Forest species diversity reduces disease risk in a generalist plant pathogen invasion

Empirical evidence suggests that biodiversity loss can increase disease transmission, yet our understanding of the 'diversity-disease hypothesis' for generalist pathogens in natural ecosystems is limited. We used a landscape epidemiological approach to examine two scenarios regarding diversity effects on the emerging plant pathogen Phytophthora ramorum across a broad, heterogeneous ecoregion: (1) an amplification effect exists where disease risk is greater in areas with higher plant diversity due to the pathogen's wide host range, or (2) a dilution effect where risk is reduced with increasing diversity due to lower competency of alternative hosts. We found evidence for pathogen dilution, whereby disease risk was lower in sites with higher species diversity, after accounting for potentially confounding effects of host density and landscape heterogeneity. Our results suggest that although nearly all plants in the ecosystem are hosts, alternative hosts may dilute disease transmission by competent hosts, thereby buffering forest health from infectious disease.     

Local host-tick coextinction in neotropical forest fragments

Ticks are obligatory parasites with complex life cycles that often depend on larger bodied vertebrates as final hosts. These traits make them particularly sensitive to local coextinction with their host. Loss of wildlife abundance and diversity should thus lead to loss of tick abundance and diversity to the point where only generalist tick species remain. However, direct empirical tests of these hypotheses are lacking, despite their relevance to our understanding of tick-borne disease emergence in disturbed environments. Here, we compare vertebrate and tick communities across 12 forest islands and peninsulas in the Panama Canal that ranged 1000-fold in size (2.6–2811.3?ha). We used drag sampling and camera trapping to directly assess the abundance and diversity of communities of questing ticks and vertebrate hosts. We found that the abundance and species richness of ticks were positively related to those of wildlife. Specialist tick species were only present in fragments where their final hosts were found. Further, less diverse tick communities had a higher relative abundance of the generalist tick species Amblyomma oblongoguttatum, a potential vector of spotted fever group rickettsiosis. These findings support the host-parasite coextinction hypothesis, and indicate that loss of wildlife can indeed have cascading effects on tick communities. Our results also imply that opportunities for pathogen transmission via generalist ticks may be higher in habitats with degraded tick communities. If these patterns are general, then tick identities and abundances serve as useful bioindicators of ecosystem health, with low tick diversity reflecting low wildlife diversity and a potentially elevated risk of interspecific disease transmission via remaining host species and generalist ticks.     

Ability of a Generalist Seed Beetle to Colonize an Exotic Host: Effects of Host Plant Origin and Oviposition Host

The colonization of an exotic species by native herbivores is more likely to occur if that herbivore is a generalist. There is little information on the life-history mechanisms used by native generalist insects to colonize exotic hosts and how these mechanisms are affected by host properties. We examined the ability of the generalist seed beetle Stator limbatus Horn to colonize an exotic species. We compared its host preference, acceptability, performance, and egg size when ovipositing and developing on two native (Pithecellobium dulce (Roxb.) Benth and Senegalia riparia (Kunth)) and one exotic legume species (Leucaena leucocephala (Lam.)). We also analyzed the seed chemistry. We found that females recognize the exotic species as an unfavorable host for larval development and that they delayed oviposition and laid fewer and larger eggs on the exotic species than on the native species. Survivorship on the exotic host was 0%. Additionally, seeds of the native species contain five chemical compounds that are absent in the exotic species, and the exotic species contains three sterols, which are absent in the native legumes. Genetically based differences between beetles adapted to different hosts, plastic responses toward new hosts, and chemical differences among seeds are important in host colonization and recognition of the exotic host. In conclusion, the generalist nature of S. limbatus does not influence its ability to colonize L. leucocephala. Explanations for the colonization of exotic hosts by generalist native species and for the success of invasive species must be complemented with studies measuring local adaptation and plasticity.     

An approach to bioassess pelagic ciliate biodiversity at different taxonomic resolutions in response to various habitats in the Amundsen Sea (Antarctica)

The rapid melting of glaciers and loss of sea ice will result in changes in habitat conditions that may drive substantial changes in biodiversity. In order to bioassess the changing polar ecosystem and evaluate biological conservation, pelagic ciliate communities at different taxonomic resolutions were studied at five habitats in the Amundsen Sea during the austral summer from December 2010 to January 2011. Distinctive spatial patterns were observed in the communities among the five habitats (oceanic areas, transitional areas, polynyas, edges of glaciers, and edges of sea ice) in response to environmental variability (e.g., temperature, salinity, chlorophyll a, and nutrients). The distributions in the numbers of different taxonomic levels and of three biodiversity indices (Shannon-Wiener H′, Pielou’s J′, and Margalef D) also revealed clear spatial variability with the maximum mean species number and indices in the polynya and maximum genus and family numbers in the transitional area. The presence/absence of data at taxonomic resolutions up to the family level provided sufficient information to evaluate the ecological patterns of pelagic ciliate communities and could accurately reflect habitat variations. The k-dominance curves illustrated clearly that maximum diversity was presented in the polynya at the species level and in the transitional area at the genus and family level. We suggest that the diversity at higher taxonomic resolutions should be considered more in future monitoring. Our findings provide basic data and an approach toward answering important questions about biological conservation, especially the biodiversity at various taxonomic resolutions in response to the increasing climate changes in polar ecosystems.     

Helminth parasite assemblages in two cyprinids with different life history strategies

Parasitic organisms can affect ecosystems by driving population dynamics of the hosts and influencing community interactions. The life history of the host can determine the relationship with its parasites. Reproductive effort and age of the host are two life history aspects often used to explain parasitic infection. In this study, we examined helminth parasite assemblages in two cyprinids with contrasting reproductive strategies, Cyprinella venusta (crevice spawners) and Notropis volucellus (broadcast spawners), in the Paluxy River (Texas) from May 2014 through October 2015. Host reproduction was measured using the gonadosomatic index, and standard length was used as an estimate of age. Parasite infection was measured using total number of helminths, parasite richness, Shannon’s diversity, and Simpson’s diversity. Our results revealed significant differences in parasite number and diversity between the two species, but not between males and females within species. Additionally, our results showed that standard length was a better predictor of parasitic infection than the gonadosomatic index. The relationship between host size and parasitic infection was expected; however, the lack of a relationship between gonadosomatic indices and parasitic infection was surprising. In conclusion, standard length was a better predictor of parasitic infection than the gonadosomatic index, and as such multiple species and life history traits should be considered when investigating host–parasite relationships.     

Experimental Evolution of Alkaloid Tolerance in Sibling <Emphasis Type="Italic">Drosophila</Emphasis> Species with Different Degrees of Specialization

Drosophila buzzatii and Drosophila koepferae are sibling species with marked ecological differences related to their patterns of host exploitation. D. buzzatii is a polyphagous species with a sub-cosmopolitan distribution, while D. koepferae is endemic to the mountain plateaus of the Andes, where it exploits alkaloidiferous columnar cacti as primary hosts. We use experimental evolution to study the phenotypic response of these cactophilic Drosophila when confronting directional selection to cactus chemical defenses for 20 generations. Flies adapted to cactus diets also experienced higher viability on alkaloid-enriched media, suggesting the selection of adaptive genetic variation for chemical-stress tolerance. The more generalist species D. buzzatii showed a rapid adaptive response to moderate levels of secondary metabolites, whereas the columnar cacti specialist D. koepferae tended to maximize fitness under harder conditions. The evolutionary dynamic of fitness-related traits suggested the implication of metabolic efficiency as a key mediator in the adaptive response to chemical stress. Although we found no evidence of adaptation costs accompanying specialization, our results suggest the involvement of compensatory evolution. Overall, our study proposes that differential adaptation to secondary metabolites may contribute to varying degrees of host specialization, favoring niche partitioning among these closely related species.     

Effects of species diversity on disease risk

The transmission of infectious diseases is an inherently ecological process involving interactions among at least two, and often many, species. Not surprisingly, then, the species diversity of ecological communities can potentially affect the prevalence of infectious diseases. Although a number of studies have now identified effects of diversity on disease prevalence, the mechanisms underlying these effects remain unclear in many cases. Starting with simple epidemiological models, we describe a suite of mechanisms through which diversity could increase or decrease disease risk, and illustrate the potential applicability of these mechanisms for both vector-borne and non-vector-borne diseases, and for both specialist and generalist pathogens. We review examples of how these mechanisms may operate in specific disease systems. Because the effects of diversity on multi-host disease systems have been the subject of much recent research and controversy, we describe several recent efforts to delineate under what general conditions host diversity should increase or decrease disease prevalence, and illustrate these with examples. Both models and literature reviews suggest that high host diversity is more likely to decrease than increase disease risk. Reduced disease risk with increasing host diversity is especially likely when pathogen transmission is frequency-dependent, and when pathogen transmission is greater within species than between species, particularly when the most competent hosts are also relatively abundant and widespread. We conclude by identifying focal areas for future research, including (1) describing patterns of change in disease risk with changing diversity; (2) identifying the mechanisms responsible for observed changes in risk; (3) clarifying additional mechanisms in a wider range of epidemiological models; and (4) experimentally manipulating disease systems to assess the impact of proposed mechanisms.     

Non-native aquatic animals introductions have driven disease emergence in Europe

In this paper it is argued, using examples of disease emergence in aquatic animals in Europe, that the introduction of non-native species drives disease emergence by both extending the geographic range of parasites and pathogens and facilitating host-switching. Enteric red mouth disease and infectious haematopoietic necrosis of salmonids have extended their geographic range from North America to Europe with the import of live fish (Pimephales promelas) and rainbow trout eggs, respectively. Host-switching results in disease emergence when previously unidentified commensal organisms or known pathogen switch to new naïve hosts. The most serious endemic diseases of wild aquatic animals in Europe in recent years can be traced to the introduction of non-native species. Across Europe dramatic populations declines have occurred in native crayfish (e.g. Astacus astacus), oysters (Ostrea edulis) and eels (Anguilla anguilla), all which can be attributed, in varying degrees, to diseases (crayfish plague, Bonamia ostreae and Anguillicoloides crassus, respectively) introduced with non-native species. The severe adverse effects at a population level can be attributed to the lack of immunity in the new hosts. The impact of parasites more recently introduced to Europe, Sphaerothecum destruens (the rosette agent), and Batrachochytrium dendrobatidis, have yet to be fully determined. Both are generalists, with wide host ranges, and may present serious threats to native species. Aquaculture is the key driver for the introduction of non-native species. Most farming systems allow pathogen exchange between farmed and wild populations which underpins host-switching. Subsequently movements of animals between farms may result in the spread of newly emerged diseases. The introduction of non-native aquatic animals drives disease emergence, thus the ex-ante assessment of these hazards is severely limited. Generic risk mitigation measures (e.g. movement of disinfected eggs in place of live animals) and improved methods for rapid detection of new diseases are vital.     

Unraveling the historical prevalence of the invasive chytrid fungus in the Bolivian Andes: implications in recent amphibian declines

We studied the historical prevalence of the invasive and pathogenic chytrid fungus Batrachochytrium dendrobatidis (Bd) among amphibians from the Bolivian Andes. Our aim was also to determine its geographic pattern of dispersion, and a potential host taxonomic signature. We collected frog tissue samples from nine museum collections covering a period from 1863 to 2005 and from the field during 2009–2016. Bd was diagnosed via quantitative PCR in 599 individuals of 17 genera and 54 species. We found an overall Bd prevalence of 41% among 44 species tested. The first incidence of Bd was from a Telmatobius culeus in 1863; this is the earliest report of detection for this pathogen in the world. Results reveal a non-random historical and geographical pattern of Bd occurrence and amphibian declines that suggests the presence of two different invasive strains, an ancient endemic and a more recent introduction. Prevalence of Bd increased significantly by the mid-1990s, particularly in the cloud-forests, and this is coincident with the timing of drastic amphibian declines. In contrast, amphibians occurring in drier altiplano habitats have persisted in spite of Bd presence. We hypothesize that the early 1990s, and the cloud-forests in central Bolivia were the center of an epidemic surge of Bd that took its toll on many species, especially in the genus Telmatobius. Further sampling of cloud-forest species, and ongoing genetic studies of Bd isolates from Bolivia should help resolve the history of this invasive pathogen and test hypotheses on the differential response of endangered hosts.     

Explaining variation in brood parasitism rates between potential host species with similar habitat requirements

Host specialization evolved in many parasite-host systems. Evolution and maintenance of host specificity may be influenced by host life-history traits, active host selection by the parasite, and host anti-parasite strategies. The relative importance of these factors is poorly understood in situations that offer parasites a choice between hosts with similar habitat requirements. The common cuckoo Cuculus canorus is a generalist parasite on the species level, but individual females prefer particular host species. In reed beds of the Yellow River Delta, China, two potential hosts with similar nest characteristics, Oriental reed warblers Acrocephalus orientalis and reed parrotbills Paradoxornis heudei, breed in sympatry. We found that warblers were parasitized at much higher rates than parrotbills. Both hosts recognized and rejected non-mimetic model eggs well, indicating that they have been involved in an arms-race with cuckoos. Cuckoo eggs closely resembled warbler eggs, and such eggs were mostly accepted by warblers but rejected by parrotbills. Only warblers recognized adult cuckoos as a specific threat. Both hosts were equally good at raising cuckoo chicks. Low nest density, partial isolation by breeding time, small scale differences in nest and nest site characteristics, and high rejection rates of natural cuckoo eggs are likely cumulatively responsible for the low current parasitism rate in parrotbills. This study emphasizes the importance of integrating the study of general host life-history characteristics and specific anti-parasitism strategies of hosts across all breeding stages to understand the evolution of host specificity.     

Lagged Population Growth in a Termite Host Colony: Cause or Consequence of Inquilinism?

The presence of foreign organisms in the colonies of social insects could affect energy allocation to growth and reproduction of these hosts. Highly specialized invaders of such long-lived hosts, however, can be selected to be less harmful. After all, it pays for these symbionts to keep their host’s good health thereby prolonging cohabitation in the homeostatic environment of the termite colony. Here, we investigated such a hypothesis, focusing on populational parameters of a termite host sharing its nest with an obligatory termite inquiline. To this end, 19 natural colonies of Constrictotermes cyphergaster (Silvestri, 1901) (Termitidae: Nasutitermitinae) were sampled and the (i) number of individuals, (ii) proportion of soldier/workers in the colonies, and (iii) presence/absence of obligatory inquiline Inquilinitermes microcerus (Silvestri, 1901) (Termitidae: Termitinae) were measured. Results revealed a negative correlation between the number of individuals and the proportion of soldier/workers in the host colonies with the presence of I. microcerus colonies. In search of causal mechanisms for such a correlation, we inspected life history traits of both, inquilines and hosts, hypothesizing that such a result could indicate either (i) a dampening effect of the inquiline upon its host population or (ii) the coincidence of the moment of inquiline infiltration with the natural reduction of C. cyphergaster populational growth at the onset of its reproductive phase.     

Ecomorph Evolution in <Emphasis Type="Italic">Myotis</Emphasis> (Vespertilionidae,Chiroptera)

The genus Myotis is unique among mammals in its high taxonomic diversity and global distribution. Their phylogenetic relationships reflect biogeographic affinities rather than phenotypes. Myotis diverged from other bats in the early Miocene, with a subsequent split between Old and New World lineages about 19 million years ago. Similar ecomorphs (‘Leuconoe’ [near-water hunters], ‘Myotis’ [gleaners], ‘Selysius’ [aerial hawkers]) emerged independently in different lineages of Myotis. We retrieved the probable ancestral ecomorph for each lineage. Phenetic diversity was estimated from the analysis of body and skull traits. It seems that evolution of Myotis fluctuated between ‘Leuconoe’, ‘Selysius’, and larger ‘Myotis’.     

To eat or not to eat infected food: a bug’s dilemma

Parasites can adversely affect host population densities, but predators can regulate disease by reducing the density of susceptible hosts and consuming parasites contained in infected hosts. Some parasites induce phenotypic modifications in their hosts that potentially lead to increased predation. We investigated the role of parasite-induced modified appearance in the interactions between the crustacean Daphnia magna, its bacterial parasite Pasteuria ramosa, and its predator, the backswimmer Anisops sp. Our aim was to test the backswimmer’s prey preference between infected and uninfected D. magna to find out whether infection by P. ramosa can affect predation risk by Anisops. We found that Anisops sp. had a strong preference for uninfected D. magna under light, but under dark conditions the preference was reversed, which suggests that the modified appearance is the cause of this preference. Such anti-parasite preference by Anisops sp. could strongly influence host population dynamics as loss of fecundity, disease mortality, and predation are additive, resulting in host population decline.     

Biodiversity of traits and species both show weak responses to hydromorphological alteration in lowland river macroinvertebrates

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An experimental test to compare potential and realised specificity in ticks with different ecologies

The majority of studies on ecological specialisation rely on data reflecting realised specificity, without considering species’ potential specificity. Most species of ticks, a large family of hematophagous ectoparasites, have a narrow host range in nature, but it is unclear whether this is due to host-driven adaptations or other processes (such as off-host abiotic environment). We investigated the potential specificity of two tick species with contrasting ecology by infesting three avian host species that occur in the same off-host macrohabitat but are unequally infested by the ticks in nature (i.e. have contrasting realised specificity). The endophilic specialist tick Ixodes arboricola resides inside the hosts’ nest and has high realised host specificity, whereas the exophilic generalist tick I. ricinus encounters hosts in the field and has very low realised specificity. As hosts, we used great tits (frequently infested by both tick species), blackbirds (frequently infested by I. ricinus but never by I. arboricola) and great spotted woodpeckers (no ticks of either species have been reported). If realised specificity is constrained by host-driven adaptations there should be no differences between potential and realised specificity, whereas if realised specificity is constrained by other processes potential specificity and realised specificity should be different. We found that attachment rates and weight during feeding of I. arboricola were lower on blackbirds than on great tits, whereas there were no such differences for I. ricinus. No ticks of either species attached to woodpeckers. These results indicate that realised host specificity of ticks is, at least partially, constrained by host-driven adaptations. This specificity therefore strongly depends on the ticks’ encounter rates with particular host types, which are affected by the ticks’ off-host ecological requirements, behaviour and life-history characteristics.     

Ecomorphological diversity of freshwater fishes as a tool for conservation priority setting: a case study from a Balkan hotspot

Biodiversity studies commonly focus on taxonomic diversity measures such as species richness and abundance. However, alternative measures based on ecomorphological traits are also critical for unveiling the processes shaping biodiversity and community assembly along environmental gradients. Our study presents the first analysis of habitat-trait-community structure in a Balkan biodiversity hotspot (Louros river, NW Greece), through the investigation of the relationships among freshwater fish assemblages’ composition, morphological traits and habitat features. In order to provide a hierarchical classification of species’ priority to protection measures, we highlight the most ecomorphologically distinct species using originality analysis. Our results suggest that the longitudinal changes of habitat variables (water temperature, depth, substrate, altitude) drive the local fish assemblages’ structure highlighting the upstream-downstream gradient. We also present evidence for environmental filtering, establishing fish assemblages according to their ecomorphological traits. The calculation of the seven available indices of ecomorphological originality indicates that Valencia letourneuxi and Cobitis hellenica, which are endemic to Louros and threatened with extinction, exhibited the highest distinctiveness; thus their protection is of great importance. The methodological approach followed and the patterns described herein can contribute further to the application of community ecology theory to conservation, highlighting the need to use ecomorphological traits as a useful ‘tool’.     

External Reinfection of a Fungal Pathogen Does not Contribute to Pathogen Growth

Chytridiomycosis is an emerging infectious disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), which has led to devastating declines in amphibian populations worldwide. Current theory predicts that Bd infections are maintained through both reproduction on the host’s skin and reinfection from sources outside of the host. To investigate the importance of external reinfection on pathogen burden, we infected captive-bred individuals of the highly susceptible Panamanian Golden Frog, Atelopus glyphus, and wild-caught glass frogs, Espadarana prosoblepon, with Bd. We housed the animals in one of three treatments: individually, in heterospecific pairs, and in conspecific pairs. For 8 weeks, we measured the Bd load and shedding rate of all frogs. We found that Atelopus had high rates of increase in both Bd load and shedding rate, but pathogen growth rates did not differ among treatments. The infection intensity of Espadarana co-housed with Atelopus was indistinguishable from those housed singly and those in conspecific pairs, despite being exposed to a large external source of Bd zoospores. Our results indicate that Bd load in both species is driven by pathogen replication within an individual, with reinfection from outside the host contributing little to the amplification of host fungal load.     

Functional traits explain waterbirds' host status,subtype richness,and community-level infection risk for avian influenza

Species functional traits can influence pathogen transmission processes, and consequently affect species' host status, pathogen diversity, and community-level infection risk. We here investigated, for 143 European waterbird species, effects of functional traits on host status and pathogen diversity (subtype richness) for avian influenza virus at species level. We then explored the association between functional diversity and HPAI H5Nx occurrence at the community level for 2016/17 and 2021/22 epidemics in Europe. We found that both host status and subtype richness were shaped by several traits, such as diet guild and dispersal ability, and that the community-weighted means of these traits were also correlated with community-level risk of H5Nx occurrence. Moreover, functional divergence was negatively associated with H5Nx occurrence, indicating that functional diversity can reduce infection risk. Our findings highlight the value of integrating trait-based ecology into the framework of diversity–disease relationship, and provide new insights for HPAI prediction and prevention.     

Multi-stage Vector-Borne Zoonoses Models: A Global Analysis

A class of models that describes the interactions between multiple host species and an arthropod vector is formulated and its dynamics investigated. A host-vector disease model where the host’s infection is structured into n stages is formulated and a complete global dynamics analysis is provided. The basic reproduction number acts as a sharp threshold, that is, the disease-free equilibrium is globally asymptotically stable (GAS) whenever \({\mathcal {R}}_0^2\le 1\) and that a unique interior endemic equilibrium exists and is GAS if \({\mathcal {R}}_0^2>1\). We proceed to extend this model with m host species, capturing a class of zoonoses where the cross-species bridge is an arthropod vector. The basic reproduction number of the multi-host-vector, \({\mathcal {R}}_0^2(m)\), is derived and shown to be the sum of basic reproduction numbers of the model when each host is isolated with an arthropod vector. It is shown that the disease will persist in all hosts as long as it persists in one host. Moreover, the overall basic reproduction number increases with respect to the host and that bringing the basic reproduction number of each isolated host below unity in each host is not sufficient to eradicate the disease in all hosts. This is a type of “amplification effect,” that is, for the considered vector-borne zoonoses, the increase in host diversity increases the basic reproduction number and therefore the disease burden.     

Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity

The range of hosts a pathogen infects (host specificity) is a key element of disease risk that may be influenced by both shared phylogenetic history and shared ecological attributes of prospective hosts. Phylospecificity indices quantify host specificity in terms of host relatedness, but can fail to capture ecological attributes that increase susceptibility. For instance, similarity in habitat niche may expose phylogenetically unrelated host species to similar pathogen assemblages. Using a recently proposed method that integrates multiple distances, we assess the relative contributions of host phylogenetic and functional distances to pathogen host specificity (functional–phylogenetic host specificity). We apply this index to a data set of avian malaria parasite (Plasmodium and Haemoproteus spp.) infections from Melanesian birds to show that multihost parasites generally use hosts that are closely related, not hosts with similar habitat niches. We also show that host community phylogenetic ß‐diversity (Pßd) predicts parasite Pßd and that individual host species carry phylogenetically clustered Haemoproteus parasite assemblages. Our findings were robust to phylogenetic uncertainty, and suggest that phylogenetic ancestry of both hosts and parasites plays important roles in driving avian malaria host specificity and community assembly. However, restricting host specificity analyses to either recent or historical timescales identified notable exceptions, including a ‘habitat specialist’ parasite that infects a diversity of unrelated host species with similar habitat niches. This work highlights that integrating ecological and phylogenetic distances provides a powerful approach to better understand drivers of pathogen host specificity and community assembly.