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Further Observations on the Development of Hypoderma Lineatum De Villiers and Hypoderma Bovis Degeer (Diptera, Oestridae) in the Bovine Host*
Brit. vet. ] . ( rg66) ,
122,
gr
FURTHER OBSERVATIONS ON THE DEVELOPMENT OF HYPODERMA LINEATUM DE VILLIERS AND HYPODERMA BOVIS DEGEER (DIPTERA, OESTRIDAE) IN THE BOVINE HOST* By
w.
N. BEESLEYt
Ministry of Agriculture, Fisheries and Food Ce ntral Veterinary Laboratory, Weybridge SUMMARY
Bovine oesophagi and spinal canals were examined for first instar larvae of Hypoderma lineatum and H. bovis, respectively. Larvae of H. lineatum were found only within the period September to March, and mainly in November, December and January. A maximum monthly infection of q.·3 per cent was recorded. Up to 52 per cent of apparently infected spinal canals contained larvae of H. bovis. It is suggested that the majority of the warble infections seen in cattle in the south-east of England may be due to H. bovis, and that the weather during the summer of one year probably has a significant effect on the warble infection in the following year. Average warble infections in hides from all parts of England and Wales fell from 3 I ·5 per cent in I 960 to I 8 ·g per cent in I 964.
INTRODUCTION
In previous papers (Beesley, 1961, Ig62) some data on the development of the first instar larvae of the ox warble flies, Hypoderma lineatum de Villiers and H. bovis Degeer, in their natural host were discussed. Additional records are now given of the seasonal occurrence of first instar larvae of H. lineatum and H. bovis in the oesophagus and epidural fat, respectively, of cattle slaughtered at Guildford and Reading abattoirs between I 960 and I 964. The observations were incidental to a programme of research on the use of systemic insecticides against larvae of ox warble flies (Beesley, 1963), but the information obtained has a direct bearing on some present-day problems. The use in Britain of systemically active insecticides against Hypoderma larvae is increasing, especially in view of the decision in I 964 to revoke the Warble Fly (Dressing of Cattle) Order of I 948. It is no longer an offence to leave warbled cattle untreated with derris during the period from mid-March to the end of June. On the other hand, farmers are now encouraged to treat their cattle once with a systemic insecticide either between September and the end of November, or from March onwards, or to use derris as recom- . mended previously. *These observations were included in a thesis accepted by the University of Reading in partial fulfilment of the requirements for a degree of Doctor of Philosophy. tPresent address: Liverpool School of Tropical Medicine, Pembroke Place, Liverpool3.
92
BRITISH VETERINARY JOURNAL,
122,
3
Severe anaphylactic reactions may occasionally follow the treatment of warbled cattle with systemic insecticides (Rosenberger, 1959; Bracewell & Schurr, 196o; Scharff, Sharman & Ludwig, 1962; Bouvier, 1964). It has been suggested ·that these toxic symptoms are due to the interaction between enzymes and other substances released from killed larvae and the tissues of the host (Scharff, Sharman & Ludwig, 1962). It is, therefore, useful to have as much information as possible about the movements of warble larvae within the body of the host. In this paper some information is also given on the relation between the incidence of warbles in hides and the weather conditions which may have influenced the free-living stages of the previous generation. EXAMINATION OF THE MATERIAL
The oesophagi and spinal canals of freshly slaughtered cattle were examined as described previously (Beesley, 1961, 1962), with the exception that epidural fat from which all evident larvae of H. bovis had been recovered at the abattoir was taken to the laboratory for further examination. It was found best to search the fat at the abattoir while it was still warm, as the larvae were then fairly easy to see. The discoloration around the larvae was also more obvious. As the fat hardened the larvae were more difficult to find, and had to be extracted with care. In the laboratory the fat was placed in a bucket containing hot water which was kept at 35 to 40°C for three to five hours. Under these conditions the remaining larvae floated away and could be collected. Because of their treatment with hot water none of these larvae were implanted into animals, but the additional records gave a better indication of the true incidence of the parasites. RESULTS
Hypoderma lineatum de Villiers The results of the examination of oesophagi at Guildford and Reading abattoirs from September, 1960 to February, 1964 are given in Table I. Some examinations were carried out in August and March, but no larvae were found in the oesophagi before September, nor did any remain after February. The maximum proportion of infected cattle in any one month was 14·3 per cent (at Reading) in December, 1961, when 236 larvae were collected from 27 cattle. The maximum number of larvae taken from a single infected animal was 28. Most of the larvae were collected in November, December or January, although the maximum percentage of infected cattle did not occur consistently in any one of the winter months. Hypoderma bovis Degeer The previous survey at Guildford abattoir (Beesley, 1962) covered the period from February, 1960 to May, 1961. The results of the examination of cattle at Guildford abattoir in 1963 and 1964 are given in Table II. It was
WARBLE FLY INFECTION OF CATTLE
93
TABLE I NUMBERS OF FIRST INSTAR LARVAE OF Hypoderma [ineatum RECOVERED FROM BOVINE OESOPHAGI AT GUILDFOllD AND READIN G ABATTOIRS DURING THE WINTERS OF 1960-61 , 1961-62, 1962-63 AND 1963-64. No . of No. cattle infected larvtu per Total warble i1ifected Abattoir Nlonth No. cattle examined Tear /arme oesof•lwgus (percentage infection in brackets) 1g6o-61
Guildford
September October November December january February March
Total 1g61-62
Guild ford
November December january February
Total 1g62-63
Guild ford
August September October November December january February
Total Reading
October November December January February
Total Ig63-64
Guildford
September October November December .January February
Total Reading
Total
Septembt'r October November December january February
I
67 68 18 77 0
0
J·O
6·7 9"7 g·o 4"5 0 0
231
6·2
1/122(o·8) 2/207(0·9) 9/3 71 (2·4) o/197(0 ) I 5/4o6(3 "7) 1/ 127(0•8)
12 8 58 0 82 2
12"0 4"0 6 ·4
28/1430(1"9)
162
5·8
12/135(8·8) 27/189(14"3) 3/212(1"4) o/22 (o )
140 8 0
11"7 8·7 2·6 0
42/558(7"5)
384
9"1
o/21 (o ) s/wo(yo) 4/286(1·4) 16/295(2"2) 1/126(0·7 ) 10/130(7·6) 2/152(1"3 )
0 32 20 115 55 6
0 6·4 5"0 7"2 1·0 5"5 g·o
38/1110(3 "4)
229
6·o
4/263(1·5 ) 13/344(3"7) 5/292(1"7) I0/389(2·6) of6J (o )
16 73 16 89 0
4"0 s·6 3"2 8·9 0
32/1349(2·4)
194
6·o
ofso (o ) I/83 (1·2 ) 1/93 (1•1 ) 4/141 (2"9) 9/257(3"5 ) 4/191(2·1)
0 2 28 23 53 38
0 2"0 28 ·o 5"7 5"9 9"5
19/815(2·3)
184
9"7
8/271 (2 ·9) 3/372 (o·8) 17/5o6(3 ·4) 18/36o(yo) 4/I 18(3·4) o/30 (o )
26 139 92 26 0
3"2 3"3 8·2 5"1 6·s 0
50/1657(3"0)
293
5"9
37/1128(3"3) September October November December January February
Total Reading
1/96 (1·0) 10/178(y6) 7/310(2 ·3) 2/170(1·2 ) .17/203(7"4) 0/124(0 ) o/47 (o )
2~
I
10
0
5"4 2"0
BRITISH VETERINARY JOURNAL, 122, 3
94
not possible to examine the spinal canals of cattle at Reading abattoir. During this investigation the object was to collect as many larvae as possible, and only the apparently infected cattle (those with discoloured epidural fat) were inspected. Hence the percentage infection rate is higher than it would have been had all cattle been examined. It was not practicable to examine as many cattle for H. bovis larvae as had been inspected in the H. lineatum survey, but certain conclusions could be drawn. Up to 52 per cent of the cattle which superficially appeared to be infected were found to have larvae in the epidural fat. The maximum monthly intensity of infection was 4 ·4 larvae per infected animal. TABLE II NUMBERS OF FIRST INSTAR LARVAE OF H. bovis RECOVERED FROM BOVINE SPINAL C ANALS AT GUILDFORD ABATTOIR, 1963 AND 1964.
Tear
No. of irifected cattle No. of cattle examined (percentage irifected in brackets )
Total warble larvae
February March April
25/48 (52 ) 39/91 (43) 9/1 18(7•6)
66 86 10
2·6 2•2
Total
73/167(43"7)
!62
2•2
.January February March April May Total
7/126(s·6) 19/103(!8•4) I 1/69 (16) o/19 (o) oj2o (o) 37/337 ( I 2·4*)
10 s8 48 0 0 II6
1"4 3"1 4"4 0
Month
No. of larvae per i'!fected spine
I·I
0
3 •1
• data from April and May (when no larvae found ) are excluded.
DISCUSSION Since 1954 the average annual percentage of hides with open warble holes has fluctuated between I5"5 and 31 ·s (Maitland, 1964t, personal communication), as shown in Table III. The majority of the warble holes observed in any one year are produced by larvae which have developed from eggs laid by adults in the previous year. Since there is only a single generation each year, one would expect that the incidence of infection with third instar larvae in the back in one year would be directly related to the incidence during the preceding winter of first instar TABLE Ill THE
AVERAGE PERCENTAGE OF HIDE THROUGHPUT WHICH SHOWED OPEN WARBLE HOLES, 1954 TO 1964. DATA FROM 40 REPRESENTATIVE HID E MARKETS , SUPPLIED BY THE HIDES AND ALLIED TRADES IMPROVEMENT SO C IETY ( MAITLAND, 1964).
Animal
1954
1955
1956
1957
1958
1959
1960
1961
1g62
1963
1964
Ox Cow Bull
27•8 14"5 J0•7
19"4 8·1 8·o
27 "9 J0•8 J0·6
28·9 9"0 12•4
:ws 15"1 12·g
37 •6 17•5 7•8
35"5 14"1 12·8
36•! 15.4 14•2
32·8 13·6 11·0
26 ·9 9"4 7•6
22'2
All hides
23•5
15" 5
23 "4
27"0
31•1
22 •1
31·5
3 1•1
28 •!
22 •4
18·g
fHide & Allied Trad es Improvement Society, Banstead , Surrey.
7•1 5"3
WARBLE FLY INFECTION OF CATTLE
95
larvae in the oesophagus and/or spinal canal. Data are available for the infection rates of cattle with first instar larvae of H. lineatum from the winter of 1957 onwards, and for larvae of H. bouis from 1959 onwards (Beesley, 1961, 1962 and present paper). More larvae of H. lineatum were recovered from cattle during the winter of 1957-58 than in that of 1958-59, and both these recovery rates tended to be higher than those in any of the succeeding winters. Similarly, more first instar larvae of H. bovis were recovered from cattle during the winter of 1959-60 and 1960-61 than during the winter of 1962-63 and 1963-64.
..
YEAR.
:r
MONTH
~J:t
F 14. A " 1 1 A S 0 N D NICTION
31·5
31-1
28·1
22·4
18·9 1FI'IAM11ASOND Fig. 1. The incidence of open warble holes in bovine hides in England and Wales, 1 ~64, as reported from 40 representative hide markets (d a ta from Maitland, personal communication). The hatched areas of the histograms show the incidence of infection in excess of 40 per cent.
These data therefore reflect the falling incidence of warble infection in hides in 1958 to 1959, and again from 1960 to 1964 (Table III and Fig. 1). There remains the anomaly of the 9 ·4 per cent increase of hides which had open warble holes in 1959 and 1960. No corresponding increase was observed in the percentages of infections of oesophagi with first instar larvae of H. lineatum between the winters of 1958 and 1959· It is possible that the increase in the infection rates in the hides was due to a larger number of larvae of H. bovis, but no relevant data are available for this period. It is now convenient to consider the relationship between weather conditions and the incidence of warble holes in the hides. It may also be possible
g6
BRITISH VETERINARY JOURNAL,
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3
to show if-one of the two species of warble fly is responsible for most of the damage. The highest incidence of open warble holes in bovine hides in Great Britain is recorded at the hide markets in April, May, June and July (Table IV) . It will be seen from Fig. 2 that warble larvae are normally found in the backs of cattle only from late January until the end of July, whereas open warble holes are recorded in each month in hides inspected at the markets. This discrepancy is due to finding old warble cysts and healed holes during the autumn alld winter months, these lesions counting as warble holes for inspection purposes. THE LIFE
HISTORIES
OF
THE
OX
WARBLE FLIE,S. HYPQDERMA IOVIS AND HYPODERMA LINEATUM MONTH
H. LINEATUM
H.IOVIS_
JANUARY LARVAE IN BACK
FEBRUARY
PUPA MARCH APRIL MAY.
T
LARVAE IN BACK
FLY
I I I
PUPA
1
JUNE
LARVAE :MIGRATING 1TO OESOPHAGUS
JULY
I
AUGUST
I
I
I I
I I
I
SEPTEMBER
FLY
T
I
I I LARVAE MIGRATING
LARVAE IN OESOPHAGUS
ro
1 lAND
OCTOBER
RESTING IN THE
NOVEMBER
EPIDURAL FAT
DECEMBER
Jl Fig.
2.
The exit holes of the larvae heal externally in about two weeks, complete cicatrization taking about three to four weeks (Simmons, I 939, and personal observations). Holes which are still open in early April could therefore have been made in March, and those seen in early July could have been made in June. Hence most of the damage to hides is being actively produced in March April, May and June. First instar larvae of H. lineatum have normally all migrated from the oesophagus by the middle of March (Fig. 2) and third instar larvae of this species are rarely seen in the backs of cattle later than the middle of April (Bevan & Edwards, 1951; Beesley, 1964). First instar larvae of H. bovis, on
WARBLE FLY INFECTION OF CATTLE
97
the other hand, have usually all left the spinal canal by the middle of May, and most of the third instar larvae appear in the back in March, April, May and June (Bevan & Edwards, 1951; Beesley, 1964). It is therefore suggested that larvae of H. bovis are responsible for more hide damage than are larvae of H. lineatum. This is emphasized by the shorter time spent in the third instar by H. lineatum than by H. bovis (Scharff, 1950). TABLE IV PERCENTAGE OF TOTAL HIDE THROUGHPUT WITH OPEN WARBLE HOLES. DATA, PROM 40 REPRESENTATIVE HIDE MARKETS, SUPPLIED BY THE HIDES AND ALLIED TRADES IMPROVEMENT SOCIETY (MAITLAND, 1964) ·
Month
Ig6o
1961
1g62
January February March April May June July August September October November December
4'5 10'1 23'1 48·2 59'1 6o·2 6•·5 46·o 25'2 14'2 6·8 5'5
7' 1 15'3 30'7 54'7 56·5 62·8 61 ·5 44'2 26•7 19 '5
4"4 9"4 17'5 39'3 47'5 44'6 43'0 29'6 12'7 7'7 4'4 2'4
2·6 5'3 13'9 27'4 36'4 35'9 37'5 26·1 16•7 6·9 3'1
5'1
6·s 12'5 22 '9 52 '2 52·6 5 1'4 50'3 36·6 20·8 11·6 5'7 3'6
Average
31'5
31'1
28•J
22'4
J8 •9
B·o
1963
1964
2•J
Most of the pupae of H. lineatum are formed in March and April (Fig. 2), and adults are on the wing in late March, April and May. Most H. bovis pupae are formed during May to August, so that the adults emerge from June to September. It has been suggested that the majority of the damage to hides is caused by H. bovis so that weather conditions during May to September would be expected to affect the free-living stages of the fly, and hence the amount of damage to hides caused by the next generation in the following spring and summer. Comparatively few hides were warbled in I955 and 1959, and the incidence ofopen warble holes had fallen each year since 1961 (Table III). It would be expected that climatic conditions were unfavourable for the development of the pupae and/or adults of H. bovis during the summer months of 1954, 1958 and from I96o to I963. The weather conditions during the summers of I 954 to I 963 have been studied by reference to the Monthly Weather Reports of the Meteorological Office (Beesley, I96I, and Table V). Practically every month from May to September in I 954 and I 958 was summarized by the Meteorological Office as "wet", "dull and cool" or "dull and unsettled". Data for the months of May to September during I960-63 are given in Table V. The summer months of I960-63 were not as wet as those of 1954 and 1958, but they were wetter and cooler than average. It is suggested that there is a reasonable correlation between the poor weather at these times and the recorded low incidence of warble infection of the hides in the corresponding following years. It is not suggested that the recent decrease in the amount
BRITISH VETERINARY JOURNAL, 122, 3 TABLE V KAXIMUM, NIEAN AND MINIKUM AIR TEMPERATURES, HOURS OF SUNSHINE AND INCHES OF RAINFALL FOR ENGLAND AND WALES DURING MAY TO SEPTEMBER, 1960-63.
Tear
Weather data
May
Jum
Ig6o
Maximum air tempera ture, °C . Mean air temperature, °C. Minimum air temperature, °C. Percentage sunshine Percentage rainfall
25·6 + •·5 - 6·7 97 72
30·6 + •·5 - 1·1 128 go
1g61
Maximum air temperature Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall
24"4 - 0•2 -6•7 Ill 64
1962
Maximum air temperature Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall Maximum air tempera ture Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall
lg63
August
September
- 1•1 85 141
25"6 -o·8 -1·1 95 140
25·6 - o·5 -1 · 1 94 147
31 "1 + o·4 -2"2 109 69
33"9 -0·9 -1 "1 92 86
31·8 -o·3 ·-I·I 103 100
31·6 +• ·4 - 1•7 97 105
21 "1 -I·O - s-6 89 104
26•7 -0"7 -5·6 119 31
27"2 - 1"5 -1 "1 74 78
25"0 -1"5 -1 ·7 92 137
27•8 - I·o -1·7 136
27•2 -o·8 - 3"9 101 82
28 ·3 +o·I + o·6 94 154
28 ·9 - [•1
26•7 -1 •7 -o·6 75 128
26·1 -0"7 -1"7 106 93
July 25"0 -[•[
-[•[
101 67
88
Mean monthly temperatures are given in the form of the difference from the mean temperature in the corresponding months of previous years. Monthly sunshine and rainfall data are given in the form of the percentage average compared with the corresponding months of previous years (Meteorological Office, Ig6
of warble infection is due entirely to the poor summer weather. The use of insecticides, and especially the introduction of the systemically active insecticides, would also be expected to have some effect on the warble fly population, and there is reason to believe that cattle which have been treated with systemic insecticides show an increased resistance to warble infection (Knapp, Brethour, Harvey & Roan, rg6o). REFERENCES
BEESLEY, W. N. (1961). Ann. trop. Med. Parasit ., 55. 18. BEESLEY, W. N. (1962). Res. vet. Sci., 3, 203. BEESLEY, W. N. ( 1963) . Ann. appl. Biol., ~. 295· BEESLEY, W. N. (1964) . Ph.D. thesis, University of Reading Library. BEVAN, W. ]. & EDWARDS, E. E. (1951). Bull. ent. Res., .f:I, 639. BouVIER, G. ( 1964) . Schweizer A rch. Tierheilk., 1o6, 339· BRACEWELL, C . D. & ScHURR, H R . ( 196o) . Vet. Rec., 72, 281. KNAPP, F. W., BRETHOUR,j. R., HARVEY, T. L. & RoAN, L. C. (196o).]. econ. Ent., 52, 1022. METEOROLOGICAL OFFICE, LoNDON (196o-63). Monthly Weather Reports, 77-8o. RosENBERGER, G. (1959). Dt. tierii.r;:;tl. Wschr., 66, 549· ScHARFF, D. K. (1950). Cattle Grubs. Bull. Mont. agri. E xp. Stn., No. 471. ScHARFF, D. K., SHARMAN, G. A.M. & LUDWIG, P. (1962 ) . ]. Am. vet. med. Ass., I.f:I, 582. SIMMONS, S. W. ( 1939) . ] . Am. vet. med. Ass., 95, 283.
(Received for publication 8 September, 1965)
122,
gr
FURTHER OBSERVATIONS ON THE DEVELOPMENT OF HYPODERMA LINEATUM DE VILLIERS AND HYPODERMA BOVIS DEGEER (DIPTERA, OESTRIDAE) IN THE BOVINE HOST* By
w.
N. BEESLEYt
Ministry of Agriculture, Fisheries and Food Ce ntral Veterinary Laboratory, Weybridge SUMMARY
Bovine oesophagi and spinal canals were examined for first instar larvae of Hypoderma lineatum and H. bovis, respectively. Larvae of H. lineatum were found only within the period September to March, and mainly in November, December and January. A maximum monthly infection of q.·3 per cent was recorded. Up to 52 per cent of apparently infected spinal canals contained larvae of H. bovis. It is suggested that the majority of the warble infections seen in cattle in the south-east of England may be due to H. bovis, and that the weather during the summer of one year probably has a significant effect on the warble infection in the following year. Average warble infections in hides from all parts of England and Wales fell from 3 I ·5 per cent in I 960 to I 8 ·g per cent in I 964.
INTRODUCTION
In previous papers (Beesley, 1961, Ig62) some data on the development of the first instar larvae of the ox warble flies, Hypoderma lineatum de Villiers and H. bovis Degeer, in their natural host were discussed. Additional records are now given of the seasonal occurrence of first instar larvae of H. lineatum and H. bovis in the oesophagus and epidural fat, respectively, of cattle slaughtered at Guildford and Reading abattoirs between I 960 and I 964. The observations were incidental to a programme of research on the use of systemic insecticides against larvae of ox warble flies (Beesley, 1963), but the information obtained has a direct bearing on some present-day problems. The use in Britain of systemically active insecticides against Hypoderma larvae is increasing, especially in view of the decision in I 964 to revoke the Warble Fly (Dressing of Cattle) Order of I 948. It is no longer an offence to leave warbled cattle untreated with derris during the period from mid-March to the end of June. On the other hand, farmers are now encouraged to treat their cattle once with a systemic insecticide either between September and the end of November, or from March onwards, or to use derris as recom- . mended previously. *These observations were included in a thesis accepted by the University of Reading in partial fulfilment of the requirements for a degree of Doctor of Philosophy. tPresent address: Liverpool School of Tropical Medicine, Pembroke Place, Liverpool3.
92
BRITISH VETERINARY JOURNAL,
122,
3
Severe anaphylactic reactions may occasionally follow the treatment of warbled cattle with systemic insecticides (Rosenberger, 1959; Bracewell & Schurr, 196o; Scharff, Sharman & Ludwig, 1962; Bouvier, 1964). It has been suggested ·that these toxic symptoms are due to the interaction between enzymes and other substances released from killed larvae and the tissues of the host (Scharff, Sharman & Ludwig, 1962). It is, therefore, useful to have as much information as possible about the movements of warble larvae within the body of the host. In this paper some information is also given on the relation between the incidence of warbles in hides and the weather conditions which may have influenced the free-living stages of the previous generation. EXAMINATION OF THE MATERIAL
The oesophagi and spinal canals of freshly slaughtered cattle were examined as described previously (Beesley, 1961, 1962), with the exception that epidural fat from which all evident larvae of H. bovis had been recovered at the abattoir was taken to the laboratory for further examination. It was found best to search the fat at the abattoir while it was still warm, as the larvae were then fairly easy to see. The discoloration around the larvae was also more obvious. As the fat hardened the larvae were more difficult to find, and had to be extracted with care. In the laboratory the fat was placed in a bucket containing hot water which was kept at 35 to 40°C for three to five hours. Under these conditions the remaining larvae floated away and could be collected. Because of their treatment with hot water none of these larvae were implanted into animals, but the additional records gave a better indication of the true incidence of the parasites. RESULTS
Hypoderma lineatum de Villiers The results of the examination of oesophagi at Guildford and Reading abattoirs from September, 1960 to February, 1964 are given in Table I. Some examinations were carried out in August and March, but no larvae were found in the oesophagi before September, nor did any remain after February. The maximum proportion of infected cattle in any one month was 14·3 per cent (at Reading) in December, 1961, when 236 larvae were collected from 27 cattle. The maximum number of larvae taken from a single infected animal was 28. Most of the larvae were collected in November, December or January, although the maximum percentage of infected cattle did not occur consistently in any one of the winter months. Hypoderma bovis Degeer The previous survey at Guildford abattoir (Beesley, 1962) covered the period from February, 1960 to May, 1961. The results of the examination of cattle at Guildford abattoir in 1963 and 1964 are given in Table II. It was
WARBLE FLY INFECTION OF CATTLE
93
TABLE I NUMBERS OF FIRST INSTAR LARVAE OF Hypoderma [ineatum RECOVERED FROM BOVINE OESOPHAGI AT GUILDFOllD AND READIN G ABATTOIRS DURING THE WINTERS OF 1960-61 , 1961-62, 1962-63 AND 1963-64. No . of No. cattle infected larvtu per Total warble i1ifected Abattoir Nlonth No. cattle examined Tear /arme oesof•lwgus (percentage infection in brackets) 1g6o-61
Guildford
September October November December january February March
Total 1g61-62
Guild ford
November December january February
Total 1g62-63
Guild ford
August September October November December january February
Total Reading
October November December January February
Total Ig63-64
Guildford
September October November December .January February
Total Reading
Total
Septembt'r October November December january February
I
67 68 18 77 0
0
J·O
6·7 9"7 g·o 4"5 0 0
231
6·2
1/122(o·8) 2/207(0·9) 9/3 71 (2·4) o/197(0 ) I 5/4o6(3 "7) 1/ 127(0•8)
12 8 58 0 82 2
12"0 4"0 6 ·4
28/1430(1"9)
162
5·8
12/135(8·8) 27/189(14"3) 3/212(1"4) o/22 (o )
140 8 0
11"7 8·7 2·6 0
42/558(7"5)
384
9"1
o/21 (o ) s/wo(yo) 4/286(1·4) 16/295(2"2) 1/126(0·7 ) 10/130(7·6) 2/152(1"3 )
0 32 20 115 55 6
0 6·4 5"0 7"2 1·0 5"5 g·o
38/1110(3 "4)
229
6·o
4/263(1·5 ) 13/344(3"7) 5/292(1"7) I0/389(2·6) of6J (o )
16 73 16 89 0
4"0 s·6 3"2 8·9 0
32/1349(2·4)
194
6·o
ofso (o ) I/83 (1·2 ) 1/93 (1•1 ) 4/141 (2"9) 9/257(3"5 ) 4/191(2·1)
0 2 28 23 53 38
0 2"0 28 ·o 5"7 5"9 9"5
19/815(2·3)
184
9"7
8/271 (2 ·9) 3/372 (o·8) 17/5o6(3 ·4) 18/36o(yo) 4/I 18(3·4) o/30 (o )
26 139 92 26 0
3"2 3"3 8·2 5"1 6·s 0
50/1657(3"0)
293
5"9
37/1128(3"3) September October November December January February
Total Reading
1/96 (1·0) 10/178(y6) 7/310(2 ·3) 2/170(1·2 ) .17/203(7"4) 0/124(0 ) o/47 (o )
2~
I
10
0
5"4 2"0
BRITISH VETERINARY JOURNAL, 122, 3
94
not possible to examine the spinal canals of cattle at Reading abattoir. During this investigation the object was to collect as many larvae as possible, and only the apparently infected cattle (those with discoloured epidural fat) were inspected. Hence the percentage infection rate is higher than it would have been had all cattle been examined. It was not practicable to examine as many cattle for H. bovis larvae as had been inspected in the H. lineatum survey, but certain conclusions could be drawn. Up to 52 per cent of the cattle which superficially appeared to be infected were found to have larvae in the epidural fat. The maximum monthly intensity of infection was 4 ·4 larvae per infected animal. TABLE II NUMBERS OF FIRST INSTAR LARVAE OF H. bovis RECOVERED FROM BOVINE SPINAL C ANALS AT GUILDFORD ABATTOIR, 1963 AND 1964.
Tear
No. of irifected cattle No. of cattle examined (percentage irifected in brackets )
Total warble larvae
February March April
25/48 (52 ) 39/91 (43) 9/1 18(7•6)
66 86 10
2·6 2•2
Total
73/167(43"7)
!62
2•2
.January February March April May Total
7/126(s·6) 19/103(!8•4) I 1/69 (16) o/19 (o) oj2o (o) 37/337 ( I 2·4*)
10 s8 48 0 0 II6
1"4 3"1 4"4 0
Month
No. of larvae per i'!fected spine
I·I
0
3 •1
• data from April and May (when no larvae found ) are excluded.
DISCUSSION Since 1954 the average annual percentage of hides with open warble holes has fluctuated between I5"5 and 31 ·s (Maitland, 1964t, personal communication), as shown in Table III. The majority of the warble holes observed in any one year are produced by larvae which have developed from eggs laid by adults in the previous year. Since there is only a single generation each year, one would expect that the incidence of infection with third instar larvae in the back in one year would be directly related to the incidence during the preceding winter of first instar TABLE Ill THE
AVERAGE PERCENTAGE OF HIDE THROUGHPUT WHICH SHOWED OPEN WARBLE HOLES, 1954 TO 1964. DATA FROM 40 REPRESENTATIVE HID E MARKETS , SUPPLIED BY THE HIDES AND ALLIED TRADES IMPROVEMENT SO C IETY ( MAITLAND, 1964).
Animal
1954
1955
1956
1957
1958
1959
1960
1961
1g62
1963
1964
Ox Cow Bull
27•8 14"5 J0•7
19"4 8·1 8·o
27 "9 J0•8 J0·6
28·9 9"0 12•4
:ws 15"1 12·g
37 •6 17•5 7•8
35"5 14"1 12·8
36•! 15.4 14•2
32·8 13·6 11·0
26 ·9 9"4 7•6
22'2
All hides
23•5
15" 5
23 "4
27"0
31•1
22 •1
31·5
3 1•1
28 •!
22 •4
18·g
fHide & Allied Trad es Improvement Society, Banstead , Surrey.
7•1 5"3
WARBLE FLY INFECTION OF CATTLE
95
larvae in the oesophagus and/or spinal canal. Data are available for the infection rates of cattle with first instar larvae of H. lineatum from the winter of 1957 onwards, and for larvae of H. bouis from 1959 onwards (Beesley, 1961, 1962 and present paper). More larvae of H. lineatum were recovered from cattle during the winter of 1957-58 than in that of 1958-59, and both these recovery rates tended to be higher than those in any of the succeeding winters. Similarly, more first instar larvae of H. bovis were recovered from cattle during the winter of 1959-60 and 1960-61 than during the winter of 1962-63 and 1963-64.
..
YEAR.
:r
MONTH
~J:t
F 14. A " 1 1 A S 0 N D NICTION
31·5
31-1
28·1
22·4
18·9 1FI'IAM11ASOND Fig. 1. The incidence of open warble holes in bovine hides in England and Wales, 1 ~64, as reported from 40 representative hide markets (d a ta from Maitland, personal communication). The hatched areas of the histograms show the incidence of infection in excess of 40 per cent.
These data therefore reflect the falling incidence of warble infection in hides in 1958 to 1959, and again from 1960 to 1964 (Table III and Fig. 1). There remains the anomaly of the 9 ·4 per cent increase of hides which had open warble holes in 1959 and 1960. No corresponding increase was observed in the percentages of infections of oesophagi with first instar larvae of H. lineatum between the winters of 1958 and 1959· It is possible that the increase in the infection rates in the hides was due to a larger number of larvae of H. bovis, but no relevant data are available for this period. It is now convenient to consider the relationship between weather conditions and the incidence of warble holes in the hides. It may also be possible
g6
BRITISH VETERINARY JOURNAL,
122,
3
to show if-one of the two species of warble fly is responsible for most of the damage. The highest incidence of open warble holes in bovine hides in Great Britain is recorded at the hide markets in April, May, June and July (Table IV) . It will be seen from Fig. 2 that warble larvae are normally found in the backs of cattle only from late January until the end of July, whereas open warble holes are recorded in each month in hides inspected at the markets. This discrepancy is due to finding old warble cysts and healed holes during the autumn alld winter months, these lesions counting as warble holes for inspection purposes. THE LIFE
HISTORIES
OF
THE
OX
WARBLE FLIE,S. HYPQDERMA IOVIS AND HYPODERMA LINEATUM MONTH
H. LINEATUM
H.IOVIS_
JANUARY LARVAE IN BACK
FEBRUARY
PUPA MARCH APRIL MAY.
T
LARVAE IN BACK
FLY
I I I
PUPA
1
JUNE
LARVAE :MIGRATING 1TO OESOPHAGUS
JULY
I
AUGUST
I
I
I I
I I
I
SEPTEMBER
FLY
T
I
I I LARVAE MIGRATING
LARVAE IN OESOPHAGUS
ro
1 lAND
OCTOBER
RESTING IN THE
NOVEMBER
EPIDURAL FAT
DECEMBER
Jl Fig.
2.
The exit holes of the larvae heal externally in about two weeks, complete cicatrization taking about three to four weeks (Simmons, I 939, and personal observations). Holes which are still open in early April could therefore have been made in March, and those seen in early July could have been made in June. Hence most of the damage to hides is being actively produced in March April, May and June. First instar larvae of H. lineatum have normally all migrated from the oesophagus by the middle of March (Fig. 2) and third instar larvae of this species are rarely seen in the backs of cattle later than the middle of April (Bevan & Edwards, 1951; Beesley, 1964). First instar larvae of H. bovis, on
WARBLE FLY INFECTION OF CATTLE
97
the other hand, have usually all left the spinal canal by the middle of May, and most of the third instar larvae appear in the back in March, April, May and June (Bevan & Edwards, 1951; Beesley, 1964). It is therefore suggested that larvae of H. bovis are responsible for more hide damage than are larvae of H. lineatum. This is emphasized by the shorter time spent in the third instar by H. lineatum than by H. bovis (Scharff, 1950). TABLE IV PERCENTAGE OF TOTAL HIDE THROUGHPUT WITH OPEN WARBLE HOLES. DATA, PROM 40 REPRESENTATIVE HIDE MARKETS, SUPPLIED BY THE HIDES AND ALLIED TRADES IMPROVEMENT SOCIETY (MAITLAND, 1964) ·
Month
Ig6o
1961
1g62
January February March April May June July August September October November December
4'5 10'1 23'1 48·2 59'1 6o·2 6•·5 46·o 25'2 14'2 6·8 5'5
7' 1 15'3 30'7 54'7 56·5 62·8 61 ·5 44'2 26•7 19 '5
4"4 9"4 17'5 39'3 47'5 44'6 43'0 29'6 12'7 7'7 4'4 2'4
2·6 5'3 13'9 27'4 36'4 35'9 37'5 26·1 16•7 6·9 3'1
5'1
6·s 12'5 22 '9 52 '2 52·6 5 1'4 50'3 36·6 20·8 11·6 5'7 3'6
Average
31'5
31'1
28•J
22'4
J8 •9
B·o
1963
1964
2•J
Most of the pupae of H. lineatum are formed in March and April (Fig. 2), and adults are on the wing in late March, April and May. Most H. bovis pupae are formed during May to August, so that the adults emerge from June to September. It has been suggested that the majority of the damage to hides is caused by H. bovis so that weather conditions during May to September would be expected to affect the free-living stages of the fly, and hence the amount of damage to hides caused by the next generation in the following spring and summer. Comparatively few hides were warbled in I955 and 1959, and the incidence ofopen warble holes had fallen each year since 1961 (Table III). It would be expected that climatic conditions were unfavourable for the development of the pupae and/or adults of H. bovis during the summer months of 1954, 1958 and from I96o to I963. The weather conditions during the summers of I 954 to I 963 have been studied by reference to the Monthly Weather Reports of the Meteorological Office (Beesley, I96I, and Table V). Practically every month from May to September in I 954 and I 958 was summarized by the Meteorological Office as "wet", "dull and cool" or "dull and unsettled". Data for the months of May to September during I960-63 are given in Table V. The summer months of I960-63 were not as wet as those of 1954 and 1958, but they were wetter and cooler than average. It is suggested that there is a reasonable correlation between the poor weather at these times and the recorded low incidence of warble infection of the hides in the corresponding following years. It is not suggested that the recent decrease in the amount
BRITISH VETERINARY JOURNAL, 122, 3 TABLE V KAXIMUM, NIEAN AND MINIKUM AIR TEMPERATURES, HOURS OF SUNSHINE AND INCHES OF RAINFALL FOR ENGLAND AND WALES DURING MAY TO SEPTEMBER, 1960-63.
Tear
Weather data
May
Jum
Ig6o
Maximum air tempera ture, °C . Mean air temperature, °C. Minimum air temperature, °C. Percentage sunshine Percentage rainfall
25·6 + •·5 - 6·7 97 72
30·6 + •·5 - 1·1 128 go
1g61
Maximum air temperature Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall
24"4 - 0•2 -6•7 Ill 64
1962
Maximum air temperature Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall Maximum air tempera ture Mean air temperature Minimum air temperature Percentage sunshine Percentage rainfall
lg63
August
September
- 1•1 85 141
25"6 -o·8 -1·1 95 140
25·6 - o·5 -1 · 1 94 147
31 "1 + o·4 -2"2 109 69
33"9 -0·9 -1 "1 92 86
31·8 -o·3 ·-I·I 103 100
31·6 +• ·4 - 1•7 97 105
21 "1 -I·O - s-6 89 104
26•7 -0"7 -5·6 119 31
27"2 - 1"5 -1 "1 74 78
25"0 -1"5 -1 ·7 92 137
27•8 - I·o -1·7 136
27•2 -o·8 - 3"9 101 82
28 ·3 +o·I + o·6 94 154
28 ·9 - [•1
26•7 -1 •7 -o·6 75 128
26·1 -0"7 -1"7 106 93
July 25"0 -[•[
-[•[
101 67
88
Mean monthly temperatures are given in the form of the difference from the mean temperature in the corresponding months of previous years. Monthly sunshine and rainfall data are given in the form of the percentage average compared with the corresponding months of previous years (Meteorological Office, Ig6
of warble infection is due entirely to the poor summer weather. The use of insecticides, and especially the introduction of the systemically active insecticides, would also be expected to have some effect on the warble fly population, and there is reason to believe that cattle which have been treated with systemic insecticides show an increased resistance to warble infection (Knapp, Brethour, Harvey & Roan, rg6o). REFERENCES
BEESLEY, W. N. (1961). Ann. trop. Med. Parasit ., 55. 18. BEESLEY, W. N. (1962). Res. vet. Sci., 3, 203. BEESLEY, W. N. ( 1963) . Ann. appl. Biol., ~. 295· BEESLEY, W. N. (1964) . Ph.D. thesis, University of Reading Library. BEVAN, W. ]. & EDWARDS, E. E. (1951). Bull. ent. Res., .f:I, 639. BouVIER, G. ( 1964) . Schweizer A rch. Tierheilk., 1o6, 339· BRACEWELL, C . D. & ScHURR, H R . ( 196o) . Vet. Rec., 72, 281. KNAPP, F. W., BRETHOUR,j. R., HARVEY, T. L. & RoAN, L. C. (196o).]. econ. Ent., 52, 1022. METEOROLOGICAL OFFICE, LoNDON (196o-63). Monthly Weather Reports, 77-8o. RosENBERGER, G. (1959). Dt. tierii.r;:;tl. Wschr., 66, 549· ScHARFF, D. K. (1950). Cattle Grubs. Bull. Mont. agri. E xp. Stn., No. 471. ScHARFF, D. K., SHARMAN, G. A.M. & LUDWIG, P. (1962 ) . ]. Am. vet. med. Ass., I.f:I, 582. SIMMONS, S. W. ( 1939) . ] . Am. vet. med. Ass., 95, 283.
(Received for publication 8 September, 1965)