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1.
Proc Natl Acad Sci U S A ; 121(19): e2311146121, 2024 May 07.
Article in English | MEDLINE | ID: mdl-38648469

ABSTRACT

The pace and scale of environmental change represent major challenges to many organisms. Animals that move long distances, such as migratory birds, are especially vulnerable to change since they need chains of intact habitat along their migratory routes. Estimating the resilience of such species to environmental changes assists in targeting conservation efforts. We developed a migration modeling framework to predict past (1960s), present (2010s), and future (2060s) optimal migration strategies across five shorebird species (Scolopacidae) within the East Asian-Australasian Flyway, which has seen major habitat deterioration and loss over the last century, and compared these predictions to empirical tracks from the present. Our model captured the migration strategies of the five species and identified the changes in migrations needed to respond to habitat deterioration and climate change. Notably, the larger species, with single or few major stopover sites, need to establish new migration routes and strategies, while smaller species can buffer habitat loss by redistributing their stopover areas to novel or less-used sites. Comparing model predictions with empirical tracks also indicates that larger species with the stronger need for adaptations continue to migrate closer to the optimal routes of the past, before habitat deterioration accelerated. Our study not only quantifies the vulnerability of species in the face of global change but also explicitly reveals the extent of adaptations required to sustain their migrations. This modeling framework provides a tool for conservation planning that can accommodate the future needs of migratory species.


Subject(s)
Animal Migration , Birds , Climate Change , Ecosystem , Animals , Animal Migration/physiology , Birds/physiology , Conservation of Natural Resources , Models, Biological
2.
Sci Total Environ ; 919: 170815, 2024 Apr 01.
Article in English | MEDLINE | ID: mdl-38336047

ABSTRACT

Wildlife are implicated in the dissemination of antimicrobial resistance, but their roles as hosts for Escherichia coli that pose a threat to human and animal health is limited. Gulls (family Laridae) in particular, are known to carry diverse lineages of multiple-antibiotic resistant E. coli, including extra-intestinal pathogenic E. coli (ExPEC). Whole genome sequencing of 431 E. coli isolates from 69 healthy Australian silver gulls (Chroicocephalus novaehollandiae) sampled during the 2019 breeding season, and without antibiotic selection, was undertaken to assess carriage in an urban wildlife population. Phylogenetic analysis and genotyping resolved 123 sequence types (STs) representing most phylogroups, and identified diverse ExPEC, including an expansive phylogroup B2 cluster comprising 103 isolates (24 %; 31 STs). Analysis of the mobilome identified: i) widespread carriage of the Yersinia High Pathogenicity Island (HPI), a key ExPEC virulence determinant; ii) broad distribution of two novel phage elements, each carrying sitABCD and iii) carriage of the transmissible locus of stress tolerance (tLST), an element linked to sanitation resistance. Of the 169 HPI carrying isolates, 49 (48 %) represented diverse B2 isolates hosting FII-64 ColV-like plasmids that lacked iutABC and sitABC operons typical of ColV plasmids, but carried the serine protease autotransporter gene, sha. Diverse E. coli also carried archetypal ColV plasmids (52 isolates; 12 %). Clusters of closely related E. coli (<50 SNVs) from ST58, ST457 and ST746, sourced from healthy gulls, humans, and companion animals, were frequently identified. In summary, anthropogenically impacted gulls host an expansive E. coli population, including: i) putative ExPEC that carry ColV virulence gene cargo (101 isolates; 23.4 %) and HPI (169 isolates; 39 %); ii) atypical enteropathogenic E. coli (EPEC) (17 isolates; 3.9 %), and iii) E. coli that carry the tLST (20 isolates; 4.6 %). Gulls play an important role in the evolution and transmission of E. coli that impact human health.


Subject(s)
Charadriiformes , Escherichia coli Infections , Extraintestinal Pathogenic Escherichia coli , Microbiota , Animals , Humans , Escherichia coli/genetics , Extraintestinal Pathogenic Escherichia coli/genetics , Escherichia coli Infections/veterinary , Escherichia coli Infections/epidemiology , Phylogeny , Australia , Anti-Bacterial Agents , Virulence Factors/genetics , Animals, Wild
3.
Biol Rev Camb Philos Soc ; 99(2): 582-597, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38062990

ABSTRACT

Avian gut microbial communities are complex and play a fundamental role in regulating biological functions within an individual. Although it is well established that diet can influence the structure and composition of the gut microbiota, foraging behaviour may also play a critical, yet unexplored role in shaping the composition, dynamics, and adaptive potential of avian gut microbiota. In this review, we examine the potential influence of coprophagic foraging behaviour on the establishment and adaptability of wild avian gut microbiomes. Coprophagy involves the ingestion of faeces, sourced from either self (autocoprophagy), conspecific animals (allocoprophagy), or heterospecific animals. Much like faecal transplant therapy, coprophagy may (i) support the establishment of the gut microbiota of young precocial species, (ii) directly and indirectly provide nutritional and energetic requirements, and (iii) represent a mechanism by which birds can rapidly adapt the microbiota to changing environments and diets. However, in certain contexts, coprophagy may also pose risks to wild birds, and their microbiomes, through increased exposure to chemical pollutants, pathogenic microbes, and antibiotic-resistant microbes, with deleterious effects on host health and performance. Given the potentially far-reaching consequences of coprophagy for avian microbiomes, and the dearth of literature directly investigating these links, we have developed a predictive framework for directing future research to understand better when and why wild birds engage in distinct types of coprophagy, and the consequences of this foraging behaviour. There is a need for comprehensive investigation into the influence of coprophagy on avian gut microbiotas and its effects on host health and performance throughout ontogeny and across a range of environmental perturbations. Future behavioural studies combined with metagenomic approaches are needed to provide insights into the function of this poorly understood behaviour.


Subject(s)
Gastrointestinal Microbiome , Animals , Coprophagia , Birds , Diet/veterinary , Feces
4.
Mol Ecol ; 33(2): e17203, 2024 Jan.
Article in English | MEDLINE | ID: mdl-37962103

ABSTRACT

The amphibian skin microbiome plays a crucial role in host immunity and pathogen defence, yet we know little about the environmental drivers of skin microbial variation across host individuals. Inter-individual variation in the availability of micro-nutrients such as dietary carotenoids, which are involved in amphibian immunity, may be one factor that influences skin microbial assembly across different life history stages. We compared the effect of four carotenoid supplementation regimes during different life stages on the adult skin microbiome using a captive population of the critically endangered southern corroboree frog, Pseudophryne corroboree. We applied 16S rRNA sequencing paired with joint-species distribution models to examine the effect of supplementation on taxon abundances. We found that carotenoid supplementation had subtle yet taxonomically widespread effects on the skin microbiome, even 4.5 years post supplementation. Supplementation during any life-history stage tended to have a positive effect on the number of bacterial taxa detected, although explanatory power was low. Some genera were sensitive to supplementation pre-metamorphosis, but most demonstrated either additive or dominant effects, whereby supplementation during one life history stage had intermediate or similar effects, respectively, to supplementation across life. Carotenoid supplementation increased abundances of taxa belonging to lactic acid bacteria, including Lactococcus and Enterococcus, a group of bacteria that have previously been linked to protection against the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd). While the fitness benefits of these microbial shifts require further study, these results suggest a fundamental relationship between nutrition and the amphibian skin microbiome which may be critical to amphibian health and the development of novel conservation strategies.


Subject(s)
Chytridiomycota , Microbiota , Humans , Animals , RNA, Ribosomal, 16S/genetics , Anura/genetics , Bacteria/genetics , Skin/microbiology , Microbiota/genetics , Carotenoids , Dietary Supplements
5.
Proc Biol Sci ; 290(1991): 20222237, 2023 01 25.
Article in English | MEDLINE | ID: mdl-36651046

ABSTRACT

Host susceptibility to parasites is mediated by intrinsic and external factors such as genetics, ecology, age and season. While waterfowl are considered central to the reservoir community for low pathogenic avian influenza A viruses (LPAIV), the role of host phylogeny has received limited formal attention. Herein, we analysed 12 339 oropharyngeal and cloacal swabs and 10 826 serum samples collected over 11 years from wild birds in Australia. As well as describing age and species-level differences in prevalence and seroprevalence, we reveal that host phylogeny is a key driver in host range. Seasonality effects appear less pronounced than in the Northern Hemisphere, while annual variations are potentially linked to El Niño-Southern Oscillation. Our study provides a uniquely detailed insight into the evolutionary ecology of LPAIV in its avian reservoir community, defining distinctive processes on the continent of Australia and expanding our understanding of LPAIV globally.


Subject(s)
Influenza A virus , Influenza in Birds , Animals , Phylogeny , Influenza in Birds/epidemiology , Seroepidemiologic Studies , Australia , Animals, Wild , Birds
6.
Biol Lett ; 18(6): 20220036, 2022 06.
Article in English | MEDLINE | ID: mdl-35702980

ABSTRACT

The energy cost of adaptive immune activation in endotherms is typically quantified from changes in resting metabolic rate following exposure to a novel antigen. An implicit assumption of this technique is that all variation in energy costs following antigenic challenge is due solely to adaptive immunity, while ignoring potential changes in the energy demands of ongoing bodily functions. We critically assess this assumption by measuring both basal metabolic rate (BMR) and exercise-induced maximal metabolic rate (MMR) in house sparrows before and after the primary and two subsequent vaccinations with either saline (sham) or two novel antigens (keyhole limpet haemocyanin and sheep red blood cells; KLH and SRBC, respectively). We also examined the effect of inducing male breeding levels of testosterone (T) on immune responses and their metabolic costs in both males and females. Although there was a moderate decrease in KLH antibody formation in T-treated birds, there was no effect of T on BMR, MMR or immunity to SRBC. There was no effect of vaccination on BMR but, surprisingly, all vaccinated birds maintained MMR better than sham-treated birds as the experiment progressed. Our findings caution against emphasizing energy costs or nutrient diversion as being responsible for reported fitness reductions following activation of adaptive immunity.


Subject(s)
Sparrows , Animals , Basal Metabolism/physiology , Energy Metabolism/physiology , Female , Male , Sheep , Sparrows/physiology
7.
PLoS Pathog ; 18(5): e1010150, 2022 05.
Article in English | MEDLINE | ID: mdl-35536868

ABSTRACT

Most of our understanding of the ecology and evolution of avian influenza A virus (AIV) in wild birds is derived from studies conducted in the northern hemisphere on waterfowl, with a substantial bias towards dabbling ducks. However, relevant environmental conditions and patterns of avian migration and reproduction are substantially different in the southern hemisphere. Through the sequencing and analysis of 333 unique AIV genomes collected from wild birds collected over 15 years we show that Australia is a global sink for AIV diversity and not integrally linked with the Eurasian gene pool. Rather, AIV are infrequently introduced to Australia, followed by decades of isolated circulation and eventual extinction. The number of co-circulating viral lineages varies per subtype. AIV haemagglutinin (HA) subtypes that are rarely identified at duck-centric study sites (H8-12) had more detected introductions and contemporary co-circulating lineages in Australia. Combined with a lack of duck migration beyond the Australian-Papuan region, these findings suggest introductions by long-distance migratory shorebirds. In addition, on the available data we found no evidence of directional or consistent patterns in virus movement across the Australian continent. This feature corresponds to patterns of bird movement, whereby waterfowl have nomadic and erratic rainfall-dependant distributions rather than consistent intra-continental migratory routes. Finally, we detected high levels of virus gene segment reassortment, with a high diversity of AIV genome constellations across years and locations. These data, in addition to those from other studies in Africa and South America, clearly show that patterns of AIV dynamics in the Southern Hemisphere are distinct from those in the temperate north.


Subject(s)
Influenza A virus , Influenza in Birds , Animals , Animals, Wild , Australia/epidemiology , Birds , Ducks , Genetic Variation , Influenza A virus/genetics , Influenza in Birds/epidemiology , Phylogeny
8.
J Virol ; 95(9)2021 04 12.
Article in English | MEDLINE | ID: mdl-33627387

ABSTRACT

Australian lineages of avian influenza A viruses (AIVs) are thought to be phylogenetically distinct from those circulating in Eurasia and the Americas, suggesting the circulation of endemic viruses seeded by occasional introductions from other regions. However, processes underlying the introduction, evolution and maintenance of AIVs in Australia remain poorly understood. Waders (order Charadriiformes, family Scolopacidae) may play a unique role in the ecology and evolution of AIVs, particularly in Australia, where ducks, geese, and swans (order Anseriformes, family Anatidae) rarely undertake intercontinental migrations. Across a 5-year surveillance period (2011 to 2015), ruddy turnstones (Arenaria interpres) that "overwinter" during the Austral summer in southeastern Australia showed generally low levels of AIV prevalence (0 to 2%). However, in March 2014, we detected AIVs in 32% (95% confidence interval [CI], 25 to 39%) of individuals in a small, low-density, island population 90 km from the Australian mainland. This epizootic comprised three distinct AIV genotypes, each of which represent a unique reassortment of Australian-, recently introduced Eurasian-, and recently introduced American-lineage gene segments. Strikingly, the Australian-lineage gene segments showed high similarity to those of H10N7 viruses isolated in 2010 and 2012 from poultry outbreaks 900 to 1,500 km to the north. Together with the diverse geographic origins of the American and Eurasian gene segments, these findings suggest extensive circulation and reassortment of AIVs within Australian wild birds over vast geographic distances. Our findings indicate that long-term surveillance in waders may yield unique insights into AIV gene flow, especially in geographic regions like Oceania, where Anatidae species do not display regular inter- or intracontinental migration.IMPORTANCE High prevalence of avian influenza viruses (AIVs) was detected in a small, low-density, isolated population of ruddy turnstones in Australia. Analysis of these viruses revealed relatively recent introductions of viral gene segments from both Eurasia and North America, as well as long-term persistence of introduced gene segments in Australian wild birds. These data demonstrate that the flow of viruses into Australia may be more common than initially thought and that, once introduced, these AIVs have the potential to be maintained within the continent. These findings add to a growing body of evidence suggesting that Australian wild birds are unlikely to be ecologically isolated from the highly pathogenic H5Nx viruses circulating among wild birds throughout the Northern Hemisphere.


Subject(s)
Animals, Wild/virology , Charadriiformes/virology , Disease Outbreaks/veterinary , Influenza A Virus, H10N7 Subtype , Influenza in Birds , Poultry/virology , Animal Migration , Animals , Australia , Gene Flow , Genes, Viral , Influenza A Virus, H10N7 Subtype/genetics , Influenza A Virus, H10N7 Subtype/isolation & purification , Influenza in Birds/epidemiology , Influenza in Birds/virology , Prevalence , Reassortant Viruses/genetics , Reassortant Viruses/isolation & purification
9.
mSphere ; 5(6)2020 11 25.
Article in English | MEDLINE | ID: mdl-33239365

ABSTRACT

Although most of the approximately 94 million annual human cases of gastroenteritis due to Salmonella enterica resolve without medical intervention, antimicrobial therapy is recommended for patients with severe disease. Wild birds can be natural hosts of Salmonella that pose a threat to human health; however, multiple-drug-resistant serovars of S. enterica have rarely been described. In 2012, silver gull (Chroicocephalus novaehollandiae) chicks at a major breeding colony were shown to host Salmonella, most isolates of which were susceptible to antibiotics. However, multiple-drug-resistant (MDR) Escherichia coli with resistance to carbapenems, ceftazidime, and fluoroquinolones was reported from this breeding colony. In this paper, we describe a novel MDR Salmonella strain subsequently isolated from the same breeding colony. SG17-135, an isolate of S. enterica with phenotypic resistance to 12 individual antibiotics but only nine antibiotic classes including penicillins, cephalosporins, monobactams, macrolides, fluoroquinolones, aminoglycosides, dihydrofolate reductase inhibitors (trimethoprim), sulfonamides, and glycylcyclines was recovered from a gull chick in 2017. Whole-genome sequence (WGS) analysis of SG17-135 identified it as Salmonella enterica serovar Agona (S Agona) with a chromosome comprising 4,813,284 bp, an IncHI2 ST2 plasmid (pSG17-135-HI2) of 311,615 bp, and an IncX1 plasmid (pSG17-135-X) of 27,511 bp. pSG17-135-HI2 housed a complex resistance region comprising 16 antimicrobial resistance genes including blaCTX-M-55 The acquisition of MDR plasmids by S. enterica described here poses a serious threat to human health. Our study highlights the importance of taking a One Health approach to identify environmental reservoirs of drug-resistant pathogens and MDR plasmids.IMPORTANCE Defining environmental reservoirs hosting mobile genetic elements that shuttle critically important antibiotic resistance genes is key to understanding antimicrobial resistance (AMR) from a One Health perspective. Gulls frequent public amenities, parklands, and sewage and other waste disposal sites and carry drug-resistant Escherichia coli Here, we report on SG17-135, a strain of Salmonella enterica serovar Agona isolated from the cloaca of a silver gull chick nesting on an island in geographic proximity to the greater metropolitan area of Sydney, Australia. SG17-135 is closely related to pathogenic strains of S Agona, displays resistance to nine antimicrobial classes, and carries important virulence gene cargo. Most of the antibiotic resistance genes hosted by SG17-135 are clustered on a large IncHI2 plasmid and are flanked by copies of IS26 Wild birds represent an important link in the evolution and transmission of resistance plasmids, and an understanding of their behavior is needed to expose the interplay between clinical and environmental microbial communities.


Subject(s)
Drug Resistance, Multiple, Bacterial/genetics , Escherichia coli/genetics , Plasmids/analysis , Salmonella enterica/genetics , Animals , Anti-Bacterial Agents/pharmacology , Australia , Charadriiformes/microbiology , DNA, Bacterial/genetics , Escherichia coli/pathogenicity , Whole Genome Sequencing
10.
Parasitol Res ; 118(1): 275-288, 2019 Jan.
Article in English | MEDLINE | ID: mdl-30456491

ABSTRACT

In nature, multiple waves of exposure to the same parasite are likely, making it important to understand how initial exposure or infection affects subsequent host infections, including the underlying physiological pathways involved. We tested whether experimental exposure to trematodes (Echinostoma trivolvis or Ribeiroia ondatrae) affected the stress hormone corticosterone (known to influence immunocompetence) in larvae representing five anuran species. We also examined the leukocyte profiles of seven host species after single exposure to R. ondatrae (including four species at multiple time points) and determined if parasite success differed between individuals given one or two challenges. We found strong interspecific variation among anuran species in their corticosterone levels and leukocyte profiles, and fewer R. ondatrae established in tadpoles previously challenged, consistent with defense "priming." However, exposure to either trematode had only weak effects on our measured responses. Tadpoles exposed to E. trivolvis had decreased corticosterone levels relative to controls, whereas those exposed to R. ondatrae exhibited no change. Similarly, R. ondatrae exposure did not lead to appreciable changes in host leukocyte profiles, even after multiple challenges. Prior exposure thus influenced host susceptibility to trematodes, but was not obviously associated with shifts in leukocyte counts or corticosterone, in contrast to work with microparasites.


Subject(s)
Amphibians/parasitology , Corticosterone/metabolism , Echinostoma/physiology , Echinostomiasis/veterinary , Larva/immunology , Amphibians/immunology , Amphibians/metabolism , Animals , Echinostomiasis/immunology , Echinostomiasis/metabolism , Echinostomiasis/parasitology , Female , Host-Parasite Interactions , Larva/metabolism , Larva/parasitology , Male
12.
J Anim Ecol ; 87(2): 354-368, 2018 03.
Article in English | MEDLINE | ID: mdl-28795407

ABSTRACT

Ecologists increasingly report the structures of metacommunities for free-living species, yet far less is known about the composition of symbiont communities through space and time. Understanding the drivers of symbiont community patterns has implications ranging from emerging infectious disease to managing host microbiomes. Using symbiont communities from amphibian hosts sampled from wetlands of California, USA, we quantified the effects of spatial structure, habitat filtering and host community components on symbiont occupancy and overall metacommunity structure. We built upon a statistical method to describe metacommunity structure that accounts for imperfect detection in survey data-detection error-corrected elements of metacommunity structure-by adding an analysis to identify covariates of community turnover. We applied our model to a metacommunity of eight parasite taxa observed in 3,571 Pacific chorus frogs (Pseudacris regilla) surveyed from 174 wetlands over 5 years. Symbiont metacommunity structure varied across years, showing nested structure in 3 years and random structure in 2 years. Species turnover was most consistently influenced by spatial and host community components. Occupancy generally increased in more southeastern wetlands, and snail (intermediate host) community composition had strong effects on most symbiont taxa. We have used sophisticated but accessible statistical methods to reveal that spatial components-which influence colonization-and host community composition-which mediates transmission-both drive symbiont community composition in this system. These methods allow us to associate broad patterns of community turnover to local, species-level effects, ultimately improving our understanding of spatial community dynamics.


Subject(s)
Anura/microbiology , Biodiversity , Host Microbial Interactions/physiology , Models, Biological , Animals , California , Population Density , Snails/microbiology , Wetlands
13.
J Anim Ecol ; 87(2): 428-437, 2018 03.
Article in English | MEDLINE | ID: mdl-29111601

ABSTRACT

Gut microbes are increasingly recognised for their role in regulating an animal's metabolism and immunity. However, identifying repeatable associations between host physiological processes and their gut microbiota has proved challenging, in part because microbial communities often respond stochastically to host physiological stress (e.g. fasting, forced exercise or infection). Migratory birds provide a valuable system in which to test host-microbe interactions under physiological extremes because these hosts are adapted to predictable metabolic and immunological challenges as they undergo seasonal migrations, including temporary gut atrophy during long-distance flights. These physiological challenges may either temporarily disrupt gut microbial ecosystems, or, alternatively, promote predictable host-microbe associations during migration. To determine the relationship between migration and gut microbiota, we compared gut microbiota composition between migrating and non-migrating ("resident") conspecific shorebirds sharing a flock. We performed this across two sandpiper species, Calidris ferruginea and Calidris ruficollis, in north-western Australia, and an additional C. ruficollis population 3,000 km away in southern Australia. We found that migrants consistently had higher abundances of the bacterial genus Corynebacterium (average 28% abundance) compared to conspecific residents (average <1% abundance), with this effect holding across both species and sites. However, other than this specific association, community structure and diversity was almost identical between migrants and residents, with migration status accounting for only 1% of gut community variation when excluding Corynebacterium. Our findings suggest a consistent relationship between Corynebacterium and Calidris shorebirds during migration, with further research required to identify causal mechanisms behind the association, and to elucidate functionality to the host. However, outside this specific association, migrating shorebirds broadly maintained gut community structure, which may allow them to quickly recover gut function after a migratory flight. This study provides a rare example of a repeatable and specific response of the gut microbiota to a major physiological challenge across two species and two distant populations.


Subject(s)
Animal Migration , Biodiversity , Birds/microbiology , Charadriiformes/microbiology , Gastrointestinal Microbiome/physiology , Host Microbial Interactions/physiology , Animals , Gastrointestinal Microbiome/genetics , Host Specificity , RNA, Ribosomal, 16S/genetics , South Australia , Western Australia
14.
J Anim Ecol ; 87(1): 301-314, 2018 Jan.
Article in English | MEDLINE | ID: mdl-28994103

ABSTRACT

Migratory animals are widely assumed to play an important role in the long-distance dispersal of parasites, and are frequently implicated in the global spread of zoonotic pathogens such as avian influenzas in birds and Ebola viruses in bats. However, infection imposes physiological and behavioural constraints on hosts that may act to curtail parasite dispersal via changes to migratory timing ("migratory separation") and survival ("migratory culling"). There remains little consensus regarding the frequency and extent to which migratory separation and migratory culling may operate, despite a growing recognition of the importance of these mechanisms in regulating transmission dynamics in migratory animals. We quantitatively reviewed 85 observations extracted from 41 studies to examine how both infection status and infection intensity are related to changes in body stores, refuelling rates, movement capacity, phenology and survival in migratory hosts across taxa. Overall, host infection status was weakly associated with reduced body stores, delayed migration and lower survival, and more strongly associated with reduced movement. Infection intensity was not associated with changes to host body stores, but was associated with moderate negative effects on movement, phenology and survival. In conclusion, we found evidence for negative effects of infection on host phenology and survival, but the effects were relatively small. This may have implications for the extent to which migratory separation and migratory culling act to limit parasite dispersal in migratory systems. We propose a number of recommendations for future research that will further advance our understanding of how migratory separation and migratory culling may shape host-parasite dynamics along migratory routes globally.


Subject(s)
Animal Migration , Birds/parasitology , Fishes/parasitology , Host-Parasite Interactions , Insecta/parasitology , Longevity , Animals , Birds/physiology , Fishes/physiology , Insecta/physiology
15.
Integr Comp Biol ; 56(2): 260-7, 2016 08.
Article in English | MEDLINE | ID: mdl-27462034

ABSTRACT

Migratory animals are simultaneously challenged by the physiological demands of long-distance movements and the need to avoid natural enemies including parasites and pathogens. The potential for animal migrations to disperse pathogens across large geographic areas has prompted a growing body of research investigating the interactions between migration and infection. However, the phenomenon of animal migration is yet to be incorporated into broader theories in disease ecology. Because migrations may expose animals to a greater number and diversity of pathogens, increase contact rates between hosts, and render them more susceptible to infection via changes to immune function, migration has the potential to generate both "superspreader species" and infection "hotspots". However, migration has also been shown to reduce transmission in some species, by facilitating parasite avoidance ("migratory escape") and weeding out infected individuals ("migratory culling"). This symposium was convened in an effort to characterize more broadly the role that animal migrations play in the dynamics of infectious disease, by integrating a range of approaches and scales across host taxa. We began with questions related to within-host processes, focusing on the consequences of nutritional constraints and strenuous movement for individual immune capability, and of parasite infection for movement capacity. We then scaled-up to between-host processes to identify what types, distances, or patterns of host movements are associated with the spread of infectious agents. Finally, we discussed landscape-scale relationships between migration and infectious disease, and how these may be altered as a result of anthropogenic changes to climate and land use. We are just beginning to scratch the surface of the interactions between infection and animal migrations; yet, with so many migrations now under threat, there is an urgent need to develop a holistic understanding of the potential for migrations to both increase and reduce infection risk.


Subject(s)
Animal Migration , Communicable Diseases/veterinary , Animals , Communicable Diseases/transmission
16.
Integr Comp Biol ; 56(2): 317-29, 2016 08.
Article in English | MEDLINE | ID: mdl-27252210

ABSTRACT

The extent to which animal migrations shape parasite transmission networks is critically dependent on a migrant's ability to tolerate infection and migrate successfully. Yet, sub-lethal effects of parasites can be intensified through periods of increased physiological stress. Long-distance migrants may, therefore, be especially susceptible to negative effects of parasitic infection. Although a handful of studies have investigated the short-term, transmission-relevant behaviors of wild birds infected with low-pathogenic avian influenza viruses (LPAIV), the ecological consequences of LPAIV for the hosts themselves remain largely unknown. Here, we assessed the potential effects of naturally-acquired LPAIV infections in Bewick's swans, a long-distance migratory species that experiences relatively low incidence of LPAIV infection during early winter. We monitored both foraging and movement behavior in the winter of infection, as well as subsequent breeding behavior and inter-annual resighting probability over 3 years. Incorporating data on infection history we hypothesized that any effects would be most apparent in naïve individuals experiencing their first LPAIV infection. Indeed, significant effects of infection were only seen in birds that were infected but lacked antibodies indicative of prior infection. Swans that were infected but had survived a previous infection were indistinguishable from uninfected birds in each of the ecological performance metrics. Despite showing reduced foraging rates, individuals in the naïve-infected category had similar accumulated body stores to re-infected and uninfected individuals prior to departure on spring migration, possibly as a result of having higher scaled mass at the time of infection. And yet individuals in the naïve-infected category were unlikely to be resighted 1 year after infection, with 6 out of 7 individuals that never resighted again compared to 20 out of 63 uninfected individuals and 5 out of 12 individuals in the re-infected category. Collectively, our findings indicate that acute and superficially harmless infection with LPAIV may have indirect effects on individual performance and recruitment in migratory Bewick's swans. Our results also highlight the potential for infection history to play an important role in shaping ecological constraints throughout the annual cycle.


Subject(s)
Animal Migration , Anseriformes , Influenza A virus/physiology , Influenza in Birds/virology , Animals , Anseriformes/physiology , Female , Influenza in Birds/immunology , Male , Netherlands , Seasons
17.
J Exp Biol ; 217(Pt 20): 3593-6, 2014 Oct 15.
Article in English | MEDLINE | ID: mdl-25189368

ABSTRACT

The aerobic capacity model proposes that endothermy is a by-product of selection favouring high maximal metabolic rates (MMR) and its mechanistic coupling with basal metabolic rate (BMR). Attempts to validate this model in birds are equivocal and restricted to phenotypic correlations (rP), thus failing to distinguish among- and within-individual correlations (rind and re). We examined 300 paired measurements of BMR and MMR from 60 house sparrows before and after two levels of experimental manipulation - testosterone implants and immune challenge. Overall, repeatability was significant in both BMR (R=0.25±0.06) and MMR (R=0.52±0.06). Only the testosterone treatment altered the rP between BMR and MMR, which resulted from contrasting effects on rind and re. While rind was high and significant (0.62±0.22) in sham-implanted birds, re was negative and marginally non-significant (-0.15±0.09) in testosterone-treated birds. Thus, the expected mechanistic link between BMR and MMR was apparent, but only in birds with low testosterone levels.


Subject(s)
Basal Metabolism/physiology , Energy Metabolism/physiology , Sparrows/physiology , Animals , Basal Metabolism/immunology , Energy Metabolism/immunology , Erythrocytes , Female , Gastropoda , Hemocyanins/immunology , Male , Multivariate Analysis , Orchiectomy , Phenotype , Sheep , Sparrows/immunology , Testosterone/pharmacology
18.
J Anim Ecol ; 83(1): 266-75, 2014 Jan.
Article in English | MEDLINE | ID: mdl-24033258

ABSTRACT

Similar to other infectious diseases, the prevalence of low pathogenic avian influenza viruses (LPAIV) has been seen to exhibit marked seasonal variation. However, mechanisms driving this variation in wild birds have yet to be tested. We investigated the validity of three previously suggested drivers for the seasonal dynamics in LPAIV infections in wild birds: (i) host density, (ii) immunologically naïve young and (iii) increased susceptibility in migrants. To address these questions, we sampled a key LPAIV host species, the mallard Anas platyrhynchos, on a small spatial scale, comprehensively throughout a complete annual cycle, measuring both current and past infection (i.e. viral and seroprevalence, respectively). We demonstrate a minor peak in LPAIV prevalence in summer, a dominant peak in autumn, during which half of the sampled population was infected, and no infections in spring. Seroprevalence of antibodies to a conserved gene segment of avian influenza virus (AIV) peaked in winter and again in spring. The summer peak of LPAIV prevalence coincided with the entrance of unfledged naïve young in the population. Moreover, juveniles were more likely to be infected, shed higher quantities of virus and were less likely to have detectable antibodies to AIV than adult birds. The arrival of migratory birds, as identified by stable hydrogen isotope analysis, appeared to drive the autumn peak in LPAIV infection, with both temporal coincidence and higher infection prevalence in migrants. Remarkably, seroprevalence in migrants was substantially lower than viral prevalence throughout autumn migration, further indicating that each wave of migrants amplified local AIV circulation. Finally, while host abundance increased throughout autumn, it peaked in winter, showing no direct correspondence with either of the LPAIV infection peaks. At an epidemiologically relevant spatial scale, we provide strong evidence for the role of migratory birds as key drivers for seasonal epizootics of LPAIV, regardless of their role as vectors of these viruses. This study exemplifies the importance of understanding host demography and migratory behaviour when examining seasonal drivers of infection in wildlife populations.


Subject(s)
Aging , Animal Migration/physiology , Ducks , Epidemics/veterinary , Influenza in Birds/virology , Seasons , Animals , Influenza A virus/classification , Influenza in Birds/epidemiology , Seroepidemiologic Studies
19.
Oecologia ; 173(4): 1471-80, 2013 Dec.
Article in English | MEDLINE | ID: mdl-23754306

ABSTRACT

In nature, hosts are exposed to an assemblage of parasite species that collectively form a complex community within the host. To date, however, our understanding of how within-host-parasite communities assemble and interact remains limited. Using a larval amphibian host (Pacific chorus frog, Pseudacris regilla) and two common trematode parasites (Ribeiroia ondatrae and Echinostoma trivolvis), we experimentally examined how the sequence of host exposure influenced parasite interactions within hosts. While there was no evidence that the parasites interacted when hosts were exposed to both parasites simultaneously, we detected evidence of both intraspecific and interspecific competition when exposures were temporally staggered. However, the strength and outcome of these priority effects depended on the sequence of addition, even after accounting for the fact that parasites added early in host development were more likely to encyst compared to parasites added later. Ribeiroia infection success was reduced by 14 % when Echinostoma was added prior to Ribeiroia, whereas no such effect was noted for Echinostoma when Ribeiroia was added first. Using a novel fluorescent-labeling technique that allowed us to track Ribeiroia infections from different exposure events, we also discovered that, similar to the interspecific interactions, early encysting parasites reduced the encystment success of later arriving parasites by 41 %, which could be mediated by host immune responses and/or competition for space. These results suggest that parasite identity interacts with host immune responses to mediate parasite interactions within the host, such that priority effects may play an important role in structuring parasite communities within hosts. This knowledge can be used to assess host-parasite interactions within natural communities in which environmental conditions can lead to heterogeneity in the timing and composition of host exposure to parasites.


Subject(s)
Anura/parasitology , Echinostoma/physiology , Host-Parasite Interactions , Trematoda/physiology , Animals , Coinfection/parasitology , Larva/parasitology
20.
Vet Parasitol ; 194(1): 9-15, 2013 May 01.
Article in English | MEDLINE | ID: mdl-23339847

ABSTRACT

Toxoplasma gondii is an intracellular coccidian parasite found worldwide and is known to infect virtually all warm-blooded animals. It requires a cat (family Felidae) to complete its full life cycle. Despite the absence of wild felids on the Arctic archipelago of Svalbard, T. gondii has been found in resident predators such as the arctic fox and polar bear. It has therefore been suggested that T. gondii may enter this ecosystem via migratory birds. The objective of this study was to identify locations where goose populations may become infected with T. gondii, and to investigate the dynamics of T. gondii specific antibodies. Single blood samples of both adults and juveniles were collected from selected goose species (Anser anser, A. brachyrhynchus, Branta canadensis, B. leucopsis) at Arctic brood-rearing areas in Russia and on Svalbard, and temperate wintering grounds in the Netherlands and Denmark (migratory populations) as well as temperate brood-rearing grounds (the Netherlands, non-migratory populations). A modified agglutination test was used on serum, for detection of antibodies against T. gondii. Occasional repeated annual sampling of individual adults was performed to determine the antibody dynamics. Adults were found seropositive at all locations (Arctic and temperate, brood-rearing and wintering grounds) with low seroprevalence in brood-rearing birds on temperate grounds. As no juvenile geese were found seropositive at any brood-rearing location, but nine month old geese were found seropositive during spring migration we conclude that geese, irrespective of species and migration, encounter T. gondii infection in wintering areas. In re-sampled birds on Svalbard significant seroreversion was observed, with 42% of seropositive adults showing no detectable antibodies after 12 months, while the proportion of seroconversion was only 3%. Modelled variation of seroprevalence with field data on antibody longevity and parasite transmission suggests seroprevalence of a population within a range of 5.2-19.9%, in line with measured values. The high occurrence of seroreversion compared to the low occurrence of seroconversion hampers analysis of species- or site-specific patterns, but explains the absence of an increase in seroprevalence with age and the observed variation in antibody titre. These findings imply that even though infection rate is low, adults introduce T. gondii to the high Arctic ecosystem following infection in temperate regions.


Subject(s)
Bird Diseases/epidemiology , Geese , Toxoplasma/isolation & purification , Toxoplasmosis, Animal/epidemiology , Age Factors , Agglutination Tests/veterinary , Animal Migration , Animals , Antibodies, Protozoan/blood , Arctic Regions , Bird Diseases/parasitology , Birds , Cats/physiology , Europe/epidemiology , Geography , Population Density , Prevalence , Seasons , Seroepidemiologic Studies , Species Specificity , Toxoplasmosis, Animal/parasitology
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