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Regulation of Trichostrongylus vitrinus and T colubriformis populations in naturally infected sheep in The Netherlands
Research in Veterinary Science /987, 42, 267-27/
Regulation of Trichostrongylus vitrinus and T colubrijormis populations in naturally infected sheep in The Netherlands M. EYSKER, Institute for Veterinary Parasitology and Parasitic Diseases, University of Utrecht, Yalelaan 1, Utrecht, The Netherlands
During a study on the epidemiology of gastrointestinal helminth infections in sheep at the University of Utrecht (1974 to 1977) information was obtained on the population regulation of small intestinal Trichostrongylus species. Comparison of the cumulative burdens in tracer lambs with those in flock lambs showed an accumulation of Trichostrongylus species in the latter until autumn followed by an expulsion of worms. The dominating species, T vitrinus, was expelled earlier than T coiubriformis. The proportion of inhibited early third stage Trichostrongylus species larvae in tracer lambs was low, but it tended to increase in autumn. In most flock lambs the levels of inhibition were also low. In non-lactating ewes, populations consisted predominantly of inhibited early third stage larvae but when adults were present they tended to be mainly T colubriformis. Similar populations were seen in some lactating ewes. In other lactating· ewes Trichostrongylus species populations with low proportions of inhibited early third stage larvae which were dominated by T vitrinus, indicated a relaxation of resistance around parturition.
TRICHOSTRONGYLUS vitrinus and T colubriformis are the most common small intestinal Trichostrongylus species in sheep. In temperate areas T vitrinus tends to dominate, whereas in warmer climates T colubriformis is more abundant. The Netherlands belong to the area where T vitrinus is dominant (Eysker 1980). However, a field study carried out at the University of Utrecht between 1974 and 1977, showed that sometimes and in some categories of animals T colubriformis was more abundant than T vitrinus. This and other factors regulating small intestinal Trichostrongylus species populations are presented in this paper. Materials and methods Texel or Friesian or Texel cross Friesian sheep grazed three adjacent pastures, one, one and half a hectare in area, between May 1974 and November 1977. These pastures were intensively grazed by sheep
throughout the year and could be considered to be highly infested with infective larvae of Trichostrongylidae when weather conditions were suitable for the development and survival of the free living stages. In winter the sheep were fed supplementary hay and concentrates. In total 40 tracer lambs, 53 lambs and 51 ewes were autopsied to provide worm counts during this period. The tracer lambs (raised helminth free), were grazed for 14 to 32 days between May 1974 and February 1975 (18), August 1975 and March 1976 (12) and July and December 1976 (10) and subsequently housed under helminth free conditions for two to four weeks before being killed. The conventional flock lambs and ewes were grazed from spring onwards and housed before being killed. Groups of lambs were housed in August (five), November (10) and December (four) 1975 and March 1976 (four); in September (five), November (five) and December (four) 1976 and March 1977 (four) and in September (seven) and November (five) 1977. Groups of ewes were housed in August (eight), November (15) and December (seven) 1975 and March 1976 (eight) and in March 1977 (14). Nine ewes housed in March 1977 were barren ewes. The five other ewes and those housed in March 1976 lambed. Ewes and flock lambs were housed for zero to five weeks, with the exception of three lactating ewes from 1976, which were housed for 7· 5 to nine weeks. Housed animals were given hay, concentrates and water ad libitum. Autopsy and worm count procedures have been described earlier (Eysker 1978). Results
Tracer lambs Fig I shows that the tracer lambs always acquired higher T vitrinus burdens than T colubriformis. It also appears that a higher proportion of the Trichostrongylus species populations consisted of T colubriformis in summer than in autumn and winter. Comparison of the proportions of T colubriformis (calculated by dividing the numbers of T colubri-
267
268
M. Eysker 50,000
10
20,000 10,000
9
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200 100
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1974
1975
1976
FIG 1: Numbers of T vitrinus ( - - I , T colubriformis (- - - I and inhibited early third stage larvae of small intestinal Trichostrongylus species ( ) in tracer lambs. Bars denote range in pairs of tracer lambs
formis males by the total numbers of Trichostrongylus species males) in tracer lambs grazed between May and September with those grazed from October to March with the test for K-independent samples of Kruskal and Wallis revealed that this trend was significant at the I per cent level of probability. Fig I also shows a seasonal tendency for the
occurrence of inhibited early third stage larvae as these stages were found predominantly in tracer lambs grazed between October and December. In all tracer lambs only a small proportion of the total Trichostrongylus species populations consisted of early third stage larvae, except for the animal grazed in November 1975 which harboured 3500.
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FIG 2: Geometric means and standard deviations of the numbers of T vitrinus ( - - I , T colubritormis (- - -I and inhibited early third I in the groups of flock lambs. Bars denote ± 1 SD stage larvae of small intestinal Trichostrongylus species (
Regulation of trichostrongyle populations Flock lambs Fig 2 suggests that in 1975-76 and 1976-77 Tvitrinus dominated Trichostrongylus species populations changed to T colubriformis dominated populations mainly as a result of a selective decrease of T vitrinus from November 1975 and 1976 onwards. In contrast, T colubriformis showed a decrease only between December 1976 and March 1977 which was less pronounced than the decrease for T vitrinus in the same period. In both these grazing seasons the numbers of third stage larvae increased until December and subsequently decreased by March. In comparison with the burdens of third stage larvae in the tracer lambs the burdens in the flock lambs were higher in December 1976, but similar in December 1975. In autumn 1977 the same trends were seen as in both the other years but because the summer was more humid high T vitrinus burdens were already present at the end of September and a decrease 0 f this species, combined with an increase in T colubriformis and burdens of third stage larvae was seen at the beginning of November. When decreases in the numbers of T vitrinus, T co/ubrijormis or third stage larvae occurred the standard deviation increased. The reason for this was a high within group variation indicating that the decrease did not occur at the same time and to the same extent in all animals. One animal housed in March 1976, for instance, harboured the largest T vitrinus burden of all animals.
269
Comparison of cumulative burdens in tracer lambs with burdens in flock lambs Table I shows a slower build up of cumulative burdens in tracer lambs in 1976 than in 1975. Furthermore, these cumulative burdens did not differ very much from the geometric mean burdens of the flock lambs until October 1975 and December 1976, indicating an accumulation of Trichostrongylus species until the autumn.
Ewes Table 2 represents the proportions of Tvitrinus and T colubriformis, calculated from the male worms. Calculation of absolute numbers for both species is very difficult as a high proportion of the trichostrongylus burdens consisted of third and fourth stage larvae and many ewes harboured only these stages. Furthermore, the worm counts of the barren ewes from 1977 were combined with those of the ewes housed between August and December 1975 as no clear seasonal trends were visible in these. Similarly the worm counts of the different groups of lactating ewes were combined.
Non-lactating ewes (38). The worm burdens were generally low and in 15 ewes no Trichostrongylus species were found. In the remaining ewes the Trichostrongylus species burdens consisted predominantly of inhibited early third stage larvae, and in II of these only third stage larvae were recovered (range 50 to
TABLE 1: Comparison of the cumulative small Trichostrongylus species burdens in the tracer lambs in 1975·76 and 1976·n with the geometric means of the burdens in flock lambs
Grazing period tracer lambs
1975-76 Cumulative burden tracer lambs
Aug 8-Aug 25* Aug 25-Sept 9*
4580
Sept 15-0ct 13*
37,640
Oct 13-Nov 3 Nov 3-Dec 1 Dec l-Dec 29 Dec 19-Jan 26 Jan 26-Feb 17 Feb 17-Mar 8
51,440 69.640 97,740 107,240 118,740 149,440
Geometric mean burdens of flock lambs
470 4450
37,590 18,950
11,340
* Pairs of tracer lambs were grazed t Estimated :I: Date~f housing of the group of flock lambs
Grazing period tracer lambs
1976-n Cumulative burden tracer lambs
June 29-July 13 July 13-July 27 July 27-Aug 10 Aug ll-Aug 25 Aug 24-Sept 7 Sept 7-Sept 24 Sept 21-0ct 5 Oct 5-0ct 19 Oct 19-Nov 2
1500 9400 9400 9500 9850 11,500 14,650 17.600
20,230
Nov 23-Dec 12
21,550t
22.690
Mar
7:1:
Geometric mean burdens of flock lambs
o
6875
320
270
M. Eysker
5800). Fifth stage male worms were found in only seven animals. Of these six only harboured T colubrijormis (50, 50, 100, 100, 300 and 300 males) and the other contained 650 male T vitrinus and 200 male T colubriformis.
Lactating ewes (13). The numbers of worms tended to be higher than in the non-lactating ewes arid the percentage of inhibited larvae lower. In contrast to the situation in the non-lactating ewes T vitrinus was the dominant species in all eight ewes which harboured fifth stage male trichostrongylus. The relatively high mean level of inhibited early third stage larvae was mainly due to the worm counts in the five animals with the lowest burdens (100, 100, 100, 500 and 2600 worms, respectively). In the last ewe 2200 third stage and 400 fourth stage larvae were present and the other ewes harboured only third stage larvae. Discussion Regulation of Trichostrongylus species populations does not seem to be based on a turnover of worms as has been reported for Ostertagia species and Haemonchus contortus (Michel 1970, Thomas and Waller 1979). Chiejina and Sewell (1974a, I974b) observed in experimentally infected young lambs that Tcolubriformis infections accumulate until resistance occurs. Subsequently, further acquisition of infection does not occur for some time and finally the worms are expelled. Waller and Thomas (1981) were able to confirm this in naturally infected lambs by comparing the cumulative burdens in tracer lambs with the burdens of lambs which were grazed permanently. A similar comparison in the present study also showed this pattern of population regulation. The lower burdens in the tracer lambs in 1976 in comparison with 1975, and subsequently the longer period of accumulation of Trichostrongylus species burdens in lambs in 1976, were probably caused by the extremely dry summer in that year. Expulsion of Trichostrongylus species burdens in the flock lambs did not begin before OctoberNovember, when the animals were six or seven months old, but the time of expulsion was variable not only between years but also within groups. For instance in one of the flock lambs housed in March 1976 expulsion had not yet occurred. The results in the flock lambs suggest that when expulsion occurs, T vitrinus is expelled selectively, while T colubriformis can remain in the intestine for some time. This indicates differences in the immune response of the host to these species. Coop et al (1979) suggested from two separate but similar experiments with both species that T vitrinus is expelled earlier than T colubriformis, which could be an explanation for the present findings. However, the earlier expulsion of T
TABLE 2: Geometric means of Trichostrongylus species and mean percentages of T colubriformis, T vitrinus and inhibited early third stage larvae (L31 in non-lactating and lactating ewes Non-lactating ewes Lactating ewes (n~38)
Geometric mean (range) Mean % T colubriformis (range) Mean % T vitrinus (range) Mean % early L3 (range)
(n~13)
45
3000
(0-16,900)
(100-39,400)
89·1
3-8
(23'5-100)
(0-20)
10·9
96·2
(0-76'5)
(80-100)
83·6
46·8
(0-100)
(0-100)
vitrinus may also be dose dependent, as the results of the tracer lambs clearly show much higher infections for T vitrinus. Inhibited development of small intestinal Trichostrongylus species was also observed by Ogunsusi and Eysker (1979) and Waller et al (1981) but they were unable to show a relation between the level of inhibition and size of worm burden, host resistance or seasonal factors. The results in the tracer lambs indicated a slight tendency for a seasonal inhibition, though this was not as pronounced as for Haemonchus contortus, Ostertagia species and the large intestinal strongyles in the same animals (Eysker 1980). The large numbers of inhibited early third stage larvae in the flock lambs in December 1976 in comparison with the numbers in the tracer lambs in that year may imply an influence of host resistance on inhibited development. That the numbers of inhibited third stage larvae were not very high in flock lambs in December 1975 in comparison to the tracer lambs can possibly be explained by a lower establishment of Trichostrongylus species infections in late autumn in flock lambs as a result of developing resistance. An influence of host resistance on inhibited development was also seen in the non-lactating and in some lactating ewes, as in these animals often 100 per cent of the Trichostrongylus species populations consisted of inhibited third stage larvae. The results of Jackson et al (1984), who observed high levels of inhibition for T vitrinus in ewes which were experimentally infected, also indicated an influence of host resistance. In the non-lactating ewes host resistance was also reflected by the dominance of T colubrijormis, as seen in older flock lambs which expelled most of their worm burdens. However, in some lactating ewes the low levels of inhibition and the dominance of T vitrinus resembled the situation in flock lambs which had not yet expelled the majority of their worms. This indicates that a relaxation of resistance occurred in some but not all ewes. This relaxation of resistance can result in the development of inhibited larvae and acquisition of overwintered larvae from pasture. In The Netherlands the latter is
Regulation oj trichostrongyle populations
probably more important (Eysker 1980). Reid and Armour (1975) showed for Ostertagia circumcincta and O'Sullivan and Donald (1973) for Haemonchus contortus and T colubrijormis that ewes have a reduced resistance to helminth infections during the last weeks of pregnancy. Jackson et al (1984) could reproduce this for 0 circumcincta but they did not see a reduced resistance to T vitrinus. This shows some resemblance with 'the situation in the five lactating ewes in the present study with the lowest Trichostrongylus species burdens, as these burdens predominantly consisted of inhibited larvae. In short, the sequence in the population regulation of small intestinal Trichostrongylus species seems to be as follows. An accumulation of worm burdens occurs in the lambs. When resistance develops in autumn or winter no further infection is required and subsequently a selective expulsion of T vitrinus occurs. In ewes T colubrijormis is usually not present and either no worms or only low burdens of predominantly inhibited larvae can be found. Around parturition a relaxation of resistance occurs in some but not all ewes, resulting in populations with low levels of inhibition, which are dominated by T vitrinus. The tracer lamb results show, as in other temperate areas such as north east England (Waller and Thomas 1981) and winter rainfall regions in Australia (Anderson 1972), that T vitrinus is the dominating species. T colubrijormis is better adapted to warmer climates as, for instance, the dominance of this species in northern Nigeria (Ogunsusi and Eysker 1979) and summer rainfall areas in Australia (Southcott et a11976) shows. In an intermediate rainfall zone in Australia, Waller et al (1981) observed a biphasic seasonal pattern of Trichostrongylus species infections in tracer lambs, with T vitrinus dominating in the spring peak and T colubrijormis in the autumn peak. This possibly indicates that the circumstances for translation of T colubrijormis are better following summer and those for T vitrinus following winter. In the present experiments a somewhat higher proportion of T colubrijormis was seen in the burdens of tracer lambs grazed between May and September than in the burdens of those grazed after September. This may be associated with the higher temperatures between May and September. Another explanation may be that initially the new wave of infection, which
271
develops on pasture during this period, is mainly the progeny of worm populations from ewes and yearling sheep. These populations would possibly contain a higher proportion of T colubrijormis than in young lambs. It has to be stressed that, despite our present results, when the whole flock is taken into consideration, Trichostrongylus species populations in The Netherlands will probably only very occasionally be dominated by T colubrijormis. Also within flocks there will be a proportion of sheep which are less resistant. These sheep will tend to harbour large T vitrinus dominated Trichostrongylus species burdens and consequently will have higher faecal egg counts. Thus these carrier animals will largely determine the contamination of the pasture with Trichostrongylus species eggs. Acknowledgement
Dr J. Jansen is thanked for his valuable criticisms of the manuscript. References ANDERSON, N. (1972) Australian Journal ofAgricultural Research 23, 1113-1129 CHIEJINA, S. N. & SEWELL, M. M. H. (l974a) Parasitology 69, 301-314 CHIEJINA, S. N. & SEWELL, M. M. H. (l974b) Parasitology 69, 315-327 COOP, R. L., ANGUS, K. W. & SYKES, A. R. (1979) Research in Veterinary Science 26, 363-371 EYSKER, M. (1978) Veterinary Parasitology 4,29-33 EYSKER, M. (1980) Thesis, University of Utrecht JACKSON, F., COOP, R. L. & WRIGHT, S. E. (1984) Parasitology 89, LXII- LXIII MICHEL, J. F. (1970) Parasitology 61,435-447 OGUNSUSI, R. A. & EYSKER, M. (1979) Research in Veterinary Science 26, 108-110 O'SULLIVAN, B. M. & DONALD, A. D. (1973) International Journal for Parasitology 3,521-530 REID, J. F. S. & ARMOUR, J. (1975) Journal for Comparative Pathology 85, 163-170 SOUTHCOTT, W. H., MAJOR, G. W. & BARGER, J. A. (1976) Australian Journal of Agricultural Research 27, 277-286 THOMAS, R. J. & WALLER, P. J. (1979) Research in Veterinary Science 26, 209-212 WAI,-LER, P. J., DONALD, A. D. & DOBSON, R. J. (1981) Research in Veterinary Science 30,213-216 WALLER, P. J. & THOMAS, R. J. (1981) International Journalfor Parasitology 8, 275-283
Accepted February 3, /987
Regulation of Trichostrongylus vitrinus and T colubrijormis populations in naturally infected sheep in The Netherlands M. EYSKER, Institute for Veterinary Parasitology and Parasitic Diseases, University of Utrecht, Yalelaan 1, Utrecht, The Netherlands
During a study on the epidemiology of gastrointestinal helminth infections in sheep at the University of Utrecht (1974 to 1977) information was obtained on the population regulation of small intestinal Trichostrongylus species. Comparison of the cumulative burdens in tracer lambs with those in flock lambs showed an accumulation of Trichostrongylus species in the latter until autumn followed by an expulsion of worms. The dominating species, T vitrinus, was expelled earlier than T coiubriformis. The proportion of inhibited early third stage Trichostrongylus species larvae in tracer lambs was low, but it tended to increase in autumn. In most flock lambs the levels of inhibition were also low. In non-lactating ewes, populations consisted predominantly of inhibited early third stage larvae but when adults were present they tended to be mainly T colubriformis. Similar populations were seen in some lactating ewes. In other lactating· ewes Trichostrongylus species populations with low proportions of inhibited early third stage larvae which were dominated by T vitrinus, indicated a relaxation of resistance around parturition.
TRICHOSTRONGYLUS vitrinus and T colubriformis are the most common small intestinal Trichostrongylus species in sheep. In temperate areas T vitrinus tends to dominate, whereas in warmer climates T colubriformis is more abundant. The Netherlands belong to the area where T vitrinus is dominant (Eysker 1980). However, a field study carried out at the University of Utrecht between 1974 and 1977, showed that sometimes and in some categories of animals T colubriformis was more abundant than T vitrinus. This and other factors regulating small intestinal Trichostrongylus species populations are presented in this paper. Materials and methods Texel or Friesian or Texel cross Friesian sheep grazed three adjacent pastures, one, one and half a hectare in area, between May 1974 and November 1977. These pastures were intensively grazed by sheep
throughout the year and could be considered to be highly infested with infective larvae of Trichostrongylidae when weather conditions were suitable for the development and survival of the free living stages. In winter the sheep were fed supplementary hay and concentrates. In total 40 tracer lambs, 53 lambs and 51 ewes were autopsied to provide worm counts during this period. The tracer lambs (raised helminth free), were grazed for 14 to 32 days between May 1974 and February 1975 (18), August 1975 and March 1976 (12) and July and December 1976 (10) and subsequently housed under helminth free conditions for two to four weeks before being killed. The conventional flock lambs and ewes were grazed from spring onwards and housed before being killed. Groups of lambs were housed in August (five), November (10) and December (four) 1975 and March 1976 (four); in September (five), November (five) and December (four) 1976 and March 1977 (four) and in September (seven) and November (five) 1977. Groups of ewes were housed in August (eight), November (15) and December (seven) 1975 and March 1976 (eight) and in March 1977 (14). Nine ewes housed in March 1977 were barren ewes. The five other ewes and those housed in March 1976 lambed. Ewes and flock lambs were housed for zero to five weeks, with the exception of three lactating ewes from 1976, which were housed for 7· 5 to nine weeks. Housed animals were given hay, concentrates and water ad libitum. Autopsy and worm count procedures have been described earlier (Eysker 1978). Results
Tracer lambs Fig I shows that the tracer lambs always acquired higher T vitrinus burdens than T colubriformis. It also appears that a higher proportion of the Trichostrongylus species populations consisted of T colubriformis in summer than in autumn and winter. Comparison of the proportions of T colubriformis (calculated by dividing the numbers of T colubri-
267
268
M. Eysker 50,000
10
20,000 10,000
9
5,000
B
2000
7
1000
+ 6 en Q;
200 100
.0
E 5
E" 4
50
c:
...J
3
20 10
2
o
0 r-j--r-j--"T-A--"T-S-'-O-'-N",""r-D--r'-j--"TI-F""" . -A--r-S"'-O--"T-N-'-D"T'"-j"T'"-F--r-,·· ..-,-j--r-A--"T-S--"T-O-"'N-I'-D--" M 1"",
1974
1975
1976
FIG 1: Numbers of T vitrinus ( - - I , T colubriformis (- - - I and inhibited early third stage larvae of small intestinal Trichostrongylus species ( ) in tracer lambs. Bars denote range in pairs of tracer lambs
formis males by the total numbers of Trichostrongylus species males) in tracer lambs grazed between May and September with those grazed from October to March with the test for K-independent samples of Kruskal and Wallis revealed that this trend was significant at the I per cent level of probability. Fig I also shows a seasonal tendency for the
occurrence of inhibited early third stage larvae as these stages were found predominantly in tracer lambs grazed between October and December. In all tracer lambs only a small proportion of the total Trichostrongylus species populations consisted of early third stage larvae, except for the animal grazed in November 1975 which harboured 3500.
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20,000 10,000 5,000 2000 1000
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FIG 2: Geometric means and standard deviations of the numbers of T vitrinus ( - - I , T colubritormis (- - -I and inhibited early third I in the groups of flock lambs. Bars denote ± 1 SD stage larvae of small intestinal Trichostrongylus species (
Regulation of trichostrongyle populations Flock lambs Fig 2 suggests that in 1975-76 and 1976-77 Tvitrinus dominated Trichostrongylus species populations changed to T colubriformis dominated populations mainly as a result of a selective decrease of T vitrinus from November 1975 and 1976 onwards. In contrast, T colubriformis showed a decrease only between December 1976 and March 1977 which was less pronounced than the decrease for T vitrinus in the same period. In both these grazing seasons the numbers of third stage larvae increased until December and subsequently decreased by March. In comparison with the burdens of third stage larvae in the tracer lambs the burdens in the flock lambs were higher in December 1976, but similar in December 1975. In autumn 1977 the same trends were seen as in both the other years but because the summer was more humid high T vitrinus burdens were already present at the end of September and a decrease 0 f this species, combined with an increase in T colubriformis and burdens of third stage larvae was seen at the beginning of November. When decreases in the numbers of T vitrinus, T co/ubrijormis or third stage larvae occurred the standard deviation increased. The reason for this was a high within group variation indicating that the decrease did not occur at the same time and to the same extent in all animals. One animal housed in March 1976, for instance, harboured the largest T vitrinus burden of all animals.
269
Comparison of cumulative burdens in tracer lambs with burdens in flock lambs Table I shows a slower build up of cumulative burdens in tracer lambs in 1976 than in 1975. Furthermore, these cumulative burdens did not differ very much from the geometric mean burdens of the flock lambs until October 1975 and December 1976, indicating an accumulation of Trichostrongylus species until the autumn.
Ewes Table 2 represents the proportions of Tvitrinus and T colubriformis, calculated from the male worms. Calculation of absolute numbers for both species is very difficult as a high proportion of the trichostrongylus burdens consisted of third and fourth stage larvae and many ewes harboured only these stages. Furthermore, the worm counts of the barren ewes from 1977 were combined with those of the ewes housed between August and December 1975 as no clear seasonal trends were visible in these. Similarly the worm counts of the different groups of lactating ewes were combined.
Non-lactating ewes (38). The worm burdens were generally low and in 15 ewes no Trichostrongylus species were found. In the remaining ewes the Trichostrongylus species burdens consisted predominantly of inhibited early third stage larvae, and in II of these only third stage larvae were recovered (range 50 to
TABLE 1: Comparison of the cumulative small Trichostrongylus species burdens in the tracer lambs in 1975·76 and 1976·n with the geometric means of the burdens in flock lambs
Grazing period tracer lambs
1975-76 Cumulative burden tracer lambs
Aug 8-Aug 25* Aug 25-Sept 9*
4580
Sept 15-0ct 13*
37,640
Oct 13-Nov 3 Nov 3-Dec 1 Dec l-Dec 29 Dec 19-Jan 26 Jan 26-Feb 17 Feb 17-Mar 8
51,440 69.640 97,740 107,240 118,740 149,440
Geometric mean burdens of flock lambs
470 4450
37,590 18,950
11,340
* Pairs of tracer lambs were grazed t Estimated :I: Date~f housing of the group of flock lambs
Grazing period tracer lambs
1976-n Cumulative burden tracer lambs
June 29-July 13 July 13-July 27 July 27-Aug 10 Aug ll-Aug 25 Aug 24-Sept 7 Sept 7-Sept 24 Sept 21-0ct 5 Oct 5-0ct 19 Oct 19-Nov 2
1500 9400 9400 9500 9850 11,500 14,650 17.600
20,230
Nov 23-Dec 12
21,550t
22.690
Mar
7:1:
Geometric mean burdens of flock lambs
o
6875
320
270
M. Eysker
5800). Fifth stage male worms were found in only seven animals. Of these six only harboured T colubrijormis (50, 50, 100, 100, 300 and 300 males) and the other contained 650 male T vitrinus and 200 male T colubriformis.
Lactating ewes (13). The numbers of worms tended to be higher than in the non-lactating ewes arid the percentage of inhibited larvae lower. In contrast to the situation in the non-lactating ewes T vitrinus was the dominant species in all eight ewes which harboured fifth stage male trichostrongylus. The relatively high mean level of inhibited early third stage larvae was mainly due to the worm counts in the five animals with the lowest burdens (100, 100, 100, 500 and 2600 worms, respectively). In the last ewe 2200 third stage and 400 fourth stage larvae were present and the other ewes harboured only third stage larvae. Discussion Regulation of Trichostrongylus species populations does not seem to be based on a turnover of worms as has been reported for Ostertagia species and Haemonchus contortus (Michel 1970, Thomas and Waller 1979). Chiejina and Sewell (1974a, I974b) observed in experimentally infected young lambs that Tcolubriformis infections accumulate until resistance occurs. Subsequently, further acquisition of infection does not occur for some time and finally the worms are expelled. Waller and Thomas (1981) were able to confirm this in naturally infected lambs by comparing the cumulative burdens in tracer lambs with the burdens of lambs which were grazed permanently. A similar comparison in the present study also showed this pattern of population regulation. The lower burdens in the tracer lambs in 1976 in comparison with 1975, and subsequently the longer period of accumulation of Trichostrongylus species burdens in lambs in 1976, were probably caused by the extremely dry summer in that year. Expulsion of Trichostrongylus species burdens in the flock lambs did not begin before OctoberNovember, when the animals were six or seven months old, but the time of expulsion was variable not only between years but also within groups. For instance in one of the flock lambs housed in March 1976 expulsion had not yet occurred. The results in the flock lambs suggest that when expulsion occurs, T vitrinus is expelled selectively, while T colubriformis can remain in the intestine for some time. This indicates differences in the immune response of the host to these species. Coop et al (1979) suggested from two separate but similar experiments with both species that T vitrinus is expelled earlier than T colubriformis, which could be an explanation for the present findings. However, the earlier expulsion of T
TABLE 2: Geometric means of Trichostrongylus species and mean percentages of T colubriformis, T vitrinus and inhibited early third stage larvae (L31 in non-lactating and lactating ewes Non-lactating ewes Lactating ewes (n~38)
Geometric mean (range) Mean % T colubriformis (range) Mean % T vitrinus (range) Mean % early L3 (range)
(n~13)
45
3000
(0-16,900)
(100-39,400)
89·1
3-8
(23'5-100)
(0-20)
10·9
96·2
(0-76'5)
(80-100)
83·6
46·8
(0-100)
(0-100)
vitrinus may also be dose dependent, as the results of the tracer lambs clearly show much higher infections for T vitrinus. Inhibited development of small intestinal Trichostrongylus species was also observed by Ogunsusi and Eysker (1979) and Waller et al (1981) but they were unable to show a relation between the level of inhibition and size of worm burden, host resistance or seasonal factors. The results in the tracer lambs indicated a slight tendency for a seasonal inhibition, though this was not as pronounced as for Haemonchus contortus, Ostertagia species and the large intestinal strongyles in the same animals (Eysker 1980). The large numbers of inhibited early third stage larvae in the flock lambs in December 1976 in comparison with the numbers in the tracer lambs in that year may imply an influence of host resistance on inhibited development. That the numbers of inhibited third stage larvae were not very high in flock lambs in December 1975 in comparison to the tracer lambs can possibly be explained by a lower establishment of Trichostrongylus species infections in late autumn in flock lambs as a result of developing resistance. An influence of host resistance on inhibited development was also seen in the non-lactating and in some lactating ewes, as in these animals often 100 per cent of the Trichostrongylus species populations consisted of inhibited third stage larvae. The results of Jackson et al (1984), who observed high levels of inhibition for T vitrinus in ewes which were experimentally infected, also indicated an influence of host resistance. In the non-lactating ewes host resistance was also reflected by the dominance of T colubrijormis, as seen in older flock lambs which expelled most of their worm burdens. However, in some lactating ewes the low levels of inhibition and the dominance of T vitrinus resembled the situation in flock lambs which had not yet expelled the majority of their worms. This indicates that a relaxation of resistance occurred in some but not all ewes. This relaxation of resistance can result in the development of inhibited larvae and acquisition of overwintered larvae from pasture. In The Netherlands the latter is
Regulation oj trichostrongyle populations
probably more important (Eysker 1980). Reid and Armour (1975) showed for Ostertagia circumcincta and O'Sullivan and Donald (1973) for Haemonchus contortus and T colubrijormis that ewes have a reduced resistance to helminth infections during the last weeks of pregnancy. Jackson et al (1984) could reproduce this for 0 circumcincta but they did not see a reduced resistance to T vitrinus. This shows some resemblance with 'the situation in the five lactating ewes in the present study with the lowest Trichostrongylus species burdens, as these burdens predominantly consisted of inhibited larvae. In short, the sequence in the population regulation of small intestinal Trichostrongylus species seems to be as follows. An accumulation of worm burdens occurs in the lambs. When resistance develops in autumn or winter no further infection is required and subsequently a selective expulsion of T vitrinus occurs. In ewes T colubrijormis is usually not present and either no worms or only low burdens of predominantly inhibited larvae can be found. Around parturition a relaxation of resistance occurs in some but not all ewes, resulting in populations with low levels of inhibition, which are dominated by T vitrinus. The tracer lamb results show, as in other temperate areas such as north east England (Waller and Thomas 1981) and winter rainfall regions in Australia (Anderson 1972), that T vitrinus is the dominating species. T colubrijormis is better adapted to warmer climates as, for instance, the dominance of this species in northern Nigeria (Ogunsusi and Eysker 1979) and summer rainfall areas in Australia (Southcott et a11976) shows. In an intermediate rainfall zone in Australia, Waller et al (1981) observed a biphasic seasonal pattern of Trichostrongylus species infections in tracer lambs, with T vitrinus dominating in the spring peak and T colubrijormis in the autumn peak. This possibly indicates that the circumstances for translation of T colubrijormis are better following summer and those for T vitrinus following winter. In the present experiments a somewhat higher proportion of T colubrijormis was seen in the burdens of tracer lambs grazed between May and September than in the burdens of those grazed after September. This may be associated with the higher temperatures between May and September. Another explanation may be that initially the new wave of infection, which
271
develops on pasture during this period, is mainly the progeny of worm populations from ewes and yearling sheep. These populations would possibly contain a higher proportion of T colubrijormis than in young lambs. It has to be stressed that, despite our present results, when the whole flock is taken into consideration, Trichostrongylus species populations in The Netherlands will probably only very occasionally be dominated by T colubrijormis. Also within flocks there will be a proportion of sheep which are less resistant. These sheep will tend to harbour large T vitrinus dominated Trichostrongylus species burdens and consequently will have higher faecal egg counts. Thus these carrier animals will largely determine the contamination of the pasture with Trichostrongylus species eggs. Acknowledgement
Dr J. Jansen is thanked for his valuable criticisms of the manuscript. References ANDERSON, N. (1972) Australian Journal ofAgricultural Research 23, 1113-1129 CHIEJINA, S. N. & SEWELL, M. M. H. (l974a) Parasitology 69, 301-314 CHIEJINA, S. N. & SEWELL, M. M. H. (l974b) Parasitology 69, 315-327 COOP, R. L., ANGUS, K. W. & SYKES, A. R. (1979) Research in Veterinary Science 26, 363-371 EYSKER, M. (1978) Veterinary Parasitology 4,29-33 EYSKER, M. (1980) Thesis, University of Utrecht JACKSON, F., COOP, R. L. & WRIGHT, S. E. (1984) Parasitology 89, LXII- LXIII MICHEL, J. F. (1970) Parasitology 61,435-447 OGUNSUSI, R. A. & EYSKER, M. (1979) Research in Veterinary Science 26, 108-110 O'SULLIVAN, B. M. & DONALD, A. D. (1973) International Journal for Parasitology 3,521-530 REID, J. F. S. & ARMOUR, J. (1975) Journal for Comparative Pathology 85, 163-170 SOUTHCOTT, W. H., MAJOR, G. W. & BARGER, J. A. (1976) Australian Journal of Agricultural Research 27, 277-286 THOMAS, R. J. & WALLER, P. J. (1979) Research in Veterinary Science 26, 209-212 WAI,-LER, P. J., DONALD, A. D. & DOBSON, R. J. (1981) Research in Veterinary Science 30,213-216 WALLER, P. J. & THOMAS, R. J. (1981) International Journalfor Parasitology 8, 275-283
Accepted February 3, /987