Oecologia

, Volume 173, Issue 3, pp 1023–1032 | Cite as

Trait-mediated indirect effects, predators, and disease: test of a size-based model

  • Christopher R. Bertram
  • Mark Pinkowski
  • Spencer R. Hall
  • Meghan A. Duffy
  • Carla E. Cáceres
Community ecology - Original research

Abstract

Increasing prevalence of wildlife disease accentuates the need to uncover drivers of epidemics. Predators can directly influence disease prevalence via density-mediated effects (e.g., culling infected hosts leading to reduced disease prevalence). However, trait-mediated indirect effects (TMIEs) of predators can also strongly influence disease—but predicting a priori whether TMIEs should increase or decrease disease prevalence can be challenging, especially since a single predator may elicit responses that have opposing effects on disease prevalence. Here, we pair laboratory experiments with a mechanistic, size-based model of TMIEs in a zooplankton host, fungal parasite, multiple predator system. Kairomones can either increase or decrease body size of the host Daphnia, depending on the predator. These changes in size could influence key traits of fungal disease, since infection risk and spore yield increase with body size. For six host genotypes, we measured five traits that determine an index of disease spread (R 0). Although host size and disease traits did not respond to kairomones produced by the invertebrate predator Chaoborus, cues from fish reduced body size and birth rate of uninfected hosts and spore yield from infected hosts. These results support the size model for fish; the birth and spore yield responses should depress disease spread. However, infection risk did not decrease with fish kairomones, thus contradicting predictions of the size model. Exposure to kairomones increased per spore susceptibility of hosts, countering size-driven decreases in exposure to spores. Consequently, synthesizing among the relevant traits, there was no net effect of fish kairomones on the R 0 metric. This result accentuates the need to integrate the TMIE-based response to predators among all key traits involved in disease spread.

Keywords

Daphnia Metschnikowia Chaoborus Host Parasite 

Notes

Acknowledgments

This research was supported by National Science Foundation grants DEB 0613510, 0614316, 1120804, and 1120316.

Supplementary material

442_2013_2673_MOESM1_ESM.doc (186 kb)
Supplementary material 1 (DOC 186 kb)

References

  1. Abrams P, Menge BA, Mittelbach GG, Spiller D, Yodzis P (1996) The role of indirect effects in food webs. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamic. Chapman and Hall, New York, pp 371–395CrossRefGoogle Scholar
  2. Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, OxfordGoogle Scholar
  3. Boersma M, Spaak P, De Meester L (1998) Predator-mediated plasticity in morphology, life history, and behavior in Daphnia: the uncoupling of responses. Am Nat 152:237–248PubMedCrossRefGoogle Scholar
  4. Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79:371–394CrossRefGoogle Scholar
  5. Cáceres CE, Knight CJ, Hall SR (2009) Predator-spreaders: predation can enhance parasite success in a planktonic host-parasite system. Ecology 90:2850–2858PubMedCrossRefGoogle Scholar
  6. Choisy M, Rohani P (2006) Harvesting can increase severity of wildlife disease epidemics. Proc R Soc B Biol Sci 273:2025–2034CrossRefGoogle Scholar
  7. Civitello DJ, Forys P, Johnson AP, Hall SR (2012) Chronic contamination decreases disease spread: a Daphnia-fungus-copper case study. Proc R Soc B Biol Sci 279:3146–3153CrossRefGoogle Scholar
  8. Civitello DJ, Penczykowski RM, Hite JL, Duffy MA, Hall SR (2013) Potassium stimulates fungal epidemics in Daphnia by increasing host and parasite reproduction. Ecology 94:380–388Google Scholar
  9. Coslovsky M, Richner H (2011) Predation risk affects offspring growth via maternal effects. Funct Ecol 25:878–888CrossRefGoogle Scholar
  10. Daly EW, Johnson PTJ (2011) Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165:1043–1050PubMedCrossRefGoogle Scholar
  11. Daszak P, Cunningham AA, Hyatt AD (2000) Wildlife ecology: emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  12. Decaestecker E, De Meester L, Ebert D (2002) In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proc Natl Acad Sci 99:5481–5485PubMedCrossRefGoogle Scholar
  13. Dobson AP, Foufopoulos J (2001) Emerging infectious pathogens in wildlife. Philos Trans R Soc Lond B 356:1001–1012CrossRefGoogle Scholar
  14. Duffy MA, Hall SR (2008) Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. Am Nat 171:499–510PubMedCrossRefGoogle Scholar
  15. Duffy MA, Sivars-Becker L (2007) Rapid evolution and ecological host-parasite dynamics. Ecol Lett 10:44–53PubMedCrossRefGoogle Scholar
  16. Duffy MA, Hall SR, Tessier AJ, Huebner M (2005) Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control? Limnol Oceanogr 50:412–420CrossRefGoogle Scholar
  17. Duffy MA, Housley JM, Penczykowski RM, Cáceres CE, Hall SR (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Funct Ecol 25:945–953CrossRefGoogle Scholar
  18. Dussaubat C, Brunet J-L, Higes M, Colbourne JK, Lopez J, Choi J-H, Martín-Hernádez R, Botías C, Cousin M, McDonnell C, Bonnet M, Belzunces LP, Moritz RF, Le Conte Y, Alaux C (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One 7(5):e37017. doi: 10.1371/journal.pone.0037017 PubMedCrossRefGoogle Scholar
  19. Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia [Internet]. National Center for Biotechnology Information, National Library of Medicine (US), Bethesda, MD. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books
  20. Hall SR, Duffy MA, Cáceres CE (2005) Selective predation and productivity jointly drive complex behavior in host-parasite systems. Am Nat 165:70–81PubMedCrossRefGoogle Scholar
  21. Hall SR, Tessier AJ, Duffy MA, Huebner M, Cáceres CE (2006) Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics. Ecology 87:1684–1695PubMedCrossRefGoogle Scholar
  22. Hall SR, Sivars-Becker L, Becker C, Duffy MA, Tessier AJ, Cáceres CE (2007) Eating yourself sick: transmission of disease as a function of foraging ecology. Ecol Lett 10:207–218PubMedCrossRefGoogle Scholar
  23. Hall SR, Becker CR, Simonis JL, Duffy MA, Tessier AJ, Cáceres CE (2009a) Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90:791–801PubMedCrossRefGoogle Scholar
  24. Hall SR, Knight CJ, Becker CR, Duffy MA, Tessier AJ, Cáceres CE (2009b) Quality matters: resource quality for hosts and the timing of epidemics. Ecol Lett 12:118–128PubMedCrossRefGoogle Scholar
  25. Hall SR, Simonis JL, Nisbet RM, Tessier AJ, Cáceres CE (2009c) Resource ecology of virulence in a planktonic host-parasite system: an explanation using dynamic energy budgets. Am Nat 174:149–162PubMedCrossRefGoogle Scholar
  26. Hall SR, Becker C, Duffy MA, Cáceres CE (2010a) Variation in resource acquisition and use among host clones creates key epidemiological trade-offs. Am Nat 176:557–565PubMedCrossRefGoogle Scholar
  27. Hall SR, Smyth R, Becker CR, Duffy MA, Knight CJ, MacIntyre S, Tessier AJ, Cáceres CE (2010b) Why are Daphnia in some lakes sicker? Disease ecology, habitat structure, and the plankton. Bioscience 60:363–375CrossRefGoogle Scholar
  28. Hall SR, Becker C, Duffy MA, Cáceres CE (2012) A power-efficiency tradeoff alters epidemiological relationships. Ecology 93:645–656PubMedCrossRefGoogle Scholar
  29. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (1999) Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–1510PubMedCrossRefGoogle Scholar
  30. Hatcher MJ, Dick JT, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1–19CrossRefGoogle Scholar
  31. Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem function. Am Nat 176:537–556PubMedCrossRefGoogle Scholar
  32. Hawlena D, Abramsky Z, Bouskila A (2010) Bird predation alters infestation of desert lizards by parasitic mites. Oikos 119:730–736CrossRefGoogle Scholar
  33. Hesse O, Engelbrecht W, Laforsch C, Wolinska J (2012) Fighting parasites and predators: how to deal with multiple threats? BMC Ecol 12:12. doi: 10.1186/1472-6785-12-12 PubMedCrossRefGoogle Scholar
  34. Holt RD, Roy M (2007) Predation can increase the prevalence of infectious disease. Am Nat 169:690–699PubMedCrossRefGoogle Scholar
  35. Johnson PTJ, Stanton DE, Preu ER, Forshay KJ, Carpenter SR (2006) Dining on disease: how interactions between infection and environment affect predation risk. Ecology 87:1973–1980PubMedCrossRefGoogle Scholar
  36. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498PubMedCrossRefGoogle Scholar
  37. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652PubMedCrossRefGoogle Scholar
  38. Kilpatrick AM (2011) Globalization, land use, and the emergence of West Nile virus. Science 334:323–327PubMedCrossRefGoogle Scholar
  39. Kooijman SALM (1993) Dynamic energy budgets in biological systems. Cambridge University Press, New YorkGoogle Scholar
  40. Lass S, Bittner K (2002) Facing multiple enemies: parasitised hosts respond to predator kairomones. Oecologia 132:344–349CrossRefGoogle Scholar
  41. Lynch M, Spitze K, Crease T (1989) The distribution of life-history variation in the Daphnia pulex complex. Evolution 43:1724–1736CrossRefGoogle Scholar
  42. Machacek J (1995) Inducibility of life-history changes by fish kairomone in various developmental stages of Daphnia. J Plankton Res 17:1513–1520CrossRefGoogle Scholar
  43. McCauley SJ, Rowe L, Fortin M-J (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048PubMedCrossRefGoogle Scholar
  44. Noonburg EG, Nisbet RM (2005) Behavioral and physiological responses to food availability and predation risk. Evol Ecol Res 7:89–104Google Scholar
  45. Ostfeld RS, Holt RD (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Front Ecol Environ 2:13–20CrossRefGoogle Scholar
  46. Overholt EP, Hall SR, Williamson CE, Meikle CK, Duffy MA, Cáceres CE (2012) Solar radiation decreases parasitism in Daphnia. Ecol Lett 15:47–54PubMedCrossRefGoogle Scholar
  47. Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol Lett 6:797–802CrossRefGoogle Scholar
  48. Pauwels K, Stoks R, De Meester L (2010) Enhanced anti-predator defense in the presence of food stress in the water flea Daphnia magna. Funct Ecol 24:322–329CrossRefGoogle Scholar
  49. Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci 98:3904–3908PubMedCrossRefGoogle Scholar
  50. 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 89:2416–2425PubMedCrossRefGoogle Scholar
  51. Pijanowska J, Dawidowicz P, Howe A, Weider LJ (2006) Predator induced shifts in Daphnia life-histories under different food regimes. Arch Hydrobiol 167:37–54CrossRefGoogle Scholar
  52. Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91:1900–1907PubMedCrossRefGoogle Scholar
  53. Ramirez RA, Snyder WE (2009) Scared sick? Predator-pathogen facilitation enhances exploitation of a shared resource. Ecology 90:2832–2839PubMedCrossRefGoogle Scholar
  54. Reede T (1995) Life history shifts in response to different levels of fish kairomones in Daphnia. J Plankton Res 17:1661–1667CrossRefGoogle Scholar
  55. Reissen HP (1999) Chaoborus predation and delayed reproduction in Daphnia: a demographic modeling approach. Evol Ecol 13:339–363CrossRefGoogle Scholar
  56. Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proc R Soc Lond B 267:171–176CrossRefGoogle Scholar
  57. Rinke K, Hulsmann S, Mooij WM (2008) Energetic costs, underlying resource allocation patterns, and adaptive value of predator-induced life-history shifts. Oikos 117:273–285CrossRefGoogle Scholar
  58. Rohrlack KC, Dittmann E, Norgueira I, Vasconcelos V, Börner T (2005) Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects. Limnol Oceanogr 50:440–448CrossRefGoogle Scholar
  59. Sakwinska O (2002) Response to fish kairomone in Daphnia galeata life history traits relies on shift to earlier instar at maturation. Oecologia 131:409–417CrossRefGoogle Scholar
  60. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954PubMedCrossRefGoogle Scholar
  61. Schmitz OJ, Suttle KB (2001) Effects of top predator species on direct and indirect interactions in a food web. Ecology 82:2072–2081CrossRefGoogle Scholar
  62. Schmitz OJ, Beckerman AP, O’Brian KM (1997) Behaviorally-mediated trophic cascades: the effects of predation risk on food web interactions. Ecology 78:1388–1399CrossRefGoogle Scholar
  63. Sell AF (2000) Morphological defenses induced in situ by the invertebrate predator Chaoborus: comparison of responses between Daphnia pulex and D. rosea. Oecologia 125:150–160CrossRefGoogle Scholar
  64. Stibor H, Lüning J (1994) Predator-induced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea, Cladocera). Funct Ecol 8:98–101CrossRefGoogle Scholar
  65. Thiemann GW, Wassersug RJ (2000) Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biol J Linn Soc 71:513–528CrossRefGoogle Scholar
  66. Tollrian R (1993) Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. J Plankton Res 15:1309–1318CrossRefGoogle Scholar
  67. Weber A, Declerck S (1997) Phenotypic plasticity of Daphnia life history traits in response to predator kairomones: genetic variability and evolutionary potential. Hydrobiologia 360:89–99CrossRefGoogle Scholar
  68. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  69. Yin M, Laforsch C, Lohr J, Wolinska J (2011) Predator-induced defense makes Daphnia more vulnerable to parasites. Evolution 65:1482–1488PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Christopher R. Bertram
    • 1
    • 2
  • Mark Pinkowski
    • 2
  • Spencer R. Hall
    • 3
  • Meghan A. Duffy
    • 4
  • Carla E. Cáceres
    • 1
    • 2
  1. 1.Program in Ecology, Evolution and Conservation BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.School of Integrative BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  3. 3.Department of BiologyIndiana UniversityBloomingtonUSA
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA

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