Linking community assembly and structure across scales in a wild mouse parasite community

Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (Apodemus sylvaticus) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales.     

Stream community richness predicts apex predator occupancy dynamics in riparian systems

Streams and adjacent riparian habitats represent linked terrestrial and aquatic ecosystems that exchange materials and energy. Recognized relationships among apex predators and ecosystem biodiversity led us to hypothesize that these predators in riparian‐stream systems were more likely to be found in sites with high stream quality, defined as increased ecosystem function and integrity. In our freshwater study system, river otter Lontra canadensis and mink Neovison vison play critical roles as apex predators. We used multi‐season occupancy modelling across three sampling years (2012–2014) to compare aspects of the stream communities that explain occupancy dynamics of river otter and mink, including their interactions with other semi‐aquatic mammals. We surveyed for semi‐aquatic mammals at 77 sites in 12 major watersheds in southern Illinois, USA (44 526 km²). Naïve occupancy differed among years but generally increased for river otter, and remained high (≥93.5%) for mink. Increasing substrate availability increased detectability of river otter, whereas mink detection varied by survey period. Occupancy of river otter during the initial survey period was higher in sites closer to reintroduction points. Probability of colonization of river otter was positively associated with macroinvertebrate index of biotic integrity, fish species richness, and beaver presence. Sites with high species richness of fish families preferred by river otter also had increased river otter persistence. Mink occupied sites with increased fish richness, muskrat presence and mussel community index. Taken together, our results show occupancy of both mink and river otter were predicted by aspects of prey diversity and presence, indicating the importance of community composition in occupancy dynamics of riparian predators. Ultimately, these relationships suggest that habitat heterogeneity and system stability are important to apex predator site use. However, the relative role of bottom–up and top–down forcing in stream systems remains to be resolved.     

Host–parasite interactions and competition between tubificid species in a benthic community

1. Parasites can be important determinants of host community structure while host community structure can influence the success of parasites, although both are often overlooked. In two laboratory experiments, we examined interactions among Myxobolus cerebralis syn Myxosoma cerebralis Höfer, the myxozoan parasite that causes salmonid whirling disease, and two coexisting tubificid species: Tubifex tubifex (Müller), which is the alternate host of the parasite, and Limnodrilus hoffmeisteri Claparède, which is not susceptible. In the first experiment, we examined T. tubifex infection prevalence when exposed to nine doses of spores. In the second experiment, we examined tubificid and parasite success under three spore doses when tubificids were combined in a response surface experimental design used to detect interactions among species. 2. The outcomes of interactions between tubificid species were complex. The number and biomass of offspring of both tubificid species were density dependent when in monoculture or in combination with the other species. Adult growth of T. tubifex was also density dependent in monoculture, but when L. hoffmeisteri replaced one‐half of the T. tubifex in the high‐density treatment, adult growth of T. tubifex was higher than in monoculture. Adult growth of L. hoffmeisteri was always density independent. Whether T. tubifex was exposed to the parasite or not did not change the outcome of these interactions. However, adult growth of T. tubifex, but not L. hoffmeisteri, was highest when M. cerebralis was present. 3. Infection prevalence of T. tubifex increased with increasing spore dose. Infection prevalence was lowest in the high‐density T. tubifex monoculture and highest in the low‐density T. tubifex monoculture and when T. tubifex was in combination with L. hoffmeisteri. 4. Both intraspecific and interspecific competition influenced tubificid success, but T. tubifex gained some competitive advantage through increased adult growth when in combination with L. hoffmeisteri. Whether T. tubifex was exposed to the parasite or not did not change the outcome of the interactions between the tubificid species. 5. The presence of L. hoffmeisteri did not decrease the prevalence of infection in T. tubifex, suggesting that parasite success was unaltered by the presence of this non‐susceptible species.     

Is a community still a community? Reviewing definitions of key terms in community ecology

Community ecology is an inherently complicated field, confounded by the conflicting use of fundamental terms. Nearly two decades ago, Fauth et al. (1996) demonstrated that imprecise language led to the virtual synonymy of important terms and so attempted to clearly define four keywords in community ecology; “community,” “assemblage,” “guild,” and “ensemble”. We revisit Fauth et al.'s conclusion and discuss how the use of these terms has changed over time since their review. An updated analysis of term definition from a selection of popular ecological textbooks suggests that definitions have drifted away from those encountered pre‐1996, and slightly disagreed with results from a survey of 100 ecology professionals (comprising of academic professors, nonacademic PhDs, graduate and undergraduate biology students). Results suggest that confusion about these terms is still widespread in ecology. We conclude with clear suggestions for definitions of each term to be adopted hereafter to provide greater cohesion among research groups.     

Ecological versus phylogenetic determinants of helminth parasite community richness

Summary We examine patterns of community richness among intestinal parasitic helminth communities in fishes, herptiles, birds and mammals with respect to the comparative number of component species in a host population. We show that terrestrial hosts have, on average, fewer component species than aquatic hosts. We also show that the mean number of component species in aquatic hosts increases from fishes through herptiles to birds before declining slightly in mammals. For terrestrial hosts, the mean number of component species increases from herptiles, through birds, reaching a maximum in mammals. We conclude that: (i) habitat of the host is more important in determining community richness than is host phylogeny; (ii) the phenomenon of host capture may be largely responsible for increased species richness in some host groups; (iii) aquatic birds harbour the richest intestinal helminth communities; and (iv) as we interpret them, our data refute the time hypothesis, which would predict that fishes as the oldest lifestyle should have the richest helminth communities.Order of authorship determined by random draw and does not imply seniority.     

Bacterial community in the rhizosphere and rhizoplane of wild type and transgenic eucalyptus

The rhizosphere is a niche exploited by a wide variety of bacteria. The expression of heterologous genes by plants might become a factor affecting the structure of bacterial communities in the rhizosphere. In a greenhouse experiment, the bacterial community associated to transgenic eucalyptus, carrying the Lhcb1-2 genes from pea (responsible for a higher photosynthetic capacity), was evaluated. The culturable bacterial community associated to transgenic and wild type plants were not different in density, and the Amplified Ribosomal DNA Restriction Analysis (ARDRA) typing of 124 strains revealed dominant ribotypes representing the bacterial orders Burkholderiales, Rhizobiales, and Actinomycetales, the families Xanthomonadaceae, and Bacillaceae, and the genus Mycobacterium. Principal Component Analysis based on the fingerprints obtained by culture-independent Denaturing Gradient Gel Electrophoresis analysis revealed that Alphaproteobacteria, Betaproteobacteria and Actinobacteria communities responded differently to plant genotypes. Similar effects for the cultivation of transgenic eucalyptus to those observed when two genotype-distinct wild type plants are compared.     

Within-host competitive interactions as a mechanism for the maintenance of parasite diversity

Variation among parasite strains can affect the progression of disease or the effectiveness of treatment. What maintains parasite diversity? Here I argue that competition among parasites within the host is a major cause of variation among parasites. The competitive environment within the host can vary depending on the parasite genotypes present. For example, parasite strategies that target specific competitors, such as bacteriocins, are dependent on the presence and susceptibility of those competitors for success. Accordingly, which parasite traits are favoured by within-host selection can vary from host to host. Given the fluctuating fitness landscape across hosts, genotype by genotype (G×G) interactions among parasites should be prevalent. Moreover, selection should vary in a frequency-dependent manner, as attacking genotypes select for resistance and genotypes producing public goods select for cheaters. I review competitive coexistence theory with regard to parasites and highlight a few key examples where within-host competition promotes diversity. Finally, I discuss how within-host competition affects host health and our ability to successfully treat infectious diseases.     

Evidence for host variation in parasite tolerance in a wild fish population

Hosts can protect themselves against parasites by actively reducing parasites burden (i.e. resistance) or by limiting the damages caused by parasites (i.e. tolerance). Disentangling between tolerance and resistance is important for predicting the evolutionary outcomes of host-parasite interaction. Dace (Leuciscus leuciscus) are often parasitized by the ectoparasite Tracheliastes polycolpus which feeds on (and destroys) fins, reducing thus the host’s condition. We tested the hypothesis that genetically-based variation in ectoparasite tolerance exists in a wild dace population. We found that moderately heterozygous dace, which are less resistant than highly heterozygous or homozygous dace, tolerated better the effect imposed by T. polycolpus for a given parasite burden. However, tolerance also varied upon environmental conditions, suggesting that genetic and environmentally-based variation exists for both resistance and tolerance in this natural host-parasite system. Moreover, a negative genetic correlation may exist between tolerance and resistance, and hence several evolutionary outcomes are possible in this interacting system.     

All hosts are not equal: explaining differential patterns of malformations in an amphibian community

1. Within a community, different host species often exhibit broad variation in sensitivity to infection and disease. Because such differences can influence the strength and outcome of community interactions, it is essential to understand differential disease patterns and identify the mechanisms responsible. 2. In North American wetlands, amphibian species often exhibit extraordinary differences in the frequency of limb malformations induced by the digenetic trematode, Ribeiroia ondatrae. By coupling field studies with parasite exposure experiments, we evaluated whether such patterns were due to differences in (i) parasite encounter rate, (ii) infection establishment, or (iii) parasite persistence within hosts. 3. Field results underscored the broad variation in malformations and infection between host species; while nearly 60% (n = 618) of emerging American toads exhibited severe limb deformities such as bony triangles, skin webbings and missing limbs, fewer than 4% (n = 251) of Eastern gray treefrogs from the same pond were abnormal. Despite similarities in the phenology and larval development period of these species, they differed sharply in Ribeiroia infection. On average, toads supported 75x more metacercariae than did metamorphic treefrogs. 4. Experimental exposures of larval toads and treefrogs to a realistic range of Ribeiroia cercariae revealed strong differences in the sensitivity of these species to infection; exposed toads suffered elevated mortality (up to 95%), delayed metamorphosis, and severe limb malformations consistent with field observations. Treefrogs, in contrast, exhibited limited mortality and no malformations, regardless of exposure level. Ribeiroia cercariae were substantially less successful in locating and infecting Hyla versicolor larvae. 5. Our results indicate that the observed differences in infection and malformations owe to a lower ability of Ribeiroia cercariae to both find and establish within larval treefrogs, possibly stemming from a heightened immune response to infection. Because Ribeiroia is a highly pathogenic parasite with negative effects on larval and metamorphic amphibian survival, variation in infection resistance among species could have important implications for understanding patterns of species co-occurrence, competition, and community diversity.     

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free‐living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host–parasite–predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.     

Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays)

The focus of many fungal endophyte studies has been how plants benefit from endophyte infection. Few studies have investigated the role of the host plant as an environment in shaping endophyte community diversity and composition. The effects that different attributes of the host plant, that is, host genetic variation, host variation in resistance to the fungal pathogen Ustilago maydis and U. maydis infection, have on the fungal endophyte communities in maize (Zea mays) was examined. The internal transcribed spacer (ITS) region of the rDNA was sequenced to identify fungi and the endophyte communities were compared in six maize lines that varied in their resistance to U. maydis. It was found that host genetic variation, as determined by maize line, had significant effects on species richness, while the interactions between line and U. maydis infection and line and field plot had significant effects on endophyte community composition. However, the effects of maize line were not dependent on whether lines were resistant or susceptible to U. maydis. Almost 3000 clones obtained from 58 plants were sequenced to characterize the maize endophyte community. These results suggest that the endophyte community is shaped by complex interactions and factors, such as inoculum pool and microclimate, may be important.     

Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats

Climate change and climate-driven increases in infectious disease threaten wildlife populations globally. Gut microbial responses are predicted to either buffer or exacerbate the negative impacts of these twin pressures on host populations. However, examples that document how gut microbial communities respond to long-term shifts in climate and associated disease risk, and the consequences for host survival, are rare. Over the past two decades, wild meerkats inhabiting the Kalahari have experienced rapidly rising temperatures, which is linked to the spread of tuberculosis (TB). We show that over the same period, the faecal microbiota of this population has become enriched in Bacteroidia and impoverished in lactic acid bacteria (LAB), a group of bacteria including Lactococcus and Lactobacillus that are considered gut mutualists. These shifts occurred within individuals yet were compounded over generations, and were better explained by mean maximum temperatures than mean rainfall over the previous year. Enriched Bacteroidia were additionally associated with TB exposure and disease, the dry season and poorer body condition, factors that were all directly linked to reduced future survival. Lastly, abundances of LAB taxa were independently and positively linked to future survival, while enriched taxa did not predict survival. Together, these results point towards extreme temperatures driving an expansion of a disease-associated pathobiome and loss of beneficial taxa. Our study provides the first evidence from a longitudinally sampled population that climate change is restructuring wildlife gut microbiota, and that these changes may amplify the negative impacts of climate change through the loss of gut mutualists. While the plastic response of host-associated microbiotas is key for host adaptation under normal environmental fluctuations, extreme temperature increases might lead to a breakdown of coevolved host–mutualist relationships.     

The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment

While avian chronic haemoparasite infections induce reproductive costs, infection has not previously been shown to affect survival. Here, we experimentally reduced, through medication, the intensity of infection by Haemoproteus parasites in wild-breeding female blue tits Cyanistes caeruleus. However, this treatment did not reduce the intensity of infection in males or the intensity of infection by Leucocytozoon. Medicated females, but not males, showed increased local survival until the next breeding season compared with control birds. To our knowledge, this is the first empirical evidence showing long-term direct survival costs of chronic Haemoproteus infections in wild birds.     

Palaeontology., adaptation and community ecology: A response to Walter and Pater son (1994)

Abstract This paper challenges Walter and Paterson's (1994) assertion that the community concept ought to be abandoned because of recent palaeontological evidence pointing to the ‘individualistic’ nature of biological communities. The ‘individualistic’ versus ‘superorganismic’ community concepts might provide good grist for the philosophical mill, but have little practical relevance to contemporary community ecology. Ecologists define communities in terms of current species distributions and interactions, and seek to integrate the roles of both biotic and abiotic factors influencing species distributions. There is no assumption of tight co-evolution among component species; Walter and Paterson confuse ‘organization’ with ‘co-adaptation’. Nor, contrary to the authors’ claims, is there an implicit assumption that all community patterns are caused by competition. For most ecologists, the ‘competition debate’ ended a decade ago. Walter and Paterson's view that competition is rarely, if ever, important in structuring communities is not even held by the main protaganists of the ‘competition is not so important’ school of the 1980s, and is in direct contradiction of the extensive, more recent literature on the subject. It entirely ignores plant ecology. Many of Walter and Paterson's misunderstandings appear to arise from the false premise that explanation of adaptation should be the ultimate goal of any ecological discipline. The authors are hostile to community ecology because, if communities are individualistic, then little light can be shed on species adaptations. Fortunately, most ecologists are not so preoccupied with adaptation.     

Eutrophication,biodiversity loss,and species invasions modify the relationship between host and parasite richness during host community assembly

Host and parasite richness are generally positively correlated, but the stability of this relationship in response to global change remains poorly understood. Rapidly changing biotic and abiotic conditions can alter host community assembly, which in turn, can alter parasite transmission. Consequently, if the relationship between host and parasite richness is sensitive to parasite transmission, then changes in host composition under various global change scenarios could strengthen or weaken the relationship between host and parasite richness. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness in response to global change, we experimentally crossed host diversity (biodiversity loss) and resource supply to hosts (eutrophication), then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post‐assembly host species richness, richness‐independent host phylogenetic diversity, and colonization by exotic host species. Overall, host richness predicted parasite richness, and as predicted, this effect was moderated by exotic abundance—communities dominated by exotic species exhibited a stronger positive relationship between post‐assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness. These results thus provide a novel mechanism to explain how global environmental change can generate contingencies in a fundamental ecological relationship—the positive relationship between host and parasite richness.     

Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes

Geographical isolation, habitat variation and trophic specialization have contributed to a large extent to the astonishing diversity of cichlid fishes in the Great East African lakes. Because parasite communities often vary across space and environments, parasites can accompany and potentially enhance cichlid species diversification. However, host dispersal may reduce opportunities for parasite‐driven evolution by homogenizing parasite communities and allele frequencies of immunity genes. To test for the relationships between parasite community variation, host dispersal and parasite‐induced host evolution, we studied two sympatric cichlid species with contrasting dispersal capacities along the shores of southern Lake Tanganyika. Whereas the philopatric Tropheus moorii evolved into several genetically differentiated colour morphs, Simochromis diagramma is phenotypically rather uniform across its distribution range and shows only weak population structure. Populations of both species were infected with divergent parasite communities and harbour differentiated variant pools of an important set of immune genes, the major histocompatibility complex (MHC). The overall extent of geographical variation of parasites and MHC genes was similar between host species. This indicates that immunogenetic divergence among populations of Lake Tanganyika cichlids can occur even in species that are strongly dispersing. However, because this also includes species that are phenotypically uniform, parasite‐induced evolution may not represent a key factor underlying species diversification in this system.     

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro‐ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga‐Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Mycorrhizas transfer carbon in a mature mixed forest

Mycorrhizal fungi transfer nutrients to plants in exchange for photosynthates. Plants allocate up to 20% of their carbon to mycorrhizal structures, mycelium and fruit bodies of their fungal partners. Individuals of mycorrhizal fungi may encompass hundreds of square metres of soil and defragmented litter, linking multiple plant individuals of different species and size (Figure 1). Using a free‐air ¹³CO₂ enrichment (web‐FACE) technique in a mature forest, interspecific transfer accounted for 40% of fine root carbon after 5 years of back and forth transfer between trees. In this issue of Molecular Ecology, Rog, Rosenstock, Körner, and Klein (2020) show that closely related trees shared relatively more mycorrhizal fungi than distantly related trees in the same experimental site, which correlated to increased carbon sharing.