Parasitism in a declining population of snowshoe hares

Prevalence and intensity of six endoparasites were determined in 346 snowshoe hares (Lepus americanus) obtained at Rochester, Alberta, during December-April 1981-1982, the second winter of a cyclic population decline. The data were analyzed for (1) differences among host sex and age classes, and among months and sample sources, and (2) evidence that parasitism was of demographic significance to the hare population. Prevalence and intensity of Obeliscoides cuniculi were consistently highest among adult hares, but rose most sharply from February to March among juveniles. In contrast, prevalence and intensity of Nematodirus triangularis were highest among juveniles; prevalence reached 90-100% by January, whereas intensity continued to rise through April. Prevalence and intensity of both Trichuris leporis and Protostrongylus boughtoni were highest also among juvenile hares; neither parameter exhibited a definite trend over time. Prevalences of Taenia pisiformis (cysticerci) and Eimeria spp. were unrelated to sex, age or month; but Taenia intensity was highest among juveniles, and Eimeria intensity tended to decrease from December to April. Intensities of Nematodirus, Protostrongylus and Eimeria were higher in male hares than in females. Prevalence and intensity were correlated directly in Obeliscoides, Nematodirus, Trichuris and Eimeria. Hares that died during trapping and handling, or from natural predation, had greater intensities of Obeliscoides than did animals killed on purpose. There was no indication, however, that risk of death was increased by the other parasitic infections. Age-related immune responses to parasitism (except Obeliscoides) were evidenced by reduced or stabilized prevalence and/or intensity among older hares. A multiple-regression model predicted depressed body weight with increasing intensities of Nematodirus, Trichuris or Protostrongylus. Other body-condition and reproductive indices were unassociated with parasite intensities. Within the hare population, Obeliscoides, Trichuris, Protostrongylus and Taenia had overdispersed distributions (typical of many endoparasites) that did not differ from a negative binomial. The frequency with which each possible combination of helminth species occurred within individual hares was consistent with the assumption that such infections occurred independently. There was no compelling reason to believe parasitism was a significant factor in the overwinter decline of this population of snowshoe hares.     

Helminths of sympatric black-tailed jack rabbits (Lepus californicus) and desert cottontails (Sylvilagus audubonii) from the high plains of eastern New Mexico

Thirty-five desert cottontails (Sylvilagus audubonii) and 35 black-tailed jack rabbits (Lepus californicus), occurring sympatrically near the Clovis-Portales area of eastern New Mexico were infected with four species of Eucestoda (adults of Raillietina salmoni and Raillietina selfi, larvae of Taenia pisiformis and Taenia serialis). Raillietina salmoni and T. pisiformis more commonly infected S. audubonii. Raillietina selfi was found in near equal prevalence in both host species. Taenia serialis was recovered only from L. californicus. Thus, three of the four helminth species were shared by both lagomorphs (Jaccard's coefficient = 75). Female hosts were most heavily infected with R. selfi and Taenia serialis.     

Systematics of Mesocestoides (Cestoda: Mesocestoididae): evaluation of molecular and morphological variation among isolates

A hypothesis-based framework was used to test if 3 genetic strains of Mesocestoides (clades A, B, and C) are distinct evolutionary lineages, thereby supporting their delimitation as species. For comparative purposes, 3 established cestode species, Taenia pisiformis, Taenia serialis, and Taenia crassiceps were assessed using the same methods. Sequence data from mitochondrial rDNA (12S) and the second internal transcribed spacer of nuclear rDNA (ITS-2) revealed derived (autapomorphic) characters for lineages representing clade A (n = 6 autapomorphies), clade B (n = 4), and clade C (n = 9) as well as T. pisiformis (n = 15) and T. serialis (n = 12). Furthermore, multivariate analysis of morphological data revealed significant differences among the 3 genetic strains of Mesocestoides and between T. pisiformis and T. serialis. The level of phenotypic variation within evolutionary lineages of Mesocestoides and Taenia spp. tapeworms was similar. Results from this study support recognizing Mesocestoides clades A, B, and C as separate species, and provide evidence that clade B and Mesocestoides vogae are conspecific.     

Parasitic helminths of the wild rabbit, Oryctolagus cuniculus, in different bioclimatic zones in Tenerife, Canary Islands

Faunistic and ecological analyses of the wild rabbit helminth fauna were undertaken in Tenerife island (Canary Islands). Rabbits were collected between 1998 and 2000 in seven bioclimatic zones in Tenerife selected by orientation and altitude. Five parasite species were identified, three cestodes (Taenia pisiformis (larvae), Andrya cuniculi and Mosgovoyia ctenoides) and two nematodes (Trichostrongylus retortaeformis and Passalurus ambiguus). Taenia pisiformis presented an irregular distribution with significant differences in prevalences between the zones. Andrya cuniculi was only found in two zones and there were no significant differences in prevalence values. Mosgovoyia ctenoides presented a wide distribution with significant prevalences, which were higher in northern compared to southern zones. Trichostrongylus retortaeformis was absent in the low southern zones of the island. Passalurus ambiguus was found in all zones with no significant difference in the prevalence of infection. The differences in prevalences are likely to be explained by abiotic factors in the case of T. retortaeformis, and by the absence of definitive and intermediate hosts in the case of T. pisiformis and A. cuniculi, respectively. All parasite species in Tenerife are common helminths in the Iberian Peninsula, from which their rabbit hosts originated. No significant differences were recorded in the mean intensities of infection of any of the parasite species identified.     

Characteristics of natural infections of the stomach worm, Obeliscoides cuniculi (Graybill), in lagomorphs and woodchucks in Canada

Wild lagomorphs and woodchucks collected predominantly in southern Ontario, Canada were examined for subspecies of Obeliscoides cuniculi (Graybill). Obeliscoides cuniculi multistriatus was found in snowshoe hares (Lepus americanus). Obeliscoides cuniculi cuniculi was found in cottontail rabbits (Sylvilagus floridanus), European hares (Lepus capensis) and woodchucks (Marmota monax). Prevalence of Obeliscoides cuniculi multistriatus in snowshoe hares was 100% and mean intensity (and range of intensity) was 760 (9-4, 198) in Lindsay, Ontario in 1980. Mean intensity in hares varied trimonthly. The highest mean intensity of worms occurred in spring when most worms were adult. Transmission occurred mainly in spring. Most worms present in fall (70%) and winter (54%) were fourth stage. Immature fifth-stage and gravid females were present in hares during fall and winter. Prevalence and mean intensity of O. c. cuniculi in cottontails was 15% and 29 (1-118). Prevalence and mean intensity of O. c. cuniculi in woodchucks was 6% and 56 (16-118). European hares were infected with O. c. cuniculi, prevalence was 10% and mean intensity was 60 (36-83). In Ontario woodchucks and European hares were common in areas frequented by cottontail rabbits and probably acquired sporadic infections of O. c. cuniculi from infected cottontails.     

Helminths of the wild rabbit (Oryctolagus cuniculus) in Macaronesia

Two hundred and four rabbits from 8 Macaronesian islands (Pico, San Jorge, San Miguel, Terceira, and Flores from Azores Archipelago; Tenerife and Alegranza from Canary Islands; and Madeira from Madeira Archipelago) were examined for helminth parasites between 1995 and 2000. Three species of cestodes, Taenia pisiformis (larvae), Andrya cuniculi, and Mosgovoyia ctenoides, and 5 species of nematodes, Trichuris leporis, Graphidium strigosum, Trichostrongylus retortaeformis, Passalurus ambiguus, and Dermatoxys hispaniensis, were identified. Only 3 species (M. ctenoides, T. retortaeformis, and P. ambiguus) were regularly distributed over the 3 archipelagos. Taenia pisiformis was not collected in Madeira, nor was A. cuniculi in the Azores and G. strigosum in the Canary Islands. Trichuris leporis and D. hispaniensis were only found in Madeira. Significant differences in the general prevalence of the nematodes G. strigosum and T. retortaeformis were detected between Azores and Madeira. The prevalence of T. retortaeformis differs significantly between the Azores and the Canaries and that of P. ambiguus was higher in Madeira than in Azores and Canaries. The helminth richness found in the wild rabbit in these Macaronesian archipelagos was very low compared with the Palearctic helminth fauna of this host. The wild rabbit was introduced from the Iberian Peninsula into different Macaronesian islands. Helminths introduced with Oryctolagus cuniculus into these islands also are commonly found in Iberian wild rabbits, which are excellent colonizers, as demonstrated in this study.     

Pathology and epizootiology of Dirofilaria scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in Sylvilagus floridanus (J.A. Allen) and Lepus americanus erxleben

Dirofilaria scapiceps was found between the synovial sheath and tendons, i.e., within the tendon sheath, in the ankle region of eastern cottontail rabbits (Sylvilagus floridanus) and snowshoe hares (Lepus americanus). In cottontail rabbits, tendons and sheaths appeared normal and all worms were adults. Only one (4%) of 24 infected rabbits contained dead worms. All female worms were gravid in rabbits killed in late winter or early spring. Microfilaremias in rabbits were high (approximately 30-100 microfilariae/60 microliter blood) and of long duration (at least 8-28 mo), and rabbits were considered normal hosts of D. scapiceps. In some snowshoe hares, tendons and sheaths also appeared normal; however, in other hares a chronic proliferative tenosynovitis, characterized by fibrinous exudate, hyperplasia and hypertrophy of the intima and inflammatory cell (predominantly lymphocytes and plasma cells) infiltration of the intimal and fibrous layers of the synovial sheath led to encapsulation of worms. Dead subadult, dead adult, and live adult worms were found in the ankles of hares; 86 (46%) of 186 infected hares contained some or only dead worms. Fibrosis commonly occurred around dead worms. Dead subadults were also found in subcutaneous connective tissues over the trunk of the body. Degenerate embryos and amorphous material were observed in uteri of some female worms in hares killed in late winter or early spring. Few (1-5 microfilariae/60 microliter blood) or no microfilariae were observed in the peripheral blood of hares and microfilaremias were of short duration (less than 8 mo). Microfilariae in hares are probably trapped and destroyed in the chronic inflammatory lesions in the tendon sheaths since normal, degenerate, and calcified microfilariae were observed in the capsules around adult worms. Some microfilariae might also be destroyed in lymph nodes. Although D. scapiceps can be maintained within snowshoe hare populations, hares are considered abnormal hosts of D. scapiceps. Dirofilaria scapiceps may have spread from cottontail rabbits to snowshoe hares relatively recently.     

Interaction of the tick (Haemaphysalis leporispalustris) with a cyclic snowshoe hare (Lepus americanus) population

Prevalence and intensity of the tick, Haemaphysalis leporispalustris, were monitored during 1963 to 1976 in a cyclic snowshoe hare (Lepus americanus) population near Rochester, Alberta, Canada. Prevalence was near zero from December through March, and near 100% among adult hares from May through September. Prevalence among juvenile hares approached 100% by age 2 mo. Intensity peaked for both adults and juveniles during May-June and again in August. Mean intensities were significantly higher among adult males than adult females in 5 of 13 yr, and almost significant in two others. Tick intensities were lowest during 3 yr, 1969 to 1971, when hare densities were highest. Tick intensities in spring were correlated with intensities the previous fall. Survival of marked adult and juvenile hares was unrelated to intensities of infestation. Mean numbers of corpora lutea and embryos tended to be lower among adult females with heavy tick infestations, and intra-uterine losses rose steadily from about 3 to 13% as tick intensities increased from none to heavy. Comparison of average tick intensities on adults 1-, 2-, and greater than or equal to 3-yr-old yielded no evidence of increased immunity with age.     

Evaluation of host preferences by helminths and ectoparasites among black-tailed jackrabbits in northern California

Fifty-four black-tailed jackrabbits (Lepus californicus) (five juvenile males, 22 adult males, five juvenile females, and 22 adult females) from Humboldt County, California (USA) were evaluated for sex and age-specific differences in parasite prevalences and intensities, 26 February through 30 October 1996. Nematodes found included Biogastranema leporis in 42 hares (78% prevalence), Rauschia triangularis in 26 hares (48%), Trichostrongylus calcaratus in 14 hares (26%), and Trichuris sylvilagi in two hares (4%). Cestodes found included Taenia sp. cysticerci in five hares (9%) and Taenia sp. coenurus found in one hare (2%). Ectoparasites found included the ticks Dermacentor variabilis on 10 hares (19%) and Ixodes spinipalpis (= Ixodes neotomae) on nine hares (17%), as well as the anoplurid louse Haemodipsus setoni on 12 hares (22%). No significant differences in the parasite prevalences or intensities were found between male and female jackrabbits; this was for all males and females collectively, juvenile males and females only, as well as adult males and females only. Combining male and female hosts, adult jackrabbits had a significantly higher prevalence of B. leporis and R. triangularis compared to juveniles. This is the first known report of Trichostrongylus calcaratus, Rauschia triangularis, Trichuris sylvilagi, and Dermacentor variabilis among black-tailed jackrabbits and the first known report of T. calcaratus and T. sylvilagi in the western USA. This is the first published report of I. spinipalpis, the vector for Lyme disease in California, on black-tailed jackrabbits.     

Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia

Thirty-seven carcasses of Eurasian lynx (Lynx lynx) collected and examined in Estonia during 1999-2001 had helminths. Parasites identified and their prevalence included Diphyllobothrium latum (5%), Taenia pisiformis (100%), Taenia laticollis (41%), Taenia hydatigena (3%), Taenia taeniaeformis (3%), Toxocara cati (68%), and Trichinella spp. (22%). The only significant relationships (P < or = 0.05) between occurrence of helminths and host age and sex were a greater number of T. pisiformis and T. laticollis in older than in youger male lynx, and older males had a greater number of species of helminth than did younger lynx. Sixty-one fecal samples collected during snow tracking of nine lynx were examined; eggs of T. cati were identified in 38 samples, and Capillaria spp were found in eight samples. This is the first systematic investigation of parasites of lynx in Estonia.     

Intestinal cestodes of stray dogs in Jordan

Five species of cestodes namely Echinococcus granulosus, Taenia hydatigena, Taenia pisiformis, Taenia ovis and Dipylidium caninum were recovered post mortem from 120 out of 173 stray dogs collected from the 5 governorates of Jordan during the period June 1979 to November 1980. Twenty-five of the examined dogs (14%) were found to be infected with E. granulosus, 79 (46%) with T. hydatigena, 14 (8%) with T. pisiformis and 5 (3%) with T. ovis. Dipylidium caninum was encountered in 33 (19%) of the examined dogs and infection with this parasite was significantly higher in males than in females. The parasites, except for D. caninum which was encountered in the ileum, were almost exclusively recovered from the duodenum and the jejunum. Single, double and triple infections with those cestodes were recorded.     

The migration of oncospheres of Taenia pisiformis, T. serialis and Echinococcus granulosus within the intermediate host

Heath D. D., 1971. The migration of oncospheres of Taenia pisiformis, T. serialis and Echinococcus granulosus within the intermediate host. International journal for Parasitology, 1: 145–152. The oncospheres of Taenia pisiformis and T. serialis hatched, became activated and penetrated the tips of the villi in the jejunal area of the rabbit small intestine. Similar results were obtained forE. granulosus, T. hydatigena and T. ovis in sheep. Most species of oncospheres appeared to progress down the villus beneath the columnar epithelium until a venule of diameter sufficient to allow passive transport to the liver was penetrated. The relatively large villus lacteal of ruminants, and the large diameter ofE. granulosus oncospheres, appeared to provide an opportunity for these organisms to penetrate the lacteal and translocate in the lymph. Parenteral inoculations of activated oncospheres indicated that T. pisiformis and E. granulosus oncospheres probably reach the liver in the portal vein. E. granulosus oncospheres infecting the lung may reach that organ in the lymph. T. serialis oncospheres were able to pass through both the liver and lungs in order to reach the muscles. A stimulus may exist in the liver causing cessation of movement and initiation of postoncospheral development for T. pisiformis and E. granulosus, but not T. serialis.     

Prevalence, intensity and aggregation of intestinal parasites in mountain hares and their potential impact on population dynamics

Mountain hare Lepus timidus populations show unstable dynamics and since hares carry a significant helminth infection and host-parasite interactions are known to be destabilising, they have been proposed as a possible causal mechanism for the observed instability. We assessed the prevalence, intensity of infection and aggregation of the helminth parasites Graphidium strigosum and Trichostrongylus retortaeformis recovered from 589 mountain hares culled from 30 Scottish sporting estates in 1999 and 2000. Graphidium strigosum showed low prevalence and intensity of infection and was highly aggregated. In contrast, T. retortaeformis showed high prevalence and intensity of infection and a low degree of aggregation. Differences in body condition of the hares were best explained by a model including sex and month of collection and interaction terms for sex-month and intensity of infection of T. retortaeformis-month. The low degree of aggregation of T. retortaeformis and the significant negative effect of intensity of infection on body condition are in accordance with the hypothesis that the host-parasite interaction is the causative destabilising mechanism for mountain hare dynamics.     

Effects of season and reproductive state on lipid intake and fatty acid composition of gastrointestinal tract contents in the European hare

We investigated lipid content and fatty acid (FA) composition of gastrointestinal tract contents in free-living, herbivorous European hares (Lepus europaeus). Mean crude fat content in hare stomachs and total gastrointestinal (GI) tracts was higher than expected for typical herbivore forages and peaked in late fall when hares massively deposited body fat reserves. Changes of FA proportions in different parts of the GI-tract indicated a highly preferential absorption of polyunsaturated fatty acids (PUFA). A further reduction of PUFA content in the caecum, along with the appearance of odd-chained FAs in caecum, caecotrophes, and colon content, pointed to a biohydrogenation of PUFA in the hare’s hindgut. GI-tract contents showed significant seasonal changes in their FA composition. Among PUFA, α-linolenic acid peaked in spring while linoleic acid was predominant in late summer and fall, which probably reflected changes in the plant composition of forage. However, independent of seasonal changes, GI-tracts of lactating females showed a significantly (+33%) higher content of linoleic acid, a FA that is known to increase reproductive performance in European hares. This finding suggests that lactating females actively selected dietary plants rich in linoleic acid, a PUFA that may represent a limited resource for European hares.     

Predator-Mediated Indirect Effects of Snowshoe Hares on Dall's Sheep in Alaska

ABSTRACT Indirect interactions among species can strongly influence population dynamics and community structure but are often overlooked in management of large mammals. We estimated survival of Dall's sheep (Ovis dalli) in the central Alaska Range, USA, during years of differing snowshoe hare (Lepus americanus) abundance to test whether indirect interactions with a cyclic hare population affect Dall's sheep either negatively, by subsidizing predators (apparent competition), or positively, by diverting predation (apparent commensalism). Annual survival of adult female sheep was consistently high (0.85 for all yr and age classes combined). In contrast, annual estimates of lamb survival ranged from 0.15 to 0.63. The main predators of lambs were coyotes (Canis latrans) and golden eagles (Aquila chrysaetos), which rely on hares as their primary food and prey on lambs secondarily. Coyotes and eagles killed 78% of 65 radiocollared lambs for which cause of death was known. Lamb survival was negatively related to hare abundance during the previous year, and lamb survival rates more than doubled when hare abundance declined, supporting the hypothesis of predator-mediated apparent competition between hares and sheep. However, stage-specific predation and delays in predator responses to changes in hare numbers led to a positive relationship between abundance of adult Dall's sheep and hares. Lacking reliable estimates of survival, a manager might erroneously conclude that hares benefit sheep. Thus, support for different indirect effects can be obtained from different types of data, which demonstrates the need to determine the mechanisms that create indirect interactions. Long-term survey data suggest that predation by coyotes is limiting this sheep population below levels typical when coyotes were rare or absent. Understanding the nature of indirect interactions is necessary to effectively manage complex predator–prey communities.     

Contribution of NADH dehydrogenase subunit I and cytochrome C oxidase subunit I sequences toward identifying a case of human coenuriasis in France

Coenuriasis is a parasitic disease induced by larval taeniid tapeworms that is rarely observed in humans. In December 2005, a case was diagnosed in Nancy, France, after surgical excision of a cyst on a 24-yr-old woman returning from the C?te d'Ivoire. Morphological and epidemiological criteria suggested that the infection was due to Taenia serialis. Molecular analysis of NADH dehydrogenase subunit I (NDI) and cytochrome c oxidase subunit I (COI) sequences was also in favor of T. serialis identification, but the absence of available genetic data on T. brauni and T. glomeratus and the small number of published sequences for T. serialis and T. multiceps must be considered with caution. The NDI partial sequences presented more variations within species of Taenia than the COI sequences, which make them more useful targets for species identification and analysis of intraspecific polymorphisms. The present study points to the usefulness of molecular biology tools to help make up for the shortcomings of the commonplace parasitological diagnosis for coenuriasis.     

Taenia spp.: 18S rDNA microsatellites for molecular systematic diagnosis

The 18S rDNA gene of adult worms of Taenia parva found in Genetta genetta in the Iberian Peninsula and larval stages of T. pisiformis from the wild rabbit (Oryctolagus cuniculus) in Tenerife (Canary Islands) were amplified and sequenced. The sequences of the 18S rDNA gene of T. parva (1768 bp) and T. pisiformis (1760 bp) are reported for the first time (GenBank accession nos. AJ555167-AJ555168 and AJ555169-AJ555170, respectively). In 168 alignment positions microsatellites in the 18S rDNA of both taxa were detected for the first time (TGC in T. parva and TGCT in T. pisiformis) and differences in their sequences with different repetition numbers were observed. The use of nucleotide sequences of this gene in the resolution of systematic problems in cestodes is discussed with reference to the systematic status of Taenia spp. and mainly in human taeniids such as T. solium, T. saginata, and Asian human isolates of Taenia.     

In vitro oncosphere-killing assays to determine immunity to the larvae of Taenia pisiformis, Taenia ovis, Taenia saginata, and Taenia solium

Taeniid cestodes infect humans and livestock, causing considerable morbidity and mortality, as well as economic loss. Substantial progress has been made toward the production of recombinant vaccines against cysticercosis in livestock animals. Further development of these vaccines would be aided if a reliable in vitro test were available to measure host-protective immune responses in vaccinated animals. Here, we describe in vitro oncosphere-killing assays for the quantification of host-protective serum antibodies against Taenia pisiformis, Taenia ovis, Taenia saginata, and Taenia solium in rabbits, sheep, cattle, and pigs, respectively. Activated oncospheres of T. pisiformis, T. ovis, T. saginata, and T. solium were incubated in vitro in culture medium, test serum, and a source of complement, and oncosphere killing was assessed after 10 days of culture. In vitro oncosphere killing reflected the presence of specific antibody, and the oncosphere-killing assay typically indicated immunity to the homologous parasite that had been determined in vivo. This study describes the first reliable oncosphere-killing assays for T. pisiformis, T. ovis, T. saginata, and T. solium. These assays will be used for further research into the optimization of recombinant vaccines against cysticercosis.     

Winter Habitat Selection by Canada Lynx in Maine: Prey Abundance or Accessibility?

Abstract: We related winter habitat selection by Canada lynx (Lynx canadensis), relative abundance of snowshoe hares (Lepus americanus), and understory stem densities to evaluate whether lynx select stands with the greatest snowshoe hare densities or the greatest prey accessibility. Lynx (3 F, 3 M) selected tall (4.4-7.3 m) regenerating clear-cuts (11-26 yr postharvest) and established partially harvested stands (11-21 yr postharvest) and selected against short (3.4-4.3 m) regenerating clear-cuts, recent partially harvested stands (1-10 yr), mature second-growth stands (>40 yr), and roads and their edges (30 m on either side of roads). Lynx selected stands that provided intermediate to high hare density and intermediate cover for hares (i.e., prey access) but exhibited lower relative preference for stand types with highest hare densities where coniferous saplings exceeded 14,000 stems/ha.     

Helminth communities of an introduced hare (Lepus granatensis) and a native hare (Lepus europaeus) in southern France

We investigated the parasite communities of introduced Iberian hares (Lepus granatensis) and native European hares (Lepus europaeus) in southern France, where Iberian hares were introduced locally 20 yr ago as a game animal. Parasite communities of sympatric populations of the two hare species and of allopatric populations of European hares were compared. Iberian hares in France harbored a depauperate community of parasites relative to the population in its native habitat in Spain. European hares in areas of sympatry also were infected by Nematodiroides zembrae, which normally infects Iberian hares on their native range.