Microhabitat use, not temperature, regulates intensity of Gyrodactylus cichlidarum long-term infection on farmed tilapia--are parasites evading competition or immunity?

Abstract

Gyrodactylids (Monogenea) are ectoparasites of fish, some of which negatively affect commercially valuable fishes. Temperature strongly regulates population dynamics of these viviparous flatworms in farmed and wild fish populations, with most gyrodactylid species showing positive temperature-abundance associations. In agreement with epidemiological theory, numerous laboratory studies demonstrate that these parasites cannot persist in confined fish populations without periodic introduction of susceptible hosts. Extinction of gyrodactylid populations is due to host immunity, which develops in several fish species. In this one-year study, we followed populations of the recognized pathogen Gyrodactylus cichlidarum infecting four genetic groups of confined tilapia (wild type Nile tilapia Oreochromis niloticus niloticus, red O. n. niloticus, Mozambique tilapia O. mossambicus and a red synthetic population called Pargo-UNAM) kept under farming conditions and subject to natural environmental fluctuations. Based on the antecedents given, we postulated the following three hypotheses: (1) parasite abundance will be regulated by water temperature; (2) parasites will induce host mortality, particularly during periods of rapid infrapopulation growth; and (3) gyrodactylid populations will eventually become extinct on confined fish hosts. We disproved the three hypotheses: (1) parasite numbers fluctuated independently of temperature but were associated to changes in microhabitat use; (2) although gyrodactylid populations exhibited considerable growth, no evidence was found of negative effects on the hosts; and (3) infections persisted for one year on confined fish. Microhabitat use changed over time, with most worms apparently migrating anteriorly from the caudal fin and ending on the pectoral fins. Gyrodactylid populations followed similar trajectories in all fish, aggregating and dispersing repeatedly. Several instances were found where increased parasite dispersion coincided with increased intensity of infection; as well as the opposite, where increased aggregation coincided with parasite population declines. Three alternative explanations could account for these observations: that parasites (1) experience differential mortality on different anatomical regions of the fish; (2) migrate to avoid intraspecific competition; and (3) migrate to escape localized immune responses induced by infection. Our data do not allow us to demonstrate which of these alternatives is correct, so we discuss the merits of each. We provide circumstantial evidence in support of the third explanation, because as shown in other fish host-gyrodactylid interactions where immune responses have been characterized, in this study worms progressively moved away from fins with high mucus cell density to those with low density - what would be anticipated if immune defenses occur and reach the fish surface through mucus.