Endoscopy as a novel method for assessing endoparasite burdens in free‐ranging European shags (<i>Phalacrocorax aristotelis</i>)

Burthe, Sarah J.; Newell, Mark A.; Goodman, Gidona; Butler, Adam; Bregnballe, Thomas; Harris, Eileen; Wanless, Sarah; Cunningham, Emma J. A.; Daunt, Francis

doi:10.1111/2041-210x.12015

Cited by 14 publications

(51 citation statements)

References 41 publications

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“…Shags on the Isle of May are infected with the gastrointestinal nematode Contracaecum 132 rudolphii (Anisakidae: Ascaridoidea; Hartwich 1964), which occur in the GI tract of nestling and 133 adult shags in this population (Reed 2007;Burthe et al 2013; E. Harris, pers. comm.…”

Section: Host-parasite System 120mentioning

confidence: 99%

“…We used a refurbished 9mm diameter medical endoscope (Olympus©, UK) to view the oesophagus 162 and proventriculus of conscious chicks under licence (full details of endoscopy procedure in 163 (Burthe et al 2013). Endoscopy was undertaken by a trained and experienced operator (S. Burthe) 164 while an assistant held the bird still and its bill open.…”

Section: Endoscopy 161mentioning

confidence: 99%

“…2015). Endoscopy of adults has found males to host more worms than females and late breeders 107 more than early breeders (Burthe et al, 2013), but among juveniles, patterns of variation in parasite 108 abundance and their link with variation in host fitness are not well quantified. It is hence unclear 109 whether these differences in treatment responses between types of juveniles arise from differences 110 in nematode burden or differences in the impact of a similar burden.…”

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confidence: 99%

“…Breeding success declines through the season, with later breeders fledging fewer 130 chicks and producing fewer recruits (Daunt et al 1999; Harris et al 1994). 131Shags on the Isle of May are infected with the gastrointestinal nematode Contracaecum 132 rudolphii (Anisakidae: Ascaridoidea; Hartwich 1964), which occur in the GI tract of nestling and 133 adult shags in this population (Reed 2007;Burthe et al 2013; E. Harris, pers. comm.…”

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confidence: 99%

“…Comparisons of necropsied and 371 endoscoped individuals was further constrained by the limited overlap in the ages of chicks used in 372 each technique: endoscopy was carried out on generally older birds and tended to yield lower 373 overall burdens but a higher proportion of large worms than necropsies of generally younger birds. 374Endoscopy may have yielded lower counts because chicks' stomachs frequently contained residual 375 food that partially obscured the view through the endoscope, a constraint that is more easily avoided 376 when endoscoping adults in this system (Burthe et al 2013). Nonetheless, endoscopy counts from 377 shags have been shown to be repeatable (Burthe et al 2013), and our successful application of this 378 technique to developing hosts thus opens opportunities for monitoring individuals' worm burdens 379 from an early stage in their long lives.…”

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Between-individual variation in nematode burden among juveniles in a wild host

et al. 2016

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Contact CEH NORA team at noraceh@ceh.ac.ukThe NERC and CEH trademarks and logos ('the Trademarks') are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. Parasite infection in young animals can affect host traits related to demographic processes such as 19 survival and reproduction, and is therefore crucial to population viability. However, variation in 20 infection among juvenile hosts is poorly understood. Experimental studies have indicated that 21 effects of parasitism can vary with host sex, hatching order and hatch date, yet it remains unclear 22 whether this is linked to differences in parasite burdens. We quantified gastrointestinal nematode 23 burdens of wild juvenile European shags (Phalacrocorax aristotelis) using two in situ measures 24 (endoscopy of live birds and necropsy of birds that died naturally) and one non-invasive proxy 25 measure (faecal egg counts). In situ methods revealed that almost all chicks were infected (98%), 26 that infections established at an early age, and that older chicks hosted more worms, but faecal egg 27 counts underestimated prevalence. We found no strong evidence that burdens differed with host sex, 28 rank or hatch date. Heavier chicks had higher burdens, demonstrating that the relationship between 29 burdens and their costs is not straightforward. In situ measures of infection are therefore a valuable 30 tool in building our understanding of the role that parasites play in the dynamics of structured 31 natural populations. The costs that parasite infection can impose on their hosts can influence key demographic traits, 45 such as reproductive success and survival, which are crucial to the growth rate and hence viability 46 of populations (Albon et al., 2002; Newey et al., 2005; Redpath et al., 2006, Tompkins 2011. 47 Between-individual variation in nematode burden among juveniles in a wild hostHowever, parasitism is unlikely to affect all individuals in a population in the same way. Firstly, 48 individuals may host different burdens as a result of differences in exposure to parasites, 49 susceptibility to infection and resistance to its impacts. This contributes to parasite abundance 50typically showing a skewed distribution among hosts, which is particularly well documented in 51 macroparasites (Randolph et al., 1999; Shaw and Dobson, 1995). Secondly, once parasitized, the 52 relationship between parasite load and host fitness may vary between individuals due to differences 53 in tolerance for a given parasite load. Siblings, for example, may vary in the level of maternal 54 antibodies they receive (Pihlaja et al., 2006), males may be affected more than females due to 55 immunosuppressive effects of testosterone (Mougeot et al., 2009), and the relative benefits of 56 allocating resources between fighting infection and reproduction may vary with age (Adamo et al., 57 2001). These factors may lead to different types of host responding differently to infection, with 58 consequenc...

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Section: Host-parasite System 120mentioning

confidence: 99%

Section: Endoscopy 161mentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Between-individual variation in nematode burden among juveniles in a wild host

et al. 2016

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Parasitism in early life: environmental conditions shape within‐brood variation in responses to infection

Granroth‐Wilding

Burthe

Lewis

et al. 2014

Ecology and Evolution

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Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last-hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last-hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life-history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.

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Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population

Hicks

Green

Daunt

et al. 2019

Ecology

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Parasites are a major component of all animal populations. Males and females often differ in their levels of parasite prevalence, potentially leading to sex differences in the impact of parasitism on fitness, with important implications for the evolution of parasite and host traits including resistance, tolerance, and virulence. However, quantitative measures of the impact of parasitism under free-living conditions are extremely rare, as they require detailed host demographic data with measures of parasite burden over time. Here, we use endoscopy for direct quantification of natural-parasite burdens and relate these to reproductive success over 7 yr in a wild population of seabirds. Contrary to predictions, only female burdens were associated with negative impacts of parasitism on breeding success, despite males having significantly higher burdens. Female reproductive success declined by 30% across the range of natural parasite burdens. These effects persisted when accounting for interannual population differences in breeding success. Our results provide quantitative estimates of profound sublethal effects of parasitism on the population. Importantly, they highlight how parasites act unpredictably to shape ecological and evolutionary processes in different components of the same population, with implications for demography and selection on host and parasite traits.

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Endoscopy as a novel method for assessing endoparasite burdens in free‐ranging European shags (Phalacrocorax aristotelis)

Cited by 14 publications

References 41 publications

Between-individual variation in nematode burden among juveniles in a wild host

Between-individual variation in nematode burden among juveniles in a wild host

Parasitism in early life: environmental conditions shape within‐brood variation in responses to infection

Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population

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