB, Galetti M, Davies AB, Goetz SJ. 2018. Animals and the zoogeochemistry of the carbon cycle. Science 362:3213.
Sirota J, Baiser B, Gotelli NJ, Ellison AM. 2013. Organic-matter loading determines regime shifts and alternative states in an aquatic ecosystem. Proc Natl Acad Sci 110:7742–7.
Smith LL, Broderius SJ, USEPA. 1976. Effect of hydrogen sulfide on fish and invertebrates. Duluth, Minn.: U.S. Environmental Protection Agency, Office of Research and Development, Environmental Research Laboratory.
Stears K, McCauley DJ, Finlay JC, Mpemba J, Warrington IT, Mutayoba BM, Power ME, Dawson TE, Brashares JS. 2018. Effects of the hippopotamus on the chemistry and ecology of a changing watershed. Proc Natl Acad Sci 115:E5028.
Stommel C, Hofer H, East ML. 2016. The effect of reduced water availability in the great Ruaha River on the vulnerable common hippopotamus in the Ruaha National Park, Tanzania. PLoS One 11:e0157145.
Stookey LL. 1970. Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42:779–81.
Subalusky AL, Dutton CL, Njoroge L, Rosi EJ, Post DM. 2018. Organic matter and nutrient inputs from large wildlife influence ecosystem function in the Mara River, Africa. Ecology 99:2558–74.
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 60:512–25.
Subalusky AL, Post DM. 2018. Context dependency of animal resource subsidies. Biol Rev 94:517–38.
Testa JM, Kemp WM. 2012. Hypoxia-induced shifts in nitrogen and phosphorus cycling in Chesapeake Bay. Limnol Oceanogr 57:835–50.
Vanni MJ. 2002. Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–70.
Wolanski E, Gereta E. 1999. Oxygen cycle in a hippo pool, Serengeti National Park, Tanzania. Afr J Ecol 37:419–23.
Zar J. 2010. Biostatistical analysis, Vol. 1. 5th edn. Upper Saddle River: Prentice Hall. pp 389–94.
Acknowledgements
We thank the Government of Kenya and the National Council for Science and Technology for authorizing this research (NCST/RRI/12/1/BS-011/25). The National Museums of Kenya provided assistance with permits and logistics. Support in the field was provided by Brian Heath and the Mara Conservancy. Paul Geemi, James Landefeld and Jordan Chancellor provided field assistance. Access to the hippo pools was facilitated by Tarquin and Lippa Wood, Amani Mara Camp, and the wardens of the Maasai Mara National Reserve, the Mara Conservancy and Naboisho Conservancy.
Funding
Funding was provided by US National Science Foundation Grants to DMP and EJR (NSF DEB 1354053, 1354062, and 1753727); a Grant from the National Geographic Society to DMP; Grants from the Yale Tropical Resources Institute, the Yale Institute for Biospheric Studies and the Yale MacMillan Center for International and Area Studies to CLD; and a fellowship from the Robert and Patricia Switzer Foundation to ALS.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Author Contributions
CLD, ALS, SKH, EJR, and DMP conceived of or designed the study; CLD, ALS, SKH, ECJ, LN, EJR, and DMP Performed the research; CLD and SKH analyzed the data; and CLD, ALS, SKH, ECJ, LN, EJR, and DMP wrote the paper.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dutton, C.L., Subalusky, A.L., Hamilton, S.K. et al. Alternative Biogeochemical States of River Pools Mediated by Hippo Use and Flow Variability. Ecosystems 24, 284–300 (2021). https://doi.org/10.1007/s10021-020-00518-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-020-00518-3