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Armand M. Kuris

Publications and source records attributed to Armand M. Kuris.

At least 37 records · Page 2Linked to original sources

A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites

For trophically transmitted parasites that manipulate the phenotype of their hosts, whether the parasites do or do not experience resource competition depends on such factors as the size of the parasites relative to their hosts, the intensity of infection, the extent to which parasites share the cost of defending against the host’s immune system or manipulating their host, and the extent to which parasites share transmission goals. Despite theoretical expectations for situations in which either no, or positive, or negative density-dependence should be observed, most studies document only negative density-dependence for trophically transmitted parasites. However, this trend may be an artifact of most studies having focused on systems in which parasites are large relative to their hosts. Yet, systems are common where parasites are small relative to their hosts, and these trophically transmitted parasites may be less likely to experience resource limitation. We looked for signs of density-dependence in Euhaplorchis californiensis (EUHA) and Renicola buchanani (RENB), two manipulative trematode parasites infecting wild-caught California killifish (Fundulus parvipinnis). These parasites are small relative to killifish (suggesting resources are not limiting), and are associated with changes in killifish behavior that are dependent on parasite-intensity and that increase predation rates by the parasites’ shared final host (indicating the possibility for cost sharing). We did not observe negative density-dependence in either species, indicating that resources are not limiting. In fact, observed patterns indicate possible mild positive density-dependence for EUHA. Although experimental confirmation is required, our findings suggest that some behavior-manipulating parasites suffer no reduction in size, and may even benefit when "crowded" by conspecifics.

Integrative and Comparative Biology

Sapronosis: a distinctive type of infectious agent

Sapronotic disease agents have evolutionary and epidemiological properties unlike other infectious organisms. Their essential saprophagic existence prevents coevolution, and no host–parasite virulence trade-off can evolve. However, the host may evolve defenses. Models of pathogens show that sapronoses, lacking a threshold of transmission, cannot regulate host populations, although they can reduce host abundance and even extirpate their hosts. Immunocompromised hosts are relatively susceptible to sapronoses. Some particularly important sapronoses, such as cholera and anthrax, can sustain an epidemic in a host population. However, these microbes ultimately persist as saprophages. One-third of human infectious disease agents are sapronotic, including nearly all fungal diseases. Recognition that an infectious disease is sapronotic illuminates a need for effective environmental control strategies.

Trends in Parasitology

Parasites affect food web structure primarily through increased diversity and complexity

Comparative research on food web structure has revealed generalities in trophic organization, produced simple models, and allowed assessment of robustness to species loss. These studies have mostly focused on free-living species. Recent research has suggested that inclusion of parasites alters structure. We assess whether such changes in network structure result from unique roles and traits of parasites or from changes to diversity and complexity. We analyzed seven highly resolved food webs that include metazoan parasite data. Our analyses show that adding parasites usually increases link density and connectance (simple measures of complexity), particularly when including concomitant links (links from predators to parasites of their prey). However, we clarify prior claims that parasites ‘‘dominate’’ food web links. Although parasites can be involved in a majority of links, in most cases classic predation links outnumber classic parasitism links. Regarding network structure, observed changes in degree distributions, 14 commonly studied metrics, and link probabilities are consistent with scale-dependent changes in structure associated with changes in diversity and complexity. Parasite and free-living species thus have similar effects on these aspects of structure. However, two changes point to unique roles of parasites. First, adding parasites and concomitant links strongly alters the frequency of most motifs of interactions among three taxa, reflecting parasites’ roles as resources for predators of their hosts, driven by trophic intimacy with their hosts. Second, compared to free-living consumers, many parasites’ feeding niches appear broader and less contiguous, which may reflect complex life cycles and small body sizes. This study provides new insights about generic versus unique impacts of parasites on food web structure, extends the generality of food web theory, gives a more rigorous framework for assessing the impact of any species on trophic organization, identifies limitations of current food web models, and provides direction for future structural and dynamical models.

PLoS Biology

New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning

Introduced species can alter the topology of food webs. For instance, an introduction can aid the arrival of free-living consumers using the new species as a resource, while new parasites may also arrive with the introduced species. Food-web responses to species additions can thus be far more complex than anticipated. In a subarctic pelagic food web with free-living and parasitic species, two fish species (arctic charr Salvelinus alpinus and three-spined stickleback Gasterosteus aculeatus ) have known histories as deliberate introductions. The effects of these introductions on the food web were explored by comparing the current pelagic web with a heuristic reconstruction of the pre-introduction web. Extinctions caused by these introductions could not be evaluated by this approach. The introduced fish species have become important hubs in the trophic network, interacting with numerous parasites, predators and prey. In particular, five parasite species and four predatory bird species depend on the two introduced species as obligate trophic resources in the pelagic web and could therefore not have been present in the pre-introduction network. The presence of the two introduced fish species and the arrival of their associated parasites and predators increased biodiversity, mean trophic level, linkage density, and nestedness; altering both the network structure and functioning of the pelagic web. Parasites, in particular trophically transmitted species, had a prominent role in the network alterations that followed the introductions.

Takvatn Lake

The role of spatial and temporal heterogeneity and competition in structuring trematode communities in the great pond snail, Lymnaea stagnalis (L.)

We assessed how spatial and temporal heterogeneity and competition structure larval trematode communities in the pulmonate snail Lymnaea stagnalis . To postulate a dominance hierarchy, mark-release-recapture was used to monitor replacements of trematode species within snails over time. In addition, we sampled the trematode community in snails in different ponds in 3 consecutive years. A total of 7,623 snails (10,382 capture events) was sampled in 7 fishponds in the Jindřichův Hradec and Třeboň areas in South Bohemia (Czech Republic) from August 2006 to October 2008. Overall, 39% of snails were infected by a community of 14 trematode species; 7% of snails were infected with more than 1 trematode species (constituting 16 double- and 4 triple-species combinations). Results of the null-model analyses suggested that spatial heterogeneity in recruitment among ponds isolated trematode species from each other, whereas seasonal pulses in recruitment increased species interactions in some ponds. Competitive exclusion among trematodes led to a rarity of multiple infections compared to null-model expectations. Competitive relationships among trematode species were hypothesized as a dominance hierarchy based on direct evidence of replacement and invasion and on indirect evidence. Seven top dominant species with putatively similar competitive abilities (6 rediae and 1 sporocyst species) reduced the prevalence of the other trematode species developing in sporocysts only.

Journal of Parasitology

A common scaling rule for abundance, energetics, and production of parasitic and free-living species

The metabolic theory of ecology uses the scaling of metabolism with body size and temperature to explain the causes and consequences of species abundance. However, the theory and its empirical tests have never simultaneously examined parasites alongside free-living species. This is unfortunate because parasites represent at least half of species diversity. We show that metabolic scaling theory could not account for the abundance of parasitic or free-living species in three estuarine food webs until accounting for trophic dynamics. Analyses then revealed that the abundance of all species uniformly scaled with body mass to the - 3/4 power. This result indicates "production equivalence," where biomass production within trophic levels is invariant of body size across all species and functional groups: invertebrate or vertebrate, ectothermic or endothermic, and free-living or parasitic.

Science

Ecology of the brain trematode Euhaplorchis californiensis and its host, the California Killifish (Fundulus parvipinnis)

We describe the distribution and abundance of the brain-encysting trematode Euhaplorchis californiensis and its second intermediate host, the California killifish ( Fundulus parvipinnis ), in 3 estuaries in southern California and Baja California. We quantified the density of fish and metacercariae at 13–14 sites per estuary and dissected 375 killifish. Density (numbers and biomass) was examined at 3 spatial scales, i.e., small replicate sites, habitats, and entire estuaries. At those same scales, factors that might influence metacercaria prevalence, abundance, and aggregation in host individuals and populations were also examined. Metacercaria prevalence was 94–100% among the estuaries. Most fish were infected with 100s to 1,000s of E. californiensis metacercariae, with mean abundance generally increasing with host size. Although body condition of fish did not vary among sites or estuaries, the abundance of metacercariae varied significantly among sites, habitats, estuaries, and substantially with host size and gender. Metacercariae were modestly aggregated in killifish ( k > 1), with aggregation decreasing in larger hosts. Across the 3 estuaries, the total populations of killifish ranged from 9,000–12,000 individuals/ha and from 7–43 kg/ha. The component populations of E. californiensis metacercariae ranged from 78–200 million individuals/ha and from 0.1–0.3 kg/ha. Biomass of E. californiensis metacercariae constituted 0.5–1.7% of the killifish biomass in the estuaries. Our findings, in conjunction with previously documented effects of E. californiensis , suggest a strong influence of this parasite on the size, distribution, biomass, and abundance of its killifish host.

Journal of Parasitology

The inverse niche model for food webs with parasites

Although parasites represent an important component of ecosystems, few field and theoretical studies have addressed the structure of parasites in food webs. We evaluate the structure of parasitic links in an extensive salt marsh food web, with a new model distinguishing parasitic links from non-parasitic links among free-living species. The proposed model is an extension of the niche model for food web structure, motivated by the potential role of size (and related metabolic rates) in structuring food webs. The proposed extension captures several properties observed in the data, including patterns of clustering and nestedness, better than does a random model. By relaxing specific assumptions, we demonstrate that two essential elements of the proposed model are the similarity of a parasite's hosts and the increasing degree of parasite specialization, along a one-dimensional niche axis. Thus, inverting one of the basic rules of the original model, the one determining consumers' generality appears critical. Our results support the role of size as one of the organizing principles underlying niche space and food web topology. They also strengthen the evidence for the non-random structure of parasitic links in food webs and open the door to addressing questions concerning the consequences and origins of this structure.

Theoretical Ecology

Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail

A robust food web is one in which few secondary extinctions occur after removing species. We investigated how parasites affected the robustness of the Carpinteria Salt Marsh food web by conducting random species removals and a hypothetical, but plausible, species invasion. Parasites were much more likely than free-living species to suffer secondary extinctions following the removal of a free-living species from the food web. For this reason, the food web was less robust with the inclusion of parasites. Removal of the horn snail, Cerithidea californica , resulted in a disproportionate number of secondary parasite extinctions. The exotic Japanese mud snail, Batillaria attramentaria , is the ecological analogue of the native California horn snail and can completely replace it following invasion. Owing to the similarities between the two snail species, the invasion had no effect on predator–prey interactions. However, because the native snail is host for 17 host-specific parasites, and the invader is host to only one, comparison of a food web that includes parasites showed significant effects of invasion on the native community. The hypothetical invasion also significantly reduced the connectance of the web because the loss of 17 native trematode species eliminated many links.

Philosophical Transactions of the Royal Society B:

Parasitic castration: the evolution and ecology of body snatchers

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.

Trends in Parasitology

Differential escape from parasites by two competing introduced crabs

Although introduced species often interact with one another in their novel communities, the role of parasites in these interactions remains less clear. We examined parasite richness and prevalence in 2 shorecrab species with different invasion histories and residency times in an introduced region where their distributions overlap broadly. On the northeastern coast of the USA, the Asian shorecrab Hemigrapsus sanguineus was discovered 20 yr ago, while the European green crab Carcinus maenas has been established for over 200 yr. We used literature and field surveys to evaluate parasitism in both crabs in their native and introduced ranges. We found only 1 parasite species infecting H. sanguineus on the US East Coast compared to 6 species in its native range, while C. maenas was host to 3 parasite species on the East Coast compared to 10 in its native range. The prevalence of parasite infection was also lower for both crabs in the introduced range compared to their native ranges; however, the difference was almost twice as much for H. sanguineus as for C. maenas. There are several explanations that could contribute to C. maenas' greater parasite diversity than that of H. sanguineus on the US East Coast, including differences in susceptibility, time since introduction, manner of introduction (vector), distance from native range, taxonomic isolation, and the potential for parasite identification bias. Our study underscores not just that non-native species lose parasites upon introduction, but that they may do so differentially, with ramifications for their direct interactions and with potential community-level influences.

Europe;Northeastern Coast Of United States

Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island

We compared parasite communities at two coral atolls in the Line Islands chain of the central Pacific (Kiritimati Island and Palmyra Atoll). Palmyra Atoll is relatively pristine while Kiritimati Island is heavily fished. At each island, we sampled five fish species for helminth and arthropod endoparasites: Chromis margaritifer , Plectroglyphidodon dickii, Paracirrhites arcatus , Acanthurus nigricans , and Lutjanus bohar . The surveys found monogeneans, digeneans, cestodes, nematodes, acanthocephalans, and copepods. Parasite richness was higher at Palmyra compared to Kiritimati for all five fish species. Fishes from Palmyra also tended to have more parasites species per host, higher parasite prevalence, and higher parasite abundance than did fishes from Kiritimati. The lower parasitism at Kiritimati may result from a simplified food web due to over fishing. Low biodiversity could impair parasite transmission by reducing the availability of hosts required by parasites with complex life cycles. Most notably, the lower abundances of larval shark tapeworms at Kiritimati presumably reflect the fact that fishing has greatly depleted sharks there in comparison to Palmyra.

EcoHealth

Homage to Linnaeus: How many parasites? How many hosts?

Estimates of the total number of species that inhabit the Earth have increased significantly since Linnaeus's initial catalog of 20,000 species. The best recent estimates suggest that there are ≈6 million species. More emphasis has been placed on counts of free-living species than on parasitic species. We rectify this by quantifying the numbers and proportion of parasitic species. We estimate that there are between 75,000 and 300,000 helminth species parasitizing the vertebrates. We have no credible way of estimating how many parasitic protozoa, fungi, bacteria, and viruses exist. We estimate that between 3% and 5% of parasitic helminths are threatened with extinction in the next 50 to 100 years. Because patterns of parasite diversity do not clearly map onto patterns of host diversity, we can make very little prediction about geographical patterns of threat to parasites. If the threats reflect those experienced by avian hosts, then we expect climate change to be a major threat to the relatively small proportion of parasite diversity that lives in the polar and temperate regions, whereas habitat destruction will be the major threat to tropical parasite diversity. Recent studies of food webs suggest that ≈75% of the links in food webs involve a parasitic species; these links are vital for regulation of host abundance and potentially for reducing the impact of toxic pollutants. This implies that parasite extinctions may have unforeseen costs that impact the health and abundance of a large number of free-living species.

Proceedings of the National Academy of Sciences of

Diversity increases biomass production for trematode parasites in snails

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.

Proceedings of the Royal Society B: Biological Sci

Ecosystem energetic implications of parasite and free-living biomass in three estuaries

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.

Nature

Parasites in food webs: the ultimate missing links

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food-web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food-web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food-web stability, interaction strength and energy flow. Food-web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food-web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food-web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.

Ecology Letters

An experimental evaluation of host specificity: The role of encounter and compatibility filters for a rhizocephalan parasite of crabs

The encounter/compatibility paradigm of host specificity provides three qualitative pathways to the success or failure of a potential host-parasite interaction. It is usually impossible to distinguish between two of these (encounter and compatibility filters closed versus encounter filter open and compatibility filter closed) because unsuccessful infection attempts are difficult to observe in nature. We were able to open the encounter filter under experimental laboratory conditions. Our analytical system used the rhizocephalan barnacle, Sacculina carcini , a parasitic castrator of the European green crab, Carcinus maenas , and Pachygrapsus marmoratus , a native European crab that occurs with C. maenas but is not parasitized by S. carcini in nature. Penetration followed by unsuccessful infection of P. marmoratus crabs by parasitic barnacle larvae leaves a uniquely permanent record in the thoracic ganglion of the crabs. This provided us with a novel tool to quantify the encounter filter in a host-parasite system in nature. We demonstrated, in the laboratory, that the compatibility filter was closed and that, in nature, even where barnacle larvae were present, the encounter filter was also effectively closed. The closure of both filters in nature explains the failure of this potential host-parasite interaction, an outcome favored by selection in both host and parasite.

International Journal for Parasitology

Endangered light-footed clapper rail affects parasite community structure in coastal wetlands

An extinction necessarily affects community members that have obligate relationships with the extinct species. Indirect or cascading effects can lead to even broader changes at the community or ecosystem level. However, it is not clear whether generalist parasites should be affected by the extinction of one of their hosts. We tested the prediction that loss of a host species could affect the structure of a generalist parasite community by investigating the role of endangered Light-footed Clapper Rails ( Rallus longirostris levipes ) in structuring trematode communities in four tidal wetlands in southern California, USA (Carpinteria Salt Marsh, Mugu Lagoon) and Mexico (Estero de Punta Banda, Bahia Falsa–San Quintín). We used larval trematode parasites in first intermediate host snails ( Cerithidea californica ) as windows into the adult trematodes that parasitize Clapper Rails. Within and among wetlands, we found positive associations between Clapper Rails and four trematode species, particularly in the vegetated marsh habitat where Clapper Rails typically occur. This suggests that further loss of Clapper Rails is likely to affect the abundance of several competitively dominant trematode species in wetlands with California horn snails, with possible indirect effects on the trematode community and changes in the impacts of these parasites on fishes and invertebrates.

Ecological Applications