Life history cost of trematode infection in Helisoma anceps using mark-recapture in Charlie's Pond

Parasitism has the potential to affect key life history traits of an infected host. Perhaps the most studied interactions are in snail-trematode systems, where infection can result in altered growth rates, survival, and/or fecundity of the individual. Positive correlations between host size and parasite prevalence are often attributed to changes in growth rates or mortality, which have been observed in the laboratory. Extending lab-based conclusions to the natural setting is problematic, especially when environmental conditions differ between the laboratory and the field. The present study uses reproduction experiments and mark-recapture methods to directly measure key life history traits of the pulmonate snail Helisoma anceps in Charlie's Pond. Based on previous laboratory and field experiments on H. anceps, we predict a significant reduction in fecundity, but not growth rate or survival, of infected snails. Individual capture histories were analyzed with multistate models to obtain estimates of survival and infection probabilities throughout the year. Recaptured individuals were used to calculate specific growth rates. Trematode infection resulted in complete castration of the host. However, neither survival nor growth rates were found to differ between infected and uninfected individuals. The probability of infection exhibited seasonal variation, but it did not vary with size of the snail. These results suggest that the correlation between host size and trematode prevalence is not due to differential mortality or changes in growth rates. Instead, the infection accumulates in large snails via the growth of smaller, infected individuals.     

Long-term analysis of Charlie's Pond: fecundity and trematode communities of Helisoma anceps

Charlie's Pond (North Carolina) harbors a diverse community of trematodes that infect the planorbid snail Helisoma anceps. Research at the Pond began in 1984 and serves as a foundation on which to investigate long-term changes in trematode communities. In 2002, 2005, and 2006 average size and fecundity of H. anceps were calculated each month, and seasonal trends analyzed with randomization tests. Concomitantly, trematode infections were recorded, and the community composition compared to those from previous studies. Helisoma anceps in 2002, 2005, and 2006 were smaller and less fecund than snails in 1984. The trematode community was consistently diverse, with 11 species recovered in 2006 versus 7 in 1984. However, the prevalence of Halipegus occidualis was much lower than previously observed (60% in 1984) and never exceeded 20% during the latter years. The decline of emergent vegetation is likely contributing to these changes. Aquatic macrophytes increase the surface area for growth of periphyton, the food source of these snails. Limited food supplies result in lower snail growth rates and fecundity. Similarly, emergent vegetation creates foci of transmission for H. occidualis between the frog definitive host and the snail intermediate host. When these areas are lost from the Pond, probability of transmission is reduced, and prevalence in the snail declines.     

The relative importance of life-history variables to population growth rate in mammals: Cole's prediction revisited

The relative importance of life-history variables to population growth rate (lambda) has substantial consequences for the study of life-history evolution and for the dynamics of biological populations. Using life-history data for 142 natural populations of mammals, we estimated the elasticity of lambda to changes in age at maturity (alpha), age at last reproduction (omega), juvenile survival (Pj), adult survival (Pa), and fertility (F). Elasticities were then used to quantify the relative importance of alpha, omega, Pj, Pa, and F to lambda and to test theoretical predictions regarding the relative influence on lambda of changes in life-history variables. Neither alpha nor any other single life-history variable had the largest relative influence on lambda in the majority of the populations, and this pattern did not change substantially when effects of phylogeny and body size were statistically removed. Empirical support for theoretical predictions was poor at best. However, analyses of elasticities on the basis of the magnitude (F) and onset (alpha) of reproduction revealed that alpha, followed by F, had the largest relative influence on lambda in populations characterized by early maturity and high reproductive rates, or when F/alpha > 0.60. When maturity was delayed and reproductive rates were low, or when F/alpha < 0.15, survival rates were overwhelmingly most influential, and reproductive parameters (alpha and F) had little relative influence on lambda. Population dynamic consequences of likely responses of biological populations to perturbations in life-history variables are examined, and predictions are made regarding the numerical dynamics of age-structured populations on the basis of values of the F/alpha ratio.     

Genotype frequency differences in Halipegus occidualis-infected and uninfected Helisoma anceps

Allozyme frequencies in Helisoma anceps infected with the hemiurid trematode, Halipegus occidualis, were compared with those of uninfected H. anceps from a small, North Carolina farm pond. Of 6 loci found to be polymorphic, the frequencies of esterase-1 and leucine aminopeptidase were different in infected and uninfected snails. Genetic heterozygosity, as determined by starch gel electrophoresis, was greater in uninfected H. anceps relative to infected individuals. These observations combined with the high prevalence (up to 60%), complete castration in patent infections, and the absence of an encapsulation response in infected snails, suggest that factors conferring incompatibility may have been selected for in the H. anceps population within the pond.     

Field observations on the population dynamics of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara area, Tanzania

The population dynamics of Bulinus globosus were studied in a stream and an adjacent pool near Ifakara, Tanzania. Experiments with caged snails were used to determine fecundity, hatching rates, growth and mortality. Growth and mortality rates were also estimated for the natural population from successive size frequency distributions. Oviposition began in snails as small as 6.6 mm and there was a positive correlation between the size of the snails at oviposition and the number of embryos per egg mass. Fecundity was season-dependent. In the pool, snail growth was constant throughout the year, while in the stream, growth was markedly reduced during the rainy season. Mortality rates correlated with fluctuations in snail population density and were highest during the rainy season and among young snails. The high intrinsic rate of natural increase observed for B. globosus enables it to exist in habitats which alternate frequently between favorable and adverse conditions.     

The component community structure of larval trematodes in the pulmonate snail Helisoma anceps

Factors that affected the component community structure of larval trematodes in the pulmonate snail Helisoma anceps in Charlie's Pond, North Carolina, were studied over a 15-mo period using a multiple mark-recapture protocol. Patent infections of 8 species were observed in 1,485 of 4,899 snails examined. Reproductive activity, population size, and survival rate of the snail population were estimated to evaluate the extent of resource availability for the parasites. Antagonistic interactions between trematode species that occurred at the infracommunity level had a neglible effect on the composition and structure of the component community. The patterns observed at this level were related to temporal heterogeneity in the abundance of infective stages (mostly miracidia), differential responses of trematode species to the diverse and constantly changing distribution of snail size and abundance, differential mortality of snails infected with certain trematode species, constant recruitment of 1 trematode species over time, and the existence of predictable disturbances such as the complete mortality of the host population and recruitment of a replacement population during a 6-8 wk period. The last factor operated as a reset mechanism for this snail-trematode system once each year. A model of patch dynamics, with snails as patch resources, best explains the organization and dynamics of this system.     

Physical and biological processes influencing zonation patterns of a subtidal population of the marine snail, Astraea (Lithopoma) undosa Wood 1828

The population density and size distribution of the marine gastropod, Astraea (Lithopoma) undosa Wood 1828, at Bird Rock, Santa Catalina Island, CA, reveal an inverse relationship between population density and mean individual size, over a depth gradient. This trend may be correlated with physical and biological differences between habitats for parameters such as water motion, competitive interactions, and predation.

The potential effect of hydrodynamic forces on the zonation patterns of Astraea undosa was tested in laboratory and field experiments. Based on theoretical predictions of the relationship between shear force and water velocity on different-sized snails, large snails are subjected to greater shear forces, as a result of water motion, than medium or small snails. Results of dislodgment experiments conducted in the laboratory indicated that for a given force per unit area, all snails dislodged at nearly the same frequency, with 50% of snails predicted to dislodge at about 4 m/s, and 100% of snails predicted to dislodge at about 8 m/s velocity. These results suggest that hydrodynamic forces may be an important factor in the shallowest subtidal zones.

A factorial-designed caging experiment was used to test the effects of snail population density on growth rates of snails of three different size classes. For small and medium size classes, results indicated an inverse relationship between population density and growth rates, which was especially pronounced for smaller snails. These data, in conjunction with long-term patterns of population density and size distribution in the field, suggest that intraspecific competition also plays a role in determining size-specific zonation patterns.

Tethering experiments, used to estimate predation rates in different algal-cover zones, suggest that there are no differences in survival rates among different snail size classes; however, survival rates differ among zones and may contribute further to the observed zonation patterns. Overall, data indicate that a combination of physical and biological processes controls the population density and size-distribution of Astraea undosa over a depth gradient at Santa Catalina Island, California.     

Habitat-specific variation in life-history traits,clonal population structure and parasitism in a freshwater snail (Potamopyrgus antipodarum)

High risk of infection by parasites may select for early reproduction in natural host populations. In a previous study of a freshwater snail (Potamopyrgus antipodarum) we found (1) that different clones of the snail are associated with different depth-structured vegetation zones and (2) that snails in shallow water, where the age-specific risk of infection is highest, mature at a smaller size than snails in deeper habitats. This result suggests that there has been selection for early reproduction in these snails, and that different clonal genotypes have different life-history strategies. Alternatively, the observed life-history variation in the snails might be due to ecological factors that are independent of parasites, but correlated with depth. In the present study, we decoupled parasitism and depth by examining life histories and clonal population structure in a second lake (Lake Tennyson) where the mean prevalence of trematode parasites was low and unrelated to depth. Consistent with the previous results, clones were structured according to vegetation zones in Lake Tennyson. However, we found no relationship between depth and life-history traits, which is inconsistent with the idea that depth-associated factors other than parasites affect snail life histories. Taken together, these results suggest that life-history variation is more likely to result from a depth-specific risk of infection than from depth per se, and that partitioning of habitat zones by different groups of clones may be a general phenomenon in P. antipodarum populations.     

Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia)

Summary This laboratory study examined the influence of parasitic infection by larval trematodes on the survival of extreme environmental conditions by the salt marsh snail, Cerithidea californica. Experimental treatments simulated the durations, combinations, and levels of potentially lethal environmental extremes to which the snail is exposed in its natural habitat, as determined from long-term field measurements. No significant difference was found in the rates of mortality suffered by infected and uninfected snails when exposed to simulated natural extremes of water temperature, water salinity, or exposure in air. Exposure to low levels of dissolved oxygen was the only treatment that caused differential mortality: infected snails died at higher rates than uninfected. This differential mortality was accentuated by high water temperature, and varied with the species of infecting parasite. The potential impact of this interaction between parasitism and anoxia on snail survival and population dynamics is discussed.     

Larval trematode antagonism: principles and possible application as a control method

The main features of trematode antagonism are reviewed briefly, and results of recent field experiments to test whether trematode antagonism can be used for control of trematode infections are discussed. These results show that it is easy to control trematode infections by dispersing large numbers of eggs of a dominant parasite in relatively small bodies of water. Such release may produce a multiple effect: (1) intertrematode antagonism; (2) considerable decrease in the snail population due to higher mortality and parasitic castration of infected snails; and (3) a microsporidan epidemic caused by a hyperparasite, affecting rediae and sporocysts and leading to suppression of cercarial production. Any one or a combination of the three effects may achieve control of the target species. The usefulness of this biological control method depends largely on whether dominant parasites can be found that fulfill the requirements for large-scale application and on whether other factors interfere with antagonism or prevent snails from becoming infected with the dominant speices. A good dominant trematode should be strongly antagonistic to the target species, have a wide geographic distribution, develop rapidly in the snail and cause complete castration, be easily maintained in the laboratory, and preferably be capable of infecting the snail hosts in their various habitats. Development of efficient methods of dispersing eggs and more field experiments are necessary to determine the advantages and limitations of this method.     

Experimental exposure of juvenile snails (Potamopyrgus antipodarum ) to infection by trematode larvae (Microphallus sp.): infectivity, fecundity compensation and growth

Host-parasite interactions that result in host castration are evolutionarily similar to predator-prey interactions because both interactions terminate reproduction for the host or prey. Yet, host-parasite interactions differ from predator-prey interactions in that infected hosts remain alive and potentially can make adjustments to their life-history strategy before castration is complete. Here we exposed juvenile snails (Potamopyrgus antipodarum) to infection by a digenetic trematode (Microphallus sp.) in order to determine whether: (1) pre-reproductive individuals could be infected, (2) individuals that were exposed to infection shifted resources to early reproduction (fecundity compensation), and (3) infected individuals exhibit altered growth rates relative to uninfected individuals. We found that juveniles are susceptible to infection; hence P. antipodarum could be selected for earlier maturation in populations where the risk of infection is high. We also found that fecundity compensation does not occur in this snail. Finally, we found that Microphallus-infected snails exhibit altered growth rates; individuals infected as juveniles have lower growth rates and are smaller than uninfected snails. These results suggest that growth is altered by infection of a trematode parasite but reproduction in uninfected snails is not induced by exposure to trematode eggs. Received: 11 January 1998 / Accepted: 19 May 1998     

Life history of a neotropical marsupial: Evaluating potential contributions of survival and reproduction to population growth rate

The relative effect of survival and reproductive rates to population growth rate is expected to be similar across species with similar life-histories. We employed a matrix population model and sensitivity and elasticity analysis to assess the absolute and relative importance of age-specific survival and fertility to population growth rate of Didelphis aurita (Didelphimorphia, Didelphidae) in a rural area of Rio de Janeiro, southeastern Brazil. The results were compared to expectations for mammals that mature early and have short generation time, such as D. aurita. Prospective analysis showed that changes in pouch young and juveniles survival would have large effects on population growth rate, relative to other vital rates, being the most critical time periods in the life cycle of D. aurita, whereas the effect of fertilities were always low. These findings do not fit to the observed pattern in mammals that mature early, where reproductive parameters have the largest relative influence on population growth rate. Although reproductive rates were characterized by a relatively small influence on population growth rate, they are still relevant because of their high variability and response to potential environmental disturbances. The first application of matrix population models to a neotropical rainforest marsupial provides information on marsupial demography and life-history strategy, increasing comprehension of this unknown group.     

Projected population persistence of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) using a stage-structured life-history model and population viability analysis

The population of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) in the Blue River, Indiana has undergone a dramatic decline over the last decade. Recruitment in these declining populations has been negligible, and populations are now composed almost entirely of older age classes (upwards of 20 years old). Given this dramatic decline, it is imperative to assess the impacts of these demographic patterns on population growth and long-term stability. Therefore, we developed a stage-structured, life-history model to examine the effects of varying levels of egg, juvenile, and adult survivorship on abundance, recruitment, and long-term population projections. We performed a sensitivity analysis of the model and determine which life-history parameters have the greatest potential to increase/stabilise hellbender population growth. Finally, we conducted a population viability analysis to determine the probability of extinction associated with varying management strategies. For eastern hellbender populations in Indiana, adults (especially females) are the most important component of long-term population viability. Sensitivity and elasticity analyses of the Lefkovitch matrix revealed that survival of adult and egg/larvae life-history stages are the most important for focused management efforts. Indeed, adults had the highest elasticity and reproductive value in the matrix model. Increasing survival by as little as 20% corresponded to the turning point at which the population ceased to decline and increased abundance (28% survival of egg/larvae). The importance of the transition from subadult to adult (transitional matrix element) was identified as an additional factor in maintaining abundance based on the relatively long period spent in this life-history stage (seven years for females). A population viability analysis was conducted to assess the likelihood and projected time frame of extinction for this population under no management (～25 years to complete extirpation; probability of extinction = 1) and if management efforts such as captive rearing and headstarting are undertaken (probability of extinction <0.2 at 25–30% survival of egg/larvae). Adult females had the greatest effect in reducing growth rate and population abundance when removed in exploitation simulations (91.3% versus 51.8% reduction in population growth rate), indicating translocation efforts should be designed to maintain females in the breeding pool. These models indicated that conservation management strategies aimed at ensuring the presence of adult females while concomitantly ameliorating survival at early life stages (population augmentation, translocations, introduction of artificial nest structures) are needed to stabilise the Indiana population of eastern hellbenders. This stage-structured model is the first to model eastern hellbenders and has broad implications for use across the geographic range where populations of eastern hellbenders are monitored and vital rates can be estimated.     

Parasitic mites influence fitness components of their host, the land snail Arianta arbustorum

Abstract. Parasites can influence the population dynamics of their hosts by affecting life-history strategies and behavior. The hematophageous mite Riccardoella limacum lives in the lung cavity of terrestrial gastropods. We used correlational and experimental approaches to investigate the influence of parasite infection on the behavior and life-history traits of the simultaneously hermaphroditic land snail Arianta arbustorum , a common host of R. limacum. Naturally infected individuals of A. arbustorum , collected in the wild, showed a decreased activity compared with uninfected snails. The reproductive output, expressed as the number of eggs deposited in a reproductive season, was reduced in mite-infected hosts. However, the hatching success of the eggs laid by parasitized snails was slightly higher than that of uninfected individuals. We also examined winter survival in 361 adults of A. arbustorum collected from four natural populations. The prevalence of mite infection ranged from 44.8% to 70.1% in three populations (snails in the fourth population were not infected). Winter survival was reduced in infected snails in two out of three populations. Furthermore, experimentally infected snails from an uninfected population showed a reduced winter survival compared with control snails. Our results indicate that parasite pressure imposed by members of R. limacum may influence life history in A. arbustorum.     

Density-dependent growth and reproduction of the apple snail, Pomacea canaliculata: a density manipulation experiment in a paddy field

To examine density dependence in the survival, growth, and reproduction of Pomacea canaliculata, we conducted an experiment in which snail densities were manipulated in a paddy field. We released paint-marked snails of 15–20 mm shell height into 12 enclosures (pens) of 16 m² at one of five densities – 8, 16, 32, 64, or 128 snails per pen. The survival rate of released snails was 95% and was independent of snail density. The snail density had a significant effect on the growth and egg production of individual snails. This density dependence may have been caused by reduced food availability. The females at high density deposited fewer and smaller egg masses than those at low density, and consequently produced fewer eggs. The females at densities 8 and 16 deposited more than 3000 eggs per female, while the females at density 128 oviposited only 414 eggs. The total egg production per pen was, however, higher at higher snail density. The survival rates of juvenile snails were 21%–37% and were independent of adult density. The juvenile density was positively correlated with the total egg production per pen and hence was higher at higher adult density. However, the density of juveniles larger than 5 mm in shell height, i.e., juveniles that can survive an overwintering period, was not significantly different among density treatments. These results suggest that snail density after the overwintering period is independent of the density in the previous year. Thus, density dependence in growth and reproduction might regulate the population of P. canaliculata in paddies. Received: October 23, 1998 / Accepted: July 16, 1999     

A stage-based matrix population model of invasive lionfish with implications for control

The rapid invasion of lionfish into the Western North Atlantic and Caribbean will undoubtedly affect native reef fishes via processes such as trophic disruption and niche takeover, yet little is known about the dynamics of this invasion. We constructed a stage-based, matrix population model in which matrix elements were comprised of lower-level parameters. Lionfish vital rates were estimated from existing literature and from new field and laboratory studies. Sensitivity analysis of lower-level parameters revealed that population growth rate is most influenced by larval mortality; elasticity analysis of the matrix indicated strong influence of the adult and juvenile survival elements. Based on this model, approximately 27% of an invading adult lionfish population would have to be removed monthly for abundance to decrease. Hierarchical modeling indicated that this point estimate falls within a broad uncertainty interval which could result from imprecise estimates of life-history parameters. The model demonstrated that sustained removal efforts could be substantially more effective by targeting juveniles as well as adults.     

The unusual life cycle of Daubaylia potomaca, a nematode parasite of Helisoma anceps

Daubaylia potomaca is a parasitic nematode that exhibits a direct life cycle using planorbid snails as their only host. Within the snail host Helisoma anceps , all developmental stages of the parasite are present at any given time. The nematode has an unusual life cycle, with the adult female being the infective stage rather than the third-stage larvae (L(3)), as is commonly the case in many other parasitic nematode life cycles. In addition, length analysis showed that L(1) and L(2) were not present in tissues, suggesting that larvae hatch from eggs as the L(3). Previous studies by other investigators show that adult females abandon Biomphalaria glabrata at some point between 3 and 9 days of host death; in the present study, adult female D. potomaca leave H. anceps up to 59 days (and a mean of 14.8 days) before host death. This observation indicates a striking physiological difference between an experimental and a natural host for the parasite.     

The combined effect of isolation and Fasciola hepatica infection on the life history traits of Fossaria cubensis.

Life history traits of Fossaria cubensis were compared between isolated and paired snails after infection with three miracidia of Fasciola hepatica. Four experimental groups were tested: isolated-unexposed, paired-unexposed, isolated-infected, and paired-infected. A repeated-measures ANOVA showed statistically significant interactions among isolation, infection, and age effects for shell size, number of egg masses per snail, number of eggs per snail, and number of viable eggs per snail. Isolated-unexposed snails exhibited the higher values of these variables and those of survival and finite and intrinsic rates of natural increase. Infection stimulated shell growth during the prepatent period, but differences were present only in paired snails since isolation causes a similar effect. Reproduction, in terms of the number of egg masses per snail and the number of eggs per mass per snail, decreases in the presence of parasitic infection, whereas isolation stimulates it. These effects were observed from early stages of infection.     

Life-history traits of Fossaria cubensis (Gastropoda: Lymnaeidae) under experimental exposure to Fasciola hepatica (Trematoda: Digenea)

The effect of exposing the lymnaeid snail Fossaria cubensis to the trematode Fasciola hepatica on the snail population's life-history traits was studied under laboratory conditions. Exposed individuals showed a lower survival rate than control snails, although from week 7 onward a slower decrease of this parameter in relation to the control group was observed. There were higher values of fecundity rate for the controls compared to the exposed group except during weeks 9, 10, 11 and 12, which was the time that followed the period when almost all of the infected snails died. Both the intrinsic and finite rates of natural increase were significantly higher for the control group, but exposed snails still attained a lower mean generation time. Age-specific trade-offs were found, mainly for the weekly increase in size versus the number of eggs per mass, the weekly increase in size versus the number of viable eggs per mass, the number of masses versus the hatching probability and the number of eggs versus the hatching probability. All these negative associations were significant for juveniles of both control and exposed snails and not for adults; however, exposed young individuals exhibited much higher values of the correlation coefficient than control animals.     

Host life history and the effect of parasitic castration on growth: A field study of Cerithidea californica Haldeman (Gastropoda : Prosobranchia) and its trematode parasites

The prevalence of parasitic infection by larval digenetic trematodes in natural populations of the mud snail, Cerithidea californica Haldeman, was found to increase with snail length; all snails ≥ 33 mm were infected. Distributions of infections by the seven most common larval trematodes were heterogeneous due to two species being more common than expected in the smaller size classes of snails, two being more common than expected in the larger size-classes of snails and three species being most prevalent in snails of intermediate length. The relative abundances of trematodes in different size-classes reflected these distributional patterns.A mark-recapture field study of snail growth rates failed to demonstrate that parasitic infection causes gigantism in Cerithidea. Parasitism tended to stunt the growth of juvenile snails and to a lesser degree, that of adult snails. The effects of trematodes on snail growth was shown to be species specific. This finding contrasts with those of earlier studies in which gigantic growth was observed in infected snails. This discrepancy is attributed to differences in the life histories of the host snails. It is predicted that gigantism will occur commonly in short-lived or semelparous species of snails but rarely, if ever, in long-lived iteroparous species which are predominately marine.