Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Abstract

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free-living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host-parasite-predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.

Keywords: Commensalism; community dynamics; disease ecology; host–parasite interactions; mutualism.

Figure 1

Chaetogaster limnaei limnaei worms on the head, foot, and shell of a planorbid snail. Photograph courtesy of Neil Phillips.

Figure 2

(A) The frequency of observed Chaetogaster infestation intensities in Helisoma trivolvis snails, (B) the frequency of echinostome metacercariae infection intensities in snails, and (C) the relationship between the number of Chaetogaster found infesting a snail, the snail's status as a first intermediate host (infected or not), and the metacercariae infection intensity in those snails, all from a field survey. Lines indicate best-fitting negative binomial models. In (C) red symbols indicate snails infected as first intermediate hosts, and black symbols indicate snails not infected as first intermediate hosts.

Figure 3

Proportion of cercariae that successfully encysted in snails across a range of Chaetogaster densities (Experiment 1). Each point shows an individual snail, and the points were jittered slightly to aid visualization. The line is the predicted fit from the binomial regression model.

Figure 4

Proportion of cercariae that successfully encysted in snails across a range of Echinostoma trivolvis cercariae densities (left y-axis; Experiment 2). Each point shows an individual snail, and the points were jittered slightly to aid visualization. The line is the predicted fit from the binomial regression model. The average number of cysts per snail at each cercariae density is indicated with a large star (right y-axis).

Figure 5

Proportion of cercariae that successfully encysted in snails across a range of Chaetogaster densities (Experiment 3). Each point shows an individual snail, and the points were jittered slightly to aid visualization. The three lines are the predicted fits from the binomial regression model for the three cercariae density treatments.

Figure 6

Possible mechanisms by which Chaetogaster may alter transmission of Echinostoma trivolvis. (1) By consuming miracidia as they attempt to penetrate snails, Chaetogaster reduce first intermediate host infection (e.g., Rodgers et al. 2005). (2) By consuming cercariae as they leave snails (e.g., Rajasekariah ; Fernandez et al. 1991), Chaetogaster might reduce the total number of cercariae entering the aquatic environment. (3) By consuming cercariae as they attempt to penetrate snails, Chaetogaster reduce second intermediate infection (this study; Sankurathri and Holmes 1976). (4) By deterring cercariae with their predatory behavior (i.e., Sankurathri and Holmes 1976), Chaetogaster might change E. trivolvis second intermediate host preference. (5) By changing the intensity of infection in second intermediate hosts (e.g., this study), Chaetogaster may change the prevalence and intensity of infection in the definitive host, thereby changing the input of eggs into the system. The gray arrow follows development from egg through adult in the life cycle of E. trivolvis. Dashed black arrows indicate movement of larval E. trivolvis into or out of a host. Numerals indicate the part of the life cycle impacted by the mechanisms above.