Parasitism in ecosystem engineer species: A key factor controlling marine ecosystem functioning

Abstract

Although parasites represent a substantial part of marine communities’ biomass and diversity, their influence on ecosystem functioning, especially via the modification of host behaviour, remains largely unknown. Here, we explored the effects of the bopyrid ectoparasite Gyge branchialis on the engineering activities of the thalassinid crustacean Upogebia pusilla and the cascading effects on intertidal ecosystem processes (e.g. sediment bioturbation) and functions (e.g. nutrient regeneration). Laboratory experiments revealed that the overall activity level of parasitized mud shrimp is reduced by a factor 3.3 due to a decrease in time allocated to burrowing and ventilating activities (by factors 1.9 and 2.9, respectively). Decrease in activity level led to strong reductions of bioturbation rates and biogeochemical fluxes at the sediment–water interface. Given the world‐wide distribution of mud shrimp and their key role in biogeochemical processes, parasite‐mediated alteration of their engineering behaviour has undoubtedly broad ecological impacts on marine coastal systems functioning. Our results illustrate further the need to consider host–parasite interactions (including trait‐mediated indirect effects) when assessing the contribution of species to ecosystem properties, functions and services.

Mussel Shutdown: Does the Fear of Trematodes Regulate the Functioning of Filter Feeders in Coastal Ecosystems?

“…Parasites themselves have been recognized as important ecosystem engineers that modulate the availability of resources to other species via biotic or abiotic changes (Thomas et al, 1999;Pascal et al, 2020). Yet, these estimations of the ecological functions of parasitism are typically only based on post-infection, i.e., consumptive, effects of parasites, which likely grossly underestimates the full impact of these organisms on their environment.…”

Cockle as Second Intermediate Host of Trematode Parasites: Consequences for Sediment Bioturbation and Nutrient Fluxes across the Benthic Interface

“…As an indirect consequence, through a cascading effect, we anticipated a reduction in oxygen penetration depth into the sediment, leading to reduced remineralization rates and inorganic nutrient fluxes toward the overlying water. Such negative indirect effects of parasites on benthic ecosystem functioning through an alteration of host bioturbation activity have been, for example, recently quantified in another marine parasite-host system Upogebia pusilla-Gyge branchialis [7]. However, it is interesting to note that parasite infection can also have the opposite effect.…”

“…These ubiquitous organisms can profoundly impact ecosystem functioning, both directly by affecting ecosystem properties and indirectly by changing the functional role of their hosts [3]. More precisely, indirect effects may result from the limitation of dominant or keystone host species abundance (i.e., density-mediated effects) or from the modification of host-specific activities, which disproportionally influence ecosystem processes and functions (i.e., traitmediated effects) [4][5][6][7]. To date, the indirect ecological consequences, at the ecosystem level, of parasite-induced engineering behavior alteration (sensu Jones et al [8]) remain poorly known and quantified, particularly in marine environments with contradictory observations depending on the studied processes and host-parasite system.…”

Parasitism dramatically alters the ecosystem services provided by freshwater mussels

“…Despite many suggestions that parasites can affect ecosystem functioning (Hatcher et al, 2012) and theoretical evidence for this (Vannatta & Minchella, 2018), empirical evidence for the impact of parasites on ecosystem-level processes remains rare (Fischhoff et al, 2020; but see Pascal et al, 2020).…”

“…While the effects of parasites at an individual level are well known for a broad range of host taxa (Sánchez et al, 2018), parasites may also affect ecosystem functioning (Wood & Johnson, 2015) and can be considered as cryptic ecosystem engineers (Selbach et al, 2022). Despite many suggestions that parasites can affect ecosystem functioning (Hatcher et al, 2012) and theoretical evidence for this (Vannatta & Minchella, 2018), empirical evidence for the impact of parasites on ecosystem‐level processes remains rare (Fischhoff et al, 2020; but see Pascal et al, 2020).…”