Skip to main content

Advertisement

Log in

How predator and parasite size interact to determine consumption of infectious stages

  • Highlighted Student Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Parasites are important players in ecological communities that can shape community structure and influence ecosystem energy flow. Yet beyond their effects on hosts, parasites can also function as an important prey resource for predators. Predators that consume infectious stages in the environment can benefit from a nutrient-rich prey item while concurrently reducing transmission to downstream hosts, highlighting the broad importance of this interaction. Less clear, however, are the specific characteristics of parasites and predators that increase the likelihood of consumption. Here, we determine what combination(s) of predator and parasite morphological traits lead to high parasite consumption. We exposed the infectious stages (cercariae) of five trematode (fluke) taxa to aquatic insect predators with varying foraging strategies and morphologies. Across the 19 predator—parasite combinations tested, damselfly predators in the family Coenagrionidae were, on average, the most effective predators of cercariae, consuming between 13 and 55% of administered cercariae. Large-bodied cercariae of Ribeiroia ondatrae had the highest average vulnerability to predation, with 37–48% of cercariae consumed. The interaction between predator head width and cercariae tail size strongly influenced the probability of consumption: small-bodied predators were the most effective consumers, particularly for larger tailed parasites. Thus, the likelihood of parasite consumption depended strongly on the relative size between predator and parasite. Our study helps establish that predation on free-living parasites largely follows a broader predator–prey framework. This will help to identify which predator and parasite combinations will likely have high consumptive interactions, potentially reducing parasite transmission in natural populations.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data are publicly available through the figshare data repository: https://doi.org/10.6084/m9.figshare.13238285.v1

References

  • Asch RG, Stock CA, Sarmiento JL (2019) Climate change impacts on mismatches between phytoplankton blooms and fish spawning phenology. Glob Chang Biol 25:2544–2559

    Article  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Google Scholar 

  • Berger L, Hyatt D, Speare R, Longcore JE (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 68:51–63

    Article  Google Scholar 

  • Bertram CR, Pinkowski M, Hall SR, Duffy MA, Cáceres CE (2013) Trait-mediated indirect effects, predators, and disease: test of a size-based model. Oecologia 173:1023–1032

    Article  PubMed  Google Scholar 

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press

    Book  Google Scholar 

  • Born-Torrijos A, Paterson RA, van Beest GS, Vyhlídalová T, Henriksen EH, Knudsen R, Kristoffersen R, Amundsen P, Soldánová M (2021) Cercarial behaviour alters the consumer functional response of three-spined sticklebacks. J Anim Ecol 90:978–988

    Article  PubMed  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  CAS  PubMed  Google Scholar 

  • Bybee SM, Johnson KK, Gering EJ, Whiting MF, Crandall KA (2012) All the better to see you with: a review of odonate color vision with transcriptomic insight into the odonate eye. Org Divers Evol 12:241–250

    Article  Google Scholar 

  • Carvalho RO, Araújo JV, Braga FR, Ferreira SR, Araujo JM, Silva AR, Frassy LN, Alves CDF (2009) Biological control of Ancylostomosis in dogs using the nematode-trapping fungus Monacrosporium thaumasium in southeastern Brazil. Vet Parasitol 165:179–183

    Article  CAS  PubMed  Google Scholar 

  • Catania SV, Koprivnikar J, McCauley S (2016) Size-dependent predation alters interactions between parasites and predators. Can J Zoo 94:631–635

    Article  Google Scholar 

  • Coblentz KE, DeLong JP (2020) Predator-dependent functional responses alter the coexistence and indirect effects among prey that share a predator. Oikos 129:1404–1414

    Article  Google Scholar 

  • Colley DG, Bustinduy AL, Secor WE, King CH (2014) Human schistosomiasis. Lancet 383:2253–2264

    Article  PubMed  PubMed Central  Google Scholar 

  • Corbet PS (1980) Biology of Odonata. Annu Rev Entomol 25:189–217

    Article  Google Scholar 

  • Corbet PS (1999) Dragonflies: behaviour and ecology of Odonata. Harley books

    Google Scholar 

  • Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293

    Article  Google Scholar 

  • 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 50:412–420

    Article  Google Scholar 

  • Duffy MA, Housley JM, Penczykowski RM, Caceres CE, Hall SR (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Funct Ecol 25:945–953

    Article  Google Scholar 

  • Esch GW, Barger MA, Fellis KJ (2002) The transmission of digenetic trematodes: style, elegance, complexity. Integr Comp Biol 42:304–312

    Article  PubMed  Google Scholar 

  • Fried B, Eyster LS, Pechenik JA (1998) Histochemical glycogen and neutral lipid in Echinostoma trivolvis cercariae and effects of exogenous glucose on cercarial longevity. J Helminthol 72:83–85

    Article  CAS  PubMed  Google Scholar 

  • Gaeta JW, Ahrenstorff TD, Diana JS, Fetzer WW, Jones TS, Lawson ZJ, McInerny MC, Santucci VJ Jr, Vander Zanden MJ (2018) Go big or… don’t? A field-based diet evaluation of freshwater piscivore and prey fish size relationships. PLoS ONE 13:e0194092

    Article  PubMed  PubMed Central  Google Scholar 

  • Gelman A, Hill J (2007) Data analysis using regression and multilevel hierarchical models, vol 1. Cambridge University Press, New York

    Google Scholar 

  • Goodchild CG, Kirk DE (1960) The life history of Spirorchis elegans Stunkard, 1923 (Trematoda: Spirorchiidae) from the painted turtle. J Parasitol 46:219–229

    Article  Google Scholar 

  • Goodman BA, Johnson PTJ (2011) Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PLoS ONE 6:e20193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109:15–29

    Article  Google Scholar 

  • Hannon ER, Calhoun DM, Chadalawada S, Johnson PTJ (2018) Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns. Parasitology 145:783–791

    Article  PubMed  Google Scholar 

  • Hansen PJ, Bjørnsen PK, Hansen BW (2000) Zooplankton grazing and growth: scaling within the 2–2,000-µm body size range. Limnol Oceanogr 45:1891–1891

    Article  Google Scholar 

  • Harper DG, Blake RW (1988) Energetics of piscivorous predator-prey interactions. J Theor Biol 134:59–76

    Article  Google Scholar 

  • Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Migrations and dispersal of marine organisms. Springer, Dordrecht, pp 163–170

    Chapter  Google Scholar 

  • Hopkins SR, Wyderko JA, Sheehy RR, Belden LK, Wojdak JM (2013) Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts. Ecol Evol 3:4427–4438

    Article  PubMed  PubMed Central  Google Scholar 

  • Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385

    Article  PubMed  Google Scholar 

  • Jacobus LM, Macadam CR, Sartori M (2019) Mayflies (Ephemeroptera) and their contributions to ecosystem services. Insects 10:170

    Article  PubMed Central  Google Scholar 

  • Jay CV (1989) Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. Am Midl Nat 121:68–77

    Article  Google Scholar 

  • Johnson PTJ, Lunde K, Zelmer DA, Werner JK (2003) Limb deformities as an emerging parasitic disease in amphibians: evidence from museum specimens and resurvey data. Conserv Biol 17:1724–1737

    Article  Google Scholar 

  • Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371

    Article  PubMed  Google Scholar 

  • Kagami M, Miki T, Takimoto G (2014) Mycoloop: chytrids in aquatic food webs. Front Microbiol 5:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Klecka J, Boukal DS (2013) Foraging and vulnerability traits modify predator–prey body mass allometry: freshwater macroinvertebrates as a case study. J Anim Ecol 82:1031–1041

    Article  PubMed  Google Scholar 

  • Koehler AV, Brown B, Poulin R, Thieltges DW, Fredensborg BL (2012) Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evol Ecol 26:1497–1512

    Article  Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546

    Article  PubMed  PubMed Central  Google Scholar 

  • Lampert W (2006) Daphnia: model herbivore, predator and prey. Pol J Ecol 54:607–620

    Google Scholar 

  • Loose CJ, Dawidowicz P (1994) Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75:2255–2263

    Article  Google Scholar 

  • McCarthy HO, Fitzpatrick S, Irwin SWB (2002) Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics. J Parasitol 88:910–918

    Article  PubMed  Google Scholar 

  • McDevitt-Galles T, Calhoun DM, Johnson PTK (2018) Parasite richness and abundance within aquatic macroinvertebrates: testing the roles of host-and habitat-level factors. Ecosphere 9:e02188

    Article  PubMed  PubMed Central  Google Scholar 

  • McDevitt-Galles T, Johnson PTJ (2018) Drought attenuates the impact of fish on aquatic macroinvertebrate richness and community composition. Freshw Biol 63:1457–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKee KM, Koprivnikar J, Johnson PTJ, Arts MT (2020) Parasite infectious stages provide essential fatty acids and lipid-rich resources to freshwater consumers. Oecologia 192:477–488

    Article  PubMed  Google Scholar 

  • Miller HM (1929) A large-tailed echinostome cercaria from North America. Trans Am Microsc Soc 48:310–313

    Article  Google Scholar 

  • Miller TE, Rudolf VH (2011) Thinking inside the box: community-level consequences of stage-structured populations. Trends Ecol Evol 26:457–466

    Article  PubMed  Google Scholar 

  • Mironova E, Gopko M, Pasternak A, Mikheev V, Taskinen J (2019) Trematode cercariae as prey for zooplankton: effect on fitness traits of predators. Parasitology 146:105–111

    Article  PubMed  Google Scholar 

  • Morley NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691:7–19

    Article  CAS  Google Scholar 

  • Mouritsen KN, Poulin R (2003) Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator’s nightmare. Int J Parasitol 33:1043–1050

    Article  PubMed  Google Scholar 

  • Murtaugh PA (1981) Size-selective predation on Daphnia by Neomysis mercedis. Ecology 62:894–900

    Article  Google Scholar 

  • Nakazawa T (2015) Ontogenetic niche shifts matter in community ecology: a review and future perspectives. Popul Ecol 57:347–354

    Article  Google Scholar 

  • Orlofske SA, Jadin RC, Preston DL, Johnson PTJ (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93:1247–1253

    Article  PubMed  Google Scholar 

  • Orlofske SA, Jadin RC, Johnson PTJ (2015) It’s a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178:537–547

    Article  PubMed  Google Scholar 

  • Ovadia O, Schmitz OJ (2002) Linking individuals with ecosystems: experimentally identifying the relevant organizational scale for predicting trophic abundances. Proc Natl Acad Sci USA 99:12927–12931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:797–802

    Article  Google Scholar 

  • Paseka RE, White LA, Van de Waal DB, Strauss AT, González AL, Everett RA, Peace A, Seabloom EW, Frenken T, Borer ET (2020) Disease-mediated ecosystem services: pathogens, plants, and people. Trends Ecol Evol 35:731–743

    Article  PubMed  Google Scholar 

  • Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032

    Article  PubMed  Google Scholar 

  • Poulin R, Morand S (2000) The diversity of parasites. Q Rev Biol 75:277–293

    Article  CAS  PubMed  Google Scholar 

  • Preston DL, Orlofske SA, Lambden JP, Johnson PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. J Anim Ecol 82:509–517

    Article  PubMed  Google Scholar 

  • Preston DL, Mischler JA, Townsend AR, Johnson PTJ (2016) Disease ecology meets ecosystem science. Ecosystems 19:737–748

    Article  CAS  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Richgels KL, Hoverman JT, Johnson PTJ (2013) Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis. Ecography 36:854–863

    Article  Google Scholar 

  • Rohr JR, Civitello DJ, Crumrine PW, Halstead NT, Miller AD, Schotthoefer AM, Stenoien C, Johnson LB, Beasley VR (2015) Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proc Natl Acad Sci USA 112:3008–3013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenkranz M, Lagrue C, Poulin R, Selbach C (2018) Small snails, high productivity? Larval output of parasites from an abundant host. Freshw Biol 63:1602–1609

    Article  Google Scholar 

  • Rudolf VH (2020) A multivariate approach reveals diversity of ontogenetic niche shifts across taxonomic and functional groups. Freshw Bio 65:745–756

    Article  Google Scholar 

  • Scharf FS, Juanes F, Rountree RA (2000) Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248

    Article  Google Scholar 

  • Schell SC (1985) Handbook of Trematodes of North America North of Mexico. University Press of Idaho

    Google Scholar 

  • Schotthoefer AM, Labak KM, Beasley VR (2007) Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. J Parasitol 93:1240–1243

    Article  PubMed  Google Scholar 

  • Schultz B, Koprivnikar J (2019) Free-living parasite infectious stages promote zooplankton abundance under the risk of predation. Oecologia 191:411–420

    Article  PubMed  Google Scholar 

  • Searle CL, Mendelson JR III, Green LE, Duffy MA (2013) Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecol Evol 3:4129–4138

    Article  PubMed  PubMed Central  Google Scholar 

  • Seda J, Petrusek A (2011) Daphnia as a model organism in limnology and aquatic biology: introductory remarks. J Limnol 70:337–344

    Article  Google Scholar 

  • Selbach C, Rosenkranz M, Poulin R (2019) Cercarial behavior determines risk of predation. J Parasitol 105:330–333

    Article  PubMed  Google Scholar 

  • Shoemaker LG, Hayhurst E, Weiss-Lehman CP, Strauss A, Porath-Krause A, Borer ET, Seabloom EW, Shaw AK (2019) Pathogens manipulate the preference of vectors, slowing disease spread in a multi-host system. Ecol Let 22:1115–1125

    Article  Google Scholar 

  • Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Evol Syst 16:269–311

    Article  Google Scholar 

  • Skalski GT, Gilliam JF (2001) Functional responses with predator interference: viable alternatives to the Holling type II model. Ecology 8:3083–3092

    Article  Google Scholar 

  • Thieltges DW, Jensen KT, Poulin R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426

    Article  CAS  PubMed  Google Scholar 

  • Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482

    Google Scholar 

  • Tollrian R (1995) Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia 101:151–155

    Article  PubMed  Google Scholar 

  • van Leeuwen A, Huss M, Gårdmark A, Casini M, Vitale F, Hjelm J, Persson L, de Roos AM (2013) Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey. Am Nat 182:53–66

    Article  PubMed  Google Scholar 

  • Vanni MJ (1988) Freshwater zooplankton community structure: introduction of large invertebrate predators and large herbivores to a small species community. Can J Fish Aquat Sci 45:1758–1770

    Article  Google Scholar 

  • Weitz JS, Levin SA (2006) Size and scaling of predator–prey dynamics. Ecol Let 9:548–557

    Article  Google Scholar 

  • Welsh JE, van der Meer J, Brussaard CP, Thieltges DW (2014) Inventory of organisms interfering with transmission of a marine trematode. J Mar Biolog 94:697–702

    Article  Google Scholar 

  • Welsh JE, Hempel A, Markovic M, Van Der Meer J, Thieltges DW (2019) Consumer and host body size effects on the removal of trematode cercariae by ambient communities. Parasitology 146:342–347

    Article  PubMed  Google Scholar 

  • Wilber MQ, Briggs CJ, Johnson PTJ (2020) Disease’s hidden death toll: using parasite aggregation patterns to quantify landscape-level host mortality in a wildlife system. J Anim Ecol 89:2876–2887

    Article  PubMed  Google Scholar 

  • Wilson DS (1975) The adequacy of body size as a niche difference. Am Nat 109:769–784

    Article  Google Scholar 

  • Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AM (2007) Parasites alter community structure. Proc Natl Acad Sci USA 104:9335–9339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood CL, Johnson PTJ (2015) A world without parasites: exploring the hidden ecology of infection. Front Ecol Environ 13:425–434

    Article  PubMed  PubMed Central  Google Scholar 

  • Woodward G, Ebenman B, Emmerson M, Montoya JM, Olesen JM, Valido A, Warren PH (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are indebted to D. Calhoun, T. Stewart Merrill and L. Pelletier for their assistance and conducting the predation trails and data collection. We are grateful for the amazing field team in California, especially, V. Klimuk and D. Saunders who provided both the insect predators as well as the infected snails. We thank Andy Dean and Andy Fenton for their insights on the conceptual framework of the project. We also acknowledge B. Hobart, T. Stewart Merrill and W. Moss for their comments and discussions that resulted in drastic improvements of the early drafts of the manuscript.

Funding

This work was supported, in part, by the National Science Foundation (DEB-1754171 and a Research Experience for Undergraduates supplement) and a fellowship from the David and Lucile Packard Foundation.

Author information

Authors and Affiliations

Authors

Contributions

TMG, JK and PTJJ designed the experiment. TMG and SAC conducted the experiment. TMG, SAC, and PTJJ conducted the data analysis. TMG and SAC wrote the initial draft of the manuscript and all the authors contributed to the conceptual development and revision of the manuscript.

Corresponding author

Correspondence to Travis McDevitt-Galles.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Additional information

Communicated by Jason Todd Hoverman.

Parasites can make up large proportions of a community’s biomass and may serve as valuable prey items for numerous predators. Identifying the drivers that determine parasite consumption will allow us to understand the likelihood of parasites serving as a viable food source for various predators and how predation on parasite can potentially reduce parasite transmission. Using an experimental approach, we demonstrate that predation on parasites is largely driven by a combination of predator and parasite size, with highest consumption patterns observed with smaller predators feeding on larger parasites.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 227 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McDevitt-Galles, T., Carpenter, S.A., Koprivnikar, J. et al. How predator and parasite size interact to determine consumption of infectious stages. Oecologia 197, 551–564 (2021). https://doi.org/10.1007/s00442-021-05010-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-05010-w

Keywords

Navigation