Infection deflection: hosts control parasite location with behaviour to improve tolerance (original) (raw)

Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites

Journal of Animal Ecology, 2015

1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-oflife', play in the evolution of resistance and tolerance to parasites. 2. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. 3. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. 4. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible reorderings of the three fastest or slowest paced species, and various measurements of tolerance. 5. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.

On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis

Canadian Journal of Zoology, 2006

Many animals respond behaviourally to the infective stages of parasites, but the efficacy of such responses in reducing risk of parasitism often is not established. It was found that tadpoles of Rana clamitans Latr., 1801 (green frogs) and R. sylvatica LeConte, 1825 (wood frogs) increased their activity when exposed to live infective stages (cercariae) of the trematode Echinostoma trivolvis Rudolphi, 1809. The susceptibility to parasitism for green frog tadpoles subjected to three different treatments was compared. Tadpoles were housed at 20 8C and allowed to respond to cercariae, held at 6-8 8C and showing reduced behavioural responses, or anesthetized and showing no responses. Low levels of parasitism were found for tadpoles that responded behaviourally to cercariae; such responses are expected to occur under normal field conditions in the absence of factors suppressing activity of tadpoles. We also demonstrate that infectivity of E. trivolvis cercariae to non-responding (anesthetized) wood frog tadpoles was higher at warm than at cool temperatures. Thus, lowered parasitism at warm temperatures in the first experiment likely resulted from host behavioural responses and not from low infectivity of cercariae. These results have implications for observing effects of environmental factors on susceptibility to parasitism where susceptibility is thought or known to be mediated by host behaviour.

Developmental variation in resistance and tolerance in a multi-host-parasite system

Functional Ecology, 2010

1. Organisms can protect themselves against parasitism by reducing either parasite burden (resistance) or damage caused by parasites at a given burden (tolerance), but little is known about resistance and tolerance to multiple parasites among wild animal populations and species. The fitness effects of parasitism can be broken down into two components: (i) cost of parasite exposure, the difference in fitness between organisms that were not exposed to parasites and those that were exposed but not infected, and (ii) tolerance, the change in host fitness as a function of parasite burden. For amphibians, a taxon that is being decimated by disease, knowing which species and ontogenetic stages are least resistant or least tolerant to which parasites would help target research and management efforts. 2. We reared American toad (Bufo americanus) and green frog (Rana clamitans) tadpoles in a common garden environment and quantified survival and trematode burdens after exposure to 20 Echinostoma trivolvis, Ribeiroia ondatrae or plagiorchid trematode cercariae. 3. All three trematodes caused significant B. americanus mortality, but R. ondatrae was the only species to induce significant mortality of R. clamitans and was the most deadly of the parasites. Young tadpoles had greater parasite-induced mortality than older tadpoles. 4. Mortality patterns were driven by B. americanus having lower resistance and a higher cost of parasite exposure than R. clamitans, older tadpoles having higher tolerance than younger tadpoles, B. americanus and R. clamitans exhibiting lower resistance and a higher cost of parasite exposure, respectively, to R. ondatrae relative to the other tested trematodes, and skin-penetrating trematodes inducing a higher cost of parasite exposure than non-skin-penetrators. Host size was not predictive of resistance but was a positive predictor of the cost of resistance and tolerance; however, size alone could not fully account for host differences in tolerance. 5. Interactions among developmental stage and host and trematode species emphasize the plasticity and context-dependency of defence strategies and the importance of considering resistance and tolerance to multiple parasites in wild host species.

Variation in anti-parasite behaviour and infection among larval amphibian species

Oecologia, 2014

Along with immune defences, many animals exhibit effective anti-parasite behaviours such as 25 parasite avoidance and removal that influence their susceptibility to infection. Host ecology and 26 life history influence investment into comparatively fixed defences such as innate immunity but 27 may affect the strength of anti-parasite behaviours as well. We investigated activity levels in 28 five different species of larval amphibian with varying life histories and ecology in control, novel 29 food stimulus, and trematode parasite (Echinoparyphium sp.) threat conditions. There was a 30 significant interaction of species and treatment given that American toad (Bufo americanus), 31 wood frog (Lithobates sylvaticus), and bullfrog (Lithobates catesbeianus) tadpoles generally 32 increased their activity when parasite infectious stages were present while grey tree frogs (Hyla 33 versicolor) and northern leopard frogs (Lithobates pipiens) did not, even though activity was 34 negatively related to infection. In addition, there was considerable variation among species in 35 their susceptibility to parasitism, with infection prevalence ranging from 17% in bullfrog 36 tadpoles to 70% in wood frogs. However, amphibian life history (larval and adult traits) was not 37 related to parasitism or level of anti-parasite behaviour at the species level. Consequently, we 38 suggest that future investigations include more species with a range of life history traits and also 39 consider host ecology, particularly if conspicuous anti-parasite behaviours are more likely in 40 amphibian species that experience a relatively low risk of predation. 41 42 43 44 45 46

Do Parasitic Trematode Cercariae Demonstrate a Preference for Susceptible Host Species?

2012

Abstract Many parasites are motile and exhibit behavioural preferences for certain host species. Because hosts can vary in their susceptibility to infections, parasites might benefit from preferentially detecting and infecting the most susceptible host, but this mechanistic hypothesis for host-choice has rarely been tested. We evaluated whether cercariae (larval trematode parasites) prefer the most susceptible host species by simultaneously presenting cercariae with four species of tadpole hosts.

Can Differences in Host Behavior Drive Patterns of Disease Prevalence in Tadpoles?

PloS one, 2011

Differences in host behavior and resistance to disease can influence the outcome of host-pathogen interactions. We capitalized on the variation in aggregation behavior of Fowler's toads (Anaxyrus [ = Bufo] fowleri) and grey treefrogs (Hyla versicolor) tadpoles and tested for differences in transmission of Batrachochytrium dendrobatidis (Bd) and host-specific fitness consequences (i.e., life history traits that imply fitness) of infection in single-species amphibian mesocosms. On average, A. fowleri mesocosms supported higher Bd prevalences and infection intensities relative to H. versicolor mesocosms. Higher Bd prevalence in A. fowleri mesocosms may result, in part, from higher intraspecific transmission due to the aggregation of tadpoles raised in Bd treatments. We also found that, independent of species, tadpoles raised in the presence of Bd were smaller and less developed than tadpoles raised in disease-free conditions. Our results indicate that aggregation behavior might increase Bd prevalence and that A. fowleri tadpoles carry heavier infections relative to H. versicolor tadpoles. However, our results demonstrate that Bd appears to negatively impact larval growth and developmental rates of A. fowleri and H. versicolor similarly, even in the absence of high Bd prevalence.

In an arms race between host and parasite, a lungworm’s ability to infect a toad is determined by host susceptibility, not parasite preference

2021

Evolutionary arms races can alter both parasite infectivity and host resistance, and it is difficult to separate the effects of these twin determinants of infection outcomes. Using a co-introduced, invasive host-parasite system (the lungworm Rhabdias pseudosphaerocephala and the cane toad Rhinella marina), we quantified behavioural responses of parasite larvae to skin-chemical cues of toads from different invasive populations, and rates at which hosts became infected following standardised exposure to lungworms. Chemical cues from toad skin altered host-seeking behaviour by parasites, similarly among populations. The number of infection attempts (parasite larvae entering the host’s body) also did not differ between populations, but rates of successful infection (establishment of adult worm in host lungs) was higher for range-edge toads than for range-core conspecifics. Thus, lower resistance to parasite infection in range-edge toads appears to be due to less effective immune defence...

Parasite-altered host behavior in the face of a predator: manipulation or not?

Parasitology Research, 2001

Parasitologists have generally accepted the idea that parasite-induced alterations in host behavior increase the chance for parasite survival and transmission or ensure the completion of its life cycle. The aim of the present study was to investigate modi®cations in the behavior of Taenia crassiceps-infected BALB/c mice in the face of a predator. The experiments showed modi®cations in the response of infected mice in comparison with uninfected controls on exposure to a predator ®nal host. However, dierent studies lead us to suggest that the observed modi®cations are likely to be a secondary eect of the impact of the parasite on host physiology and immunity that favors its development and proliferation.