Host centrality in food web networks determines parasite diversity

Background

Parasites significantly alter topological metrics describing food web structure, yet few studies have explored the relationship between food web topology and parasite diversity.

Methods/Principal Findings

This study uses quantitative metrics describing network structure to investigate the relationship between the topology of the host food web and parasite diversity. Food webs were constructed for four restored brackish marshes that vary in species diversity, time post restoration and levels of parasitism. Our results show that the topology of the food web in each brackish marsh is highly nested, with clusters of generalists forming a distinct modular structure. The most consistent predictors of parasite diversity within a host were: trophic generality, and eigenvector centrality. These metrics indicate that parasites preferentially colonise host species that are highly connected, and within modules of tightly interacting species in the food web network.

Conclusions/Significance

These results suggest that highly connected free-living species within the food web may represent stable trophic relationships that allow for the persistence of complex parasite life cycles. Our data demonstrate that the structure of host food webs can have a significant effect on the establishment of parasites, and on the potential for evolution of complex parasite life cycles.     

Parasites: Small Players with Crucial Roles in the Ecological Theater

Effective management of our natural resources requires an understanding of ecosystem structure and function; effectively, an ecosystem-based approach to management. Parasites occur, albeit cryptically, in almost all ecosystems, yet they are usually neglected in studies on populations and communties of organisms. Parasites can have pronounced or subtle effects on hosts affecting host behavior, growth, fecundity, and mortality. Furthermore, parasites may regulate host population dynamics and influence community structure. Many parasites have complex life cycles and depend for transmission on the presence of a variety of invertebrate and vertebrate intermediate hosts. Often transmission involves predator–prey interactions. Thus, parasites reflect the hosts position in the food web and are indicative of changes in ecosystem structure and function. Parasites can provide information on population structure, evolutionary hypotheses, environmental stressors, trophic interactions, biodiversity, and climatic conditions. I use examples from diverse freshwater and marine systems to demonstrate that parasites should be incorporated into research and monitoring programs to maximize information gathered in ecosystem-based studies and resource management.Supplementary Tables 3, 4, 5, 6 and additional references for this article are available for viewing by subscribers only at     

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.     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Resource tracking in marine parasites: going with the flow?

Understanding how diversity interacts with energy supply is of broad ecological interest. Most studies to date have investigated patterns within trophic levels, reflecting a lack of food webs which include information on energy flow. We added parasites to a published marine energy‐flow food web, to explore whether parasite diversity is correlated with energy flow to host taxa. Parasite diversity was high with 36 parasite taxa affecting 40 of the 51 animal taxa. Adding parasites increased the number of trophic links per species, trophic link strength, connectance, and food chain lengths. There was evidence of an asymptotic relationship between energy flowing through a food chain and parasite diversity, although there were clear outliers. High parasite diversity was associated with host taxa which were highly connected within the food web. This suggests that energy flow through a taxon may favour parasite diversity, up to a maximal value. The evolutionary and energetic basis for that limitation is of key interest in understanding the basis for parasite diversity in natural food webs and thus their role in food web dynamics.     

Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission

While the recent inclusion of parasites into food‐web studies has highlighted the role of parasites as consumers, there is accumulating evidence that parasites can also serve as prey for predators. Here we investigated empirical patterns of predation on parasites and their relationships with parasite transmission in eight topological food webs representing marine and freshwater ecosystems. Within each food web, we examined links in the typical predator–prey sub web as well as the predator–parasite sub web, i.e. the quadrant of the food web indicating which predators eat parasites. Most predator– parasite links represented ‘concomitant predation’ (consumption and death of a parasite along with the prey/host; 58–72%), followed by ‘trophic transmission’ (predator feeds on infected prey and becomes infected; 8–32%) and predation on free‐living parasite life‐cycle stages (4–30%). Parasite life‐cycle stages had, on average, between 4.2 and 14.2 predators. Among the food webs, as predator richness increased, the number of links exploited by trophically transmitted parasites increased at about the same rate as did the number of links where these stages serve as prey. On the whole, our analyses suggest that predation on parasites has important consequences for both predators and parasites, and food web structure. Because our analysis is solely based on topological webs, determining the strength of these interactions is a promising avenue for future research.     

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.     

Integrating ecosystem engineering and food webs

Ecosystem engineering, the physical modification of the environment by organisms, is a common and often influential process whose significance to food web structure and dynamics is largely unknown. In the light of recent calls to expand food web studies to include non‐trophic interactions, we explore how we might best integrate ecosystem engineering and food webs. We provide rationales justifying their integration and present a provisional framework identifying how ecosystem engineering can affect the nodes and links of food webs and overall organization; how trophic interactions with the engineer can affect the engineering; and how feedbacks between engineering and trophic interactions can affect food web structure and dynamics. We use a simple integrative food chain model to illustrate how feedbacks between the engineer and the food web can alter 1) engineering effects on food web dynamics, and 2) food web responses to extrinsic environmental perturbations. We identify four general challenges to integration that we argue can readily be met, and call for studies that can achieve this integration and help pave the way to a more general understanding of interaction webs in nature. Synthesis All species are affected by their physical environment. Because ecosystem engineering species modify the physical environment and belong to food webs, such species are potentially one of the most important bridges between the trophic and non‐trophic. We examine how to integrate the so far, largely independent research areas of ecosystem engineering and food webs. We present a conceptual framework for understanding how engineering can affect food webs and vice versa, and how feedbacks between the two alter ecosystem dynamics. With appropriate empirical studies and models, integration is achievable, paving the way to a more general understanding of interaction webs in nature.     

Emergence of non-random structure in local food webs generated from randomly structured regional webs

Previous studies have shown that high-resolution, empirical food webs possess a non-random network structure, typically characterized by uniform or exponential degree distributions. However, the empirical food webs that have been investigated for their structural properties represent local communities that are only a subset of a larger pool of regionally coexisting species. Here, we use a simple model to investigate the effects of regional food web structure on local food webs that are assembled by two simple processes: random immigration of species from a source web (regional food web), and random extinction of species within the local web. The model shows that local webs with non-random degree distributions can arise from randomly structured source webs. A comparison of local webs assembled from randomly structured source webs with local webs assembled from source webs generated by the niche model shows that the former have higher species richness at equilibrium, but have a nonlinear response to changing extinction rates. These results imply that the network structure of regional food webs can play a significant role in the assembly and dynamics of local webs in natural ecosystems. With natural landscapes becoming increasingly fragmented, understanding such structure may be a necessary key to understanding the maintenance and stability of local species diversity.     

Disease-induced stabilization of predator-prey oscillations

Parasites are an integral part of virtually all food webs and species communities. Here we consider the invasion of a resident predator-prey system by an infectious disease with frequency-dependent transmission spreading within the predator population. We derive biologically plausible and insightful quantities (demographic and epizootiological reproduction numbers) that allow us to completely determine community composition. Successful disease invasion can have two contrary effects in driving its host population to extinction or in stabilizing predator-prey cycles. Our findings contradict predictions from previous models suggesting a destabilizing effect of parasites. We show that predator infection counteracts the paradox of enrichment. In turn, parasite removal from food webs can have catastrophic effects. We discuss the implications for biological control and resource management on more than one trophic level.     

Connectance and parasite diet breadth in flea-mammal webs

The number of links in webs of species interactions, which lies at the heart of the biodiversity-stability debate, has given rise to controversy during the last 20 yr. Studies exploring these web properties have mainly focused on symmetric webs where each species can potentially feed on any other species; asymmetric webs such as host-parasite webs, where one set of species feed on another set of species, have been overlooked. However, food webs are incomplete without parasites and the study of parasite-host sub-web properties deserves attention. Here, using a large database involving 33 regional interaction webs between mammals and their flea parasites, we found a negative relationship between species richness and host-parasite connectance. We suggest that some phylogenetic constraints on flea diet may explain our observed patterns because we found that parasite diet breadth, measured as host taxonomic diversity, was invariant along our host richness gradient. We found that the slope of the logarithmic relationship between the number of realized links and species richness is lower than slope values reported for food webs. We suggest that connectance may not respond to increasing species richness as rapidly in host-parasite webs as in predator-prey food webs due to stronger coevolutionary requirements.     

Sea lice escape predation on their host

Parasites seldom have predators but often fall victim to those of their hosts. How parasites respond to host predation can have important consequences for both hosts and parasites, though empirical investigations are rare. The exposure of wild juvenile salmon to sea lice (Lepeophtheirus salmonis) from salmon farms allowed us to study a novel ecological interaction: the response of sea lice to predation on their juvenile pink and chum salmon hosts by two salmonid predators-coho smolts and cut-throat trout. In approximately 70% of trials in which a predator consumed a parasitized prey, lice escaped predation by swimming or moving directly onto the predator. This trophic transmission is strongly male biased, probably because behaviour and morphology constrain female movement and transmission. These findings highlight the potential for sea lice to be transmitted up marine food webs in areas of intensive salmon aquaculture, with implications for louse population dynamics and predatory salmonid health.     

Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay

Parasites that are transmitted through predator–prey interactions may be used as indicators of trophic relationships between organisms. Yet, they are rarely used as such in the construction of topological (predator–prey) food webs. We constructed food webs of vertebrate trophic interactions using observed diet alone, trophically transmitted parasites alone, and the combination of the two based on data from 31 species of fish from the Bothnian Bay, Finland. The fish food web contained 530 links derived from observed diet, 724 links inferred from parasitism, and 1,058 links calculated from a combination of both stomach contents and parasites. This sub-web constructed from stomach contents had a mean of 17.1 links per fish species, while that using parasites had 23.4 links per fish. Combining the two diet indicators yielded 34.1 links per fish species, illustrating the complementarity of the two methods. Mean number of prey species per fish species was 12.5 using observed diet items, 15.8 using parasites, and 24.5 using both measures together. Mean number of predators per fish species was 7.4 using observed diet, 11.7 using parasites and 15.0 using both. A positive correlation was found between the mean number of parasites and the number of prey taxa in the diet among the fishes. Omnivorous fish had the highest diversity of both parasite species and prey items, while benthophagous fish had among the lowest. Mean total abundance and mean total prevalence of parasites correlated positively with fish size, with piscivores being the largest with the highest abundance and prevalence, while planktivores and benthivores had the lowest. Trophically transmitted parasites may be used to help construct vertebrate sub-webs and derive information about food web processes. Parasites alone provided equivalent if not more information than observed diet. However, resolution is improved by using parasites and observed diet together.     

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.     

Predicting food‐web structure with metacommunity models

Synthesis Metacommunity theory aims to elucidate the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity research has focused largely on assemblages of competing organisms within a single trophic level. Here, we test the ability of metacommunity models to predict the network structure of the aquatic food web found in the leaves of the northern pitcher plant Sarracenia purpurea. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions play an important role in structuring Sarracenia food webs. Our approach can be applied to any well‐resolved food web for which data are available from multiple locations. The metacommunity framework explores the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity models and empirical studies have focused mostly on assemblages of competing organisms within a single trophic level. Studies of multi‐trophic metacommunities are predominantly restricted to simplified trophic motifs and rarely consider entire food webs. We tested the ability of the patch‐dynamics, species‐sorting, mass‐effects, and neutral metacommunity models, as well as three hybrid models, to reproduce empirical patterns of food web structure and composition in the complex aquatic food web found in the northern pitcher plant Sarracenia purpurea. We used empirical data to determine regional species pools and estimate dispersal probabilities, simulated local food‐web dynamics, dispersed species from regional pools into local food webs at rates based on the assumptions of each metacommunity model, and tested their relative fits to empirical data on food‐web structure. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions were important in structuring Sarracenia food webs. However, differences in dispersal abilities were also important in models that accurately reproduced empirical food web properties. Although the models were tested using pitcher‐plant food webs, the approach we have developed can be applied to any well‐resolved food web for which data are available from multiple locations.     

Biodiversity loss decreases parasite diversity: theory and patterns

Past models have suggested host-parasite coextinction could lead to linear, or concave down relationships between free-living species richness and parasite richness. I explored several models for the relationship between parasite richness and biodiversity loss. Life cycle complexity, low generality of parasites and sensitivity of hosts reduced the robustness of parasite species to the loss of free-living species diversity. Food-web complexity and the ordering of extinctions altered these relationships in unpredictable ways. Each disassembly of a food web resulted in a unique relationship between parasite richness and the richness of free-living species, because the extinction trajectory of parasites was sensitive to the order of extinctions of free-living species. However, the average of many disassemblies tended to approximate an analytical model. Parasites of specialist hosts and hosts higher on food chains were more likely to go extinct in food-web models. Furthermore, correlated extinctions between hosts and parasites (e.g. if parasites share a host with a specialist predator) led to steeper declines in parasite richness with biodiversity loss. In empirical food webs with random removals of free-living species, the relationship between free-living species richness and parasite richness was, on average, quasi-linear, suggesting biodiversity loss reduces parasite diversity more than previously thought.     

Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant

Parasites and hosts live in communities consisting of many interacting species, but few studies have examined how communities affect parasite virulence and transmission. We studied a food web consisting of two species of milkweed, two milkweed herbivores (monarch butterfly and oleander aphid) and a monarch butterfly-specific parasite. We found that the presence of aphids increased the virulence and transmission potential of the monarch butterfly's parasite on one milkweed species. These increases were associated with aphid-induced decreases in the defensive chemicals of milkweed plants. Our experiment suggests that aphids can indirectly increase the virulence and transmission potential of monarch butterfly parasites, probably by altering the chemical composition of a shared food plant. These results indicate that species that are far removed from host-parasite interactions can alter such interactions through cascading indirect effects in the food web. As such, indirect effects within ecological communities may drive the dynamics and evolution of parasites.