Predation cues amplify the effects of parasites on the personality of a keystone grazer

Abstract

1. Parasites can alter species interactions either by modifying infected host behaviour or by influencing behavioural responses in uninfected individuals. Salt marsh ecosystems are characterized by a predator-prey interaction between the keystone grazer, Littoraria irrorata, and its main predator, Callinectes sapidus, both integral players in mediating the productivity of these habitats. 2. Littoraria also acts as the first intermediate host for at least four species of digenetic trematode. Parasite infection has been shown to decrease grazing and climbing in populations of Littoraria, although effects on infected host response to predators have not been investigated. Moreover, how infection might increase or decrease among-individual variation in behaviour (i.e. animal personality) is still unknown. Here we ask how trematode infection affects the expression of boldness in the anti-predator responses of L. irrorata in both the absence and presence of a predator cue.3. We find that individual boldness varies substantially, and repeatability tends to increase as the number of stressors increases, with infected individuals exposed to a predator cue showing the strongest expression of behavioural types. 4. Parasitism amplifies this effect, although the parasite itself does not appear to directly induce behavioural changes: infected snails show no evidence of decreased climbing or differences in refuge use as compared to their uninfected counterparts. Infection might therefore drive the expression of condition-dependent personality differences evident only under high-risk conditions. 5. Group infection status strongly influenced behavioural reaction norms: uninfected individuals grouped with an infected snail were more responsive to predation risk, exhibiting increased climbing behaviour and spending less time in the water. Here parasites are influencing personality indirectly by inducing avoidance behaviours in healthy individuals, although only in high-risk environments.6. The potential for exposure to parasites and predators fluctuates greatly across marsh ecosystems. Given the ecological importance of this predator-prey relationship, trematode infection can act as an important, although indirect, determinant of overall salt marsh community structure, health and function.

Grazer host density mediates the ability of parasites to protect foundational plants from overgrazing

“…This is in line with previous investigations in this system on the trait‐mediated reductions in the top–down impacts of snails on cordgrass biomass by P. acanthus (Morton 2018, Morton and Silliman 2020). However, recent laboratory behavioral assays investigating the influence of trematode parasitism on Littoraria boldness found that infected snails influenced predator avoidance behaviors in healthy conspecifics in high risk environments (Salerno et al 2023). It is possible that infected snails may yield outsized effects by influencing the behavior of conspecifics under certain circumstances.…”

Mechanisms and consequences of infection‐induced phenotypes

“…Population‐level effects likely reverberate through communities and ecosystems when such changes impact hosts' heterospecific interactions, such as predator–prey encounters and heterospecific communication. Salerno et al (2023) found that the presence of predator cues and infected conspecifics together drive phenotypic outcomes, such as personality, in snails. An understanding of the complex spatial interactions between predators and parasites in a given habitat (the overlaid ‘landscape of fear’ and ‘landscape of disgust’; Buck et al, 2018) will be critical for predicting variation within and among hosts, especially in variable environments.…”

“…Recognition of the pivotal role that parasites play in the variability of animal phenotypes in nature is surprisingly low (Chretien et al, 2023). Several contributions to this special feature present practical guidance for researchers working in a range of disciplines to assess the role of infection in their study system, including behaviour (Salerno et al, 2023; Stockmaier et al, 2023; Tillman & Adelman, 2023; Vindas et al, 2023), performance (Chretien et al, 2023), physiology (Alves & Aubin‐Horth, 2023; Lopes, 2023; Seguel et al, 2023; Wu, 2023) and epigenetics (Ngo et al, 2023). Yet, there are still many unanswered questions.…”

“…This special feature highlights the various ways that parasites drive variation in host phenotypes. The contributed articles highlight diverse host–parasite systems across a broad range of taxa and include perspective and concept articles (Adamo, 2023; Lopes, 2023; Pavey & Vyas, 2023; Poulin et al, 2023; Stockmaier et al, 2023; Tillman & Adelman, 2023), a systematic literature review (Chretien et al, 2023), a meta‐analysis (Wu, 2023) and observational and experimental research conducted in laboratory and field settings (Alves & Aubin‐Horth, 2023; Ngo et al, 2023; Salerno et al, 2023; Seguel et al, 2023; Vindas et al, 2023; Will et al, 2023). In this Editorial, we contextualize each featured article's contribution to our understanding of how parasites generate intra‐ and interindividual differences in host phenotypes, how this trait variation reverberates across levels of biological organization from cells to communities and the role of the host's external environment in modulating these effects.…”