, Volume 179, Issue 1, pp 117–127 | Cite as

Reciprocal transplant reveals trade-off of resource quality and predation risk in the field

  • Clifton B. Ruehl
  • Joel C. Trexler
Population ecology - Original research


Balancing trade-offs between avoiding predators and acquiring food enables animals to maximize fitness. Quantifying their relative contribution to vital rates in nature is challenging because predator abundance and nutrient enrichment are often confounded. We employed a reciprocal transplant study design to separate these confounded effects on growth and reproduction of snails at wetland sites along a gradient of predator threats and phosphorus (P) enrichment associated with a canal. We held snails in mesh bags that allowed the passage of waterborne predator cues and fed them local or transplanted periphyton. Molluscivores were more abundant near the canal, and snails tethered near the canal suffered 33 % greater mortality than those tethered far from it (far sites). The greatest difference in snail growth rates was at the far sites where growth on far periphyton was 48 % slower than on P-enriched (near canal) periphyton. Close proximity to the canal reduced growth on near periphyton by 21 % compared to growth on the same periphyton far from the canal; there was no difference in growth rate on either periphyton type when snails were raised near the canal. Snails laid 81 % more egg masses at far sites than at near sites, regardless of periphyton origin. Top–down and bottom–up processes were elevated near the canal, and their effects canceled on growth, but not reproduction. Phenotypic trade-offs such as these may explain why some taxa show little response to nutrient enrichment, compared to others, or that the effects of nutrient enrichment may be context dependent.


Nonlethal Predator–prey Phosphorus enrichment Pulmonate snails Everglades 



We thank J. Dummit, L. Harrison, L. Jiang, R. Lomax, A. Obaza, A. Parker, A. Taylor, and A. Williams, F. Tobias and P. Parker for field and lab assistance. The Everglades Foundation and the FIU graduate school provided financial support to CBR. Tom Fink at East Carolina University kindly provided access to a microscope for soft algae counts. Field data were provided by ENP-FIU Cooperative Agreement H5000060104, Task numbers J5284060023 and J5297070024 to JCT. This material was developed with help from the FCE-LTER program under NSF Grant No. DBI-0620409 and is contribution number 721 from the Southeast Environmental Research Center at FIU.


  1. Abrams PA (1984) Foraging time optimization and interactions in food webs. Am Nat 124:80–96CrossRefGoogle Scholar
  2. Benard MF, Fordyce JA (2003) Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84:68–78CrossRefGoogle Scholar
  3. Brönmark C, Lakowitz T, Nilsson PA, Ahlgren J, Lennartsdotter C, Hollander J (2012) Costs of inducible defence along a resource gradient. PLoS One 7:1–7CrossRefGoogle Scholar
  4. Browder JA, Gleason PJ, Swift DR (1994) Periphyton in the Everglades: spatial variation, environmental correlates, and ecological implications. In: Davis SM, Ogden JC (eds) Everglades: the ecosystem and its restoration. St. Lucie Press, Delray Beach, pp 379–418Google Scholar
  5. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014CrossRefGoogle Scholar
  6. Chase JM (1999) To grow or to reproduce? The role of life-history plasticity in food web dynamics. Am Nat 154:571–586CrossRefPubMedGoogle Scholar
  7. Clausen J, Keck DD, Hiesey W (1940) Experimental studies on the nature of species I: effects of varied environments on western North American plants. Carnegie Institution of Washington, BaltimoreGoogle Scholar
  8. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201CrossRefPubMedGoogle Scholar
  9. Cross WF, Wallce JB, Rosemond AD, Eggert SL (2006) Whole-system nutrient enrichment increases secondary production in a detritus-based ecosystem. Ecology 87:1556–1565CrossRefPubMedGoogle Scholar
  10. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951CrossRefPubMedGoogle Scholar
  11. Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  12. Dorn NJ, Trexler JC (2007) Crayfish assemblage shifts in a large drought-prone wetland: the roles of hydrology and competition. Freshw Biol 52:2399–2411CrossRefGoogle Scholar
  13. Duever MJ, Meeder JF, Meeder LC, McCollom JM (1994) The climate of South Florida and its role in shaping the Everglades ecosystem. In: Davis SM, Ogden JC (eds) The ecosystem and its restoration. St. Lucie Press, Boca Raton, pp 225–248Google Scholar
  14. Elser JJ et al (2005) Response of grazing snails to phosphorus enrichment of modern stromatolitic microbial communities. Freshw Biol 50:1826–1835CrossRefGoogle Scholar
  15. Ewe SML, Gaiser EE, Childers DL, Iwaniec D, Rivera-Monroy VH, Twilley RR (2006) Spatial and temporal patterns of aboveground net primary productivity (ANPP) along two freshwater-estuarine transects in the Florida Coastal Everglades. Hydrobiologia 569:459–474CrossRefGoogle Scholar
  16. Forrester GE, Dudley TL, Grimm NB (1999) Trophic interactions in open systems: effects of predators and nutrients on stream food chains. Limnol Oceanogr 44:1187–1197CrossRefGoogle Scholar
  17. Frost PC, Stelzer RS, Lamberti GA, Elser JJ (2002) Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C:N: P ratios in lentic and lotic habitats. J North Am Benthol Soc 21:515–528CrossRefGoogle Scholar
  18. Gaiser EE, Trexler JC, Richards JH, Childers DL, Lee D, Edwards AL, Scinto LJ, Jayachandran K, Noe GB, Jones RD (2005) Cascading ecological effects of low-level phosphorus enrichment in the Florida Everglades. J Environ Qual 34:717–723CrossRefPubMedGoogle Scholar
  19. Gaiser EE, Richards JH, Trexler JC, Jones RD, Childers DL (2006) Periphyton responses to eutrophication in the Florida Everglades: cross-system patterns of structural and compositional change. Limnol Oceanogr 51:617–630CrossRefGoogle Scholar
  20. Gaiser EE, McCormick PV, Hagerthey SE (2011) Landscape patterns of periphyton in the Florida Everglades. Crit Rev Environ Sci Technol 41:92–120CrossRefGoogle Scholar
  21. Geddes P, Trexler JC (2003) Uncoupling of omnivore-mediated positive and negative effects on periphyton mats. Oecologia 136:585–595CrossRefPubMedGoogle Scholar
  22. Gérard C, Carpentier A, Paillisson JM (2008) Long-term dynamics and community structure of freshwater gastropods exposed to parasitism and other environmental stressors. Freshw Biol 53:470–484CrossRefGoogle Scholar
  23. Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856–1862CrossRefGoogle Scholar
  24. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588CrossRefPubMedGoogle Scholar
  25. Hoang TC, Schuler LJ, Rogevich EC, Bachman PM, Rand GM, Frakes RA (2009) Copper release, speciation, and toxicity following multiple floodings of copper enriched agriculture soils: implications in Everglades restoration. Water Air Soil Pollut 199:79–93CrossRefGoogle Scholar
  26. Hoverman JT, Auld JR, Relyea RA (2005) Putting prey back together again, integrating predator-induced behavior, morphology, and life history. Oecologia 144:481–491CrossRefPubMedGoogle Scholar
  27. Johnson PTJ, Chase JM (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecol Lett 7:521–526CrossRefGoogle Scholar
  28. Jordan F, Coyne S, Trexler JC (1997) Sampling fishes in vegetated habitats: effects of habitat structure on sampling characteristics of the 1-m2 throw trap. Trans Am Fish Soc 126:1012–1020CrossRefGoogle Scholar
  29. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  30. McCormick PV, Shuford RBE, Rawlik PS (2004) Changes in macroinvertebrate community structure and function along a phosphorus gradient in the Florida Everglades. Hydrobiologia 529:113–132CrossRefGoogle Scholar
  31. Moran MD, Scheidler AR (2002) Effects and nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes. Oikos 98:116–124CrossRefGoogle Scholar
  32. Obaza AO, Ruehl CB (2013) Regressions for estimating gastropod biomass with multiple shell metrics. Malacologia 56:343–349CrossRefGoogle Scholar
  33. Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261CrossRefGoogle Scholar
  34. Parkos JJI, Trexler JC (2014) Origins of functional connectivity in a human-modified wetland landscape. Can J Fish Aquat Sci 71:1418–1429CrossRefGoogle Scholar
  35. Peacor SD, Werner EE (2004) Context dependence of non-lethal effects of a predator on prey growth. Isr J Zool 50:139–167CrossRefGoogle Scholar
  36. Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC (2008) Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89:2416–2425CrossRefPubMedGoogle Scholar
  37. Peckarsky BL, McIntosh AR, Álvarez M, Moslemi JM (2013) Nutrient limitation controls the strength of behavioral trophic cascades in high elevation streams Ecosphere, vol 4, part 110Google Scholar
  38. Pisani O, Scinto LJ, Munyon JW, Jaffe R (2015) The respiration of flocculent detrital organic matter (floc) is driven by phosphorus limitation and substrate quality in a subtropical wetland. Geoderma 241–242:272–278CrossRefGoogle Scholar
  39. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  40. Rand GM, Schuler LJ (2009) Aquatic risk assessment of metals in sediment from South Florida canals. Soil Sediment Contam 18:155–172CrossRefGoogle Scholar
  41. Rehage JS, Trexler JC (2006) Assessing the net effect of anthropogenic disturbance on aquatic communities in wetlands: community structure relative to distance from canals. Hydrobiologia 569:359–373CrossRefGoogle Scholar
  42. Relyea RA (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:541–554CrossRefGoogle Scholar
  43. Rosenzweig ML (1973) Exploitation in three trophic levels. Am Nat 107:275–294CrossRefGoogle Scholar
  44. Ruehl CB (2010) The interactive effects of predators, resources, and disturbance on freshwater snail populations from the Everglades. PhD dissertation. Florida International University, MiamiGoogle Scholar
  45. Ruehl CB, Trexler JC (2013) A suite of prey traits determine predator and nutrient enrichment effects in a tri-trophic food chain. Ecosphere 4:art75. doi: 10.1890/ES13-00065.1
  46. Sargeant BL, Gaiser EE, Trexler JC (2011) Indirect and direct controls of macroinvertebrates and small fish by abiotic factors and trophic interactions in the Florida Everglades. Freshw Biol 56:2334–2346CrossRefGoogle Scholar
  47. Sih A (1980) Optimal behavior: can foragers balance two conflicting demands. Science 210:1041–1043CrossRefPubMedGoogle Scholar
  48. Solorzano L, Sharp JH (1980) Determination of total dissolved phosphorus and particulate phosphorus in natural-waters. Limnol Oceanogr 25:754–757CrossRefGoogle Scholar
  49. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  50. Tibbets TM, Krist AC, Hall RO, Riley LA (2010) Phosphorus-mediated changes in life history traits of the invasive New Zealand mudsnail (Potamopyrgus antipodarum). Oecologia 163:549–559CrossRefPubMedGoogle Scholar
  51. Trexler JC, Gaiser EE, Kominoski JS, Sanchez J (2015) The role of periphyton mats in structuring consumer structure and function in calcareous wetlands: Lessons learned from the Everglades. In: Entry JA, Gottlieb AD, Jayachandrahan K, Ogram A (eds) Microbiology of the Everglades Ecosystem. CRC Press, Boca Raton, FL (in press)Google Scholar
  52. Turner AM (2004) Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions. Oikos 104:561–569CrossRefGoogle Scholar
  53. Turner AM, Montgomery SL (2003) Spatial and temporal scales of predator avoidance: experiments with fish and snails. Ecology 84:616–622CrossRefGoogle Scholar
  54. Turner AM, Trexler JC, Jordan CF, Jordan SJ, Geddes P, Chick JH, Loftus WF (1999) Targeting ecosystem features for conservation: standing crops in the Florida Everglades. Conserv Biol 13:898–911CrossRefGoogle Scholar
  55. Vymazal J (1995) Algae and element cycling in wetlands. CRC Press, Boca RatonGoogle Scholar
  56. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  57. Werner EE, Peacor SD (2006) Lethal and nonlethal predator effects on an herbivore guild mediated by system productivity. Ecology 87:347–361CrossRefPubMedGoogle Scholar
  58. Wootton JT, Power ME (1993) Productivity, consumers, and the structure of a river food chain. Proc Natl Acad Sci 90:1384–1387PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Biological SciencesFlorida International UniversityNorth MiamiUSA
  2. 2.Department of BiologyColumbus State UniversityColumbusUSA

Personalised recommendations