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Some parasites manipulate their hosts phenotype to enhance predation rates by the next host in the parasites life cycle. Our understanding of this parasite-increased trophic transmission is often stymied by study-design challenges. A recurring difficulty has been obtaining uninfected hosts with a coevolutionary history with the parasites, and conducting experimental infections that mimic natural processes. In 1996, Lafferty and Morris provided what has become a classic example of parasite-increased trophic transmission; they reported a positive association between the intensity of a brain-infecting trematode (Euhaplorchis californiensis) in naturally infected California killifish (Fundulus parvipinnis) and the frequency of conspicuous behaviors, which was thought to explain the documented 10-30× increase in predation by the final host birds. Here, we address the primary gap in that study by using experimental infections to assess the causality of E. californiensis infection for increased conspicuous behaviors in F. parvipinnis. We hatched and reared uninfected F. parvipinnis from a population co-occurring with E. californiensis, and infected them 1-2 times/week over half their life span with E. californiensis and a small cyathocotylid trematode (SMCY) that targets the hosts muscle tissue. At 3 time points throughout the hosts lives, we quantified several conspicuous behaviors: contorting, darting, scratching, surfacing, and vertical positioning relative to the waters surface. Euhaplorchis californiensis and SMCY infection caused 1.8- and 2.5-fold overall increases in conspicuous behaviors, respectively. Each parasite was also associated with increases in specific conspicuous behaviors, particularly 1.9- and 1.4-fold more darting. These experimental findings help solidify E. californiensis-F. parvipinnis as a classic example of behavioral manipulation. Yet our findings for E. californiensis infection-induced behavioral change were less consistent and strong than those previously documented. We discuss potential explanations for this discrepancy, particularly the idea that behavioral manipulation may be most apparent when fish are actively attacked by predators. Our findings concerning the other studied trematode species, SMCY, highlight that trophically transmitted parasites infecting various host tissues are known to be associated with conspicuous behaviors, reinforcing calls for research examining how communities of trophically transmitted parasites influence host behavior.

Modulation of brain serotonin (5-HT) signalling is associated with parasite-induced changes in host behaviour, potentially increasing parasite transmission to predatory final hosts. Such alterations could have substantial impact on host physiology and behaviour, as 5-HT serves multiple roles in neuroendocrine regulation. These effects, however, remain insufficiently understood, as parasites have been associated with both increased and decreased serotonergic activity. Here, we investigated effects of trematode Euhaplorchis californiensis metacercariae on post-stress serotonergic activity in the intermediate host California killifish (Fundulus parvipinnis). This parasite is associated with conspicuous behaviour and increased predation of killifish by avian end-hosts, as well as inhibition of post-stress raphe 5-HT activity. Until now, laboratory studies have only been able to achieve parasite densities (parasites/unit host body mass) well below those occurring in nature. Using laboratory infections yielding ecologically relevant parasite loads, we show that serotonergic activity indeed decreased with increasing parasite density, an association likely indicating changes in 5-HT neurotransmission while available transmitter stores remain constant. Contrary to most observations in the literature, 5-HT activity increased with body mass in infected fish, indicating that relationships between parasite load and body mass may in many cases be a real underlying factor for physiological correlates of body size. Our results suggest that parasites are capable of influencing brain serotonergic activity, which could have far-reaching effects beyond the neurophysiological parameters investigated here.

Parasites can have profound effects on intra‐ and interspecific interactions at the population and community levels through their influence on host behaviour, physiology and fitness. While host phenotypic changes are typically thought of in terms of established infections, parasite encounters may be sufficient to induce behavioural changes, even when no viable infections are established.Here, we use the Japanese rice fish medaka Oryzias latipes and the brain‐infecting microsporidan parasite Pseudoloma neurophilia to understand how parasite resistance influences behaviour.Although a previous study suggested that medaka are a suitable host for P. neurophilia, an eight‐week parasite exposure regime resulted in no detectable infection in our study. Both parasite‐exposed and control (no parasite exposure) medaka were tested in behavioural assays that assessed boldness, activity and sociality. We detected considerable changes in medaka behaviour following parasite exposure, with parasite‐exposed fish being more active, less bold and more social when compared to control fish.These data indicate that parasite encounters may induce behavioural alterations even in non‐susceptible hosts. In addition to established infection, individual differences in parasite exposure must also be considered in studies of host responses across ecological scales. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]