Dirofilaria Scapiceps Research Articles

Endoparasites found in European brown hares (Lepus europaeus) hunted in Macedonia, Greece

Abstract The European brown hare (Lepus europaeus) is widespread throughout Europe with population declines in some countries. Parasites can be one of the natural regulative factors of hare population. The information about the prevalence of endoparasites of European hares in Southern Europe is limited while relevant data from Greece are lacking. Gastrointestinal tracts of 84 Lepus europaeus, hunted in Macedonia, Greece, were examined for endoparasites. Sixty two (73.8 %) of the animals were parasitized by one or multiple parasitic species. Eimeria spp. was found in 54 (64.28 %) of the gastrointestinal tracts, Trichostrongylus retortaeformis in 42 (50 %), Trichuris leporis in 18 (21.42 %), Dicrocoelium dentriticum in 8 (9.52 %), Passalurus ambiguus in 4 (4.76 %) and Protostrongylus spp. in 2 (1.22 %). Moreover, Linguatula serrata larvae were found in 16 (19.04 %) animals and Dirofilaria scapiceps in one. Mixed infections were significantly more common than single infections. Although the parasites found do not represent a threat for other animal species, under certain conditions, they may play an important role in the health status of hares.

DO PARASITISM AND NUTRITIONAL STATUS INTERACT TO AFFECT PRODUCTION IN SNOWSHOE HARES?

We evaluated the hypothesis that the effects of parasitism on animal body condition are accentuated when host nutritional status is compromised. In a field experiment we manipulated natural burdens of five nematode species via anthelmintic treatment in one- half the free-ranging snowshoe hares (Lepus americanus) on each of six study areas and supplemented overwinter food level on three areas, to assess whether treatments interacted synergistically. We predicted that the effects of parasitism would be aggravated in mal- nourished hares (i.e., hares not administered supplemental food), and that animals receiving both treatments would have (1) lower parasite burdens, and (2) higher body mass, fat storage, and reproduction, than those receiving only one or no treatments. Mean numbers of Trichuris leporis were lower in hares subjected to food supplementation, suggesting that nutritional status affected immunity to that species. Obeliscoides cuniculi, Nematodirus triangularis, Dirofilaria scapiceps, and Protostrongylus boughtoni numbers were not directly affected by supplementation. Body mass of parasite-normal controls (i.e., not administered the anthelmintic treatment) was negatively correlated to nematode abundance during May- June, implying that parasitism had a deleterious effect on hare mass at that time. However, the anthelmintic treatment failed to directly affect hare body mass, fat storage, or repro- duction. Food supplementation had a positive effect on body mass, fat storage, and repro- duction, although effects of food were neither strong nor consistent among study areas and body condition parameters being measured. Only 2 of 22 analyses of hare production yielded marginally significant (i.e., 0.05 < P < 0.10) interactions between food and parasitism; therefore, we concluded that the two factors were not strongly linked. However, because our snowshoe hare population was at low densities and likely exposed to neither severe food shortage nor high rates of nematode parasitism, failure to detect an interaction between treatments may not comprise a general refutation of the hypothesis. Rather, hare populations subject to more serious food limitation (i.e., during a cyclic peak in numbers) may be apt to display stronger interactions between nutrition and parasitism.

Interactive Effects of Sublethal Nematodes and Nutritional Status on Snowshoe Hare Vulnerability to Predation

1. We studied the effect of parasitism on snowshoe hare (Lepus americanus) survival through a field experiment that reduced natural burdens of sublethal nematodes in a free-ranging hare population. We treated half the hares on each of six study areas year-round with an anthelminthic drug, and the other half with a placebo. Potential interactive effects of parasitism and nutrition were examined by supplementing the natural food supply on three of the six study areas during two winters. Survival was measured by radio-collaring a total of 612 hares with mortality-sensitive transmitters and monitoring survival daily between April 1991 and June 1993. 2. Overall, nematode burdens in hares were highest between March and October, and Obeliscoides cuniculi was the most abundant of the five species present. The proximate cause of 95% of mortalities (n = 318) during the study was predation. Predators killed hares with heavy burdens of O. cuniculi disporportionately during May-June, but burdens of the four other species (Nematodirus triangularis, Trichuris leporis, Dirofilaria scapiceps, Protostrongylus boughtoni) were similar between predator-killed hares and the live population. 3. During May-October 1991, the anthelminthic treatment did not affect hare survival, but during May-October 1992 survival of parasite-reduced hares was 2.4-times higher than that of controls. During November 1991-April 1992 survival of food supplemented hares was 21% higher than food-normal animals, but survival was similar during November 1992-April 1993. 4. The effect of parasite-reduction on hare survival was apparently contingent on overwinter food supplies between November 1991 and April 1992, with survival being highest in hares subjected to both treatments, intermediate in those receiving only food supplementation, and lowest in unfed hares. We conclude that the effect of sublethal nematode parasitism on hare survival can be important if interactive with predation, and that synergistic effects of parasitism and nutrition may affect hares if food availability is limited.

The efficacy of anthelmintic treatment on the parasite abundance of free-ranging snowshoe hares

We examined the efficacy of an anthelmintic agent (ivermectin, Merck–Agvet) on the parasitic nematodes of free-ranging snowshoe hares (Lepus americanus) during 27 months in southern Manitoba. Marked hares on six 25-ha sites were injected bimonthly with ivermectin (treatment, n = 134) or propylene glycol (control; n = 149) and carcasses were necropsied to determine prevalence and intensity of Obeliscoides cuniculi, Nematodirus triangularis, Trichuris leporis, Dirofilaria scapiceps, and Protostrongylus boughtoni. We supplemented the control sample with hares (n = 175) captured off the study sites and not given propylene glycol. Mean prevalence (percentage of hosts infected) and intensity (number of parasites among infected hosts) of each nematode species decreased after treatment and were 35 – 85% lower than controls after 20–40 days. Treatment significantly reduced prevalence of D. scapiceps and P. boughtoni for about 50 days and of O. cuniculi and N. triangularis for longer periods. Overall intensity of O. cuniculi, N. triangularis, and P. boughtoni was significantly lower in treated than in control hares, and intensity of D. scapiceps was marginally (P &lt; 0.10) lower for 50 days post treatment. Total reductions in nematode abundance (prevalence × intensity) ranged from 29 to 88% among the five species. Neither prevalence nor intensity of ticks (Haemaphysalis leporispalustris) was reduced following treatment. We conclude that ivermectin is effective at controlling nematodes in snowshoe hares but that its efficacy is variable among species. We use our results as a basis for discussing the applicability of anthelmintics to the conservation and management of free-ranging wild mammals.

Prevalence of helminths in a cyclic snowshoe hare population.

Five species of helminths were monitored in a population of snowshoe hares (Lepus americanus) near Rochester, Alberta, during 1961-1977. Prevalence of both Obeliscoides cuniculi and Protostrongylus boughtoni among young hares averaged about 50% by age 2 mo, then tended to level off. Prevalence of Taenia pisiformis (cysticerci) and Dirofilaria scapiceps rose more slowly, but continued to increase steadily beyond their mean levels of 8% and 1% at age 2 mo. There were well defined seasonal (within-year) cycles in prevalence of O. cuniculi and P. boughtoni that were generated evidently to a major degree by arrested development of larvae in fall and renewed development in late winter. It was hypothesized that renewed larval development was triggered (in February) in O. cuniculi by the seasonal rise of circulating pituitary gonadotrophins, and (in April) in P. boughtoni by the seasonal rise of gonadal androgens and estrogens. Indices to gonadal hormone levels in hares indicated that these increased most rapidly among males, and may have accounted for the higher prevalences of P. boughtoni in males during April-May. Neither T. pisiformis nor D. scapiceps exhibited conspicuous seasonal changes in prevalence. Maximum prevalence of T. pisiformis was attained at about 1 yr of age, whereas D. scapiceps increased among adult snowshoes through age 2 yr before stabilizing. Long-term (between-year) changes in prevalence of O. cuniculi, T. pisiformis, and D. scapiceps were correlated significantly with the cyclic hare population which declined from a peak in fall 1961 to a low in 1965-1966, rose to another peak by fall 1970, and declined again to a low in 1975. There was no detectable time lage between this "10-yr" cycle in hare density and the cycles of parasite prevalence among juveniles (less than 1 yr of age). Among adult hares, the cycle of O. cuniculi prevalence was likewise synchronous with that of the hare population, but the cycles of D. scapiceps and T. pisiformis lagged by approximately 1 and 2 yr, respectively. This lag in T. pisiformis prevalence was largely inexplicable to us. Our data on P. boughtoni were not suitable for analyses of between-year trends; nor were those for the fifth helminth, Taenia serialis (coenuri), because mean prevalence was less than 1% among both juveniles and adults. An apparent decline in T. serialis after the early 1950's, and its continued scarcity thereafter, paralleled a major change in numbers of one important definitive host--the red fox (Vulpes vulpes).(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Development of Dirofilaria scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in lagomorphs

Development of Dirofilaria scapiceps (Leidy, 1886) was followed in 34 experimentally infected cottontail rabbits (Sylvilagus floridanus). Worms were recovered from all rabbits and intensity ranged from 8 to 76% of the number of infective larvae inoculated. Development to subadults occurred in subcutaneous tissues in various regions of the body; the specific region was influenced by the site of inoculation. The third and fourth moults occurred at 6 and 12 days postinoculation, respectively. Subadults migrated through the subcutaneous tissues and arrived in the ankles as early as 16 days postinoculation. Worms were sexually mature by 67 days. The prepatent period was 137–234 days and the microfilaraemia was nonperiodic. Few worms in cottontail rabbits degenerated or died and rabbits with 1-year-old infections could be reinfected. Dirofilaria scapiceps was recovered from 12 of 14 experimentally inoculated snowshoe hares (Lepus americanus) and 2 of 4 New Zealand white domestic rabbits (Oryctolagus cuniculus). Intensity in snowshoe hares and domestic rabbits ranged from 0.4 to 15% and 6 to 7%, respectively, of the number of infective larvae inoculated. Many worms in these hosts degenerated or died.

Development of Dirofilaria scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in Aedes spp. and Mansonia perturbans (Walker) and responses of mosquitoes to infection

Dirofilaria scapiceps (Leidy, 1886) developped in the abdominal fat body of Aedes canadensis, A. euedes, A. excrucians, A. provocans, A. punctor, A. stimulans/fitchii, A. vexans, and Mansonia perturbans which occur in enzootic areas in Ontario. Abundances of third-stage larvae were greatest in A. euedes and A. excrucians. Transmission took place in July and August. Development also occurred in Aedes aegypti (Liverpool strain) but not in A. triseriatus and A. trivittatus. Larvae in A. euedes and A. excrucians developed within syncytia containing hypertrophied adipocyte nuclei; third-stage larvae were first observed at 10 days postinfection (26 °C) and all larvae invariably developed to the third stage. Syncytia containing hypertrophied adipocyte nuclei apparently act as a nutrient source and may be essential for normal development of larvae. In A. stimulans/fitchii, syncytia did not form or formed abnormally, a longer period (12 days) was required for development to the third stage, and many larvae failed to reach the third stage. Many developing larvae in A. aegypti were surrounded by syncytia but adipocyte nuclei in them were not hypertrophied. Larvae in A. aegypti given one blood meal commonly did not reach the third-stage, although development proceeded normally in A. aegypti given two blood meals. Third-stage larvae have postdeirids, two terminal caudal papillae, and a terminal caudal cuticular cap and are readily distinguished from third-stage larvae of other Dirofilaria species. Male third-stage D. scapiceps possess spicular pouch primordia, previously unreported in infective filarioid larvae.

Zoogeography and taxonomy of Dirofilaria scapiceps (Leidy, 1886) and D. uniformis Price, 1957 (Nematoda: Filarioidea) of lagomorphs in North America

Dirofilaria scapiceps (Leidy, 1886) was found in 62% of 404 Lepus americanus, 27% of 89 Sylvilagus floridanus, 13% of 31 Orytolagus cuniculus (domestic), 4% of 26 L. capensis, and none of 15 L. timidus, 2 L. californicus, and 50 L. townsendii collected in various regions of North America. Dirofilaria scapiceps in L. capensis is a new host record. The two species of Dirofilaria, D. scapiceps and D. uniformis Price, 1957, known from lagomorphs are redescribed. Dirofilaria scapiceps occurs predominantly in connective tissue surrounding tendons in the ankle region and rarely in intermuscular fascia near the knee joint of the hind leg; D. uniformis occurs in subcutaneous tissues of the trunk. Both D. scapiceps and D. uniformis are known only from lagomorphs in North America, D. scapiceps from L. americanus, L. capensis, S. floridanus, S. palustris and O. cuniculus and D. uniformis from S. floridanus, S. palustris and O. cuniculus. Dirofilaria scapiceps is present in lagomorphs in Alaska, Canada, eastern United States and Wyoming whereas D. uniformis is known only from lagomorphs in southeastern and south central United States. Dirofilaria uniformis may have evolved, through paedomorphosis, from D. scapiceps.

Endoparasites of selected populations of cottontail rabbits (Sylvilagus floridanus) in the southeastern United States.

During the fall of 1966 and spring of 1967, 260 cottontail rabbits (Sylvilagus floridanus) were collected from 13 sites in 8 southeastern states and examined for endoparasites. In order of prevalence, the endoparasites found were: Obeliscoides cuniculi, Trichostrongylus calcaratus, Trichostrongylus affinis, Taenia pisiformis (cysticerci), Raillietina salmoni, Eimeria spp., Longistriata noviberiae, Cittotaenia variabilis, Hasstilesia tricolor, Trichuris leporis, Dermatoxys veligera, Passalurus ambiguus, Dirofilaria scapiceps, Sarcocystis sp., Linguatula serrata, Nematodirus leporis, and Gongylonema pulchrum. Data are presented on prevalance and intensity of infection with each parasite along with information on geographic distribution. Cottontail rabbits in the southeastern United States show a higher level of parasitism than has been reported from other regions, although these higher parasite burdens were not necessarily associated with increased host morbidity.

HELMINTH PARASITES IN SNOWSHOE HARES FROM NORTHERN MICHIGAN

The incidence of helminth parasites in snowshoe hares (Lepus americanus) was studied in 1957–1962 in Michigan's Upper Peninsula. Seventy-five hares were examined for the presence of all helminths, 210 only for certain parasites. Adult tapeworms were present in 5 of 75 (6.7%) hares examined, cysticerci of Taenia pisiformis in 88 of 210 (41.9%), and coenuri of Multiceps sp. in 15 of 179 (8.4%). Nine genera of nematodes were found. Obeliscoides cuniculi occurred most frequently, Nematodirus sp. least frequently. Protostrongylus sp. and Obeliscoides cuniculi appeared to produce pathogenic effects, and Multiceps sp. and Dirofilaria scapiceps may have impaired movement of some hares.

Dirofilaria scapiceps from Snowshoe Hare in Connecticut

Dirofilaria scapiceps from Snowshoe Hare in Connecticut

Vectors, Transmission, Development, and Incidence of Dirofilaria scapiceps (Leidy, 1886) (Nematoda) from the Snowshoe Hare in Minnesota

Microfilariae were recovered from the blood contained in the gut of an engorged tick removed from the ear of a snowshoe hare, Lepus americanus phaeonotus Allen, which was captured near Baudette, Minnesota. The hare, from which subsequently 8 adult female and 7 adult male Dirofilaria scapiceps (Leidy, 1886) were recovered, was subjected to feeding experiments with mosquitoes in order to determine some of the susceptible vectors of the parasite, and to transmit the infection experimentally.