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The manipulation of host organisms by their parasites has captured the attention of ecologists, parasitologists, and the public. However, our knowledge of parasite behavior independent of a host is limited despite the far-reaching implications of parasite behavior. Parasite behaviors can help explain trematode community structure, the aggregation of parasites within host populations, and can potentially be harnessed in biocontrol measures. In this study, we used a simple choice chamber design to examine whether trematode parasites can detect the infection status of a potential host and avoid hosts infected with a competitively dominant species. Our results show that Schistosoma mansoni, a competitively subordinate species, can detect and avoid hosts infected with a competitively dominant parasite, Echinostoma caproni. However, E. caproni, despite showing a significant preference for snails infected with S. mansoni over uninfected snails, showed little ability to detect the infection status of the host or even the host's presence. We propose subordinate species may be under stronger selection to avoid dominant competitors whereas dominant competitors may be more strongly selected to find any suitable host, regardless of infection status. Previous research has focused on parasites distinguishing between ‘host’ and ‘non-host’, which does not fully capture the complexity of these interactions. However, the ability of subordinate parasites to determine the infection status of a host results in a consistent evolutionary advantage.
The Gulf Coast tick, Amblyomma maculatum, is of public and veterinary health concern, as it is the primary vector of Rickettsia parkeri and Hepatozoon americanum, causative agents of Rickettsiosis and American canine hepatozoonosis. The Gulf Coast tick's range has expanded over the last 50 yr into the mid-Atlantic states, and its expansion is expected to continue northward. We are reporting the presence of A. maculatum for the first time in Illinois, including a total of 18 specimens collected at 6 different sites during surveys in 2013 and 2019. Fourteen of these specimens were screened for Rickettsia parkeri, which resulted in the detection of this bacteria in 8 samples from 4 counties. By depositing these specimens in scientific collections, we provide materialistic evidence of their establishment in 2 counties. We urge health officials to rely on and use scientific collections to document the expansion of these and other vectors across the country. Additionally, we recommend that health practitioners become aware of the clinical similarities between Rocky Mountain Spotted Fever (caused by Rickettsia rickettsii) and “tidewater” fever (caused by R. parkeri).
Human head lice and body lice (Pediculus humanus) are neglected ectoparasites. Head lice continue to be prevalent in children worldwide, and insecticide resistance in these insects has complicated their treatment. Meanwhile, body lice, which are most common in the developing world, are resurging among marginalized populations in developed nations. Today, the microbiome is being increasingly recognized as a key mediator of insect physiology. However, the microbial communities that inhabit human lice have remained unknown beyond only a few species of bacteria. Knowledge of the microbiomes of head and body lice could improve our understanding of the observed physiological differences between the 2 ecotypes and potentially inform the development of novel interventions against lice infestations and louse-borne infectious diseases. Toward these goals, here we performed 16S rRNA gene amplicon sequencing to characterize the microbiomes of both head and body lice and identify patterns of interest among these communities. Our data reveal that head and body lice harbor limited but distinct communities of bacteria that include known intracellular endosymbionts (“Candidatus Riesia pediculicola”), extracellular bacteria that may be horizontally acquired from the host environment, and a number of taxa of known or potential public health significance. Notably, in body lice, the relative abundance of vertically transmitted endosymbionts is lower than in head lice, which is a significant driver of greater alpha diversity. Further, several differentially abundant non-endosymbiont taxa and differences in beta diversity were observed between head lice and body lice. These findings support the hypothesis that microbiome differences could contribute to the divergence between human louse ecotypes and underscore the need for future studies to better comprehend the acquisition and physiological roles of human lice microbiomes.
The prevalence and intensity of the trematode, Otodistomum hydrolagi, were determined for the first time in Spotted Ratfish, Hydrolagus colliei. Spotted Ratfish specimens were collected during bottom-trawl surveys in Queen Charlotte Sound (QCS, n = 31) and off the west coast of Vancouver Island (WCVI, n = 242). In all instances, the flukes were found within the abdominal cavity. Most flukes were mature (intrauterine eggs were present) and ranged in length from 9.1 to 61.5 mm, with a mean ± SD length of 28.5 ± 12.1 mm (n = 52). Fluke length was positively correlated with Spotted Ratfish precaudal length (PCL), and no Spotted Ratfish smaller than 247-mm PCL was infected by O. hydrolagi. The overall prevalence (95% confidence interval [CI]) and mean intensity (95% CI) of O. hydrolagi were 27.8% (22.6–33.6) and 1.24 (1.09–1.43), respectively. Neither prevalence nor mean intensity differed between host location or host sex. The majority (86%) of infected hosts harbored a single fluke (range 1–5), but 4 Spotted Ratfish were infected with 3 or more flukes, which accounted for 16% of all observed O. hydrolagi. The fluke population exhibited an aggregated distribution with 80% of individuals found in 21% of the hosts, but among infected hosts there was low variability in the intensity of infection. This is the first ecological study of O. hydrolagi from its Spotted Ratfish host, and the first record of this trematode in Canadian waters, which extends the range of O. hydrolagi to include Canadian coastal Pacific waters.
Ixodes scapularis is currently known to transmit 7 pathogens responsible for Lyme disease, anaplasmosis, babesiosis, tick-borne relapsing fever, ehrlichiosis, and Powassan encephalitis. Ixodes scapularis can also be colonized by endosymbiotic bacteria including those in the genus of Rickettsia. We screened 459 I. scapularis ticks submitted to the Connecticut Agricultural Experiment Station Tick Testing Laboratory with the objectives to (1) examine differences in infection prevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, Babesia microti, and Borrelia miyamotoi, (2) evaluate whether prevalence of co-infections occur at the same frequency that would be expected based on single infection, and (3) determine the presence of rickettsial endosymbionts in I. scapularis. The prevalence of infection in I. scapularis was highest with Bo. burgdorferi sensu lato (nymph = 45.8%; female = 47.0%), followed by A. phagocytophilum (nymph = 4.0%; female = 6.9%), Ba. microti (nymph = 5.7%; female = 4.7%), and Bo. miyamotoi (nymph = 0%; female = 7.3%). We also identified rickettsial endosymbionts in 93.3% of I. scapularis. Nymphs were significantly more likely to be infected with Bo. burgdorferi if they were infected with Ba. microti, whereas adult females were significantly more likely to be infected with Bo. burgdorferi if they were infected with A. phagocytophilum. Our study suggests that the infection prevalence of Bo. burgdorferi is not independent of other co-circulating pathogens and that there is a substantially higher infection of Bo. miyamotoi in I. scapularis females compared with nymphs in this study. High prevalence of infection and co-infection with multiple pathogens in I. scapularis highlights the public health consequences in Connecticut, a state endemic for Lyme and other tick-borne diseases.
Hosts that overlap geographically, are less phylogenetically divergent, and/or share similar ecological conditions (e.g., climate, habitat type) are also likely to share parasites. Here we assessed the ectoparasite communities sustained by 3 solitary species of Bathyergidae (Georychus capensis, Bathyergus suillus, and Bathyergus janetta) as well as the endoparasites exploiting G. capensis and compared them with those reported in the literature for other sympatric and parapatric African mole-rat species. In addition to 1 nematode (Trichuris sp.) and 1 symbiotic ciliate (Meistoma georychi), we collected mites of the genera Androlaelaps and Bathyergolichus as well as unidentified trombiculids from these hosts. Host specificity was high at either the species, genus, or family level for Androlaelaps spp. and Bathyergolichus spp. irrespective of geographic proximity, host phylogeny, or ecological conditions. Host sharing was more limited for helminths but observed among sympatric host species. Our results suggest that ecological similarity and geographic proximity may be more important determinants of host sharing than phylogeny within Bathyergidae.
Recently, the heteroxenous eyeworm, Oxyspirura petrowi, has gained attention due to its prevalence in the declining game bird, Northern bobwhite (Colinus virginianus), but the intermediate hosts of many nematodes remain unknown. However, identifying the intermediate host of O. petrowi with traditional techniques would be difficult and time-consuming, especially considering there are more than 80 potential orthopteran hosts just in Texas. To screen a large number of samples quickly and effectively, primers for nested PCR (nPCR) were developed using the internal transcribed spacer 1 (ITS1) region. Then the nPCR was used to identify which of the 35 species collected from the Order Orthoptera were potential intermediate hosts of O. petrowi. With this technique, 18 potential intermediate hosts were identified. Later, we collected live specimens of species that tested positive to confirm the presence of larvae, but larvae were not found in the live specimens, nor in the extra tissue of the species that had tested positive for O. petrowi DNA. Despite this, this study demonstrated that nPCR is more sensitive than traditional techniques and can be a valuable tool in determining the intermediate hosts of parasites.
A new species of monogenean, Dactylogyrus pisolabrae n. sp., was found parasitizing the gills of the Pealip Redhorse, Moxostoma pisolabrum, from Oklahoma. Dactylogyrus pisolabrae is morphologically similar to Dactylogyrus apos, Dactylogyrus atripinnei, Dactylogyrus duquesnei, and Dactylogyrus niger, all parasitizing other species of suckers, by possessing a robust, sickle-shaped male copulatory organ, but differs from these and all other species of North American Dactylogyrus by possessing 2 unique wing-like projections opposite each other on the proximal portion of the accessory piece. Dactylogyrus pisolabrae represents the first monogenean reported from the Pealip Redhorse.
Rhadinorhynchus hiansiSoota and Bhattacharya, 1981, has remained unknown since its original incomplete description from 2 male specimens collected from the flat needlefish Ablennes hians Valenciennes (Belonidae) off Trivandrum, Kerala, India. Recent collections of fishes along the Pacific coast of Vietnam in 2016 and 2017 produced many specimens of the same species from the striped bonito Sarda orientalis Temminck and Schlegel (Scombridae) off the southern Pacific coast of Vietnam at Nha Trang. We describe females for the first time, assign a female allotype status, and provide an expanded description of males from a larger collection completing missing information on hooks and hook roots, receptacle, lemnisci, cement glands, Saefftigen's pouch, and trunk spines. Specimens of R. hiansi characteristically have no dorsal spines in the posterior field of trunk spines and a long proboscis with 36–48 dorso-ventrally differentiated proboscis hooks per row becoming progressively smaller posteriorly then increasing in size near the posterior end to a maximum at the posterior-most ring. Trunk, testes, and lemnisci in our specimens were considerably larger than those reported in the original description, but the proboscis was relatively smaller. The females had long reproductive system and corrugated elliptic eggs without polar prolongation of fertilization membrane. Energy Dispersive X-ray Analysis (EDXA) demonstrates high levels of calcium and phosphorus in large gallium cut hooks and high levels of sulfur in tip cuts of large and small hooks and in spines. This EDXA pattern is a characteristic fingerprint of R. hiansi. The molecular profile of R. hiansi is described from 18S rDNA and COI genes, and phylogenetic relationships with most closely related species are discussed.
An unusual coccidian parasite was described previously from the prostate of a male Antechinus flavipes (family: Dasyuridae; common name: yellow-footed antechinus). Morphometrics and a partial nuclear 18S small subunit rDNA (18S rDNA) sequence were used to assign this parasite to the genus Eimeria; it was named Eimeria taggarti. We generated full nuclear 18S rDNA and mitochondrial genome sequences from this parasite and used the newly completed 18S rDNA and mitochondrial cytochrome c oxidase subunit I (COI) sequences to perform a more in-depth phylogenetic analysis. The parasite clustered closely with Choleoeimeria spp. and Acroeimeria spp. infecting herptiles in a well-supported clade that was the sister lineage to the Eimeriidae sensu stricto. The mitochondrial genome of this parasite contained 2 inverted segments compared to mitochondrial genomes from parasites in the Eimeriidae sensu stricto (i.e., Stieda body-possessing coccidia with 4 dizoic sporocysts); this mitochondrial genome arrangement was shared with the only Choleoeimeria species for which sequence data were available publicly. Examination of histological preparations and TEM images uncovered bivalvate sporocysts and otherwise confirmed previously described morphological features of the parasite. Based on our phylogenetic analyses and histological observations, we propose the generic reclassification of E. taggarti to Choleoeimeria taggarti n. comb.
Quill mites of the family Syringophilidae (Acariformes: Prostigmata) are permanent ectoparasites that live inside the hollow quills of feathers and use their long chelicerae to pierce the quill wall to feed on living tissue of the quill follicle. Ovenbirds (Parulidae: Seiurus aurocapilla (Linnaeus)) are host to the quill mite Betasyringophiloidus seiuri (Clark), which has been previously reported to infest only 5.1% of this host's tail feathers; however, this species has also been reported to inhabit the wing feathers of ovenbirds, but without any data on prevalence or intensity. We examined all 1,008 flight feathers from 21 dead ovenbirds from Canada for quill mites and calculated infestation parameters per feather location. Nine of the 21 birds were infested with mites (prevalence of 42.9%). Feathers with the highest prevalence were Primaries 1 and 2 and Secondaries 1, 2, and 5. Only 2 of the 9 infested birds had mites in their tail feathers; in each case, only a single feather was infested. Mean intensity was 28.4 mites/feather with a range of 2–135.6, and ∼88% of the adult mites were female. To determine if quill volume and quill wall thickness correlated with mite presence and abundance, we took quill measurements from the flight feathers of 3 additional ovenbirds. There was a strong positive correlation between quill volume and mean mite intensity. Feathers that had quill walls thicker in some areas than the mites' extended chelicerae had lower prevalences than did feathers with walls consistently thinner than the length of the chelicerae. We conclude that B. seiuri is much more likely to be found in wing than in tail feathers and that it has greater reproductive success in quills with both large volumes and thin walls; however, whether foundress mites preferentially choose to colonize these feathers requires more study.
The order Crocodylia (suborder Eusuchia) includes 27 species of alligators, caimans, crocodiles, and gharials that are cosmopolitan in distribution, inhabiting subtropical and tropical locations. Numerous surveys (many of them trivial, with small sample sizes) have reported a wide variety of blood and intestinal apicomplexans from 17/27 (63%) crocodilian hosts, but neither a summation for the group nor a revisionary systematic approach to species evaluation has ever been provided. Herein, we summarize information on the 16 species of apicomplexans that we consider to be valid, including 8 Eimeria, 1 Haemogregarina (that eventually may be transferred to Hepatozoon), 4 Hepatozoon, 2 Isospora, and 1 Progarnia species. In addition, there are 46 apicomplexan forms that we have relegated to species inquirendae and/or only partially identified forms that await further study. We hope this review provides a foundation for future research between parasitologists and herpetologists on parasitism of all reptiles and their relatives. Since many apicomplexans seem to be reasonably host-specific, knowledge of shared species and/or genera may assist herpetologists to better understand the phylogenetic relationships among the New World crocodilians and the direction of their dispersal in the New World.
A total of 20 specimens of Tolypeutes matacus (Desmarest, 1804) from the Chaco Region in Argentina were examined. This study revealed the presence of 3 species of the genus Mathevotaenia Akumyan, 1946 (Cestoda Anoplocephalidae), two of them new for science. These species are described, illustrated, and compared with related species. Mathevotaenia chamicalensis n. sp. is characterized by having a small body with 45–65 proglottids; a globose scolex, longer than wide and well delimited from strobila; a long neck; mature and gravid proglottids longer than wide; and 20–35 testes located in a single field. Mathevotaenia yepesi n. sp. is characterized by having a small body with 86–128 proglottids; a rectangular scolex, wider than long and not well delimited from strobila; neck absent; mature and gravid proglottids wider than long; and 23–50 testes located in the medial portion of the proglottid. The finding of Mathevotaenia argentinensisCampbell et al., 2003 parasitizing T. matacus represents the first record in armadillos.
Four new species of Paraorygmatobothrium are described from carcharhinid shark species from the Gulf of Mexico and the U.S. coast of the northwestern Atlantic Ocean. Paraorygmatobothrium bullardi n. sp. is described from Carcharhinus brevipinna as its type host, and from Carcharhinus acronotus and Carcharhinus limbatus. Paraorygmatobothrium campbelli n. sp. is described from Rhizoprionodon terraenovae. Paraorygmatobothrium deburonae n. sp. is described from Carcharhinus isodon as its type host, as well as from C. brevipinna, C. limbatus, and R. terraenovae. Paraorygmatobothrium mattisi n. sp. is described from R. terraenovae as its type host, and from C. brevipinna and C. limbatus. These 4 species differ from other species of Paraorygmatobothrium and from each other in bothridial microthrix shape, and in various combinations of features such as the total length of the worm, apical sucker size, bothridial musculature, proglottid number, testes number, and genital pore position. Difficulty in differentiating these 4 species from one another, and from other species of Paraorygmatobothrium, points to limitations in the use of morphology alone to recognize species diversity in this genus. A phylogenetic analysis of Paraorygmatobothrium and related genera, based on partial (D1–D3) 28S rDNA sequence data, confirms that the genus is not monophyletic. Genetic distances of COI revealed that sequence divergence between species of Paraorygmatobothrium is generally at least an order of magnitude larger than COI divergence within a species. Patterns of host use for 3 of the new species are consistent with previous findings that point to a lack of host specificity in Paraorygmatobothrium.
This study provides additional taxonomic features based on scanning electron microscopy (SEM) and molecular data for Paracamallanus cyathopharynx (Baylis, 1923) (Nematoda: Camallanidae). Parasites were collected from the posterior end of the intestine of cultured freshwater Sharptooth catfish Clarias gariepinus (Burchell, 1822) from Kibos fish farm, Kisumu County, Kenya, from December 2017 to March 2018. Additional taxonomic features recorded for P. cyathopharynx include the occurrence of 4–5 equal length digitate processes on the caudal end of the female, 4 processes (2 smaller and 2 larger) on the male caudal end, and a description of the shape of the distal tip of the right spicule. The study provides SEM images of the exposed sclerotized buccal capsule. This gives more information on the tridents, the sclerotized plate that extends laterally from the buccal capsule, and the narrow isthmus separating the anterior buccal capsule from the posterior. The prevalence, intensity, mean intensity, and mean abundance was 52.91%, 2–38, 12.37 and 6.54, respectively. 18S rDNA fragments were amplified, sequenced, and compared to other camallanid taxa, and 18S data confirmed the identity of the newly obtained sequences (MN396556) as that of P. cyathopharynx, being identical to sequence DQ813445 from Tanzania. This represents the first geographical record of P. cyathopharynx in Kenya.
Allopreening occurs when 1 bird preens another bird. The behavior is normally directed at the head and neck of the recipient, i.e., regions that the bird cannot self-preen. Studies of penguins, pigeons, and other groups of birds suggest that allopreening plays a role in the control of ectoparasites, such as ticks and feather lice. However, it is not known whether allopreening increases in response to increases in parasite load, or whether it is a programmed response that occurs independently of parasite load. We conducted a laboratory experiment using wild-caught rock pigeons (Columba livia) to test the relationship between ectoparasite load and allopreening rate. We added feather lice (Columbicola columbae) to captive pigeons and tested for changes in allopreening rates compared to control birds with no lice added. Allopreening rates did not change in response to the addition of lice. Interestingly, however, our data revealed a negative correlation between allopreening and self-preening rates.
A new species of the nematode TriumphalisnemaKloss, 1962 (Oxyuridomorpha), is described from the wood beetle Proculejus hirtus Truqui from the mountain mesophilic forest in Hidalgo State, Mexico. Triumphalisnema zuuei n. sp. is distinguished from the other 4 congeners species by the presence of an expanded cervical ring, well-developed lateral alae, an obtuse cauda with a short and bifurcated caudal appendage, series of cuticular folds at ventral and dorsal body surface from excretory pore level to anal region, and ellipsoidal eggs ornamented with numerous small mushroom-like structures over the surface. The phylogenetic position of the new species is inferred based on a Maximum Likelihood and Bayesian Inference analysis of partial sequences of 18S SSU rRNA. The phylogenetic analysis showed that Triumphalisnema zuuei n. sp., the only representative of the Traklosiidae in our study, is closely related to Coynema poeyi and species of Longior, Hystrignathus, and Lepidonema, all of them members of Hystrignathidae. These relationships are supported by high support values. The present study increases to 5 the number of species assigned to Triumphalisnema, all of them parasites of Passalidae. Additionally, a taxonomic key to the species of the genus is provided.
Max R. Werneck, Hassan Jerdy, Rachel B. Ribeiro, Mariah Bianchi, Leide Laura Figueiredo Maciel, João Carlos de Aquino Almeida, Paula Baldassin, Hugo Gallo, Eulógio C. Q. Carvalho
The present study offers the first description of proventriculitis associated with the presence of gravid female nematodes of the genus Tetrameres (Nematoda: Tetrameridae) in 3 juvenile Magellanic penguins (Spheniscus magellanicus) found dead on the coast of Brazil. This study broadens knowledge on parasites associated with these hosts and the real impact of this association.
Echinostomiasis is prevalent in southeastern as well as northeastern Asian countries. This endemicity notwithstanding, no echinostome egg has as yet been reported by paleoparasitological studies conducted in Asian countries. Recently we analyzed geological-strata specimens retrieved from the ancient capital city of the Baekje Kingdom to uncover clues to the possible prevalence of echinostomiasis among contemporaneous populations of Korea. By means of archaeoparasitological technique, we found ancient Isthmiophora hortensis eggs in the specimens, thus revealing for the first time that ancient Korean people experienced isthmiophoriasis. Our report can be considered to have effectively broadened the spatial and temporal scope of research on echinostomiasis in human history.
Siri H. Helland-Riise, Lauren E. Nadler, Marco A. Vindas, Erik Bengston, Andrew V. Turner, Ida B. Johansen, Kelly L. Weinersmith, Ryan F. Hechinger, Øyvind Øverli
Some parasite species alter the behavior of intermediate hosts to promote transmission to the next host in the parasite's life cycle. This is the case for Euhaplorchis californiensis, a brain-encysting trematode parasite that causes behavioral changes in the California killifish (Fundulus parvipinnis). These manipulations increase predation by the parasite's final host, piscivorous marsh birds. The mechanisms by which E. californiensis achieves this manipulation remain poorly understood. As E. californiensis cysts reside on the surface of the killifish's brain, discerning regional differences in parasite distribution could indicate mechanisms for host control. In this study, we developed a method for repeated experimental infections. In addition, we measured brain-region specific density using a novel methodology to locate and quantify parasite infection. We show that E. californiensis cysts are non-randomly distributed on the fish brain, aggregating on the diencephalon/ mesencephalon region (a brain area involved in controlling reproduction and stress coping) and the rhombencephalon (an area involved in controlling locomotion and basal physiology). Determining causal mechanisms behind this pattern of localization will guide future research examining the neurological mechanisms of parasite-induced host manipulation. These findings suggest that parasites are likely targeting the reproductive, monoaminergic, and locomotor systems to achieve host behavioral manipulation.
Salmincola californiensis (Dana, 1853) (Subclass Copepoda: Family Lernaeopodidae) is known to parasitize salmonids of the genus Oncorhynchus including Oncorhynchus mykiss (rainbow trout), Oncorhynchus tshawytscha (chinook salmon), and Oncorhynchus kisutch (coho salmon). These 3 salmonids have been introduced to the Great Lakes intermittently since the mid-1800s. As we demonstrate here, the introduction of these salmonids to the Great Lakes was followed, at some point, by the introduction of their parasitic gill copepod, S. californiensis. Given anecdotal accounts of S. californiensis in introduced salmonids in Lake Ontario since 2012, we chose to conduct a survey to formally document the occurrence of this introduced species. Our survey took place during spring, summer, and fall of 2018 and during spring of 2019 at the south-eastern side of Lake Ontario. Prevalence of S. californiensis was 69, with a mean intensity of 2.7 in 61 rainbow trout examined in 2018. In 2019, prevalence of S. californiensis was 71, with a mean intensity of 3.6 in 59 rainbow trout examined. The prevalence of S. californiensis was 39, with a mean intensity of 1.6 in 223 chinook salmon examined in 2018. No specimens of S. californiensis were found in the 100 coho salmon examined in 2018. The prevalence of S. californiensis in rainbow trout is of great concern considering that it is double that found in rainbow trout in the native range (69 [in 2018] and 71 [in 2019] vs. 35). This is the first formal documentation of the invasion of S. californiensis in Lake Ontario. Future fisheries management decisions in Lake Ontario and its tributaries should take into account these data.
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