Friendly competition: evidence for a dilution effect among competitors in a planktonic host–parasite system

Abstract

The "dilution effect" concept in disease ecology offers the intriguing possibility that clever manipulation of less competent hosts could reduce disease prevalence in populations of more competent hosts. The basic concept is straightforward: host species vary in suitability (competence) for parasites, and disease transmission decreases when there are more incompetent hosts interacting with vectors or removing free-living stages of a parasite. However, host species also often interact with each other in other ecological ways, e.g., as competitors for resources. The net result of these simultaneous, multiple interactions (disease dilution and resource competition) is challenging to predict. Nonetheless, we see the signature of both roles operating concurrently in a planktonic host-parasite system. We document pronounced spatiotemporal variation in the size of epidemics of a virulent fungus (Metschnikowia bicuspidata) in Midwestern U.S. lake populations of a dominant crustacean grazer (Daphnia dentifera). We show that some of this variation is captured by changes in structure of Daphnia assemblages. Lake-years with smaller epidemics were characterized by assemblages dominated by less suitable hosts ("diluters," D. pulicaria and D. retrocurva, whose suitabilties were determined in lab experiments and field surveys) at the start of epidemics. Furthermore, within a season, less suitable hosts increased as epidemics declined. These observations are consistent with a dilution effect. However, more detailed time series analysis (using multivariate autoregressive models) of three intensively sampled epidemics show the signature of a likely interaction between dilution and resource competition between these Daphnia species. The net outcome of this interaction likely promoted termination of these fungal outbreaks. Should this outcome always arise in "friendly competition" systems where diluting hosts compete with more competent hosts? The answers to this question lie at a frontier of disease ecology.

Antipredator Behavior Produced by Heterosexual and Homosexual Tandem Running in the Termite Reticulitermes chinensis (Isoptera: Rhinotermitidae)

“…The dilution effect could reduce an individual's risk of predation in group-forming animals (Hamilton, 1971;Hall et al, 2009;Marcoux, 2011;Rodgers et al, 2011). Our reOur reOur results suggested that colonies of R. chinensis experienced the same dilution effect as described previously in R. speratus .…”

Epidemic size determines population-level effects of fungal parasites on Daphnia hosts

“…Three lines of evidence suggest that this decline was due, at least in part, to food limitation in both treatments. First, densities of the competitor D. pulicaria, which completely resists Metschnikowia infection (Hall et al 2009c), increased in both treatments over time ( Fig. 4d; time F 7,42 = 24.7, P \ 0.0001).…”

“…Then, with more finely scaled time series data, we first calculated cross-correlations between total host density and infection prevalence at different lags, ranging from one to four sampling visits (i.e., a lag of four visits means that infection prevalence now correlates with host density four sampling dates (12-16 days) from this time onwards). Multivariate autoregressive (MAR) models were used to quantify interaction strengths between infected hosts (I) and two stage classes of uninfected hosts, namely, adults (A U ) and juveniles (J U ) [following Ives et al (2003) and especially Hall et al (2009c); see ESM for details of this analysis].…”

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

“…A negative correlation between community diversity and parasite incidence is therefore expected. However, the net benefit of the dilution effect for the most sensitive host species depends on the trade-off between lower parasite incidence and higher interspecific competition Hall et al 2009).…”