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Novel Parasite Invasion Leads to Rapid Demographic Compensation and Recovery in an Experimental Population of Guppies

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Novel Parasite Invasion Leads to Rapid Demographic Compensation and Recovery in an Experimental Population of Guppies Novel parasite invasion leads to rapid demographic compensation and recovery in an experimental population of guppies Emma L.B. Rogowskia, Andy D. Van Alsta, Joseph Travisb, David N. Reznickc, Tim Coulsond, and Ronald D. Bassara,1 aDepartment of Biology, Williams College, Williamstown, MA 01267; bDepartment of Biological Science, Florida State University, Tallahassee, FL 32304; cDepartment of Biology, University of California, Riverside, CA 92521; and dDepartment of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved August 3, 2020 (received for review April 3, 2020) The global movement of pathogens is altering populations and densities in either fecundity or juvenile survival. The assumption communities through a variety of direct and indirect ecological that such overcompensation occurs is a major element in regu- pathways. The direct effect of a pathogen on a host is reduced lating harvests via hunting and fishing (14–16). Empirical evi- survival, which can lead to decreased population densities. How- dence for its occurrence in nature outside of anthropogenic ever, theory also suggests that increased mortality can lead to no influences is scant. There is evidence for it in some laboratory change or even increases in the density of the host. This paradox- populations (17–19), but experiments with natural predators ical result can occur in a regulated population when the patho- have produced equivocal evidence (20, 21). gen’s negative effect on survival is countered by increased There is even less empirical evidence for overcompensation in reproduction at the lower density. Here, we analyze data from a response to a novel pathogen. Like predators, pathogens are long-term capture–mark–recapture experiment of Trinidadian capable of regulating host populations (e.g., refs. 22–25). How- guppies (Poecilia reticulata) that were recently infected with a ever, there is only a single demonstration that a host population nematode parasite (Camallanus cotti). By comparing the newly is capable of overcompensation in response to the immediate infected population with a control population that was not in- effect of a pathogen (26). fected, we show that decreases in the density of the infected This scarcity of examples could reflect a fundamental difference guppy population were transient. The guppy population compen- between predator–prey and host–parasite systems. In contrast to sated for the decreased survival by a density-dependent increase predator–prey interactions, mortality in host–pathogen systems is not in recruitment of new individuals into the population, without any immediate. A lag in mortality of infected individuals could maintain change in the underlying recruitment function. Increased recruit- host densities high enough that uninfected individuals do not expe- ment was related to an increase in the somatic growth of uninfected rience a competitive release before they, too, become infected. Al- fish. Twenty months into the new invasion, the population had fully ternatively, increased mortality of infected individuals could increase recovered to preinvasion densities even though the prevalence of the per-capita resources available to uninfected individuals, causing infection of fish in the population remained high (72%). These re- an increase in their survival, growth, and reproduction. sults show that density-mediated indirect effects of novel parasites Infections by novel pathogens are usually noticed only long can be positive, not negative, which makes it difficult to extrapolate after the initial invasion. As a consequence, much of what we to how pathogens will affect species interactions in communities. know about the early stages of these invasions is based on We discuss possible hypotheses for the rapid recovery. Significance density-dependent compensation | host–parasite interactions | population dynamics | hydra effect Does increased mortality from novel predators or parasites always lead to decreased prey or host population sizes? Theory ncreased movement of humans and human products around says no, but we have too few examples of such compensatory Ithe globe is breaking down dispersal barriers and increasing the effects to answer this question conclusively. We address this frequency at which pathogens are contacting novel hosts and gap using long-term data from populations recently invaded ecosystems (1, 2). These novel interactions are often detrimental by a nematode parasite. We combine analyses of the subse- to the host populations and are contributing to the decline of quent changes in population dynamics with comparable data natural populations and ecosystems (3–6). While the spread of from an uninfected population and laboratory assays of the pathogens clearly affects wild populations through negative di- effect of the parasite on fitness components. Our results show rect effects on infected individuals, pathogens may also play an that the negative effect of the novel parasite was short-lived. indirect role in restructuring communities via density- and trait- The host population quickly recovered, even while experienc- mediated indirect effects (7, 8). While density-mediated indirect ing high levels of parasite prevalence (72%). Host recovery was effects can, in theory, create new opportunities for competitors a consequence of increased survival and a density-dependent through the reduction in the host population density, theory also increase in recruitment. predicts that increased mortality can lead to little or no change in the host population density or even a counterintuitive increase in Author contributions: E.L.B.R. and R.D.B. designed research; E.L.B.R., A.D.V.A., J.T., D.N.R., host population densities (9–13). T.C., and R.D.B. performed research; E.L.B.R. and R.D.B. analyzed data; and E.L.B.R., From the theoretical perspective, increases in population size A.D.V.A., J.T., D.N.R., T.C., and R.D.B. wrote the paper. with increased mortality can result from several mechanisms (9). The authors declare no competing interest. In stable populations that do not exhibit endogenous cycles, in- This article is a PNAS Direct Submission. creases in equilibrium population size can occur when the mor- Published under the PNAS license. tality imposed by the predator or pathogen precedes the action 1To whom correspondence may be addressed. Email: [email protected]. of the density-dependent response. This can happen, for exam- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ ple, when recruitment of new individuals overcompensates for doi:10.1073/pnas.2006227117/-/DCSupplemental. adult mortality via a response to lowered adult population First published August 26, 2020. 22580–22589 | PNAS | September 8, 2020 | vol. 117 | no. 36 www.pnas.org/cgi/doi/10.1073/pnas.2006227117 Downloaded by guest on September 26, 2021 ABPopulation 3.0 LL (reference) 2.5 CA (infected) 2.0 1.0 1.5 0.5 1.0 1.5 0.5 40 60 80 100 120 40 60 80 100 120 Month of Experiment Month of Experiment CD 0.15 0.20 0.05 0.10 0.1 0.2 0.3 0.4 0.5 0.6 0.0 0.00 40 60 80 100 120 40 60 80 100 120 Month of Experiment Month of Experiment EF POPULATION BIOLOGY 0.8 1.0 0.8 1.0 0.6 0.4 0.4 0.6 40 60 80 100 120 40 60 80 100 120 Month of Experiment Month of Experiment Fig. 1. Female and male population number densities (A and B), biomass densities (C and D), and survival (E and F) in the control (LL: Lower Lalaja) and infected (CA: Caigual) from month 30 to month 131. Month 30 roughly corresponds to when both populations reached their initial peak densities. See SI Appendix, Fig. S1 for individual estimates and SEs for the entire experimental period. The vertical line in each denotes the first month when C. cotti was observed in the infected population (100). This first observation was a late-stage infection in a single individual. Based on the life cycle of C. cotti, the actual initial invasion into the Caigual was likely several months prior. laboratory experiments (27). Studies in nature are also limited by mark–recapture surveys of the guppy populations yield estimates the inability to contrast the effects of a pathogen invasion against of parasite prevalence, number, and biomass densities of gup- the population dynamics and demography of an otherwise pies, probability of survival and capture, recruitment, and the age comparable but uninfected host population. As a result, we know and size structure of the guppy populations (Fig. 1 and SI Ap- little about the ecological and evolutionary dynamics of host pendix, Fig. S1). populations as novel parasites are becoming established and We ask whether the demographic response of the population have few opportunities to test hypotheses about how invasion of shows signs of density-dependent compensation in the numerical pathogens influences the demography of the host. dynamics of the guppy population after the initial invasion of the Here, we examine how the advent of a novel nematode par- parasite and whether any compensation via recruitment occurred asite (Camallanus cotti) alters the demography of Trinidadian through a change in the relationship with density or a simple guppies (Poecilia reticulata) in the wild. Guppies are small live- decrease in density. We asked how the individual cost of infec- bearing fish native to the streams of Trinidad, West Indies. Since tion changed over the course of the invasion by examining the 2008, we have been monitoring the guppy populations in four demographic responses of infected versus noninfected individ- streams on the island through monthly mark–recapture censuses uals across the preinvasion, epidemic, and endemic phases of the of each population (28). Each month we capture the majority of invasion in comparison with the demography of an uninfected the fish in the streams and individually mark them to identify population (Lower Lalaja) over the same time periods.
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