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
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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
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EF POPULATION BIOLOGY 0.8 1.0 0.8 1.0 0.6 0.4 0.4 0.6
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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. We also individuals over capture periods (average probability of capture asked how the demography of uninfected individuals in the in- 89.1%; see Materials and Methods for details). In June 2016, one vaded population benefitted from the decreased density. We of the four populations (Caigual) became infected by C. cotti complemented these field data with a laboratory experiment from an unknown source. We monitored guppy populations designed to address how parasite load affects individual growth throughout the invasion of C. cotti in the Caigual. Our monthly and reproduction.
Rogowski et al. PNAS | September 8, 2020 | vol. 117 | no. 36 | 22581 Downloaded by guest on September 26, 2021 Results AB We first observed the invasion of C. cotti in the Caigual (CA) in June 2016, which was the 100th month of the experiment. Our observation coincided with a period of steady decrease in adult survival in the Caigual (Fig. 1). This decrease in adult survival in the Caigual did not occur in the Lower Lalaja (LL), another experimental stream with similar characteristics but that is un- infected by C. cotti. Almost immediately following the invasion of C. cotti in the Caigual, the decrease in survival of infected indi- viduals in the Caigual drastically decreased the number (indi- viduals per square meter) and biomass density (grams per square meter) of guppies in the Caigual compared to the Lower Lalaja (Fig. 1). Both populations experienced a similarly drastic de- C crease in survival between months 105 and 106 due to a large flood (Fig. 1). As the parasite invasion progressed, however, guppy densities recovered in the Caigual through increased re- cruitment. The increase in recruitment was associated with an increase in the somatic growth of uninfected individuals, which can increase the fertility of survivors through body size–fecundity relationships in guppies (29). Eventually, adult survival in- creased, despite no decrease in the observed proportion of in- dividuals infected, and the densities in Caigual returned to the levels in Lower Lalaja. The critical observation is that density began to recover well before adult survival because of the density-dependent compensation occurring through enhanced Fig. 2. The parasite prevalence from monthly mark–recapture and labora- recruitment. This enhanced recruitment arose in response to the tory dissection (A), observed and expected number of parasites per host reduced population density and via a change in the underlying from dissection (B), and the number of parasites as a function of host body recruitment–density function. This entire process unfolded in a length (C). In A, proportion of captured individual females observed with ∼ late-stage infections in the Caigual until month 141 (black lines) and pro- period of about 20 mo, which is the equivalent of 3.5 guppy portion of dissected individuals observed infected for month 131 collection generations. (red dot). For the monthly captures, individuals were considered infected when the adult C. cotti worms were protruding from the anus of the fish. Late-Stage Infections Appeared in Month 100. The observation of C. Fish that are infected by earlier parasite stages cannot be identified in the cotti infection began at month 100 with only a few individuals and field. Thus, these estimates represent a minimum proportion of infected quickly spread so that over 15% of the population was observed individuals. Dissection of a sample of fish at month 131 showed that 72% of infected with late-stage infections (Fig. 2A). The onset of in- the fish carried C. cotti at various stages of development (see Results for fection occurred earlier than month 100, and the prevalence of details). In B, bars represent the observed number of 104 fish with parasite C. cotti counts along the x axis. The solid black line represents the expected number infections was probably higher than we estimated. This is of fish assuming parasites are distributed according to a Poisson distribution because we can only detect the presence of C. cotti in living fish (see Results for details and tests). In C, black symbols represent the observed during the final stage of infection when individual females pro- number of parasites for fish of various sizes, and the red line is the best-fit trude outside the anus of the fish to release infective larvae (see line including linear and quadratic terms for fish (host) size. Materials and Methods for details). Female nematodes require ∼110 d to mature after infecting a fish (30). Dissection of 104 female fish, collected from the Caigual just Invasion of the Parasite Initially Decreased Population Densities by downstream of our censused portion of the stream at month 131, Decreasing Adult Survival. In our analyses below, we assume that C. cotti confirmed that 75 (72%) of the fish in the Caigual carried the months 30 to 100 of the experiment represent a “preinva- in various stages of development. This is much higher than the sion” period. We then divide the period when C. cotti was ob- maximum parasite prevalence calculated from observations of served in the population (“postinvasion”) into “epidemic” the late stage of the infection during our monthly census (17.8%) (months 100 to 110) and “endemic” (months 111 to 131) periods because our censuses only reveal individuals harboring mature for analysis. parasites. Only 8% of the 104 dissected fish were infected with Analyses of covariance showed that the temporal trends in mature parasites that yielded visible signs of infection, which is population density and biomass density differed between the similar to the observed average prevalence of 5.4% in the infected and uninfected populations across the preinvasion and monthly census. postinvasion periods. For both females and males, this repre- A goodness-of-fit test against a Poisson distribution of dis- sented a significant change in the dynamics during the preinva- sected fish showed that the parasite incidence was overdispersed: sion and postinvasion periods for number density [period × Light infections and heavy infections were greater than expected density: females: F(1,98) = 11.2, P = 0.001, males: F(1,98) = 7.75, by chance (χ2 = 74.6, df = 9, P < 0.001; μ = 2.54, σ2 = 6.76; P = 0.006; Fig. 3 A and B] and for biomass density [period × B Fig. 2 ). A generalized linear model with quasi-Poisson errors density: females: F(1,98) = 11.9, P = 0.001, males: F(1,98) = 10.7, and predictors for linear and quadratic effects of guppy size [as P = 0.001; Fig. 3 C and D]. Prior to observation of C. cotti in the standard length (SL)] showed that the number of parasites in- Caigual, the number densities of females and males in the Caigual F = P < creased with host size [SL: (101) 20.0, 0.001; Fig. 2] and and Lower Lalaja were positively correlated with each other that intermediate-sized fish had more parasites than smaller and [females: F(1,98) = 31.5, P < 0.001, males: F(1,98) = 30.3, P < 0.001; 2 larger fish [SL : F(101) = 16.4, P < 0.001; Fig. 2C]. The quasi- Fig. 3 A and B], suggesting that the dynamics in each of the Poisson dispersion parameter was 1.82, indicating significant populations was driven by the same ecological factors. Following overdispersion remained even after accounting for body size. the invasion of C. cotti into the Caigual, female and male number
22582 | www.pnas.org/cgi/doi/10.1073/pnas.2006227117 Rogowski et al. Downloaded by guest on September 26, 2021 AB distribution showed that guppies with detectable late-stage in- fections in the epidemic period were 44.2% less likely to survive to the following month compared to guppies in the preinvasion period [F(1,95) = 108.7, P < 0.001] and 49.3% less likely to survive than contemporaries without late-stage infections [F(1,95) = 92.8, P < 0.001]. Compared to survival in the preinvasion period, guppies that were not visibly infected during the epidemic ex- perienced only a 10.4% decrease in survival [F(1,95) = 13.3, P < 0.001]. This decrease in the survival of guppies that were not visibly infected may indicate that early-stage infection, which cannot be detected in live fish, was detrimental to survival. Survival of females in the Lower Lalaja did not change between F = P = CDthe preinvasion and epidemic periods [ (1,95) 0.45, 0.503]. In the endemic period (months 111 to 130), mean female survival in the infected Caigual increased relative to the epi- demic period [Fig. 4A: F(1,99) = 25.5, P < 0.001]. The increase in survival was greater than the increase in survival in the Lower Lalaja across the same period [F(1,99) = 17.0, P < 0.001] and eventually attained a similar level as female survival in the un- infected Lower Lalaja [F(1,99) = 3.87, P = 0.052]. This increase in female survival in the Caigual was driven by an increase in sur- vival of both fish that were and were not visibly infected (Fig. 4B). The probability of survival for fish with late-stage in- fections increased 60.2% between the epidemic and endemic periods of the invasion [Fig. 4B: F(1,95) = 15.8, P < 0.001], while survival for fish that were not observed to have late-stage in- Fig. 3. Mean female and male number density (A and B) and biomass fections also increased by 15.2% [F = 19.3, P < 0.001]. The density (C and D) preinvasion and postinvasion (epidemic and endemic pe- (1,95)
riods) in the Caigual. The preinvasion period corresponds to months 30 to probability of survival of fish without visible infections in the POPULATION BIOLOGY 100 of the experiment. C. cotti was first observed in month 100. The post- endemic period did not differ from that in the Lower Lalaja invasion period represents months 100 to 131 of the experiment. Prior to [F(1,95) = 0.769, P = 0.383]. invasion, the number and biomass dynamics between the two populations were correlated with each other. In the postinvasion period, they were Increased Density-Dependent Recruitment Compensated for Lower significantly different from each other (see Results for details). Survival. Increased recruitment of juvenile individuals during the invasion compensated for the decrease in adult survival (Fig. 5A), and ultimately buoyed the population against more densities between the two populations were no longer corre- drastic declines in population density. We used a general linear lated with each other [females: F(1,98) = 0.048, P = 0.827; males: mixed model with per-capita recruit density as the dependent F(1,98) = 0.677, P = 0.413; Fig. 3 A and B]. This was also the case variable, population, infection period, and their interaction as for biomass density. Prior to invasion of C. cotti, the biomass fixed effects, and sampling month as a random effect to show dynamics between the populations were correlated with each that the change in the rate of female recruitment from the other [females: F(1,98) = 25.1, P < 0.001; males: F(1,98) = 34.7, P < 0.001; Fig. 3 C and D] and following the invasion they were not [females: F(1,98) = 0.058, P = 0.811; males: F(1,98) = 0.717, AB P = 0.399; Fig. 3 C and D]. The invasion of C. cotti decreased population sizes in the Caigual by decreasing adult survival (Fig. 4A). A general linear mixed model with logit transformed survival estimates as a de- pendent variable, population, infection period, and their inter- action as fixed effects, and sampling month as a random effect showed that mean female survival probability was 24.7% lower in the Caigual during the 10 mo of the epidemic period as com- pared to the average survival across the 70 mo of the preinvasion period [months 100 to 110 vs. 30 to 99: F(1,99) = 16.3, P < 0.001]. In contrast, mean female survival in the uninfected Lower Lalaja did not change over the same time period [months 100 to 110 vs. F = P = Fig. 4. (A) Time course of monthly survival probabilities of females in the 30 to 99: (1,99) 0.780, 0.379]. The decline in survival in the infected population (CA: Caigual) and a reference population that is not Caigual actually began a few months prior to our initial obser- infected (LL: Lower Lalaja). Vertical lines delineate the preinvasion, epi- vation of the parasite (Fig. 4A), which coincides with the 3- to demic, and endemic periods used in the analyses. The preinvasion period 4-month life cycle of C. cotti that precedes the maturation of corresponds to months 30 to 100 of the experiment. C. cotti was first ob- female nematodes and our ability to see them extruded from the served in month 100. The epidemic period represents months from 100 to anus of the host. 110, and the endemic period represents months 111 to 131 of the experi- ment. Error bars of 95% confidence intervals estimated from capture– The decrease in mean female survival in the Caigual during – the epidemic period was largely caused by a decrease in the mark recapture methods (see Materials and Methods). The large decline in B survival at month 105 (November 2016) was due to heavy rains and flooding survival of fish with late-stage infections (Fig. 4 ). A generalized in both streams. (B) Mean monthly survival of females in the preinvasion, linear mixed model with logit-transformed survival between epidemic, and endemic periods in CA and LL. In the Caigual, we calculated months as the dependent variable, population, infection status, survival of individuals that were not observed infected and those that were and infection period as fixed effects, and a binomial error observed infected separately. Error bars are 95% confidence intervals.
Rogowski et al. PNAS | September 8, 2020 | vol. 117 | no. 36 | 22583 Downloaded by guest on September 26, 2021 AB
C
Fig. 5. (A) Mean per-female recruitment of females in infected population (CA: Caigual) and a reference population that is not infected (LL: Lower Lalaja). Vertical lines delineate the preinvasion, epidemic, and endemic periods used in the analyses. The preinvasion period corresponds to months 30 to 100 of the experiment. C. cotti was first observed in month 100. The epidemic period represents months from 100 to 110, and the endemic period represents months 111 to 131 of the experiment. Error bars of 95% confidence intervals estimated from capture–mark–recapture methods (see Materials and Methods). (B) Esti- mated relationship between female recruitment and female density in the Lower Lalaja and Caigual during the preinvasion, epidemic, and endemic periods of the parasite in Caigual. Solid lines are the estimated recruitment relationships for both populations during the preinvasion and endemic periods, and are not significantly different from each other (see Results for details). Dashed line is the estimated relationship during the epidemic period, which is significantly steeper for both populations than the preinvasion and endemic periods (see Results for details). (C) Estimated levels of recruitment in the Lower Lalaja and Caigual during the preinvasion, epidemic, and endemic periods of invasion of the parasite in the Caigual. For each period, the estimate for the Lower Lalaja is for the mean density in the Lower Lalaja during the respective periods. For the Caigual, the gray points represent the mean levels of recruitment assuming the same density as the Lower Lalaja and the black points are the estimated levels of recruitment using the mean densities in the Caigual during the respective periods. Error bars are 95% confidence intervals.
preinvasion period to the epidemic period was much larger in the intercept; Fig. 5 B and C; period; F(2,197) = 8.29, P < 0.001; infected Caigual compared to the Lower Lalaja [population × epidemic vs. preinvasion and endemic: F(1,197) = 11.1, P = 0.001]. period: F(1,99) = 16.7, P < 0.001; Fig. 5C]. Recruitment of fe- Second, there was higher sensitivity to density in the epidemic males in the Caigual was 65% higher during epidemic period period than in the preinvasion or endemic periods [more nega- than the preinvasion period [F(1,99) = 21.7, P < 0.001; Fig. 5C]. tive slope of recruitment on density: period × density; F(2,197) = The rate of female recruitment in the Lower Lalaja did not 2.53, P = 0.083; epidemic vs. preinvasion and endemic: F(1,197) = change across these time periods [F(1,99) = 0.010, P = 0.920; 4.82, P = 0.029]. However, these differences in the relationship Fig. 5C]. between recruitment and density did not differ between the Increases in recruitment levels in the infected population populations [population × period; F(2,192) = 1.49, P = 0.226; could arise through either 1) a change in the relationship be- population × period × density; F(2,192) = 0.064, P = 0.937] and so tween recruitment and density or 2) decreases in density without could not explain the observed difference in recruitment. any change in the recruitment functions. We addressed both We then asked whether the higher levels of recruitment in the questions using a general linear model (glm) with per-capita infected population were due to decreases in density. We used female recruitment as a dependent variable and invasion pe- linear combinations of parameters from the glm to test whether riod, population, female density, and their interactions as pre- differences between the populations during the epidemic period dictors in the model. We first asked whether there was a were due to changes in density. To do so, we first compared the difference in the recruitment function with density and whether levels of recruitment across populations assuming both pop- this difference depended on invasion period and population. ulations had densities observed in the uninfected Lower Lalaja. Prior to invasion of the parasite, the recruitment functions of This density-independent difference between the populations new females into the populations declined with increased female was small [0.037 recruits per female; Fig. 5C: mean of gray circles densities in a similar fashion between populations [Fig. 5B; vs. mean of open circles; F(1,197) = 13.1, P < 0.001]. We then density: F(1,136) = 26.3, P < 0.001; density × population: F(1,136) = asked what additional contribution to recruitment was due to 0.412, P = 0.522]. Recruitment for a given level of density was differences in density by comparing the estimated recruitment in higher in the epidemic period than either the preinvasion or the epidemic period in the Caigual using densities observed in endemic periods. This occurred through two changes. First, the the Lower Lalaja to the level of recruitment estimated using overall level of recruitment in the epidemic period exceeded densities observed in the Caigual. The contribution of decreased those in the preinvasion and endemic periods [increase in the density to the observed difference in recruitment between the
22584 | www.pnas.org/cgi/doi/10.1073/pnas.2006227117 Rogowski et al. Downloaded by guest on September 26, 2021 populations in the epidemic period was large [Fig. 5C: black vs. parameters to test how the decrease in density contributed to gray points; F(1,197) = 26.2, P < 0.001]. The contribution to re- changes in somatic growth. cruitment from decreased density in the infected population was Mean somatic growth of uninfected individuals in the Caigual 3.4 times larger than the density-independent difference [0.124 vs. increased 66% from the preinvasion to the epidemic period −2 0.037 recruits per female per m ;Fig.5C: open vs. gray circles – black [Fig. 6B: black circles, preinvasion vs. epidemic: F(1,68) = 21.2, P < vs. gray circles; F(1,197) = 19.8, P < 0.001]. Overall, this means 0.001]. The somatic growth of individuals in the Lower that the increased levels of recruitment in the Caigual following Lalaja did not change over the same time period [Fig. 6B: open F = P = invasion were due to a decreased density rather than a change in circles, preinvasion vs. epidemic: (1,68) 1.95, 0.167]. The the recruitment function. increase in growth was significantly higher for the uninfected group in the Caigual compared to guppies in the Lower Lalaja Recruitment Increased Because Lowered Densities Promoted Increased [Fig. 6B: black vs. open circles preinvasion – black vs. open cir- Somatic Growth. Decreased density in guppies is known to cause cles epidemic; F(1,68) = 59.4, P < 0.001]. increased fecundity for a given sized individual due to increased The majority of the observed increase in the somatic growth resource availability (29, 31). Increased per-capita resource avail- increment of uninfected fish in the Caigual was due to decreased ability also increases the somatic growth increment of guppies (29, density. Independent of density, fish without visible infection in 31), which can result in elevated fecundity because fecundity in- the Caigual grew significantly less than in the uninfected Lower creases as body size increases. Lalaja during the epidemic [Fig. 6B: epidemic: gray vs. open We asked whether decreases in density in the Caigual during circles: F(1,68) = 11.3, P = 0.001]. This is possibly attributable to a the epidemic and endemic periods increased the somatic growth decrease in the growth of the fish that are carrying early-stage of the uninfected and infected individuals. We included body size infections, but are not counted as infected. Comparing the at the beginning of each sampling month, density, invasion pe- growth of apparently uninfected fish in the Caigual using riod, population, infected status and their interactions with initial the density of fish in the Lower Lalaja or the density of fish in the size and density in a glm and used linear combinations of the Caigual shows that the effect of decreased density on somatic
AB POPULATION BIOLOGY
CD
Fig. 6. (A) Somatic growth increment versus somatic mass for female guppies at the beginning of the monthly interval. (B) Estimated mean growth in- crements and SEs for 0.1-g female guppies during the preinvasion, epidemic, and endemic periods of invasion of C. cotti at month 100. The preinvasion period corresponds to months 30 to 100 of the experiment. C. cotti was first observed in month 100. The epidemic period represents months from 100 to 110, and the endemic period represents months 111 to 131 of the experiment. For each period, the estimate for the Lower Lalaja is for a 0.1-g fish at the mean density in the Lower Lalaja during the respective periods. For the Caigual, the gray points represent the mean levels of somatic growth of an uninfected 0.1-g fish assuming the same density as the Lower Lalaja, and the black points are the estimated levels of somatic growth using the mean densities in the Caigual during the respective periods. Black triangles are the estimated somatic growth increments of an infected 0.1-g fish at the mean density observed in the Caigual. The difference between the gray and black circles during the invasion period is an estimate of the effect of reduced densities of fish on growth. Histogramsofthe size distributions of (C) uninfected and (D) infected fish in the Caigual in the epidemic and endemic periods. In all cases, infected means that the fish was observed to have late-stage C. cotti during the monthly capture event. Actual levels of infection are known to be considerably higher (see Results for details).
Rogowski et al. PNAS | September 8, 2020 | vol. 117 | no. 36 | 22585 Downloaded by guest on September 26, 2021 growth increment was large [Fig. 6B: epidemic gray vs. black We did not find evidence for a transient or permanent in- circles; F(1,68) = 55.5, P < 0.001]. This density effect was larger crease in population size with increased mortality. Instead, the than the stream effect [Fig. 6B: epidemic open vs. gray circles – population size of the infected Caigual initially decreased with black vs. gray circles; F(1,68) = 29.6, P < 0.001] and is attributable increased mortality. Recruitment in the Caigual then increased, to the decreased survival of fish in the Caigual. but this change could only partially compensate for decreased survival. Part of this increase in recruitment resulted from a A Laboratory Study Confirmed a Significant Cost of Infection. Our change in the relationship between recruitment and density, but results point toward a significant cost of infection on somatic this change was also observed in the uninfected Lower Lalaja growth and other aspects of reproductive demography. Infected during the same time period; suggesting the change in the re- individuals in the Caigual grew significantly less than visibly cruitment function was due to a common environmental factor uninfected individuals in the epidemic period [Fig. 6B:trianglevs. between the populations. Recovery of preinvasion populations black circle; F(1,68) = 13.1, P = 0.001] and in the endemic period size was attained with a decline in the mortality rate of infected [Fig. 6B: triangle vs. black circle; F(1,68) = 9.63, P = 0.003]. We individuals and a return to the recruitment levels that were ob- confirmed the cost of parasite infection on somatic growth and served during the preinvasion period. other demographic rates in a laboratory experiment using fish A shortcoming of our data on the population dynamics and collected from the Caigual. We collected fish from the Caigual demographic rates from the field is that we can only identify at month 131 (January 2019), fed them a controlled ration of food individuals as infected when female C. cotti protrude from the for 28 d in a laboratory setting, and then dissected them to assess anus of the fish to lay eggs at the late stage of infection. This parasite load (wet mass of parasites in the guts of dissected fish). means that our classification scheme of infected or not infected Somatic growth decreased with increasing body size [t(1,91) = 13.4, individuals groups fish with early-stage infections with uninfected fish, making our statistical comparisons between infected and P < 0.001] and decreased with increasing parasite load [t(1,91) = 2.43, P = 0.017], measured as the wet mass of the parasites at the uninfected fish conservative. Our laboratory study shows that end of the growth trials. The growth of larger fish was less affected parasites from all developmental stages significantly reduced the growth and reproductive performance of the guppies and that by parasite load [length × load: t(1,91) = 12.7, P = 0.047]. Among the infected fish, parasite load ranged from 0.2 to 31.6 mg and was the magnitude of the impact increases with parasite load. De- only weakly associated with the length of the fish at the beginning spite this limitation, we found that late-stage infected fish paid a large cost compared to the uninfected individuals in the same of the experiment [t(1,74) = 1.23, P = 0.222]. Female fish with higher parasite loads were also less likely to be pregnant at the population during the epidemic, while the demographic perfor- mance of our uninfected class of fish was often higher than the end of the experiment [t(1,92) = 2.32, P = 0.020]. Those fish with higher parasite loads that were pregnant also had more aborted uninfected control population. embryosorunfertilizedeggscomparedtofishwithlowerpar- One of the most striking observations of the time course of a asite loads [t = 2.30, P = 0.024] even after controlling for novel parasite invasion was how rapidly the guppy population (1,71) recovered following C. cotti invasion. While the initial invasion of body size [t = 4.64, P < 0.001] and the number of viable (1,71) C. cotti initiated a decline in the population size of guppies, the offspring [t = 4.52, P < 0.001]. Parasite load did not sig- (1,71) populations had recovered after about 20 mo and much of the nificantly affect the number of offspring a female carried if recovery comprised an increase in survival of infected individuals. pregnant or the size of offspring (all P > 0.64). There are at least four hypotheses for this rapid recovery. Discussion First, the prevalence of infection in the guppies in the Caigual might have been substantially lower at the end of the 20-mo The introduction of novel parasites can have large detrimental period due to increased guppy resistance to infection that de- effects on natural populations, communities, and ecosystems veloped during the period on which we have focused. In fact, (3–6). Predicting how ecosystems may change through indirect prevalence of late-stage parasites remained at the levels ob- pathways depends on whether mortality due to parasitism will served in the epidemic period through the end of 2019 and 72% decrease or increase the population size of the host (7, 8). Here, C. cotti of dissected individuals had parasites of various stages of de- we showed that the invasion of a novel parasite ( ) velopment (Fig. 2). Second, guppies may have rapidly developed yielded no long-term change in the population size of the host P. reticulata or evolved increased tolerance to the parasite. The high parasite ( ). This lack of a long-term change occurred despite prevalence combined with increased survival of infected guppies the parasites initially producing a large survival cost to infected during the endemic period supports this as a possibility. Third, C. individuals, which caused the population to decline. The re- cotti may have evolved decreased virulence during the course of covery of the initial population size was driven by two the initial invasion. The large decreases in survival of the guppy mechanisms. First, the decreased densities promoted partial hosts early in the invasion suggests that a significant fraction of density compensation through increased recruitment, which the C. cotti may have killed the host before they themselves were couldhavebeendrivenbyanincreaseinthefecundityof able to reproduce. Whether these hypotheses can explain the survivors, increased prerecruitment survival, or through in- observed population dynamics remains to be tested, but the in- creased somatic growth. Second, longer-term recovery of the crease in survival of infected individuals while the prevalence of population resulted from an increase in survival, even though infection remained high may reflect increased tolerance either prevalence of infection remained high (72% of females at from guppy evolution (33, 34), effects of plasticity on the im- month 131). mune system, or decreased virulence of the parasite. From a theoretical perspective, an increase in mortality can A possible fourth hypothesis is based on expanding our view of result in a decrease, no change, or an increase in the equilibrium the interaction with the other fish in the system, the killifish population size. There are a variety of mechanisms that can lead (Rivulus hartii). Guppies and killifish both inhabit the areas of to no change or increased population sizes with increased mor- the streams where our experimental populations live. Killifish tality in a wide variety of models, including unstructured and also live without guppies in areas of the stream immediately stage-structured models (9, 10, 32). In stable populations, this upstream from these experimental populations. When they live can occur when the mortality imposed by the pathogen precedes together, guppies and killifish interact negatively as intraguild the density compensation response in time, such that the density predators. Killifish densities are lower where they live with compensation responds to the decreased population size result- guppies compared to where they do not (35, 36). The killifish in ing from the imposed mortality. the Caigual are also infected with the parasite. Because C. cotti
22586 | www.pnas.org/cgi/doi/10.1073/pnas.2006227117 Rogowski et al. Downloaded by guest on September 26, 2021 infects both species, it could act similarly to a predator and We established four experimental populations of guppies in the upper mediate the interactions between the species (37). In this light, Guanapo drainage in the Northern Mountain Range of Trinidad, West Indies. the rapid recovery of the guppy population could have occurred Data collection was conducted under Institutional Animal Care and Use because C. cotti evolved to more effectively parasitize killifish. Committee Animal Use Protocols from Williams College (BR-17) and the This hypothesis could explain the recovery of the guppy pop- Unversity of California, Riverside (A20170006). All four populations were ulation through two different pathways. First, as the parasite established from a single source population on the lower Guanapo River where guppies live in diverse fish communities and with other species that evolved to become more virulent in killifish, it would decrease frequently prey upon guppies. The guppies from these high predation the effects of competition and predation on guppies through communities were moved to the experimental streams, which previously lowered killifish population sizes. Second, if there were a trade- lacked guppies, but were otherwise similar to natural upstream locations off between the ability of the parasite to infect each species, then without predators. Upstream barriers prevent the upstream movement of an increased virulence in killifish could be associated with a guppies out of the experimental populations. More details of the experi- decreased virulence in guppies. mental translocations can be found elsewhere (28, 40, 41). The structure of the stream communities in Trinidad makes During our monthly recapture, each fish greater than 14-mm SL is mea- this hypothesis plausible. Immediately above our experimental sured for mass, photographed, and if not previously marked, marked with a communities with guppies and killifish are stream reaches that unique color combination of subcutaneous elastomer implants (Northwest contain only killifish (28). The killifish in this guppy-free stream Marine Technologies). Each fish receives two colors in two of eight locations reach are also infected with C. cotti. Without guppies, killifish on the body, allowing us to individually identify 4,032 fish of each sex. Fish are and C. cotti could wage a coevolutionary arms race unimpeded lightly anesthetized with MS-222 for processing, housed overnight in med- by any other potential host species. A by-product of this arms icated water to prevent infections from marking, and returned to the race is that C. cotti larvae, adapted to killifish, could be washed streams the following day. down and infect both guppies and killifish in our experimental In June 2016, one of the four experimental populations (Caigual) became infected with the nematode Camallanus cotti. We had never observed C. stream reach. The recovery of guppy population could then result, cotti in any of the fish in any of the streams on the island prior to this initial not from the adaptation of the guppies to the parasite, but rather observation in the Caigual. Since this initial observation, C. cotti has become from the adaptation of the parasite to killifish. The more intense – endemic in the Caigual, infecting both guppies and killifish. Camallanus cotti killifish parasite interactions upstream could result in parasites is native to Asia and has spread to other continents via the pet trade (42). that are less successful at infecting guppies downstream. Unlike other species in the genus, C. cotti does not require intermediate The results we present here are from a single instance of the cyclopoid copepod host; it can directly infect the final host (30, 43). It can invasion of C. cotti, and so we are unable to say, for now, if the also infect a wide variety of fish taxa. C. cotti is ovoviviparous with females POPULATION BIOLOGY recovery we observed will play out in the same way in other in- releasing larvae that are motile and can directly infect copepods or fish (43). vasions of C. cotti.However,C. cotti has been observed in other After being ingested, the larvae then mature from first-stage larvae to independent drainages with similar and more complex fish as- fourth-stage larvae (30). The worms feed and grow in the host’s gut, semblages and is poised to become a ubiquitous member of the eventually becoming sexually mature male or female worms. While in the stream communities in Trinidad. Understanding how interactions fish, the worms latch on the host’s gut with its buccal capsule and feed on ’ between C. cotti and the fish communities evolve is important the fish s blood or tissue fluid (44). Infection by the worm can cause rectal from both basic knowledge and conservation perspectives. inflammation, anemia, and emaciation (45). The maximum time for the How will these novel interactions affect the structure of eco- larvae to develop from first-stage larvae to mature adults is thought to be about 110 d (30). After mating, mature, red-colored (due to blood feeding) systems and alter the flow of energy and matter? While our females protrude from the fish’s anus and release first-stage larvae into the hypotheses are relevant to this system, they also apply broadly to water. The larvae settle to the stream bed where they can survive for up to natural systems where novel pathogens are rapidly spreading. 3 wk (30). Each captured fish is visually inspected for C. cotti during pro- The impact of these novel pathogens on the recipient commu- cessing. The parasite is easily visible with the naked eye or under a dissecting nities and ecosystems will depend on the interactions among microscope during the late stage of infection when they protrude from the different host and pathogen species and how these communities anus of infected individuals. change across the landscape with varying levels of connectivity. In some cases, these novel interactions will be on par with the Estimates of Population Size, Survival, and Recruitment. We estimated the types of changes that are observed when predators are intro- population size, survival, and recruitment of females and male guppies in the duced or removed (38). population using the POPAN module of program MARK implemented in Our theoretical and empirical work with guppies in Trini- program R. For each population, we fitted models that were fully time de- dadian streams, mesocosms, and the laboratory have shown that pendent (apparent survival and probability of capture) and crossed by sex. evolutionary change and the resultant communities are initiated Because our populations are introduced and we know exactly how many by a change in predation regime and subsequently depend upon individuals were released into each stream, we constrained the probably of capture parameter for the first time period (ρ ) to be equal to unity. Other interactions between ecological and evolutionary processes (e.g., t=1 than this parameter, the default settings were used for each model. refs. 28, 29, 39, and 40). Addressing hypotheses about the role of novel infections in structuring communities will require a similar Selection of Time Periods to Analyze. Following the introduction of guppies synergistic approach that confronts theory with data in replicated into the experimental reaches, both of the introduced guppy populations invasion events across the landscape as the novel interactions increased in size rapidly and then declined (SI Appendix, Fig. S1). We limited unfold. We are well placed to do so. Whether changes in novel our analysis of population dynamics to time periods after which both pop- pathogens will lead to the same types of dynamic interactions ulations reached their initial peak and declined (month 30 of the experi- between evolution and ecology at the ecosystem level remains to ment). More individuals were introduced into the Caigual (52 male female be characterized. pairs) than Lower Lalaja (38 male female pairs). We considered the time period from month 30 to month 99 as the preinvasion time period. Our first Materials and Methods observation of late-stage parasites in the Caigual occurred in month 100, Experimental Populations. Guppies are small live-bearing fish that inhabit the and we considered month 100 to month 110 as the epidemic time period. streams on the island of Trinidad. In lowland areas, guppies live in diverse This duration is rather arbitrary, but roughly corresponds to two guppy fish communities that contain a number of predatory species. Upstream, generations and is about the time when the observed prevalence of late- most other fish species are excluded from the streams by barrier waterfalls. stage infection roughly settled (Fig. 2). We considered the time period Here, guppies live with only one other fish species, Hart’s killifish (Rivulus after month 110 as the endemic period. We ended our analysis at month 131 hartii). Further upstream, additional barrier waterfalls exclude guppies and when we conducted the laboratory study of the effect of parasite load on killifish live by themselves. growth and reproduction in a subset of the population.
Rogowski et al. PNAS | September 8, 2020 | vol. 117 | no. 36 | 22587 Downloaded by guest on September 26, 2021 Statistical Analyses of Population Data. infection status affected somatic growth using a generalized linear mixed Temporal correlations. We analyzed the change in the temporal correlation model. We used the change in mass (grams) over two consecutive capture between the populations (Fig. 3) using a glm with female or male number periods as a dependent variable and included mass at the beginning of the density in the Lower Lalaja as the dependent variable. Female number interval, infection period, estimated female density, a composite variable density in the Caigual, time period (preinvasion vs. combined epidemic and representing population and infection status, and all of their interactions as endemic period), and the interaction between female density in the Caigual fixed predictors. Sampling period was entered as random effect on the in- and time period were predictors. We grouped the epidemic and endemic tercept, and errors were assumed to be normally distributed. The four-way time periods into a postinvasion period for this analysis so we could inves- interaction was significant (P < 0.05), and so we retained all of the predic- tigate how population sizes differed with and without C. cotti. We exam- tors, reran the model using a means parameterization, and constructed ined the interaction between density and period to ask whether the linear combinations from the multiple-effects parameters. The means pa- correlations between densities of guppies in the streams differed between rameterization retains the effects associated with each level of predictors, the time periods. We then examined whether the correlations within each but simplifies the construction of the contrasts from the linear model. We time period were significant using linear combinations of parameters from then constructed similar linear combinations of predictors to answer similar the glm and F tests. We also performed the same analysis on biomass density questions as were asked about the recruitment data. We created a coun- to ask whether there were unique signatures of the invasion on the two terfactual outcome by using density data from Lower Lalaja as the predictor measures of density. for Caigual and used this to evaluate whether the differences in density Population-level survival. We compared mean female survival across time pe- between the two populations could account for the observed differences in riods (preinvasion, epidemic, and endemic) and between populations using a somatic growth between the periods among uninfected individuals in the glm analysis on the estimated mean survival probabilities from the POPAN Caigual. We also present contrasts for the infected individuals and compare analysis. Logit-transformed monthly survival was used as a dependent vari- them to the uninfected individuals in the Caigual under densities observed able with time period, population, and their interaction entered as fixed for the Caigual. effects. Using the estimated parameters from this model, we created linear combinations of parameters and SEs to test how the survival changed in the Laboratory Experiment. We conducted a laboratory experiment to confirm Caigual and Lower Lalaja comparing preinvasion and epidemic time periods. the cost of the parasite infection to somatic growth and to ask whether The magnitude of the changes was assessed via percent differences of the parasite load influences individual level reproduction. Since only the most back-transformed estimates. We subsequently asked how the change in mature worms are externally visible, and thus only the most advanced stages survival differed between the populations using an interaction contrast that of infection can be identified under the stereomicroscope during monthly compared the difference between the two populations during the prein- processing, the dissections conducted during the laboratory-based portion of vasion to the difference during the epidemic period. this experiment allowed earlier stages of infection to be identified and Survival as a function of infection status. We asked whether the decrease in the provided a better measure of the true proportion prevalence of C. cotti in survival of the fish in the Caigual could be due to the parasite infection via a the population and the demographic costs to the fish associated with other generalized linear mixed model analysis of the raw capture data. Each in- stages of development of the parasite. dividual was given a survival value of 1 for each of the captures they were Experimental design. Each of the experimental streams are bounded by barrier observed alive and a 0 for the capture period they were last observed alive. waterfalls upstream to prevent the movement of guppies and to provide a We then used this binomial status as a dependent variable in a linear mixed control community without guppies. Guppies occasionally wash downstream model with survival status as the dependent variable and time period, a from the experimental reaches in high-flow events such that there are ad- composite variable representing the population and infection status, and the ditional sites immediately below a downstream barrier that had previously interaction between these as fixed predictors. We included the sampling been guppy-free but now contain guppies. These additional “extra-limital” sites period crossed with population as a random effect and used a binomial provide a sample of guppies from the initial introduction that are used for distribution for the analysis. We elected to perform this analysis instead of a additional laboratory experiments without disturbing the focal populations. formal multistate mark–recapture analysis for simplicity. Such an analysis Female guppies (n = 104) were collected from the extralimital site in the could introduce strong bias if the capture probabilities were low. Our mean Caigual in January 2019 (month 131). All guppies were caught using but- capture probabilities are relatively high (89.1%), and hence there is little terfly nets and transported back to the field station in 2-L Nalgene bottles scope for an introduction of bias. As in the other analyses, we tested hy- filled with stream water. A wide range of guppy sizes were chosen to un- potheses about the survival of the fish based on period, population, and derstand the impact of the parasite in all life stages and sizes of the fish. The infection status using linear combinations of parameters and assessed the initial SL (distance from the tip of the snout to the hypural plate) of the fish magnitude of the effects via percent differences on back-transformed esti- ranged from 7.99 to 33.35 mm. mates of survival. In the laboratory, the fish were housed in 3-gallon tanks that received Recruitment. We asked whether recruitment of new individuals into the constant aeration and were under ambient temperature and light conditions. population compensated for decreased survival using a glm with per-capita The fish were not marked but were housed individually for the duration of female recruitment estimates from the POPAN model as a dependent vari- the experiment, making them individually identifiable by tank number. The able. We initially included invasion period, population, female density (es- water was changed every third day. timated from the POPAN model), and their full set of interactions as At the start of the experiment and each week thereafter, the SL of each predictors in the model. We sequentially removed terms, beginning with the fish was measured to the nearest 0.01 mm using digital calipers (Mitutoyo) third order term, if the P value for that term was greater than 0.10 (all in- and the fish was weighed to the nearest 0.001 g on an Ohaus Scout scale. teractions except period × female density). We then used linear combina- During these weekly measurements, all fish were individually anesthetized tions of parameters to make two general types of comparisons. First, we with 0.2% Tricaine S (MS-222) and screened for visible signs of infection used the observed mean densities in each of the populations for each of the using a stereo-microscope (Carl Zeiss; Stemi 305). time periods as variables and asked whether there were differences in re- Fish were fed twice daily with live, freshly hatched brine shrimp napauli cruitment in the preinvasion and epidemic periods in each of the pop- (Artemia spp.). Fish were fed food rations proportional to their size using a ulations. We also calculated the difference in the change in recruitment glass microliter syringe (Hamilton 50- or 250-μL micropipette). Food amount between the populations using an interaction contrast between these first was calculated each week according to the fish’s most recent weight, using two time periods. We then asked whether the differences we observed were the following equation: food = mass*e(4−(0.5*mass)). Tanks were checked due to differences in the observed densities between the populations. To do twice daily for offspring and dead fish. Any offspring born during the course this, we used the observed mean densities in the Lower Lalaja for each pe- of the experiment were counted and housed separately from the mother. riod as variables in the linear contrasts. We then asked whether these Fish that died during the course of the experiment were immediately pre- substituted densities produced a significant contrast between the predicted served in 7% buffered formalin and saved for later dissection. values for the Caigual when its own density was used and when the density After 4 wk, the fish were killed with an overdose of MS-222 and preserved of the Lower Lalaja during the invasion period was used. We subsequently in 7% buffered formalin or pure ethanol. Only females were selected for asked whether the levels of recruitment in the epidemic period (using the dissection because we sought to determine the effect of infection on fe- densities from Caigual) differed from those in the preinvasion and cundity (number of embryos) and offspring size. The gastrointestinal tract of epidemic periods. each fish was examined for worms, and if worms were present, the number Somatic growth from the mark–recapture data as a function of infected status. We and wet weight of the worms were recorded to quantify parasite load. The asked whether changes in the somatic growth of uninfected individuals number of embryos and regressors (aborted embryos or unfertilized eggs) contributed to the increased recruitment during the invasion and how was recorded. The somatic tissue, ovary tissue, regressors, and embryos were
22588 | www.pnas.org/cgi/doi/10.1073/pnas.2006227117 Rogowski et al. Downloaded by guest on September 26, 2021 dried at 50 °C for at least 24 h in a drying oven (Quincy Lab Model 40), and the offspring (0 to 50) as offspring decrease in dry mass through develop- dry weights were recorded. ment (31). Only offspring that were greater than stage 0 were used in the Statistical analysis of laboratory data. We analyzed the data from the laboratory analysis because stage 0 offspring are often still being provisioned by the experiment for the effects of infection on the demographic rates using mother and are not full size. generalized linear models. For somatic growth, we calculated the change in SL over the course of the experiment and used this as the dependent variable. Data Accessibility. All data from the natural streams and laboratory experi- For the probability of pregnancy, we entered a 1 for individuals that were ment and code used in the manuscript have been deposited in the publicly observed pregnant at the end of the experiment and a 0 for those that were accessible Dryad Digital Repository (DOI: 10.5061/dryad.jm63xsj7z) (46). not carrying developing embryos. We assumed a binomial error distribution with logit link function for model fitting. For number of offspring and ACKNOWLEDGMENTS. We thank Jogi Ramlal and family for providing aborted or unfertilized embryos (i.e., regressors), we used the natural log of housing and logistical support in Trinidad, Yuridia Reynoso for helping with the count of the number of developing offspring or regressors as the de- data management for the experimental range extensions, and the numer- pendent variable and assumed a quasi-Poisson distribution for the errors. For ous interns who have helped with the monthly mark–recapture experiments offspring size, we used the estimated dry mass of the developing embryos as over the years. We are also indebted to Sonya Auer for reading previous a dependent variable. For each of the analyses, we included SL at the be- drafts of the manuscript and to two anonymous reviewers for their very ginning of the experiment, parasite load estimated at the end of the ex- helpful comments. Parts of the research in this manuscript were completed periment, and their interaction as fixed predictors. For the analysis of the as a senior undergraduate thesis for E.L.B.R. and was partially funded by the regressors, we also included the number of normally developing embryos as Collin and Lili Roche 1993 Student Research Program Fellowship. Other fund- a predictor because individuals carrying more offspring should abort more ing was provided by faculty startup funds to R.D.B. and NSF grants offspring given a constant per-embryo abortion probability. For offspring (EF0623632, 9419823, 1556884) to D.N.R., J.T., and R.D.B. T.C. acknowledges size, we also included an effect of the numerical stage of development of funding through Natural Environment Research Council (Grant ATR00350).
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