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Review
. 2018 May 5;373(1745):20170094.
doi: 10.1098/rstb.2017.0094.

Responses of migratory species and their pathogens to supplemental feeding

Affiliations
Review

Responses of migratory species and their pathogens to supplemental feeding

Dara A Satterfield et al. Philos Trans R Soc Lond B Biol Sci. .

Abstract

Migratory animals undergo seasonal and often spectacular movements and perform crucial ecosystem services. In response to anthropogenic changes, including food subsidies, some migratory animals are now migrating shorter distances or halting migration altogether and forming resident populations. Recent studies suggest that shifts in migratory behaviour can alter the risk of infection for wildlife. Although migration is commonly assumed to enhance pathogen spread, for many species, migration has the opposite effect of lowering infection risk, if animals escape from habitats where pathogen stages have accumulated or if strenuous journeys cull infected hosts. Here, we summarize responses of migratory species to supplemental feeding and review modelling and empirical work that provides support for mechanisms through which resource-induced changes in migration can alter pathogen transmission. In particular, we focus on the well-studied example of monarch butterflies and their protozoan parasites in North America. We also identify areas for future research, including combining new technologies for tracking animal movements with pathogen surveillance and exploring potential evolutionary responses of hosts and pathogens to changing movement patterns. Given that many migratory animals harbour pathogens of conservation concern and zoonotic potential, studies that document ongoing shifts in migratory behaviour and infection risk are vitally needed.This article is part of the theme issue 'Anthropogenic resource subsidies and host-parasite dynamics in wildlife'.

Keywords: Danaus plexippus; host–parasite interactions; pathogen; resident; seasonal migration; supplemental feeding.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1.
Figure 1.
Mechanisms (red text) through which migration lowers infection risk, illustrated with a transmission model for susceptible (S), infected (I) and recovered (R) hosts, and allowing for pathogen transmission through direct contact or via encounters with parasite infectious stages shed into the environment (W). (i) Migratory escape allows susceptible hosts (S) to escape environments where infectious stages accumulate over time, limiting both shedding (λ, not shown) and transmission rate (βSW) for environmentally transmitted parasites. (ii) Migratory culling lowers the number of infected individuals (I) by increasing infection-induced mortality (α) during strenuous migration. (iii) Migratory allopatry and separation reduce transmission by separating more susceptible (S) and more infected (I) individuals in different age classes during migration, thus limiting contact rates. (iv) Migratory recovery reduces the number of infected individuals (I), as infected animals recover (at rate ϒ) due to conditions during migration.(Online version in colour.)
Figure 2.
Figure 2.
Conceptual diagram illustrating how supplemental resources from unintentional (e.g. crops, landfills) and intentional sources (e.g. bird feeders) can cause changes in migratory behaviour, with consequences that raise or reduce infection risk. Diminished migrations, including shifts to residency and short-stopping behaviours, can result in some processes that increase transmission, such as the loss of migratory culling and migratory escape. Other mechanisms may reduce transmission, such as if resident animals experience higher immunity. (Image credits: Public domain).
Figure 3.
Figure 3.
(a) Some monarch butterflies are responding to (b) the widespread availability of tropical milkweed (Asclepias curassavica) by breeding year-round in the same locations of the southern USA, rather than migrating, raising infection risk from (c) the protozoan parasite Ophryocystis elektroscirrha. A study involving citizen scientists [23] showed that resident monarchs at (d) winter-breeding sites (blue points) compared to migratory sites (orange points for summer breeding; green points for overwintering) show (e) five times higher infection prevalence on average. Image credits: (a) Pat Davis, (b) Dara Satterfield, (c) Sonia Altizer.

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