A parasite-induced maternal effect can reduce survival times of fleas feeding on great tit nestlings

Parents can increase their reproductive success by assisting their neonate offspring in parasite defence. In birds, parental tactics include post-hatching parental responses such as increased parental care and pre-hatching maternal effects such as the transfer of maternal antibodies via the egg. These parasite-induced parental responses are known to reduce the effects of parasites on offspring, but their costs for the parasite are largely unknown. In two separate experiments on great tits Parus major we assessed these costs for hen fleas Ceratophyllus gallinae . Half of the parents where exposed to fleas during egg-laying to induce the parental response, while control nests were left flea-free. In experiment 1 parents raised their own young and we measured the effect of combined pre- and post-hatching parental effects, while in experiment 2 a cross-foster design allowed us to assess the effects of pre-hatching maternal effects alone. In both experiments we let fleas take a blood meal on nestlings from either flea-exposed or unexposed parents. We then measured flea-feeding duration, the quantity of extracted blood, and the fleas' subsequent survival time. We found in both experiments that on the largest nestlings of a brood flea survival was significantly reduced by the parental effects, whereas on the smaller nestlings it was independent of parental effects. The pre- and post-hatching parental responses did neither affect duration nor size of a flea blood meal. These results suggest first that the pre-hatching maternal effects, i.e. the substances transferred to the nestling via the egg, have the potential to harm fleas without reducing flea feeding capacity, and second that the strength of the maternal response varies between the nestlings, either because maternal products are unequally distributed among eggs within a clutch, or because large nestlings can build up a response that enhances the effect of the maternal products.     

Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas

Blue Tit nests are often heavily infested by fleas, which feed on the incubating female and the nestlings. Depending on habitat quality, the drawing of blood by fleas reduces offspring quality, or it is compensated by an increase in food provisioning by the adults and may reduce their future reproduction. Given these fitness costs, tits are expected to have evolved behavioural responses enabling them to remove, destroy or minimize the contact with fleas. To identify these traits, we video-recorded the changes in frequency and duration of the hosts' potential anti-flea behavioural defences in nests experimentally infested with low and high flea densities. We also investigated whether flea load affected the number of male feeds delivered to incubating females, and whether the parents increased their rate of food provisioning to the nestlings equally at high flea density. Flea density significantly affected the nest sanitation and sleeping behaviour of Blue Tit females but had no significant effect on grooming. Female Blue Tits increased the frequency but decreased the duration of bouts of these behavioural traits, and hence their time-budgets, based on per hour duration of behaviour, were not significantly affected by flea density. High flea density reduced nestling weight at the early nestling stage but these costs were fully compensated by an increase in female feeding effort. Males did not increase their frequency of food provisioning to incubating females nor to nestlings in heavily infested nests. The results are discussed in the light of parasite-mediated selection on host behaviour and the reciprocal host selection on flea life-history and behavioural traits.     

Notes on the life-history of the rabbit flea Caenopsylla laptevi ibera Beaucournu & Marquez, 1987 (Siphonaptera: Ceratophyllidae) in eastern Spain

The rabbit flea Caenopsylla laptevi ibera occurs in arid environments of central and eastern Spain. Although the fleas breed during the coolest, most humid part of the year, the larvae survive and grow in sand at only 50-60% relative humidity. At 22 degrees C and 80% relative humidity eggs hatch in six days and the cocoon stage is reached 10-11 days after hatching. Female fleas emerge from pupation at about 17 days after cocoon spinning; males emerge a little later at a mean of 20 days. Adult fleas are mainly found on the host Oryctolagus cuniculus. Measurements of burrow microclimate confirmed that in south-eastern Spain burrow humidity was adequate for the development of C. I. ibera larvae over most of the year. However, breeding may be restricted for at least part of the year, as the larvae of C. I. ibera apparently cannot complete development at 25 degrees C or above. In the laboratory, fleas can enter a prolonged quiescent period while in the cocoon. This is possibly a facultative, pre-pupal diapause and the likely mechanism that accounts for the disappearance of adult fleas from the field by spring and their reappearance each autumn.     

Ectoparasitism in marsh tits: costs and functional explanations

Among hole-nesting birds, the blood-sucking hen flea is a commonparasite affecting both nestlings and parents. By adding fleasto marsh tit (Parus palustris) nests, I aimed to investigatethe effect of fleas on nestling growth rate and parental effortas well as evaluating a potential mechanism by which fleas affectnestlings (i.e., resting metabolic rate; RMR). Nestlings fromflea-infested broods were lighter than nestlings from controlbroods. This reduced growth rate was evident as soon as 3 daysafter adding extra fleas to the nest, but the reduction didnot increase after this initial drop in mass. Parents did notalter their feeding frequency in response to the manipulation;thus the small size of nestlings in manipulated nests seemsto be directly caused by the fleas. Mass-specific RMR was significantlyhigher in nestlings from flea-infested nests compared to nestlingsfrom control nests. I used the results to evaluate the suggestedmechanisms for parasite-related decrease in host growth rate.The increase in RMR and the very rapid reduction in nestlinggrowth rate after experimental addition of fleas can be explainedby an immune reaction, mainly by the innate immune system, tosubstances in the saliva of the fleas.     

Feeding performance of fleas on different host species: is phylogenetic distance between hosts important?

We asked if and how feeding performance of fleas on an auxiliary host is affected by the phylogenetic distance between this host and the principal host of a flea. We investigated the feeding of 2 flea species, Parapulex chephrenis and Xenopsylla ramesis, on a principal (Acomys cahirinus and Meriones crassus, respectively) and 8 auxiliary host species. We predicted that fleas would perform better (higher proportion of fleas would feed and take larger bloodmeals) on (a) a principal rather than an auxiliary host and (b) auxiliary hosts phylogenetically closer to a principal host. Although feeding performance of fleas differed among different hosts, we found that: (1) fleas did not always perform better on a principal host than on an auxiliary host; and (2) flea performance on an auxiliary host was not negatively correlated with phylogenetic distance of this host from the principal host. In some cases, fleas fed better on hosts that were phylogenetically distant from their principal host. We concluded that variation in flea feeding performance among host species results from interplay between (a) inherent species-specific host defence abilities, (b) inherent species-specific flea abilities to withstand host defences and (c) evolutionary tightness of association between a particular host species and a particular flea species.     

Abiotic factors influencing the ecology of wild rabbit fleas in north-eastern Spain

During 1992, the population dynamics of rabbit fleas were compared at two sites in north-eastern Spain. The sites differed mainly in terms of annual rainfall and soil type. All flea species showed seasonal cycles of abundance, although peaks in numbers occurred at different times, reflecting their specific adaptations for coping with climatic variables. Adult Spilopsyllus cuniculi (Dale) (Siphonaptera: Pulicidae) were found largely parasitizing rabbits in spring and adult Caenopsylla laptevi (Beaucournu etal.) (Siphonaptera: Ceratophyllidae) in the autumn. In contrast, monthly flea indices of Xenopsylla cunicularis (Smit) (Siphonaptera: Pulicidae) and Echidnophaga iberica (Ribeiro et al.) (Siphonaptera: Pulicidae) peaked in summer. Spilopsyllus cuniculi was present at both sites, but was less common on the drier site, where monthly mean temperature and annual rainfall approached the flea's physiological limits. By contrast, E. iberica, X. cunicularis and C. laptevi, known to be better adapted for dryness, showed the opposite patterns of abundance. Nevertheless, even these arid-adapted species took advantage of the milder and wetter spring (X. cunicularis and E. iberica) or autumn (C. laptevi) for breeding and larval development. Although environmental temperature, rainfall and soil texture will influence the microclimate of the burrows where the flea larvae develop, burrow humidity seems to be more dependent on soil characteristics and past rainfall rather than the humidity of the external air.     

The Effect of Initial Infection of <Emphasis Type="Italic">Citellophilus tesquorum altaicus</Emphasis> Ioff, 1936 (Siphonaptera: Ceratophyllidae) with <Emphasis Type="Italic">Yersinia pestis</Emphasis> on Its Alimentary Activity,Mortality, and Biofilm Formation

Alimentary activity and mortality was assessed in fleas Citellophilus tesquorum altaicus non-infected with Yersinia pestis and those with initial infection levels 50 and 100% during feeding on a non-specific host (white mice). The presence of the plague pathogen in fleas significantly stimulated their feeding activity, especially in females. No effect of infection on flea mortality was observed. At the same time, male fleas died more frequently than females.     

Effects of fleas on nest success of Arctic barnacle geese: experimentally testing the mechanism

Parasites have detrimental effects on their hosts’ fitness. Therefore, behavioural adaptations have evolved to avoid parasites or, when an individual is already in contact with a parasite, prevent or minimize infections. Such anti‐parasite behaviours can be very effective, but can also be costly for the host. Specifically, ectoparasites can elicit strong host anti‐parasite behaviours and interactions between fleas (Siphonaptera) and their hosts are one of the best studied. In altricial bird species, nest fleas can negatively affect both parent and offspring fitness components. However, knowledge on the effects of fleas on precocial bird species is scarce. Research on geese in the Canadian Arctic indicated that fleas have a negative impact on reproductive success. One possible hypothesis is that fleas may affect female incubation behaviour. Breeding females with many fleas in their nest may increase the frequency and/or duration of incubation breaks and could even totally desert their nest. The aim of our study was to 1) determine if a similar negative relationship existed between flea abundance and reproductive success in our study colony of Arctic breeding barnacle geese Branta leucopsis and 2) experimentally quantify if such effects could be explained by a negative effect of nest fleas on female behaviour. We compared host anti‐parasite and incubation behaviour between experimentally flea‐reduced and control nests using wildlife cameras and temperature loggers. We found that flea abundance was negatively associated with hatching success. We found little experimental support, however, for changes in behaviour of the breeding female as a possible mechanism to explain this effect.     

Seasonal dynamics of a flea number (Siphonaptera) on the common shrew (Sorex araneus) in the north part of the Novgorod oblast

In the course of 5-year stationary investigations of the common shrew Sorex araneus in the north part of the Novgorod oblast, 12 flea species have been recorded on this host. Among them, Palaeopsylla soricis and Doratopsilla dasycnema are specific parasites of small insectivores, including the common shrew. Hystrichopsylla talpae is a polyxenous species, parasitizing both rodents and insectivores. Other 9 flea species are not common parasites of S. araneus and apparently have come to this host from other mammal species inhabiting the forest biotopes in the area of investigation. P. soricis and D. dasycnema have similar phenology of parasitism. These fleas appear in spring (April), are present during summer and autumn and disappear in winter. During a year, the abundance of these species shows three pikes, which correspond to three generations: spring (April), summer (June-July) and autumn (September-October) generation. The first species dominates in spring (April-May) and in the autumn-winter period, while the second species predominates in summer. These two species comprise over 90% of total number of fleas collected and determine general dynamics of the flea number on the shrews; during the year the flea number has a sinusoidal increasing from spring to autumn and minimum in winter.     

On the equivalence of host local adaptation and parasite maladaptation: an experimental test

In spatiotemporally varying environments, host-parasite coevolution may lead to either host or parasite local adaptation. Using reciprocal infestations over 11 pairs of plots, we tested local adaptation in the hen flea and its main host, the great tit. Flea reproductive success (number of adults at host fledging) was lower on host individuals from the same plot compared with foreign hosts (from another plot), revealing flea local maladaptation. Host reproductive success (number of fledged young) for nests infested by foreign fleas was lower compared with the reproductive success of controls, with an intermediate success for nests infested by local fleas. This suggests host local adaptation although the absence of local adaptation could not be excluded. However, fledglings were heavier and larger when reared with foreign fleas than when reared with local fleas, which could also indicate host local maladaptation if the fitness gain in offspring size offsets the potential cost in offspring number. Our results therefore challenge the traditional view that parasite local maladaptation is equivalent to host local adaptation. The differences in fledgling morphology between nests infested with local fleas and those with foreign fleas suggest that flea origin affects host resource allocation strategy between nestling growth and defense against parasites. Therefore, determining the mechanisms that underlie these local adaptation patterns requires the identification of the relevant fitness measures and life-history trade-offs in both species.     

Distribution of fleas in rodent colonies in the Northwestern Precaspian region

Quantitative characteristics of phoresy of fleas on their rodent hosts inhabiting the sand landscapes of the northwestern Precaspian region were obtained. The structure of parasitic contact networks formed in the process was determined. The probability of a host change by fleas as the result of periodic feeding was assessed as high. The parameters of flea distribution were shown to be similar in the Northwestern Precaspian region and the Volgo-Ural sands. The ability of the flea Xenopsylla conformis to parasitize on social voles without significantly decreasing its abundance was revealed.     

Sampling fleas: the reliability of host infestation data

The use of measures of host infestation as a reliable indicator of a flea population size to be used in interspecific comparisons was considered. The abundance of fleas collected from host bodies and collected from host burrows was compared among 55 flea species, controlling for the effect of flea phylogeny. The mean number of fleas on host bodies correlated positively with the mean number of fleas in host burrows/nests both when the entire data pool was analysed and for separate subsets of data on 'fur' fleas and 'nest' fleas. This was also true for a within-host (Microtus californicus) between-flea comparison. The results of this study demonstrate that, in general, the index of host body infestation by fleas can be used reliably as an indicator of the entire population size.     

Aspects of the biology of Glaciopsyllus antarcticus (Siphonaptera: Ceratophyllidae) during the breeding season of a host (Fulmarus glacialoides)

Summary The breeding period of the Antarctic flea, Glaciopsyllus antarcticus (Smit and Dunnet), was synchronised with the breeding period of the host, Southern Fulmar (Fulmarus glacialoides Smith). Although eggs were laid in the host nest, larvae developed amongst the down (particularly on the belly) of host chicks. Larvae were blood feeders and pupated amongst the down of host chicks. The development of pupae was arrested by ambient temperatures (mean temperature of +2.5°C in January), but recommenced when pupae were warmed. Female fleas comprised 55.8% of a collection of 1988 adults. Low numbers of adult fleas were found in nests prior to host breeding and subsequent to host fledging in comparison to numbers on the host; adults are therefore presumed to overwinter on the host, remote from the nest.     

Horizontal transmission of Rickettsia felis between cat fleas, Ctenocephalides felis

Rickettsia felis is a rickettsial pathogen primarily associated with the cat flea, Ctenocephalides felis. Although laboratory studies have confirmed that R. felis is maintained by transstadial and transovarial transmission in C. felis, distinct mechanisms of horizontal transmission of R. felis among cat fleas are undefined. Based on the inefficient vertical transmission of R. felis by cat fleas and the detection of R. felis in a variety of haematophagous arthropods, we hypothesize that R. felis is horizontally transmitted between cat fleas. Towards testing this hypothesis, flea transmission of R. felis via a bloodmeal was assessed weekly for 4 weeks. Rhodamine B was used to distinguish uninfected recipient and R. felis-infected donor fleas in a rickettsial horizontal transmission bioassay, and quantitative real-time PCR assay was used to measure transmission frequency; immunofluorescence assay also confirmed transmission. Female fleas acquired R. felis infection more readily than male fleas after feeding on a R. felis-infected bloodmeal for 24 h (69.3% and 43.3%, respectively) and both Rickettsia-uninfected recipient male and female fleas became infected with R. felis after cofeeding with R. felis-infected donor fleas (3.3-40.0%). Distinct bioassays were developed to further determine that R. felis was transmitted from R. felis-infected to uninfected fleas during cofeeding and copulation. Vertical transmission of R. felis by infected fleas was not demonstrated in this study. The demonstration of horizontal transmission of R. felis between cat fleas has broad implications for the ecology of R. felis rickettsiosis.     

The inadvertent introduction into Australia of Trypanosoma nabiasi, the trypanosome of the European rabbit (Oryctolagus cuniculus), and its potential for biocontrol

Wild rabbits (Oryctolagus cuniculus) in Australia are the descendents of 24 animals from England released in 1859. We surveyed rabbits and rabbit fleas (Spilopsyllus cuniculi) in Australia for the presence of trypanosomes using parasitological and PCR-based methods. Trypanosomes were detected in blood from the European rabbits by microscopy, and PCR using trypanosome-specific small subunit ribosomal RNA (SSU rRNA) gene primers and those in rabbit fleas by PCR. This is the first record of trypanosomes from rabbits in Australia. We identified these Australian rabbit trypanosomes as Trypanosoma nabiasi, the trypanosome of the European rabbit, by comparison of morphology and SSU rRNA gene sequences of Australian and European rabbit trypanosomes. Phylogenetic analysis places T. nabiasi in a clade with rodent trypanosomes in the subgenus Herpetosoma and their common link appears to be transmission by fleas. Despite the strict host specificity of trypanosomes in this clade, phylogenies presented here suggest that they have not strictly cospeciated with their vertebrate hosts. We suggest that T. nabiasi was inadvertently introduced into Australia in the 1960s in its flea vector Spilopsyllus cuniculi, which was deliberately introduced as a potential vector of the myxoma virus. In view of the environmental and economic damage caused by rabbits in Australia and other islands, the development of a virulent or genetically modified T. nabiasi should be considered to control rabbits.     

Sex ratio in flea infrapopulations: number of fleas, host gender and host age do not have an effect

This study set out to determine whether the sex ratio of fleas collected from host bodies is a reliable indicator of sex ratio in the entire flea population. To answer this question, previously published data on 18 flea species was used and it was tested to see whether a correlation exists between the sex ratio of fleas collected from host bodies and the sex ratio of fleas collected from host burrows. Across species, the female:male ratio of fleas on hosts correlated strongly with the female:male ratio of fleas in their burrows, with the slope of the regression overlapping 1. Controlling for flea phylogeny by independent contrasts produced similar results. It was also ascertained whether a host individual is a proportional random sampler of male and female fleas and whether the sex ratio in flea infrapopulations depends on the size of infrapopulations and on the gender and age of a host. Using field data, the sex ratio in infrapopulations of 7 flea species parasitic on 4 rodent species was analysed. Populations of 3 species (Nosopsyllus iranus, Parapulex chephrenis and Xenopsylla conformis) were significantly female-biased, whereas male bias was found in 1 species (Synosternus cleopatrae). In general, the sex ratio of fleas collected from an individual rodent did not differ significantly from the sex ratio in the entire flea population. Neither host gender, and age nor number of fleas co-occurring on a host affected (a) the sex ratio in flea infrapopulations and (b) the probability of an infrapopulation to be either female- or male-biased.     

Blood-feeding of the gerbil flea Nosopsyllus laeviceps kuzenkovi (Yagubyants), vector of plague in Inner Mongolia,China

Abstract. The gerbil flea Nosopsyllus laeviceps (Wagner) (Siphonaptera: Ceratophyllidae) is an important Palaearctic vector of enzootic plague among sylvan and campestral rodents. Laboratory blood-feeding experiments with the subspecies N.l.kuzenkovi (Yagubynts) from Inner Mongolia, China, using three rodent species including the natural host Meriones unguiculatus (Milne-Edwards), demonstrated a positive relationship between per cent feeding and time allowed for feeding, particularly for female fleas. Also the bloodmeal size was proportional to sucking time and was significantly greater in females, which are larger, than in males. However, on all four strains of host tested, there was no significant correlation between the feeding success rate of the fleas and the amount of blood they imbibed. Fleas fed better on active compared to confined M.unguiculatus. These findings agree with studies of other flea species.     

Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters

We studied reproductive performance in two flea species (Parapulex chephrenis and Xenopsylla ramesis) exploiting either a principal or one of eight auxiliary host species. We predicted that fleas would produce more eggs and adult offspring when exploiting (i) a principal host than an auxiliary host and (ii) an auxiliary host phylogenetically close to a principal host than an auxiliary host phylogenetically distant from a principal host. In both flea species, egg production per female after one feeding and production of new imago after a timed period of an uninterrupted stay on a host differed significantly between host species. In general, egg and/or new imago production in fleas feeding on an auxiliary host was lower than in fleas feeding on the principal host, except for the auxiliary host that was the closest relative of the principal host. When all auxiliary host species were considered, we did not find any significant relationship between either egg or new imago production in fleas exploiting an auxiliary host and phylogenetic distance between this host and the principal host. However, when the analyses were restricted to auxiliary hosts belonging to the same family as the principal host (Muridae), new imago production (for P. chephrenis) or both egg and new imago production (for X. ramesis) in an auxiliary host decreased significantly with an increase in phylogenetic distance between the auxiliary and principal host. Our results demonstrated that a parasite achieves higher fitness in auxiliary hosts that are either the most closely related to or the most distant from its principal host. This may affect host associations of a parasite invading new areas.     

Factors affecting the cost of polygynous breeding for female Great Reed Warblers Acrocephalus arundinaceus

The male's role in feeding young and his effect on the mortality of eggs and nestlings of the Great Reed Warbler Acrocephalus arundinaceus were studied in Kahokugata, central Japan, during eight breeding seasons. Three potential costs of polygynous breeding for females were examined:(i) a reduction of male parental care per brood, (ii) an attraction of predators due to concentration of nests, and (iii) an increase of unfertilized eggs due to the reduced frequency of copulation per female. Only the first cost was found to occur:polygynous males fed their young, especially of their second broods, less frequently than monogamous ones. The lowered paternal feeding frequency, however, did not increase the mortality by starvation in second-hatched broods. This was because the warm climate emancipated females from brooding and enabled them to compensate for the deficiency of feeding by males. The paper discusses possible roles of the staggering of the time of laying among harem mates and the shift of breeding status of females caused by nesting failure, in reducing potential costs of polygynous breeding for females.     

Trait‐based and phylogenetic associations between parasites and their hosts: a case study with small mammals and fleas in the Palearctic

We investigated the associations between ecological (density, shelter structure), morphological (body mass, hair morphology) and physiological traits (basal metabolic rate) of small mammals and ecological (seasonality of reproduction, microhabitat preferences, abundance, host specificity) and morphological (presence and number of combs) traits of their flea parasites that shape host selection processes by fleas. We adapted the extended version of the three‐table ordination and linked species composition of flea assemblages of host species with traits and phylogenies of both hosts and fleas. Fleas with similar trait values, independent of phylogenetic affinities, were clustered on the same host species. Fleas possessing certain traits selected hosts possessing certain traits. Fleas belonging to the same phylogenetic lineage were found on the same host more often than expected by chance. Certain phylogenetic lineages of hosts harbored certain phylogenetic lineages of fleas. The process of host selection by fleas appeared to be determined by reciprocal relationships between host and flea traits, as well as between host and flea phylogenies. We concluded that the connection between host and flea phylogenies, coupled with the connection between host and flea traits, suggests that the species compositions of the host spectra of fleas were driven by the interaction between historical processes and traits.