Parasite–Parasite Interactions in the Wild: How To Detect Them?

Hellard, Éléonore; Fouchet, David; Vavre, Fabrice; Pontier, Dominique

doi:10.1016/j.pt.2015.07.005

Cited by 84 publications

(70 citation statements)

References 82 publications

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“…We present evidence that biotic associations play important roles in the occurrences and infection likelihoods of haematozoan parasites. Our description of parasite cooccurrence patterns provides critical new insights into disease ecology, as parasite associations are expected across many host systems (Bell et al 2006;P erez-Tris et al 2007;Johnson & Buller 2011;Vaumourin et al 2015), yet evidence from wildlife is biased towards mammalian hosts (Lello et al 2004;Tompkins et al 2011;Hellard et al 2015). Additionally, we show that co-infections are difficult to identify using PCR alone, a finding demonstrated for many host-pathogen systems (Valki unas et al 2006;Dyachenko et al 2010;Grybchuk-Ieremenko et al 2014;Moustafa et al 2016).…”

Section: Discussionmentioning

confidence: 70%

“…; Hellard et al . ). Additionally, we show that co‐infections are difficult to identify using PCR alone, a finding demonstrated for many host–pathogen systems (Valkiūnas et al .…”

Section: Discussionmentioning

confidence: 97%

“…Based on evidence for parasite competition in mammals (Bell et al 2006;Telfer et al 2010;Hellard et al 2015), we predicted that distinct avian malaria parasites would exhibit negatively correlated infection probabilities when accounting for environmental drivers, indicating possible parasite competition. We predicted that malaria species would positively correlate with microfilaria, based on experimental evidence that immune-modulating nematodes can facilitate malaria co-infections (Druilhe, Tall & Sokhna 2005;Su et al 2005).…”

Section: Introductionmentioning

confidence: 99%

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Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Clark

Wells

Dimitrov

et al. 2016

Journal of Animal Ecology

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Summary 1.Experimental work increasingly suggests that non-random pathogen associations can affect the spread or severity of disease. Yet due to difficulties distinguishing and interpreting co-infections, evidence for the presence and directionality of pathogen co-occurrences in wildlife is rudimentary. 2. We provide empirical evidence for pathogen co-occurrences by analysing infection matrices for avian malaria (Haemoproteus and Plasmodium spp.) and parasitic filarial nematodes (microfilariae) in wild birds (New Caledonian Zosterops spp.). 3. Using visual and genus-specific molecular parasite screening, we identified high levels of co-infections that would have been missed using PCR alone. Avian malaria lineages were assigned to species level using morphological descriptions. We estimated parasite co-occurrence probabilities, while accounting for environmental predictors, in a hierarchical multivariate logistic regression. 4. Co-infections occurred in 36% of infected birds. We identified both positively and negatively correlated parasite co-occurrence probabilities when accounting for host, habitat and island effects. Two of three pairwise avian malaria co-occurrences were strongly negative, despite each malaria parasite occurring across all islands and habitats. Birds with microfilariae had elevated heterophil to lymphocyte ratios and were all co-infected with avian malaria, consistent with evidence that host immune modulation by parasitic nematodes facilitates malaria co-infections. Importantly, co-occurrence patterns with microfilariae varied in direction among avian malaria species; two malaria parasites correlated positively but a third correlated negatively with microfilariae. 5. We show that wildlife co-infections are frequent, possibly affecting infection rates through competition or facilitation. We argue that combining multiple diagnostic screening methods with multivariate logistic regression offers a platform to disentangle impacts of environmental factors and parasite co-occurrences on wildlife disease.

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Section: Discussionmentioning

confidence: 70%

“…; Hellard et al . ). Additionally, we show that co‐infections are difficult to identify using PCR alone, a finding demonstrated for many host–pathogen systems (Valkiūnas et al .…”

Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

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Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Clark

Wells

Dimitrov

et al. 2016

Journal of Animal Ecology

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“…Second, confounding factors such as a common vector, behavior or other host heterogeneities in disease exposure, or spatial heterogeneities in disease risk might also account for the association (Johnson and Buller , Hellard et al. , ). Third, chronic malaria may compromise immune function, making birds more susceptible to active pox infection and increasing the likelihood of severe pox infections, which lead to permanent deformities seen in old pox.…”

Section: Discussionmentioning

confidence: 99%

The epidemiology of avian pox and interaction with avian malaria in Hawaiian forest birds

Samuel

Woodworth

Atkinson

et al. 2018

Ecological Monographs

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Despite the purported role of avian pox (Avipoxvirus spp.) in the decline of endemic Hawaiian birds, few studies have been conducted on the dynamics of this disease, its impact on free‐living avian populations, or its interactions with avian malaria (Plasmodium relictum). We conducted four longitudinal studies of 3–7 yr in length and used generalized linear models to evaluate cross‐sectional prevalence of active pox infection and individuals with healed deformities that had recovered from pox. Our goal was to understand how species, season, elevation, malaria infection, and other biological characteristics influenced pox infection in ʻApapane, Hawaiʻi ʻAmakihi, ʻIʻiwi, and Japanese White‐eye across low‐, mid‐, and high‐elevation forests on the island of Hawaiʻi. We also used multi‐state capture‐recapture (longitudinal) models to estimate pox infection rates, recovery rates, and potential pox‐related mortality. Pox infection rates were typically highest in low‐elevation forests, followed by mid‐elevation forests, and lowest in high‐elevation forests. We also found seasonal changes in pox prevalence throughout the annual cycle; typically increasing from spring through summer, peaking in fall, and declining in winter. These seasonal changes occurred in low‐ and mid‐elevation forests, but not in high elevations where pox infection was low. Seasonal and elevation patterns of pox infection are like those for avian malaria, strongly implicating mosquito vectors, rather than other biting arthropods or contact transmission, as the primary source of transmitting both diseases. Most native Hawaiian birds recovered from pox infection within 6 months; frequently without permanent lesions. Contrary to our expectations, we found no direct evidence that pox is a substantial mortality factor in any of the three native bird species we studied. Birds with chronic malaria infection were more likely to have both active pox infection and healed pox lesions suggesting a synergistic interaction that may influence the evolution of pox virulence. Because pox infection can be assessed visually, and birds have a high recovery rate, this disease may be a sensitive indicator of the seasonal and annual risk of transmission of malaria in Hawaiʻi.

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“…While these models can reliably measure interactions within hosts (Hellard et al . ), they implicitly assume that the strength and direction of pairwise interactions among coinfecting symbionts is the same regardless of the historical context in which they occur (i.e. ‘deterministic’ following Fukami ).…”

Section: Introductionmentioning

confidence: 99%

Interactions among symbionts operate across scales to influence parasite epidemics

2017

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Parasite epidemics may be influenced by interactions among symbionts, which can depend on past events at multiple spatial scales. Within host individuals, interactions can depend on the sequence in which symbionts infect a host, generating priority effects. Across host individuals, interactions can depend on parasite phenology. To test the roles of parasite interactions and phenology in epidemics, we embedded multiple cohorts of sentinel plants, grown from seeds with and without a vertically transmitted symbiont, into a wild host population, and tracked foliar infections caused by three common fungal parasites. Within hosts, parasite growth was influenced by coinfections, but coinfections were often prevented by priority effects among symbionts. Across hosts, parasite phenology altered host susceptibility to secondary infections, symbiont interactions and ultimately the magnitude of parasite epidemics. Together, these results indicate that parasite phenology can influence parasite epidemics by altering the sequence of infection and interactions among symbionts within host individuals.

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Parasite–Parasite Interactions in the Wild: How To Detect Them?

Cited by 84 publications

References 82 publications

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

The epidemiology of avian pox and interaction with avian malaria in Hawaiian forest birds

Interactions among symbionts operate across scales to influence parasite epidemics

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