Helminth Collection and Identification from Wildlife

Wild animals are commonly parasitized by a wide range of helminths. The four major types of helminths are "roundworms" (nematodes), "thorny-headed worms" (acanthocephalans), "flukes" (trematodes), and "tapeworms" (cestodes). The optimum method for collecting helminths is to examine a host that has been dead less than 4-6 hr since most helminths will still be alive. A thorough necropsy should be conducted and all major organs examined. Organs are washed over a 106 μm sieve under running water and contents examined under a stereo microscope. All helminths are counted and a representative number are fixed (either in 70% ethanol, 10% buffered formalin, or alcohol-formalin-acetic acid). For species identification, helminths are either cleared in lactophenol (nematodes and small acanthocephalans) or stained (trematodes, cestodes, and large acanthocephalans) using Harris'' hematoxylin or Semichon''s carmine. Helminths are keyed to species by examining different structures (e.g. male spicules in nematodes or the rostellum in cestodes). The protocols outlined here can be applied to any vertebrate animal. They require some expertise on recognizing the different organs and being able to differentiate helminths from other tissue debris or gut contents. Collection, preservation, and staining are straightforward techniques that require minimal equipment and reagents. Taxonomic identification, especially to species, can be very time consuming and might require the submission of specimens to an expert or DNA analysis.     

Endoparasites of black-bellied whistling ducks in southern Texas.

Endoparasites detected in the black-bellied whistling duck (Dendrocygnaautumnalis) include one nasal mite, four nematodes, three trematodes, five cestodes, and two acanthocephalans. Each of these represents a new host record. Overall, 47% of the birds were parasitized with an average of 12 helminths per infected bird. Helminths were significantly more common in juveniles than in adults; more females than males were parasitized, but the difference was not statistically significant. No correlation existed between the parasite load and the physical condition of the host. Tissue damage in infected birds was minimal and limited to nematode cysts in the proventriculi. Parasite loads were light, apparently reflecting the food habits of the host.     

Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents

The latitudinal diversity gradient (LDG), or the trend of higher species richness at lower latitudes, has been well documented in multiple groups of free‐living organisms. Investigations of the LDG in parasitic organisms are comparatively scarce. Here, I investigated latitudinal patterns of parasite diversity by reviewing published studies and by conducting a novel investigation of the LDG of helminths (parasitic nematodes, trematodes and cestodes) of cricetid rodents (Rodentia: Cricetidae). Using host–parasite records from 175 parasite communities and 60 host species, I tested for the presence and direction of a latitudinal pattern of helminth richness. Additionally, I examined four abiotic factors (mean annual temperature, annual precipitation, annual temperature range and annual precipitation range) and two biotic variables (host body mass and host diet) as potential correlates of parasite richness. The analyses were performed with and without phylogenetic comparative methods, as necessary. In this system, helminths followed the traditional LDG, with increasing species richness with decreasing latitude. Nematode richness appeared to drive this pattern, as cestodes and trematodes exhibited a reverse LDG and no latitudinal pattern, respectively. Overall helminth richness and nematode richness were higher in areas with higher mean annual temperatures, annual precipitation and annual precipitation ranges and lower annual temperature ranges, characteristics that often typify lower latitudes. Cestode richness was higher in areas of lower mean annual temperatures, annual precipitation and annual precipitation ranges and higher annual temperature ranges, while trematode richness showed no relationship with climate variables when phylogenetic comparative methods were used. Host diet was significantly correlated with cestode and trematode species richness, while host body mass was significantly correlated with nematode species richness. Results of this study support a complex association between parasite richness and latitude, and indicate that researchers should carefully consider other factors when trying to understand diversity gradients in parasitic organisms.     

Helminth parasites of wild boar, Sus scrofa, in Iran.

Fifty-seven wild boars (Sus scrofa) from protected regions of Iran were examined for helminths. Sixteen species of helminths were collected; there were ten nematodes, one acanthocephalan, two trematodes and three larval cestodes. New host and distribution records were established for all helminths except of Taenia solium cysticerci. Wild boar shared nine of these helminths with domestic pigs, six with ruminants and three with human beings in Iran. Metastrongylus pudendotectus and M. salmi are reported for the first time from Iran.     

A comparative analysis of the helminth fauna of kittiwake Rissa tridactyla (Linnaeus, 1758) and glaucous gull Larus hyperboreus Gunnerus, 1767 from different parts of the Barents Sea

The article is based on the results of helminthological observations made on kittiwake Rissa tridactyla and glaucous gull Larus hyperboreus in 1991-2001 in different areas of the Barents Sea (Eastern Murman coast, Franz Josef Land, Novaya Zemlya, Spitzbergen). 18 helminth species (2 trematodes, 11 cestodes, 4 nematodes, and 2 acanthocephalans) were recorded in the kittiwakes and 19 (3 trematodes, 9 cestodes, 5 nematodes and 2 acanthocephalans) species were recorded in the glaucous gulls. Trematodes were absent in the birds collected at the Franz Josef Land and the northern island of Novaya Zemlya. 3 trematode species, namely Gymnophallus sp. (somateria?), Microphallus sp. 1 (M. pseudopygmaeus), and Cryptocotyle lingua were found in the glaucous gulls of western Spitzbergen. It was supposed that the life cycles of these parasites can be completed there. On the other hand, coastal ecosystems of Arctic archipelagoes turn out to be favourable for the transmission of some cestodes. This is closely connected with the regional traits in the marine bird diet, namely the increase of the amphipod (intermediate hosts of hymenolepidids and some dilepidids) and polar cod (supposed second intermediate host for some tetrabothriids) portion in Arctic. As a result, cestodes are the base of the helminth fauna of kittiwakes and glaucous gulls of the Barents Sea, by their species richness, prevalence and abundance. Nematodes and acanthocephalans were represented by a few species with low infection intensity. The main ecological factors affected the regional difference in the species richness and abundance of the helminths parasitising kittiwakes and glaucous gulls in the Barents Sea are proposed. Those are regional climatic features and regional traits in the behaviour and food priorities of birds, and also the distribution of the helminths intermediate hosts, invertebrates and fishes. The phenomenon of host specificity lowering with respect to the definitive host was recorded in some cestode species (Microsomacanthus diorchis, M. microsoma, and Arctotaenia tetrabothrioides) on the border of their distribution ranges, the coastal ecosystems of Arctic.     

Life history, ecology and parasite community structure in Soviet birds

The paper describes an investigation of parasite richness in relation to host life history and ecology using data from an extensive survey of helminth parasites (cestodes, trematodes and nematodes) in Soviet birds. Correlates of parasite richness (number of parasite species per host species) were sought among 13 life-history variables, 13 ecological variables and one non-biological variable (number of host individuals examined) across a sample of 158 species of host. A statistical method to control for the effects of phylogenetic association was adopted throughout. Parasite richness correlates positively with the number of hosts examined (sample size) in all three parasite groups. Positive correlations (after controlling for the effects of sample size) were also found between host body weight and parasite richness for trematodes and nematodes, but not for cestodes.
A number of ecological variables were associated with parasite richness. However, when the effects of sample size and body weight were controlled for, only a single significant correlation (an association between trematode richness and aquatic habitat) remained. Similarly, a number of significant correlates of parasite richness were found among the life-history variables examined. Though several of these were robust to the confounding effects of sample size, all could be explained by the co-variation between life-history traits and body weight among the host species under investigation.     

Helminths of Hudsonian godwits, Limosa haemastica, from Alaska and Manitoba

In total, 21 Hudsonian godwits, Limosa haemastica (Charadriiformes: Scolopacidae), were examined for helminths, 10 from Bristol Bay, Alaska, and 11 from Churchill, Manitoba. Seventeen species of helminths (9 trematodes, 6 cestodes, 2 nematodes) were collected, but only 1 trematode species, Plagiorchis elegans, was found in common between the 2 sample sites. All 17 species are new records for this host and 2 cestodes, Capsulata edenensis and Malika limosa, are new records for North America. In general, both prevalence and intensities were low, and species richness ranged from 1 to 6 (mean = 2.4). Most of the differences in the helminth faunas between the 2 sites were attributed to difference in habitats, freshwater in Manitoba versus saltwater in Alaska.     

Parasitic helminths of flying starlings (Sturnus vulgaris L.) in their nesting area

1.150 flying starlings and 226 pulli have been necropsied and their helminth parasites collected. Localities where the birds has been captured are given in table 1 and the map. Flying birds are parasited in the proportion of 97.1%. There are three trematodes species, eight cestodes, six nematodes and one acanthocephalan (table 2). Differences are noted according with the locality, the season and the age of the bird. Pulli are parasited by 47% with a very important difference between the two places. The number of parasitic species is lesser: one trematode, two cestodes and three nematodes. The helminthological fauna of belgian starlings seems common but more important and much varied that in the birds hibernating in North Africa.     

Latitudinal gradient in the taxonomic composition of parasite communities

Although latitudinal gradients in diversity have been well studied, latitudinal variation in the taxonomic composition of communities has received less attention. Here, we use a large dataset including 950 surveys of helminth endoparasite communities in 650 species of vertebrate hosts to test for latitudinal changes in the relative contributions of trematodes, cestodes, nematodes and acanthocephalans to parasite assemblages. Although the species richness of helminth communities showed no consistent latitudinal variation, their taxonomic composition varied as a function of both host type and latitude. First, trematodes and acanthocephalans accounted for a higher proportion of species in helminth communities of fish, whereas nematodes achieved a higher proportion of the species in communities of bird and especially mammal hosts. Second, the proportion of trematodes in helminth communities of birds and mammals increased toward higher latitudes. Finally, the proportion of nematodes per community increased toward lower latitudes regardless of the type of host. We present tentative explanations for these patterns, and argue that new insights in parasite community ecology can be gained by searching for latitudinal gradients not only in parasite species richness, but also in the taxonomic composition of parasite assemblages.     

Helminth community structure of sympatric eastern American toad, Bufo americanus americanus, northern leopard frog, Rana pipiens, and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin

One-hundred twelve amphibians, including 51 blue-spotted salamanders, Ambystoma laterale, 30 eastern American toads, Bufo americanus americanus, and 31 northern leopard frogs, Rana pipiens, were collected during April-October 1996 from Waukesha County, Wisconsin and examined for helminth parasites. The helminth compound community of this amphibian assemblage consisted of at least 10 species: 9 in American toads, 8 in leopard frogs, and 3 in blue-spotted salamanders. American toads shared 7 species with leopard frogs, and 2 species occurred in all 3 host species. Although there was a high degree of helminth species overlap among these sympatric amphibians, statistically significant differences were found among host species and percent of indirect or direct-life cycle parasites of amphibian species individual component communities (chi2 = 1,015, P < 0.001). American toads had a higher relative abundance of nematodes, 59%, than larval cestodes, 31%, and larval and adult trematodes, 10%, whereas leopard frogs had a higher relative abundance of larval cestodes, 71.3%, and larval and adult trematodes, 25.3%, than nematodes 3.4%. This is related to ecological differences in habitat and dietary preferences between these 2 anuran species. Helminth communities of blue-spotted salamanders were depauperate and were dominated by larval trematodes, 94%, and few nematodes, 6%. Low helminth species richness in this host species is related to this salamander's relatively small host body size, smaller gape size, lower vagility, and more fossorial habitat preference than the other 2 anuran species. Adult leopard frogs and toads had significantly higher mean helminth species richness than metamorphs, but there was no significant difference in mean helminth species richness among adult and metamorph blue-spotted salamanders. Considering adult helminths, the low species richness and low vagility of caudatans as compared with anurans suggest that local factors may be more important in structuring caudatan helminth communities of salamanders than of anuran hosts. Helminth species infecting salamanders may be more clumped in their geographic distribution as compared with anurans, and the role of other hosts and their parasites at the compound community level may be important in structuring helminth communities of salamanders.     

The serotonin and dopamine content of helminths in different classes

Analysis of the presented data shows that in all representatives of cestodes serotonin is present, dopamine being found only in few species. In trematodes, the dominant amine is presented by dopamine, whereas in some trematodes serotonin was also found. Concentration of biogenic amines in other classes of helminths is usually essentially lower than that in cestodes and trematodes.     

Qualitative and quantitative aspects of recent research on helminth parasites

Relationships between the species diversity of different taxa, the mean number of articles published per year on each taxon, and the mean impact factor of the journals in which they appear, were examined across six taxa of helminths: Nematomorpha, Acanthocephala, Monogenea, Trematoda, Cestoda and Nematoda, the latter including only animal parasitic nematodes. The mean annual output of scientific articles per taxon was not related to the species diversity of these taxa or, at least, not significantly. Thus, the large volume of publications on nematodes is not merely a reflection of their estimated diversity. There were significant differences among taxa in the mean impact factor of the journals in which papers on each taxon appeared, with nematodes having the highest mean score, followed by trematodes and cestodes. In addition, across the six taxa, the mean journal impact factor correlated positively and significantly with the mean annual number of papers published: not only are there more papers published on nematodes and trematodes than on nematomorphs or acanthocephalans, but they are also generally published in higher-ranking journals. These results suggest that there is an increasing gap in the quantity and general importance of the research carried out on different helminth taxa.     

Intestinal helminths of capybaras, Hydrochoerus hydrochaeris, from Venezuela

Quantitative parameters of intestinal helminth species and their potential relations to host characteristics in a population of capybaras (Hydrochoerus hydrochaeris) from Venezuela are reported for the first time. The intestines of 40 capybaras were collected during the 1992-annual harvest at Hato El Cedral. Six helminth species were found: 2 cestodes (Monoecocestus macrobursatum, M. hagmanni), 2 nematodes (Viannella hydrochoeri, Protozoophaga obesa), and 2 trematodes (Hippocrepis hippocrepis, Taxorchis schistocotyle). This is the first report for M. macrobursatum in Venezuela. Helminth abundance did not differ between sexes or age classes. Although patterns of distribution for all helminth species were overdispersed, the high prevalence found for all species (over 70%) and the high abundance observed for nematodes made it difficult to assess the effect that these helminths may produce on capybaras. Nevertheless, the negative associations found between the body condition of capybaras and helminth intensity for M. macrobursatum and V. hydrochoeri, might be pointing out potential host population regulatory role for these parasites which require further research.     

Distribution patterns and microhabitat segregation in gastrointestinal helminths of Sorex shrews

We studied the distribution patterns and microhabitat use in gastrointestinal helminths of the shrews Sorex araneus and S. caecutiens in Finland. The distribution of species prevalences was bimodal, and in S. araneus the abundance (mean intensity) was positively associated with commonness (prevalence), as assumed by the core-satellite species hypothesis (Hanski 1982). However, the positive correlation between prevalence and intensity was observed only when the effects of helminth body size and taxonomic group (cestodes vs nematodes) on intensity were controlled for. The nematodes of the genus Longistriata occurred predictably as core species, whereas the identity of the core cestodes was more variable between host species and regions. Helminth body size and taxonomic group were not related to the degree of aggregation in shrew populations, but helminth body size seemed to explain the differences in the distribution patterns of helminths between shrews and voles. The core species did not show more segregation in microhabitat use than randomly selected species. In fact, the two core nematodes showed largely overlapping intestinal distributions. We conclude that linear intestinal space is not a key resource for shrew nematodes, but it may be for shrew cestodes.     

Ecdysteroids in helminths and annelids

Summary

This review focuses on recent research developments in the past three years concerning ecdysteroid biochemistry in helminths and annelids, with emphasis on results reported at the IXth Ecdysone Workshop in Paris, France, in September 1989. During the past three years, most of the research in this area has been concentrated on nematodes, in several species of which the occurrence of ecdysteroids has been demonstrated. Interesting biological effects of exogenously applied ecdysteroids have been discovered on meiotic reinitiation in oocytes of the dog heartworm, Dirofilaria immitis, and on microfilarial production by Brugia pahangi. These effects, together with previous discoveries, demonstrate the feasibility of affecting nematode physiology with exogenously applied ecdysteroids. However, experiments with four species of nematodes in three separate laboratories have failed to demonstrate that nematodes biosynthesize ecdysteroids from cholesterol. Therefore, it remains to be proven whether ecdysteroids are truly endogenous nematode hormones or are merely compounds with strong biological activity. Research with cestodes and trematodes has similarly revealed that ecdysteroids occur in these organisms and that the compounds have possible regulatory roles, but experiments demonstrating endogenous biosynthesis have yet to be performed. Annelids, which are more closely related to insects than helminths, also contain ecdysteroids; recent research has demonstrated the C-20 hydroxylation of ecdysone to 20-hydroxyecdysone, the active moulting hormone of most insects. Experiments to demonstrate this metabolic step in helminths have failed.     

The component helminth community in six sympatric species of Ardeidae

We studied the helminth communities in 6 sympatric species of Ardeidae (Ixobrychus minutus (Linnaeus, 1766), Nycticorax nycticorax (Linnaeus, 1758), Bubulcus ibis (Linnaeus, 1758), Egretta garzetta (Linnaeus, 1766), Ardea cinerea (Linnaeus, 1758), and Ardea purpurea (Linnaeus, 1766)) from "La Albufera de Valencia," Spain. The survey revealed 13 species of helminth parasites: 5 digeneans, 2 cestodes, and 6 nematodes. The component helminth communities of the Ardeidae examined are depauperate and conform to the pattern typically found in isolationist communities, probably because of their high trophic dependence on a few prey species. Evenness was positively correlated with richness and abundance, but host body weight was not correlated with the number of helminth species or with the total number of helminths. Ardea cinerea is more heavily infected than E. garzetta by Apharyngostrigea cornu, and B. ibis is more heavily infected than both Ardea cinerea and E. garzetta by Desportesius spinulatus. Apharyngostrigea cornu was positively associated with Desmidocercella numidica and D. spinulatus in A. cinerea.     

A study of the internal parasites of small rodents from woodland areas in Surrey

The occurrence of helminth parasites and leptospires from the Long-tailed field mouse, Apodemus sylvaticus , the Bank vole, Clethrionomys giareolus and the Short-tailed vole, Microtus agrestis has been studied from four woodland areas in Surrey. The composition of the helminth fauna of these rodents, particularly A. sylvaticus and C. giareolus , differs from that of previous studies carried out in the British Isles in consisting largely of cestodes and fewer species of digeneans and nematodes. On the other hand the degree of infection of the rodents with nematodes as in the case of A. sylvaticus infected with the trichostrongylid Nematospiroides dubius and theoxyurid Syphacia stroma and of C. giareolus with thecap-illarid Capillaria muris sylvatici is greater than the cestode and digenean infections and is probably linked with the monoxenous nature of the nematode life cycles.
Differences in the number, incidence and degree of infection of mice and voles with species of helminths is undoubtedly linked with differences in the feeding habits of the respective hosts but the present study has also confirmed that infection levels in both leptospires and helminths are influenced by the age/sex relationships of the host together with season and habitat. The relationship between the distribution of rodents infected with leptospires and some helminths suggests similarities in the mode of their transmission.     

Parasitic helminths of Eurasian collared-doves (Streptopelia decaocto) from Florida

Sixty-three Eurasian collared-doves (ECDs) (Streptopelia decaocto) from Florida were examined for parasitic helminths from June to December 2001. Nine species of helminths were identified (5 nematodes, 2 cestodes, and 2 trematodes). The most prevalent helminths were Ascaridia columbae (73.0%), Fuhrmannetta crassula (28.6%), Ornithostrongylus quadriradiatus (12.7%), and Bruscapillaria obsignata (11.1%). The helminths with the greatest mean intensity were Tanaisia bragai (13.5), A. columbae (9.3), and O. quadriradiatus (7.1). In Florida, the mean intensity of A. columbae in ECDs (9.3) was similar to that found in white-winged doves (Zenaida asiatica) (9.1) (P = 0.461), and both the intensities were significantly higher than that in the native mourning doves (Zenaida macroura) (3.7) (P = 0.001 and 0.005, respectively). Fuhrmannetta crassula is reported for the first time in columbids from Florida.     

Helminth infracommunities of the frogs Rana catesbeiana and Rana clamitans from Turkey Marsh, Michigan

One hundred twenty-seven bullfrogs, Rana catesbeiana, and 120 green frogs, Rana clamitans, collected in July and August 1987 from Turkey Marsh, Michigan, were examined for helminths. Of the 16 helminth species found, Falcaustra catesbeianae had the highest prevalence and mean intensity in bullfrogs. In green frogs, Megalodiscus temperatus had the highest prevalence and Haematoloechus parviplexus had the highest mean intensity. Taxonomically, 1,030 (30.5%) trematodes and 2,348 (69.5%) nematodes occurred in bullfrogs; 2,874 (96.4%) trematodes, 2 (0.1%) cestodes, and 105 (3.5%) nematodes were found in green frogs. The larger and more aquatic of the 2 hosts, R. catesbeiana, had the highest mean number of helminth species, helminth intensity, diversity, and evenness. Adult frogs of both species had a significantly higher mean number of helminth species than did juveniles. Significant correlations existed between the number of helminth species and frog length. Although the helminth communities of Turkey Marsh frogs are isolationist in character, they are more diverse than other helminth communities studied in amphibians.     

Helminthiasis, metabolic rates and cold resistance in the red-backed vole from a natural population

Estimation of the standard metabolic rate (SMR), maximal oxygen consumption (MOC) and thermoregulation ability in males of red-backed vole (Clethrionomys rutilus Pallas, 1779) have shown that individuals infected with nematodes Heligmosomum mixtum, regardless of intensity of worm infection, had an increased level of oxygen consumption in the cold exposition, while the individuals infected with the cestodes Arostrilepis horrida, had a lover oxygen consumption than non-invaded individuals. Worm burden of A. horrida correlated negatively with MOC value in the hosts. Thermo-conductance of individuals infected with A. horrida was significantly lower than in ones infected with H. mixtum. Opposite effects of these two helminthes seems to be determined by the specificity of pathogenesis and different body mass of parasites. Total body mass of nematodes are usually less than 0.2% of the host body mass whereas the total body mass of cestodes may exceed 5% of the host body mass.