Animal-Mediated Nutrient Cycling in Aquatic Ecosystems of the Cuatro Ciénegas Basin

  • Eric K. Moody
  • Evan W. Carson
  • Jessica R. Corman
  • Hector Espinosa-Pérez
Part of the Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis book series (CUCIBA)


Consumers can alter nutrient cycling and create biogeochemical hotspots by excreting nutrients such as nitrogen and phosphorus at varying rates and stoichiometric ratios. Variation in these rates and ratios is in turn driven by traits such as body size, diet, and nutrient assimilation efficiency. These traits often vary considerably among and within species. As aquatic ecosystems in the Cuatro Ciénegas Basin are nutrient-poor, animals may play a large role in recycling key nutrients such as nitrogen (N) and phosphorus (P). We investigated this question by studying nutrient excretion rates of snails (Mexithauma quadripaludium and Nymphophilus minckleyi), a poeciliid fish (Gambusia marshi), and two cyprinodontid fishes (Cyprinodon atrorus and C. bifasciatus) over a variety of environments. Snails were collected from oncolites in the Río Mesquites, C. atrorus were measured in Laguna Intermedia, C. bifasciatus were measured in Poza La Becerra, and G. marshi were measured at nine sites around the basin as well as in laboratory experiments with fish from Poza La Becerra and Los Hundidos. We found substantial variation in nutrient excretion rates both among and within species and suggest that differences in diet and feeding rate could explain much of this variation. We also calculated the potential contribution of recycled P to supporting oncolite production and found that snails are likely not a major source of P to primary production in oncolites. Finally, we discuss how changes in these environments may lead to shifts in consumer-mediated nutrient recycling.


Aquatic ecosystem Fishes Phosphorus Nutrient cycling Snail 


  1. Allgeier JE, Wenger SJ, Rosemond AD et al (2015) Metabolic theory and taxonomic identity predict nutrient recycling in a diverse food web. PNAS 112:E2640–E2647CrossRefGoogle Scholar
  2. Araújo MS, Langerhans RB, Giery ST et al (2014) Ecosystem fragmentation drives increased diet variation in an endemic livebearing fish of the Bahamas. Ecol Evol 4:3298–3308CrossRefGoogle Scholar
  3. Arnold ET (1972) Behavioral ecology of two pupfishes (Cyprinodontidae, genus Cyprinodon) from northern Mexico. Ph.D. dissertation, Arizona State University, TempeGoogle Scholar
  4. Atkinson CL, Vaughn CC, Forshay KJ et al (2013) Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology 94:1359–1369CrossRefGoogle Scholar
  5. Atkinson CL, Capps KA, Rugenski AT et al (2017) Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev 92:2003–2023CrossRefGoogle Scholar
  6. Carson EW (2009) Threatened fishes of the world: Cyprinodon bifasciatus Miller 1968 (Cyprinodontidae). Environ Biol Fish 86:445–446CrossRefGoogle Scholar
  7. Carson EW, Dowling TE (2006) Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorus and C. bifasciatus. Mol Ecol 15:667–679CrossRefGoogle Scholar
  8. Carson EW, Elser JJ, Dowling TE (2008) Importance of exogenous selection in a fish hybrid zone: insights from reciprocal transplant experiments. Copeia 2008:794–800CrossRefGoogle Scholar
  9. Corman JR, Poret-Peterson AT, Uchitel A et al (2016) Interaction between lithification and resource availability in the microbialites of Río Mesquites, Cuatro Ciénegas, Mexico. Geobiology 14:176–189CrossRefGoogle Scholar
  10. Devine JA, Vanni MJ (2002) Spatial and seasonal variation in nutrient excretion by benthic invertebrates in a eutrophic reservoir. Freshw Biol 47:1107–1121CrossRefGoogle Scholar
  11. Dinger EC, Cohen AE, Hendrickson DA et al (2005) Aquatic invertebrates of Cuatro Ciénegas, Coahuila, Mexico: natives and exotics. Southwest Nat 50:237–281CrossRefGoogle Scholar
  12. Doughty CE, Roman J, Faurby S et al (2016) Global nutrient transport in a world of giants. PNAS 113:868–873CrossRefGoogle Scholar
  13. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751CrossRefGoogle Scholar
  14. Elser JJ, Elser MM, MacKay NA et al (1988) Zooplankton-mediated transitions between N-and P-limited algal growth. Limnol Oceanogr 33:1–14CrossRefGoogle Scholar
  15. Elser JJ, Schampel JH, Garcia-Pichel F et al (2005a) Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities. Freshw Biol 50:1808–1825CrossRefGoogle Scholar
  16. Elser JJ, Schampel JH, Kyle M et al (2005b) Response of grazing snails to phosphorus enrichment of modern stromatolitic microbial communities. Freshw Biol 50:1826–1835CrossRefGoogle Scholar
  17. Garcia-Pichel F, Al-Horani FA, Farmer JD et al (2004) Balance between microbial calcification and metazoan bioerosion in modern stromatolitic oncolites. Geobiology 2:49–57CrossRefGoogle Scholar
  18. Garrett P (1970) Phanerozoic stromatolites: noncompetitive ecologic restriction by grazing and burrowing animals. Science 169:171–173CrossRefGoogle Scholar
  19. Hernández A, Espinosa-Pérez HS, Souza V (2017) Trophic analysis of the fish community in the Ciénega Churince, Cuatro Ciénegas, Coahuila. PeerJ 5:e3637CrossRefGoogle Scholar
  20. Hershler R (1984) The hydrobiid snails (Gastropoda: Rissoacea) of the Cuatro Cienegas basin: systematic relationships and ecology of a unique fauna. J Arizona Nevada Acad Sci 19:61–76Google Scholar
  21. Kodric-Brown A (1988) Effect of population density, size of habitat, and oviposition substrate on the breeding system of pupfish (Cyprinodon pecosensis). Ethology 77:28–43CrossRefGoogle Scholar
  22. Lee ZMP, Poret-Peterson AT, Siefert JL et al (2017) Nutrient stoichiometry shapes microbial community structure in an evaporitic shallow pond. Front Microbiol 8:949CrossRefGoogle Scholar
  23. McIntyre PB, Flecker AS, Vanni MJ et al (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots. Ecology 89:2335–2346CrossRefGoogle Scholar
  24. Meffe GK (1985) Life history patterns of Gambusia marshi (Poeciliidae) from Cuatro Cienegas, Mexico. Copeia 1985:898–905CrossRefGoogle Scholar
  25. Minckley WL (1962) Two new species of fishes of the genus Gambusia (Poeciliidae) from northeastern Mexico. Copeia 1962:391–396CrossRefGoogle Scholar
  26. Minckley WL (1969) Environments of the bolsόn of Cuatro Cienegas, Coahuila, Mexico. Texas Western Press, University of Texas Press, El PasoGoogle Scholar
  27. Minckley WL (1992) Three decades near Cuatro Ciénegas, México: photographic documentation and a plea for area conservation. J Arizona Nevada Acad Sci 26:89–118Google Scholar
  28. Minckley WL, Cole GA (1968) Preliminary limnologic information on waters of the Cuatro Cienegas Basin, Coahuila, Mexico. Southwest Nat 13:421–431CrossRefGoogle Scholar
  29. Moody EK, Carson EW, Corman JR et al (2018) Consumption explains intraspecific variation in nutrient recycling stoichiometry in a desert fish. Ecology 99:1552–1561CrossRefGoogle Scholar
  30. Moody EK, Lozano-Vilano ML (2018) Predation drives morphological convergence in the Gambusia panuco species group among lotic and lentic habitats. J Evol Biol 31:491–501CrossRefGoogle Scholar
  31. Moody EK, Corman JR, Elser JJ et al (2015) Diet composition affects the rate and N: P ratio of fish excretion. Freshw Biol 60:456–465CrossRefGoogle Scholar
  32. Riding R (2000) Microbial carbonates: the geological record of calcified bacterial–algal mats and biofilms. Sedimentology 47:179–214CrossRefGoogle Scholar
  33. Small GE, Pringle CM, Pyron M et al (2011) Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams. Ecology 92:386–397CrossRefGoogle Scholar
  34. Souza V, Espinosa-Asuar L, Escalante AE et al (2006) An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. PNAS 103:6565–6570CrossRefGoogle Scholar
  35. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136:209–229CrossRefGoogle Scholar
  36. Subalusky AL, Dutton CL, Rosi EJ et al (2017) Annual mass drownings of the Serengeti wildebeest migration influence nutrient cycling and storage in the Mara River. PNAS 114:7647–7652CrossRefGoogle Scholar
  37. Tobler M, Carson EW (2010) Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes. J Evol Biol 23:1475–1489CrossRefGoogle Scholar
  38. Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370CrossRefGoogle Scholar
  39. Vanni MJ, McIntyre PB (2016) Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis. Ecology 97:3460–3471CrossRefGoogle Scholar
  40. Vanni MJ, Boros G, McIntyre PB (2013) When are fish sources vs. sinks of nutrients in lake ecosystems? Ecology 94:2195–2206CrossRefGoogle Scholar
  41. Whiles MR, Hall RO, Dodds WK et al (2013) Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16:146–157CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Eric K. Moody
    • 1
  • Evan W. Carson
    • 2
  • Jessica R. Corman
    • 3
  • Hector Espinosa-Pérez
    • 4
  1. 1.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA
  2. 2.U.S. Fish and Wildlife ServiceBay-Delta Fish and Wildlife OfficeSacramentoUSA
  3. 3.University of NebraskaSchool of Natural ResourcesLincolnUSA
  4. 4.La Universidad Autónoma de MexicoColección Nacional de PecesMexico D.F.Mexico

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