No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Parasitic castration: the evolution and ecology of body snatchers
Abstract
Castration is a response to the tradeoff between consumption and longevity faced by parasites. Common parasitic castrators include larval trematodes in snails, and isopod and barnacle parasites of crustaceans. The infected host (with its many unique properties) is the extended phenotype of the parasitic castrator. Because an individual parasitic castrator can usurp all the reproductive energy from a host, and that energy is limited, intra- and interspecific competition among castrators is generally intense. These parasites can be abundant and can substantially depress host density. Host populations subject to high rates of parasitic castration appear to respond by maturing more rapidly.
... The reduction in tissue size, particularly in the gonads, is caused by a variety of factors including the reduced integrity of the mantle tissue as the sporocyst grow, loss of nutrients to the parasites, and potentially toxic metabolites from the parasites (Uzmann 1953). Bivalve hosts will sacrifice reproduction to compensate for the loss of energy caused by the trematodes (Lafferty and Kuris, 2009). The growth of sporocysts within bivalves leads to a mechanical compression within the gonads, preventing gonadal growth and gamete production. ...
... (December 2020 is not shown because although we have trematode infection data for this time point (Fig. 2 and 3) there were no histology samples collected at this time point.) neuroendocrine system of their hosts (Lafferty and Kuris, 2009). In bivalves, trematodes can prevent gametogenesis by inhibiting gonadal mitosis in a dose-dependent manner (Coustau et al., 1993). ...
... In bivalves, trematodes can prevent gametogenesis by inhibiting gonadal mitosis in a dose-dependent manner (Coustau et al., 1993). Similarly in gastropods, larval trematodes disrupt growth and reproduction, leading to castration (Lafferty and Kuris, 2009;Loker and Adema, 1995). ...
... A central strategy of rhizocephalan infection is the coopting of host reproductive investment for parasite growth and reproduction (Høeg, 1995). By targeting resources that would be otherwise "wasted," from its perspective, the rhizocephalan can leave other host functions intact, thereby facilitating both host and parasite longevity at the expense of host reproduction (Baudoin, 1975;Lafferty and Kuris, 2009). Parasitic castration is employed across diverse parasitic taxa, including trematode worms, bopyrid isopods, and various protists (Baudoin, 1975;Lafferty and Kuris, 2009). ...
... By targeting resources that would be otherwise "wasted," from its perspective, the rhizocephalan can leave other host functions intact, thereby facilitating both host and parasite longevity at the expense of host reproduction (Baudoin, 1975;Lafferty and Kuris, 2009). Parasitic castration is employed across diverse parasitic taxa, including trematode worms, bopyrid isopods, and various protists (Baudoin, 1975;Lafferty and Kuris, 2009). Hosts infected by rhizocephalans may have degenerated gonad and/or gametes, reflecting the diversion of resources from their reproduction (e.g., Lützen, 1981;Bower and Boutillier, 1990a;Høeg, 1995;Fazhan et al., 2020). ...
Rhizocephalan barnacles are parasites of crustaceans that are known for dramatic effects on hosts, including parasitic castration, feminization, molt inhibition, and the facilitation of epibiosis. Most research on rhizocephalans has focused on carcinized hosts, with relatively little research directed to shrimp hosts that may experience distinct consequences of infection. Here, we describe a high-prevalence rhizocephalan-shrimp system in which multiple host changes are associated with infection: the dock shrimp Pandalus danae infected by the rhizocephalan Sylon hippolytes. In field-collected P. danae, infection by Sylon was associated with development of female sex characters at a smaller size and greater probability of epibiosis. Standardized video observations showed that infected P. danae performed grooming activities at higher rates than uninfected shrimp, suggesting that inhibited molting rather than direct behavioral modification is a likely mechanism for higher epibiosis rates. There was no difference in the composition of grooming behavior types or in general activity between infected and uninfected shrimp. Fatty acid compositions differed with infection, but total lipid concentrations did not, suggesting that parasite-driven shifts in host resource allocation were compensated or redirected from unmeasured tissues. Our results show that Sylon alters its host's role by provisioning an epibiotic substrate and also that it influences host physiology, resulting in feminization and fatty acid shifts. This study lays the groundwork for expanding rhizocephalan-shrimp research and encourages recognition of oft-ignored roles of parasitism in ecological communities.
... Despite decades of research on both parasites and their impacts on the behavior of grass shrimp, this study represents the first exploration of the interaction between the two. Furthermore, a conflict of interest between castrators and trophically transmitted parasites is considered a potentially strong evolutionary pressure (Lafferty and Kuris 2009;Cezilly et al. 2014) but lacks thorough investigation in a natural system. ...
... Bopyrids consume up to 10% of their host's energy by feeding on hemolymph and can affect respiratory ability, metabolic rate, and oxygen consumption (Chaplin-Ebanks and Curran 2007; Brinton and Curran 2015b). Energy drain caused by the bopyrid "shuts off" reproduction, making the bopyrid isopod a parasitic castrator (Lafferty and Kuris 2009). Male hosts experience reduced reproductive ability, but female hosts are completely sterilized. ...
A conflict of interest occurs when parasites manipulate the behavior of their host in contradictory ways to achieve different goals. In grass shrimp (Palaemonetes pugio), trematode parasites that use shrimp as an intermediate host cause the shrimp to be more active than usual around predators, whereas bopyrid isopod parasites that use shrimp as a final host elicit the opposite response. Since these parasites are altering the host’s behavior in opposing directions, a conflict of interest would occur in co-infected shrimp. Natural selection should favor attempts to resolve this conflict through avoidance, killing, or sabotage. In a field survey of shrimp populations in four tidal creeks in the Cape Fear River, we found a significant negative association between the two parasites. Parasite abundance was negatively correlated in differently sized hosts, suggesting avoidance as a mechanism. Subsequent mortality experiments showed no evidence of early death of co-infected hosts. In behavior trials, co-infected shrimp did not show significantly different behavior from singly infected or uninfected shrimp, suggesting that neither parasite sabotages the manipulation of the other. Taken together, our results suggest that rather than sabotaging or killing one another, bopyrid and trematode parasites tend to infect differently sized hosts, thus avoiding a conflict and confirming the importance of testing assumptions in natural contexts.
... Once it penetrates the first intermediate host, the miracidium further develops and multiplies through asexual reproduction into cercariae, another free-living larval stage of the trematode parasite (Sukhdeo 2012). It is within this first intermediate host that the trematode larvae may usurp energy that the host has allocated to reproduction, essentially castrating the host (Lafferty and Kuris 2009b). Parasitic castration reduces the impact the parasite has on host viability while still accessing large amounts of energy for its own growth. ...
... In this analysis, trematodes disproportionately increased the connectance of the web, thereby increasing stability, yet when represented at the life-stage level they are much more sensitive to secondary extinction, which leads to decreases in stability (Lafferty and Kuris 2009a). These secondary extinctions can have serious consequences for the population size of the freeliving hosts parasitized by trematodes, which could further encourage trophic cascades in the ecosystem benefitting or harming other free-living species as well (Lafferty and Kuris 2009b). Therefore, parasites can be useful bioindicators of degradation and recovery to assess the health of an ecosystem (Lafferty 2012). ...
We compared three sets of highly resolved food webs with and without parasites for a subarctic lake system corresponding to its pelagic and benthic compartments and the whole-lake food web. Key topological food-web metrics were calculated for each set of compartments to explore the role parasites play in food-web topology in these highly contrasting webs. After controlling for effects from differences in web size, we observed similar responses to the addition of parasites in both the pelagic and benthic compartments demonstrated by increases in trophic levels, linkage density, connectance, generality, and vulnerability despite the contrasting composition of free-living and parasitic species between the two compartments. Similar effects on food-web topology can be expected with the inclusion of parasites, regardless of the physical characteristics and taxonomic community compositions of contrasting environments. Additionally, similar increases in key topological metrics were found in the whole-lake food web that combines the pelagic and benthic webs, effects that are comparable to parasite food-web analyses from other systems. These changes in topological metrics are a result of the unique properties of parasites as infectious agents and the links they participate in. Trematodes were key contributors to these results, as these parasites have distinct characteristics in aquatic systems that introduce new link types and increase the food web’s generality and vulnerability disproportionate to other parasites. Our analysis highlights the importance of incorporating parasites, especially trophically transmitted parasites, into food webs as they significantly alter key topological metrics and are thus essential for understanding an ecosystem’s structure and functioning.
... Although correlations between pathogen prevalence and spatial limits of host species have been observed, it is challenging to directly test the hypothesis that pathogens impact species distributions. The impact of disease on host abundance or spatial distribution can be obscured by other factors that also affect host recruitment, such as the immigration of hosts from disease-free zones (Lafferty & Kuris, 2009). Discrepancies between the spatial scale of host recruitment and pathogen transmission could also affect the expected relationship between pathogen prevalence and host abundance. ...
... Whether these effects of habitat variation are observable in pathogen prevalence and abundance data depends critically on how far and how fast the pathogen can spread relative to the scale of variation in habitat. If the pathogen is transmitted broadly relative to variation in habitat quality, then correlations between infection status and abundance may be obscured (Lafferty & Kuris, 2009). In the anther-smut system, most spores are deposited within 1 m of an infected host plant (Bruns et al., 2017). ...
Theoretical models suggest that infectious diseases could play a substantial role in determining the spatial extent of host species, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency‐dependent transmission could have especially strong effects on the limits of species' distributions because diseased hosts that are sterilized but not killed may continue to produce infectious stages and frequency‐dependent transmission mechanisms are effective even at very low population densities. We collected spatial pathogen prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogen Microbotryum dianthorum, a parasite that is spread through both frequency‐dependent (vector‐borne) and density‐dependent (aerial spore transmission) mechanisms. Our 13‐year study reveals rapid declines in population abundance without a compensatory decrease in pathogen prevalence. We apply a stochastic, spatial model of parasite spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency‐dependent and density‐dependent) transmission. We found that the observed rate of population decline could plausibly be explained by multimodal transmission, but is unlikely to be explained by either frequency‐dependent or density‐dependent mechanisms alone. Multimodal pathogen transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature.
... Hence, the prevalence of chronic diseases is higher in regions inhabited predominantly by long-lived individuals. High pathogen load might cause local demographic depression if infections reduce host fecundity [28]. By contrast, shortlived individual populations should harvest fewer pathogens and therefore reproduce faster. ...
... reduce population density [28]. Infertility in humans can result from many chronic viral and bacterial diseases [31][32][33]. ...
Aging is often attributed to the detrimental side effects of beneficial traits but not a programmed adaptive process. Alternatively, the pathogen control hypothesis posits that defense against infectious diseases may provide a strong selection force for restriction of lifespan. Aging might have evolved to remove older individuals who carry chronic diseases that may transmit to their younger kin. Thus, selection for shorter lifespans may benefit kin’s fitness. The pathogen control hypothesis addresses arguments typically raised against adaptive aging concepts: it explains the benefit of shorter lifespan and the absence of mutant variants that do not age. We discuss the consistency and explanatory power of this hypothesis and compare it with classic hypotheses of aging.
... However, it is not clear how C. maenas handles the extra energy requirements of infection. Although some morphological changes induced by Sacculina, such as the size reduction of walking legs (Kristensen et al., 2012) and chelipeds of feminized males (Høeg, 1995;Mouritsen and Jensen, 2006;Lafferty and Kuris, 2009;Kristensen et al., 2012) can impact the crabs' feeding behaviour, host food consumption appears to be unaffected by infection (Larsen et al., 2013). The energy requirements of the parasite should then match the energy which the crab would allocate for its own growth and reproduction (Larsen et al., 2013). ...
... Besides the impact on crabs' growth, Sacculina tend to feminize male hosts both morphological and behaviourally (Høeg, 1995;Mouritsen and Jensen, 2006;Lafferty and Kuris, 2009;Kristensen et al., 2012). In shore crabs, sexual dimorphism is largely confined to a relatively broader abdomen and smaller master chelae in females (Shen, 1935;Elner, 1980). ...
The impact of Sacculina carcini infection on the nutritional status of the shore crab Carcinus maenas was investigated in the western Dutch Wadden Sea for a period of 20 months. About 3.3% of the population was sacculinized, i.e. externally infected with S. carcini and only 0.7% presented scars of previous infection. The results of mixed linear models showed that sacculinized and non-sacculinized crabs had similar morphometric condition, while the energy density of parasitized crabs (externa excluded) was significantly reduced by about 4.3% overall, and by up to 5.8% in crabs under 40 mm carapace width. However, when Sacculina externa was included in the energy determinations, the difference in energy density decreased to 1.2%, while total energy content of the pair infected crab-parasite including externa was 30.8% higher than non-sacculinized crabs of similar size. The total energy content of ovigerous females (eggs included) was even higher, near doubling the energy of similar-sized crabs. The same way, total energy content of Sacculina externa was about 4 times lower than total energy of egg mass. The results suggest that the rhizocephalan parasite is efficient in consuming the energy that the host may allocate for growth and maintenance, but require future studies to disentangle the impact of the degree of internal infection and the implications for the dynamics of the population.
... In contrast, even a single specimen of a "castrator" parasite can annihilate its host's reproductive ability. In doing that, the parasite transforms its host into a walking dead with zero fitness, which constitutes the parasite's extended phenotype [49,50]. This strategy is quite common among parasites, with typical examples of parasitic castrators being larval trematodes infecting snails and parasitic barnacles infecting decapod crustaceans [50]. ...
... In doing that, the parasite transforms its host into a walking dead with zero fitness, which constitutes the parasite's extended phenotype [49,50]. This strategy is quite common among parasites, with typical examples of parasitic castrators being larval trematodes infecting snails and parasitic barnacles infecting decapod crustaceans [50]. ...
Networks offer a convenient model to represent countless real-world situations. The use of networks as a framework to explore ecological complexity has become increasingly popular in the last couple of decades. The study of food webs, which has a long history in ecology, has been complemented by a partially distinct and entirely novel research field focusing on direct, pairwise mutualistic and antagonistic interactions (such as pollination and parasitism). There are obvious conceptual (and sometimes structural) differences between networks that map different kinds of ecological interactions. However, even networks aimed at representing the same ecological entity (e.g. a plant-pollinator system) can be substantially different in terms of the quality and quantity of information they convey. Such differences originate, in most cases, from the challenges in obtaining the relevant ecological data. For example, we might build a plant-pollinator network by spending a few hours in a field looking at flowers and their visiting insects during a single spring day, taking note of each observed visit. Alternatively, we might perform multiple campaigns using sophisticated equipment and performing complementary laboratory experiments. The first network would include basic (and possibly unreliable) information on non-verified interactions between a small set of flowers and insects. It will provide no additional ecological information, such as details on link weights. By contrast, the latter network, built through a substantially higher effort, might include that information level. However, in most real-world cases, technical limitations make it very hard to retrieve all the information that we should ideally include in an ecological network to make it “truly realistic”. Consequently, ecologists often focus on networks that are likely telling only one part of the story. Although the exercise remains extremely valuable, considering the potential data limitations is a crucial step: caution is needed before generalizing results obtained on networks with low informative content since those results might be possibly reversed when additional information is included in the networks.
... The interactions between salamanders and their resident parasites may be particularly important in headwater streams where salamanders are so abundant. Parasites are critical components of the broader ecosystems in which they live because they can affect multiple processes in interactive communities through their influence on host energy budgets (Gé rard and Thé ron 1997), growth (Sorensen and Minchella 1998;Miura et al. 2006), metabolism (Nadler et al. 2021), and reproduction (Sorensen and Minchella 1998;Lafferty and Kuris 2009). Moreover, given the recent emphasis on amphibian disease (Densmore and Green 2007) and the surprising interactions infective parasites can have with other diseases (e.g., Wuerthner et al. 2017), understanding the role that such parasites have on their host's biology is important to the conservation of amphibians. ...
Headwater streams are critical, fragile ecosystems that supply food and nutrients for an array of organisms that are vital to the overall health of a stream. As the dominant vertebrates in headwater streams of the southern Appalachian Mountains, plethodontid salamanders are critical to healthy headwater communities. However, a neglected feature of these ecosystems is the community of parasites that infect salamanders. The digenetic trematode Metagonimoides oregonensis uses the aquatic snail Elimia proxima as its first intermediate host and the plethodontid salamander Desmognathus amphileucus as its second intermediate host. In a series of southern Appalachian streams, we tested the hypothesis that variance in the prevalence and intensity of infection in salamander hosts is related to respective densities of the snail and salamander species. Infection prevalence was 100% across all streams. There was a strong relationship between the density of the snail host and infection-intensity level in the salamander host. However, the relationship with salamander density was not important, a finding that conflicts with the results of parasitological studies involving lentic and marine systems. The influence of this trematode on the ecology of headwater streams and the resident salamanders has been underappreciated, and a number of aspects of this relationship remain unknown.
... Parasitic castration in molluscs has been widely reported [12,19,50]. Lafferty and Kuris [51] indicated that parasitic castration involves mechanical and physiological damage. This damage initially affects the gonads and subsequently alters the overall physiological balance of the host. ...
Simple Summary
The apple snail is one of the most dangerous invasive species in freshwater environments. Using molecular and morphological tools, we re-describe an echinostomatid digenean parasitizing snails from two sites in the Buenos Aires Province, Argentina. The two stages found (i.e., rediae and metacercariae) demonstrate that the apple snail acts as the first and second intermediate host in its life cycle. The prevalence of the parasite was higher at one of the sampling sites, probably because the birds bearing the adult stage are more abundant in that area. A histological study showed that this parasite quickly invades multiple organs of the snail, which is different from most digenean infections, which only infect the gonad and digestive glands. Heavy deterioration of female and male reproductive structures associated with the presence of the parasite was also observed, which indicates castration.
Abstract
Pomacea canaliculata is one of the most dangerous invasive species. Morphological and molecular analyses have revealed that a digenean species belonging to the family Echinostomatidae parasitizes this snail at two sites in Buenos Aires Province, Argentina, South America. Molecular results confirmed that the species belongs to a genus closely related to Patagifer. Analysis of the 28S rDNA showed that the sequences of the rediae and metacercariae are identical, indicating that the apple snail acts as the first and second intermediate host. The cercariae may encyst as metacercaria inside the redia and also emerge and re-infect the same snail or another snail. The prevalence of digeneans was higher in one of the sampling locations (15.1% vs. 0.72%), probably because the bird species that acts as the definitive host is more abundant in that area. Histopathological examination showed that the parasite quickly invades multiple host organs (gills, intestines, albumen gland, lung, kidney, and mantle border) besides the gonad and digestive gland, as is usual in digeneans. In addition, the partial or total castration of snails was observed in cases of moderate and high infection intensity. In males, there was loss of integrity in testicular tubules, while in females, the replacement of ovarian tissue by rediae was found.
... In some cases, parasitism can have sublethal effects, such as shortterm lethargy; for example, female Drosophila melanogaster sleep more when infected with Drosophila-C virus [13], which may incur only minor fitness costs. In other cases, parasitism can have severe consequences, as shown by mortality from Nuclear Polyhedrosis Virus (NPV) in larval Lepidoptera [14], honey bee mortality due to American Foulbrood disease [15], or complete castration of freshwater snails by trematodes [16], all of which would have major fitness consequences. The importance of direct versus indirect fitness costs will depend on the animal's level of sociality [17]. ...
Like humans, animals use plants and other materials as medication against parasites. Recent decades have shown that the study of insects can greatly advance our understanding of medication behaviors. The ease of rearing insects under laboratory conditions has enabled controlled experiments to test critical hypotheses, while their spectrum of reproductive strategies and living arrangements – ranging from solitary to eusocial communities – has revealed that medication behaviors can evolve to maximize inclusive fitness through both direct and indirect fitness benefits. Studying insects has also demonstrated in some cases that medication can act through modulation of the host’s innate immune system and microbiome. We highlight outstanding questions, focusing on costs and benefits in the context of inclusive host fitness.
... Finally, as Merilä and Eloranta (2017) demonstrated in sticklebacks with some "giants" among them, the largest individuals were not affected by parasites, while this was the case in many of the smaller fish of the same population. For all these reasons, and because it appears to occur-if at all-in only small fish species (Lafferty & Kuris, 2009), parasitic castration will likely remain peripheral to a general explanation of Goliathan gigantism. ...
Two forms of gigantism are differentiated in fish, Brobdingnagian and Goliathan gigantism, the former applying to populations whose individuals are all larger than is typical for the taxon, the latter to single individuals within a population. While Brobdingnagian gigantism is largely explained by various ecological and evolutionary rules, Goliathan gigantism is not. A mechanistic hypothesis is proposed which explains Goliathan gigantism in terms of the reduction of oxygen requirements of individual fish via moving to cooler temperatures and/or acquiring larger, more energy‐dense prey, which enable them to get bigger, and, in the process, sometimes generate bimodal size distributions that may qualify as gradual forms between Goliathan and Brobdingnagian gigantism. This mechanism, which relies on the manner in which their gill surface area grows, is more likely to operate in fish that can get big in the first place than in fish that remain small.
... Increased feeding behavior in infected individuals has been interpreted as a compensatory response to nutrient deprivation caused by parasites or as a modification of the host's growth rate, such as gigantism [15,16]. Other researchers have described the reduced fecundity in infected snails as castration, suggesting that the trematode parasite alleviates the energetic demands of reproduction, allowing the host to allocate this energy towards other life-history traits, such as growth and survival [61,62]. Another possible explanation for increased feeding is starvation autolysis, which occurs due to the compression of digestive tubules at various locations, hindering the passage of food into the tubules. ...
Background
Trematode infections of the genus Schistosoma can induce physiological and behavioral changes in intermediate snail hosts. This is because the parasite consumes essential resources necessary for the host's survival, prompting hosts to adapt their behavior to maintain some level of fitness before parasite-induced mortality occurs.
Methods
In this study, the reproductive and biochemical parameters of Biomphalaria alexandrina and Bulinus truncatus were examined during the cercareal shedding stage of infection with Schistosoma mansoni and Schistosoma haematobium , respectively, compared with controls.
Results
The study revealed an infection rate of 34.7% for S. mansoni and 30.4% for S. haematobium . In B. alexandrina infected with S. mansoni , a survival rate of 65.2% was recorded, along with a mean prepatent period of 30.3 ± 1.41 days, a mean shedding duration of 14.2 ± 0.16 days, and a mean lifespan of 44.1 ± 0.24 days. Meanwhile, in B. truncatus infected with S. haematobium , a survival rate of 56.4% was observed, with a mean prepatent period of 44.3 ± 1.41 days, a mean shedding duration of 22.6 ± 2.7 days, and a mean lifespan of 66.9 ± 1.6 days. Feeding increased in both infected species of snails, while the net reproductive rate (Ro) of the infected snails decreased. Total antioxidant (TAO) and lipid peroxidation activity increased in the two infected snail species during shedding, while Glutathione- S -transferase levels decreased. Lipid peroxidase activity and nitrogen oxide levels significantly decreased in infected B. alexandrina and increased in infected Bulinus. Steroid hormone levels were elevated in infected Biomphalaria, whereas they were reduced in infected Bulinus . Comet assay parameters showed an increase in the two infected genera after infection compared to control snails, indicating genotoxic damage and histopathological damage was observed.
Conclusions
These findings demonstrate that infection with larva species diverse biochemical, hormonal, genotoxic, and histopathological changes in the tissues responsible for fecundity and reproduction in B . alexandrina and B. truncates comparing with controls.
... It is likely that castrators in snails weaken the immune system or alter host behaviour, making successful infection by metacercariae more likely (Magalhães et al. 2015; Fig. 5B). It has been shown that infection with castrators significantly affects energy budgets of molluscs, and thus their ability to cope with other stressors (Jokela et al. 2005;Lafferty and Kuris 2009). In contrast, any immune response by mussels to castrator infection does not appear to cascade to facilitating E. recurvatum (Fig. 5A). ...
Understanding the ecological assembly of parasite communities is critical to characterise how changing host and environmental landscapes will alter infection dynamics and outcomes. However, studies frequently assume that (a) closely related parasite species or those with identical life-history strategies are functionally equivalent, and (b) the same factors will drive infection dynamics for a single parasite across multiple host species, oversimplifying community assembly patterns. Here, we challenge these two assumptions using a naturally occurring host-parasite system, with the mussel Anodonta anatina infected by the digenean trematode Echinoparyphium recurvatum, and the snail Viviparus viviparus infected by both E. recurvatum and Echinostoma sp. By analysing the impact of temporal parasite dispersal, host species and size, and the impact of coinfec-tion (moving from broader environmental factors to within-host dynamics), we show that neither assumption holds true, but at different ecological scales. The assumption that closely related parasites can be functionally grouped is challenged when considering dispersal to the host (i.e. larger scales), while the assumption that the same factors will drive infection dynamics for a single parasite across multiple host species is challenged when considering within-host interspecific competition (i.e. smaller scales). Our results demonstrate that host identity, parasite identity and ecological scale require simultaneous consideration in studies of parasite community composition and transmission.
... Sometimes, ectodermic epibionts like parasitic gastropods may produce attachment lesions involving host reactions, like the induction of galls, and it has also been reported that many internal symbionts can partially or totally castrate their hosts (Jangoux, 1987;Lafferty & Kuris, 2009;Parmentier et al., 2006). Others, such as ectoparasitic gastropods that draw energy from the haemal fluid, occur mostly on holothuroids (Jangoux, 1987); however, assessments of trophic interactions using stable isotope analysis have not been performed for most eulimid gastropods, especially genera related to holothuroid hosts. ...
... On patent field co-infections (not mycoparasitism) by B. bassiana and M. anisopliae on the same insect (weevil) cadaver, growth and sporulation of both fungi was observed, but the fungi occupied separate sections of the insect (Sanchez-Peña et al., 2001). Niveomyces acts as a sterilising parasite, supporting the concept of mycoparasitic association, which in this case can be considered parasitic castration (Lafferty & Kuris, 2009). This kind of parasites diverts the resources and energy of the host and cancel out host reproduction, since this constitutes a resource sink. ...
Diaphorina citri Kuwayama (Asian citrus psyllid, ACP) is a devastating pest due to transmission of Liberibacter spp. to citrus plants. We identified presumed entomopathogenic fungi (EF) naturally associated with field-collected adult ACP, both killed (mycosed) and alive, at 14 field sites in the Gulf Coastal Plain of NE Mexico. On dead ACP, five species of EF (Hypocreales) were observed: Hirsutella citriformis Speare (Ophiocordycipitaceae), Cordyceps javanica (Frieder. & Bally) Kepler, Shrestha & Spatafora, Beauveria cf. bassiana (Bals.) Vuill., and Akanthomyces cf. lecanii (Cordycipitaceae); also, Niveomyces J.P.M. Araújo & C. de Bekker (Cordycipitaceae), a hyperparasite of Ophiocordycipitaceae, in this case H. citriformis. The most prevalent fungi on field ACP were H. citriformis and C. javanica, on dead and on live, incubated insects, respectively. In laboratory bioassays, C. javanica and H. citriformis conidia from cultures killed >60% of ACP adults. H. citriformis, C. javanica, and A. lecanii killed >60% nymphs. Niveomyces was observed only growing on H. citriformis fructifications on field-killed ACP; it was absent from live incubated insects, indicating Niveomyces is a mycoparasite on H. citriformis. Niveomyces cultures (ARSEF 10230) on agar grew as a Pleurodesmospora synanamorph; its LSU rRNA region D1–D2 sequences (Genbank OM780101) were 99.81% identical to Niveomyces sequences. Conidia from Niveomyces cultures were entomopathogenic on ACP nymphs and adults. These are the first reports of Niveomyces associated with H. citriformis; of the in vitro dimorphic growth (synanamorphs) Niveomyces/Pleurodesmospora; and of experimental verification of entomopathogenicity of Niveomyces. Understanding the interactions of these fungi will support sustainable ACP management.
... and, may be attributed to histopathogenic effects on the snail host and depletion of nutrient by the parasite especially near the time of the maturation of infection and shedding of cercariae (El-Sayed et al., 1999).allowing the host to invest this energy towards other life history traits, such as growth and survival(Poulin, 2006;Lafferty and Kuris, 2009 ...
Trematodes infection of genus Schistosoma can lead to physiological and behavioral changes in intermediate snail hosts. This is because the parasite consumes essential resources required for the host's survival, but the hosts can adaptively modify their behavior to ensure some level of fitness before parasite-induced mortality. The present study examined the reproductive and biochemical parameters of Biomphalaria alexandrina and Bulinus truncatus during the shedding stage of infection with Schistosoma mansoni and haematobium , respectively. The study found that the infection rate with S. mansoni was 34.7% and 30.4% with S. haematobium . In B.alexandrina infected with S. mansoni , a survival rate of 65.2% was recorded, along with a mean duration of shedding of 32.8 ± 5.5 days, a mean prepatent period of 37.5 ± 1.15 days, and a mean life span of 57.0 ± 1.21 days. Meanwhile, in B. truncatus infected with S. haematobium , a survival rate of 56.4% was recorded, with a mean duration of shedding of 42.6 ± 2.6 days, a mean prepatent period of 46.7 ± 2.3 days, and a mean life span of 65.9 ± 1.6 days. The feeding behavior was increased in the two infected species snail, while the net reproductive rate (R o ) of the infected species snails was reduced. Total antioxidant (TAO) and lipid peroxidation activity were increased in the two infected snails during shedding, while Glutathione-S-transferase was reduced. Lipid peroxidase (LPO) activity and nitrogen oxide (NO) levels decreased significantly in infected B. alexandrina and increased in infected Bulinus . Steroid hormone measurements were increased in the infected Biomphalaria , while they were reduced in infected Bulinus . Comet assay parameters were increased in the two infected genera after infection than control snails, and histopathological damage occurred. These observations demonstrated that infection initiates diverse biochemical, hormonal, genotoxic, and histopathological change to the tissues responsible for fecundity and reproduction in B. alexandrina and B. truncatus.
... The origin of unusually large individuals of L. cf. terebra in the studied pond can tentatively be related to the effect of parasitic castration, not rare among aquatic gastropods [Wilke, Falniowski, 2001;Lafferty, Kuris, 2009], including the lymnaeids [Wilson, Davison, 1980;Chapuis, 2009]. The dissection of two particularly large individuals collected in August 2022, whose shell height exceeded 30 mm, has shown that they were heavily infected by trematode larvae; their hepatopancreas was enlarged, and numerous trematode parthenitae were seen in the mantle cavity (Fig. 4). ...
The article reports the finding of a population of freshwater snails morphologically and genetically identified as Ladislavella cf. terebra (Westerlund, 1885), in a reservoir situated in Penza City. This is the first reliable record of representatives of the genus Ladislavella on the territory of European Russia, at a considerable distance from the previously known boundaries of its range. Molecular data suggest that the examined population belongs to the previously unknown species of Ladislavella. The morphoanatomic and ecological characteristics of the studied population and some information about parasites and commensals of the mollusсs are given
... We propose that the apparent absence of sexual dimorphism in summiting is a consequence of effective castration by the fungus. Histological data showed that summiting flies either have severely damaged gonads or lack them entirely ( Figure 5G1), similar to other instances of parasitic castration (Cooley et al., 2018;Ewen, 1966;Lafferty and Kuris, 2009). As JHRs are present in gonads (Abdou et al., 2011;Baumann et al., 2017), it follows that in the absence of these sexually dimorphic tissues, JH-mediated behavioral differences between the sexes would be minimized. ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... We propose that the apparent absence of sexual dimorphism in summiting is a consequence of effective castration by the fungus. Histological data showed that summiting flies either have severely damaged gonads or lack them entirely ( Figure 5G1), similar to other instances of parasitic castration (Cooley et al., 2018;Ewen, 1966;Lafferty and Kuris, 2009). As JHRs are present in gonads (Abdou et al., 2011;Baumann et al., 2017), it follows that in the absence of these sexually dimorphic tissues, JH-mediated behavioral differences between the sexes would be minimized. ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... We propose that the apparent absence of sexual dimorphism in summiting is a consequence of effective castration by the fungus. Histological data showed that summiting flies either have severely damaged gonads or lack them entirely ( Figure 5G1), similar to other instances of parasitic castration (Cooley et al., 2018;Ewen, 1966;Lafferty and Kuris, 2009). As JHRs are present in gonads (Abdou et al., 2011;Baumann et al., 2017), it follows that in the absence of these sexually dimorphic tissues, JH-mediated behavioral differences between the sexes would be minimized. ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... Parasitism is a common lifestyle in nature, with all organismal groups being infected by parasites (Poulin, 1996). Parasites can affect host growth, reproduction, and survival (Agnew et al., 2000;Lafferty & Kuris, 2009;Segar et al., 2018); can manipulate host behavior (Poulin, 2010); impair host population growth (Hudson et al., 1998); and affect host fitness in general. Because of these effects, parasites are considered potential drivers of host evolution, including host ecological divergence and speciation (Kaltz & Shykoff, 1998). ...
Because of potentially strong eco-evolutionary interactions with their hosts, parasites may initiate or enhance host diversification. The adaptive radiation of cichlid fish in Lake Victoria provides a good system to study the role of parasites at different stages of host speciation. We analysed the macroparasite infection of four replicates of sympatric blue and red Pundamilia species pairs that vary in their age and extent of differentiation. Sympatric host species differed in parasite community composition and in the infection levels of some of these parasite taxa. Most infection differences were consistent between sampling years, indicating temporal consistency in parasite-mediated divergent selection between species. Infection differentiation increased linearly with genetic differentiation. However, significant infection differences between sympatric species were only found in the oldest, most strongly differentiated Pundamilia species pair. This is inconsistent with parasite-driven speciation. Next, we identified five distinct species of Cichlidogyrus, a genus of highly specific gill parasites that has radiated elsewhere in Africa. Infection profiles of species of Cichlidogyrus differed between sympatric cichlid species only in the oldest and most differentiated pair, again inconsistent with parasite-mediated speciation. To conclude, parasites may contribute to host differentiation after speciation, but do not initiate host speciation.
... The finding that larger snails produce more parasites has been reported in other snail-trematode studies and supports the idea that energetics and nutrient availability is a key regulator of cercarial production. Energy diverted from reproduction after parasitic castration is converted to enhanced snail growth and thus parasite growth (Baudoin, 1975;Sorensen & Minchella, 2001;Lafferty & Kuris, 2009;Faro et al., 2013). Additionally, high quality nutrient diets, or increased availability of nutrients, such as through reduced competition, results in larger snails that produce more cercariae (Sandland & Minchella, 2003 In the present study, dose-dependent effects on infection status, but not on cercarial production when comparing 5 vs 10 miracidia were observed. ...
Interactions between Schistosoma mansoni and its snail host are understood primarily through experimental work with one South American vector species, Biomphalaria glabrata. However, 90% of schistosomiasis transmission occurs in Africa, where a diversity of Biomphalaria species may serve as vectors. With the long-term goal of determining the genetic and ecological determinants of infection in African snail hosts, we developed genetic models of Biomphalaria sudanica, a principal vector in the African Great Lakes. We determined laboratory infection dynamics of two S. mansoni lines in four B. sudanica lines. We measured the effects of the following variables on infection success and the number of cercariae produced (infection intensity): (i) the combination of parasite and snail line; (ii) the dose of parasites; and (iii) the size of snail at time of exposure. We found one snail line to be almost completely incompatible with both parasite lines, while other snail lines showed a polymorphism in compatibility: compatible with one parasite line while incompatible with another. Interestingly, these patterns were opposite in some of the snail lines. The parasite-snail combination had no significant effect on the number of cercariae produced in a successful infection. Miracidia dose had a strong effect on infection status, in that higher doses led to a greater proportion of infected snails, but had no effect on infection intensity. In one of the snail-schistosome combinations, snail size at the time of exposure affected both infection status and cercarial production in that the smallest size class of snails (1.5–2.9 mm) had the highest infection rates, and produced the greatest number of cercariae, suggesting that immunity increases with age and development. The strongest predictor of the infection intensity was the size of snail at the time of shedding: 1 mm of snail growth equated to a 19% increase in cercarial production. These results strongly suggest that infection status is determined in part by the interaction between snail and schistosome genetic lines, consistent with a gene-for-gene or matching allele model. This foundational work provides rationale for determining the genetic interactions between African snails and schistosomes, which may be applied to control strategies.
... However, hosts infected with spores subjected to 46°C lived longer in comparison to all infected Daphnia ( figure 4). Pasteuria ramosa is a castrating parasite that uses the growth energy of its host as a resource, in order to redirect host resources from reproduction into body-mass investment [44,55,58]. This ability is subjected to an evolutionary arms race, where the host produces offspring earlier than normal (i.e. ...
Disease agents play an important role in the ecology and life history of wild and cultivated populations and communities. While most studies focus on the adaptation of parasites to their hosts, the adaptation of free-living parasite stages to their external (off-host) environment may tell us a lot about the factors that shape the distribution of parasites. Pasteuria ramosa is an endoparasitic bacterium of the water flea Daphnia with a wide geographical distribution. Its transmission stages rest outside of the host and thus experience varying environmental regimes. We examined the life history of P. ramosa populations from four environmental conditions (i.e. groups of habitats): the factorial combinations of summer-dry water bodies or not, and winter-freeze water bodies or not. Our goal was to examine how the combination of winter temperature and summer dryness affects the parasite's ability to attach to its host and to infect it. We subjected samples of the four groups of habitats to temperatures of 20, 33, 46 and 60°C in dry and wet conditions, and exposed a susceptible clone of Daphnia magna to the treated spores. We found that spores which had undergone desiccation endured higher temperatures better than spores kept wet, both regarding attachment and subsequent infection. Furthermore, spores treated with heightened temperatures were much less infective and virulent. Even under high temperatures (60°C), exposed spores from all populations were able to attach to the host cuticle, albeit they were unable to establish infection. Our work highlights the sensitivity of a host-free resting stage of a bacterial parasite to the external environment. Long heatwaves and harsh summers, which are becoming more frequent owing to recent climate changes, may therefore pose a problem for parasite survival.
This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.
... Given that snails are castrated and therefore have zero fitness, it is difficult to posit how personality differences are of adaptive value to the host (Lafferty & Kuris, 2009). The interactive effects of predation risk and parasite infection suggest that personality may be condition dependent, with boldness now varying along a continuum of 'sickness' (Dantzer, 2001). ...
Parasites can alter species interactions either by modifying infected host behaviour or by influencing behavioural responses in uninfected individuals. Salt marsh ecosystems are characterized by a predator–prey interaction between the keystone grazer, Littoraria irrorata, and its main predator, Callinectes sapidus, both integral players in mediating the productivity of these habitats.
Littoraria also acts as the first intermediate host for at least four species of digenetic trematode. Parasite infection has been shown to decrease grazing and climbing in populations of Littoraria, although effects on infected host response to predators have not been investigated. Moreover, how infection might increase or decrease among‐individual variation in behaviour (i.e. animal personality) is still unknown. Here we ask how trematode infection affects the expression of boldness in the anti‐predator responses of L. irrorata in both the absence and presence of a predator cue.
We find that individual boldness varies substantially, and repeatability tends to increase as the number of stressors increases, with infected individuals exposed to a predator cue showing the strongest expression of behavioural types.
Parasitism amplifies this effect, although the parasite itself does not appear to directly induce behavioural changes: infected snails show no evidence of decreased climbing or differences in refuge use as compared to their uninfected counterparts. Infection might therefore drive the expression of condition‐dependent personality differences evident only under high‐risk conditions.
Group infection status strongly influenced behavioural reaction norms: uninfected individuals grouped with an infected snail were more responsive to predation risk, exhibiting increased climbing behaviour and spending less time in the water. Here parasites are influencing personality indirectly by inducing avoidance behaviours in healthy individuals, although only in high‐risk environments.
The potential for exposure to parasites and predators fluctuates greatly across marsh ecosystems. Given the ecological importance of this predator–prey relationship, trematode infection can act as an important, although indirect, determinant of overall salt marsh community structure, health and function.
... Such pathogens are present in nature: evolutionary parasitology predicts pathogens to rather sterilize their hosts than shorten their lifespan to facilitate transmission [163]. Some pathogens use the host's sterilization as a part of their reproductive strategies [164,165]. Several human sexually transmitted diseases, such as gonorrhea, chlamydia, and syphilis, cause infertility [166,167]. Reduced fecundity occurs in other chronic diseases, such as HIV [168], leprosy [169], HCV [170], tuberculosis [171], herpes [172], and many others. ...
Aging is an evolutionary paradox. Several hypotheses have been proposed to explain it, but none fully explains all the biochemical and ecologic data accumulated over decades of research. We suggest that senescence is a primitive immune strategy which acts to protect an individual's kin from chronic infections. Older organisms are exposed to pathogens for a longer period of time and have a higher likelihood of acquiring infectious diseases. Accordingly, the parasitic load in aged individuals is higher than in younger ones. Given that the probability of pathogen transmission is higher within the kin, the inclusive fitness cost of infection might exceed the benefit of living longer. In this case, programmed lifespan termination might be an evolutionarily stable strategy. Here, we discuss the classical evolutionary hypotheses of aging and compare them with the pathogen control hypothesis, discuss the consistency of these hypotheses with existing empirical data, and present a revised conceptual framework to understand the evolution of aging.
... We propose that the apparent absence of sexual dimorphism in summiting is a consequence of effective castration by the fungus. Histological data showed that summiting flies either have severely damaged gonads or lack them entirely (Fig 5G, I), similar to other instances of parasitic castration (Cooley et al., 2018;Ewen, 1966;Lafferty and Kuris, 2009). As JHRs are present in gonads (Abdou et al., 2011;Baumann et al., 2017), it follows that in the absence of these sexually dimorphic tissues, JH-mediated behavioral differences between the sexes would be minimized. ...
For at least two centuries, scientists have been enthralled by the zombie behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the recently established Entomophthora muscae-Drosophila melanogaster zombie fly system to reveal the molecular and cellular underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a new, high-throughput behavior assay to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), who are solely responsible for juvenile hormone (JH) synthesis and release. Summiting is a fleeting phenomenon, posing a challenge for physiological and biochemical experiments requiring tissue from summiting flies. We addressed this with a machine learning classifier to identify summiting animals in real time. PI-CA neurons and CA appear to be intact in summiting animals, despite E. muscae cells invading the host brain, particularly in the superior medial protocerebrum (SMP), the neuropil that contains DN1p axons and PI-CA dendrites. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb fly hemolymph, activating the neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... A particular form of behavioural change also occurs in hostparasite relationships. Trematode parasites castrate their host and divert nutritional resources away from costly reproductive activities towards maintaining the parasites (Lafferty & Kuris, 2009). ...
Parasitism of mice by Toxoplasma gondii reduces the host's aversion to cat odours, likely increasing predation and transmission of the parasite to its definitive host. This behavioural change suggests a parasitic manipulation where host behaviour becomes an extended phenotype of the parasite.
Independently, epigenetic changes within an organism are now known to create behavioural change.
The results described here provide an experimental connection between these disparate strands of extended phenotypes and the role of epigenetics in behavioural diversity.
Using mice captured on Kangaroo Island in Australia, we demonstrate that Toxoplasma gondii infection leads to specific DNA hypomethylation events in the host brain.
Previous laboratory studies have shown that these epigenetic changes underlie the central processing of cat odours. We posit that the concept of extended phenotype can be expanded to extended epiphenotype, thus linking parasite genes to host behaviour through epigenesis. This phenomenon has broad implications for inter‐species relationships.
Read the free Plain Language Summary for this article on the Journal blog.
... When disease affects adults, besides increasing adult mortality, disease can also reduce reproductive success (Auld et al. 2014). Indeed, livestock experience various aspects of infertility (miscarriage, stillbirth) as a consequence of infection by protozoan parasites (Kaltungo and Musa 2013), and many vertebrates and invertebrates can experience sterilization in response to parasite infection (Antonovics 2009;Lafferty and Kuris 2009). ...
All individuals transition through various life stages over the course of their development and nearly all organisms must contend with infectious disease at some point in their lives. Yet the intersection of these two universal features of life—stage structure and infectious disease—and their joint effects on population dynamics are poorly understood. Here, we develop a two-stage population model in which density dependence acts on juvenile maturation, and infectious disease affects either juveniles or adults via reduction in maturation, reproduction, or survival. In the absence of disease, this form of density dependence can generate persistent population oscillations. We examine whether infectious disease further accentuates these oscillations (by augmenting their amplitude) or stabilizes them (by reducing their amplitude). We find that, for moderate transmission rates (a proxy for disease incidence), disease can stabilize dynamics. In contrast, fast disease transmission is not generally stabilizing, which is, at least in part, due to disease overexploitation of the infectious class. Hydra effects are possible in the model due to density overcompensation and occur when disease increases juvenile mortality or decreases adult fecundity (but do not occur when disease augments adult mortality or reduces maturation). Slow maturation, large disease-free population size, and strong density-dependent population regulation can each lower the transmission rate required for the infectious disease to invade the population.
Graphical abstract
... Several parasites spread across diverse taxa castrate their host to ensure metabolic investment by the host in sustaining the parasite rather than in reproduction (Lafferty & Kuris, 2009). Gypsy moths infected by baculovirus climb to the top of trees and die there, creating a 'rain' of infectious virus towards new possible hosts below (Hoover et al., 2011). ...
Biologists have long known that environmental context can create diverse phenotypes from identical genotypes. Thus, cells of the same foetus can grow into various organs depending on the molecular environment. Also, animals of the same genetic heritage can show different behaviours in different environments. Conrad Hal Waddington conceptualized epigenotypes in the 1930s, whereby modifications of genetic material could generate alternative modules of development arising out of nonvariant genetic information. His concept paved the way for a neo‐Darwinian synthesis by creating bidirectionality between the environment and genes.
In a completely independent intellectual universe, Richard Dawkins introduced the idea of extended phenotype in the early 1980s. The hypothesis posits that the appropriate phenotype of genetic information is not limited to the organism but can ‘extend’ beyond the environment. Parasite manipulation of host behaviour presents a dramatic example of such extended phenotypes.
In this perspective, we propose a synthesis between the earlier concept of epigenotypes and the later idea of extended phenotypes, namely a novel concept of extended epiphenotypes.
Read the free Plain Language Summary for this article on the Journal blog.
... In other words, a single individual parasitic castrator will prevent or block host reproduction when the parasite matures. Such type of parasitic castration is commonly found in most of the fast breeder aquatic animals such as gastropod molluscs or snails [46][47][48][49][50][51][52][53][54], bivalves [55][56][57] and number of crustaceans and other invertebrate animals [58][59][60]. Interesting, besides the sterilization of snail host, parasitic castration also induces the growth of young snail host called gigantism [58,61], sex reversal [62] and potential to alter the gene expression in brain of the snail host also [63]. ...
Snails are invertebrate gastropod molluscs inhabited both the terrestrial and aquatic habitats. Most of these animals are dioeciously and their sexes are separated. In many monoecious (hermaphrodite) snail species, individuals have both male and female gonads. But in pulmonate monoecious snail species individuals have only single gonad called "ovotestis" which contains both testicular and ovarian tissues. In general, aquatic snail species are intermediate hosts of digenean trematode parasites of vertebrates including man and animals. In addition, aquatic snails are also act as vector of diverse trematodiases, such as schistosomiasis, clonorchiasis, opisthorchiasis, fascioliasis, amphistomiasis, etc. The prevalence of these digenetic trematode parasitic diseases in diverse geographical provinces is depending on the population of vector or intermediate host snail species. In fact, the various larval stages of digenean trematode parasites, such as sporocysts, rediae and cercariae are developed and multiplied asexually in the organ of hepatopancreas and/or gonads of host snails. These parasitic trematode larvae also act as castrators for snails and potential to prevent or block partially or completely their reproduction called "parasitic castration". In this biological process, trematode larvae destroy the gonads in two ways, one is mechanically and the other physiologically. Parasitic castration is also induces sex conversion, gigantism and alteration the gene expression in brain of snails. In present communication, the most common vector snail species, different forms of trematode larvae and their basic biology and mode of parasitic castration in aquatic snails and its contribution in control of diverse vector snail populations and spreading of trematodiases are considered and brief and critically reviewed. Simultaneously, research gaps have also been highlighted for further advance research work. This review is helpful in understanding of biology or mechanism of parasitic castration and its contributory role in the balancing of aquatic ecosystem.
... Inside the snail, trematodes occupy the mantle, the digestive and/or reproductive organs and reproduce asexually. They can disrupt the endocrine system of the host and may cause serious damage either by diverting nutrients or by feeding directly on host tissue (Lafferty and Kuris, 2009). Depending on the specific interaction between host and parasite, infections can increase snail mortality and/or decrease fecundity, up to castration of the host (Sorensen and Minchella, 2001). ...
Trematodes can increase intraspecific variation in the phenotype of their intermediate snail host. However, the extent of such phenotypic changes remains unclear. We investigated the influence of trematode infection on the shell morphology of Bulinus tropicus, a common host of medically important trematodes. We focused on a snail population from crater lake Kasenda (Uganda). We sampled a single homogeneous littoral habitat to minimize the influence of environmental variation on shell phenotype, and barcoded snails to document snail genotypic variation. Among the 257 adult snails analysed, 99 tested positive for trematode infection using rapid-diagnostic PCRs. Subsequently we used high-throughput amplicon sequencing to identify the trematode (co-)infections. For 86 out of the 99 positive samples trematode species delineation could discriminate among combinations of (co-)infection by 11 trematode species. To avoid confounding effects, we focused on four prevalent trematode species. We performed landmark-based geometric morphometrics to characterize shell phenotype and used regressions to examine whether shell size and shape were affected by trematode infection and the developmental stage of infection (as inferred from read counts). Snails infected by Petasiger sp. 5, Echinoparyphium sp. or Austrodiplostomum sp. 2 had larger shells than uninfected snails or than those infected by Plagiorchiida sp. Moreover, the shell shape of snails infected solely by Petasiger sp. 5 differed significantly from that of uninfected snails and snails infected with other trematodes, except from Austrodiplostomum sp. 2. Shape changes included a more protuberant apex, an inward-folded outer apertural lip and a more adapically positioned umbilicus. Size differences were more pronounced in snails with ‘late’ infections (>25 days) compared to earlier-stage infections. No phenotypic differences were found between snails infected by a single trematode species and those harbouring co-infections. Further work is required to assess the complex causal links between trematode infections and shell morphological alterations of snail hosts.
... In other words, a single individual parasitic castrator will prevent or block host reproduction when the parasite matures. Such type of parasitic castration is commonly found in most of the fast breeder aquatic animals such as gastropod molluscs or snails [46][47][48][49][50][51][52][53][54], bivalves [55][56][57] and number of crustaceans and other invertebrate animals [58][59][60]. Interesting, besides the sterilization of snail host, parasitic castration also induces the growth of young snail host called gigantism [58,61], sex reversal [62] and potential to alter the gene expression in brain of the snail host also [63]. ...
Snails are invertebrate gastropod molluscs inhabited both the terrestrial and aquatic habitats. Most of these animals are dioeciously and their sexes are separated. In many monoecious (hermaphrodite) snail species, individuals have both male and female gonads. But in pulmonate monoecious snail species individuals have only single gonad called "ovotestis" which contains both testicular and ovarian tissues. In general, aquatic snail species are intermediate hosts of digenean trematode parasites of vertebrates including man and animals. In addition, aquatic snails are also act as vector of diverse trematodiases, such as schistosomiasis, clonorchiasis, opisthorchiasis, fascioliasis, amphistomiasis, etc. The prevalence of these digenetic trematode parasitic diseases in diverse geographical provinces is depending on the population of vector or intermediate host snail species. In fact, the various larval stages of digenean trematode parasites, such as sporocysts, rediae and cercariae are developed and multiplied asexually in the organ of hepatopancreas and/or gonads of host snails. These parasitic trematode larvae also act as castrators for snails and potential to prevent or block partially or completely their reproduction called "parasitic castration". In this biological process, trematode larvae destroy the gonads in two ways, one is mechanically and the other physiologically. Parasitic castration is also induces sex conversion, gigantism and alteration the gene expression in brain of snails. In present communication, the most common vector snail species, different forms of trematode larvae and their basic biology and mode of parasitic castration in aquatic snails and its contribution in control of diverse vector snail populations and spreading of trematodiases are considered and brief and critically reviewed. Simultaneously, research gaps have also been highlighted for further advance research work. This review is helpful in understanding of biology or mechanism of parasitic castration and its contributory role in the balancing of aquatic ecosystem.
... As such, parasite communities can be used to recreate food webs. This process assumes that A) parasite presence and composition reflect the local food web; B) host-parasite life histories are understood well enough and traceable among species; or 3) are generalist in nature and can be excluded from infracommunity assessments (Lafferty and Kuris, 2009). Host-specificity of parasites can vary widely both taxonomically and among life stages (Marcogliese, 2003). ...
The emergence of novel human pathogens is frequently linked with zoonotic events and human-wildlife interactions that promote disease transmission. Consequently, surveillance of wildlife populations for candidate diseases that could spread to humans is beneficial, but requires widespread collections of numerous samples. A legitimate means to acquire large sample sizes of waterfowl is through cooperation between researchers and hunters, who also work in concert with natural resource managers, landowners, and agricultural entities-e.g., aquaculture facilities. In addition to understanding the occurrence and spread of parasites and pathogens by birds, these samples can be used to answer questions about the ecology of various waterbird species. Body mass and morphometric data on hunter-donated specimen are useful for understanding bird condition and other dynamics of birds; however, when breast meat is removed prior to the acquisition of specimen weight, samples might not be as desirable. Here, we evaluate the utility of data obtained from a bird species that might be targeted by hunters and subsequently used to learn about their disease dynamics. Lesser Scaup (Aythya affinis) collected at aquaculture facilities were assessed for their stable isotope concentrations and parasites communities to learn about the birds' foraging ecology. Discriminant analyses designed to classify birds by the aquaculture pond type from which they were collected included isotope data, Principal Components derived from parasite community data of 7 types, and birds' body mass. We compared these to Double-crested Cormorants (Nannop-terum auritum) feeding on catfish and found the two waterbird species exhibited different infracommunities of parasites Furthermore, some scaup demonstrated fish aquaculture pond type fidelity. Bird body mass was an important metric to include in analytical models when all parasite datatypes were not available. However, the combination of stable isotope concentrations and parasite infracommunity data (that includes prevalence, abundance, volume, and energy use) in models resulted in host ecology differentiation equal or better than models where bird body mass was included. Hunter-derived samples should be encouraged as a means for sample acquisition and be considered as an approach for aquaculture-wildlife conflict management as the information that can be obtained through these samples is multifaceted.
The sex ratio is nearly equal in most organisms, while several ecological and evolutionary factors skew the sex ratio. We evaluated the sex ratios of 12 species in the freshwater snail genus Semisulcospira in and around Lake Biwa. We found highly female-biased sex ratios in all 12 species. The sex ratios were nearly equal or slightly female-biased in the smaller shell-size classes, while they were highly female-biased in the larger size classes. We also found that females were significantly larger in most of these species. Further, the species with a larger size difference between the sexes tended to exhibit a more female-biased sex ratio. Considering the general correlation between shell size and age, this pattern can be explained by longer lifespans in females, shaping the observed female-biased sex ratios. We also found that some Semisulcospira species showed female-biased sex ratios in all shell size classes. This pattern suggests that the distinct longevity hypothesis can not solely explain the observed biased sex ratios. We discussed the possible contributions of the sampling errors and selfish genetic elements to the observed biased sex ratios. This study provides essential information to disentangle the mechanisms of the biased sex ratio in the Semisulcospira snails.
Coastal ecosystems and their marine populations are increasingly threatened by global environmental changes. Bivalves have emerged as crucial bioindicators within these ecosystems, offering valuable insights into biodiversity and overall ecosystem health. In particular, bivalves serve as hosts to trematode parasites, making them a focal point of study. Trematodes, with their life cycles intricately linked to external factors, provide excellent indicators of environmental changes and exhibit a unique ability to accumulate pollutants beyond ambient levels. Thus, they act as living sentinels, reflecting the ecological condition of their habitats. This paper presents a comprehensive review of recent research on the use of bivalve species as hosts for trematodes, examining the interactions between these organisms. The study also investigates the combined impact of trematode infections and other pollutants on bivalve molluscs. Trematode infections have multifaceted consequences for bivalve species, influencing various aspects of their physiology and behavior, including population-wide mortality. Furthermore, the coexistence of trematode infections and other sources of pollution compromises host resistance, disrupts parasite transmission, and reduces the abundance of intermediate hosts for complex-living parasites. The accumulation process of these parasites is influenced not only by external factors but also by host physiology. Consequently, the implications of climate change and environmental factors, such as temperature, salinity, and ocean acidification, are critical considerations. In summary, the intricate relationship between bivalves, trematode parasites, and their surrounding environment provides valuable insights into the health and sustainability of coastal ecosystems. A comprehensive understanding of these interactions, along with the influence of climate change and environmental parameters, is essential for effective management and conservation strategies aimed at preserving these delicate ecosystems and the diverse array of species that rely on them.
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
Although parasites can kill their hosts, they also commonly cause nonlethal effects on their hosts, such as altered behaviors or feeding rates. Both the lethal and nonlethal effects of parasites can influence host resource consumption. However, few studies have explicitly examined the joint lethal and nonlethal effects of parasites to understand the net impacts of parasitism on host resource consumption. To do this, we adapted equations used in the indirect effects literature to quantify how parasites jointly influence basal resource consumption through nonlethal effects (altered host feeding rate) and lethal effects (increased host mortality). To parametrize these equations and to examine the potential temperature sensitivity of parasite influences, we conducted a fully factorial lab experiment (crossing trematode infection status and a range of temperatures) to quantify feeding rates and survivorship curves of snail hosts. We found that infected snails had significantly higher mortality and ate nearly twice as much as uninfected snails and had significantly higher mortality, resulting in negative lethal effects and positive nonlethal effects of trematodes on host resource consumption. The net effects of parasites on resource consumption were overall positive in this system, but did vary with temperature and experimental duration, highlighting the context dependency of outcomes for the host and ecosystem. Our work demonstrates the importance of jointly investigating lethal and nonlethal effects of parasites and provides a novel framework for doing so.
Given their sheer cumulative biomass and ubiquitous presence, parasites are increasingly recognized as essential components of most food webs. Beyond their influence as consumers of host tissue, many parasites also have free-living infectious stages that may be ingested by non-host organisms, with implications for energy and nutrient transfer, as well as for pathogen transmission and infectious disease dynamics. This has been particularly well-documented for the cercaria free-living stage of digenean trematode parasites within the Phylum Platyhelminthes. Here, we aim to synthesize the current state of knowledge regarding cercariae consumption by examining: (a) approaches for studying cercariae consumption; (b) the range of consumers and trematode prey documented thus far; (c) factors influencing the likelihood of cercariae consumption; (d) consequences of cercariae consumption for individual predators (e.g. their viability as a food source); and (e) implications of cercariae consumption for entire communities and ecosystems (e.g. transmission, nutrient cycling and influences on other prey). We detected 121 unique consumer-by-cercaria combinations that spanned 60 species of consumer and 35 trematode species. Meaningful reductions in transmission were seen for 31 of 36 combinations that considered this; however, separate studies with the same cercaria and consumer sometimes showed different results. Along with addressing knowledge gaps and suggesting future research directions, we highlight how the conceptual and empirical approaches discussed here for consumption of cercariae are relevant for the infectious stages of other parasites and pathogens, illustrating the use of cercariae as a model system to help advance our knowledge regarding the general importance of parasite consumption.
Parasites are taxonomically and functionally diverse members of biological communities, and can play key roles in species interactions, community structure, and ecosystem functioning. For their reliance on host species, parasites are theorized to be particularly sensitive to disturbances that alter host diversity and abundance, especially in isolated habitats, which present challenges to introduction and establishment. In this thesis, I investigate habitat isolation and disturbance as drivers of parasite diversity, with an emphasis on parasite life history strategies related to colonization and persistence. I focus on an island-like, frequently disturbed habitat, deep sea hydrothermal vents at 9°50’N on the East Pacific Rise, to explore the boundaries of parasite persistence in an extreme environment. First, I analyze recovery in the vent community for 11 years after a catastrophic eruption in 2006 to test successional hypotheses in a new setting with distinct fauna and a chemosynthesis-based food web. Second, I compare parasite diversity at isolated, disturbed vents to marine ecosystems that are similarly isolated but undisturbed (atoll sandflat) and both well connected and undisturbed (kelp forest). Overall, parasite diversity within host species was not significantly lower at vents, but the vent community had many fewer parasite species because there are fewvertebrate predator species (fish). Parasites with indirect (multi-host) life cycles were relatively diverse in the disturbed environment, which contradicts expectation based on theory. To explore this further, I investigate the three-host life cycles of trematodes at vents, whichwas the most diverse and abundant parasite taxon. All life stages of the trematode life cyclewere discovered in vent fauna and several taxawere traced across multiple life stages via morphology and genetics. Finally, I use a computational model to investigate how different parasite strategies (colonization capability and impact on hosts) contribute to parasite success under a range of disturbance conditions in island habitats. Parasites that reduce host reproduction reached higher densities than parasites that cause mortality across all disturbance frequencies explored, and disturbance facilitated the evolution of more virulent parasites. These studies demonstrate that life history traits and the ability to adapt allow diverse parasite taxa to persist in isolated, ephemeral environments.
While experimental studies have demonstrated within-population variation in host tolerance to parasitism, theoretical studies rarely predict for polymorphism to arise. However, most theoretical models do not consider the crucial distinction between tolerance to the effects of infection-induced deaths (mortality tolerance) and tolerance to the parasite-induced reduction in the reproduction of infected hosts (sterility tolerance). While some studies have examined trade-offs between host tolerance and resistance mechanisms, none has considered a correlation within different tolerance mechanisms. We assume that sterility tolerance and mortality tolerance are directly traded-off in a host population subjected to a pathogen and use adaptive dynamics to study their evolutionary behaviour. We find that such a trade-off between the two tolerance strategies can drive the host population to branch into dimorphic strains, leading to coexistence of strains with sterile hosts that have low mortality and fully fertile with high mortality rates. Further, we find that a wider range of trade-off shapes allows branching at intermediate- or high-infected population size. Our other significant finding is that sterility tolerance is maximised (and mortality tolerance minimised) at an intermediate disease-induced mortality rate. Additionally, evolution entirely reverses the disease prevalence pattern corresponding to the recovery rate, compared to when no strategies evolve. We provide novel predictions on the evolutionary behaviour of two tolerance strategies concerning such a trade-off.
A conflict of interest occurs when parasites manipulate the behavior of their host in contradictory ways. In grass shrimp ( Palaemonetes pugio) , trematode parasites cause the shrimp to be more active than usual around predators, while bopyrid isopod parasites elicit the opposite response. Since these parasites are altering the host’s behavior in opposing directions, a conflict of interest should occur in doubly infected shrimp. Natural selection should favor attempts to resolve this conflict through avoidance, killing, or sabotage. In a field survey of shrimp populations in four tidal creeks in the Cape Fear River, we found a significant negative association between the two parasites. Parasite abundance was negatively correlated in differently sized hosts, suggesting avoidance as a mechanism. Subsequent mortality experiments showed no evidence of early death of doubly infected hosts. In behavior trials, doubly infected shrimp did not show significantly different behavior from other infection statuses, suggesting that neither parasite sabotages the manipulation of the other. Taken together, our results suggest that rather than sabotaging one another directly, bopyrid and trematode parasites reduce conflict by preferentially infecting differently sized hosts. Because grass shrimp exist at high biomass in salt marsh ecosystems and are infected at high prevalence, our findings have implications for ecosystem structure and function.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
This study aimed to investigate the presence of Sarcotaces sp. in Epinephelus epilistictus (the dotted grouper) in Saudi Arabia. So, during our routine clinical examination of fish health conditions at Jubail province in the eastern region of Saudi Arabia (Arabian Gulf), nine grouper fish species were examined for Sarcotaces sp. (Copepoda: Phylichthyidae). Only the dotted grouper ( Epinephelus epilistictus ) harbored parasitic Sarcotaces spp. with an incidence of 9.06% of 1600 clinically examined fish samples. The collected Sarcotaces sp. was Sarcotaces arcticus ( S. arcticus ). The copepods were completely encapsulated cysts with a pyriform or pear-like shape, small to large, white-grayish, fluid-filled with thick black ink beneath the skin, or fully embedded in the muscular layer. The cysts present in the lateral aspect of trunk muscles, flank, caudal peduncle, near the anal opening, or pelvic and pectoral fin with an infestation rate (1–6 cysts) per fish. The cyst histopathology reveals the capsular layer of the cyst consisting of fibrous connective with pressure atrophy of the adjacent muscles associated with dilated blood vessels. The absence of infestation in other kinds of grouper fish species from the water of the Arabian Gulf in Jubail province may indicate parasitic host specificity and geographic locality distribution.
Parasitism is increasingly recognized as a critical element of ecosystem dynamics but remains understudied due to observational limitations, especially in rapidly fluctuating marine plankton populations. We combined 3 new techniques— in situ imaging microscopy, automated classification, and empirical dynamic modeling—to quantify interactions between Oithona spp. and the rhizarian parasite Paradinium spp. at hourly resolution for over 1 yr in the Southern California Bight. We investigate the time scales, host population effects, and potential environmental drivers of infection. Our study suggests that Paradinium spp. is consistently present in the local copepod population at low levels throughout the year and that the parasite exerts control on the host population on a 22-23 d lag—a delay consistent with known Oithona spp. generation times. The interaction strength was pronounced at higher temperatures, suggesting that Paradinium spp. will have a significant role in local ecosystem dynamics as surface ocean temperatures rise.
On the basis of a sampling program performed monthly, a total of 12,033 fiddler crabs, Uca uruguayensis, were collected at the southern end of the Samborombón Bay, Río de la Plata estuary, Argentina, from February 1995 to March 1996. Density ranged from 133 to 207 ind/m2 over the 13-mo study period. The overall proportion of male crabs was 0.62. For small crabs, sex ratio was 1:1, but as crab size increased, sex ratio first became female biased and then male biased. Crabs carried eggs from mid-spring to late summer. Prevalence of the parasite Leidya distorta varied between 5.24% and 17.8% throughout the study. Infested male crabs ≥10.5 mm carapace width, which represented only 5.9% of the crabs collected, housed 68.8% of the total parasites recovered. Cryptoniscus larvae were much more frequent among molting (soft) than intermolt (hard) crabs. The cryptonisci infesting intermolt (hard) crabs were aggregated; i.e., they showed a contagious distribution. Females of L. distorta were actively breeding in spring and summer. In autumn, reproductive activity gradually decreased, and by winter, all the adult female parasites showed empty marsupia. The growth of immature parasites appears to stop in winter and resume in spring. The size of the adult marsupial female parasite was positively correlated with that of the host. Because only 1.1% of the mature female crabs carried marsupial parasites, it is unlikely that L. distorta plays a regulatory role in the reproductive potential of the host population.
I investigated life-history and parasitism in the salt marsh snail, Cerithidea californica. Latitude and growing conditions were important factors determining maturation size. After accounting for environmental variation, there was a negative association between the maturation size of snails and the prevalence of parasitic castration by larval trematodes. As predicted by life-history theory, this may represent an adaptation against parasitism that is similar to previous observations of life-history adaptations in species subject to predation or disturbance. However, it was unclear whether this adaptation was due to phenotypic plasticity or genetic differences among populations resulting from natural selection so I conducted a reciprocal transplant between sites with high and low prevalence and found source population differences in maturation size. It appears, therefore, that the life-history differences between these populations are at least partially genetic or may represent an adaptive developmental switch that was initiated prior to the transplant.
Biological control, as used in terrestrial systems, may hold promise for use against exotic marine species. We first review some marine pests, displaying their diversity, the damage they cause, and possible controls. We then contrast approaches for marine and terrestrial pest control, providing guidelines for adapting terrestrial controls to the marine environment. Although several of the same principles apply in terrestrial and marine environments, marine systems differ with respect to the types of control agents available, the degree of pest-population reduction needed for effective control, the spatial scale over which biological control must operate effectively, the practicality of implementation, and the nature and degree of concern over safety. As an example, we propose a strategy for developing a biological control program against the European green crab, Carcinus maenas, which has had substantial negative impacts where previously introduced (New England, Atlantic Canada, South Africa, south Australia) and which has recently been introduced to central California, and to Tasmania. We conclude that biological control may be possible for some marine pests, but that existing strategies and expectations will require modification.
Introduced species often seem to perform better than conspecifics in their native range. This is apparent in the high densities they may achieve or the larger individual sizes they attain. A prominent hypothesis explaining the success of introduced terrestrial species is that they are typically free of or are less affected by the natural enemies (competitors, predators, and parasites) they encounter in their introduced range compared to their native range. To test this hypothesis in a marine system, we conducted a global assessment of the effect of parasitism and predation on the ecological performance of European green crab populations. In Europe, where the green crab is native, crab body size and biomass were negatively associated with the prevalence of parasitic castrators. When we compared native crab populations with those from introduced regions, limb loss (an estimator of predation) was not significantly lower in introduced regions, parasites infected introduced populations substantially less and crabs in introduced regions were larger and exhibited a greater biomass. Our results are consistent with the general prediction that introduced species suffer less from parasites compared to populations where they are native. This may partly explain why the green crab is such a successful invader and, subsequently, why it is a pest in so many places.
I investigated the prediction that parasitic castrators can reduce host population density. A survey of the salt marsh snail Cerithidea californica suggested a negative association between snail density and the prevalence of larval trematodes which castrate parasitized snails. Field experiments were conducted to determine the mechanisms by which larval trematodes might affect snail populations. Manipulations of snail density and trematode prevalence indicated that larval trematodes reduced the reproductive output of the snail population and caused differential mortality of parasitized hosts. Furthermore, an effect of competition between parasitized and unparasitized snails was detected by comparing snail growth rates. As expected this was deemed to be a simple density effect and was not due to any special qualities of the parasitized snails. Analysis of chlorophyll a levels in the sediment suggested that competition may have occurred due to limited amounts of food. These results suggest that larval trematodes can reduce snail population densities by reducing snail reproduction, competing with parasitized snails for food and increasing the mortality rates of parasitized snails.
This paper surveys the literature on parasitic castration and attempts to provide an evolutionary interpretation of the phenomenon. Previous explanations are considered and a unifying hypothesis is proposed. The main theses of this paper are (1) that parasitic castration can be viewed as a parasite's adaptation and (2) that advantages derived from this adaptation are a result of a reduction in host reproductive effort; which in turn gives rise to increased host survivorship, increased host growth and/or increased energy available to the parasite, thereby increasing the parasite's Darwinian fitness. A survey of the literature indicates: a) That castration effects on the hosts are beneficial to the parasite but not to the host; b) That the genetic relationship of castrators within individual hosts is such that natural selection at the level of individual genotypes can account for the observed effects; and c) That the widespread occurrence of hormonal castration favors the interpretation outlined above. Incidental castration and the possibility of parasitic castration as a host's adaptation are considered, and a definition of parasitic castration is proposed.
Ecological studies have demonstrated that parasites are capable of influencing various aspects of host life history and can play an important role in the structure of animal populations. We investigated the influence of infection by castrating trematodes on the reproduction, survival and population density of the intertidal snail Zeacumantus subcarinatus, using both laboratory and field studies. The results demonstrate a highly significant reduction in the reproductive output in heavily infected populations compared to populations with low trematode prevalence. A long-term laboratory study showed reduced survival of infected snails compared to uninfected specimens, for snails held at 18 and 25 degrees C. Furthermore, parasite-induced mortality in the field was inferred from a reduction in prevalence of infection among larger size classes, indicating that infected individuals disappear from the population, although the effect of parasites varied between localities. A field survey from 13 localities including 2897 snails demonstrated that prevalence of castrating trematodes had a significant negative effect on both population density and biomass of Z subcarinatus. This study provides one of the first demonstrations of population-level effects of parasites on their hosts in the field. The results of this study emphasise the importance of castrating parasites as potential agents of population regulation in host species with limited dispersal ability.
An analysis of life history features of insect parasitoids and crustacean parasitic castrators suggests that these are similar trophic phenomena, distinct from parasitism and predation. A parasitoid consumes only one host during its lifetime; parasitic castrators cause the reproductive death of only one host. Since population densities of many insect species are regulated by parasitoids, parasitic castrators may also play an important role in host population regulation. Parasitoids of insects and parasitic castrators of crustaceans (1) in single infections always kill the host; whereas lone parasites do not affect host viability; and predators kill many prey; (2) do not cause increasing pathology or increasing likelihood of mortality in multiple infections; whereas parasites often have an additive impact; (3) do not cause increasing damage in mixed species infections; whereas mixed parasite infections often have interactive negative effect; (4) Usually have mechanisms to reduce or eliminate multiple infec...
In species assemblages of larval trematodes in individual snail hosts, fewer multispecies infections are observed than might be expected by chance. Both interspecific competition and the isolating effect of heterogeneity in recruitment may explain this pattern of community structure. Here, we analyzed the expected and observed frequency of double infections, using data culled from 62 studies. Our analysis included 296,180 host snails. Of these, 62,942 were infected with one or more species of trematode (23% pooled over all studies, 24% average across studies). By incorporating information from subsamples, we were able to estimate the proposed isolating effect of heterogeneity in recruitment. Surprisingly, spatial and temporal heterogeneity as well as differential prevalence among host size classes typically led to intensification of interactions (average increases in interactions by +19%, +19%, and +23%, respectively), while partitioning among host species usually led to isolation of potential competitors (a -1% average decrease in interactions). We calculated the expected number of interspecific double infections by applying rules of independent assortment to the frequency of trematode species. The majority of the 14,333 expected interactions did not persist; only 4,346 double infections were actually observed (a 69% decrease, 62% average). Competition, via a variety of interspecific competitive mechanisms by dominant species, is the structuring process most consistent with this paucity of observed multispecies interactions. How important is competition? Overall, we estimated that 13% (10% average) of the trematode infections were lost to interspecific interactions. Subordinate species in particular suffered very high losses.
The shore crabs, Hemigrapsus oregonensis and H. nudus, sometimes kill the female endoparasitic entoniscid isopod, Portunion conformis, a parasitic castrator. Studies of host populations from Baja California, Mexico to Vancouver Island, Canada, show that the incidence of parasitized hosts with dead parasites and the percentage of the parasite population found dead vary markedly with locality but only occasionally with season. Both higher incidences of hosts with dead P. conformis and higher proportions of the total parasite population found dead are associated with (1) high prevalence of parasitism, (2) female hosts and (3) large hosts. Within a host, the proportion of the parasites that are dead is not related to the degree of multiple infection. Typically, either all or none of the parasites in a multiple infection are dead. Supernumerary juvenile parasites do not suffer differential mortality. The developmental stage of the female parasite does not seem to influence the likelihood of death. The presence of dead parasites may not confer an acquired immunity to re-infection. These features suggest that parasite death is typically the result of activation of a successful host defensive process rather than indicative of a defect on the part of the parasites. Parasitized female hosts can regain their reproductive capabilities following death of the parasite. Post-parasitic broods are smaller than normal. Reproductive recovery is presumed to provide the selective pressure favouring evolution of a lethal host response. The host-produced sheath surrounding female parasites is a haemocytic response. Sheaths enclosing dead parasites are thicker and more electron dense than those containing healthy parasites. The sheath of a healthy P. conformis may actually protect the parasite from a more intense host response.
This review describes aspects of the life cycle and ecology of the Rhizocephala emphasizing (i) comparison with more conventional Cirripedia, and (ii) evolutionary and phylogenetic perspectives. Despite numerous extreme specializations to living as parasites in other Crustacea, most features of the rhizocephalan life cycle resemble those seen in other Cirripedia, and only the process of host invasion and the ensuing redifferentiation of the adult parasite represent truly unique features. Larval biology of the Rhizocephala has developed under selection pressures induced by the difficulty of locating the substratum for settlement, host defences against parasite invasion, and the special demands imposed on the sexual system of a parasite. Thus rhizocephalans have (i) lecithotrophy coupled with very small-sized larvae, (ii) special sensory organs in the cyprid, (iii) a very rapid host invasion accomplished by minute, female stages, and (iv) dwarf males nourished by the adult female parasite, such that it emulates a true hermaphrodite. This review also surveys the nature and underlying causes of the numerous effects that rhizocephalan parasites can induce on their hosts in terms of morphology, physiology, and behaviour. The ‘host control’ induced by rhizocephalans ensures that both male and female hosts accept the parasite as their own brood and care for it accordingly. This, and other details of host-parasite co-evolutions are discussed. © 1995, Marine Biological Association of the United Kingdom. All rights reserved.
The morphology, biology and life history of the immature stages, the free-living and the neotenic females (of the suborders Mengenillidia and Stylopidia respectively) and the free-living males of the order Strepsiptera are discussed. Strepsiptera are entomophagous parasitoids and are known to parasitize seven orders and thirty-five families of Insecta. The morphological and physiological changes they cause to the host insect are outlined. The classification of the order is revised; the geographical distribution, phylogenetic system and keys to the families, subfamilies and genera (when possible) are given. As the sexes are dimorphic, separate keys are provided for adult males and neotenic females.
Recent population-dynamic theory suggests that mechanisms of lethal interference competition can have profound effects on parasitoid coexistence and pest suppression in biological control systems. We investigated lethal intraspecific and interspecific interference competition in Eretmocerus eremicus and Encarsia sophia, parasitoids of the whitefly pest, Bemisia tabaci. Our first experiments evaluated whether one or both species could suppress the progeny production of the other species through two mechanisms of lethal interference competition: (1) usurpation of hosts in cases of multiparasitism, and (2) host feeding on and killing parasitised hosts. We found that both species could suppress the progeny production of the other. E. eremicus' effect on E. sophia appeared to reflect multiparasitism. E. sophia's effect on E. eremicus appeared to reflect a combination of multiparasitism and host feeding on parasitised hosts. Second, we investigated the effects of lethal intraspecific interference on conspecific progeny production in both species. E. sophia interfered intraspecifically by host feeding on parasitised hosts. E. eremicus also apparently host fed on parasitised hosts, however the effect of host feeding on conspecific progeny production was slight. Third, host dissections and behavioral observations confirmed the mechanisms inferred from the progeny production experiments. Our results suggest a need to consider mechanisms of lethal interference competition in theoretical and empirical research on parasitoid competition.
Carapidae (or pearlfish) are eel-like fishes that live inside different invertebrates, such as holothurians, sea stars, or bivalves. Those of the genus Carapus are commensal and use their host as a shelter, while Encheliophis species are parasitic and eat the hosts gonads. In areas where they live in sympatry, C. boraborensis, C. homei, C. mourlani and E. gracilis are able to inhabit the same host species. Infestation is considered as monospecific when several conspecifics are observed in the same host. However, many aspects of this particular relation remain obscure, e.g. communication between carapids and the defence systems of the different protagonists (carapids and hosts). Experiments have been conducted in the field and laboratory to investigate several aspects of the carapids relationships with their hosts. Sampling carried out in the Bay of Opunohu (Moorea, French Polynesia) determined the sex ratio of C. boraborensis (3:1) and C. homei (1:1) and their distribution rate within different Echinodermata. Our study showed that neither species was capable of determining whether a heterospecific already occupied a sea cucumber or not. They were, however, able to locate the sea cucumbers cloaca, due to the excurrent resulting from respiration. The sea cucumbers defence system (Cuverian tubules) minimises predator attacks, but is not effective against carapid intrusion. The Carapidae defence system is twofold. Due to a passive system related to the sea cucumbers low cloacal position, the Cuverian tubules are not expelled when fish enter the cloaca. Moreover, carapids resist sea cucumber toxins better than other reef fish. Their increased resistance might be related to their gills rather than to their mucus coating; however, the latter may assist the fish in resisting the sticky substances emitted by the Cuverian tubules.
Parasitic dinoflagellates have recently emerged as significant disease agents of commercially important crustaceans. For example, epizootics of Hematodinium have seriously affected certain crab and lobster fisheries. The parasitic dinoflagellates of crustaceans are, however, relatively unknown. Marine crustaceans are parasitized by two orders of dinoflagellates: the Blastodinida and the Syndinida. Crustaceans are also parasitized by the Paradinida and the Ellobiopsidae, taxa that have close historical ties and possible taxonomic affinities with the dinoflagellates. The taxonomy and life history patterns of the different parasitic species are largely dictated by their host-parasite relationships. For example, sporulation in the blastodinids occurs internally but is completed externally with the expulsion of spores via the anus of the host. The egg-parasitic chytriodinids sporulate externally after destroying their host egg. The tissue-dwelling syndinids have plasmodia that sporulate internally and generally kill their hosts upon the expulsion of the dinospores. Unfortunately, complete life cycles have not been elucidated for any of the parasitic forms, hence characteristics of the life cycles must be applied cautiously to the systematics of the taxa. For example, gamogony and the presence of resting cysts are only known from a few species; they probably occur in most species. Further work on the life cycles of the parasitic dinoflagellates of crustaceans should concentrate on establishing the life cycles of representative species from each order or family. Parasitic dinoflagellates infect copepods, amphipods, mysids, euphausiids, and decapods. Their pathogenicity varies with their invasiveness in the host. The gut-dwelling blastodinids are relatively benign, while the chytriodinids kill their host egg. Members of the pervasive Syndinida and Paradinida are overtly pathogenic and insidiously ramify throughout the hemal sinuses and organs of their hosts. Members of the Ellobiopsidae vary from the commensal Ellobiocystis to the overtly parasitic Thalassomyces. Host castration and feminization are common pathologic results of infection by these parasites. The severity of the castration is dependent upon the invasiveness of the parasitic species and the duration of the infection, while the degree of feminization is related to the stage at which the host acquires the infection. Most of the parasitic dinoflagellates occur in epizootics in their host populations. Recent epizootics of Hematodinium spp. have had severe effects on crustacean fisheries in Alaska, Virginia, and Scotland, and may potentially result in changes to the benthic communities of the hosts. The epizootics are often associated with host-parasite systems that occur in regions with unique hydrological features, such as fjords or poorly draining estuaries with shallow sills. These regions are ideal for the application of a “landscape” ecology approach that could lead to a better understanding of the epizootiology of parasitic dinoflagellates and other marine pathogens.
A primary difference between predators and parasites is the number of victims that an individual attacks throughout a life-history stage. A key division within natural enemies is whether a successful attack eliminates the fitness of the prey or the host. A third distinctive axis for parasites is whether the host must die to further parasite development. The presence or absence of intensity-dependent pathology is a fourth factor that separates macroparasites from microparasites; this also distinguishes between social and solitary predators. Combining these four dichotomies defines seven types of parasitism, seven corresponding parasites, three forms of predation and, when one considers obligate and facultative combinations of these forms, four types of predator. Here, we argue that the energetics underlying the relative and absolute sizes of natural enemies and their victims is the primary selective factor responsible for the evolution of these different trophic strategies.
Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.
It has been suggested that the harm parasites cause to their hosts is an unavoidable consequence of parasite reproduction with costs not only for the host but also for the parasite. Castrating parasites are thought to minimize their costs by reducing host fecundity, which may minimize the chances of killing both host and parasite prematurely. We conducted a series of experiments to understand the evolution of virulence of a castrating bacterium in the planktonic crustacean Daphnia magna. By manipulating food levels during the infection of D. magna with the bacterium Pasteuria ramosa, we showed that both antagonists are resource-limited and that a negative correlation between host and parasite reproduction exists, indicating resource competition among the antagonists. Pasteuria ramosa also induces enhanced growth of its hosts (gigantism), which we found to be negatively correlated with host fecundity but positively correlated with parasite reproduction. Because infected hosts never recovered from infections, we concluded that gigantism is beneficial only for the parasite. Hosts, however, have evolved counteradaptations. We showed that infected hosts have enhanced reproduction before castration. This shift to earlier reproduction increases overall host fecundity and compromises parasite reproduction. Finally, we showed that this resource conflict is subject to genetic variation among host and parasite genotypes within a population and is therefore likely to be an important force in the coevolution of virulence in this system. A verbal model is presented and suggests that the adaptive value of gigantism is to store host resources, which are liberated after parasitic castration for later use by the growing parasite. This hypothesis assumes that infections are long lasting, that is, that they have a high life expectancy.
This study analyses the effect of host-specific pathogens on range restriction of their hosts across environmental gradients at population margins. Sterilizing diseases can limit host range by causing large reductions in population size in what would otherwise be the central area of a species range. Diseases showing frequency-dependent transmission can also pull back a population from its disease-free margin. A wide range of disease prevalence versus abundance patterns emerge which often differ from the classical expectation of increasing prevalence with increasing abundance. Surprisingly, very few empirical studies have investigated the dynamics of disease across environmental gradients or at range limits.
Increasing species diversity typically increases biomass in experimental assemblages. But there is uncertainty concerning the mechanisms of diversity effects and whether experimental findings are relevant to ecological process in nature. Hosts for parasites provide natural, discrete replicates of parasite assemblages. We considered how diversity affects standing-stock biomass for a highly interactive parasite guild: trematode parasitic castrators in snails. In 185 naturally occurring habitat replicates (individual hosts), diverse parasite assemblages had greater biomass than single-species assemblages, including those of their most productive species. Additionally, positive diversity effects strengthened as species segregated along a secondary niche axis (space). The most subordinate species--also the most productive when alone--altered the general positive effect, and was associated with negative diversity effects on biomass. These findings, on a previously unstudied consumer class, extend previous research to illustrate that functional diversity and species identity may generally both explain how diversity influences biomass production in natural assemblages of competing species.
Host fecundity reduction is a life-history trait that is commonly exhibited in parasitic associations. It is particularly prevalent in female invertebrate hosts that invest heavily in egg production during a relatively short life span. Here, Hilary Hurd uses examples of parasitized insects and trematode infections of snails to consider the evolutionary significance of this response to infection. Studies of host egg production and reports of the physiological mechanisms underlying reduction of host reproductive success are used to evaluate the hypotheses that fecundity reduction might be a by-product of infection, or an adaptive strategy on the part of parasite or host.
This book addresses the behavioural adaptations of parasites across a broad range of taxa, including parasitoid wasps, entomopathogenic nematodes, seed-feeding insects and plant-parasitic nematodes. The chapters emphasize the fundamental principles of parasitism and address the diversity and sophistication of parasite behavioural adaptations. The chapters are arranged in 4 sections discussing foraging for hosts, host infection, interactions among parasites within hosts and parasite-host interactions.
Protein synthesis was measured in ovary and hepatopancreas of intact and eyestalk-ablated fiddler crabs (Uca pugilator) in vitro. A crude extract of eyestalks from the shrimp Penaeus setiferus inhibited ovarian weight gain in eyestalk-ablated crabs. This crude eyestalk extract also inhibited in vitro protein synthesis in ovaries from intact and eyestalk-ablated crabs. A polyclonal antibody to crab vitellogenin was used to measure vitellogenin synthesis in ovaries, hepatopancreas, and hemolymph in vitro. Gonad-inhibiting hormone was partially purified from the crude eyestalk extract. The partially purified material inhibited vitellogenin synthesis in ovarian tissues in vitro.
Pachygrapsus transversus (N = 1814) from intertidal locations in eastern Bermuda were examined from 1973–78 for the branchially infesting bopyrid isopod Leidya bimini. In two main collecting areas, Whalebone Bay(N = 1280) and Ferry Reach (N = 489), the incidence of infestations with all life history stages was 9.0 and 29.5%, respectively. This difference is explained by the larger numbers of older crabs in the Ferry Reach samples. The mean width of crabs infested with mature female isopods was similar for both locations (14.4 versus 16.0 mm, respectively). Five-hundred and eleven isopods were recovered from 1814crabs: 106 (20.7 %) cryptoniscids, 45 (8.8 %) sexually undifferentiatedjuveniles, 152(29.7%) males, 112(21.9%) immature females, and 96 (18.8%) mature females. Limited data suggest that the main period for cryptoniscid invasion of crabs is from April through July. None of the 149 ovigerous crabs, among 857 females from the two main collecting areas, harbored mature isopods, indicating castration. It was further shown that a preponderance of nonovigerous infested crabs (= 10mm wide) had little or no gonad development as compared to uninfested animals. Morphometric data on the life history stages of Leidya are compiled and some female developmental stages are illustrated. Mature isopods produce at least two broods of embryos, with as many as 21 000 per brood in the larger females. While female isopod size may be controlled by host size, evidence indicates that maturation occurs independently, i.e. the parasites mature at a smaller size in smaller hosts. Mature as well as some ofthe large immature female parasites produce a relatively subtle lateral swelling of the crab§ carapace. As two mature female isopods have never been found in a single crab, this swelling was always unilateral. The height of the body on the infested side is also increased. Left and right branchial chambers are equally susceptible to invasion and development ofthe isopod. Recognizable gill damage and sometimes damage to maxillary epipodites occurred in 52.5% of infested crabs, particularly in the larger ones harboring the larger parasites (i.e. crabs= 15mm wide). Forty three Pachygrapsus gracilis sympatric with P. transversus at Ferry Reach were devoid of bopyrids.
The Rhizocephala is a group of extremely reduced parasitic crustaceans, that exclusively parasitize other Crustacea. In the family Sacculinidae, the external sac-like part (externa) of the adult parasite contains the reproductive apparatus and is attached beneath the abdomen of the host crab. Hosts with more than one externa may occur and are in most cases believed to have arisen from multiple cyprid larvae. However, in three species of the genus Sacculina, multiple externae have been shown to originate by asexual reproduction from a single parasitic cypris larva. We present a phylogenetic analysis of ten species of Sacculina and outgroups based on partial sequences from the cytochrome oxidase 1 (CO1) and the entire 18s rDNA gene. A separate parsimony analysis from the 18s rDNA and CO1 genes resulted in two trees with almost identical topologies. Both genes strongly support a monophyletic, asexually reproducing clade and fail to support a monophyletic Sacculina genus. As a consequence we have established a new genus, Polyascus, to accommodate three members of this clade which also share a number of common morphological features.
Fiddler crabs Uca uruguayensis were collected monthly in Punta Rasa, at the southern end of the Samborombón Bay, Río de la Plata, Argentina, from February, 1995, to March, 1996. Throughout the study, 1,115 of 12,033 crabs (9.3%) were infested by different developmental stages of the branchial bopyrid Leidya distorta, which is herein reported for the first time as infesting U. uruguayensis. The distribution of this parasite, previously known from New Jersey to Rio de Janeiro, is now extended even farther south, to the mouth of the Río de la Plata. Prevalence of L. distorta increased as a function of crab size. The newly settled cryptoniscus larvae were found in the space between contiguous gill lamellae after invading a previously uninfested branchial chamber. The cryptoniscus larva transformed into an early juvenile and, after molting one or more times, migrated to the roof of the branchial chamber, where it grew and finally reached the ovigerous condition. Female parasites usually carried cryptonisci or males, eventually both, on their bodies. Males were found in different positions on the females as the latter developed. Crabs housing a mature female parasite frequently bore an unpigmented area on the lateral wall of the branchial chamber. An additional faded area was sometimes observed on the bottom of the eye orbit. Adult female parasites usually produced a subtle lateral swelling on the carapace of the host, this deformation being more marked in smaller crabs than in larger ones. The major chela of the male crabs parasitized by adult females was, on average, 6.5% shorter than that of unparasitized ones. Alterations of the gills of the host were noticed: the adult female parasite had a strong dorsal carina that fitted between the fourth and fifth gills of the crab, displacing them laterally and making contact with the floor of the branchial chamber. The inner surface of the crab branchiostegite bore a large horizontal vessel from which the parasite presumably obtained hemolymph. Besides the bopyrid isopod forming the subject of this report, we found 61 crabs harboring a nematode larva, identified as Skrjabinoclava sp., among the internal organs of the crab.
Over half of all living species of plants and animals are parasitic, which by definition involves intimate association with and unfavourable impact on hosts (Price, 1980). This paper will only consider parasites whose ‘unfavourable impact’ adversely affects the birth and/or mortality rates of their hosts (Anderson, 1978). Most organisms are potential hosts and must deal with the problem of parasitism. The probability of parasitic infection of a host is influenced by both environmental and genetic factors. Traditionally it was assumed that a host was either resistant or susceptible to a particular parasite and therefore the interaction between a parasite and potential host had only two possible outcomes: either the resistant host rebuffed the parasitic attack and remained uninfected or the parasite successfully invaded and significantly reduced the reproductive success of the susceptible host. This approach, however, ignored the intraspecific genetic variation present within both host and parasite populations (Wakelin, 1978). Since the outcome is determined by the interaction of a finite set of host genes and parasite genes, genetic variation in host susceptibility and parasite infectivity (Richards, 1976; Wakelin, 1978) suggests that more than two outcomes are possible. Variation in host and parasite genomes does not begin and end at the susceptibility/infectivity loci. Other genes may also influence the outcome of host–parasite interactions by altering the life-history patterns of hosts and parasites, and lead to a variety of outcomes.(Accepted June 25 1984)
(1) Three categories of biological processes are shown to have a destabilizing influence on the dynamical behaviour of model host-parasite associations: parasite induced reduction in host reproductive potential, parasite reproduction within a host which directly increases parasite population size and time delays in parasite reproduction and transmission. (2) The importance of parasitic species as regulators of host population growth is examined in light of empirical evidence. Data from two particular laboratory studies used to indicate the magnitude of this regulatory influence. Suggestions are made concerning the type of information required from field studies to facilitate critical assessment of theoretical predictions.
1. Few studies have directly addressed the role played by parasites in the structure and function of ecosystems. Parasites influence the behaviour, reproduction and overall fitness of their hosts, but have been usually overlooked in community and ecosystem-level studies. We investigated the effects of trematode parasites on snail–periphyton interactions.
2. Physa acuta (Gastropoda: Pulmonata) snails infected with the trematode Posthodiplostomum minimum (often >30% of within-shell biomass) grazed more rapidly than uninfected snails. Trematode effects on snail grazing indirectly affected the standing stock and community structure of periphyton. Populations of snails with 50% infected individuals reduced algal biomass by 20% more than populations with lesser (10% or 0%) infection rates.
3. The alga Cladophora glomerata dominated periphyton communities grazed by snail populations with 50% infection rates, whereas diatoms and blue–green algal taxa dominated when grazed by snail populations with lower infection rates.
4. Thus, trematodes indirectly affected periphyton communities by altering host snail behaviour, a trait-mediated indirect effect. These results indicate that trematodes can indirectly influence benthic community structure beyond simple population fitness, with possible related effects on ecosystem function.
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.
Kuris A. M. 1980. Effect of exposure to Echinostoma liei miracidia on growth and survival of young Biomphalaria glabrata snails. International Journal for Parasitology10: 303–308. Exposure to miracidia of Echinostoma liei resulted in increased mortality and reduced growth of 1–2 mm albino Biomphalaria glabrata snails whether or not the snails became infected. Growth rates for infected and exposed but uninfected snails were significantly more variable than growth rates of unexposed snails. Retarded growth and increased mortality were detected as rapidly as seven to nine days after exposure. Neither growth nor survivorship of 4–6 mm snails was altered upon exposure to or infection by E. liei.
The digenetic trematodes Schistosoma mansoni and Echinostoma paraensei have a common snail host Biomphalaria glabrata. In this article, Eric Loker and Coen Adema discuss how these parasite species evade the host immune response in fundamentally different ways.
An analogy between the tropic interactions of insect pest-hymenopterous parasitoid and snail-larval trematode systems is proposed. The goal of most agricultural pest management programs is increase in production of a plant crop, the deleterious agent is an herbivorous insect pest, the controlling agent, a parasitoid. Other parasitoid species may or may not have a significant effect on the control of the host by the key mortality factor.In snail—schistosome systems the goal is reduction of worm burdens in human populations, removed in space and time from the snail-sporocyst interaction; the deleterious agent is the schistosome, trophically equivalent to the hymenopterous parasitoid. Therefore, control may be achieved through competitive displacement of the schistosomes by other larval trematodes having superior intrinsic competitive abilities and better searching efficiencies at low host densities.Hyperparasites, sciomyzid Diptera and Daubaylia may also play a role in this view of schistosomiasis control. The Hassell-Varley parasite quest theory is applied to larval trematodes. The inversely proportional relationship between the area of discovery and miracidial density when logarithmically transformed is further evidence for the dynamic similarity of snail-trematode and insect-parasitoid systems.Other applications of the generally accepted principles of insect pest biological control to a medically important trematode indicate that (1) schistosome population control, not eradication, is the appropriate goal of public health programs, (2) the criteria for implementation and success of such programs must be in terms of the relationship between medical injury and the frequency distribution of worms in humans, and (3) a good biological control agent is likely to have a high searching efficiency at low host densities, kill more than one snail host, be highly host specific, be scarce when successful, reside in regions were schistosomiasis is negligible as a medical problem.
Models of the evolution of virulence have typically focused on increased mortality, one of two negative effects that parasites can inflict on their host. Those that consider the other effect, fecundity reduction, can predict that parasites should completely sterilize their hosts. Although this prediction seems extreme, sterilization features prominently in a fascinating strategy, parasitic castration. Such castration can be accompanied by gigantism (unusually large growth of infected hosts), long infectious periods, and fecundity compensation (where, before heavy parasite burdens ensue, newly infected hosts reproduce earlier/more than they would if not infected). Using a model of dynamic energy budgets (DEB), we show how these results readily emerge, assuming that parasites consume energy reserves of the host. The simple, but mechanistic, DEB model follows energy flow though hosts and parasites, starting with ingestion, and continuing with storage of assimilated energy, and use of those reserves for growth and reproduction, as allocated by the host according to the "κ-rule". Using this model, we compare and contrast two strategies for parasites. "Consumers" only steal energy from their hosts, thereby indirectly altering allocation of energy to growth and reproduction, reducing fecundity, and enhancing mortality. "Castrators" steal energy but also directly modify the scheme by which hosts allocate reserve energy, shunting resources from reproduction to growth. Not surprisingly, the model predicts that this strategy should promote gigantism, but it also forecasts longer infectious periods and fecundity compensation. Thus, commonly observed characteristics of parasitic castration readily emerge from a mechanistic model of energy flow using a minimal number of assumptions. Finally, the DEB model for both "consumers" and "castrators" highlight that variation in resources supplied to hosts promotes variation in virulence in a given host-parasite system, holding all else equal. Such predictions highlight the potential importance of resource ecology for virulence in disease systems.
Parasite-induced alteration of host behaviour is a widespread transmission strategy among pathogens. Understanding how it works is an exciting challenge from both a mechanistic and an evolutionary perspective. In this review, we use key examples to examine the proximate mechanisms by which parasites are known to control the behaviour of their hosts. Special attention is given to the recent developments of post-genomic tools, such as proteomics, for determining the genetic basis of parasitic manipulation. We then discuss two novel perspectives on host manipulation (mafia-like strategy and exploitation of host compensatory responses), arguing that parasite-manipulated behaviours could be the result of compromises between host and parasite strategies. Such compromises may occur when collaborating with the parasite is less costly for the host in terms of fitness than is resisting parasite-induced changes. Therefore, even when changes in host behaviour benefit the parasite, the host may still play some role in the switch in host behaviour. In other words, the host does not always become part of the parasite's extended phenotype. For example, parasites that alter host behaviour appear to induce widely disseminated changes in the hosts' central nervous system, as opposed to targeted attacks on specific neural circuits. In some host-parasite systems, the change in host behaviour appears to require the active participation of the host (e.g., via host immune-neural connections). Even when the change in host behaviour results in clear fitness benefits for the parasite, these behavioural changes may sometimes be produced by the host. Changes in host behaviour that decrease the fitness costs of infection could be selected for, even if these changes also benefit the parasite.
Parasitic castration, the specific blocking of host reproductive output by an individual parasite, is a host-parasite interaction common to many invertebrates, particularly crustaceans, echinoderms and molluscs. It can reduce host density, alter host population dynamics and the evolution of host life history traits. Here we show that parasitisation by a single female cymothoid isopod, Anilocra apogonae, castrates its vertebrate host, the five-lined cardinalfish, Cheilodipterus quinquelineatus. Parasitised male fish fail to mouthbrood their young. The gonads of parasitised fish are smaller and parasitised female fish have substantially fewer and smaller ova than do the gonads of unparasitised fish. As for parasitic castrators of invertebrate hosts, A. apogonae on C. quinquelineatus are uniformly dispersed amongst infested hosts (one adult female isopod per host), are site specific, and their body size is highly correlated with that of their host. These isopods are large relative to the body size of their hosts, averaging 3.8% of the weight of the host. Parasitised fish also weigh less and are shorter than unparasitised fish of the same age. Despite the presence of other potential hosts, A. apogonae only infests C. quinquelineatus. The consistency of the ecological correlates amongst known parasitic castrators suggests that the parasitic castrator host-parasite relationship will be recognised for other parasites of vertebrates.
Larval trematodes frequently castrate their snail intermediate hosts. When castrated, the snails do not contribute offspring to the population, yet they persist and compete with the uninfected individuals for the available food resources. Parasitic castration should reduce the population growth rate lambda, but the magnitude of this decrease is unknown. The present study attempted to quantify the cost of parasitic castration at the level of the population by mathematically modeling the population of the planorbid snail Helisoma anceps in Charlie's Pond, North Carolina. Analysis of the model identified the life-history trait that most affects lambda, and the degree to which parasitic castration can lower lambda. A period matrix product model was constructed with estimates of fecundity, survival, growth rates, and infection probabilities calculated in a previous study. Elasticity analysis was performed by increasing the values of the life-history traits by 10% and recording the percentage change in lambda. Parasitic castration resulted in a 40% decrease in lambda of H. anceps. Analysis of the model suggests that decreasing the size at maturity was more effective at reducing the cost of castration than increasing survival or growth rates of the snails. The current matrix model was the first to mathematically describe a snail population, and the predictions of the model are in agreement with published research.
We analyze the evolutionary consequences of host resistance (the ability to decrease the probability of being infected by parasites) for the evolution of parasite virulence (the deleterious effect of a parasite on its host). When only single infections occur, host resistance does not affect the evolution of parasite virulence. However, when superinfections occur, resistance tends to decrease the evolutionarily stable (ES) level of parasite virulence. We first study a simple model in which the host does not coevolve with the parasite (i.e., the frequency of resistant hosts is independent of the parasite). We show that a higher proportion of resistant host decreases the ES level of parasite virulence. Higher levels of the efficiency of host resistance, however, do not always decrease the ES parasite virulence. The implications of these results for virulence management (evolutionary consequences of public health policies) are discussed. Second, we analyze the case where host resistance is allowed to coevolve with parasite virulence using the classical gene-for-gene (GFG) model of host-parasite interaction. It is shown that GFG coevolution leads to lower parasite virulence (in comparison with a fully susceptible host population). The model clarifies and relates the different components of the cost of parasitism: infectivity (ability to infect the host) and virulence (deleterious effect) in an evolutionary perspective.
We investigate the evolution of virulence of pathogens that reduce their hosts' fitness primarily by affecting host fecundity. We show that, under many conditions, such sterilizing pathogens evolve high rather than intermediate levels of virulence, and this pushes the pathogen population and sometimes the host population toward extinction. We also show that spatial population structure can reverse this evolutionary result and allow the persistence of intermediate-virulence pathogens. Thus, spatial population structure may be vital to the persistence of sterilizing pathogens in nature.
Redial populations of Paryphostomum segregatum were examined in Biomphalaria glabrata. In mature infections the number of rediae was proportional to the size of the snail host. The maximum size of the redial population in snails of similar size remained approximately the same whether the snails were exposed to 1, 10 or 100 miracidia each.
Frequency distributions from 49 published wildlife host-macroparasite systems were analysed by maximum likelihood for goodness of fit to the negative binomial distribution. In 45 of the 49 (90%) data-sets, the negative binomial distribution provided a statistically satisfactory fit. In the other 4 data-sets the negative binomial distribution still provided a better fit than the Poisson distribution, and only 1 of the data-sets fitted the Poisson distribution. The degree of aggregation was large, with 43 of the 49 data-sets having an estimated k of less than 1. From these 49 data-sets, 22 subsets of host data were available (i.e. host data could be divided by either host sex, age, where or when hosts were sampled). In 11 of these 22 subsets there was significant variation in the degree of aggregation between host subsets of the same host-parasite system. A common k estimate was always larger than that obtained with all the host data considered together. These results indicate that lumping host data can hide important variations in aggregation between hosts and can exaggerate the true degree of aggregation. Wherever possible common k estimates should be used to estimate the degree of aggregation. In addition, significant differences in the degree of aggregation between subgroups of host data, were generally associated with significant differences in both mean parasite burdens and the prevalence of infection.
A panel of 4 digenetic trematode species (Echinostoma paraensei, E. trivolvis, Schistosoma mansoni, and Schistosomatium douthitti) and 5 snail species (Biomphalaria glabrata, Helisoma trivolvis, Lymnaea stagnalis, Stagnicola elodes, and Helix aspersa) was examined to determine if known patterns of host specificity could be explained by the tendency of digenean larvae to be bound by snail hemocytes, or by the ability of larvae to influence the spreading behavior of hemocytes. In short-term (1 hr) in vitro adherence assays, there was no overall pattern to suggest that sporocysts were more likely to be bound by hemocytes from incompatible than compatible snails. Compared with the other parasites, sporocysts of E. paraensei were less likely to be bound by hemocytes from any of the snail species tested. All rediae examined, including those of another species Echinoparyphium sp., were also remarkably refractory to binding by hemocytes from any of the snails. Of all the larvae examined, only sporocysts and young daughter rediae of E. paraensei caused hemocytes to round up in their presence. This was true for hemocytes from the compatible species B. glabrata and the incompatible lymnaeid species S. elodes and L. stagnalis. The patterns of host specificity shown by this particular panel of parasites and snails were not predicted by either the extent of hemocyte adherence to digenean larvae or by the ability of larvae to affect hemocyte spreading behavior. The results of this study suggest that a role for hemocytes, although likely, may require different assays, possibly of a more prolonged nature, for its detection. Also, different parasite species (notably E. paraensei) and intramolluscan stages have distinctive interactions with host hemocytes, suggesting that the determinants of specificity vary with the host-parasite combination, and with the parasite life cycle stage.