Mussel memory: can bivalves learn to fear parasites?

Abstract

Fear plays a crucial role in predator-prey interactions and can have cascading impacts on the structure of whole ecosystems. Comparable fear effects have recently been described for hosts and their parasites but our understanding of the underlying mechanisms remains limited by the lack of empirical examples. Here, we experimentally tested if bivalves Mytilus edulis can potentially 'learn to fear' the infective transmission stages (cercariae) of the trematode Himasthla elongata, and if experienced mussels change their parasite-avoidance behaviour accordingly. Our results show that previous experience with parasites, but not established infections, lead to a reduced filtration activity in mussels in the presence of cercariae compared to parasite-naive conspecifics. This reduction in filtration activity resulted in lower infection rates in mussels. Since parasite avoidance comes at the cost of lower feeding rates, mussels likely benefit from the ability to adjust their defence behaviour when infection risks are high. Overall, these dynamic processes of avoidance behaviour can be expected to play a significant role in regulating the bivalves' ecosystem engineering function in coastal habitats.

Keywords: Himasthla elongata; Mytilus edulis; ecology of fear; non-consumptive effects; trematode.

Figure 1.

Post-experimental chlorophyll-a concentration (mean μg l⁻¹ ± s.e.) after 2 h of filtration by blue mussels Mytilus edulis exposed and unexposed to Himasthla elongata cercariae. Naive: pre-experimentally uninfected mussels; pre-infected: mussels exposed to H. elongata prior to the experiment. N = 9–10 for each treatment combination. table 1 for summary statistics (main analysis). Asterisks above plots denote statistically significant differences between treatments (*p < 0.01; **p < 0.001; n.s. = not significant; Tukey HSD post hoc tests).

Figure 2.

Relationship between post-experimental total metacercarial load in blue mussels Mytilus edulis (log-transformed no. ind.⁻¹) and chlorophyll-a concentration (μg l⁻¹) for pre-experimentally uninfected (naive) mussels exposed to Himasthla elongata cercariae. Linear regression: $r_8^2=0.610$, p = 0.008).