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Rambouillet ewes
TRICHOSTRONGYLID PARASITE POPULATIONS IN PmGNANT OR LACTATING AND CITED FLORIDA NATrVE AND DORSET/ ~MBOUILLET EWES A. M. ZAJAC,* R. P.
HERDt
and K. E. MCCLURE*
*Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A. ~Department of Veterinary Pathobioiogy, The Ohio State University, Cohnnbus, OH 43210, U.S.A. $Department of Animal Science, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, U.S.A. (Received 4 March 1987; accepted 26 May 1988)
A. M., HERDR. P. and MCCLURE K. E. 1988. Trichostrongylid parasite populations in pregnant or lactating and unmated Florida Native and Dorset~mbouilIet ewes. ~nfe~afiona~ Jo~rn~~for Fffru~~60~0~7 18: 981-985. This study was undertaken to identify factors which might contribute to differences in the periparturient rise (‘PPR) in fecal egg counts observed in two sheep breeds. The popuiation dynamics of naturally acquired trichostrongyle infections were studied in unbred and pregnant or lactating Dorset/Rambouillet and Florida Native ewes. The sheep grazed infective pastures in the fall and were housed from December until the end of the experiment in June. Fecal examination showed consistently higher egg counts in Dorset/Rambouillet sheep than in Florida Natives throughout the experiment. Lambing DorsetRambouillet ewes showed a significant periparturient rise (PPR) while the fecal eggcounts of perip~turient Florida Natives did not differ from controls of that breed. The total worm burdens and parasite species composition were determined in pregnant or lactating and unbred animafs of each breed at about 65 and 125 days post-breeding and at approximately 6 weeks post-lambing. Dorset/Rambouillet ewes had significantly higher trichostrongyle burdens than Florida Natives throughout the experiment. At the point 6 weeks post-lambing, unbred Dorset/Rambouillet and Florida Native ewes had significantly lower worm burdens than lactating animals. When the developmental stages of the parasite were examined, pregnant animals of the two breeds were found to have fewer arrested larvae than unbred animals. These resuhs suggest that although a distinct periparturient egg rise does not occur in Florida Native sheep, they may still be subject to some of the i~unosuppressive changes associated with lactation. AbStraCf-ZAJAC
INDEX KEY WORDS: Sheep: trichostrongyles; periparturient rise; genetic resistance; arrested larvae.
INTRODUCTION THE peripartu~ent rise (PPR) in t~chostron~lid egg numbers in the feces of lambing ewes is a well recognized phenomenon in the common European sheep breeds. This increase in parasite ova is usually seen within a period extending from 2 weeks before lambing to 8 weeks post-lambing and is thought to be the result of an i~unosuppression associated with lactation (Arundel & Ford, 1969; O’Sullivan & Ronald, 1970,1973; Connan, 1974). Recently, Courtney, Parker, McClure & Herd (1984) reported that in naturally infected St. Croix, Barbados Blackbelly and Florida Native ewes, the PPR was reduced or absent when compared with Rambouillet or Finn-Dorset X Rambouillet crossbred ewes. This effect was present in grazing animals and confined ewes and reflected differences in resistance to both existing and newly acquired parasites. No specific information is available, however, showing whether similar differences in worm burdens are present in these breeds during pregnancy and lacta981
tion. In a preliminary report, Loggins, Swanson & Koger (1965) suggested that lower worm burdens were present in Florida Native ewes grazing naturally infected pasture than in Hampshire or Rambouillet ewes. In contrast, in a study using adult animals, Courtney, Parker, McClure & Herd (1985) found that Barbados Blackbelly and St. Croix ewes, which also show a reduced PPR developed worm burdens equal to those of domestic crossbred ewes by the end of the summer grazing season. The present study was undertaken in an attempt to identify differences in the acquisition and/or loss of trichostrongylid parasites between parasite-resistant sheep (Florida Native) and parasite-susceptible sheep (Dorset/~mbouillet crossbred ewes) which might help explain the observed differences in the PPR. MATERIALS AND METHODS Animals. Twenty-five pregnant and 20 unbred Dorset/
Rambouillet ewes and nine pregnant and 12 unbred Florida Native ewes from the Ohio Agricultural Research and
982
A. M.
ZAJAC,
R. P.
HERD
Development Center in Wooster, Ohio were included in the study. AH animals were more than 1 year of age except eight sexually mature Florida Native ewes which were 6-8 months old at the beginning of the study. These sheep were equally divided between experimental groups and no differences between younger and older animals were seen in the results. The Florida Native sheep were derived from a flock maintained at the University of Florida which had not been treated with anthelmintics for more than 23 years. All sheep had grazed naturally infected pasture through the spring and summer of 1983. Experimental design. The sheep were removed from summer grazing pastures in Iate September 1983 and treated with anthelmintic (levamisole, 8 mg kg-‘). At this time ail animals were non-lactating and unbred. Sheep were rotated through three trichostrongyle contaminated pastures of fescue, bluegrass and clover from 1 October until 15 December 1983. Approximately one half of the ewes of each breed were exposed to rams from 1 November to 1 December. Twenty-five Dorset/RambouiIlet and nine Florida Native ewes became pregnant. Following housing in December all animals remained in confinement until the end of the experiment on 6 June 1984 to prevent further infection. All parasitological data, therefore, were derived from infection acquired the previous fall. Fecal egg counts and the development of the PPR were monitored through pregnancy and the first 6 weeks of lactation. Rectal fecal samples were collected once in January. twice in February and then weekly from 6 March to 6 June. Lambing occurred during the period 11 April-5 May. In order to characterize the parasite populations through pregnancy and lactation, both bred and unbred ewes from each breed were necropsied and their worm burdens determined at three points during this period. Four pregnant dnd four unbred Dorset/Rambouillet and two pregnant and five unbred Florida Native ewes were necropsied on 18 January (49-79 days post-breeding). On 22 March (112-142 days post-breeding, or about 1 month before lambing) four pregnant and five unbred Dorset/ Rambouillet and three pregnant and three unbred Florida Native ewes were killed. Florida Native ewes lambed between 11 April and 14 April while ~orset/Rambouillet ewes lambed between 1I April and 5 May. Worm burdens
40
CI
DIEM/ Rambwllet Dorset/Aombou~Ilet
-
Florldo
Native
Preg./Lac.
CI
Florida
Native
Unbred
and K. E. MCCLURE during early lactation were determined by killing ewe5 approximately 6 weeks after lambing when the PPR was expected to be present. Because the average lambing dates of the two breeds were separated by approximately 2 weeks, three unbred and four lactating Florida Native ewes were killed on 22 May and four unbred and six lactating Dorseti Rambouillet ewes on 6 June. Parasifologiculrechniques. Fecal egg counts were made by the modified McMaster technique (Whitlock, 1948). Total worm burdens were obtained by counting parasites in 10% aliquots of abomasal and small intestinal contents. In addition, scrapings of the abomasal mucosa were digested at 40°C in a 1%hydrochloric acid and 1% pepsin solution for approximately 2 h. Digestion was stopped by adding formalin and a 10% aliquot was collected and examined for parasites. The large intestine and cecum were visually inspected for parasites at the time of necropsy. Scatisfics.Data were analysed by analysis of variance. Multiple comparisons were made by Duncan’s New Multiple Range test. Worm burdens were log transformed and fecal egg counts expressed as the square root of the value to stabilize the variance and facilitate analysis. RESULTS
Fecal egg counts As expected, a PPR occurred in Dorset/Rambouillet ewes from 1 week before the average lambing date (25 April) to 6 weeks post-lambing, when the experiment was terminated (Fig. 1). Lactating Dorset/ Rambouillet ewes reached a peak of 1760 epg during this period compared to a peak of 940 epg in the unbred ewes. An earlier peak in fecal egg counts was seen in the pregnant ewes on 20 March. This was primarily due to one very high sample (20,000 epg), although the presence of large numbers of adult Trichostrongylus axei in the Dorset/Rambouillet ewes from January to March maintained elevated fecal egg counts during this period. In contrast. Florida Native ewes had consistently lower egg counts throughout the experiment with a peak of only
Preg /Lot Unbred
P
DATE FIG. 1. Mean
square
root of fecal egg counts
of confined unbred and pregnant/lactating Rambouillet ewes.
Florida
Native
and Dorset/
Reproductive
status in parasite
300 epg. No differences in fecal egg counts were seen between lactating and unbred Florida Native ewes.
The changes occurring in the trichostrongyl~d population of the four groups of ewes are shown in Fig. 2. Little change occurred in the parasite populations of both breeds from January to March. In the unmated DorseURambouillet ewes a considerable decline is evident between March and June. A similar though smaller decrease is seen in the Florida Native unmated ewes. The effect of reproductive status on total worm burden is evident only at 6 weeks postlambing when lactating ewes had greater worm burdens than unmated ewes. A three-way analysis of variance was performed on log-transformed worm burdens using the variables of time, breed and reproductive status. Dorset/Rambouillet ewes had significantly greater worm burdens than Florida Natives (P< 0.001). The decline in worm burdens for all groups over the course of the experiment was statistically significant also (P< 0.02). Lactating animals of both breeds had significantly greater (P < 0.05) worm burdens than unbred ewes at 6 weeks post-lambing. Tables 1 and 2 show the composition and developmental stages of the trichostrongylid parasite burdens of the abomasum and small intestine of each group. Since the earliest point at which animals were killed was 1 month after housing and removal from infection it can be assumed that 4th stage Haemonchus and Ostertagia and 3rd stage Tri&hostron~l~ axei larvae represent arrested larvae. Although some fourth stage T. uxei larvae were present in small numbers, it is not clear whether they represented an additional arrested population or whether they were arrested larvae which had resumed development. T. axei was the
D4TE
FIG. 2. Mean total worm burdens of confined unbred and pregnant/lactating Florida Native and Dorsev’Rambouiltet eWeS.
983
resistance
most prevalent parasite throughout the study and also occurred in the highest numbers. The greatest number of arrested larvae of the abomasai parasites was present in January in both breeds. Although the proportion of T. axei larvae was low compared to adults, more than 90% of all Haemonchus and Ostertagia were 4th stage arrested larvae. This number decreased in March (Ostertagia 39%, Haemonchus 23%) and, by the end of the experiment, both lactating Florida Native and Dorset/ Rambouillet ewes had few arrested larvae remaining. In contrast, unbred ewes of both breeds showed low worm numbers but a high proportion of arrested larvae in May and June. This difference between the percentage of arrested larvae in lactating (1.8%) and unbred animals (44.6%) 6 weeks post-lambing was significant (P< 0.05). DISCUSSION
The results of this study provide further information on the dynamics of trichostrongyle populations in a parasite-resistant breed, the Florida Native. In addition to con~r~ng the finding of Courtney e&al. (1984) that confined FIorida Native ewes of the lineage maintained at OARDC in Ohio do not develop a PPR, the results also showed that Florida Native ewes carried significantly lower trichostrongylid worm burdens than crossbred domestic ewes throughout pregnancy and the periparturient period. While marked variation in the total worm burdens and fecal egg counts of Florida Native and Dorset/ Rambouiliet sheep were seen, there appeared to be little difference between the two breeds in the dynamics of the parasite populations during pregnancy. In both pregnant and unmated ewes the largest number of arrested larvae was found in January. No significant loss of parasites occurred between January and March in any of the groups. However, the proportion of larval parasites was smaller in March. The percentage of arrested Ostertagia circumcincta decreased from a combined mean (both breeds) of 96% in January to 39% in March. Similarly, arrested larvae of H. coniort~s decreased from 92% in January to 23% in March. These results suggest that in northern Ohio resumption of development by arrested larvae which produces the ‘spring rise’ has begun by late March. The reproductive status of the sheep influenced worm burdens only during lactation in late May and June. At this time total worm burdens of unbred ewes of both breeds had decreased by 90%. In contrast, there were si~~cantly more t~chostron~le parasites in lactating than in unmated ewes of both breeds, although the total worm burdens of the Florida Native ewes remained lower than those of Dorset/Rambouillet ewes in both lactating and unbred animals. Another indication of the alterations in the normal host/parasite equilibrium seen in lactating animals is the proportion of adult parasites present in periparturient animals. In this study, the worm burdens of lactating ewes were composed almost entirely (greater
984
A. M. ZAJAC,
TABLE 1-ABOMASAI.
TRICHOSTRONGYIX
SPECIES
COMPOSITION
AND FLORIDA NATIVE
Trichostrongylus axei
R. P. HERD and K. E. MCCLURE
UNBRED
DEVELOPMENTAL STAGE (MEAN) IN DORSET/RAMBOUILLET AND LACTATINGEWES
AND AND
PREGNANT
%
Ostertagia circumcincia
%
Arrested larvae
Arrested (L3)
(L4)
Q-5)
larvae
G-4)
G-5)
Haemonchus contnrim @-4)
(L5)
x0 ATreSted larvae
Dar/Ram-Unbred 0 0 0
8000 11,000 320
4 0 9
4650 320 740
340 1030 60
93 24 93
600 80 10
110 100 10
85 44 50
1118 50 3/22 0 616 0 Fla Nat-Unbred
40 0 0
7330 8700 3900
1 0 0
2380 510
70 5510
97 8
830 50
60 1200
93 4
280
3630
7
0
130
0
l/18 40 3/22 0 5/22 40 Fla Nat-Preg/Lac
30 0 20
1118 3/22 s/22
0 0 10
l/18 280 3/22 0 6/6 30 DoriRam-Preg/Lac
Note: All
20 10 0
% rounded
890 250 10 730 220 1250
4 0 57
hOO 350 160
30 90 210
95 80 43
210 10 0
10 70 70
95 13 0
3 4 0
440 30 0
0 50 100
100 38 0
105 SO 0
10 90 30
92 36 0
to nearest digit; all other numbers
to nearest 10.
than 90%) of adult worms regardless of sheep breed. In contrast, the unmated ewes of both breeds had proportionately fewer adult worms and correspondingly more larvae. Connan (1968), Ayalew & Gibbs (1973) and Blitz & Gibbs (1972) also found that the number of larval parasites was low in lactating ewes not exposed to new infection. Data from this study suggest that resumption of development of arrested larvae was similar in both mated and unmated animals and that both adult Trichostrongylus and arrested larvae which matured in early spring were not expelled in the lactating ewes. These results are similar
TABLE
z--SMALL
INTESTINAL
T~ICHOSTRONGYLE
BREED
Dar/Ram-Unbred l/18 31’22
6i6 Dar/Ram-Preg/Lac l/18 3/22 6/6 Fla Nat-Unbred l/18 3/22 5/22 Fla Nat-Preg/Lac l/18 3/22 s/22
to those of Donald, Morley, Wailer, Axelsen, Dobson & Donnelly (1982) who found that larval arrest and resumption of development were unaffected by lactation and that the PPR was due to reduced loss of adult parasites in ewes exposed to reinfection during lactation. The absence of the PPR in the Florida Native ewes might seem to suggest that the pe~parturient suppression of immunity does not develop in this breed. The population dynamics observed in this study, however. indicate that Florida Native sheep may be partially subject to the immunosuppressive changes associated
AND
REPRODUCTIVE
SPECIES
CO~~POSITION
(MEA3)
By
STATUS
Nematodirus
Trichostrongyius
Cooperia
SPP*
VP.
VP,
2YOO 4400 0
0
90 4200 HO0
0 0 10
1500 140 0
10 0
0 70 4YO
0 0 0
0 0
0
Reproductive
status in parasite
with lactation. Thus, lactating Florida Native ewes had a lower proportion of arrested larvae and larger worm burdens than unbred animals. In Dorset/Rambouillet ewes the periparturient suppression also affects adult worm turnover but may have a more substantial impact on egg production than in the Florida Native. The existence of an immunosuppression affecting both breeds but varying in the degree of its effects is supported by the finding of Courtney, Gessner, Scholz & Loggins (1985, Abstract in Proceedings of the 30th Annual Meeting of the American Association of Veterinary Parasitologists, Las Vegas, Nevada, p. 17) that other strains
Florida Native which have undergone less rigorous selection for parasite resistance (i.e. more frequent anthelmintic treatment) do show a PPR. While the pattern of acquisition and loss of trichostrongyles appears to be similar between the Florida Native and domestic breeds, the lower worm burdens and absence of the PPR make this breed potentially valuable in breeding programs for parasite resistance. As the problem of anthelmintic resistance increases this type of host-mediated control becomes more appeating, especially in areas where sheep are intensively grazed and anthelmintic treatments are not always effective. of
Acknowledgements-We are very grateful for the assistance provided by Mr Gary Lowe, Mr Russell Stall and the staff at the sheep production unit of the Ohio Agricultural Research and Development Center in Wooster, Ohio. We also wish to thank MS Karen Willardsen for her technical assistance.
REFERENCES ARUNDEL J. H. & FORD G. anthelmintic treatment to in faecal worm egg counts Journal 45: 89-93. AYALEW H. & GIBBS H. C.
E. 1969. The use of a single control the post-parturient rise in sheep. Australian Veterinar) 1973. Seasonal
fluctuations
of
resistance
985
nematode populations in breeding ewes and lambs. Canudian Journal of Comparative Medicine 31: 79-89. BLITZ N. M. & GIBBS H. C. 1972. Studies on the arrested development of ~aemonr~~ rontortus in sheep--II. Termination of arrested development and the spring rise phenomenon. International Journal fur Parasitology 2: 13-22. CONNANR. M. 1968. Studies on the worm populations in the alimentary tract of breeding ewes. Journal ofHelminthology 48: 9-28. CONNANR. M. 1974. The spring rise in the fecal egg count. In: Helminth Disease of Cattle, Sheep and Horses in Europe (Edited by URQHUART G. M. and ARMOUR J.), Proceedings of a workshop held at the Veterinary School, U~versity-of Glasgow, April, lY73, pp. 36-4i. Robert MacLehose, The University Press, Glasgow. COURTNEY C. H., PARKER C:F., M&r.& K. E. & HERD R. P. 1984. A comparison of the periparturient rise in fecal egg counts of exotic and domestic ewes. International Journalfor Parasitology 14: 377-38 1, COURTNEY C. H., PARKER C. F., MCCLURE K. E. & HERD R. P. 1985. Resistance of non-lambing exotic and domestic ewes to naturally acquired gastrointestinal nematodes. International Journalfor Parasitology 15: 239-243. DONALD A. D., MORLEY F. H. W., WALLER D. J., AXELSON A., DOBSON R. J. & DONNELLY J. R. 1982. Effects of reproduction, genotype and anthelmintic treatment of ewes on Ostertagia spp. populations. International Journal for Parasitology 12: 403-4 11. LOGGINS P. E., SWANSON L. E. & KOCER M. 1965. Parasite levels in sheep as affected by heredity. Journal ofAnimal Science 24: 286-287. O’SULLIVAN B. M. & DONALD A. D. 1970. A field study of nematode parasite populations in the lactating ewe. Parasitology 6 1: 30 1-3 I S O’SULLIVAN B. M. & DONALD A. D. 1973. Responses to infection with ~aemonchus cont~rtus and Trichosrrongy1t.t~cohbriformis in ewes of different reproductive status. International Journal for Parasitology 3: 52 i-530. WHITLOCK H. V. 1948. Some modifications of the McMaster helminth egg-counting technique apparatus. Journal of the Council on Scientific and Industrial Research 21: 177-180.
HERDt
and K. E. MCCLURE*
*Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A. ~Department of Veterinary Pathobioiogy, The Ohio State University, Cohnnbus, OH 43210, U.S.A. $Department of Animal Science, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, U.S.A. (Received 4 March 1987; accepted 26 May 1988)
A. M., HERDR. P. and MCCLURE K. E. 1988. Trichostrongylid parasite populations in pregnant or lactating and unmated Florida Native and Dorset~mbouilIet ewes. ~nfe~afiona~ Jo~rn~~for Fffru~~60~0~7 18: 981-985. This study was undertaken to identify factors which might contribute to differences in the periparturient rise (‘PPR) in fecal egg counts observed in two sheep breeds. The popuiation dynamics of naturally acquired trichostrongyle infections were studied in unbred and pregnant or lactating Dorset/Rambouillet and Florida Native ewes. The sheep grazed infective pastures in the fall and were housed from December until the end of the experiment in June. Fecal examination showed consistently higher egg counts in Dorset/Rambouillet sheep than in Florida Natives throughout the experiment. Lambing DorsetRambouillet ewes showed a significant periparturient rise (PPR) while the fecal eggcounts of perip~turient Florida Natives did not differ from controls of that breed. The total worm burdens and parasite species composition were determined in pregnant or lactating and unbred animafs of each breed at about 65 and 125 days post-breeding and at approximately 6 weeks post-lambing. Dorset/Rambouillet ewes had significantly higher trichostrongyle burdens than Florida Natives throughout the experiment. At the point 6 weeks post-lambing, unbred Dorset/Rambouillet and Florida Native ewes had significantly lower worm burdens than lactating animals. When the developmental stages of the parasite were examined, pregnant animals of the two breeds were found to have fewer arrested larvae than unbred animals. These resuhs suggest that although a distinct periparturient egg rise does not occur in Florida Native sheep, they may still be subject to some of the i~unosuppressive changes associated with lactation. AbStraCf-ZAJAC
INDEX KEY WORDS: Sheep: trichostrongyles; periparturient rise; genetic resistance; arrested larvae.
INTRODUCTION THE peripartu~ent rise (PPR) in t~chostron~lid egg numbers in the feces of lambing ewes is a well recognized phenomenon in the common European sheep breeds. This increase in parasite ova is usually seen within a period extending from 2 weeks before lambing to 8 weeks post-lambing and is thought to be the result of an i~unosuppression associated with lactation (Arundel & Ford, 1969; O’Sullivan & Ronald, 1970,1973; Connan, 1974). Recently, Courtney, Parker, McClure & Herd (1984) reported that in naturally infected St. Croix, Barbados Blackbelly and Florida Native ewes, the PPR was reduced or absent when compared with Rambouillet or Finn-Dorset X Rambouillet crossbred ewes. This effect was present in grazing animals and confined ewes and reflected differences in resistance to both existing and newly acquired parasites. No specific information is available, however, showing whether similar differences in worm burdens are present in these breeds during pregnancy and lacta981
tion. In a preliminary report, Loggins, Swanson & Koger (1965) suggested that lower worm burdens were present in Florida Native ewes grazing naturally infected pasture than in Hampshire or Rambouillet ewes. In contrast, in a study using adult animals, Courtney, Parker, McClure & Herd (1985) found that Barbados Blackbelly and St. Croix ewes, which also show a reduced PPR developed worm burdens equal to those of domestic crossbred ewes by the end of the summer grazing season. The present study was undertaken in an attempt to identify differences in the acquisition and/or loss of trichostrongylid parasites between parasite-resistant sheep (Florida Native) and parasite-susceptible sheep (Dorset/~mbouillet crossbred ewes) which might help explain the observed differences in the PPR. MATERIALS AND METHODS Animals. Twenty-five pregnant and 20 unbred Dorset/
Rambouillet ewes and nine pregnant and 12 unbred Florida Native ewes from the Ohio Agricultural Research and
982
A. M.
ZAJAC,
R. P.
HERD
Development Center in Wooster, Ohio were included in the study. AH animals were more than 1 year of age except eight sexually mature Florida Native ewes which were 6-8 months old at the beginning of the study. These sheep were equally divided between experimental groups and no differences between younger and older animals were seen in the results. The Florida Native sheep were derived from a flock maintained at the University of Florida which had not been treated with anthelmintics for more than 23 years. All sheep had grazed naturally infected pasture through the spring and summer of 1983. Experimental design. The sheep were removed from summer grazing pastures in Iate September 1983 and treated with anthelmintic (levamisole, 8 mg kg-‘). At this time ail animals were non-lactating and unbred. Sheep were rotated through three trichostrongyle contaminated pastures of fescue, bluegrass and clover from 1 October until 15 December 1983. Approximately one half of the ewes of each breed were exposed to rams from 1 November to 1 December. Twenty-five Dorset/RambouiIlet and nine Florida Native ewes became pregnant. Following housing in December all animals remained in confinement until the end of the experiment on 6 June 1984 to prevent further infection. All parasitological data, therefore, were derived from infection acquired the previous fall. Fecal egg counts and the development of the PPR were monitored through pregnancy and the first 6 weeks of lactation. Rectal fecal samples were collected once in January. twice in February and then weekly from 6 March to 6 June. Lambing occurred during the period 11 April-5 May. In order to characterize the parasite populations through pregnancy and lactation, both bred and unbred ewes from each breed were necropsied and their worm burdens determined at three points during this period. Four pregnant dnd four unbred Dorset/Rambouillet and two pregnant and five unbred Florida Native ewes were necropsied on 18 January (49-79 days post-breeding). On 22 March (112-142 days post-breeding, or about 1 month before lambing) four pregnant and five unbred Dorset/ Rambouillet and three pregnant and three unbred Florida Native ewes were killed. Florida Native ewes lambed between 11 April and 14 April while ~orset/Rambouillet ewes lambed between 1I April and 5 May. Worm burdens
40
CI
DIEM/ Rambwllet Dorset/Aombou~Ilet
-
Florldo
Native
Preg./Lac.
CI
Florida
Native
Unbred
and K. E. MCCLURE during early lactation were determined by killing ewe5 approximately 6 weeks after lambing when the PPR was expected to be present. Because the average lambing dates of the two breeds were separated by approximately 2 weeks, three unbred and four lactating Florida Native ewes were killed on 22 May and four unbred and six lactating Dorseti Rambouillet ewes on 6 June. Parasifologiculrechniques. Fecal egg counts were made by the modified McMaster technique (Whitlock, 1948). Total worm burdens were obtained by counting parasites in 10% aliquots of abomasal and small intestinal contents. In addition, scrapings of the abomasal mucosa were digested at 40°C in a 1%hydrochloric acid and 1% pepsin solution for approximately 2 h. Digestion was stopped by adding formalin and a 10% aliquot was collected and examined for parasites. The large intestine and cecum were visually inspected for parasites at the time of necropsy. Scatisfics.Data were analysed by analysis of variance. Multiple comparisons were made by Duncan’s New Multiple Range test. Worm burdens were log transformed and fecal egg counts expressed as the square root of the value to stabilize the variance and facilitate analysis. RESULTS
Fecal egg counts As expected, a PPR occurred in Dorset/Rambouillet ewes from 1 week before the average lambing date (25 April) to 6 weeks post-lambing, when the experiment was terminated (Fig. 1). Lactating Dorset/ Rambouillet ewes reached a peak of 1760 epg during this period compared to a peak of 940 epg in the unbred ewes. An earlier peak in fecal egg counts was seen in the pregnant ewes on 20 March. This was primarily due to one very high sample (20,000 epg), although the presence of large numbers of adult Trichostrongylus axei in the Dorset/Rambouillet ewes from January to March maintained elevated fecal egg counts during this period. In contrast. Florida Native ewes had consistently lower egg counts throughout the experiment with a peak of only
Preg /Lot Unbred
P
DATE FIG. 1. Mean
square
root of fecal egg counts
of confined unbred and pregnant/lactating Rambouillet ewes.
Florida
Native
and Dorset/
Reproductive
status in parasite
300 epg. No differences in fecal egg counts were seen between lactating and unbred Florida Native ewes.
The changes occurring in the trichostrongyl~d population of the four groups of ewes are shown in Fig. 2. Little change occurred in the parasite populations of both breeds from January to March. In the unmated DorseURambouillet ewes a considerable decline is evident between March and June. A similar though smaller decrease is seen in the Florida Native unmated ewes. The effect of reproductive status on total worm burden is evident only at 6 weeks postlambing when lactating ewes had greater worm burdens than unmated ewes. A three-way analysis of variance was performed on log-transformed worm burdens using the variables of time, breed and reproductive status. Dorset/Rambouillet ewes had significantly greater worm burdens than Florida Natives (P< 0.001). The decline in worm burdens for all groups over the course of the experiment was statistically significant also (P< 0.02). Lactating animals of both breeds had significantly greater (P < 0.05) worm burdens than unbred ewes at 6 weeks post-lambing. Tables 1 and 2 show the composition and developmental stages of the trichostrongylid parasite burdens of the abomasum and small intestine of each group. Since the earliest point at which animals were killed was 1 month after housing and removal from infection it can be assumed that 4th stage Haemonchus and Ostertagia and 3rd stage Tri&hostron~l~ axei larvae represent arrested larvae. Although some fourth stage T. uxei larvae were present in small numbers, it is not clear whether they represented an additional arrested population or whether they were arrested larvae which had resumed development. T. axei was the
D4TE
FIG. 2. Mean total worm burdens of confined unbred and pregnant/lactating Florida Native and Dorsev’Rambouiltet eWeS.
983
resistance
most prevalent parasite throughout the study and also occurred in the highest numbers. The greatest number of arrested larvae of the abomasai parasites was present in January in both breeds. Although the proportion of T. axei larvae was low compared to adults, more than 90% of all Haemonchus and Ostertagia were 4th stage arrested larvae. This number decreased in March (Ostertagia 39%, Haemonchus 23%) and, by the end of the experiment, both lactating Florida Native and Dorset/ Rambouillet ewes had few arrested larvae remaining. In contrast, unbred ewes of both breeds showed low worm numbers but a high proportion of arrested larvae in May and June. This difference between the percentage of arrested larvae in lactating (1.8%) and unbred animals (44.6%) 6 weeks post-lambing was significant (P< 0.05). DISCUSSION
The results of this study provide further information on the dynamics of trichostrongyle populations in a parasite-resistant breed, the Florida Native. In addition to con~r~ng the finding of Courtney e&al. (1984) that confined FIorida Native ewes of the lineage maintained at OARDC in Ohio do not develop a PPR, the results also showed that Florida Native ewes carried significantly lower trichostrongylid worm burdens than crossbred domestic ewes throughout pregnancy and the periparturient period. While marked variation in the total worm burdens and fecal egg counts of Florida Native and Dorset/ Rambouiliet sheep were seen, there appeared to be little difference between the two breeds in the dynamics of the parasite populations during pregnancy. In both pregnant and unmated ewes the largest number of arrested larvae was found in January. No significant loss of parasites occurred between January and March in any of the groups. However, the proportion of larval parasites was smaller in March. The percentage of arrested Ostertagia circumcincta decreased from a combined mean (both breeds) of 96% in January to 39% in March. Similarly, arrested larvae of H. coniort~s decreased from 92% in January to 23% in March. These results suggest that in northern Ohio resumption of development by arrested larvae which produces the ‘spring rise’ has begun by late March. The reproductive status of the sheep influenced worm burdens only during lactation in late May and June. At this time total worm burdens of unbred ewes of both breeds had decreased by 90%. In contrast, there were si~~cantly more t~chostron~le parasites in lactating than in unmated ewes of both breeds, although the total worm burdens of the Florida Native ewes remained lower than those of Dorset/Rambouillet ewes in both lactating and unbred animals. Another indication of the alterations in the normal host/parasite equilibrium seen in lactating animals is the proportion of adult parasites present in periparturient animals. In this study, the worm burdens of lactating ewes were composed almost entirely (greater
984
A. M. ZAJAC,
TABLE 1-ABOMASAI.
TRICHOSTRONGYIX
SPECIES
COMPOSITION
AND FLORIDA NATIVE
Trichostrongylus axei
R. P. HERD and K. E. MCCLURE
UNBRED
DEVELOPMENTAL STAGE (MEAN) IN DORSET/RAMBOUILLET AND LACTATINGEWES
AND AND
PREGNANT
%
Ostertagia circumcincia
%
Arrested larvae
Arrested (L3)
(L4)
Q-5)
larvae
G-4)
G-5)
Haemonchus contnrim @-4)
(L5)
x0 ATreSted larvae
Dar/Ram-Unbred 0 0 0
8000 11,000 320
4 0 9
4650 320 740
340 1030 60
93 24 93
600 80 10
110 100 10
85 44 50
1118 50 3/22 0 616 0 Fla Nat-Unbred
40 0 0
7330 8700 3900
1 0 0
2380 510
70 5510
97 8
830 50
60 1200
93 4
280
3630
7
0
130
0
l/18 40 3/22 0 5/22 40 Fla Nat-Preg/Lac
30 0 20
1118 3/22 s/22
0 0 10
l/18 280 3/22 0 6/6 30 DoriRam-Preg/Lac
Note: All
20 10 0
% rounded
890 250 10 730 220 1250
4 0 57
hOO 350 160
30 90 210
95 80 43
210 10 0
10 70 70
95 13 0
3 4 0
440 30 0
0 50 100
100 38 0
105 SO 0
10 90 30
92 36 0
to nearest digit; all other numbers
to nearest 10.
than 90%) of adult worms regardless of sheep breed. In contrast, the unmated ewes of both breeds had proportionately fewer adult worms and correspondingly more larvae. Connan (1968), Ayalew & Gibbs (1973) and Blitz & Gibbs (1972) also found that the number of larval parasites was low in lactating ewes not exposed to new infection. Data from this study suggest that resumption of development of arrested larvae was similar in both mated and unmated animals and that both adult Trichostrongylus and arrested larvae which matured in early spring were not expelled in the lactating ewes. These results are similar
TABLE
z--SMALL
INTESTINAL
T~ICHOSTRONGYLE
BREED
Dar/Ram-Unbred l/18 31’22
6i6 Dar/Ram-Preg/Lac l/18 3/22 6/6 Fla Nat-Unbred l/18 3/22 5/22 Fla Nat-Preg/Lac l/18 3/22 s/22
to those of Donald, Morley, Wailer, Axelsen, Dobson & Donnelly (1982) who found that larval arrest and resumption of development were unaffected by lactation and that the PPR was due to reduced loss of adult parasites in ewes exposed to reinfection during lactation. The absence of the PPR in the Florida Native ewes might seem to suggest that the pe~parturient suppression of immunity does not develop in this breed. The population dynamics observed in this study, however. indicate that Florida Native sheep may be partially subject to the immunosuppressive changes associated
AND
REPRODUCTIVE
SPECIES
CO~~POSITION
(MEA3)
By
STATUS
Nematodirus
Trichostrongyius
Cooperia
SPP*
VP.
VP,
2YOO 4400 0
0
90 4200 HO0
0 0 10
1500 140 0
10 0
0 70 4YO
0 0 0
0 0
0
Reproductive
status in parasite
with lactation. Thus, lactating Florida Native ewes had a lower proportion of arrested larvae and larger worm burdens than unbred animals. In Dorset/Rambouillet ewes the periparturient suppression also affects adult worm turnover but may have a more substantial impact on egg production than in the Florida Native. The existence of an immunosuppression affecting both breeds but varying in the degree of its effects is supported by the finding of Courtney, Gessner, Scholz & Loggins (1985, Abstract in Proceedings of the 30th Annual Meeting of the American Association of Veterinary Parasitologists, Las Vegas, Nevada, p. 17) that other strains
Florida Native which have undergone less rigorous selection for parasite resistance (i.e. more frequent anthelmintic treatment) do show a PPR. While the pattern of acquisition and loss of trichostrongyles appears to be similar between the Florida Native and domestic breeds, the lower worm burdens and absence of the PPR make this breed potentially valuable in breeding programs for parasite resistance. As the problem of anthelmintic resistance increases this type of host-mediated control becomes more appeating, especially in areas where sheep are intensively grazed and anthelmintic treatments are not always effective. of
Acknowledgements-We are very grateful for the assistance provided by Mr Gary Lowe, Mr Russell Stall and the staff at the sheep production unit of the Ohio Agricultural Research and Development Center in Wooster, Ohio. We also wish to thank MS Karen Willardsen for her technical assistance.
REFERENCES ARUNDEL J. H. & FORD G. anthelmintic treatment to in faecal worm egg counts Journal 45: 89-93. AYALEW H. & GIBBS H. C.
E. 1969. The use of a single control the post-parturient rise in sheep. Australian Veterinar) 1973. Seasonal
fluctuations
of
resistance
985
nematode populations in breeding ewes and lambs. Canudian Journal of Comparative Medicine 31: 79-89. BLITZ N. M. & GIBBS H. C. 1972. Studies on the arrested development of ~aemonr~~ rontortus in sheep--II. Termination of arrested development and the spring rise phenomenon. International Journal fur Parasitology 2: 13-22. CONNANR. M. 1968. Studies on the worm populations in the alimentary tract of breeding ewes. Journal ofHelminthology 48: 9-28. CONNANR. M. 1974. The spring rise in the fecal egg count. In: Helminth Disease of Cattle, Sheep and Horses in Europe (Edited by URQHUART G. M. and ARMOUR J.), Proceedings of a workshop held at the Veterinary School, U~versity-of Glasgow, April, lY73, pp. 36-4i. Robert MacLehose, The University Press, Glasgow. COURTNEY C. H., PARKER C:F., M&r.& K. E. & HERD R. P. 1984. A comparison of the periparturient rise in fecal egg counts of exotic and domestic ewes. International Journalfor Parasitology 14: 377-38 1, COURTNEY C. H., PARKER C. F., MCCLURE K. E. & HERD R. P. 1985. Resistance of non-lambing exotic and domestic ewes to naturally acquired gastrointestinal nematodes. International Journalfor Parasitology 15: 239-243. DONALD A. D., MORLEY F. H. W., WALLER D. J., AXELSON A., DOBSON R. J. & DONNELLY J. R. 1982. Effects of reproduction, genotype and anthelmintic treatment of ewes on Ostertagia spp. populations. International Journal for Parasitology 12: 403-4 11. LOGGINS P. E., SWANSON L. E. & KOCER M. 1965. Parasite levels in sheep as affected by heredity. Journal ofAnimal Science 24: 286-287. O’SULLIVAN B. M. & DONALD A. D. 1970. A field study of nematode parasite populations in the lactating ewe. Parasitology 6 1: 30 1-3 I S O’SULLIVAN B. M. & DONALD A. D. 1973. Responses to infection with ~aemonchus cont~rtus and Trichosrrongy1t.t~cohbriformis in ewes of different reproductive status. International Journal for Parasitology 3: 52 i-530. WHITLOCK H. V. 1948. Some modifications of the McMaster helminth egg-counting technique apparatus. Journal of the Council on Scientific and Industrial Research 21: 177-180.