Anti-parasite Behaviour Research Articles

How Birds Combat Ectoparasites

Birds are plagued by an impressive diversity of ectoparasites, ranging from feather-feeding lice, to feather- degrading bacteria. Many of these ectoparasites have severe negative effects on host fitness. It is therefore not surprising that selection on birds has favored a variety of possible adaptations for dealing with ectoparasites. The functional signifi- cance of some of these defenses has been well documented. Others have barely been studied, much less tested rigorously. In this article we review the evidence - or lack thereof - for many of the purported mechanisms birds have for dealing with ectoparasites. We concentrate on features of the plumage and its components, as well as anti-parasite behaviors. In some cases, we present original data from our own recent work. We make recommendations for future studies that could im- prove our understanding of this poorly known aspect of avian biology.

Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnowsPimephales promelas

Fathead minnowsPimephales promelasexposed to cercariae of the trematodeOrnithodiplostomumsp. incurred a significant mass loss 17 days after exposure to 20 or 120 cercariae. Parasite‐naïveP. promelasshowed no evidence of innate recognition or avoidance of cercariae. After a single exposure to cercariae, however, fish responded to chemical and visual cues of dead (thawed) cercariae with a reduction in activity. Encounter rate with cercariae, and hence infection rate, increased with fish activity. The data indicated that experiencedP. promelasassociated parasitism risk with novel chemical and visual cues that later triggered avoidance behaviour. Parallels and interactions between antiparasite behaviour and antipredator behaviour open new avenues for behavioural ecological research in risk‐sensitive decision‐making.

Helper contributions to antiparasite behavior in the cooperatively breeding bell miner

Cooperatively breeding bell miners (Manorina melanophrys) have numerous male helpers assisting at multiple nests. Helpers are often related to the brood they aid, consistent with kin selection. However, there are also unrelated helpers for which other direct fitness benefits are likely to accrue. Bell miner nestlings can become infested by the larvae of a parasitic fly (Passeromyia indecora), which reduce growth and can be fatal. We investigated the amount of time that breeding pairs and helpers closely inspected nests and preened nestlings, behaviors apparently directed at detecting and removing parasites, a form of helping previously unstudied in a cooperative bird. Female breeders provided the greatest antiparasite effort, with breeding males and helpers not differing in effort regardless of their relatedness to the breeding female or brood. We also experimentally infested nests with nonparasitic flies and larvae. All individuals removed the introduced “parasites” if and when they encountered them. Compared with control sessions, inspection effort increased for all birds immediately after the experimental infestations, but only for a short, 5-min period. Further, we detected no changes in helper antiparasite behaviors after the temporary experimental removal of either breeding females or males. Such consistent helping behavior, independent of relatedness and potential audience effects, suggests that antiparasite behavior in bell miners is not particularly kin directed or operating as a signal of helper quality. Our results instead suggest that helper antiparasite effort appears to represent adaptive investment in the welfare of the brood, consistent with direct fitness benefits from group augmentation.

Plasticity in antiparasite behaviours and its suggested role in invasion biology

Plasticity in antiparasite behaviours and its suggested role in invasion biology

Nest desertion by a cowbird host: an antiparasite behavior or a response to egg loss?

Natural selection can favor songbirds that desert nests containing eggs of the parasitic brown-headed cowbird (Molothrus ater). However, the high variability in desertion of parasitized nests within species is perplexing in light of the typically high costs of parasitism. Because nest desertion can also be a response to partial clutch predation, we first asked if Bell’s vireos (Vireo bellii) deserted nests in response to the presence of cowbird eggs (antiparasite response hypothesis) or to egg removal by predators and female cowbirds (egg predation hypothesis). Second, we asked whether variation in nest desertion was due to intrinsic differences among individuals or to variation in nest contents. We monitored a large number of nests (n ¼ 494) and performed a clutch manipulation experiment to test these hypotheses. The number of vireo eggs that remained in a nest was a strong predictor of desertion both within and among pairs. Neither the presence of a single cowbird egg, which leads to nest failure for this host, nor the number of cowbird eggs received in a vireo nest influenced nest desertion. Furthermore, vireos did not desert experimental nests when we immediately exchanged cowbird eggs for vireo eggs but deserted if we removed vireo eggs and replaced them with cowbird eggs the following morning. Desertion of parasitized nests by Bell’s vireos can be almost entirely explained as a response to partial or complete clutch loss and does not appear to have been altered by selection from brood parasitism. Key words: Bell’s vireo, brown-headed cowbird, egg predation, evolutionary lag, host‐parasite coevolution, Molothrus ater, Vireo bellii. [Behav Ecol]

Selective Defecation and Selective Foraging: Antiparasite Behavior in Wild Ungulates?

AbstractSelective defecation and selective foraging are two potential antiparasite behaviors used by grazing ungulates to reduce infection by fecal–oral transmitted parasites. While there is some evidence that domestic species use these strategies, less is known about the occurrence and efficacy of these behaviors in wild ungulates. In this study, I examined whether wild antelope use selective defecation and selective foraging strategies to reduce exposure to gastrointestinal nematode parasites. By quantifying parasite levels in the environment in relation to the defecation patterns of three species, dik‐dik (Madoqua kirkii), Grant's gazelle (Gazella granti), and impala (Aepyceros melampus), I found that nematode larval concentrations in pasture were higher in the vicinity of clusters of feces (dung middens) compared to single fecal pellet groups or dung‐free areas. In addition, experimental feeding trials in free‐ranging dik‐dik showed that individuals selectively avoided feeding near concentrations of feces. Given that increased parasite contamination was found in the immediate vicinity of fecal clusters, fecal avoidance could help reduce host consumption of parasites and may therefore be an effective antiparasite behavior for certain species. On the other hand, while the concentration of parasite larvae in the vicinity of middens coupled with host avoidance of these areas during grazing could reduce host contact with parasites, results showing a positive correlation between the number of middens in a habitat and larval abundance at control sites suggest that dung middens might increase and not decrease overall host exposure to parasites. If this is the case, dung midden formation may not be a viable antiparasite strategy.

Use of California bay foliage by wood rats for possible fumigation of nest-borne ectoparasites

Studies were conducted to test the hypothesis that dusky-footed wood rats (Neotoma fuscipes) place bay leaves (Umbellularia californica) on or near the sleeping nest in their stickhouses, with the result that the leaves act as a fumigant against nest-borne ectoparasites. Although many stickhouses were found to contain bay, oak, and toyon leaves, only bay was found significantly more often near the nest than away from the nest. Bay leaves were nibbled in a fashion consistent with the release of fumigating volatiles. Oak leaves, a known food staple, were nibbled in a fashion more consistent with eating. Analysis of the density of ectoparasites in samples of sleeping nest material showed few parasites in most nests, but heavy infestations in a few nests revealed the potential for large numbers of nest-borne ectoparasites. Samples of 1 g of whole and torn leaves of bay, toyon, and oak were incubated with flea larvae in mason jars for 72 h. Torn leaves (to simulate nibbling effects) of bay significantly reduced larval survival to 26% compared to 87–94% survival of larvae incubated with torn oak and toyon leaves. These findings provide evidence that dusky-footed wood rats place bay foliage around the sleeping nest with the effect of reducing their exposure to nest-borne ectoparasites. Key words: antiparasite behavior, ectoparasites, Neotoma fuscipes, nest fumigation, plant volatiles, Umbellularia californica, wood rats. [Behav Ecol 13:381–385 (2002)]

Roost Site Selection of Great Horned Owls in Relation to Black Fly Activity: An Anti-Parasite Behavior?

Abstract We document a shift in roosting behavior of Great Horned Owls (Bubo virginianus) from winter and late spring to summer. During summer, Great Horned Owls roosted near the ground or exposed on open ground, whereas they chose concealed perches at mid-canopy level for the rest of the year as typical for forest owls. This shift of roosting behavior coincided with the emergence of ornithophilic black flies, which transmit avian malaria (Leucocytozoon spp.). The shift in roosting behavior was consistent with measurements of parasite exposure at different habitat positions. Black fly activity was highest at mid-canopy level, and almost no black flies were active on open ground. Ground-roosting was not caused by poorly developed flying capability of juveniles, because solitarily-roosting adult owls showed the same behavioral shift in a second year of study. Black flies and avian malaria are widely distributed, and the effect of the vertical distribution of these parasites in forests on roosting, nesting, and foraging of sylvatic birds deserves further study.

Roost Site Selection of Great Horned Owls in Relation to Black Fly Activity: An Anti-Parasite Behavior?

Roost Site Selection of Great Horned Owls in Relation to Black Fly Activity: An Anti-Parasite Behavior?

Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world

On Wicken Fen and nearby watercourses eastern England, parasitism by cuckoos, Cuculus canorus, declined from 26 and 16 of reed warbler (Acrocephalus scirpaceus) nests in 1985 and 1986, respectively...

Intraspecific nest parasitism and anti-parasite behavior in the grey starling,Sturnus cineraceus

I studied intraspecific nest parasitism in the grey starlingSturnus cineraceus in 1992 and 1993. The population in this study consisted of 290 nests (157 nests in 1992 and 133 nests in 1993) in which the clutches were completed before May 10 in the year studied. Twenty-nine nests in 1992 and 32 nests in 1993 contained at least 1 parasitic egg. Hatching success per nest of parasitized nests was slightly higher than that of non-parasitized nests. However, fledging success per nest of parasitized nests was significantly lower than that of non-parasitized nests. Thus parasitism appeared to reduce the reproductive success of hosts. Hosts exhibited a few behaviors that minimized the potential cost of brood parasitism. These behaviors included throwing out the parasitic egg and nest guarding. Hosts threw out parasitic eggs before the onset of laying, but they never did so to parasitic eggs laid after that period. The nest guarding level was low during the hosts’ laying periods, and one observed nest was parasitized during this time. Thus, nest-guarding behavior was not effective as an anti-parasite behavior. Grey starlings do not appear to adopt strategies effective in reducing parasitism.

Conflict between antipredator and antiparasite behaviour in larval damselflies.

Larval damselflies resist infestation by parasitic larval mites by exhibiting behaviours such as grooming, crawling, swimming, and striking at host-seeking mites. Larval damselflies are known to increase time spent in these behaviours in the presence of mites but reduce time spent in these behaviours in the presence of fish predators. The presence of both fish and larval mites presents an obvious conflict: a larval damselfly may actively avoid parasitism by mites, thus increasing its risk of predation, or it may reduce its activity when fish are present, thus increasing its risk of parasitism. We analysed the behaviour of larval Ischnura verticalis in an experiment where we crossed presence and absence of fish with presence and absence of larval mites. Presence of mites induced a large increase in activity of larval I. verticalis but fish had no effect and there were no interpretable interactions between effects of mites and fish. Subsequent experiments indicated that larval I. verticalis in the presence of both mites and fish were more likely to be attacked and killed by fish than those exposed only to fish. The high activity level of I. verticalis larvae in the presence of both fish and mites may suggest that costs of parasitism are high, or that under field conditions it is rare for larvae to be in the immediate presence of both fish predators and potentially parasitic mites.

Of great tits and fleas: sleep baby sleep . . .

Many bird parasites reduce their hosts' fitness and, as a consequence, anti-parasite behaviour such as preening and nest sanitation has evolved. These activities are time consuming and, during the day, compete directly with time devoted to foraging and food provisioning to nestlings. Moreover, infested hosts may have to allocate extra time to foraging in order to compensate for the energy loss that ectoparasites impose on the nestlings and parents. Alternatively, brooding females could, at the expense of sleeping, allocate more time to preening and nest sanitation at night. If sleeping has a short-term restoring function, one may then expect a reduction in feeding efficiency of sleep-deprived females. In this study, the effect of a haematophagous ectoparasite, the hen flea, on the activity budgets of breeding female great tits during the day and at night was investigated experimentally. Time allocated to nest sanitation increased only slightly from 0.6 % of daytime in ectoparasite-free nests to 2.8% of daytime in infested nests, thus demonstrating the higher priority given to food provisioning than parasite control. Females in infested nests reduced their sleeping time significantly (73.5% of night-time in parasite-free nests versus 48.1% in infested nests). The time freed from the reduction of sleeping time was mainly used for nest sanitation (8.3% of night-time in parasite-free nests versus 27.1% in infested nests). Despite this strong decrease in sleeping time, there was no effect of ectoparasites on the females' rate of food provisioning to nestlings.

Nest desertion by blue-gray gnatcatchers in association with brown-headed cowbird parasitism

The blue-gray gnatcatcher,Polioptila caerulea, is one of the smallest regular hosts of the brown-headed cowbird,Molothrus ater. Gnatcatchers typically raise none of their own young when parasitized, yet anti-parasite behaviours have not been reported. A blue-gray gnatcatcher population in which pairs often desert nests when parasitized by cowbirds was studied to examine the success of a desertion response and to determine factors that stimulate desertion. Of 83 gnatcatcher nests, 76% were parasitized; of nests parasitized during the egg-laying stage, 45% were deserted. Desertion occurred independently of the timing of the parasitism event during the breeding season and the number of cowbird eggs laid per nest. All cowbird eggs laid after the completion of the gnatcatcher's egg-laying stage were accepted. Parasitism rates were lower late in the breeding season, and nesting success of unparasitized nests was higher. Pairs that deserted often obtained cowbird-free clutches, allowing them to raise gnatcatcher young. Nest desertion appears to be a means of avoiding parasitism and increasing fitness. The nest desertion response was inconsistent, but it cannot be explained by the adaptiveness of acceptance or by the possibility that blue-gray gnatcatchers are in transition between being acceptors or rejectors of cowbird parasitism. Nest desertion by blue-gray gnatcatchers appears to be a generalized response to a disturbance at the nest induced by cowbirds. The cue that elicits the desertion response remains unclear.

Intraspecific nest parasitism in the swallow Hirundo rustica: the importance of neighbors

Intraspecific nest parasitism in the swallow Hirundo rustica involves several parasite and anti-parasite tactics. Neighboring swallows breed asynchronously, perhaps because neighboring nests with overlapping egg-laying periods have higher frequency of intraspecific nest parasitims than neighboring nests with no such overlap. Since nest guarding prevents nest parasitism, the effect of nest guarding was removed by putting up old swallow nests. Such experimental nests were parasitized by swallows more often when the nests contained eggs, than when empty, and when the nests were far away from, rather than close to, an active neighboring nest. Close experimental nests with eggs were, however, parasitized less frequently if asynchronous (non-overlapping egg-laying periods), rather than synchronous, to active neighboring nests. Aggressive anti-parasite behavior of nest owners was determined from responses towards female intruders. Responses were more often aggressive before and especially during egg laying than during incubation. Nest owners also behaved aggressively more often when the intruder approached close to as compared to at some distance from their nest. Focal pairs behaved aggressively more often towards closely approaching intruders during the incubation period than towards distantly approaching intruders during the egg-laying period. Swallows reduce the frequency of intraspecific nest parasitism by nesting asynchronously with and close to a neighboring nest. Aggression by neighbors may reduce the success of potential parasitic swallows.

Intraspecific nest parasitism and anti-parasite behaviour in swallows, Hirundo rustica

Intraspecific nest parasitism was relatively frequent (overall 16·5% of 261 nests) among swallows, Hirundo rustica, during four consecutive years. Parasite eggs were laid by neighbouring females. Those females, but not their mates, visited strange nests during the egg-laying period of the female owner. Parasite eggs were laid during and immediately after the egg-laying period of the parasitized female. Parasitism tended to be frequent in years with large populations and was more frequent in large colonies (of 17–32 pairs) than in groups of 1–4 pairs. The same females were parasites more frequently than expected during both first and second broods. Parasite females had more fledglings per breeding attempt than either non-parasite hosts or females not being parasitized. Females guarded their nest sites less during egg laying than during pre-laying and incubation because of their large feeding demands when producing eggs. Nest guarding rates of colonial females were significantly higher during and following egg laying than those of solitarily nesting swallows. Parasitized females had lower nest guarding rates than other females. Parasite eggs were usually evicted by female nest owners during pre-laying, but never during egg laying and incubation.