Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum)

Vertebrate immune responses to ectoparasites influence pathogen transmission and host fitness costs. Few studies have characterized natural immune responses to ectoparasites and resultant fitness effects on the ectoparasite. These are critical gaps in understanding vertebrate-ectoparasite interaction, disease ecology and host-parasite co-adaptation. This study focused on an ectoparasite of birds—the northern fowl mite (NFM) (Ornithonyssus sylviarum). Based on prior evidence that chickens develop resistance to NFM, these experiments tested two hypotheses: (i) skin inflammation blocks mite access to blood, impairing development, reproduction and survival; and (ii) host immunogenetic variation influences the inflammatory response and subsequent effects on the ectoparasite. On infested hosts, histology of skin inflammation revealed increased epidermal cell number and size, immigration of leukocytes and deposition of serous exudates on the skin surface. Survival of adult mites and their offspring decreased as the area of skin inflammation increased during an infestation. Inflammation increased the distance to blood vessels beyond the length of mite mouthparts (100-160 μm) and prevented protonymphs and adults from reaching a blood source. Consequently, protonymphs could not complete development, evidenced by a significant inverse relationship between inflammation and protonymph feeding success, as well as an increasing protonymph/adult ratio. Adult females were unable to feed and reproduce, indicated by an inverse relationship between inflammation and egg production, and decreasing female/juvenile ratio. These combined impacts of host inflammation reversed NFM population growth. Intensity of inflammation was influenced by the genotype of the major histocompatibility complex (MHC), supporting previous research that linked these immunological loci with NFM resistance. Overall, these data provide a model for a mechanism of avian resistance to an ectoparasitic arthropod and the fitness costs to the parasite of that host defense.     

Ectoparasites of Chevrier's field mouse, Apodemus chevrieri, in a focus of plague in southwest China

Chevrier's field mouse, Apodemus chevrieri Milne-Edwards (Rodentia: Muridae), has been identified as the main wild reservoir of plague in the sylvatic plague focus of Yunnan Province, southwest China. Here, the ectoparasite communities of A. chevrieri and the potential medical and veterinary importance of these ectoparasites are described. A high proportion (66%) of 321 mice were found to be infested with ectoparasites. A total of 81 species of ectoparasite, including 48 species of chigger mite, 25 species of mesostigmatid (gamasid) mite, six species of flea and two species of sucking louse were collected. Most species of ectoparasite were relatively uncommon, but a few were abundant. Within this ectoparasite complex, 16 species have previously been reported to be vectors of human disease agents. Apodemus chevrieri would appear therefore to be a natural reservoir for plague bacilli and epidemic haemorrhagic fever (Korean haemorrhagic fever) viruses.     

Evidence for the 'good genes' model: association of MHC class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris

The adaptive immune system has a major impact on parasite resistance and life history strategies. Immunological defence is costly both in terms of immediate activation and long-term maintenance. The 'good genes' model predicts that males with genotypes that promote a good disease resistance have the ability to allocate more resources to reproductive effort which favours the transmission of good alleles into future generations. Our study shows a correlation between immune gene constitution (Major Histocompatibility Complex, MHC class II DRB), ectoparasite loads (ticks and bat flies) and the reproductive state in a neotropical bat, Noctilio albiventris. Infestation rates with ectoparasites were linked to specific Noal-DRB alleles, differed among roosts, increased with body size and co-varied with reproductive state particularly in males. Non-reproductive adult males were more infested with ectoparasites than reproductively active males, and they had more often an allele (Noal-DRB*02) associated with a higher tick infestation than reproductively active males or subadults. We conclude that the individual immune gene constitution affects ectoparasite susceptibility, and contributes to fitness relevant trade-offs in male N. albiventris as suggested by the 'good genes' model.     

Immunoparasitology in Avian Species

There has been no work on the immunological response of birdsto helminth infections since the late 1960s, an area of investigationthat has been too long ignored. Similarly, studies of arthropod-mediatedresponses in birds are lacking except for a few scattered investigations.Recently, a serum antibody response has been seen against onearthropod, the northern fowl mite. The appearance of antibodiesrecognizing an 8–10 kilodalton mite antigen seems to correlatewith a reduction in the mite population on infested chickens.Most of the studies on parasite immunity in avian species havecentered on the economically important Eimeria species, protozoanparasites that infect the intestine of chickens and turkeys.These investigations encompass wide areas of interest includingthe effect of immunity on parasite invasion, development ofT-cell proliferation assays and T-cell clones, inhibition ofparasite penetration and development by hybridoma antibody treatment,production of genetically engineered Eimeria antigens used inbird immunization studies, and studies using inbred or congeniclines of birds to determine what effect the major histocompatibilitycomplex has on parasite immunity. From these efforts it hasbeen learned that not only is the immunity species-specific,but also depending on where in the intestine the parasite invades,penetration is either not affected or inhibited by as much as50%. The T-cell proliferation assays suggest that this specificitymay be due to a species-specific T-cell response. Immunizationstudies using a genetically engineered antigen have indicatedthat at least partial protection against one species of Eimeriais possible. Studies done with the inbred congenic lines ofbirds have shown that the genetic makeup of the bird is importantin how it responds to either a natural infection or to immunizationwith a genetically engineered antigen. Clearly, these resultsshow not only the complexity of the bird response to parasiteinfection, but also the amount of work still undone.     

Horizontal and vertical ectoparasite transmission of three species of Malophaga, and individual variation in european bee-eaters (Merops apiaster)

Dispersal of avian ectoparasites can occur through either vertical transmission from adult birds to their offspring in the nest or through horizontal transmission between adult birds or through phoresy. In this study, we investigated the importance of the 2 main transmission modes in the colonial European bee-eater and examined whether individual differences in ectoparasite intensity exist in relation to age, sex, and morphological features of the birds. The intensity of 3 chewing lice species was investigated. Almost all adult bee-eaters (98.3%, n = 176) were infested with 1 of the 3 ectoparasite species, whereas only 10.8% (n = 167) of all chicks were infested. Meropoecus meropis was the most frequent ectoparasite species on adult bee-eaters (prevalence 94.3%), whereas Meromenopon meropis was the most common species on chicks (prevalence 9.6%). Our results suggest that chewing lice are mainly horizontally transmitted among adult bee-eaters and mainly among pair members, whereas vertical transmission between parents and nestlings is less frequent. These conclusions were supported by a relation in ectoparasite intensity of pair members and a parasite removal experiment. Ectoparasite intensity was in general low in nestlings and did not correlate with ectoparasite intensity of their parents. Host age, sex, weight, and other morphological features did not explain variation in chewing lice infestation.     

Influence of bill and foot morphology on the ectoparasites of barn owls

Preening is the principle behavioral defense used by birds to combat ectoparasites. Most birds have a small overhang at the tip of their bills that is used to shear through the tough cuticle of ectoparasitic arthropods, making preening much more efficient. Birds may also scratch with their feet to defend against ectoparasites. This is particularly important for removing ectoparasites on the head, which birds cannot preen. Scratching may be enhanced by the comb-like serrations that are found on the claws of birds in many avian families. We examined the prevalence and intensity of ectoparasites of barn owls (Tyto alba pratincola) in southern Idaho in relation to bill hook length and morphological characteristics of the pectinate claw. The barn owls in our study were infested with 3 species of lice (Phthiraptera: Ischnocera): Colpocephalum turbinatum , Kurodaia subpachygaster, and Strigiphilus aitkeni . Bill hook length was associated with the prevalence of these lice. Owls with longer hooks were more likely to be infested with lice. Conventional wisdom suggests that the bill morphology of raptors has been shaped by selection for efficient foraging; our data suggest that hook morphology may also play a role in ectoparasite defense. The number of teeth on the pectinate claw was also associated with the prevalence of lice. Owls that had claws with more teeth were less likely to be infested with lice, which suggests that larger pectinate claws may offer relatively more protection against ectoparasitic lice. Experiments that manipulate the bill hook and pectinate claw are needed to confirm whether these host characters are involved in ectoparasite defense. Finally, we recovered mammalian ectoparasites from 4 barn owls. We recovered species of mammalian lice (Phthiraptera:Anoplura) and fleas (Siphonaptera) that are commonly found on microtine rodents. The owls probably acquired these parasites from recently eaten prey. This represents 1 of the few documented cases of parasites "straggling" from prey to predator.     

New hosts for the mite Ornithonyssus bursa in Argentina

The mite Ornithonyssus bursa (Berlese) (Mesostigmata: Macronyssidae) is considered a poultry pest causing important infestations in chickens and it is considered a potential vector of arbovirus. Despite being considered a common parasite in wild birds, there is scarce published information about its potential hosts and effects on them. Here we present new bird hosts for O. bursa, assess the presence of Alphavirus, Flavivirus and Bunyavirus in mites from three host species, and discuss its potential impact on wild bird populations. We found O. bursa infecting five raptor and six passerine wild bird species. For nine of these species, this is the first record of infection by O. bursa. Although all analysed mites were negative for the examined arboviruses, the small sample size of mites does not allow further conclusions at the present moment. Because of the general nature of this ectoparasite, its presence in migratory long dispersal and endangered bird species, and the seropositivity for arboviruses in some of the species studied here, we consider it critical to assess the role of O. bursa and other ectoparasites as vectors and reservoirs of pathogens and as potential deleterious agents in wild bird populations.     

Host-ectoparasite associations; the role of host traits,season and habitat on parasitism interactions of the rodents of northeastern Iran

Rodents play a significant role as reservoirs of zoonotic diseases. Nevertheless, in general their ectoparasite assemblage and host-ectoparasite associations are poorly known. This study intended to provide new insights into the relationships between ectoparasites and rodents in northeastern Iran. Rodents were captured using live traps during the years 2016–2020, and their ectoparasites were collected. Parasitological indices such as infestation rate, prevalence and mean intensity of infestation were analyzed. A total of 284 rodents, belonging to 17 species, were trapped and found to be infested by 178 ectoparasites from five orders Siphonaptera, Phthiraptera, Ixodida, Mesostigmata and Trombidiformes. The overall infestation rate was 50.3%. The flea Nosopsyllus fasciatus and the louse Polyplax asiatica dominated among all fleas and lice, respectively. Haemaphysalis punctata and Haemolaelaps sp. were recorded as the most abundant tick and mite, respectively. Nosopsyllus fasciatus exhibited low and Polyplax asiatica moderate host specificity. Approximately 64.2% of ectoparasites shared more than one host, and others were singletons. Seasonal fluctuations were found in the occurrence of ectoparasite; fleas and lice were more abundant in spring and winter, respectively. Ticks demonstrated high abundance in spring and summer and mites were more common in autumn. The overall prevalence of ectoparasite on male rodents was greater than that on females (56.4% vs. 44.4%), while similar mean intensities were detected for both sexes. This study extends the knowledge on the distribution, seasonality and host choice of four main groups of ectoparasites in association with rodents. Further studies are needed to provide deep insight into how relationships and interactions between ectoparasite and rodents are formed, and how they can be applied in epidemiology.     

Ectoparasites in an urban population of big brown bats (Eptesicus fuscus) in Colorado

Ectoparasites of an urban population of big brown bats (Eptesicus fuscus) in Fort Collins, Colorado, were investigated during summers 2002, 2003, and 2004. Eleven species of ectoparasites were found (the macronyssid mite Steatonyssus occidentalis, the wing mite Spinturnix bakeri, the myobiid mites Acanthophthirius caudata and Pteracarus aculeus, the chirodiscid mite Alabidocarpus eptesicus, the demodicid mite Demodex sp., the chigger Leptotrombidium myotis, the soft tick Carios kelleyi, the batfly Basilia forcipata, the batbug Cimex pilosellus, and the flea Myodopsylla borealis). Five species were analyzed by prevalence and intensity (C. pilosellus, M. borealis, L. myotis, S. bakeri, and S. occidentalis) based on 2161 counts of 1702 marked individual bats over the 3 summer study periods. We investigated 4 factors potentially influencing prevalence and intensity: age class of the host, reproductive status of adult female hosts, roosts in which the hosts were found, and abiotic conditions during the year sampled. The macronyssid mite, S. occidentalis, was the most prevalent and abundant ectoparasite. Adult big brown bats had more ectoparasites than volant juveniles for most of the species analyzed. In a sample of known age bats at 1 large colony, bats of 4 yr of age or greater had higher ectoparasite loads of S. occidentalis and S. bakeri when compared with younger bats. Lactating female bats had the highest prevalence and intensities of most ectoparasites. Annual differences in ectoparasite prevalence and intensity were related to temperature and humidity, which can affect the nidicolous species of ectoparasites. Residents of 2 buildings sprayed insecticides in response to Cimex sp., and this appeared to reduce ectoparasitism of S. occidentalis and C. pilosellus present at these buildings. Intensity of S. occidentalis had no influence on annual survival of big brown bats.     

Seasonal variation of infestation by ectoparasitic chigger mite larvae (Acarina: Trombiculidae) on resident and migratory birds in coffee agroecosystems of Chiapas, Mexico

Parasitism is not well documented for birds found in tropical habitats. Long-distance migratory birds may face additional risks to an already hazardous journey when infected. This study explores the ecology of an ectoparasite infestation in Chiapas, Mexico. During a mist-netting project in 2 different coffee management systems, chigger mites (Acarina: Trombiculidae), ectoparasitic during the larval stage, were found on both resident and migratory birds. Using a rapid assessment protocol, it was observed that 17 of 26 species of long-distance migrants and 33 of 71 resident species had at least 1 infested individual. Infestation prevalences were unexpectedly high on some long-distance migrants, as high as 0.73 for Swainson's thrush (Catharus ustulatus), a value on par with heavily infested resident species. Prevalence was highest during winter sampling: 0.18 overall, 0.16 of migrants, and 0.23 of residents. Prevalence was 0.14 for resident birds during the summer breeding season. Mean abundance and mean intensity of infestation are reported for 97 species captured and inspected during the course of this study. In this region, chigger mite larvae are relatively common on birds and their abundance varies seasonally. High prevalence for some migratory birds suggests that more research and monitoring of ectoparasites are needed, especially in light of emerging diseases.     

Ectoparasites on reintroduced roe deer Capreolus capreolus in Israel

The ectoparasite fauna of reintroduced roe deer (Capreolus capreolus) was surveyed in a Mediterranean forest in Israel. Ectoparasites were collected from four female hand-reared deer during 2004 and 2005. Seasonality, predilection sites of infestation, and the apparent effect of the parasites are presented. This is the first study of roe deer parasites in the East Mediterranean. The ectoparasite fauna included three hippoboscid fly (Lipoptena capreoli, Hippobosca equina, and Hippobosca longipennis), four tick (Rhipicephalus sanguineus, Rhipicephalus turanicus, Rhipicephalus kohlsi, and Hyalomma marginatum), and one unidentified trombiculid mite species. For most of these ectoparasites, this is the first record on roe deer. All ectoparasite species were documented in Israel prior to the reintroduction program; exotic ectoparasites were not detected.     

Comprehensive investigation of ectoparasite community and abundance across life history stages of avian host

Fitness consequences of ectoparasitism are expressed over the lifetime of their hosts in relation to variation in composition and abundance of the entire ectoparasite community and across all host life history stages. However, most empirical studies have focused on parasite species-specific effects and only during some life history stages. We conducted a systematic, year-long survey of an ectoparasite community in a wild population of house finches Carpodacus mexicanus Müller in south-western Arizona, with a specific focus on ecological and behavioral correlates of ectoparasite prevalence and abundance. We investigated five ectoparasite species: two feather mite genera – both novel for house finches – Strelkoviacarus (Analgidae) and Dermoglyphus (Dermoglyphidae), the nest mite Pellonyssus reedi (Macronyssidae), and the lice Menacanthus alaudae (Menoponidae) and Ricinus microcephalus (Ricinidae). Mite P. reedi and louse Menacanthus alaudae abundance peaked during host breeding season, especially in older birds, whereas feather mite abundance peaked during molt. Overall, breeding birds had more P. reedi than non-breeders, molting males had greater abundance of feather mites than molting females and non-molting males, and young males had more feather mites than older males. We discuss these results in relation to natural history of ectoparasites under study and suggest that ectoparasites might synchronize their life cycles to those of their hosts. Pronounced differences in relative abundance of ectoparasite species among host's life history stages have important implications for evolution of parasite-specific host defenses.     

Ectoparasites on small mammals in Iceland: Origin and population characteristics of a species-poor insular community

The Icelandic small mammal fauna is depauperated as is the associated ectoparasite fauna. Three small mammal species occur, viz. Apodemus sylvaticus L., Mus musculus L., and Rattus norvegicus Berk. ( R. rattus is probably not a regular member). The mice supposedly came to the island by settlers from the 10th century and onwards.
Apodemus and Mus from five localities altogether had seven ectoparasite species, five mites and two fleas. All species occurred on Apodemus whereas Mus was infested by four. Compared with the numbers of ectoparasite species recorded in similar studies in the Nordic countries, there are conspicuously few species in Iceland. Further, Apodemus had an overall higher infestation frequency than Mus (90% and 30%, respectively) and a higher total density of ectoparasites (3.3–20.3 and 0.5 inds/host, respectively). The density figures were high compared with those for mainland Apodemus . Especially the mite Laelaps agilis C. L. Koch and the flea Ctenophthalmus agyrtes (Heller) were common on Icelandic Apodemus . Reduced competition among parasites and/or low predator pressure on small mammals may explain the density figures obtained.
The ectoparasite species compositions on small mammals in Scandinavia and Iceland have many features in common that renders it probable that Apodemus originate from Scandinavia.     

Structure and Seasonal Dynamics of the Ectoparasite Community of the Pygmy Shrew <Emphasis Type="Italic">Sorex minutus</Emphasis> in the Ilmen-Volkhov Lowland

The species composition and seasonal dynamics of ectoparasites of the pygmy shrew Sorex minutus L., 1756 were studied in coniferous and mixed forests of the Ilmen-Volkhov Lowland (Novgorod Province of Russia) in 1999–2003. Examination of 265 specimens of the pygmy shrew revealed 670 specimens of ectoparasites that belonged to 13 species: 8 species of fleas, 2 species of ixodid ticks, 1 species of gamasid mites, and 2 species of myobiid mites. In total, 55.8% of shrew specimens were infested with ectoparasites. No more than 4 species of ectoparasites were found simultaneously on one host, and most of the examined shrews (64.8%) were infested with only 1 ectoparasite species. The pygmy shrew had lower infestation intensity and species diversity of acarines and fleas as compared with those of the common shrew Sorex araneus L., 1758 and the bank vole Myodes glareolus (Schreber, 1780) (13 vs. 23 and 29 species, respectively). Unlike these two other hosts, the prevalent ectoparasite of the pygmy shrew was the tick Ixodes trianguliceps Birula, 1895.     

Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study

Nests of cavity‐nesting birds usually harbor some species of haematophagous ectoparasites that feed on the incubating adults and nestlings. Given the negative impact of ectoparasites on nestlings there will be selection on hosts to reduce parasite infestations through behavioural means. We have experimentally reduced the abundance of all ectoparasites in nests of pied flycatchers Ficedula hypoleuca to explore both whether there are changes in the frequency and duration of putative anti‐parasite behaviours by tending adults, as well as whether such anti‐parasite behaviours are able to compensate for the deleterious effects that parasites may have on nestlings. Heat treatment of nests substantially decreased the density of ectoparasites, and thereby positively affected nestling growth. The frequency and intensity of female grooming and nest sanitation behaviours during the incubation and nestling periods decreased as a consequence of the experimental reduction of ectoparasite infestation. Although nestlings begged more intensely in infested nests, the experiment had no significant effect on parental provisioning effort. Reduction of parasites resulted in larger nestlings shortly before fledging and increased fledging success. This study shows a clear effect of a complete natural nest ectoparasite fauna on parental behaviour at the nest and nestling growth in a cavity‐nesting bird. Although ectoparasites induce anti‐parasite behaviours in females, these behaviours are not able to fully remove parasite's deleterious effects on nestling growth and survival.     

中国云南洱海周边褐家鼠的体表寄生虫群落组成

褐家鼠Rattus norvegicus可能是云南省部分鼠疫流行区的储存宿主之一, 其体表的某些寄生虫种类可能是人类疾病的传播媒介。为了解洱海周边地带褐家鼠的体表寄生虫群落, 并对其医学和兽医学的重要性进行描述。用U检验和相关分析的统计方法对2003-2004年采自云南洱海（中国滇西北著名的淡水湖泊）周边地区的431头褐家鼠的体表寄生虫群落进行了研究。用构成比（C）, 侵染率(P)和平均丰富度(A)反映体表寄生虫的流行和密度状况。调查点位于我国11大鼠疫自然疫源地之一, 此地也是我国恙虫病和流行性出血热的流行地区。结果表明: 431头褐家鼠中307头寄生有体表寄生虫, 侵染率为71%。采集到的体表寄生虫有47种, 包括23种恙螨、16种革螨、6种蚤和2种吸虱, 其中16种以前已经被证明是人类疾病的媒介。结果提示褐家鼠的体表寄生虫物种多样性高。     

Marek's disease and major histocompatibility complex haplotypes in chickens selected for high or low antibody response

Sublines of chickens differing in genotypes at the major histocompatibility complex (MHC) were developed from lines selected for high (HA) and low (LA) antibody response to sheep erythrocytes. To evaluate the influence of MHC genotypes in diverse background genomes on resistance to Marek's disease, chicks with MHC genotypes B13B13, B13B21 and B21B21 from both background genomes were exposed naturally commencing at 1 day of age. Individuals which died up to 120 days of age were autopsied to determine cause of death. Mortality due to Marek's disease was greater for HA than LA chickens and greater for males than females. Interactions of MHC genotypes with background genome and with sex suggest a complex picture of the influence of MHC genotypes. A heterozygous advantage for resistance to Marek's disease was noted, as would be predicted by genetic theory concerning maintenance of polymorphism at the MHC.     

Chicken major histocompatibility complex congenic lines differ in the percentages of lymphocytes bearing CD4 and CD8 antigens

In the experiments to be described two congenic inbred lines CB and CC and two recombinant lines CB.R1 and CC.R1 were used. All four lines differ only in regard to the major histocompatibility complex (MHC). To determine the percentage distributions of the two cell subsets in peripheral blood lymphocytes (PBL) in these lines, monoclonal antibodies to these two antigens were used. By FACScan there were more CD4+PBL in CB and CB.R1 lines (share B-F/B-L region, controlling class I/class II antigens with line CB) than CC and CC.R1, while the reverse was true with CD8+ subsets. There were more CD8+ PBL in the CC and CC.R1 lines and less in CB and CB.R1 lines. The ratio of CD4+ to CD8+ in CB chickens was 3.4 +/- 0.2 and in CC chickens 1.6 +/- 0.1.     

Genetic mapping of the major histocompatibility complex in the zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>)

Genes of the major histocompatibility complex (MHC) have received much attention in immunology, genetics, and ecology because they are highly polymorphic and play important roles in parasite resistance and mate choice. Until recently, the MHC of passerine birds was not well-described. However, the genome sequencing of the zebra finch (Taeniopygia guttata) has partially redressed this gap in our knowledge of avian MHC genes. Here, we contribute further to the understanding of the zebra finch MHC organization by mapping SNPs within or close to known MHC genes in the zebra finch genome. MHC class I and IIB genes were both mapped to zebra finch chromosome 16, and there was no evidence that MHC class I genes are located on chromosome 22 (as suggested by the genome assembly). We confirm the location in the MHC region on chromosome 16 for several other genes (BRD2, FLOT1, TRIM7.2, GNB2L1, and CSNK2B). Two of these (CSNK2B and FLOT1) have not previously been mapped in any other bird species. In line with previous results, we also find that orthologs to the immune-related genes B-NK and CLEC2D, which are part of the MHC region in chicken, are situated on zebra finch chromosome Z and not among other MHC genes in the zebra finch.