Anti-parasite Behaviour Research Articles

Breeding pairs with color aberrations in oriental reed warblers.

In 2017, one pair of Oriental reed warblers (Acrocephalus orientalis) with color aberrations was found in Yongnianwa National Wetland Park, Hebei, China. The female bird exhibited white feathers on the head, neck, and upper back, and the base of the beak was flesh-red in color. The male had a few feathers on the outer edges of the left and right primary wing coverts that were white, which was determined to be leucism after analysis. The breeding pairs laid their first egg on May 29, with a clutch size of four eggs. After an incubation period of 13 days, two chicks hatched on June 13, 2017. The nest was found empty on June 20 when the chicks were 7 days old and before fledging age; therefore, it was presumed that the chicks had been predated. A white parrot egg was added to the nest during the incubation period to test the egg recognition ability of breeding pairs and was successfully rejected. To the best of our knowledge, this is the first report of color aberrations in the Oriental reed warbler, and we found that this color aberrations did not affect some reproductive and antiparasitic behaviors of the birds, but whether it affects their breeding success needs to be further studied.

Behave yourself: effects of exogenous-glucocorticoid exposure on larval amphibian anti-parasite behaviour and physiology.

Parasites represent a ubiquitous threat for most organisms, requiring potential hosts to invest in a range of strategies to defend against infection-these include both behavioural and physiological mechanisms. Avoidance is an essential first line of defence, but this behaviour may show a trade-off with host investment in physiological immunity. Importantly, while environmental stressors can lead to elevated hormones in vertebrates, such as glucocorticoids, that can reduce physiological immunity in certain contexts, behavioural defences may also be compromised. Here, we investigate anti-parasite behaviour and immune responses against a trematode (flatworm) parasite by larval amphibians (tadpoles) exposed or not to a simulated general stressor in the form of exogenous corticosterone. Tadpoles that were highly active in the presence of the trematode infectious stage (cercariae) had lower infection loads, and parasite loads from tadpoles treated only with dechlorinated water were significantly lower than those exposed to corticosterone or the solvent control. However, treatment did not affect immunity as measured through white blood-cell profiles, and there was no relationship between the latter and anti-parasite behaviour. Our results suggest that a broad range of stressors could increase host susceptibility to infection through altered anti-parasite behaviours if they elevate endogenous glucocorticoids, irrespective of physiological immunity effects. How hosts defend themselves against parasitism in the context of multiple challenges represents an important topic for future research, particularly as the risk posed by infectious diseases is predicted to increase in response to ongoing environmental change.

The effect of Common Cuckoo parasitism on the annual productivity of a host population

Avian interspecific brood parasitism is an excellent system for studying coevolutionary processes in nature because brood parasites directly affect host reproductive success. Most research on avian brood parasitism has, therefore, focused primarily on specific host anti-parasite behaviours and parasite counter-adaptations. However, the population-level consequences of brood parasitism for host species are poorly understood. This study investigated the effect of Common Cuckoo (Cuculus canorus) parasitism on the productivity of a local population of the Great Reed Warbler (Acrocephalus arundinaceus) host in south-western Slovakia. A total of 495 females nesting at the studied site successfully fledged 1321 of their own young and 63 young of the Common Cuckoo over the course of 15 years (2008–2022), and the annual rate of successful parasitism ranged from 18% to 44% over this period. As predicted, higher rates of successful cuckoo parasitism significantly reduced the annual productivity of the local Great Reed Warbler population, and its contribution to decreased host reproductive success was at about the same rate as overall nest failure caused by predation and other environmental factors. Such a heavily parasitized population was probably maintained by immigrants from other populations and density-dependent selection, which is also consistent with source–sink dynamics. However, further long-term studies monitoring parasitized populations are required to confirm these findings.

Defense behavior of two closely related but geographically distant host species against cuckoo parasitism: A next test for the parallel coevolution.

Interactions between avian brood parasites, such as common cuckoos (Cuculus canorus), and their hosts are one of the best-studied examples of the coevolutionary arms race. Different stages of this arms race can be seen in different races of common cuckoos and their hosts across their range. However, little is known whether selected populations of two closely related but geographically distant species with probably different coevolutionary histories with the common cuckoo are also at different stages of the arms race. In this study, we tested this prediction experimentally using the same non-mimetic model eggs and three-dimensional (3D) printed models of the gray adult common cuckoo (Cuculus canorus). We examined egg recognition and egg rejection and aggression against the common cuckoo in the great reed warbler (Acrocephalus arundinaceus) and Oriental reed warbler (Acrocephalus orientalis), in Slovakia of Europe and northeast China of Asia. The results showed that the great reed warbler exhibited stronger responses to experimental model eggs and 3D models of the common cuckoo than the Oriental reed warbler. We conclude that both the great reed warbler and Oriental reed warbler have well-developed antiparasitic behaviors against common cuckoos in the studied populations, but with different levels of defense intensity, which may be due to local differences in parasitic pressure and the risk of parasitism. This provides an opportunity to study coevolutionary processes between the brood parasite and its hosts together in both species at large geographical scales.

Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills.

Social animals are particularly exposed to infectious diseases. Pathogen-driven selection pressures have thus favoured the evolution of behavioural adaptations to decrease transmission risk such as the avoidance of contagious individuals. Yet, such strategies deprive individuals of valuable social interactions, generating a cost-benefit trade-off between pathogen avoidance and social opportunities. Recent studies revealed that hosts differ in these behavioural defences, but the determinants driving such inter-individual variation remain understudied. Using 6 years of behavioural and parasite data on a large natural population of mandrills (Mandrillus sphinx), we showed that, when parasite prevalence was high in the population, females avoided grooming their conspecifics' peri-anal region (PAR), where contagious gastro-intestinal parasites accumulate. Females varied, however, in their propensity to avoid this risky body region: across years, some females consistently avoided grooming it, while others did not. Interestingly, hygienic females (i.e. those avoiding the PAR) were less parasitized than non-hygienic females. Finally, age, dominance rank and grooming frequency did not influence a female's hygiene, but both mother-daughter and maternal half-sisters exhibited similar hygienic levels, whereas paternal half-sisters and non-kin dyads did not, suggesting a social transmission of this behaviour. Our study emphasizes that the social inheritance of hygiene may structure behavioural resistance to pathogens in host populations with potential consequences on the dynamics of infectious diseases.

Defensive adaptations to cuckoo parasitism in the black-browed reed warbler (Acrocephalus bistrigiceps): recognition and mechanism.

Hosts of avian brood parasites suffer a high cost of reproductive loss due to parasitism, driving them to evolve a variety of anti-parasitic defenses. These defenses comprise a series of components, including the recognition of brood parasites and the eggs laid by the parasites, cues used for recognition, and the mechanisms on which these behaviors are based. In this study, we conducted egg recognition and nest intruder experiments to examine these components of anti-parasitic behavior in the black-browed reed warbler (Acrocephalus bistrigiceps), a rare host of the common cuckoo (Cuculus canorus). We found that the host possessed strong recognition capacity, rejecting 100% of parasitic eggs, and used a template-based mechanism for egg recognition. The host birds also rejected 80% of their own eggs on which artificial markings were added to the blunt pole; however, they accepted all eggs with the same manipulation on the sharp pole, implying that the blunt pole was an important recognition cue. Furthermore, the host exhibited stronger aggression to cuckoos than to harmless controls; a behavior specific to the incubation stage rather than the nestling stage. Therefore, the host was able to distinguish the cuckoo from other nest intruders as being a brood parasite. These results together help explain the near absence of cuckoo parasitism in black-browed reed warblers and provide new information concerning anti-parasitic defenses in this host species.

Egg rejection and egg recognition mechanisms in Oriental Reed Warblers

BackgroundNest parasitism by cuckoos (Cuculus spp.) results in enormous reproductive failure and forces hosts to evolve antiparasitic strategies, i.e., recognition of own eggs and rejection of cuckoo eggs. There are often sexual conflicts between male and female individuals in the expression of antiparasitic behavior due to the differences in reproductive inputs and division of labor.MethodsBy adding a foreign egg made of blue soft clay to the host nest during early incubation period in the field, and by removing several host eggs and adding experimental eggs to control the proportion of two egg types in the nest, we examined egg rejection ability, egg recognition mechanism and sexual difference in egg rejection of the Oriental Reed Warbler (Acrocephalus orientalis), one of the major hosts of Common Cuckoos (Cuculus canorus).ResultsOur results indicated that Oriental Reed Warblers can recognize and reject nearly 100% (73/75) of the non-mimetic eggs made of blue soft clay, and they could reject foreign eggs with 100% accuracy, regardless of the ratio of experimental eggs and its own eggs in the nest. Furthermore, all cases of egg rejections recorded by videos were only carried out by females.ConclusionsOriental Reed Warblers have a high egg recognition ability and show a true recognition mechanism. Only female warblers perform egg rejection, suggesting that the sex for host egg incubation seems to play an important role in the evolution of egg recognition mechanisms.

Activity of Fluorinated Curcuminoids against Leishmania major and Toxoplasma gondii Parasites.

A new 3,4-difluorobenzylidene analog of curcumin, CDF, was recently reported, which demonstrated significantly enhanced bioavailability and in vivo anticancer activity compared with curcumin. For highlighting the antiparasitic behavior of CDF, we tested this compound together with its new O-methylated analog MeCDF against Leishmania major and Toxoplasma gondii parasites. Both CDF and MeCDF were tested in vitro against L. major and T. gondii. In addition, the in vitro cytotoxicity against Vero cells and macrophages was determined and selectivity indices were calculated. The DPPH radical scavenging activity assay was carried out in order to determine the antioxidant activity of the test compounds. Both compounds showed high activities against both parasite forms with EC50 values in the (sub-)micromolar range (0.35 to 0.8 μM for CDF, 0.31 to 1.2 μM for MeCDF). The higher activity of CDF against L. major amastigotes when compared with MeCDF can in parts be attributed to the antioxidant activity of CDF while MeCDF lacking any antioxidant activity was more active than CDF against T. gondii parasites. In conclusion, CDF and MeCDF are promising antiparasitic drug candidates due to their high activities against L. major and T. gondii parasites.

Trade-offs between reproduction and behavioural resistance against ectoparasite infection

Reproduction is a key determinant of organismal fitness, but organisms almost always face the threat of parasite infection. Thus, potential trade-offs between mating and parasite resistance may have substantial impacts on the ecology and evolution of host species. Although trade-offs between microbial resistance and mating in arthropods are well-documented, there is a paucity of evidence that mating compromises host resistance to the ubiquitous threat posed by ectoparasites. Despite the centrality of reproduction to host fitness and the widespread risk of parasites, there is a dearth of experiments showing a trade-off between mating/reproduction and anti-parasite behaviours. In this study, we test if mating increases the susceptibility of female flies to mite infection. We also investigated a potential underlying mechanism for the trade-off: that mating reduces overall endurance and hence anti-parasitic defenses among female flies. We experimentally mated female Drosophila nigrospiracula, with or without a chance to recover from male harassment, and challenged them with a natural ectoparasite, the mite Macrocheles subbadius. Mated females, regardless of time for recovery from male harassment, acquired more infections than unmated females. Furthermore, mated females had lower endurance in negative geotaxis assays, suggesting the increased susceptibility is due to reduced endurance. Our research shows a trade-off between reproduction and parasite resistance in a host-macroparasite system and suggests that trade-off theory is a fruitful direction for understanding these associations.

Insights into the Antimicrobial Potential of Dithiocarbamate Anions and Metal-Based Species

Bacterial infection remains a worldwide problem that requires urgent addressing. Overuse and poor disposal of antibacterial agents abet the emergence of bacterial resistance mechanisms. There is a clear need for new approaches for the development of antibacterial therapeutics. Herein, the antibacterial potential of molecules based on dithiocarbamate anions, of general formula R(R’)NCS2(−), and metal salts of transition metals and main group elements, is summarized. Preclinical studies show a broad range of antibacterial potential, and these investigations are supported by appraisals of possible biological targets and mechanisms of action to guide chemical syntheses. This bibliographic review of the literature points to the exciting potential of dithiocarbamate-based therapeutics in the crucial battle against bacteria. Additionally, included in this overview, for the sake of completeness, is mention of the far fewer studies on the antifungal potential of dithiocarbamates and even less work conducted on antiparasitic behavior.

Integrating concepts of physiological and behavioral resistance to parasites.

Conceptual parallels between physiological and behavioral forms of resistance to parasites have led to the development of terminology like "the behavioral immune system" to refer to behaviors that combat parasites. I extend this metaphor by applying findings from research on physiological resistance to generate predictions for the ecology and evolution of behavioral resistance (here, synonymous with avoidance). In certain cases, behavioral resistance may follow similar evolutionary dynamics to physiological resistance. However, more research on the nature of the costs of behavioral resistance is needed, including how parasite transmission mode may be a key determinant of these costs. In addition, "acquiring" behavioral resistance may require specific mechanisms separate from classical forms of conditioning, due to constraints on timing of host learning processes and parasite incubation periods. Given existing literature, behavioral resistance to infectious disease seems more likely to be innate than acquired within the lifetime of an individual, raising new questions about how individual experience could shape anti-parasite behaviors. This review provides a framework for using existing literature on physiological resistance to generate predictions for behavioral resistance, and highlights several important directions for future research based on this comparison.

Antiparasitic Behavior of Trifluoromethylated Pyrazole 2-Amino-1,3,4-thiadiazole Hybrids and Their Analogues: Synthesis and Structure-Activity Relationship.

A series of trifluoromethylated pyrazole thiosemicarbazone, trifluromethylated pyrazole isothiosemicarbazone, and trifluoromethylated pyrazole 2-amino-1,3,4-thiadiazole hybrids were synthesized and evaluated in vitro against the promastigote form of Leishmania amazonensis and the epimastigote form of Trypanosoma cruzi, the pathogens causing the neglected tropical diseases leishmaniasis and Chagas disease, respectively. The results show the potential of these compounds regarding their antiparasitic properties. Studies on the structure-activity relationship demonstrated that compounds containing a bulky group at the para position of the phenyl ring attached to the 5-position of the pyrazole core had better antiparasitic effects. Among the substituents attached at the 3-position of the pyrazole ring, the insertion of the 2-amino-1,3,4-thiadiazole nucleus led to the most potent compounds compared to the thiosemicarbazone derivative.

Experimental study of micro-habitat selection by ixodid ticks feeding on avian hosts

Mechanisms of on-host habitat selection of parasites are important to the understanding of host-parasite interactions and evolution. To this end, it is important to separate the factors driving parasite micro-habitat selection from those resulting from host anti-parasite behaviour. We experimentally investigated whether tick infestation patterns on songbirds are the result of an active choice by the ticks themselves, or the outcome of songbird grooming behaviour. Attachment patterns of three ixodid tick species with different ecologies and host specificities were studied on avian hosts. Ixodes arboricola, Ixodes ricinus and Ixodes frontalis were put on the head, belly and back of adult great tits (Parus major) and adult domestic canaries (Serinus canaria domestica) which were either restricted or not in their grooming capabilities. Without exception, ticks were eventually found on a bird’s head. When we gave ticks full opportunities to attach on other body parts – in the absence of host grooming – they showed lower attachment success. Moreover, ticks moved from these other body parts to the host's head when given the opportunity. This study provides evidence that the commonly observed pattern of ticks feeding on songbirds’ heads is the result of an adaptive behavioural strategy. Experimental data on a novel host species, the domestic canary, and a consistent number of published field observations, strongly support this hypothesis. We address some proximate and ultimate causes that may explain parasite preference for this body part in songbirds. The link found between parasite micro-habitat preference and host anti-parasite behaviour provides further insight into the mechanisms driving ectoparasite aggregation, which is important for the population dynamics of hosts, ectoparasites and the micro-pathogens for which they are vectors.

Differently sized cuckoos pose different threats to hosts.

Hole-nesting tits Parus spp. have been classified as “unsuitable” hosts for cuckoo parasitism because cuckoos cannot enter a cavity if the entrance is too small. However, Chinese tits could reject alien eggs and egg ejection rate increased with the local diversity of parasitic cuckoo species. Antiparasitic behavior among Chinese tits may have evolved due to greater size variation among sympatric cuckoo species. This raises the question of whether differently sized parasitic cuckoos pose different threats to Chinese tits. A green-backed tit Parus monticolus population that is sympatric with Asian emerald cuckoo Chrysococcyx maculatus (eme-cuckoo, small-sized parasite) and common cuckoo Cuculus canorus (com-cuckoo, large-sized parasite), and a cinereous tit P. cinereus population that is only sympatric with com-cuckoo were chosen as study organisms. We observed behavioral response and recorded alarm calls of the 2 tit species to eme-cuckoo, com-cuckoo, chipmunk Tamias sibiricus (a nest predator) and dove Streptopelia orientalis (a harmless control), and subsequently played back alarm calls to conspecific incubating females. In dummy experiments, both tit species performed intense response behavior to chipmunk, but rarely responded strongly to the 3 avian species. In playback experiments, both tit species responded strongly to conspecific chipmunk alarm calls, but rarely responded to dove alarm calls. The intensity of response of incubating female green-backed tits to eme-cuckoo and com-cuckoo alarm calls were similar to that of chipmunk alarm calls, while the intensity to eme-cuckoo alarm calls was higher than the intensity to dove alarm calls which was similar to that of com-cuckoo alarm calls. In contrast, few female cinereous tits responded to eme-cuckoo and com-cuckoo alarm calls. These findings indicated that the threat level of eme-cuckoo was slightly greater than that of com-cuckoo for sympatric green-backed tits, but not for allopatric cinereous tits.

Hygienic personalities in wild grey mouse lemurs vary adaptively with sex.

Detecting the risk of infection and minimizing parasite exposure represent the first lines of host defence against parasites. Individuals differ in the expression of these behavioural defences, but causes of such variation have received little empirical attention. We therefore experimentally investigated the effects of several individual and environmental factors on the expression level of faecal avoidance in the context of feeding, drinking, sleeping and defecating in a wild primate population. We found a strong sex bias in the expression level of anti-parasite behaviours of grey mouse lemurs (Microcebus murinus), with only females strongly avoiding contaminated food, water and nests, and exhibiting selective defecation. Our results further suggest that individuals adapted their protective behaviours according to variation in intrinsic and ecological factors that may influence the cost-benefit balance of behavioural defences. Overall, individuals exhibited high consistency of investment in protective behaviours across behavioural contexts and time, suggesting that grey mouse lemurs exhibit different hygienic personalities. Finally, the global hygienic score was negatively correlated with faecal-orally transmitted parasite richness, suggesting that variation in behavioural defence has fitness consequences. We suggest that integrating inter-individual variation in behavioural defences in epidemiological studies should improve our ability to model disease spread within populations.

Ecology of fear: environment-dependent parasite avoidance among ovipositing Drosophila.

Habitat avoidance is an anti-parasite behaviour exhibited by at-risk hosts that can minimize exposure to parasites. Because environments are often heterogeneous, host decision-making with regards to habitat use may be affected by the presence of parasites and habitat quality simultaneously. In this study we examine how the ovipositing behaviour of a cactiphilic fruit fly, Drosophila nigrospiracula, is affected by the presence of an ectoparasitic mite, Macrocheles subbadius, in conjunction with other environmental factors - specifically the presence or absence of conspecific eggs and host plant tissue. We hypothesized that the trade-off between site quality and parasite avoidance should favour ovipositing at mite-free sites even if it is of inferior quality. We found that although flies avoided mites in homogeneous environments (86% of eggs at mite-free sites), site quality overwhelmed mite avoidance. Both conspecific eggs (65% of eggs at infested sites with other Drosophila eggs) and host plant tissue (78% of eggs at infested sites with cactus) overpowered mite avoidance. Our results elucidate the context-dependent decision-making of hosts in response to the presence of parasites in variable environments, and suggest how the ecology of fear and associated trade-offs may influence the relative investment in anti-parasite behaviour in susceptible hosts.

Costs of breeding far away from neighbors: Isolated host nests are more vulnerable to cuckoo parasitism

A series of parasitic and anti-parasitic strategies has evolved during the long-term coevolution between cuckoos and their hosts. The first stage of the arms race is host nest choice by cuckoos, followed by nest defense by hosts. This study examined nest defense strategies of the Oriental reed warbler (Acrocephalus orientalis) in relation to parasitism by the common cuckoo (Cuculus canorus). Attack rate of Oriental reed warblers against common cuckoo dummies was 100% and neighboring individuals participated in 87.1% of such attacks. Furthermore, the number of hosts attacking cuckoo dummies was significantly positively correlated with the number of neighbors at a distance from 40 to 70 m, indicating social anti-parasitic behavior. Analysis of nest-site parameters indicated that the distance to the nearest neighboring unparasitized nest was significantly shorter than that of parasitized nests. Our study demonstrated that isolated nests of Oriental reed warblers with distant neighbors were more vulnerable to common cuckoo parasitism suggesting a cost of breeding far away from neighbors. We hypothesize that cooperative behavior within local populations of Oriental reed warblers can probably be considered as an anti-parasitic strategy developed through long-term coevolution. Choice and parasitism of isolated host nests far away from neighbors may be an adaptive parasitic strategy by common cuckoos to increase the probability of successful parasitism.

Anti-parasite behaviour of birds

Birds have many kinds of internal and external parasites, including viruses, bacteria and fungi, as well as protozoa, helminths and arthropods. Because parasites have negative effects on host fitness, selection favours the evolution of anti-parasite defences, many of which involve behaviour. We provide a brief review of anti-parasite behaviours in birds, divided into five major categories: (i) body maintenance, (ii) nest maintenance, (iii) avoidance of parasitized prey, (iv) migration and (v) tolerance. We evaluate the adaptive significance of the different behaviours and note cases in which additional research is particularly needed. We briefly consider the interaction of different behaviours, such as sunning and preening, and how behavioural defences may interact with other forms of defence, such as immune responses. We conclude by suggesting some general questions that need to be addressed concerning the nature of anti-parasite behaviour in birds.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood-parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D-printed model eggs of two cuckoo host-races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti-parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti-parasite behaviors, with only one of 96 models rejected; the rejecters were Red-throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naive hosts and become established in North America whether or not their historic host species are widely available. (Less)

From wetland specialist to hand-fed generalist: shifts in diet and condition with provisioning for a recently urbanized wading bird.

Many wildlife species shift their diets to use novel resources in urban areas. The consequences of these shifts are not well known, and consumption of reliable-but low quality-anthropogenic food may present important trade-offs for wildlife health. This may be especially true for carnivorous species such as the American white ibis (Eudocimus albus), a nomadic wading bird which has been increasingly observed in urban parks in South Florida, USA. We tested the effects of anthropogenic provisioning on consumer nutrition (i.e. dietary protein), body condition and ectoparasite burdens along an urban gradient using stable isotope analysis, scaled mass index values and GPS transmitter data. Ibises that assimilated more provisioned food were captured at more urban sites, used more urban habitat, had lower mass-length residuals, lower ectoparasite scores, assimilated less δ15N and had smaller dietary isotopic ellipses. Our results suggest that ibises in urban areas are heavily provisioned with anthropogenic food, which appears to offer a trade-off by providing low-quality, but easily accessible, calories that may not support high mass but may increase time available for anti-parasite behaviours such as preening. Understanding such trade-offs is important for investigating the effects of provisioning on infection risk and the conservation of wildlife in human-modified habitats.This article is part of the theme issue 'Anthropogenic resource subsidies and host-parasite dynamics in wildlife'.