Prevention of population cycles by parasite removal.

The regular cyclic fluctuations in vertebrate numbers have intrigued scientists for more than 70 years, and yet the cause of such cycles has not been clearly demonstrated. Red grouse populations in Britain exhibit cyclic fluctuations in abundance, with periodic crashes. The hypothesis that these fluctuations are caused by the impact of a nematode parasite on host fecundity was tested by experimentally reducing parasite burdens in grouse. Treatment of the grouse population prevented population crashes, demonstrating that parasites were the cause of the cyclic fluctuations.

Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep.

For hundreds of years, the unmanaged Soay sheep population on St Kilda has survived despite enduring presumably deleterious co-infections of helminth, protozoan and arthropod parasites and intermittent periods of starvation. Important parasite taxa in young Soay sheep are strongyles (Trichostrongylus axei, Trichostrongylus vitrinus and Teladorsagia circumcincta), coccidia (11 Eimeria species) and keds (Melophagus ovinus) and in older animals, Teladorsagia circumcincta. In this research, associations between the intensity of different parasite taxa were investigated. Secondly, the intensities of different parasite taxa were tested for associations with variation in host weight, which is itself a determinant of over-winter survival in the host population. In lambs, the intensity of strongyle eggs was positively correlated with that of Nematodirus spp. eggs, while in yearlings and adults strongyle eggs and coccidia oocysts were positively correlated. In lambs and yearlings, of the parasite taxa tested, only strongyle eggs were significantly and negatively associated with host weight. However, in adult hosts, strongyles and coccidia were independently and negatively associated with host weight. These results are consistent with the idea that strongyles and coccidia are exerting independent selection on Soay sheep.

Studies on the host-parasite relationship between Trichostrongylus colubriformis and susceptible and resistant sheep.

This study examined whether infective larvae (L3) of Trichostrongylus colubriformis could establish throughout the small intestine and were not restricted to the anterior duodenum in susceptible and resistant sheep. The location of worms was similar in susceptible animals given doses of T. colubriformis between 10,000 and 80,00 T. colubriformis larvae, with 90% of worms located in the proximal 3 m of the small intestine. Those worms recovered from resistant sheep were also found in the first 9 m of the intestine. However, worms recovered from immune sheep were significantly (P = 0.0074) relocated posteriorly from the first 3 m into the next 6 m of the intestine. By the surgical introduction of worms, it was found that T. colubriformis could establish at any site in the small intestine and to some extent in the caecum. Immunity was generated principally in the site of predilection in the anterior 3 m of the small intestine and effectively expelled challenges given at distal sites and caecum, indicating dissemination of immunity throughout the gastrointestinal tract. Moreover, the rejection episode had removed worms from the entire small intestine within 2 h of introduction through the pylorus.

The response of breeding doses to nematodiasis: segregation into "responders" and "non-responders".

Responder and non-responder does were identified from a flock of 95 Scottish cashmere 2-6 year-old does exposed to natural nematode infection over a 12-month period. Every 5 weeks, the does were faecal sampled for worm-egg counts prior to anthelmintic treatment. Responsive and non-responsive individuals were identified on the basis of their cumulative faecal egg count (FEC) rankings: the 8 lowest and 8 highest rankings were deemed to be responders and non-responders, respectively. Retrospective analysis showed that the mean egg count of the 8 responders was significantly lower than that of the 8 non-responders. The selected responders and non-responders were subsequently housed together with 8 randomly selected does from a control line, and given a mixed trickle challenge with Teladorsagia circumcincta and Trichostrongylus vitrinus larvae (L3). Mean responders FEC was significantly lower following artificial infection than that of non-responder and unselected does. Peripheral eosinophilia was significantly greater in responders in the first 3 weeks of this infection. On day 60, the infection was terminated with anthelmintic and 7 days later the goats were given a single challenge of 50,000 T. circumcincta L3. The mean responder worm burden was lower, and exhibited greater evidence of retardation of worm development, than those of non-responder and unselected does. Responders had significantly more mast cells and globule leukocytes post-challenge than did the other 2 groups. These results suggest that under the conditions encountered in this experiment, it is possible to segregate goats into responders and non-responders using simple parasitological criteria, as individual responsiveness is a relatively repeatable phenomenon.

Temporal effects of protein nutrition on the growth and immunity of lambs infected with Trichostrongylus colubriformis.

The aim of this research was to determine whether metabolisable protein supply during the early period of infection with Trichostrongylus colubriformis influenced resilience and the later stages in the development and magnitude of host resistance in previously nematode-naïve lambs. Eighty TexelxGreyface lambs were fed pelleted feeds calculated to provide grossly different amounts of metabolisable protein. Sixty of the lambs received a trickle infection of T. colubriformis and 20 lambs were kept as uninfected controls. There were four initial groups, namely infected or uninfected and fed either a moderate or a high protein feed. After 5weeks of infection, a further four groups were established by changing the feed of half of the animals fed the moderate protein feed to the high protein feed and of half of the animals fed high protein to the moderate protein feed. Live weight gain and feed conversion ratio were greatest for lambs fed the high protein feed and were reduced by infection. Faecal egg counts, worm burdens and per capita fecundity of adult female nematodes were unaffected by changes to metabolisable protein supply. Decreasing metabolisable protein supply following 5weeks of infection reduced live weight gain without any effect on resistance to T. colubriformis. Haematological variables, indicative of improved resistance, were also largely unaffected by metabolisable protein supply. It is concluded that the requirements of immune function probably had priority over those of growth and that the metabolisable protein supply provided by the moderate protein feed was sufficient to account for the requirements for the expression of immunity. It is probable that the potential for metabolisable protein supply to enhance resistance to infection from T. colubriformis is dependent on the levels and magnitude (i.e. in relation to maintenance requirements) of metabolisable protein supply being compared and the demand of other competing physiological functions.

Long-term subclinical infection with Trichostrongylus colubriformis: effects on food intake, diet selection and performance of growing lambs.

Growing lambs (mean liveweight 22.4 kg) were used to test for the effects of long-term subclinical infection with Trichostrongylus colubriformis (2500 larvae per day) on the voluntary food intake (VFI), diet selection and performance of sheep given a choice between two foods of different protein content (low versus high). Sheep were either uninfected controls or parasitised for 27 weeks (Group 27P). Additional sheep were infected for either 9 or 18 weeks (before and after the development of complete resistance to parasites, as assessed by faecal egg counts) and then treated with anthelmintic to remove the parasites (Groups 9P and 18P). Group 18P remained uninfected after anthelmintic treatment whereas Group 9P was infected again for the last 9 weeks after a 9 week worm-free period. The VFI declined or remained static from Week 5 up to Week 11/12 of continuous infection, for the 27P and 18P groups. For 9P sheep, VFI recovered within a few days after the anthelmintic administration and was unaffected during re-infection over the last 9 weeks of the experiment. Diet selection changed in such a pattern that the proportion of the high protein food (prop H) in the selected diet started to increase from Week 6 of the infection. The prop H selected remained higher over the interval 10-18 weeks of the continuous infection for 27P and 18P groups than the uninfected controls. There were no significant differences in diet selection among any of the groups beyond Week 18 of the experiment. The infection caused a growth check from Week 7 to approximately Week 12/14 of dosing; these was no evidence of compensatory growth following the development of resistance or recovery. The results are consistent with the view that sheep given a choice between two appropriate foods will modify their diet selection in order to moderate the adverse effects of subclinical nematode infection. The performance and diet selection of all sheep beyond Week 18 of infection suggest that no obvious nutritional penalties are incurred with the continuation of the infection once the animals have become resistant to parasites.

Effects of concurrent copper deficiency and gastro-intestinal nematodiasis on circulating copper and protein levels, liver copper and bodyweight in sheep.

Sheep were rendered hypocupraemic using parenteral ammonium tetrathiomolybdate (ATM). Fifteen thousand third stage larvae of Trichostrongylus axei and T. colubriformis in the ratio 1:1 were administered three times per week for six weeks, starting four weeks after cessation of ATM treatment. The changes in liver and plasma copper (Cu), caeruloplasmin activity, serum proteins, faecal nematode egg counts and total nematode counts were measured in the sheep for 10 weeks after infection. Decreases in liver Cu, plasma Cu and caeruloplasmin activities were detected soon after infection. There was a significant (P less than 0.05) interaction of the effects of Cu deficiency and nematode infection on these changes. Hypoproteinaemia, attributed to serum albumin loss, was demonstrated seven weeks after infection, but this was not associated with the interaction of Cu deficiency and nematode infection. No changes in serum globulins were detected. Although the results support the contention that gastro-intestinal nematodiasis can significantly exacerbate an existing Cu deficiency in sheep, there was no evidence that hypocuprosis would predispose sheep to higher nematode burdens.

Response to challenge infection with Haemonchus contortus and Trichostrongylus colubriformis in dairy goats. Consequences on milk production.

The objective of the study was to examine the ability of dairy goats to develop a response to nematode parasites of the digestive tract after a previous contact with the worms. One hundred dairy goats were initially divided into 2 groups. One remained free of parasites (not previously infected: NPI). The second group was infected thrice at 50 days interval with a mixture of Haemonchus contortus and Trichostrongylus colubriformis (previously infected: PI). After this initial exposure to nematodes, the goats were drenched with fenbendazole to eliminate the worms and remained free of parasites for 2 months around kidding. One month after kidding, 24 lactating dairy goats from each initial group were challenged with a mixture of H. contortus and T. colubriformis and parasitological, pathophysiological and milk production parameters were measured fortnightly to assess the effects of challenge infection and the response of the goats. No difference in parasite egg excretion was found between group NPI and PI after challenge infection. Similarly, no difference in worm counts was detected in 5 culled goats from each group killed one month post challenge. In contrast, differences between both groups were detected when considering the pathophysiological parameters (packed cell volume, inorganic phosphate and pepsinogen concentrations) with consequences of infection being more severe in the previously infected animals. Moreover, the milk production was also depressed in the PI group when compared to the NPI one. These results indicate that the response developed by adult dairy goats after the challenge infection was unable to limit the worm populations but could have pathophysiological repercussions and consequences on production.

Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis.

The effects of protein supplementation and infection with Trichostrongylus colubriformis on production responses and immune function in young sheep and on nematode population dynamics were assessed. Eighty-four 3-month-old Merino wether sheep were housed in individual pens and fed ad libitum chopped oaten hay containing 0.5% urea, together with 50 g day-1 lucerne meal. Fish meal (FM) was given as a source of protected protein at 0, 50 or 100 g day-1 (FM0, FM50, FM100; from Days --28 to 140). From Days 1 to 140, 0 or 1000 T. colubriformis infective larvae were given on Mondays, Wednesdays and Fridays. Infected sheep were slaughtered after 35, 70, 105, or 140 days of infection. Live-weight gain was reduced significantly by infection with T. colubriformis in sheep given FM0, but not in sheep given FM50 or FM100. Greasy wool production and fibre diameter were increased by FM, whereas the effects of infection with T. colubriformis on wool measurements depended on the level of FM given. Worm egg concentrations in faeces were significantly lower for sheep given FM100 than for those given FM0 or FM50 during the last 28 days of infection. Similarly, the apparent rate of worm expulsion was considerably higher in sheep given FM than in those not given FM. The rate of expulsion of T. colubriformis correlated with levels of circulating eosinophils as well as with the concentration of intestinal sheep mast cell proteases. Levels of parasite-specific and non-specific circulating antibodies were either unaffected or reduced as a result of supplementation with FM, although lymphocyte stimulation in vitro in response to T. colubriformis third stage larval antigen was enhanced significantly in infected animals given FM100. It was concluded that supplementary feeding with FM substantially reduced the production losses attributable to infection with T. colubriformis and was associated with enhanced expulsion of the parasite burden.

Pathogenesis of trichostrongylosis.

Trichostrongylosis is a major cause of impaired productivity in ruminants. The pathogenesis of such infections is principally associated with inappetence and increased losses of proteins into the gastrointestinal tract. Resultant changes in host metabolism account for the poor productivity in infected animals, although the precise mechanisms require further investigation. Studies are also required to investigate in greater detail the interactions between trichostrongylosis and the nutritional and immunological status of the host.

The pathophysiology and development of immunity during long-term subclinical infection with Trichostrongylus colubriformis of sheep receiving different nutritional treatments.

The objective of this study was to investigate the relationship between protein nutrition, the pathophysiology, and acquisition and expression of immunity in long-term subclinical intestinal parasitism in sheep. Growing sheep were either uninfected controls or parasitised for 27 weeks with a daily dose of 2500 larvae of Trichostrongylus colubriformis, whilst they were given access to: (1) a low protein food, (2) a high protein food, or (3) a choice between the two foods, where they were allowed to select their diet. Blood samples were taken weekly for determination of serum albumin, total protein, Ca, P, urea and fructosamine concentrations. At the end of the study all sheep received a single (secondary) challenge infection (30,000 T. colubriformis L3) after treatment with anthelmintic to assess their immune status. The concentrations of sheep-mast cell proteinases (SMCP) in intestinal tissue, the number of circulating eosinophils and the total worm numbers recovered from the intestinal tract were used to investigate the effects of previous nutrition on the acquisition and expression of immunity. From the biochemical variables measured over 27 weeks, only serum fructosamine was affected by the interaction between feeding treatment and parasitism: fructosamine concentrations declined only in the parasitised animals on the low protein food during Weeks 6-15 of infection. This casts doubt on the usefulness of plasma fructosamine levels as an indicator of gastrointestinal parasitism, due to its being influenced by the nutritional environment. Total protein, albumin, calcium and phosphorus concentrations in the serum were affected by parasitism, but independently of feeding treatment. During the period of secondary challenge eosinophil numbers and SMCP concentrations were higher in the parasitised animals, reflecting the animals immune responsiveness. The numbers of worms recovered from the intestine of previously parasitised sheep were low; all three indicators of the development of acquired immunity were unaffected by previous nutritional treatment of the sheep. The results do not support the view that the pathophysiology of long term subclinical intestinal parasitism and the expression of acquired immunity induced by a trickle infection could be affected by the feeding treatment of the sheep (protein nutrition).

Haemonchus contortus and other trichostrongylid infections in parturient, lactating and dry ewes.

From autumn (April) to spring (November), groups of pregnant and dry Merino ewes grazed pasture contaminated with infective larvae of Haemonchus contortus, Ostertagia circumcincta and Trichostrongylus colubriformis. A periparturient rise in faecal egg counts occurred in the pregnant ewes, following the maturation in early spring of arrested fourth-stage larvae of H. contortus and failure of pregnant ewes to expel the resulting adult worms. Peak egg counts were seen in September, just before lambing. In dry ewes, egg counts were slightly elevated at the time of the rise in the pregnant ewes, but fell to very low levels as adult worms developing from previously arrested larvae were expelled. Lactating ewes acquired greater burdens of O. circumcincta and T. colubriformis than did dry ewes, but were equally refractory to new infections with H. contortus. It is therefore suggested that the impairment of immunity to helminth infection seen in reproductive ewes may be more specific than was previously envisaged.

The effects of urea supplementation on production and parasitological responses of sheep infected with Haemonchus contortus and Trichostrongylus colubriformis.

Merino wether lambs were individually confined and fed a basal diet of oaten chaff containing essential minerals which was untreated or contained 3% urea. Within each dietary group animals were orally infected with either 200 H. contortus (H), 1000 T. colubriformis (T) or both species (H + T) thrice weekly or remained uninfected (C). Weight gain, wool production, and parasite burden were measured over a 19-week period. Sheep on the diet containing urea gained more weight, consumed more feed and grew more wool of higher fibre diameter than their counterparts given no urea. On both diets uninfected sheep consumed more feed than infected sheep and the sheep given no urea and infected with both H and T worm species consumed the least feed. Parasitised sheep gained less weight than uninfected control sheep. Sheep with urea in their diet had lower faecal egg counts when infected with H alone or with H and T but there was no effect of urea on egg count of sheep infected with T alone. In contrast, T numbers after slaughter were reduced in sheep fed diets containing urea whereas H numbers were not affected by diet. It was concluded that supplementation with urea can increase resilience to parasitism thereby improving production and also enhance resistance mechanisms against worms in young sheep on low quality roughage diets. These responses can be partly attributed to stimulation of feed intake, presumably due to enhanced ruminal digestion, but also to elevated rumen NH3-N levels which would be expected to have increased rumen microbial protein synthesis and availability to the intestines.

Susceptibility of the pre-parturient ewe to infection with Trichostrongylus vitrinus and Ostertagia circumcincta.

During two successive years, groups of pregnant ewes and non-pregnant worm-free sheep were given anthelmintic, challenged one week later with 10,000 infective larvae of either Trichostrongylus vitrinus or Ostertagia circumcincta and killed two, four and six weeks after challenge. All of the ewes were killed within three days of their predicted lambing date. There was no annual variation in the response of the ewes to infection with either species. Compared to adult naive animals, ewes expressed resistance to infection with T vitrinus at all times, with significantly lower worm burdens composed largely of inhibited third stage larvae. Ewes challenged with O circumcincta were fully as susceptible as naive animals with regard to the size and stage of development of their worm populations. Mechanisms regulating the numbers of adult O circumcincta were operative in the adult naive animals but not in the ewes.

Functioning of the thyroid gland in sheep infected with Trichostrongylus colubriformis.

Radioactive tracers were used to to study the kinetic behaviour of inorganic iodine (I) and thyroxine (T4) in sheep (1) uninfected and fed ad libitum, (2) infected with Trichostronglylus colubriformis and fed ad libitum and (3) uninfected but pair-fed to the infected animals. Plasma concentration and pool size of inorganic I were each significantly lower in groups 2 and 3 than in 1. Irreversible loss of inorganic I in both groups 2 and 3 was significantly greater than in 1. The turnover rate of T4 increased after infection, whereas in pair-fed sheep the T4 turnover rate was not significantly different from that in uninfected controls. The pool size and rate of irreversible loss of T4 in infected sheep were significantly reduced. The increased T4 turnover rate and reduced availability of I probably caused the depletion of colloid seen in the thyroid gland of infected sheep. The depletion of colloid may account for the reduced response to thyroid stimulating hormone in these sheep.

Effects of the caecal nematode Trichostrongylus tenuis on egg-laying by captive red grouse.

Captive hen red grouse infected with Trichostrongylus tenuis larvae started to lay later in spring and laid fewer eggs at a slower rate than uninfected hens. March-infected hen grouse showed greater effects than December-infected ones, probably because developing larvae were more pathogenic than adult worms. The mechanism by which parasites interfered with egg production involved reduction in food intake. Infected hens also gained less weight than controls before laying.

Influence of two levels of concurrent infection with Ostertagia circumcincta and Trichostrongylus vitrinus on the growth performance of lambs.

Groups of seven lambs were infected on five days each week for 11 weeks with either 1000 or 2000 Trichostrongylus vitrinus larvae alone or concurrently with 1500 or 2500 Ostertagia circumcincta larvae and their growth performance compared to that of worm-free controls. The cumulative liveweight gain of the infected groups was significantly lower than that of the controls but the gain of the concurrently infected lambs did not differ significantly from the respective T vitrinus group. There were no significant differences in the numbers of T vitrinus or O circumcincta recovered from the single and concurrently infected groups, although there was a tendency for lower mean T vitrinus burdens at the higher level of ostertagia/trichostrongylus infection. The distribution of T vitrinus along the small intestine was similar in single and concurrently infected lambs. The reason for the lack of a marked additive effect on growth rate with concurrent infection is discussed in relation to changes in the concentration of two plasma constituents and lesions in the gastrointestinal tract.

Effect of anthelmintic treatment on the productivity of lambs infected with the intestinal nematode, Trichostrongylus colubriformis.

Liveweight gain, food intake, wool growth and concentration of serum constituents were measured in four groups of three-month-old lambs. Groups 1 and 2 were infected on five days each week with 2500 Trichostrongylus colubriformis larvae for 18 weeks. Group 2 lambs were treated with fenbendazole (5 mg kg-1) at week 10 and week 15. Group 3 lambs were similarly infected for 10 weeks, treated with fenbendazole, but given no further larvae. A fourth control group remained uninfected throughout the trial. All lambs were killed at week 20. Mean worm populations were 16,130, 430 and zero for groups 1, 2 and 3 respectively. Over the first 10 weeks of infection, liveweight gain was reduced by 52, 43 and 51 per cent and wool growth by 33, 28 and 27 per cent respectively, in groups 1, 2 and 3. Serum hypophosphataemia and hypoalbuminaemia occurred in all three infected groups. Between weeks 10 and 20 overall weight gain and wool growth in group 1 lambs were 44 and 46 per cent lower than the controls, whereas weight gains of group 2 and group 3 lambs were similar to or slightly higher than in the controls. However, wool growth in these two groups after treatment was only 73 to 74 per cent of control values. Serum phosphorus concentrations increased to control levels within one week of anthelmintic treatment and serum albumin concentrations by two to four weeks. The ability of group 2 lambs to improve their performance after anthelmintic treatment, in the face of continued challenge, was attributed to development of resistance to reinfection.

Interaction of dichlorvos-crotoxyphos insecticide with phenothiazine anthelmintic in sheep with or without Haemonchus and Trichostrongylus infections.

The temporal interaction of an emulsifiable mixture of 2.3% dichlorvos and 10% crotoxyphos with phenothiazine anthelmintic was studied in 8 groups of 5 lambs each, free from or parasitized with Haemonchus and Trichostrongylus spp. Each lamb in 1 of 3 parasitized groups and 1 of 3 nonparasitized groups was treated with phenothiazine orally (12.5 g initially and 4 days later with 6.25 g every 3 days for 9 treatments) and/or the mixture of dichlorvos and crotoxyphos dermally (1,550 ml of 0.25% emulsion sprayed every 2 weeks for 3 applications). Two groups served as controls. Onset of clinical signs of toxicosis, lethality, and erythrocyte acetylcholinesterase (EACE) activity were monitored. After each dichlorvos-crotoxyphos mixture spray, clinical signs of toxicosis were seen within 40 minutes in parasitized and nonparasitized lambs regardless of concurrent phenothiazine treatment. Phenothiazine alone was not toxic and did not inhibit EACE activity. The EACE activities of dichlorvos-crotoxyphos mixture-sprayed lambs were significantly (P less than 0.05) depressed regardless of parasitism or concurrent phenothiazine treatments. The severity of inhibition increased with each dichlorvos-crotoxyphos mixture spray, but EACE activity recovered within 48 hours after each spray although base-line values were never attained. There was no apparent potentiation of the toxic effects of the dichlorvos-crotoxyphos mixture by phenothiazine.

Comparison of the effects on milk production of concurrent infection with Haemonchus contortus and Trichostrongylus colubriformis in high- and low-producing dairy goats.

The impact of nematode parasitism of the digestive tract on milk output and milk quality was examined in dairy goats. In addition, the consequences of worm infection were compared in goats with different lactation performance (ie, with initial high or low milk production). Forty-eight goats in the second month of lactation were allotted equally to 2 groups. The first group was given 5,000 Haemonchus contortus and 20,000 Trichostrongylus colubriformis larvae. The 24 additional goats remained free of parasites. Parasitologic, serologic, and milk data were collected every 2 weeks for 5 months, and body condition of the goats was scored throughout the study. Results of strongyle egg count in feces, increase in pepsinogen values, and reduction in RBC count, PCV, and serum inorganic phosphate concentration indicated subclinical infection. This subclinical parasitism induced a decrease in body condition scoring and led to persistent decrease in milk yield, ranging from 2.5 to 10% reduction from control values. Changes in fat and protein contents were not detected. In contrast, the consequences of infection were more severe in the 6 goats with the highest milk production at the start of the study. Decrease in milk output ranged between 13.0 to 25.1%, and was associated with decrease in fat content. Comparison of the response to parasitism in the 6 goats with the highest lactation performance and the 6 goats with the lowest performance indicated differences between both subgroups. According to parasitologic and pathologic data, high-producer goats had less resistance and/or resilience to infection associated with more severe consequences on milk production.