Density- and trait-mediated effects of a parasite and a predator in a tri-trophic food web.
Despite growing interest in ecological consequences of parasitism in food webs, relatively little is known about effects of parasites on long-term population dynamics of non-host species or about whether such effects are density or trait mediated. We studied a tri-trophic food chain comprised of (i) a bacterial basal resource (Serratia fonticola), (ii) an intermediate consumer (Paramecium caudatum), (iii) a top predator (Didinium nasutum) and (iv) a parasite of the intermediate consumer (Holospora undulata). A fully factorial experimental manipulation of predator and parasite presence/absence was combined with analyses of population dynamics, modelling and analyses of host (Paramecium) morphology and behaviour. Predation and parasitism each reduced the abundance of the intermediate consumer (Paramecium), and parasitism indirectly reduced the abundance of the basal resource (Serratia). However, in combination, predation and parasitism had non-additive effects on the abundance of the intermediate consumer, as well as on that of the basal resource. In both cases, the negative effect of parasitism seemed to be effaced by predation. Infection of the intermediate consumer reduced predator abundance. Modelling and additional experimentation revealed that this was most likely due to parasite reduction of intermediate host abundance (a density-mediated effect), as opposed to changes in predator functional or numerical response. Parasitism altered morphological and behavioural traits, by reducing host cell length and increasing the swimming speed of cells with moderate parasite loads. Additional tests showed no significant difference in Didinium feeding rate on infected and uninfected hosts, suggesting that the combination of these modifications does not affect host vulnerability to predation. However, estimated rates of encounter with Serratia based on these modifications were higher for infected Paramecium than for uninfected Paramecium. A mixture of density-mediated and trait-mediated indirect effects of parasitism on non-host species creates rich and complex possibilities for effects of parasites in food webs that should be included in assessments of possible impacts of parasite eradication or introduction.
Institut für Evolutionsbiologie und Umweltwissenschaften, Universität Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Aabir
A
Banerji
Institut des Sciences de l'Evolution, UMR 5554, Université Montpellier II, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France.
Alison B
AB
Duncan
Institut des Sciences de l'Evolution, UMR 5554, Université Montpellier II, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France.
Joanne S
JS
Griffin
School of Life Sciences, University of Lincoln, Brayford Pool, Lincoln, Lincolnshire, LN6 7TS, UK.
Stuart
S
Humphries
Institut für Evolutionsbiologie und Umweltwissenschaften, Universität Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Owen L
OL
Petchey
Institut des Sciences de l'Evolution, UMR 5554, Université Montpellier II, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France.
Oliver
O
Kaltz
D000818:Animals; D001522:Behavior, Animal; D016798:Ciliophora / Q000502:physiology*; D020387:Food Chain; D042281:Holosporaceae / Q000502:physiology*; D054884:Host-Pathogen Interactions; D048488:Paramecium caudatum / Q000382:microbiology / Q000502:physiology*; D011157:Population Dynamics; D011235:Predatory Behavior; D012705:Serratia / Q000502:physiology*
Didinium; Holospora; Paramecium; density‐mediated indirect interaction; trait‐mediated indirect interaction